Endangered and Threatened Wildlife and Plants; Proposed Threatened Status for the Rufa Red Knot (Calidris canutus rufa)
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Proposed rule.
CFR Part: "50 CFR Part 17"
RIN Number: "RIN 1018-AY17"
Citation: "78 FR 60024"
Document Number: "Docket No. FWS-R5-ES-2013-0097; 4500030113"
"Proposed Rules"
SUMMARY: We, the
   EFFECTIVE DATE: We will accept all comments received or postmarked on or before
   ADDRESSES: Document availability: You may obtain copies of the proposed rule and its four supplemental documents on the Internet at http://www.regulations.gov at Docket Number FWS-R5-ES-2013-0097, or by mail from the
   Comment submission: You may submit written comments by one of the following methods:
   (1) Electronically: Go to the Federal eRulemaking Portal: http://www.regulations.gov. In the Search box, enter FWS-R5-ES-2013-0097, which is the docket number for this rulemaking. You may submit a comment by clicking on "Comment Now!"
   (2) By hard copy: Submit by U.S. mail or hand-delivery to: Public Comments Processing, Attn: FWS-R5-ES-2013-0097;
   We request that you send comments only by the methods described above. We will post all information received on http://www.regulations.gov. This generally means that we will post any personal information you provide us (see the Public Comments section below for more details).
   FOR FURTHER INFORMATION CONTACT:
   SUPPLEMENTARY INFORMATION: Why we need to publish a rule. Under the Act, if a species is determined to be endangered or threatened throughout all or a significant portion of its range, we are required to promptly publish a proposal in the
   This rule proposes listing the rufa red knot (Calidris canutus rufa) as a threatened species. The rufa red knot is a candidate species for which we have on file sufficient information on biological vulnerability and threats to support preparation of a listing proposal, but for which development of a listing regulation has been precluded by other higher priority listing activities. This rule reassesses all available information regarding status of and threats to the rufa red knot. We will also publish a proposal to designate critical habitat for the rufa red knot under the Act in the near future.
   The basis for our action. Under the Act, we may determine that a species is an endangered or threatened species based on any of five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) Overutilization for commercial, recreational, scientific, or educational purposes; (C) Disease or predation; (D) The inadequacy of existing regulatory mechanisms; or (E) Other natural or manmade factors affecting its continued existence.
   We have determined that the rufa red knot is threatened due to loss of both breeding and nonbreeding habitat; potential for disruption of natural predator cycles on the breeding grounds; reduced prey availability throughout the nonbreeding range; and increasing frequency and severity of asynchronies ("mismatches") in the timing of the birds' annual migratory cycle relative to favorable food and weather conditions.
   We will seek peer review. We will seek comments from independent specialists to ensure that our designation is based on scientifically sound data, assumptions, and analyses. We will invite these peer reviewers to comment on our listing proposal. Because we will consider all comments and information received during the comment period, our final determinations may differ from this proposal.
Information Requested
Public Comments
   We intend that any final action resulting from this proposed rule will be based on the best scientific and commercial data available and be as accurate and as effective as possible. Therefore, we request comments or information from the public, other concerned governmental agencies, Native American tribes, the scientific community, industry, or any other interested parties concerning this proposed rule. We particularly seek comments concerning:
   (1) The rufa red knot's biology, range, and population trends, including:
   (a) Biological or ecological requirements of the species, including habitat requirements for feeding, breeding, and sheltering;
   (b) Genetics and taxonomy;
   (c) Historical and current range including distribution patterns;
   (d) Historical and current population levels and current and projected trends; and
   (e) Past and ongoing conservation measures for the species, its habitat, or both.
   (2) Factors that that may affect the continued existence of the species, which may include habitat modification or destruction, overutilization, disease, predation, the inadequacy of existing regulatory mechanisms, or other natural or manmade factors.
   (3) Biological, commercial trade, or other relevant data concerning any threats (or lack thereof) to this species and regulations that may be addressing those threats.
   (4) Additional information concerning the historical and current status, range, distribution, and population size of this species, including the locations of any additional populations of this species.
   (5) Genetic, morphological, chemical, geolocator, telemetry, survey (e.g., resightings of marked birds), or other data that clarify the distribution of Calidris canutus rufa versus C.c. roselaari wintering and migration areas, including the subspecies compositions of those C. canutus that occur from southern
   (6) Information regarding intra- and inter-annual red knot movements within and between the
   (7) Information that helps clarify the geographic extent of the rufa red knot's breeding range, and the extent to which rufa red knots from different wintering areas interbreed, as well as the geographic extent of the Calidris canutus islandica breeding range.
   (8) Data regarding rates of rufa red knot reproductive success.
   (9) Information regarding habitat loss or predation in rufa red knot breeding areas.
   (10) Information regarding important rufa red knot stopover areas, including inland areas (such as the
   (11) Data that support or refute the concept that juvenile rufa red knots at least partially segregate from adults during the nonbreeding seasons. We particularly seek information on juvenile wintering and migration locations; frequency, timing, and duration of juvenile use; numbers of juveniles and adults in these areas; juvenile habitat and prey characteristics; juvenile foraging and roosting habits; juvenile survival rates; and any threats associated with these areas.
   (12) Data that clarify the degree of rufa red knot site fidelity to breeding locations, wintering regions, or migration stopover sites.
   (13) Data regarding the percentage of rufa red knots that do not use
   (14) Data regarding rufa red knot use of the
   (15) Data regarding red knot use of wrack material as a microhabitat for foraging or roosting.
   (16) Information regarding the frequency and severity of the threats to red knots (e.g., documented mortality levels from disease, harmful algal blooms, contaminants, oil spills, wind turbines), their habitats (e.g., effects of sea level rise, development, aquaculture), or their food resources (e.g., harvest of marine resources, climate change) outside
   (17) Information regarding legal and illegal harvest (i.e., hunting or poaching) rates and trends in nonbreeding areas and the effects of harvest on the red knot.
   (18) Information regarding non-U.S. laws, regulations, or policies relevant to the regulation of red knot hunting; classification of the red knot as a protected species; protection of red knot habitats; or threats to the red knot (e.g., to address the data gaps identified under Summary of Factors Affecting the Species).
   Please include sufficient information with your submission (such as scientific journal articles or other publications) to allow us to verify any scientific or commercial information you include.
   Please note that submissions merely stating support for or opposition to the action under consideration without providing supporting information, although noted, will not be considered in making a determination, as section 4(b)(1)(A) of the Act directs that determinations as to whether any species is an endangered or threatened species must be made "solely on the basis of the best scientific and commercial data available."
   You may submit your comments and materials concerning this proposed rule by one of the methods listed in the ADDRESSES section. We request that you send comments only by the methods described in the ADDRESSES section.
   If you submit information via http://www.regulations.gov, your entire submission--including any personal identifying information--will be posted on the Web site. If your submission is made via a hardcopy that includes personal identifying information, you may request at the top of your document that we withhold this information from public review. However, we cannot guarantee that we will be able to do so. We will post all hardcopy submissions on http://www.regulations.gov. Please include sufficient information with your comments to allow us to verify any scientific or commercial information you include.
   Comments and materials we receive, as well as supporting documentation we used in preparing this proposed rule, will be available for public inspection on http://www.regulations.gov, or by appointment, during normal business hours, at the
Public Hearings
   Section 4(b)(5) of the Act provides for one or more public hearings on this proposal, if requested. Requests must be received within 45 days after the date of publication of this proposed rule in the
   Persons needing reasonable accommodations to attend and participate in a public hearing should contact the
Peer Review
   In accordance with our joint policy on peer review published in the
Previous Federal Action
   Comprehensive information regarding previous federal actions relevant to the proposed listing of the rufa red knot is available as a supplemental document ("Previous Federal Actions") on the Internet at http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see ADDRESSES section for further access instructions).
Background
Species Information
   Comprehensive information regarding the rufa red knot's taxonomy, distribution, life history, habitat, and diet, as well as its historical and current abundance, is available as a supplemental document ("Rufa Red Knot Ecology and Abundance") on the Internet at http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see ADDRESSES section for further access instructions). A brief summary is provided here.
   The rufa red knot (Calidris canutus rufa) is a medium-sized shorebird about 9 to 11 inches (in) (23 to 28 centimeters (cm)) in length. (Throughout this document, "rufa red knot," "red knot," and "knot" are used interchangeably to refer to the rufa subspecies. " Calidris canutus " and " C. canutus " are used to refer to the species as a whole or to birds of unknown subspecies. References to other particular subspecies are so indicated.) The red knot migrates annually between its breeding grounds in the Canadian Arctic and several wintering regions, including the
Taxonomy
   Calidris canutus is classified in the Class Aves, Order Charadriiformes, Family Scolopacidae, Subfamily Scolopacinae (
   Calidris canutus canutus, C.c. piersma, and C.c. rogersi do not occur in
   Subspecies Calidris canutus roselaari breeds in western
   Pursuant to the definitions in section 3 of the Act, "the term species includes any subspecies of fish or wildlife or plants, and any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature." Based on the information in the supplemental document Rufa Red Knot Ecology and Abundance, the Service accepts the characterization of Calidris canutus rufa as a subspecies because each recognized subspecies is believed to occupy separate breeding areas, in addition to having morphological and behavioral character differences. Therefore, we find that C.c. rufa is a valid taxon that qualifies as a listable entity under the Act.
Breeding</p>
   Based on estimated survival rates for a stable population, few red knots live for more than about 7 years (Niles et al. 2008, p. 28). Age of first breeding is uncertain but for most birds is probably at least 2 years (Harrington 2001, p. 21). Red knots generally nest in dry, slightly elevated tundra locations, often on windswept slopes with little vegetation. Breeding territories are located inland, but near arctic coasts, and foraging areas are located near nest sites in freshwater wetlands (Niles et al. 2008, p. 27; Harrington 2001, p. 8). On the breeding grounds, the red knot's diet consists mostly of terrestrial invertebrates such as insects (Harrington 2001, p. 11). Breeding occurs in June (Niles et al. 2008, pp. 25-26). Breeding success of High Arctic shorebirds such as Calidris canutus varies dramatically among years in a somewhat cyclical manner. Two main factors seem to be responsible for this annual variation: weather that affects nesting conditions and food availability (see Summary of Factors Affecting the Species--Factor E--Asynchronies) and the abundance of arctic lemmings (Dicrostonyx torquatus and Lemmus sibericus) that affects predation rates (see Summary of Factors Affecting the Species--Factor C--Predation--Breeding).
Wintering
   In this document, "winter" is used to refer to the nonbreeding period of the red knot life cycle when the birds are not undertaking migratory movements. Red knots occupy all known wintering areas from December to February, but may be present in some wintering areas as early as September or as late as May. In the Southern Hemisphere, these months correspond to the austral summer (i.e., summer in the Southern Hemisphere), but for consistency in this document the terms "winter" and "wintering area" are used throughout the subspecies' range.
   Wintering areas for the red knot include the Atlantic coasts of
Migration
   Each year red knots make one of the longest distance migrations known in the animal kingdom, traveling up to 19,000 miles (mi) (30,000 kilometers (km) annually. Red knots undertake long flights that may span thousands of miles without stopping. As Calidris canutus prepare to depart on long migratory flights, they undergo several physiological changes. Before takeoff, the birds accumulate and store large amounts of fat to fuel migration and undergo substantial changes in metabolic rates. In addition, leg muscles, gizzard (a muscular organ used for grinding food), stomach, intestines, and liver all decrease in size, while pectoral (chest) muscles and heart increase in size. Due to these physiological changes, C. canutus arriving from lengthy migrations are not able to feed maximally until their digestive systems regenerate, a process that may take several days. Because stopovers are time-constrained, C. canutus requires stopovers rich in easily digested food to achieve adequate weight gain (Niles et al. 2008, pp. 28-29;
   Major spring stopover areas along the Atlantic coast include Rio Gallegos, Peninsula Valdes, and San Antonio Oeste (
   Texas knots follow an inland flyway to and from the breeding grounds, using spring and fall stopovers along western
Migration and Wintering Habitat
   Long-distance migrant shorebirds are highly dependent on the continued existence of quality habitat at a few key staging areas. These areas serve as stepping stones between wintering and breeding areas. Conditions or factors influencing shorebird populations on staging areas control much of the remainder of the annual cycle and survival of the birds (Skagen 2006, p. 316;
   Habitats used by red knots in migration and wintering areas are similar in character, generally coastal marine and estuarine (partially enclosed tidal area where fresh and salt water mixes) habitats with large areas of exposed intertidal sediments. In
Migration and Wintering Food
   Across all subspecies, Calidris canutus is a specialized molluscivore, eating hard-shelled mollusks, sometimes supplemented with easily accessed softer invertebrate prey, such as shrimp- and crab-like organisms, marine worms, and horseshoe crab (Limulus polyphemus) eggs (Piersma and
   The primary prey of the rufa red knot in non-breeding habitats include blue mussel (Mytilus edulis) spat (juveniles); Donax and
   Red knots and other shorebirds that are long-distance migrants must take advantage of seasonally abundant food resources at intermediate stopovers to build up fat reserves for the next non-stop, long-distance flight (Clark et al. 1993, p. 694). Although foraging red knots can be found widely distributed in small numbers within suitable habitats during the migration period, birds tend to concentrate in those areas where abundant food resources are consistently available from year to year.
Abundance
   In the United States, red knot populations declined sharply in the late 1800s and early 1900s due to excessive sport and market hunting, followed by hunting restrictions and signs of population recovery by the mid-1900s (Urner and Storer 1949, pp. 178-183; Stone 1937, p. 465; Bent 1927, p. 132). However, it is unclear whether the red knot population fully recovered its historical numbers (Harrington 2001, p. 22) following the period of unregulated hunting.
   More recently, long-term survey data from two key areas (
Climate Change
   Comprehensive background information regarding climate change is available as a supplemental document ("Climate Change Background") on the Internet at http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see ADDRESSES section for further access instructions). As explained in the supplemental document, the
Summary of Factors Affecting the Species
   Section 4 of the Act (16 U.S.C. 1533), and its implementing regulations at 50 CFR part 424, set forth the procedures for adding species to the Federal Lists of Endangered and Threatened Wildlife and Plants. Under section 4(a)(1) of the Act, we may list a species based on any of the following five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; and (E) other natural or manmade factors affecting its continued existence. Listing actions may be warranted based on any of the above threat factors, singly or in combination. Each of these factors is discussed below.
Overview of Threats Related to Climate Change
   We discuss the ongoing and projected effects of climate change, and the levels of certainty associated with these effects, in the appropriate sections of the five-factor analysis. For example, habitat loss from sea level rise is discussed under Factor A, and asynchronies ("mismatches") in the timing of the annual cycle are discussed under Factor E. Here we present an overview of threats stemming from climate change, which are addressed in more detail in the sections that follow.
   The natural history of Arctic-breeding shorebirds makes this group of species particularly vulnerable to global climate change (e.g., Meltofte et al. 2007, entire; Piersma and Lindstroem 2004, entire; Rehfisch and Crick 2003, entire; Piersma and Baker 2000, entire; Zoeckler and Lysenko 2000, entire; Lindstroem and Agrell 1999, entire). Relatively low genetic diversity, which is thought to be a consequence of survival through past climate-driven population bottlenecks, may put shorebirds at more risk from human-induced climate variation than other avian taxa (Meltofte et al. 2007, p. 7); low genetic diversity may result in reduced adaptive capacity as well as increased risks when population sizes drop to low levels.
   In the short term, red knots may benefit if warmer temperatures result in fewer years of delayed horseshoe crab spawning in
   Several threats are related to the possibility of changing storm patterns. While variation in weather is a natural occurrence and is normally not considered a threat to the survival of a species, persistent changes in the frequency, intensity, or timing of storms at key locations where red knots congregate (e.g., key stopover areas) can pose a threat (see Factor E and the "Coastal Storms and Extreme Weather" section of the Climate Change Background supplemental document). Storms impact migratory shorebirds like the red knot both directly and indirectly. Direct impacts include energetic costs from a longer migration route as birds avoid storms, blowing birds off course, and outright mortality (Niles et al. 2010a, p. 129). Indirect impacts include changes to habitat suitability, storm-induced asynchronies between migration stopover periods and the times of peak prey availability, and possible prompting of birds to take refuge in areas where shorebird hunting is still practiced (Niles et al. 2012, p. 1; Dey et al. 2011b, pp. 1-2; Nebel 2011, p. 217).
   With arctic warming, vegetation conditions in the red knot's breeding grounds are expected to change, causing the zone of nesting habitat to shift and perhaps contract, but this process may take decades to unfold (Feng et al. 2012, p. 1366; Meltofte et al. 2007, p. 36;
   In summary, climate change is expected to affect red knot fitness and, therefore, survival through direct and indirect effects on breeding and nonbreeding habitat, food availability, and timing of the birds' annual cycle. Ecosystem changes in the arctic (e.g., changes in predation patterns and pressures) may also reduce reproductive output. Together, these anticipated changes will likely negatively influence the long-term survival of the rufa red knot.
Factor A. The Present or Threatened Destruction, Modification, or Curtailment of Its Habitat or Range
   In this section, we present and assess the best available scientific and commercial data regarding ongoing threats to the quantity and quality of red knot habitat. Within the nonbreeding portion of the range, red knot habitat is primarily threatened by the highly interrelated effects of sea level rise, shoreline stabilization, and coastal development. Lesser threats to nonbreeding habitat include agriculture and aquaculture, invasive vegetation, and beach maintenance activities. Within the breeding portion of the range, the primary threat to red knot habitat is from climate change. With arctic warming, vegetation conditions in the breeding grounds are expected to change, causing the zone of nesting habitat to shift and perhaps contract. Arctic freshwater systems--foraging areas for red knots during the nesting season--are particularly sensitive to climate change.
Factor A--Accelerating Sea Level Rise
   For most of the year, red knots live in or immediately adjacent to intertidal areas. These habitats are naturally dynamic, as shorelines are continually reshaped by tides, currents, wind, and storms. Coastal habitats are susceptible to both abrupt (storm-related) and long-term (sea level rise) changes. Outside of the breeding grounds, red knots rely entirely on these coastal areas to fulfill their roosting and foraging needs, making the birds vulnerable to the effects of habitat loss from rising sea levels. Because conditions in coastal habitats are also critical for building up nutrient and energy stores for the long migration to the breeding grounds, sea level rise affecting conditions on staging areas also has the potential to impact the red knot's ability to breed successfully in
   According to the
   The amount of sea level change varies regionally because of different rates of settling (subsidence) or uplift of the land, and because of differences in ocean circulation (NRC 2010, p. 43). In the last century, for example, sea level rise along the U.S. mid-Atlantic and Gulf coasts exceeded the global average by 5 to 6 in (13 to 15 cm) because coastal lands in these areas are subsiding (
Table 1--Local Sea Level Trends From Within the Range of the Red Knot [NOAA 2012a] Station Mean local Data period sea level trend (mm per year) Pointe-Au-Pre, Canada -0.36 +/- 1900-1983 0.40 Woods Hole, Massachusetts 2.61 +/- 0.20 1932-2006 Cape May, New Jersey 4.06 +/- 0.74 1965-2006 Lewes, Delaware 3.20 +/- 0.28 1919-2006 Chesapeake Bay Bridge Tunnel, Virginia 6.05 +/- 1.14 1975-2006 Beaufort, North Carolina 2.57 +/- 0.44 1953-2006 Clearwater Beach, Florida 2.43 +/- 0.80 1973-2006 Padre Island, Texas 3.48 +/- 0.75 1958-2006 Punto Deseado, Argentina -0.06 +/- 1970-2002 1.93
   Data from along the U.S. Atlantic coast suggest a relationship between rates of sea level rise and long-term erosion rates; thus, long-term coastal erosion rates may increase as sea level rises (
Sea Level Rise--International
International--Overview
   We conducted an analysis to consider the possible effects of a 3.3-ft (1-m) increase in sea level in important nonbreeding habitats outside
   We selected a 3.3-ft (1-m) sea level increase based on the availability of a global dataset, and because it falls within the current range of 2.6 to 6.6 ft (0.8 to 2 m) projected by 2100 (NRC 2010, p. 44). Along with topography (e.g., land elevation relative to sea level), the local tidal regime is an important factor in attempting to forecast the likely effects of sea level rise (Strauss et al. 2012, pp. 2, 6-8). Therefore, we also considered local tidal ranges (the vertical distance between the high tide and the succeeding low tide) and other factors that may influence the extent or effects of sea level rise when site-specific information was available and appropriate. In the 1990s, some studies (e.g., Gornitz et al. 1994, p. 330) classified coastlines with a large tidal range ("macrotidal") (i.e., with a tidal range greater than 13 ft (4 m)) as more vulnerable to sea level rise because a large tidal range is associated with strong tidal currents that influence coastal behavior (Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 1999). More recently, however, the USGS inverted this ranking such that a macrotidal coastline is classified as low vulnerability. This change was based primarily on the potential influence of storms on coastal evolution, and the impact of storms relative to the tidal range. For example, on a tidal coastline, there is only a 50 percent chance of a storm occurring at high tide. Thus, for a region with a 13.1-ft (4-m) tidal range, a storm having a 9.8-ft (3-m) surge height is still up to 3.3 ft (1 m) below the elevation of high tide for half of the duration of each tidal cycle. A microtidal coastline (with a tidal range less than 6.6 ft (2 m)), on the other hand, is essentially always "near" high tide and, therefore, always at the greatest risk of significant storm impact (Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 1999).
   Notwithstanding uncertainty about how tidal range will influence overall effects of sea level rise on coastal change, tidal range is also important due to the red knot's dependence on intertidal areas for foraging habitat. Along macrotidal coasts, large areas of intertidal habitat are exposed during low tide. In such areas, some intertidal habitat is likely to remain even with sea level rise, whereas a greater proportion of intertidal habitats may become permanently inundated in areas with smaller tidal ranges.
International--Analysis
   Although no local modeling is available, large tidal ranges in the southernmost red knot wintering areas suggest extensive tidal flats will persist, although a projected 3.3-ft (1-m) rise in sea level will likely result in some habitat loss. Despite decreases in recent decades, Bahia Lomas in the
   On the Patagonian coast of
   Despite decreases in recent decades, Lagoa do Peixe is a key spring stopover site for red knots on the east coast of
   Coastal areas in North-
   The IPCC (2007c, p. 58) evaluated the effects of a 1.6-ft (0.5-m) rise in sea level on small
   In Canada, the islands of the Mingan Archipelago could be inundated by a 3.3-ft (1-m) sea level rise. The topographic mapping shows some inundation of the adjacent mainland coastline (
International--Summary
   Based on our analysis of topography, tidal range, and other factors, some habitat loss in
Sea Level Rise--United States
United States--Mechanisms of
   Comparing topography to best available scenarios of sea level rise provides an estimate of the land area that may be vulnerable to the effects of sea level rise, but does not incorporate regional variation in tidal regimes (Strauss et al. 2012, p. 2), coastal processes (e.g., barrier island migration), or environmental changes that may occur as sea level rises (e.g., salt marsh deterioration) (CCSP 2009b, p. 44). Because the majority of the Atlantic and Gulf coasts consist of sandy shores, inundation alone is unlikely to reflect the potential consequences of sea level rise. Instead, long-term shoreline changes will involve contributions from both inundation and erosion, as well as changes to other coastal environments such as wetland losses. Most portions of the open coast of
   By altering coastal geomorphology, sea level rise will cause significant and often dramatic changes to coastal landforms including barrier islands, beaches, and intertidal flats (CCSP 2009b, p. 13; Rehfisch and Crick 2003, p. 89), primary red knot habitats. Due to increasing sea levels, storm-surge-driven floods now qualifying as 100-year events are projected to occur as often as every 10 to 20 years along most of the U.S. Atlantic coast by 2050, with even higher frequencies of such large floods in certain localized areas (Tebaldi et al. 2012, pp. 7-8). Rising sea level not only increases the likelihood of coastal flooding, but also changes the template for waves and tides to sculpt the coast, which can lead to loss of land orders of magnitude greater than that from direct inundation alone (Ashton et al. 2007, p. 1). Although scientists agree that the predicted sea level rise will result in severe beach erosion and shoreline retreat through the next century, quantitative predictions of these changes are uncertain, hampered by limited understanding of coastal responses and the innate complexity of the coastal zone (Ashton et al. 2007, p. 9). Coastal responses to climate change will not likely be homogeneous along the coast, due to local differences in geology and other factors (Ashton et al. 2007, p. 9).
   Beach losses accumulate over time, mostly during infrequent, high-energy events, both seasonal events and rare extreme storms (Ashton et al. 2009, p. 7). Even the long-term coastal response to sea level rise depends on the magnitudes and timing of stochastically unpredictable future storm events (Ashton et al. 2009, p. 9). Most erosion events on the Atlantic and Gulf coasts are the result of storms. With sea level rise, increased erosion is caused by longer storm surges and greater wave action from both tropical (especially on the southeast Atlantic and Gulf coasts) and extra-tropical storms (
   In addition to the effects of storm surges, red knot habitats could also be affected by the increasing frequency and intensity of extreme precipitation events (see supplemental document--Climate Change Background). Since the ecological dynamics of sandy beaches can be linked to freshwater discharge from rivers, global changes in land-ocean coupling via freshwater outflows are predicted to affect the ecology of beaches (Schlacher et al. 2008a, p. 84). For example, persistent increases in freshwater discharges could cause localized habitat changes by allowing invasive or incompatible vegetation to become established, changing the seed distribution of native grasses, or altering salinity (F. Weaver pers. comm.
   Red knot migration and wintering habitats in
Mechanisms--Estuarine Beaches
   As sea level rises, the fate of estuarine beaches (e.g., along
Mechanisms--Barrier Island Beaches
   The barrier islands of the Atlantic and Gulf coasts have evolved in the context of modest and decelerating sea level rise over the past 5,000 years. If human activities do not interfere, these barrier systems can typically remain intact as they migrate landward, given sea level rise rates typical of those of the last few millennia (CCSP 2009b, p. 186; Ashton et al. 2007, p. 2). Without stabilization, many low-lying, undeveloped islands will migrate toward the mainland, pushed by the overwashing of sand eroding from the seaward side that gets re-deposited in the bay (Scavia et al. 2002, p. 152). However, even without human intervention, some barrier islands may respond to sea level rise by breaking up and drowning in place, rather than migrating (Titus 1990, p. 67). Coastal geologists are not yet able to forecast whether a particular island will migrate or break up, although island disintegration appears to be more frequent in areas with high rates of relative sea level rise (Titus 1990, p. 67); thus, disintegration may occur more often as rates of sea level rise accelerate.
   Whether the barrier systems can continue to evolve with accelerated sea level rise is not clear, particularly as human intervention often does not permit the islands to continue to freely move landward (Ashton et al. 2007, p. 2). Sea level rise of 3.3 ft (1 m) may cause many narrow barrier islands to disintegrate (USEPA 2012). Because the coastal marshes behind many barrier islands become increasingly inundated, sufficiently high rates of sea level rise could result in threshold behaviors that produce wholesale reorganizations of entire barrier systems (CCSP 2009b, p. 2; Ashton et al. 2007, p. 10). Crossing threshold levels of interaction between coastal elevation, sea level, and storm-driven surges and waves can result in dramatic changes in coastal topography, including the loss of some low-lying islands (
United States--Coastal Vulnerability Index
   At the national scale, the USGS CVI combines the coastal system's susceptibility to change with its natural ability to adapt to changing environmental conditions. The output is a relative measure of the system's natural vulnerability to the effects of sea level rise. Classification of vulnerability (very high, high, moderate, or low) is based on variables such as coastal geomorphology, regional coastal slope, rate of sea level rise, wave and tide characteristics, and historical shoreline change rates. The combination of these variables and the association of these variables to each other furnishes a broad overview of regions where physical changes are likely to occur due to sea level rise (Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 1999).
   We conducted a Geographic Information System (GIS) analysis to overlay the CVI mapping with important red knot habitats, which were delineated using data from the
Table 2--Percent of Coastline (by Length) in Each Coastal Vulnerability Category; Important Red Knot Habitats Versus theEntire Coast Very high High Moderate Low Important Red Knot Habitats Massachusetts 0 10 23 67 New York 0 7 50 43 New Jersey--Atlantic 69 10 22 0 New Jersey--Delaware Bay 0 77 14 9 Delaware 0 37 0 63 Virginia 99 1 0 0 North Carolina 59 15 25 1 South Carolina 59 23 18 0 Georgia 29 35 27 8 Florida--Atlantic 8 7 79 6 Florida--Gulf 2 41 53 3 Mississippi 100 0 0 0 Louisiana 100 0 0 0 Texas 63 20 17 0 All States combined 49 21 23 7 Entire Coast * Atlantic coast 27 22 23 28 Gulf coast 42 13 37 8 Atlantic and Gulf coasts combined 31 19 26 23 * Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 1999.
United States--Northeast and Mid-Atlantic
   In the Northeast (
Mid-Atlantic--Delaware Bay Shorebird Habitat
   The rate of sea level rise in the
   Glick et al. (2008, p. 31) found that existing marsh along
   Galbraith et al. (2002, pp. 177-178) examined several different scenarios of future sea level rise and projected major losses of intertidal habitat in
Mid-Atlantic--Delaware Bay Horseshoe Crab Habitat
   The narrow sandy beaches used by spawning horseshoe crabs in
   At present, the degree to which horseshoe crab populations will decline as beaches are lost remains unclear. Botton et al. (1988, p. 331) found that even subtle alteration of the sediment, such as through erosion, may affect the suitability of habitat for horseshoe crab reproduction, and that horseshoe crab spawning activity is lower in areas where erosion has exposed underlying peat (Botton et al. 1988, p. 325). Through habitat modeling, Czaja (2009, p. 9) found overall horseshoe crab habitat suitability in
   In 2012,
United States--Southeast and the
   Rates of erosion for the Southeast Atlantic region are generally highest in
   The barrier islands in the Georgia Bight (southern
   In contrast to the more stable southern Atlantic shores of
   In Alabama, coastal land loss is caused primarily by beach and bluff erosion, but other mechanisms for loss, such as submergence, appear to be minor. Barrier islands in
   Erosion is rapid along some barrier islands and headlands in
   Rates of erosion for the
   Compared to shoreline erosion in some other
   Strauss et al. (2012, p. 4) found more than 78 percent of the coastal dry land and freshwater wetlands on land less than 3.3 ft (1 m) above local Mean High Water in the continental
United States--Summary
   Important red knot habitats tend to occur along higher-vulnerability portions of the U.S. shoreline. Red knot habitats along the Atlantic coast of
Sea Level Rise--Summary
   Due to background rates of sea level rise and the naturally dynamic nature of coastal habitats, we conclude that red knots are adapted to moderate (although sometimes abrupt) rates of habitat change in their wintering and migration areas. However, rates of sea level rise are accelerating beyond those that have occurred over recent millennia. In most of the red knot's nonbreeding range, shorelines are expected to undergo dramatic reconfigurations over the next century as a result of accelerating sea level rise. Extensive areas of marsh are likely to become inundated, which may reduce foraging and roosting habitats. Marshes may be able to establish farther inland, but the rate of new marsh formation (e.g., intertidal sediment accumulation, development of hydric soils, colonization of marsh vegetation) may be slower than the rate of deterioration of existing marsh, particularly under the higher sea level rise scenarios. The primary red knot foraging habitats, intertidal flats and sandy beaches, will likely be locally or regionally inundated, but replacement habitats are likely to reform along the shoreline in its new position. However, if shorelines experience a decades-long period of high instability and landward migration, the formation rate of new beach habitats may be slower than the inundation rate of existing habitats. In addition, low-lying and narrow islands (e.g., in the
Factor A--U.S. Shoreline Stabilization and
   Much of the U.S. coast within the range of the red knot is already extensively developed. Direct loss of shorebird habitats occurred over the past century as substantial commercial and residential developments were constructed in and adjacent to ocean and estuarine beaches along the Atlantic and Gulf coasts. In addition, red knot habitat was also lost indirectly, as sediment supplies were reduced and stabilization structures were constructed to protect developed areas.
   Sea level rise and human activities within coastal watersheds can lead to long-term reductions in sediment supply to the coast. The damming of rivers, bulk-heading of highlands, and armoring of coastal bluffs have reduced erosion in natural source areas and consequently the sediment loads reaching coastal areas. Although it is difficult to quantify, the cumulative reduction in sediment supply from human activities may contribute substantially to the long-term shoreline erosion rate. Along coastlines subject to sediment deficits, the amount of sediment supplied to the coast is less than that lost to storms and coastal sinks (inlet channels, bays, and upland deposits), leading to long-term shoreline recession (
   In addition to reduced sediment supplies, other factors such as stabilized inlets, shoreline stabilization structures, and coastal development can exacerbate long-term erosion (
   Past and ongoing stabilization projects fundamentally alter the naturally dynamic coastal processes that create and maintain beach strand and bayside habitats, including those habitat components that red knots rely upon. Past loss of stopover and wintering habitat likely reduce the resilience of the red knot by making it more dependent on those habitats that remain, and more vulnerable to threats (e.g., disturbance, predation, reduced quality or abundance of prey, increased intraspecific and interspecific competition) within those restricted habitats. (See Factors C and E, below, for discussions of these threats, many of which are intensified in and near developed areas.)
Shoreline Stabilization--Hard Structures
   Hard structures constructed of stone, concrete, wood, steel, or geotextiles have been used for centuries as a coastal defense strategy (Defeo et al. 2009, p. 6). The most common hard stabilization structures fall into two groups: structures that run parallel to the shoreline (e.g., seawalls, revetments, bulkheads) and structures that run perpendicular to the shoreline (e.g., groins, jetties). Groins are often clustered in groin fields, and are intended to protect a finite section of beach, while jetties are normally constructed at inlets to keep sand out of navigation channels and provide calm-water access to harbor facilities (
   Prior to the 1950s, the general practice in
   Hard shoreline stabilization projects are typically designed to protect property (and its human inhabitants), not beaches (Kana 2011, p. 31; Pilkey and Howard 1981, p. 2). Hard structures affect beaches in several ways. For example, when a hard structure is put in place, erosion of the oceanfront sand continues, but the fixed back-beach line remains, resulting in a loss of beach area (USACE 2002, p.
   Structural development along the shoreline and manipulation of natural inlets upset the naturally dynamic coastal processes and result in loss or degradation of beach habitat (Melvin et al. 1991, pp. 24-25). As beaches narrow, the reduced habitat can directly lower the diversity and abundance of biota (life forms), especially in the upper intertidal zone. Shorebirds may be impacted both by reduced habitat area for roosting and foraging, and by declining intertidal prey resources, as has been documented in
   In
   In a few isolated locations, however, hard structures may enhance red knot habitat, or may provide artificial habitat. In
Shoreline Stabilization--
   Several types of sediment transport are employed to stabilize shorelines, protect development, maintain navigation channels, and provide for recreation (Gebert 2012, pp. 14, 16; Kana 2011, pp. 31-33; USACE 2002, p.
Sediment Transport--Beach Nourishment
   Beach nourishment is an engineering practice of deliberately adding sand (or gravel or cobbles) to an eroding beach, or the construction of a beach where only a small beach, or no beach, previously existed (NRC 1995, pp. 23-24). Since the 1970s, 90 percent of the Federal appropriation for shore protection has been for beach nourishment (USACE 2002, p.
   Where shorebird habitat has been severely reduced or eliminated by hard stabilization structures, beach nourishment may be the only means available to replace any habitat for as long as the hard structures are maintained (
   In addition to disturbing the birds and impacting the prey base, beach nourishment can affect the quality and quantity of red knot habitat (
   Following placement of sediments much coarser than those native to the beach,
Sediment Transport--Backpassing and Scraping
   Sediment backpassing is a technique that reverses the natural migration of sediment by mechanically (via trucks) or hydraulically (via pipes) transporting sand from accreting, downdrift areas of the beach to eroding, updrift areas of the beach (Kana 2011, p. 31; Chasten and Rosati 2010, p. 5). Currently less prevalent than beach nourishment, sediment backpassing is an emerging practice because traditional nourishment methods are beginning to face constraints on budgets and sediment availability (Hafner 2012, pp. 31, 35; Chase 2006, p. 19). Beach bulldozing or scraping is the process of mechanically redistributing beach sand from the littoral zone (along the edge of the sea) to the upper beach to increase the size of the primary dune or to provide a source of sediment for beaches that have no existing dune; no new sediment is added to the system (Kana 2011, p. 30;
   Many of the effects of sediment backpassing and beach scraping are similar to those for beach nourishment (USFWS 2011c, pp. 11-24; Lindquist and Manning 2001, p. 1), including disturbance during and after construction, alteration of prey resources, reduced habitat area and quality, and precluded formation of new habitats. Relative to beach nourishment, sediment backpassing and beach scraping can involve considerably more driving of heavy trucks and other equipment on the beach including areas outside the sand placement footprint, potentially impacting shorebird prey resources over a larger area (see Factor E, below, for discussion of vehicle impacts on prey resources) (USFWS 2011c, pp. 11-24). In addition, these practices can directly remove sand from red knot habitats, as is the case in one red knot concentration area in
Sediment Transport--Dredging
   Sediments are also manipulated to maintain navigation channels. Many inlets in the U.S. range of the red knot are routinely dredged and sometimes relocated. In addition, nearshore areas are routinely dredged ("mined") to obtain sand for beach nourishment. Regardless of the purpose, inlet and nearshore dredging can affect red knot habitats. Dredging often involves removal of sediment from sand bars, shoals, and inlets in the nearshore zone, directly impacting optimal red knot roosting and foraging habitats (Harrington 2008, p. 2; Harrington in Guilfoyle et al. 2007, pp. 18-19;
   In addition to causing this direct habitat loss, the dredging of sand bars and shoals can preclude the creation and maintenance of red knot habitats by removing sand sources that would otherwise act as natural breakwaters and weld onto the shore over time (
Shoreline Stabilization and Coastal Development--Existing Extent
Existing Extent--
   The mid-Atlantic coast from
   By area, more than 80 percent of the land below 3.3 ft (1 m) in
   New Jersey's Atlantic coast has the longest history of stabilized barrier island shoreline in
   Although much less developed than
Table 3--Percent * of Dry Land Within 3.3 ft (1 m) of High Water by Intensity of Development Along theUnited States Atlantic Coast [Titus et al. 2009, p. 5] Developed Intermediate Undeveloped Conservation Massachusetts 26 29 22 23 Rhode Island 36 11 48 5 Connecticut 80 8 7 5 New York 73 18 4 6 New Jersey 66 15 12 7 Pennsylvania 49 21 26 4 Delaware 27 26 23 24 Maryland 19 16 56 9 District of 82 5 14 0 Columbia Virginia 39 22 32 7 North Carolina 28 14 55 3 South Carolina 28 21 41 10 Georgia 27 16 23 34 Florida 65 10 12 13 Coastwide 42 15 33 9 * Percentages may not add up to 100 due to rounding.
Existing Extent--Southeast Atlantic and Gulf Coasts
   The U.S. southeastern coast from
   The 43 percent of preserved beaches generally overlap with the undeveloped beach category (1,264 miles or 60 percent, as shown in table 4), but may also include some developed areas such as recreational facilities or private inholdings within parks (USFWS 2012a, p. 15). To account for such recreational or inholding development, we rounded down the estimated preserved, undeveloped beaches to about 40 percent. Adding the preserved, undeveloped 40 percent estimate to the 40 percent that is already developed, we conclude that only about 20 percent of the beaches from
Table 4--The Lengths and Percentages of Sandy, Oceanfront Beach That Are Developed and Undeveloped Along the Southeast Atlantic and Gulf Coasts [T. Rice pers. comm.January 3, 2013 ; Rice 2012a, p. 6; USFWS 2012a, p. 15] State Miles of Miles and Miles and shoreline percent of percent of developed beach undeveloped beach * North Carolina 326 159 (49%) 167 (51%) South Carolina 182 93 (51%) 89 (49%) Georgia 90 15 (17%) 75 (83%) Florida 809 459 (57%) 351 (43%) Alabama 46 25 (55%) 21 (45%) Mississippi 27 0 (0%) 27 (100%) barrier island Mississippi 51 41 (80%) 10 (20%) mainland ** Louisiana 218 13 (6%) 205 (94%) Texas 370 51 (14%) 319 (86%) Coastwide 2,119 856 (40%) 1,264 (60%) * Beaches classified as "undeveloped" occasionally include a few scattered structures. ** The mainlandMississippi coast along Mississippi Sound includes 51.3 mi of sandy beach as of 2010-2011, out of approximately 80.7 total shoreline miles (the remaining portion is nonsandy, either marsh or armored coastline with no sand).
Table 5--Approximate Shoreline Miles of Sandy, Oceanfront Beach That Have Been Modified by Armoring With Hard Erosion Control Structures, and by Sand Placement Activities,North Carolina toTexas , as ofDecember 2011 [Rice 2012a, p. 7; USFWS 2012a, p. 24] Known Known approximate approximate miles of miles of armored beach beach receiving (percent sand placement of total (percent coastline) of total coastline) North Carolina Not available 91.3 (28%) South Carolina Not available 67.6 (37%) Georgia 10.5 (12%) 5.5 (6%) Florida 117.3 * 379.6 (47%) Alabama 4.7(10%) 7.5 (16%) Mississippi barrier island 0 (0%) 1.1 (4%) Mississippi mainland 45.4 (89%) 43.5 (85%) Louisiana 15.9 (7%) 60.4 (28%) Texas 36.6 (10%) 28.3 (8%) Total * 230.4 * 684.8 (32%) * Partial data.
Existing Extent--Inlets
   Of the nation's top 50 ports active in foreign waterborne commerce, over 90 percent require regular dredging. Over 392 million yd3 (300 million m3) of dredged material are removed from navigation channels each year, not including inland waterways. Most inlets and harbors used for commercial navigation in
Table 6--Inlet Condition Along the Southeast Atlantic and Gulf Coasts,December 2011 [Rice 2012b, p. 8] Existing inlets Artifi- cially closed Number Number Habitat modification type of of mo- inlets dified inlets Struc- Dredged Relo- Mined Artifi- tures * cated cially opened North 20 17 7 16 3 4 2 11 Carolina (85%) South 47 21 17 11 2 3 0 1 Carolina (45%) Georgia 23 6 (26%) 5 3 0 1 0 0 Florida east 21 19 19 16 0 3 10 0 (90%) Florida west 48 24 20 22 0 6 7 1 (50%) Alabama 4 4 4 3 0 0 0 2 (100%) Mississippi 6 5 (67%) 0 4 0 0 0 0 Louisiana 34 10 7 9 1 2 0 46 (29%) Texas 18 14 10 13 2 1 11 3 (78%) Total 221 119 89 97 8 (4%) 20 (9%) 30 64 (54%) (40%) (44%) (14%) * Structures include jetties, terminal groins, groin fields, rock or sandbag revetments, seawalls, and offshore breakwaters.
Shoreline Stabilization and Coastal Development--Future Practices
   As shown in tables 3 and 4 and explained above, much of the Atlantic and Gulf coasts are approaching "buildout," the condition that exists when all available land is either developed or preserved and no further development is possible. Table 3 shows that about one-third of dry land within 3.3 ft (1 m) of high tide on the Atlantic coast is still available for development (i.e., not already developed or preserved), but the percent of developable land in or near red knot habitats is probably lower because oceanfront beach areas are already more developed than other lands in this dataset (see Titus et al. 2009, p. 4). Focused on beach habitats, USFWS (2012a, p. 15) found that only about 20 percent of the coast from
   However, development pressures continue, driven by tourism (
   Although the likely extent of future coastal development is highly uncertain, continued efforts to protect existing and any new developments is more certain, at least over the next 10 to 20 years. As shown in tables 3 and 4, about 40 percent of the coast within the U.S. range of the red knot is already developed, and much of this area is protected by hard or soft means, or both. Shoreline stabilization over the near term is likely to come primarily through the maintenance of existing hard structures along with beach nourishment programs. As described below, it is unknown if these practices can be sustained in the longer term (CCSP 2009b, p. 87), but protection efforts seem likely to continue over shorter timeframes (Kana 2011, p. 34; Titus et al. 2009, pp. 2-3; Leatherman 1989, p. 2-27).
   States have shown a commitment to beach nourishment that is likely to persist. Of the 18 Atlantic and Gulf coast States with federally approved Coastal Zone Management Programs, 16 have beach nourishment policies. Nine of these 18 States have a continuing funding program for beach nourishment, and 6 more fund projects on a case-by-case basis (
   In attempting to infer the likely future quantity of red knot habitat, major sources of uncertainty are when and where the practice of routine beach nourishment may become unsustainable and how communities will respond. It is uncertain whether beach nourishment will be continued into the future due to economic constraints, as well as often limited supplies of suitable sand resources (CCSP 2009b, p. 49). Despite the current commitment to beach nourishment, it does seem likely that this practice will eventually become unsustainable. Given rising sea levels and increased intensity of storms predicted by climate change models, a steady increase in beach replenishment would be needed to maintain usable beaches and protect coastal development (NJDEP 2010, p. 3). For example,
   Even if it remains physically possible for beach nourishment to keep pace with sea level rise, this option may be constrained by cost and sand availability (Pietrafesa 2012, entire; NJDEP 2010, p. 2; Titus et al. 1991, entire; Leatherman 1989, entire). For example, there is a large deficit of readily available, nearshore sand in some coastal
   For the Atlantic and Gulf coasts, Titus et al. (1991, p. 24) estimated the cumulative cost of beach nourishment in 2100 at
   Table 7 shows the estimated nationwide quantities of sand needed to maintain current beaches (including the Pacific and
Table 7--Cumulative Nationwide Estimates of Sand Quantities Needed (in Millions of Cubic Yards) To Maintain Current Beaches Through Nourishment Under Various Sea Level Rise Scenarios [Leatherman 1989; p. 2-24] Global sea level rise by 2100/year 2.01 ft 3.65 ft 5.30 ft 6.94 ft (0.6 m) (1.1 m) (1.6 m) (2.1 m) 2020 405 531 654 778 2040 750 1,068 1,395 1,850 2100 2,424 4,345 6,768 9,071
   Under current policies, protection of coastal development is standard practice. However, coastal communities were designed and built without recognition of rising sea levels. Most protection structures are designed for current sea level and may not accommodate a significant rise (CCSP 2009b, p. 100). Policymakers have not decided whether the practice of protecting development should continue as sea level rises, or be modified to avoid adverse environmental consequences and increased costs of protecting coastal development (CCSP 2009b, p. 87; Titus et al. 2009, entire). It is unclear at what point different areas may be forced by economics or sediment availability to move beyond beach nourishment (Leatherman 1989, p. 2-27). Due to lower costs and sand recycling, sediment backpassing may prolong the ability of communities to maintain artificial beaches in some areas. However, in those times and places that artificial beach maintenance is abandoned, the remaining alternatives would likely be limited to either a retreat from the coast or increased use of hard structures to protect development (CCSP 2009b, p. 87; Defeo et al. 2009, p. 7;
   Hurricane Sandy recovery efforts show that retreat is not yet being contemplated as an option on the highly developed coasts of
Shoreline Stabilization and Coastal Development--Summary
   About 40 percent of the U.S. coastline within the range of the red knot is already developed, and much of this developed area is stabilized by a combination of existing hard structures and ongoing beach nourishment programs. In those portions of the range for which data are available (
Factor A--
   The red knot's breeding area is very sparsely developed, and development is not considered a threat in this part of the subspecies' range. We have little information about coastal development in the red knot's non-U.S. migration and wintering areas, compared to U.S. migration and wintering areas. However, escalating pressures caused by the combined effects of population growth, demographic shifts, economic development, and global climate change pose unprecedented threats to sandy beach ecosystems worldwide (DeFeo et al. 2009, p. 1; Schlacher et al. 2008a, p. 70).
International Development--Canada
   Cottage-building to support tourism and expansion of suburbs is taking place along coastal areas of the Bay of Fundy (Provinces of
   Although there is good potential for further tidal barrage development in
   At another important red knot stopover,
International Development--Central and
   Moving from north to south, below is the limited information we have about development in the red knot's Central and South American migration and wintering areas.
   In the Costa del Este area of
   Due to the region's remoteness, relatively little is known about threats to red knot habitat in
   Development is a threat to red knot stopover habitat along the Patagonian coast of
   Further south, the beaches along Bahia San Antonio,
   Habitat loss and deterioration are among the threats confronting the urban shorebird reserves at Rio Gallegos, an important red knot site in
   Two of
   Ongoing development continues to encroach in parts of Argentinean Tierra del Fuego, an important red knot wintering area (Niles et al. 2008, p. 17). In the area called
International Development--Summary
   Relative to
Factor A--Beach Cleaning
   On beaches that are heavily used for tourism, mechanical beach cleaning (also called beach grooming or raking) is a common practice to remove wrack (seaweed and other organic debris are deposited by the tides), litter, and other natural or manmade debris by raking or sieving the sand, often with heavy equipment (Defeo et al. 2009, p. 4). Beach raking became common practice in
   Practiced routinely, beach cleaning can cause considerable physical changes to the beach ecosystem. In addition to removing humanmade debris, beach cleaning and raking machines remove accumulated wrack, topographic depressions, emergent foredunes and hummocks, and sparse vegetation (USFWS 2012a, p. 28; Defeo et al. 2009, p. 4;
   Wrack removal also has significant ecological consequences, especially in regions with high levels of marine macrophyte (e.g., seaweed) production. The community structure of sandy beach macroinvertebrates can be closely linked to wrack deposits, which provide both a food source and a microhabitat refuge against desiccation (drying out). Wrack-associated animals, such as amphipods, isopods, and insects, are significantly reduced in species richness, abundance, and biomass by beach grooming (Defeo et al. 2009, p. 4). Invertebrates in the wrack are a primary prey base for some shorebirds such as piping plovers (USFWS 2012a, p. 28), but generally make up only a secondary part of the red knot diet (see the "Wintering and Migration Food" section of the Rufa Red Knot Ecology and Abundance supplemental document). Overall shorebird numbers are positively correlated with wrack cover and the biomass of their invertebrate prey that feed on wrack; therefore, grooming can lower bird numbers (USFWS 2012a, p. 28; Defeo et al. 2009, p. 4). Due to their specialization on benthic, intertidal mollusks, red knots may be less impacted by these effects than some other shorebird species. However, removal of wrack may cause more significant localized effects to red knots at those times and places where abundant mussel spat are attached to deposits of tide-cast material, or where red knots become more reliant on wrack-associated prey species such as amphipods, insects, and marine worms. In
   The heavy equipment used in beach grooming can cause disturbance to red knots (see Factor E--Human Disturbance, below). Only minimal disturbance is likely to occur on mid-Atlantic and northern Atlantic beaches because raking in these areas is most prevalent from
   In summary, the practice of intensive beach raking may cause physical changes to beaches that degrade their suitability as red knot habitat. Removal of wrack may also have an effect on the availability of red knot food resources, particularly in those times and places that birds are more reliant on wrack-associated prey items. Beach cleaning machines are likely to cause disturbance to roosting and foraging red knots, particularly in the U.S. wintering range. Mechanized beach cleaning is widespread within the red knot's U.S. range, particularly in developed areas. We anticipate beach grooming may expand in some areas that become more developed but may decrease in other areas due to increasing environmental regulations, such as restrictions on beach raking in piping plover nesting areas (e.g.,
Factor A--Invasive Vegetation
   Defeo et al. (2009, p. 6) cited biological invasions of both plants and animals as global threats to sandy beaches, with the potential to alter food webs, nutrient cycling, and invertebrate assemblages. Although the extent of the threat is uncertain, this may be due to poor survey coverage more than an absence of invasions. The propensity of invasive species to spread, and their tenacity once established, make them a persistent problem that is only partially countered by increasing awareness and willingness of beach managers to undertake control efforts (USFWS 2012a, p. 27). Like most invasive species, exotic coastal plants tend to reproduce and spread quickly and exhibit dense growth habits, often outcompeting native plants. If left uncontrolled, invasive plants can cause a habitat shift from open or sparsely vegetated sand to dense vegetation, resulting in the loss or degradation of red knot roosting habitat, which is especially important during high tides and migration periods. Many invasive species are either affecting or have the potential to affect coastal beaches (USFWS 2012a, p. 27), and thus red knot habitat.
   Beach vitex (Vitex rotundifolia) is a woody vine introduced into the Southeast as a dune stabilization and ornamental plant that has spread from
   Japanese (or Asiatic) sand sedge (Carex kobomugi) is a 4- to 12-in (10- to 30-cm) tall perennial sedge adapted to coastal beaches and dunes (
   Australian pine (Casuarina equisetifolia) is not a true pine, but is actually a flowering plant. Australian pine affects shorebirds by encroaching on foraging and roosting habitat and may also provide perches for avian predators (USFWS 2012a, p. 27;
   In summary, red knots require open habitats that allow them to see potential predators and that are away from tall perches used by avian predators. Invasive species, particularly woody species, degrade or eliminate the suitability of red knot roosting and foraging habitats by forming dense stands of vegetation. Although not a primary cause of habitat loss, invasive species can be a regionally important contributor to the overall loss and degradation of the red knot's nonbreeding habitat.
Factor A--Agriculture and Aquaculture
   In some localized areas within the red knot's range, agricultural activities or aquaculture are impacting habitat quantity and quality. For example, on the Magdalen Islands,
   Luckenbach (2007, p. 15) found that aquaculture of clams (Mercenaria mercenaria) in the lower
   Shrimp (Family Penaeidae, mainly Litopenaeus vannamei) farming has expanded rapidly in
   In the region of
   Farther west along the North-Central coast of
   On the east coast of
   The red knot wintering and stopover area of Rio Gallegos is located on the south coast of
   Grazing of the upland buffer is also a problem at Bahia Lomas in Chilean
   In summary, moderate numbers of red knots that winter or stopover in
Factor A--Breeding Habitat Loss From
   For several decades, surface air temperatures in
   To evaluate predicted changes in breeding habitat resulting from climate change, we note the eco-regional classification of the red knot's current breeding range. Most of the red knot's current breeding range (see supplemental document--Rufa Red Knot Ecology and Abundance--figure 1, and Niles et al. 2008, p. 16) is classified as High Arctic, although some known and potential nesting areas are at the northern limits of the Low Arctic zone (CAFF 2010, p. 11). Based on mapping by the
Arctic Warming--Eco-Regional Changes
   Arctic plants, animals, and microorganisms have adapted to climate change in the geologic past primarily by relocation, and their main response to future climate change is also likely to be through relocation. In many areas of
   Where their migration is not prevented by regional and geographic barriers, vegetation zones are generally expected to migrate north in response to warming conditions. Warming is "very likely" to lead to slow northward displacement of tundra by forests, while tundra will in turn displace High Arctic polar desert; tundra is projected to decrease to its smallest extent in the last 21,000 years, shrinking by a predicted 33 to 44 percent by 2100 (Feng et al. 2012, pp. 1359, 1366; Meltofte et al. 2007, p. 35; ACIA 2005, pp. 991, 998). Projections suggest that arctic ecosystems could change more in the next 100 years than they did over the last 6,000 years (
   Arctic communities are "very likely" to respond strongly and rapidly to high-latitude temperature change (ACIA 2005, p. 257). The likely initial response of arctic communities to warming is an increase in the diversity of plants, animals, and microbes, but reduced dominance of currently widespread species (ACIA 2005, p. 263). Species that are important community dominants are likely to have a particularly rapid and strong effect on ecosystem processes where regional warming occurs. Hemiarctic plant species (those that occur throughout
   Temperature is not the only factor that currently prevents some plant species from occurring in
   Studies have already documented shifts in arctic vegetation. For example, the "greenness" of North American tundra vegetation has increased during the period of satellite observations, 1982 to 2010 (Walker et al. in Richter-Menge et al. 2011, p. 89). Over the 29-year record,
   In addition, the disappearance of dense ice cover on large parts of the
   In addition to changes in plant communities and loss of sea ice, changes in freshwater hydrology of red knot breeding habitats are expected. Arctic freshwater systems, key foraging areas for red knots (Niles et al. 2008, p. 27), are particularly sensitive to even small changes in climatic regimes. Hydrologic processes may change gradually but may also respond abruptly as environmental thresholds are exceeded (ACIA 2005, p. 1012). Rising global temperatures are expected to result in permafrost degradation, possible decline in precipitation, and lowering of water tables, leading to drying of marshes and ponds in the southern parts of
Arctic Warming--Effects on Red Knot Habitat
   In the long term, loss of tundra breeding habitat is a serious threat to shorebird species. The preferred habitats of shorebird populations that breed in the High Arctic are predicted to decrease or disappear as vegetation zones move northward (Meltofte et al. 2007, p. 34; Lindstroem and Agrell 1999, p. 145). High Arctic shorebirds such as the red knot seem to be particularly at risk, because the High Arctic already constitutes a relatively limited area "squeezed in" between the extensive Low Arctic biome and the
   Potential impacts to shorebirds from changing arctic ecosystems go well beyond the loss of tundra breeding habitat (e.g., see
   It is unlikely that any major changes in the extent of Calidris canutus breeding habitat have occurred to date, but long-term changes in breeding habitat resulting from climate change are likely to negatively affect this species in the future (COSEWIC 2007, p. 16). Using two early-generation climate models and two different climate scenarios (temperature increases of 3 and 9 [degrees] F (1.7 and 5 [degrees] C)), Zoeckler and Lysenko (2000, pp. iii, 8) predicted 16 to 33 percent loss of breeding habitat across all Calidris canutus subspecies by 2070 to 2099. Some authors (Meltofte et al. 2007, p. 36; Piersma and Lindstroem 2004, p. 66) have suggested that the 16 to 33 percent prediction is low, in part because it does not reflect ecological changes beyond outright loss of tundra. In 2007, COSEWIC concluded that, as the High Arctic zone is expected to shift north, C. canutus is likely to be among the species most affected. This would be the case particularly for populations breeding toward the southern part of the High Arctic zone, such as the rufa subspecies breeding in the central Canadian Arctic (COSEWIC 2007, p. 40), as such areas would be the first converted from tundra vegetation to shrubs and trees.
   Using multiple, recent-generation climate models and three emissions scenarios, Feng et al. (2012, p. 1366) found that tundra in northern
   Vegetation changes may go beyond the replacement of tundra by forest and include the northward migration of vegetative subtypes within the remaining tundra zone. While predictions show forest establishment limited to the southern end of the red knot's current breeding range by 2100, migration of tundra subtypes may be widespread across the breeding range. A simulation by
Arctic Warming--Summary
   Arctic regions are warming much faster than the global average rates, and the Canadian Archipelago is predicted to experience some of the fastest warming in
Factor A--Conservation Efforts
   We are unaware of any broad-scale conservation measures to reduce the threat of destruction, modification, or curtailment of the red knot's habitat or range. Specifically, no conservation measures are specifically aimed at reducing sea level rise or warming conditions in
Factor A--Summary
   Within the nonbreeding portion of the range, red knot habitat is primarily threatened by the highly interrelated effects of sea level rise, shoreline stabilization, and coastal development. The primary red knot foraging habitats, intertidal flats and sandy beaches, will likely be locally or regionally inundated as sea levels rise, but replacement habitats are likely to re-form along eroding shorelines in their new positions. However, if shorelines experience a decades-long period of rapid sea level rise, high instability, and landward migration, the formation rate of new foraging habitats may be slower than the inundation rate of existing habitats. In addition, low-lying and narrow islands (e.g., in the
   Superimposed on changes from sea level rise are widespread human efforts to stabilize the shoreline, which are known to exacerbate losses of intertidal habitats by blocking their landward migration. About 40 percent of the U.S. coastline within the range of the red knot is already developed, and much of this developed area is stabilized by a combination of existing hard structures and ongoing beach nourishment programs. Hard stabilization structures and dredging degrade and often eliminate existing red knot habitats, and in many cases prevent the formation of new shorebird habitats. Beach nourishment may temporarily maintain suboptimal shorebird habitats where they would otherwise be lost as a result of hard structures, but beach nourishment also has adverse effects to red knots and their habitats. In those times and places where artificial beach maintenance is abandoned, the remaining alternatives available to coastal communities would likely be limited to either a retreat from the coast or increased use of hard structures to protect development. The quantity of red knot habitat would be markedly decreased by a proliferation of hard structures. Red knot habitat would be significantly increased by retreat, but only where hard stabilization structures do not exist or where they get dismantled. Relative to
   Lesser threats to nonbreeding habitat include beach cleaning, invasive vegetation, agriculture, and aquaculture. The practice of intensive beach raking may cause physical changes to beaches that degrade their suitability as red knot habitat. Although not a primary cause of habitat loss, invasive vegetation can be a regionally important contributor to the overall loss and degradation of the red knot's nonbreeding habitat. Agriculture and aquaculture are a minor but locally important contributor to overall loss and degradation of the red knot's nonbreeding habitat, particularly for moderate numbers of red knots that winter or stopover in
   Within the breeding portion of the range, the primary threat to red knot habitat is from climate change. With arctic warming, vegetation conditions on the breeding grounds are expected to change, causing the zone of nesting habitat to shift north and perhaps contract. These effects may be exacerbated by loss of sea ice. Arctic freshwater systems, foraging areas for red knots during the nesting season, are particularly sensitive to climate change. Unpredictable but profound ecosystem changes (e.g., interactions among predators, prey, and competitors) may also occur.
   Threats to the red knot from habitat destruction and modification are occurring throughout the entire range of the subspecies. These threats include climate change, shoreline stabilization, and coastal development, exacerbated regionally or locally by lesser habitat-related threats such as beach cleaning, invasive vegetation, agriculture, and aquaculture. The subspecies-level impacts from these activities are expected to continue into the future.
Factor B. Overutilization for Commercial, Recreational, Scientific, or Educational Purposes
   In this section, we discuss historic shorebird hunting in
Factor B--Hunting
   Since the late 19th century, hunters concerned about the future of wildlife and the outdoor tradition have made countless contributions to conservation. In many cases, managed hunting is an important tool for wildlife management. However, unregulated or illegal hunting can cause population declines, as was documented in the 1800s for red knots in
Hunting--
   Red knots were heavily hunted for both market and sport during the 19th and early 20th centuries (Harrington 2001, p. 22) in the Northeast and the mid-Atlantic. Red knot population declines were noted by several authors of the day, whose writings recorded a period of intensive hunting followed by the introduction of regulations and at least partial population recovery. As early as 1829, Wilson (1829, p. 140) described the red knot as a favorite among hunters and bringing a good market price. Giraud (1844, p. 225) described red knot hunting in the
   Mackay (1893, p. 29) described a practice on
   Shriner (1897, p. 94) reported, "This bird was formerly very plentiful in migrations in
   By 1927, Bent (1927, p. 132) noted signs of red knot population recovery, "Excessive shooting, both in spring and fall reduced this species to a pitiful remnant of its former numbers; but spring shooting was stopped before it was too late and afterwards this bird was wisely taken off the list of game birds; it has increased slowly since then, but is far from abundant now." Urner and Storer (1949, pp. 192-193) reached the same conclusion, and documented population increases along
Hunting--
   Both legal and illegal sport and subsistence hunting of shorebirds takes place in several known red knot wintering and migration stopover areas. This analysis focuses on areas where both red knots and hunting are known to occur, although in many areas we lack specific information regarding levels of red knot mortality from hunting. Therefore, we document the activity and explain that red knots could be affected, but draw no conclusions about direct mortality unless specifically noted.
   Moving from north to south, hunting is known from the
   Hunting birds is popular in
Current Hunting--Lesser Antilles Shooting Swamps
   In parts of the Lesser Antilles, legal sport hunters target shorebirds in "shooting swamps." Most of the migratory shorebird species breeding in eastern
Lesser Antilles--Barbados
   Barbados has a tradition of legal shorebird hunting that began with the colonists in the 17th and 18th centuries. The current shooting swamps were artificially created and can attract large numbers of migrant shorebirds during inclement weather. The open season for shorebirds is
   Although hunting pressure on shorebirds remains high, red knots have not been documented in
Lesser Antilles--French West Indies
   The French West Indies consist of
   Like Barbados, legal sport hunting of shorebirds has a long tradition on the French territories of
   Although shorebird hunting has been previously documented on
   Although the red knot was (until recently) listed as a game bird, mortality from hunting was probably low because red knots occur only in small numbers. In
Current Hunting--The Guianas
   Band recoveries indicate that red knots are killed commonly for food in some regions of
   Rice fields and other impoundments are prevalent in
   Harvest of any shorebirds has been illegal in Suriname since 2002, but there is little enforcement. Law enforcement is hampered by limited resources (e.g., working boats, gasoline), and several tens of thousands of shorebirds are trapped and shot each year. A 2006 survey indicated that virtually all shorebird species occurring in Suriname were illegally hunted and trapped in some quantity, with the lesser yellowlegs (Tringa flavipes) and semipalmated sandpiper (Calidris pusilla) being the dominant species. The survey also documented an illegal food trade of shorebirds, including selling to local markets. Shorebirds are harvested by shooting, netting, and using choke wires. Many shorebirds are taken by Guyanese fishermen working in Suriname. The Suriname coast is mainly mudflats and much of the coast is legally protected. Three coastal areas in Suriname are designated as sites of hemispheric importance by WHSRN, and it is likely that hunting occurs in at least two of them. Education and awareness programs have begun along the coast of Suriname, and a hunter training program is being developed (USFWS 2011e, p. 3).
   Red knots are primarily passage migrants in the Guyanas, with many more birds documented in
Current Hunting--Brazil
   Hunting migratory shorebirds for food was previously common among local communities in
   Commercial and recreational hunting are prohibited in all Brazilian territory, except for the state of Rio Grande do Sul, which includes the Logoa do Peixe stopover site. The Rio Grande do Sul hunting law provides a list of animals that can be hunted, prohibits trapping, and bans commercialized hunting (
Factor B--Scientific Study
   About 1,000 red knots per year are trapped for scientific study in
   Through 2008, about 50 of the birds caught in
   Considerable care is taken to minimize disturbance caused to shorebirds from these research activities. Numbers of birds per catch and total numbers caught over the season are limited, and careful handling protocols are followed, including a 3-hour limit on holding times (Niles et al. 2010a, p. 124;
Factor B--Conservation Efforts
   As discussed above, a few countries where shorebird hunting is legal have implemented voluntary restrictions on red knot hunting, increased hunter education efforts, established "no-shoot" shorebird refuges, and are developing models of sustainable harvest. Ongoing scientific research has benefitted red knot conservation in general and, through leg-band recoveries, has provided documentation of hunting-related mortality. Research activities adhere to best practices for the careful capture and handling of red knots.
Factor B--Summary
   Legal and illegal sport and market hunting in the mid-Atlantic and
   Threats to the red knot from overutilization for commercial, recreational, scientific, or educational purposes exist in parts of the
Factor C. Disease or Predation
   Red knots are exposed to several diseases and experience variable rates of predation from avian and mammalian predators throughout their range. In this section, we discuss known parasites and viruses, and the direct and indirect effects of predation in the red knot's breeding, wintering, and migration areas.
Factor C--Disease
   Red knots are exposed to parasites and disease throughout their annual cycle. Susceptibility to disease may be higher when the energy demands of migration have weakened the immune system. Studying red knots in
Disease--Parasites
   An epizootic disease (epidemic simultaneously affecting many animals) that caused illness or death of about 150 red knots on the west coast of
   On
   Blood parasites represent a complex, spatially heterogeneous host-parasite system having ecological and evolutionary impacts on host populations. Three closely related genera, (Plasmodium, Haemoproteus and Leucocytozoon) are commonly found in wild birds, and infections in highly susceptible species or age classes may result in death (D'Amico et al. 2008, p. 195). Reported red knot mortalities in
   In 2008, Escudero et al. (2012, pp. 362-363) observed a high prevalence of a Digenea parasitic flatworm (Bartolius pierrei) in clams (
   Ectoparasites, which live on the surface of the body, can affect birds by directly hindering their success in obtaining food and by acting as vectors and invertebrate hosts to microorganisms. For example, lice and mites infest skin and feathers leaving their hosts susceptible to secondary infections (D'Amico et al. 2008, p. 195). Individual red knots examined in 1968 (
   D'Amico et al. (2008, pp. 193, 197) examined red knots for ectoparasites at three sites in 2004 and 2005. All ectoparasites observed during this study were feather lice (Phthiraptera: Mallophaga (Amblycera)). Only 5 of 113 (4 percent) of red knots examined on
   Associating characteristics of breeding and wintering habitats, chick energetics, and apparent immunocompetence (the ability of the body to produce a normal immune response following exposure to disease), Piersma (1997, p. 623) suggested that shorebird species make tradeoffs of immune system function versus growth and sustained exercise. This author suggested that these tradeoffs determine the use of particular habitat types by long-distance migrating shorebirds. Some species appear restricted to parasite-poor habitats such as
   Species adapted to parasite-poor habitats may be particularly susceptible to parasites and pathogens (USFWS 2003, p. 22; Piersma 1997, p. 623). For example, captive Calidris canutus are susceptible to common avian pathogens (e.g., the avian pox virus, bacterial infections, feather lice), and reconstructing a marine environment (i.e., flushing the cages with seawater) helps to reduce at least the external signs of infections (Piersma 1997, pp. 624-625).
   In summary, three localized red knot die-off events have been attributed to parasites, but these kinds of parasites (sporozoans, hookworms) have not been documented elsewhere or implicated in further red knot mortality. Blood parasites have caused red knot deaths, but blood parasite infections were not detected by testing that took place across the knot's geographic range in the 2000s. In contrast, flatworm infection is widespread in
Disease--Viruses
   Type A influenza viruses, also called avian influenza (AI), are categorized by two types of glycoproteins on their surface, abbreviated HA and NA (or H and N when given in various combinations to identify a unique type of AI virus). The AI viruses are also classified as high or low pathogenicity (HPAI and LPAI). The term HPAI (high pathogenicity avian influenza) has a specific meaning relating to the ability of the virus to cause disease in experimentally inoculated chickens, and does not necessarily reflect the capacity of these viruses to produce disease in other species (
   Anseriformes (swans, geese, and ducks) and Charadriiformes (gulls and shorebirds) are the natural hosts of LPAI (FAO 2013;
   Since 1985, AI surveillance has been conducted annually from mid-May to early June in shorebirds and gulls in
   In wild red knots in
   Newcastle disease is a contagious bird disease (an avian paramyxovirus), and one of the most important poultry diseases worldwide. While people in direct contact with infected birds can get swelling and reddening of tissues around the eyes (conjunctivitis), no human cases of Newcastle disease have occurred from eating poultry products (
   From 2000 to 2005, Coffee et al. (2010, p. 481) tested 9,128 shorebirds and gulls of 33 species captured in 10 U.S. States and 3 countries in the
   Since 2002, migratory birds in
   For the most prevalent viruses found in shorebirds within the red knot's geographic range, infection rates in red knots are low, and health effects are minimal. We conclude that viral infections documented to date do not cause significant mortality and are not currently a threat to the red knot. However, see Cumulative Effects, below, regarding an unlikely but potentially high-impact, synergistic effect among avian influenza, environmental contaminants, and climate change in
Factor C--Predation
Predation--Nonbreeding Areas
   In wintering and migration areas, the most common predators of red knots are peregrine falcons (Falco peregrinus), harriers (Circus spp.), accipiters (Family Accipitridae), merlins (F. columbarius), shorteared owls (Asio flammeus), and greater black-backed gulls (Larus marinus) (Niles et al. 2008, p. 28). In addition to greater black-backed gulls, other large gulls (e.g. herring gulls (Larus argentatus)) are anecdotally known to prey on shorebirds (Breese 2010, p. 3). Predation by a great horned owl (Bubo virginianus) has been documented in
   Ellis et al. (2002, pp. 316-317) summarized the documented prey species taken by peregrine falcons in
   Peregrine falcons have been seen frequently along beaches in
   Raptor predation has been shown to be an important mortality factor for shorebirds at several sites (Piersma et al. 1993, p. 349). However, Niles et al. (2008, p. 28) concluded that increased raptor populations have not been shown to affect the size of shorebird populations. Based on studies of other Calidris canutus subspecies in the
   Red knots' selection of high-tide roosting areas on the coast appears to be strongly influenced by raptor predation, something well demonstrated in other shorebirds (Niles et al. 2008, p. 28). Red knots require roosting habitats away from vegetation and structures that could harbor predators (Niles et al. 2008, p. 63). Red knots' usage of foraging habitat can also be affected by the presence of predators, possibly affecting the birds' ability to prepare for their final flights to the arctic breeding grounds (Watts 2009b) (e.g., if the knots are pushed out of those areas with the highest prey density or quality). In 2010, horseshoe crab egg densities were very high in
   In addition to affecting habitat use, predation has been shown to affect migration strategies in Arctic-breeding shorebirds (Lank et al. 2003, p. 303). Studying two other Calidris species, Hope et al. (2011, p. 522) found that both adults and juveniles shortened their stopover durations during the period of increased peregrine falcon abundance. Butler et al. (2003, p. 132) demonstrated how recovering raptor populations in
   Red knots can also be affected by peregrines through repeated disturbance. Red knots in
   The vulnerability of red knots, and their reactivity to perceived predation danger, may be related to their field of vision. Studying other subspecies,
   In the United States, most peregrine falcons in coastal areas rely on artificial nest sites (Niles et al. 2008, p. 101). In some areas, land managers have begun to remove peregrine nesting platforms in strategic locations where they are having the greatest impact on shorebirds (Niles 2010a; Watts 2009b; Kalasz 2008, p. 39).
   Peregrine falcon populations in
   We conclude that, outside of the breeding grounds (which are discussed below), predation is not directly impacting red knot populations despite some direct mortality. At key stopover sites, however, localized predation pressures are likely to exacerbate other threats to red knot populations, such as habitat loss (Factor A), food shortages (Factor E), and asynchronies between the birds' stopover period and the occurrence of favorable food and weather conditions (Factor E). Predation pressures worsen these threats by pushing red knots out of otherwise suitable foraging and roosting habitats, causing disturbance, and possibly causing changes to stopover duration or other aspects of the migration strategy (see Cumulative Effects below).
Predation--Breeding Areas
   Although little information is available from the breeding grounds, the long-tailed jaeger (Stercorarius longicaudus) is prominently mentioned as a predator of red knot chicks in most accounts. Other avian predators include parasitic jaeger (S. parasiticus), pomarine jaeger (S. pomarinus), herring gull, glaucous gull (Larus hyperboreus), gyrfalcon (Falcon rusticolus), peregrine falcon, and snowy owl (Bubo scandiacus). Mammalian predators include arctic fox (Alopex lagopus) and sometimes arctic wolves (Canis lupus arctos) (Niles et al. 2008, p. 28; COSEWIC 2007, p. 19). Predation pressure on Arctic-nesting shorebird clutches varies widely regionally, interannually, and even within each nesting season, with nest losses to predators ranging from close to 0 percent to near 100 percent (Meltofte et al. 2007, p. 20), depending on ecological factors.
   Abundance of arctic rodents, such as lemmings, is often cyclical, although less so in
   In addition to affecting reproductive output, these cyclic predation pressures have been shown to influence shorebird nesting chronology and distribution. Studying 12 shorebird species, including red knot, over 11 years at 4 sites in the eastern Canadian Arctic, Smith et al. (2010a, pp. 292; 300) found that both snow conditions and predator abundance have significant effects on the chronology of breeding. Higher predator abundance resulted in earlier nesting than would be predicted by snow cover alone (Smith et al. 2010a, p. 292). Based on the adaptations of various species to deal with predators, Larson (1960, pp. 300-303) concluded that the distribution and abundance of Calidris canutus and other Arctic-breeding shorebirds were strongly influenced by arctic fox and rodent cycles, such that birds were in low numbers or absent in areas without lemmings because foxes preyed predominately on birds in those areas (as cited in
   Years with few lemmings and many predators can be extremely unproductive for red knots, although predator cycles are usually not uniform across all breeding areas so that in most years there is generally some production of young (Niles et al. 2008, p. 63). Unsuccessful breeding seasons contributed to at least some of the observed reductions in the red knot population in the 2000s. However, rodent-predator cycles have always affected the productivity of Arctic-breeding shorebirds and have generally caused only minor year-to-year changes in otherwise stable populations (Niles et al. 2008, pp. 64, 101).
   In northern
   At two sites in northeast
   Disruption of rodent-predator cycles may constitute a large-scale impact on predation pressure on arctic shorebird nests (Meltofte et al. 2007, p. 22). In the Siberian Arctic, lemmings are keystone species, and any climate effects on their abundance or population dynamics may indirectly affect shorebird populations through predation. The role of lemmings in the eastern Canadian Arctic is unclear, but large annual fluctuations in lemming or other rodent populations suggest that similar dynamics operate there (Meltofte et al. 2007, p. 34).
   McKinnon et al. (2010, p. 326) used artificial nests to measure predation risk along a 2,083-mi (3,350-km) south-north gradient in the Canadian Arctic and found that nest predation risk declined more than twofold along the latitudinal gradient. The study area included the entire latitudinal range of known and modeled red knot breeding habitat, extending both farther south (into the sub-Arctic) and farther north (to encompass the breeding range of Calidris canutus islandica). Nest predation risk was negatively correlated with latitude. For an increase in 1 [degrees] of latitude, the relative risk of predation declined by 3.6 percent, equating to a 65 percent decrease in predation risk over the 29 [degrees] latitudinal transect. The results provide evidence that birds migrating farther north may acquire reproductive benefits in the form of lower nest predation risk (McKinnon et al. 2010, p. 326). Predation pressure on red knots could increase if, due to climate change, a new suite of predators expands their ranges northward from the sub-Arctic into the knot's breeding range.
   We conclude that cyclic predation in
Factor C--Conservation Efforts
   We are unaware of any conservation efforts to reduce disease in red knots. We are also unaware of any conservation efforts to reduce predation of the red knot in its breeding range. As discussed above, land managers in some areas of
Factor C--Summary
   Red knots may be adapted to parasite-poor habitats and may, therefore, be susceptible to parasites when migrating or wintering in high-parasite regions. However, we have no evidence that parasites have affected red knot populations beyond causing normal, background levels of mortality, and we have no indications that parasite infection rates or red knot fitness impacts are likely to increase. Therefore, we conclude that parasites are not a threat to the red knot. For the most prevalent viruses found in shorebirds within the red knot's geographic range, infection rates in red knots are low, and health effects are minimal or have not been documented. Therefore, we conclude that viral infections do not cause significant mortality and are not a threat to the red knot. However, see Cumulative Effects (below) regarding an unlikely but potentially high-impact, synergistic effect among avian influenza, environmental contaminants, and climate change in
   Outside of the breeding grounds, predation is not affecting red knot populations despite some direct mortality. At key stopover sites, however, localized predation pressures are likely to exacerbate other threats to red knot populations by pushing red knots out of otherwise suitable foraging and roosting habitats, causing disturbance, and possibly causing changes to stopover duration or other aspects of the migration strategy. We expect the direct and indirect effects of predators to continue at the same level or decrease slightly over the next few decades.
   Within the breeding range, normal 3- to 4-year cycles of high predation, mediated by rodent cycles, result in years with extremely low reproductive output but do not threaten the survival of the red knot at the subspecies level. However, these rodent-predator cycles are being interrupted for reasons that are not yet fully clear but may be linked to climate change. Disruptions in the rodent-predator cycle pose a substantial threat to the red knot, as they may result in prolonged periods of very low reproductive output. Such disruptions have already occurred and may increase due to climate change. The substantial impacts of elevated egg and chick predation on shorebird reproduction are well known, although the red knot's capacity to adapt to long-term changes in predation pressure is unknown. The threat of persistent increases in predation in
Factor D. The Inadequacy of Existing Regulatory Mechanisms
   Under this factor, we examine the effects of existing regulatory mechanisms in relation to the threats to the red knot discussed under the other four factors. Section 4(b)(1)(A) of the Act requires the Service to take into account "those efforts, if any, being made by any State or foreign nation, or any political subdivision of a State or foreign nation, to protect such species . . ." In relation to Factor D under the Act, we interpret this language to require the Service to consider relevant Federal, state, and tribal laws, regulations, and other such mechanisms that may reduce any of the threats we describe in our threat analyses under the other four factors. We give strongest weight to statutes and their implementing regulations and to management direction that stems from those laws and regulations. An example would be State governmental actions enforced under a State statute, or Federal actions under Federal statute.
   A comprehensive discussion of international, Federal, State, and local laws, regulations, policies, and treaties that apply to the red knot is available as a supplemental document ("Factor D: The Inadequacy of Existing Regulatory Mechanisms") on the Internet at http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see ADDRESSES section for further access instructions). We provide a brief summary below.
   In Canada, the Species at Risk Act provides protections for the red knot and its habitat, both on and off Federal lands. The red knot is afforded additional protections under the Migratory Birds Convention Act and by provincial law in four of
   Within the United States, the Migratory Bird Treaty Act of 1918 (16 U.S.C.
   There are no provisions in the MBTA that prevent habitat destruction unless the activity causes direct mortality or the destruction of active nests, which would not apply since red knots do not breed in
   Among coastal States from
   As discussed under Factors A and E, shoreline stabilization has significant impacts on red knot habitats, and can also impact knots through disturbance and via impacts on prey resources. Shoreline stabilization is often federally funded (e.g., through the Water Resources Development Acts) or authorized (e.g., under section 404 of the Clean Water Act (33 U.S.C.
   The Coastal Zone Management Act of 1972 (Pub. L. 92-583) (86
   Other threats to habitat and food supplies and from disturbance are partially, but not fully, abated by various State and Federal regulations. First, State regulations provide varying levels of protection from impacts associated with beach grooming (i.e., mechanical raking or cleaning), but we do not have comprehensive information for each State. Above the high tide line, beach grooming activities are typically not regulated by the USACE, and thus fall under State and local jurisdictions. In those jurisdictions for which information is available, beach grooming is generally permitted in red knot habitat, including while the birds are present. Second, several Federal and State regulatory and nonregulatory measures are in effect to stem the introductions and effects of invasive and harmful species (e.g., Executive Order 13112; the Plant Protection Act of 2000 (Pub. L. 106-224); the Nonindigenous Aquatic Nuisance Prevention and Control Act of 1990 (Pub. L. 101-646); the National Invasive Species Act of 1996 (Pub. L. 104-332); the
   In addition to above-mentioned regulatory mechanisms addressing threats to habitat, food resources, and from disturbance, there are Federal laws and policies to reduce the red knot's collision risks from new terrestrial and offshore wind turbine development (e.g., construction and operation). The MBTA applies to all Federal and non-Federal activities that result in the "take" of migratory birds. To assist wind developers comply with MBTA, the Service's voluntary Land-Based Wind Energy Guidelines provide a structured, scientific process for addressing wildlife conservation concerns at all stages of land-based wind energy development (USFWS 2012d, p. vi). In addition to the MBTA, other Federal regulatory mechanisms and nonregulatory policies (e.g., NEPA, Executive Order 13186, NSPOA, NWRSIA, and section 10 of the Endangered Species Act) may apply to terrestrial wind energy development, depending on the nature of the Federal nexus, if any, in turbine construction and operation. Regarding offshore wind energy development, section 388 of the Energy Policy Act of 2005 granted the DOI discretionary authority to issue leases, easements, or rights-of-way for activities on the OSC for wind and other types of renewable energy development. Under NEPA, DOI has prepared a Programmatic Environmental Impact Statement setting forth policies and best management practices, and has promulgated regulations and guidelines (
Factor E. Other Natural or Manmade Factors Affecting Its Continued Existence
   In this section, we present and assess the best available information regarding a range of other ongoing and emerging threats to the red knot, including reduced food availability, asynchronies ("mismatches") between the timing of the red knot's annual cycle and the windows of optimal food and weather conditions on which it depends, human disturbance, oil spills, environmental contaminants, and wind energy development.
Factor E--Reduced Food Availability
   Declining food resources can have major implications for the survival and reproduction of long-distance migrant shorebirds (
   Commercial harvest of horseshoe crabs has been implicated as a causal factor in the decline of the rufa red knot, by decreasing the availability of horseshoe crab eggs in the
Food Availability--Ocean Acidification
   During most of the year, bivalves and other mollusks are the primary prey for the red knot (see the "Migration and Wintering Food" section of the Rufa Red Knot Ecology and Abundance supplemental document). Mollusks in general are at risk from climate change-induced ocean acidification (Fabry et al. 2008, pp. 419-420). Oceans become more acidic as carbon dioxide emitted into the atmosphere dissolves in the ocean. The pH (percent hydrogen, a measure of acidity or alkalinity) level of the oceans has decreased by approximately 0.1 pH units since preindustrial times, which is equivalent to a 25 percent increase in acidity. By 2100, the pH level of the oceans is projected to decrease by an additional 0.3 to 0.4 units under the highest emissions scenarios (NRC 2010, pp. 285-286). As ocean acidification increases, the availability of calcium carbonate declines. Calcium carbonate is a key building block for the shells of many marine organisms, including bivalves and other mollusks (USEPA 2012; NRC 2010, p. 286). Vulnerability to ocean acidification has been shown in bivalve species similar to those favored by red knots, including mussels (Gaylord et al. 2011, p. 2586; Bibby et al. 2008, p. 67) and clams (Green et al. 2009, p. 1037). Reduced calcification rates and calcium metabolism are also expected to affect several mollusks and crustaceans that inhabit sandy beaches (Defeo et al. 2009, p. 8), the primary nonbreeding habitat for red knots. Relevant to
   To study the effects of ocean acidification on marine invertebrates, Hale et al. (2011, p. 661) collected representative species, including mollusks, from the extreme low intertidal zone and exposed them in the laboratory to varying levels of pH and temperature. These authors found significant changes in community structure and lower diversity in response to reduced pH. At lower pH levels, warmer temperatures resulted in lower species abundances and diversity. The species losses responsible for these changes in community structure and diversity were not randomly distributed across the different phyla examined, with mollusks showing the greatest reduction in abundance and diversity in response to low pH and elevated temperature. This and other studies support the idea that ocean acidification-induced changes in marine biodiversity will be driven by differential vulnerability within and between different taxonomic groups. This study also illustrates the importance of considering indirect effects that occur within multispecies assemblages when attempting to predict the consequences of ocean acidification and global warming on marine communities (Hale et al. 2011, p. 661). With climate change, interactions between temperature and pH may cause detrimental ecological changes to red knot prey species at both wintering and migration stopover areas.
Food Availability--Temperature Changes
  &#160;In addition to being sensitive to acidification, mollusks and other marine invertebrates are sensitive to temperature changes. Global average air temperature is expected to warm at least twice as much in the next century as it has over the previous century, with an expected increase of 2 to 11.5 [degrees] F (1.1 to 6.4 [degrees] C) by 2100 (USEPA 2012). Coastal waters are "very likely" to continue to warm by as much as 4 to 8 [degrees] F (2.2 to 4.4 [degrees] C) in this century, both in summer and winter (USGCRP 2009, p. 151). In the mid-Atlantic, changes in water temperature (and quality) are expected to have mostly indirect effects on red knots and other shorebirds, primarily through changes in the distribution and abundance of food resources (Najjar et al. 2000, p. 227). Changes in sea temperatures can have major effects on marine populations, as witnessed during severe events such as
   Asynchronies ("mismatches") between the timing of the red knot's annual cycle and the peak abundance periods of its prey are discussed in the next section. However, repeated asynchronies can also occur between a prey species' own annual cycles and environmental conditions, leading to long-term declines of these invertebrate populations and thereby affecting the absolute quantity of red knot food supplies (in addition to the timing). For example, Philippart et al. (2003, p. 2171) found that rising water temperatures upset the timing of reproduction in the intertidal bivalve Macoma balthica, with the timing of the first vulnerable life stages thrown out of sync with respect to the most optimal environmental conditions (a phytoplankton bloom and the settlement of juvenile shrimps). These authors concluded that prolonged periods of lowered bivalve recruitment and stocks may lead to a reformulation of estuarine food webs and possibly a reduction of the resilience of the system to additional disturbances, such as shellfish harvest (Philippart et al. 2003, p. 2171).
   Blue mussel spat is an important prey item for red knots in
Food Availability--Other Aspects of Climate Change
   Invertebrate prey species may also be affected by other aspects of climate change. For example, freshwater inputs, tidal prisms (the volume of water in an estuary between high and low tide), and salinity regimes may be much altered, which could significantly alter the composition of estuarine communities. Furthermore, rising sea levels are expected to affect the physical shape (e.g., dimensions, configuration) of estuaries, changing their sediment compositions. This habitat change in turn would change invertebrate densities and community composition, thus affecting shorebirds (Rehfisch and Crick 2003, p. 88; Najjar et al. 2000, p. 225), such as the red knot.
Food Availability--Disease, Parasites, Invasive Species, and Unknown Factors
   Red knot prey species are also vulnerable to disease, parasites, invasive species, and unknown factors influencing their quality and quantity. For example, at the single largest wintering area, Bahia Lomas on
   In Rio Grande,
   Globally, coastal marine habitats are among the most heavily invaded systems, stemming in part from human-mediated transport of nonnative species in the ballast of ships and from intentional introductions for aquaculture and fisheries enhancement (Grosholz 2002, p. 22). For example, introduction of nonnative oysters (Crassostrea spp.) has been widespread within the range of the red knot (Ruesink et al. 2005, p. C-1). Worldwide, introduced oysters have been vectors for several invasive species of marine algae, invertebrates, and protozoa (Ruesink et al. 2005, pp. 669-670). Invasive species can cause disease in native mollusks, displace native invertebrates through competition or predation, alter ecosystems, and affect species at higher trophic levels such as shorebirds (Ruesink et al. 2005, pp. 671-674; Grosholz 2002, p. 23).
Food Availability--Sediment Placement
   The quantity and quality of red knot prey may also be affected by the placement of sediment for beach nourishment or disposal of dredged material (see Factor A above for a discussion of the extent of these practices in
   The invertebrate community structure and size class distribution following sediment placement may differ considerably from the original community (Zajac and Whitlatch 2003, p. 101;
   Beach nourishment is a regular practice on the
Food Availability--Recreational Activities
   Recreational activities can likewise affect the availability of shorebird food resources by causing direct mortality of prey. Studies from
   Although pedestrians exert relatively low ground pressures, extremely heavy foot traffic can cause direct crushing of intertidal invertebrates. In
   In many areas, habitat for the piping plover overlaps considerably with red knot habitats. A preliminary review of ORV use at piping plover wintering locations (from
   Some early studies found minimal impacts to intertidal beach invertebrates from ORV use (Steinback and Ginsberg 2009, pp. 4-6; Van der Merwe and Van der Merwe 1991, p. 211;
   Other studies have found higher impacts to benthic invertebrates from driving (
   In summary, several studies have shown impacts from recreational activities on invertebrate species typical of those used by red knots, and in similar habitats. The extent to which mortality of beach invertebrates from recreational activities propagates through food webs is unresolved (Defeo et al. 2009, p. 3). However, we conclude that these activities likely cause at least localized reductions in red knot prey availability.
Food Availability--Horseshoe Crab Harvest
   Reduced food availability at the
   Under the current management framework (known as Adaptive Resource Management, or ARM), the present horseshoe crab harvest is not considered a threat to the red knot because harvest levels are tied to red knot populations via scientific modeling. Most data suggest that the volume of horseshoe crab eggs is currently sufficient to support the
   Many studies have established that red knots stopping over in
   The causal chain from horseshoe crab harvest to red knot populations has several links, each with different lines of supporting evidence and various levels of uncertainty: (a) Horseshoe crab harvest levels and
Horseshoe Crab--Harvest and Population Levels (Link A)
   Historically, horseshoe crabs were harvested commercially for fertilizer and livestock feed. From the mid-1800s to the mid-1900s, harvest ranged from about 1 to 5 million crabs annually. Harvest numbers dropped to 250,000 to 500,000 crabs annually in the 1950s, which are considered the low point of horseshoe crab abundance. Only about 42,000 crabs were reported annually by the early 1960s. Early harvest records should be viewed with caution due to probable underreporting. The substantial commercial-scale harvesting of horseshoe crabs ceased in the 1960s (ASMFC 2009, p. 1). By 1977, the spawning population of horseshoe crabs in
   During the 1990s, reported commercial harvest of horseshoe crabs on the Atlantic coast of
   Although also used in scientific research and for other medical purposes, the major biomedical use of horseshoe crabs is in the production of Limulus Amebocyte Lysate (LAL). The LAL is a clotting agent in horseshoe crab blood that makes it possible to detect human pathogens in patients, drugs, and intravenous devices (ASMFC 2009, p. 2). The "LAL test" is currently the worldwide standard for screening medical equipment and injectable drugs for bacterial contamination (ASMFC 2009, p. 2; ASMFC 1998, p. 12). Horseshoe crab blood is obtained from adult crabs that are released alive after extraction is complete (ASMFC 2009, p. 2) or that are sold into the bait market (ASMFC 2009, p. 18). The ASMFC previously assumed a constant 15 percent mortality rate for bled crabs that are not turned over to the bait fishery (ASMFC 2009, p. 3) but now considers a range from 5 to 30 percent mortality (ASMFC 2012a, p. 6) more appropriate. The estimated mortality rate includes all crabs rejected for biomedical use any time between capture and release.
   Bait harvest and biomedical collection have been managed separately by the ASMFC since 1999 (ASMFC 1998, pp. iii-57). Biomedical collection is currently not capped, but ASMFC considers implementing action to reduce mortality if estimated mortality exceeds a threshold of 57,500 crabs. This threshold has been exceeded several times, but thus far the ASMFC has opted only to issue voluntary guidelines to the biomedical industry (ASMFC 2009, p. 18). The ASMFC implemented key reductions in the bait harvest in 2000, 2004, and 2006 (ASMFC 2009, p. 3), and several member States have voluntarily restricted harvests below their allotted quotas (ASMFC 2012a, pp. 4, 13; N.J.S.A. 23:2B-21; N.J.R. 2139(a)). Along with the widespread use of bait-saving devices, these restrictions reduced reported landings (ASMFC 2009, p. 1) from 1998 to 2011 by over 75 percent (table 9). Further, a growing number of horseshoe crabs are being biomedically bled first before being used as bait; because such crabs count against harvest quotas (ASMFC 2012a, p. 6), this practice helps reduce total mortality rates. In addition, the
   Evidence that commercial harvests caused horseshoe crab population declines in recent decades comes primarily from a strong temporal correlation between harvest levels (as measured by reported landings, tables 8 and 9) and population levels (as characterized by ASMFC during stock assessments).
Link A, Part 1--Horseshoe Crab Harvest Levels
   The horseshoe crab landings given in pounds in tables 8 and 9 come from data reported to NMFS, but should be viewed with caution as these records are often incomplete and represent an underestimate of actual harvest (ASMFC 1998, p. 6). In addition, reporting has increased over the years, and the conversion factors used to convert crab numbers to pounds have varied widely. Despite these inaccuracies, the reported landings show that commercial harvest of horseshoe crabs increased substantially from 1990 to 1998 and has generally declined since then (ASMFC 2009, p. 2). The ASMFC (1998, p. 6) also considered other data sources to corroborate a significant increase in harvest in the 1990s. These landings (pounds) may include biomedical collection, live trade, and bait fishery harvests (ASMFC 2009, p. 17).
   Table 9 also shows the number of crabs harvested for bait, and the estimated number of crabs killed incidental to biomedical collection, as reported to ASMFC. Since 1998, States have been required to report annual bait landings to ASMFC, which considers these data reliable (ASMFC 2009, p. 2). A subtotal of the bait harvest is shown for the
   Estimates of biomedical collection increased from 130,000 crabs in 1989 to 260,000 in 1997 (ASMFC 2004, p. 12). Since mandatory reporting requirements took effect in 2004, biomedical-only crabs collected (i.e., crabs not counted against State bait harvest quotas) rose from 292,760 in 2004 (ASMFC 2009, pp. 18, 41) to 545,164 in 2011 (ASMFC 2012a, p. 6). Total estimated mortality of biomedical crabs for 2011 was 80,827 crabs (using a 15 percent post-release estimated mortality; see table 9), with a range of 31,554 to 154,737 crabs (using 5 to 30 percent estimated mortality) (ASMFC 2012a, p. 6). Using a constant 15 percent mortality of bled crabs, the estimated contribution of biomedical collection to total (biomedical plus bait) mortality rose from about 6 percent in 2004 to about 11 percent in 2011.
   To put the reported harvest numbers in context, two recent assessments using different methods both estimated the population of horseshoe crabs in the
Table 8--Reported Atlantic Coast Horseshoe Crab Landings (Pounds), 1970 to 2011 [NOAA 2012d] Year Total Year Total pounds pounds reported reported to NMFS to NMFS 1970 15,900 1991 385,487 1971 11,900 1992 321,995 1972 42,000 1993 821,205 1973 88,700 1994 1,171,571 1974 16,700 1995 2,416,168 1975 62,800 1996 5,159,326 1976 2,043,100 1997 5,983,033 1977 473,000 1998 6,835,305 1978 728,500 1999 5,246,598 1979 1,215,630 2000 3,756,475 1980 566,447 2001 2,336,645 1981 326,695 2002 2,772,010 1982 526,700 2003 2,624,248 1983 468,600 2004 974,425 1984 225,112 2005 1,421,957 1985 614,939 2006 1,548,900 1986 635,823 2007 1,804,968 1987 511,758 2008 1,315,963 1988 688,839 2009 1,830,506 1989 1,106,645 2010 869,630 1990 519,057 2011 1,497,462
Table 9--Reported Atlantic Coast Horseshoe Crab Landings (Pounds and Crabs), 1998 to 2011 [(A. Nelson Pers . Comm.February 22, 2013 andNovember 27, 2012 ; ASMFC 2012a, pp. 6, 13; NOAA 2012d; ASMFC 2009, pp. 38-41); ND = No Data Available] Year Total pounds Numbers of Numbers of Estimated reported to crabs crabs numbers of NMFS harvested for harvested for crabs killed (from Table 8) bait reported bait reported by to ASMFC to ASMFC, biomedical Delaware Bay collection, Region based on 15 subtotal percent of the total biomedical collection reported to ASMFC 1998 6,835,305 2,748,585 862,462 ND 1999 5,246,598 2,600,914 1,013,996 ND 2000 3,756,475 1,903,415 767,988 ND 2001 2,336,645 1,013,697 607,602 ND 2002 2,772,010 1,265,925 728,266 ND 2003 2,624,248 1,052,493 584,394 ND 2004 974,425 681,323 278,280 45,670 2005 1,421,957 769,429 347,927 44,830 2006 1,548,900 840,944 270,241 49,182 2007 1,804,968 827,554 169,255 63,432 2008 1,315,963 660,794 190,828 63,285 2009 1,830,506 756,484 250,699 60,642 2010 869,630 604,548 165,852 75,428 2011 1,497,462 650,539 195,153 80,827
Link A, Part 2--Horseshoe Crab Population Levels
   Through stock assessments, ASMFC analyzes horseshoe crab data from many different independent surveys and models (ASMFC 2004, pp. 14-24; ASMFC 2009, pp. 14-23). In the 2004 assessment, ASMFC found a clear preponderance of evidence that horseshoe crab populations in the
   Though no formal horseshoe crab stock assessment has been conducted since 2009, the ASMFC's Delaware Bay Ecosystem Technical Committee recently reviewed current data from the same trawl and dredge surveys that were evaluated in the 2004 and 2009 assessments. From these data, the committee concluded that declines were observed during the 1990s, stabilization occurred in the early 2000s, various indicators have differed with no consistent trends since 2005, confidence intervals are large, there is no clear trend apparent in recent data, and the population has at least stabilized (ASMFC 2012c, pp. 10-12). These conclusions generally support the link between harvest levels and available indicators of horseshoe crab abundance. The committee noted, however, that sustained horseshoe crab population increases have not been realized as expected. The reasons for this stagnation are unknown, and a recent change in sex ratios is also unexplained (i.e., several surveys found that the ratio of males to females increased sharply since 2010 despite several years of reduced female harvests) (S.
    * Insufficient time since management actions were taken. There would likely be at least a 10-year time lag between fishery restrictions and significant population changes, corresponding to the horseshoe crab's estimated age at sexual maturity (Sweka et al. 2007, p. 285; ASMFC 2004, p. 31). Based on modeling, Davis et al. (2006, p. 222) found that the horseshoe crab population in the
    * An early life-history (recruitment) bottleneck. Sweka et al. (2007, pp. 277, 282, 284) found that early-life-stage mortality, particularly mortality during the first year of life, was the most important parameter affecting modeled population growth, and that estimates of egg mortality have high uncertainty.
    * Undocumented or underestimated mortality.
    * One possible source of error is the use of a constant 15 percent mortality for biomedically bled crabs. Leschen and Correia (2010a, p. 135) reported mortality rates of nearly 30 percent, although this result has been disputed (Dawson 2010, pp. 2-3; Leschen and Correia 2010b, pp. 8-10). The ASMFC now considers a range from 5 to 30 percent mortality (ASMFC 2012a, p. 6).
    * Poaching may be another factor, as documented by enforcement actions in
    * The harvest of horseshoe crabs from Federal waters that are not landed in any state, but exchanged directly to a dependent fishery, is unregulated, and, therefore, the magnitude of any such harvest is unknown (ASMFC 1998, p. 27). However, there is no evidence that such boat-to-boat transfers are occurring, and the level of any such unreported harvest is thought to be small and unlikely to have population-level effects (
    * The extent of horseshoe crab mortality due to bycatch from other fisheries is unknown (ASMFC 1998, pp. 22, 26); however, at least one State does regulate and limit such bycatch (
    * Limitations in the ability of surveys to capture trends. Inherent variability in most of the data sets decreases the predictive power of the surveys, especially over short time periods. For the majority of horseshoe crab indices, detecting small changes in population size would require 10 to 15 years of data. Over the short term, these indices would be able to identify only a catastrophic decline in the horseshoe crab population (ASMFC 2004, p. 31).
    * An ecological shift. Examples are available from other fisheries, such as weakfish (Cynoscion regalis). The weakfish quota was dramatically cut, but the population never rebounded. Despite some years of excellent recruitment, adult weakfish stocks have not recovered perhaps due to increased predation (S. Doctor pers. comm.
   In addition to the aforementioned potential causes for lack of recent growth in horseshoe crab populations, threats to horseshoe crab spawning habitat are discussed under Factor A above. Another potential threat to horseshoe crab populations recently emerged--the proposed importation of nonnative horseshoe crab species for use as bait. Nonnative species could carry diseases and parasites that could put the native species at risk, and exports to the U.S. bait market could hasten declines in the Asian species, which is discussed below. The Service currently lacks the regulatory authority to restrict the importation of these species on the Federal level (i.e., under the Lacey Act, see supplemental document--Factor D), although Congress is deliberating legislation to expand that authority (USFWS 2013, pp. 1-2). In the meantime, ASMFC has recommended that all member States ban the import and use of Asian horseshoe crabs as bait in State water fisheries along the Atlantic coast (ASMFC 2013, entire), although no such State bans have yet gone into effect.
   Asian horseshoe crab species are themselves in decline (ASMFC 2013, p. 2), and their status could indirectly affect the American species. Chinese scientists have reported rapid growth in biomedical collection and correspondingly rapid population declines in harvested populations. Anecdotal observations and predictions from scientists close to the industry suggest that such harvest is unsustainable. If the Asian biomedical industry were to collapse due to exhausted stocks of these species, then the worldwide demand for amebocyte lysate would be focused on the American horseshoe crab alone, potentially increasing biomedical collection pressure in
Horseshoe Crab--Crab Population and
   Attempts have generally not been made to tie weight gain in red knots during the spring stopover to the total horseshoe crab population size in the
Link B, Part 1--Horseshoe Crab Spawning Abundance
   A baywide horseshoe crab spawning survey has been conducted under consistent protocols since 1999. Based on data through 2011, numbers of spawning females have not increased or decreased, while numbers of spawning males showed a statistically significant increase. Though not statistically significant, female crab trends were negative in
   Strong evidence for a link between numbers of spawning crabs and red knot weight gain comes from the modeling that underpins the ARM. The probability that a bird arriving at
Link B, Part 2--Horseshoe Crab Egg Density
   Due to the considerable vertical redistribution (digging up) of buried eggs (4 to 8 in (10 to 20 cm) deep) by waves and further spawning activity, surface egg densities (in the top 2 in (5 cm) of sediment) are not necessarily correlated with the density of spawning horseshoe crabs (Smith et al. 2002b, p. 733). Therefore, egg density surveys are not meant as an index of horseshoe crab abundance. Instead, attempts have been made to use the density of eggs in the top few inches of sediment as an index of food availability for shorebirds (Dey et al. 2013, p. 8), for example by correlating these egg densities with red knot weight gain.
   Egg density surveys were conducted in New Jersey in 1985, 1986, 1990, and 1991, and annually since 1996. Surveys have been carried out in Delaware since 1997. Methodologies have evolved over time, but have been relatively consistent since 2005. Direct comparisons between New Jersey and Delaware egg density data are inappropriate due to differences in survey methodology between the two States, despite standardization efforts (ASMFC 2012d, pp. 11-12; Niles et al. 2008, pp. 33, 44, 46).
   Niles et al. (2008, p. 45) reported egg densities from 1985, 1986, 1990, and 1991 an order of magnitude higher than for the period starting in 1996. Conversion factors were developed to allow for comparison between the 1985 to 1986 and the 1990 to 1991 data points (Niles et al. 2008, p. 44), and statistical analysis found that data points from 2000 to 2004 can be directly compared to those from 2005 to 2012 without a conversion factor (i.e., a 2005 change in sampling method did not affect the egg density results) (Dey et al. 2011b, p. 12). However, comparisons between the earlier data points (1985 to 1999) and egg densities since 2000 are confounded by changes in methodology and investigators, and lack of conversion factors.
   Higher confidence is attached to trends since 2005 because methodologies have been consistent over that period. The ASMFC's Delaware Bay Ecosystem Technical Committee recently reviewed the most current egg density data from both States. The committee concluded there was no significant trend in baywide egg densities from 2005 to 2012. Looking at the two States separately, Delaware showed no significant trend in egg density, while the trends in New Jersey were positive. Markedly higher egg densities on some beaches (e.g.,
   Using data from 2005 to 2012, Dey et al. (2013, pp. 8, 18) found a statistically strong relationship between the proportion of red knots reaching the estimated optimal departure weight (6.3 oz (180 g) or more) from
   Regarding the egg surveys, samples are similarly collected across the bay, but egg separation and counting methodologies are substantially different between New Jersey and Delaware and have not been fully documented in either State. In addition, very high spatial and temporal variability in surface egg densities limits the statistical power of the surveys (ASMFC 2012d, p. 11). Based on the sampling methodology used in both States (Dey et al. 2011b, pp. 3-4), the surveys would be expected to have only about a 75 percent chance of detecting a major (50 percent) decline in egg density over 5 years (Pooler et al. 2003, p. 700). In addition, the sampled segments on a particular beach may not be representative of egg densities throughout that larger beach (Pooler et al. 2003, p. 700) and may not reflect the red knots' preferential feeding in microhabitats where eggs are concentrated, such as at horseshoe crab nests (Fraser et al. 2010, p. 99), the wrack line (Karpanty et al. 2011, p. 990; Nordstrom et al. 2006a, p. 438), and shoreline discontinuities (Botton et al. 1994, p. 614).
   Data on the proportion of birds caught at 6.3 oz (180 g) or greater from
   Despite the high uncertainty of the egg density data and a known bias in recorded red knot weights, these metrics do show a significant positive correlation to one another, and we have, therefore, considered this information. Although the birds captured and weighed at the end of May are very likely lighter than the population-wide average departure weight, these birds may represent a useful index of late-departing knots that may be particularly dependent on a superabundance of horseshoe crab eggs (see Asynchronies, below).
Link B, Part 3--Trends in Horseshoe Crab Egg Sufficiency
   Looking at the duration that shorebirds spent in
   By 2002 and 2003, Gillings et al. (2007, p. 513) found that few beaches provided high enough densities of buried eggs (2 to 8 in (5 to 20 cm) deep) for rapid egg consumption (i.e., through vertical redistribution, as discussed above), making birds dependent on a smaller number of sites where conditions were suitable for surface deposition (e.g., from the receding tide). Comparing survey data from 1992 and 2002, usage of
   Newer evidence suggests that the apparent downward trend in egg sufficiency may have stabilized by the mid-2000s. In 2004 and 2005, Karpanty et al. (2011, p. 992) found that eggs became depleted in the wrack line, but also found several other lines of evidence that egg numbers were sufficient for the red knot stopover populations present in those years. This evidence included egg counts over time, bird foraging rates and behaviors, egg exclosure experiments, and lack of competitive exclusion (Karpanty et al. 2011, p. 992).
Link B, Part 4--Trends in Red Knot Weight Gain
   From 1997 to 2002, Baker et al. (2004, p. 878) found that an increasing proportion of red knots, particularly those birds that arrived late in
   Dey et al. (2011a, p. 6) found a significant quadratic (a mathematical relationship between one variable and the square of another variable) relationship between the percent of red knots weighing 6.3 oz (180 g) or more in late May (
   It is noteworthy that the downward trend in the percent of late-May heavy birds appears to have leveled off around 2005 (A. Dey pers. comm.
Horseshoe Crab--Red Knot Weight Gain and Survival/Reproduction (Link C)
   In the causal chain from horseshoe crab harvest to red knot populations, the highest uncertainty is associated with the link between red knot weight gain at the
   More recently, two benchmark studies have attempted to measure the strength of the relationship between departure weight from
   Baker et al. (2004, pp. 878-897) found that average annual survival declined significantly from an average of 85 percent from 1994 to 1998 to 56 percent from 1998 to 2001. Linking weight gain to survival, Baker et al. (2004, p. 878) found that red knots known to survive to a later year, through recaptures or resightings throughout the flyway, were heavier at initial capture than birds never seen again. According to Baker et al. (2004, entire), mean predicted body mass of known survivors was greater than 6.3 oz (180 g) in each year of the study (as cited in McGowan et al. 2011a, p. 14).
   Using data from 1997 to 2008, McGowan et al. (2011a, p. 13) found considerably higher survival rates (around 92 percent) than Baker et al. (2004, entire) had reported. McGowan et al. (2011a, p. 9) did confirm that heavy birds had a higher average survival probability than light birds, but the difference was small (0.918 versus 0.915). Based on the work of Baker et al. (2004), McGowan et al. (2011a, p. 13) had expected a larger difference in survival rates between heavy and light birds.
   However, the average survival rate (1997 to 2008) can mask differences among years. Looking at these temporal differences, the findings of McGowan et al. (2011a, entire) were more consistent with Baker et al. (2004, entire), and McGowan's year-specific survival rate estimates for 1997 to 2002 fell within the ranges presented by Baker et al. (2004). McGowan's lowest survival estimates occurred in 1998, just before the period of sharpest declines in red knot counts (McGowan et al. 2011a, p. 13) (see supplemental document--Rufa Red Knot Ecology and Abundance--tables 2 and 10). Also, the survival of light birds was lower than heavy birds in 6 of the 11 years analyzed. For example, the 1998 to 1999 survival rate estimate was 0.851 for heavy birds and only 0.832 for light birds (McGowan et al. 2011a, p. 9). Finally, McGowan et al. (2011a, p. 14) noted that the data presented by Baker et al. (2004) show survival rates increased during 2001 and 2002. These points of comparison between the two studies suggest that the years of the Baker et al. (2004, entire) study may have corresponded to the period of sharpest red knot declines that have subsequently begun to stabilize. Stabilization around the mid-2000s is also supported by several other lines of evidence, as discussed under Trends in Red Knot Weight Gain (Link B, Part 4), above. However, McGowan et al. (2011a, p. 14) suggested several possible methodological reasons why their results differed from Baker et al. (2004, entire); primarily, that the newer study attempted to account for the known bias toward capturing lighter birds.
   McGowan et al. (2011b, entire) simulated population changes of horseshoe crabs and red knots using reported horseshoe crab harvest from 1998 to 2008 and the red knot survival and mass relationships reported by McGowan et al. (2011a). These tests demonstrated that the survival estimates reported by McGowan et al. (2011a) are potentially consistent with a projected median red knot population decline of over 40 percent (McGowan et al. 2011a, p. 13), over the same period in which declining counts were recorded in both
   A line of corroborating evidence comes from the demonstration of similar linkages in other Calidris canutus subspecies. For example, Morrison (2006, pp. 613-614) and Morrison et al. (2007, p. 479) linked survival rates to the departure condition of spring migrants in C.c. islandica.
   In addition to survival, breeding success was suggested by Baker et al. (2004, pp. 875, 879) as being linked to food availability in
   Although Baker et al. (2004, p. 879) postulated that the observed decrease in second-year birds was linked to food availability in
Horseshoe Crab--Adaptive Resource Management
   In 2012, the ASMFC adopted the ARM for the management of the horseshoe crab population in the
   As long as the ARM is in place and functioning as intended, ongoing horseshoe crab harvests should not be a threat to the red knot. However, the harvest regulations recommended by the ARM require data from two annual, baywide monitoring programs--the trawl survey conducted by the
   In addition, some uncertainty exists regarding how to define the
Food Availability--Summary
   Reduced food availability at the
   The causal role of reduced
Factor E--Asynchronies During the Annual Cycle
   For shorebirds, the timing of arrivals and departures from wintering, stopover, and breeding areas must be precise because prey abundance at staging areas is cyclical, and there is only a narrow window in the arctic summer for courtship and reproduction (Botton et al. in Shuster et al. 2003, p. 6). Because the arctic breeding season is short, northbound birds must reach the nesting grounds as soon as the snow has melted. Early arrival and rapid nesting increases reproductive success. However, a countervailing time constraint is that the seasonal supply of food resources along the migration pathways prevents shorebirds from moving within flight distance of the breeding grounds until late spring (Myers et al. 1987, pp. 21-22). The timing of southbound migration is also constrained, because the abundance of quality prey at stopover sites gradually decreases as the fall season progresses (van Gils et al. 2005b, pp. 126-127; Myers et al. 1987, pp. 21-22). Migration timing is also influenced by the enormous energy required for birds to complete the long-distance flights between wintering and breeding grounds. Northbound shorebirds migrate in a sequence of long-distance flights alternating with periods of intensive feeding to restore energy reserves. Most of the energy stores are depleted during the next flight; thus, a bird's ability to accumulate a small additional energetic reserve may be crucial if its migration gets delayed by poor weather or if feeding conditions are poor upon arrival at the next destination (Myers et al. 1987, pp. 21-22).
   Particularly for species like the red knot that show fidelity to sites with ephemeral food and habitat resources used to fuel long-distance migration, migrating animals may incur fitness consequences if their migration timing and the availability of resources do not coincide (i.e., are asynchronous or "mismatched"). The joint dynamics of resource availability and migration timing may play a key role in influencing annual shorebird survival and reproduction. The mismatch hypothesis is of increasing relevance because of the potential asynchronies created by changes in phenology (periodic life-cycle events) related to global climate change (McGowan et al. 2011a, p. 2; Smith et al. 2011a, p. 575; Meltofte et al. 2007, p. 36).
   Shorebird migration depends primarily on celestial cues (e.g., day length) and is, therefore, less influenced by environmental variation (e.g., water or air temperatures) than are the life cycles of many of their prey species (McGowan et al. 2011a, p. 16); thus, shorebirds are vulnerable to worsening asynchronies due to climate change. Studying captive Calidris canutus canutus held under a constant temperature and light regime for 20 months, Cadee et al. (1996, p. 82) found evidence for endogenous (caused by factors inside the animal) circannual (approximately annual) rhythms of flight feather molt, body mass, and plumage molt. Studying C.c. canutus and C.c. islandica, Jenni-Eiermann et al. (2002, p. 331) and Landys et al. (2004, p. 665) found evidence that thyroid and corticosterone hormones play a role in regulating the annual cycles of physical changes.
   We have no evidence concerning the exact nature of the external timers that synchronize these endogenous rhythms to the outside world (Cadee et al. 1996, p. 82). Photoperiod is known to be a powerful timer for many species' circannual rhythms, and a role for day length as a timer is consistent with observations that captive C.c. canutus exposed to day length variation in outdoor aviaries retained pronounced annual cycles in molt and body mass; however, these experiments do not exclude a role for additional timers besides photoperiod. The complex nature of the annual changes in photoperiod experienced by trans-equatorial migrants is not fully understood; this is especially true for such birds like C. canutus where some populations winter in the southern hemisphere while other populations winter in the northern hemisphere (Cadee et al. 1996, p. 82). While uncertainty exists about the extent to which the timing of the red knot's annual cycle is controlled by endogenous and celestial factors (as opposed to environmental factors); based on the experiments with captive C.c. canutus, it is reasonable to conclude that these factors will constrain the knot's ability to adapt to the shifting temporal and geographic patterns of favorable food and weather conditions that are expected to occur with global climate change.
   Looking at data from Northern Europe from 1923 to 2008 for 43 taxonomically diverse birds (including shorebirds but not Calidris canutus), Petersen et al. (2012, p. 65) found that short-distance migrants arrived an average of 0.38 days earlier per year, while the spring arrival of long-distance migrants had advanced an average of 0.17 days per year. Pooling both groups, spring arrival had shifted an average of 3 weeks earlier over the 80-year study period. Changes in environmental conditions (e.g., temperature, precipitation) during winter and spring explained much of the change in phenology. These findings suggest that short-distance migrants may respond more strongly to climate change than long-distance migrants, such as the red knot, which might adapt more slowly resulting in less time for breeding and potentially mis-timed breeding in this group. These results also suggest that differential adaptation capacities between short- and long-distance migrants could alter the interspecific competition pressures faced by various species (Petersen et al. (2012, p. 70) caused by the formation of new and novel assemblages of bird species that did not previously occur together in space and time.
   The successful annual migration and breeding of red knots is highly dependent on the timing of departures and arrivals to coincide with favorable food and weather conditions. The frequency and severity of asynchronies is likely to increase with climate change. In addition, stochastic encounters with unfavorable conditions are more likely to result in population-level effects for red knots now than when population sizes were larger, as reduced numbers may have reduced the resiliency of this subspecies to rebound from impacts.
Asynchronies--
   Because shorebird staging times are shortest and fueling rates are highest at the last stopover site before birds head to the arctic breeding grounds, there appears to be little "slack" time at late stages in the migration (Gonzalez et al. 2006, p. 115; Piersma et al. 2005, p. 270) (i.e., birds need to arrive and depart within a narrow time window and need to attain rapid weight gain during that window). For a large majority of red knots, the final stopover before the Arctic is in
Delaware Bay--Late Arrivals
   Baker et al. (2004, p. 878) found that the late arrival of red knots in
   Research has shown that late-arriving birds have the ability to make up lost time by gaining weight at a higher rate than usual, provided they have sufficient food resources (Niles et al. 2008, p. 2; Atkinson et al. 2007, pp. 885, 889; Robinson et al. 2003, pp. 12-13). However, late-arriving birds failed to do so in years (e.g., 2003, 2005) when horseshoe crab egg availability was low (Niles et al. 2008, p. 2; Atkinson et al. 2007, p. 885). Looking at data from 1998 to 2002, Atkinson et al. (2003b, p. 16) found that intra-season rates of weight gain had not changed significantly. Using an early model linking red knot weight gain and subsequent survival, these authors concluded that arriving late was actually a more significant factor than food availability in the declining percentage of red knots reaching target weights by the end of May (Atkinson et al. 2003b, p. 16). In a later modeling effort, Atkinson et al. (2007, p. 892) confirmed that fueling (temporal patterns and rates of weight gain) proceeded as normal from 1997 to 1999, from 2001 to 2002, and in 2004, but fueling was below normal in 2000, 2003, and 2005 due to poor foraging and weather conditions. The results of Atkinson et al. (2007, p. 892) suggest that the reduced survival rates calculated by Baker et al. (2004, entire) from 1998 to 2002 were more likely the result of late arrivals than food availability, since fueling was normal in all but one of those years.
   The effects of weather on the red knot's migratory schedule were documented in 1999, when a La Nina event (an occasional abnormal cooling of tropical waters in the eastern Pacific from unknown causes) occurred and the red knots migrating to
Delaware Bay--Timing of Horseshoe Crab Spawning
   Even those red knots arriving early or on time in
Horseshoe Crab Spawn--Storms and Weather
   Normal variation in weather is a natural occurrence and is not considered a population-level threat to the red knot. However, adverse weather events in
   
   High wave conditions curtail horseshoe crab spawning (Nordstrom et al. 2006a, p. 439). Smith et al. (2011a, pp. 575, 581) found that onshore winds that generate waves can delay spawning and create an asynchrony for migrating red knots. High levels of food abundance can offset some small mismatches in migration timing. Thus, increasing abundance of horseshoe crab eggs throughout the stopover period could act as a hedge against temporal mismatches between the horseshoe crab and shorebird migrations, at least in the near term. Also, select beaches with high spawning activity and capacity to retain eggs in surface sediments during episodes of high onshore winds could provide a reserve of horseshoe crab eggs during the shorebird stopover period, even in years when winds cause asynchrony between species migrations (Smith et al. 2011a, pp. 575, 581). Therefore, a superabundance of horseshoe crab eggs and sufficient high-quality foraging habitats can serve to partially offset asynchronies between the red knot stopover and the peak of horseshoe crab spawning.
   Future frequency or intensity of storms in
Horseshoe Crab Spawn--Water Temperatures
   More certainty is associated with a correlation between the timing of horseshoe crab spawning and ocean water temperatures, based on a study by Smith and Michels (2006, pp. 487-488). Although horseshoe crabs spawn from late spring into early summer, migratory shorebirds use
   Climate change does not necessarily mean a linear increase in temperatures and an amelioration of winters in the mid-Atlantic region. As the climate changes, we could see both extremes of weather from year to year, with some years being warmer and others being colder. The colder years could cause horseshoe crab spawning to be delayed past the shorebird stopover period (Kalasz 2008, p. 41). In addition, impacts to red knots from increasingly extreme precipitation events (see supplemental document--Climate Change Background) are not known, but may include temporary water temperature changes that could affect the timing of horseshoe crab spawning activity.
   Conversely, average air and water temperatures are expected to continue rising. In the Northeast, annual average air temperature has increased by 2 [degrees] F (1.1 [degrees] C) since 1970, with winter temperatures rising twice as much (USGCRP 2009, p. 107). Over the next several decades, temperatures in the Northeast are projected to rise an additional 2.5 to 4 [degrees] F (1.4 to 2.2 [degrees] C) in winter and 1.5 to 3.5 [degrees] F (0.8 to 1.9 [degrees] C) in summer (USGCRP 2009, p. 107). Coastal waters are "very likely" to continue to warm by as much 4 to 8 [degrees] F (2.2 to 4.4 [degrees] C) in this century, both in summer and winter (USGCRP 2009, p. 151). Spring migrating red knots could benefit if warming ocean temperatures result in fewer years of delayed horseshoe crab spawning. However, earlier spawning could exacerbate the problems faced by late-arriving knots that already struggle to gain sufficient weight. Under extreme warming, the timing of peak spawning could theoretically even shift earlier than the peak red knot stopover season. Using the findings of Smith et al. (2010b, entire), spawning could shift nearly 9 to 18 days earlier with water temperature increases of 4 to 8 [degrees] F (2.2 to 4.4 [degrees] C).
Asynchronies--Other Spring Stopover Areas
   Outside of
   Based on observations from 1998 to 2003, Gonzalez et al. (2006, p. 109) found that an early March departure date of red knots from San Antonio Oeste, Argentina, generally corresponded to an early arrival date in
   At Fracasso Beach on Peninsula Valdes, Argentina, Hernandez (2009, p. 208) found a significant correlation during March and April between the presence of shorebirds and the biomass of the clam Darina solenoids, suggesting that the occurrence of shorebirds at this site must depend largely on the available food supply. Analysis of weekly counts at Fracasso Beach during March and April from 1994 to 2005 showed some trends in the phenology of the migration of red knots. Generally, from 1994 to 1999, red knots occurred during both March and April, but in 2000 practically none arrived in March. Moreover, in 2004 and 2005, the first red knots were not recorded until May. Hernandez (2009, p. 208) concluded that this delayed stopover at Peninsula Valdes was reflected in similar changes at other sites along the West Atlantic Flyway (e.g., San Antonio Oeste,
   After 2000, increasing proportions of birds arrived late and with low weights at stopover sites in South and North America, suggesting that red knots face additional problems somewhere en route. Indeed, observations from a key Tierra del Fuego wintering area (Rio Grande) in 1995, 2000, and 2008 indicated that wintering conditions at this site had deteriorated, as energy intake rates dropped sharply due to smaller prey sizes and human disturbance (Escudero et al. 2012, p. 362). Escudero et al. (2012, p. 362) suggested declining foraging conditions at Rio Grande might offer at least a partial explanation for red knots after 2000 arriving late, and with low weights at stopover sites in South and North America.
   We have no information to explain why the spring migration of some red knots wintering in Argentina and Chile apparently shifted later in the mid-2000s, exacerbating the population effects from reduced horseshoe crab egg supplies in
   However, red knots may show at least some adaptive capacity in their migration strategies. For example, from 2000 to 2003, a study of a Tierra del Fuego wintering area (Rio Grande) and the first major South American stopover site (San Antonio Oeste) found that red knots took a direct northward flight between the two areas in 2000 and 2001. However, in 2002, birds stopped to feed in intermediate wetlands, leaving Rio Grande earlier but arriving later in San Antonio Oeste. In 2003, both early and late patterns were observed. Red knots arriving early at San Antonio Oeste also arrived significantly earlier in
Asynchronies--Fall Migration
   Preliminary results of efforts to track red knot migration routes using geolocators found that two of three birds likely detoured from normal migration paths to avoid adverse weather during the fall migration (Niles et al. 2010a, p. 129). These birds travelled an extra 640 to 870 mi (1,030 to 1,400 km) to avoid storms. The extra flying represents substantial additional energy expenditure, which on some occasions may lead to mortality (Niles et al. 2010a, p. 129). The timing of fall migration coincides with hurricane season. As discussed in the supplemental document "Climate Change Background," increasing hurricane intensity is ongoing and expected to continue. Hurricane frequency is not expected to increase globally in the future, but may have increased in the North Atlantic over recent decades. However, predictions about changing storm patterns are associated with "low" to "medium" confidence levels (IPCC 2012, p. 13). Therefore, we are uncertain how or to what extent red knots will be affected by changing storm patterns during fall migration.
   Red knots may also face asynchronies with the periods of peak prey abundance in fall, similar to those discussed above for the spring migration. Studying Calidris canutus islandica in the
Asynchronies--Breeding Grounds
   As explained previously, the northbound red knot migration is time-constricted. Birds must arrive on arctic breeding grounds at the right time and with sufficient remaining energy and nutrient stores. In fitness terms, everything else in the annual cycle may be subservient to arrival timing. Knots need to reach the Arctic just as snow is melting, lay their eggs, and hatch them in time for the insect emergence (Piersma et al. 2005, p. 270; Clark in Farrell and Martin 1997, p. 23). Insects are the primary food source for red knot chicks, and for adults during the breeding season. Modeling results from the ARM suggest that indices of arctic conditions are predictors of the annual survival probability of adult red knots, and have stronger effects on survival than departure weights from
   Adverse weather in the Arctic can cause years with little to no productivity for shorebird species. Conditions for breeding are highly variable among sites and regions. The factors most affected by annual variation in weather include whether to breed upon arrival on the breeding grounds, the timing of egg-laying, and the chick growth period (Meltofte et al. 2007, p. 7). In much of the Arctic, initiation dates of clutches (the group of eggs laid by one female) are highly correlated with snowmelt dates. In regions and years where extensive snowmelt occurs before or soon after shorebird arrival, the decision to breed and clutch initiation dates both appear to be a function of food availability for females. Once incubation is initiated, adult shorebirds appear fairly resilient to variations in temperature, with nest abandonment generally limited to cases of severe weather when new snow covers the ground. Feeding conditions for chicks are highly influenced by weather, affecting juvenile production (Meltofte et al. 2007, p. 7). For a number of shorebird species, productivity has been correlated with climate variables known to affect nesting (in June) or brood-rearing (in July) success in a positive (temperature) or negative (snow depth, wind, precipitation) manner (Meltofte et al. 2007, p. 25).
   Anticipated climate changes are expected to be particularly pronounced in the Arctic, and extensive and dramatic changes in snow and weather regimes are predicted for most tundra areas (Meltofte et al. 2007, p. 11) where red knots breed. (See Factor A--Breeding
Breeding Grounds--Insect Prey
   Schekkerman et al. (2003, p. 340) found that growth rates of Calidris canutus chicks were strongly correlated with weather-induced and seasonal variation in the availability of invertebrate prey within arctic nesting habitats, underscoring the importance of timing of reproduction so that chicks can make full use of the summer peak in insect abundance. During studies of C. canutus islandica at a nesting area in eastern Canada, both adults and juveniles were found to put on large amounts of fat prior to migration, suggesting that they make a long-haul flight out of the Arctic to the first fall stopover site. The period of peak arthropod availability is not only during the peak chick rearing season, but also when many adult shorebirds (principally females that have abandoned broods to the care of the male) are actively accumulating fat and other body stores before departure from the Arctic (Meltofte et al. 2007, p. 24).
   Tulp and Schekkerman (2008, p. 48) developed models of the relationship between weather and arthropod (i.e., insect) abundance based on 4 recent years, then used the models to project insect abundance backwards in time ("hindcast") based on weather records over a 30-year period. The hindcasted dates of peak arthropod abundance advanced during the study period, occurring 7 days earlier in 2003 than in 1973. The timing of the period during which shorebirds have a reasonable probability of finding enough food to grow has also changed, with the highest probabilities now occurring at earlier dates than in the past. At the same time, the overall length of the period with probabilities of finding enough food has remained unchanged (e.g., same number of days of availability, only sooner). The result is an advancement of the optimal breeding date for breeding birds. To take advantage of the new optimal breeding time, arctic shorebirds must advance the start of breeding, and this change could affect the entire migration schedule (Tulp and Schekkerman 2008, p. 48). If such a change is beyond the adaptive capacity of red knots, this species will likely face increasing asynchronies with its insect prey during the breeding season, thereby affecting reproductive output. The potential uncoupling of phenology of food resources and breeding events is a major concern for the red knot (COSEWIC 2007, p. 40).
   Even when insect abundance is high, energy budgets of breeding red knots may be tight due to high energy expenditure levels. During the incubation phase in the High Arctic, tundra-breeding shorebirds appear to incur among the highest daily energy expenditure levels of any time of the year (Piersma et al. 2003b, p. 356). The rates of energy expenditure measured in this region are among the highest reported in the literature, reaching inferred ceilings of sustainable energy turnover rates (Piersma et al. 2003b, p. 356). If decreased prey abundance requires birds to spend more time foraging, adverse effects to the energy budget would be further exacerbated, possibly impacting survival rates because red knots foraging away from the nest on open tundra expend almost twice as much energy as during nest incubation (Piersma et al. 2003b, p. 356).
   Although not yet documented for red knots, the links between temperature, prey, and reproductive success have been established in other northern-nesting shorebirds. In one sub-Arctic-breeding shorebird species, Pearce-Higgens et al. (2010, p. 12) linked population changes to previous August temperatures through the effect of temperature on the abundance of the species' insect prey. Predictions of annual productivity, based on temperature-mediated reductions in prey abundance, closely match observed bird population trends, and forecasted warming indicates significant likelihood of northward range contraction (e.g., local extinction) (Pearce-Higgens et al. 2010, p. 12).
   The best available scientific data indicate that red knots will likely be negatively affected by increased asynchronies between the breeding season and the window of optimal insect abundance. However, we are uncertain how or to what extent red knots may be able to adapt their annual cycle, geographic range, or breeding strategy to cope with these predicted ecosystem changes in the Arctic.
Breeding Grounds--Snowmelt
   Field studies from several breeding sites have shown the sensitivity of red knots to the date of snow melt. At 4 sites in the eastern Canadian Arctic, Smith et al. (2010a, p. 292) monitored the arrival of 12 species (including red knot) and found 821 nests over 11 years. Weather was highly variable over the course of the study, and the date of 50 percent snow cover varied by up to 3 weeks among years. In contrast, timing of bird arrival varied by 1 week or less at the sites and was not well predicted by local conditions such as temperature, wind, or snow melt. Timing of breeding was related to the date of 50 percent snow melt, with later snow melt resulting in delayed breeding (Smith et al. 2010a, p. 292). These findings suggest that the suite of cues that control the timing of shorebird arrival in the Arctic are not equipped to adjust for annual weather variations that take place on the breeding grounds.
   In 1999, Morrison et al. (2005, p. 455) found that post-arrival body masses of Calidris canutus islandica at a breeding site on
   Trends toward earlier snowmelt dates have been documented in North America in recent years (IPCC 2007b, p. 891). Earlier snowmelts in the Arctic from 2020 to 2080 are "very likely" (ACIA 2005, p. 470). As years of late snowmelt have typically had an adverse effect on shorebird breeding, reduced frequency of late-melt years may have a short-term benefit to red knots. Warming trends may benefit arctic shorebirds in the short term by increasing both survival and productivity (Meltofte et al. 2007, p. 7). However, it is unknown how red knots would be affected if snowmelts become substantially earlier than the start of the breeding season (see Ims and Fuglei 2005 for consideration of the complex ways tundra ecosystems may respond to climate change).
Breeding Grounds--Snow Depth
   Modeling for the ARM suggested that higher snow depth in the breeding grounds on
Asynchronies--Summary
   The red knot's life history strategy makes this species inherently vulnerable to mismatches in timing between its annual cycle and those periods of optimal food and weather conditions upon which it depends. For unknown reasons, more red knots arrived late in
   Superimposed on this existing threat of late arrivals in
   The red knot's adaptive capacity to deal with numerous changes in the timing of resource availability across its geographic range is largely unknown. A few examples suggest some flexibility in migration strategies. However, available information suggests that the timing of the red knot's annual cycle is controlled at least partly by celestial and endogenous cues, while the reproductive seasons of prey species, including horseshoe crabs and mollusks, are largely driven by environmental cues such as water temperature. These differences between the timing cues of red knots and their prey suggest limitations on the adaptive capacity of red knots to deal with numerous changes in the timing of resource availability across their geographic range.
   Based on the combination of documented past impacts and a spectrum of ongoing and emerging threats, we conclude that asynchronies (mismatches between the timing of the red knot's annual cycles and the periods of favorable food and weather upon which it depends) are likely to cause deleterious subspecies-level effects.
Factor E--Human Disturbance
   In some wintering and stopover areas, red knots and recreational users (e.g., pedestrians, ORVs, dog walkers, boaters) are concentrated on the same beaches (Niles et al. 2008, pp. 105-107; Tarr 2008, p. 134). Recreational activities affect red knots both directly and indirectly. These activities can cause habitat damage (Schlacher and Thompson 2008, p. 234; Anders and Leatherman 1987, p. 183), cause shorebirds to abandon otherwise preferred habitats, negatively affect the birds' energy balances, and reduce the amount of available prey (see Reduced Food Availability, above). Effects to red knots from vehicle and pedestrian disturbance can also occur during construction of shoreline stabilization projects including beach nourishment. Red knots can also be disturbed by motorized and nonmotorized boats, fishing, kite surfing, aircraft, and research activities (K. Kalasz pers. comm.
Disturbance--Timing and Extent
   Although the timing, frequency, and duration of human and dog presence throughout the red knot's U.S. range are not fully known, periods of recreational use tend to coincide with the knot's spring and fall migration periods (WHSRN 2012; Maddock et al. 2009, entire; Mizrahi 2002, p. 2; Johnson and Baldassarre 1988, p. 220; Burger 1986, p. 124). Burger (1986, p. 128) found that red knots and other shorebirds at two sites in New Jersey reacted more strongly to disturbance (i.e., flew away from the beach where they were foraging or roosting) during peak migration periods (May and August) than in other months.
   Human disturbance within otherwise suitable red knot migration and winter foraging or roosting areas was reported by biologists as negatively affecting red knots in Massachusetts, Virginia, North Carolina, South Carolina, Georgia, and Florida (USFWS 2011b, p. 29). Some disturbance issues also remain in New Jersey (both
   In many areas, migration and wintering habitat for the piping plover overlaps considerably with red knot habitats. Because the two species use similar habitats in the Southeast, and both are documented to be affected by disturbance, we can infer the extent of potential human disturbance to red knots from piping plover data in this region. Based on a preliminary review of disturbance in piping plover wintering habitats from North Carolina to Texas, pedestrians and dogs are widespread on beaches in this region (USFWS 2009, p. 46). LeDee et al. (2010, pp. 343-344) surveyed land managers of designated wintering piping plover critical habitat sites across seven southern States and documented the extent of beach access and recreation. All but 4 of the 43 reporting sites owned or managed by Federal, State, and local governmental agencies or by nongovernmental organizations allowed public beach access year-round (88 percent of the sites). At the sites allowing public access, 62 percent of site managers reported more than 10,000 visitors from September to March, and 31 percent reported more than 100,000 visitors in this period. However, more than 80 percent of the sites allowing public access did not allow vehicles on the beach, and half did not allow dogs during the winter season (as cited in USFWS 2012a, p. 35).
   Disturbance of red knots has also been reported from Canada. In the Province of Quebec, specifically on the Magdalen Islands, feeding and resting red knots are frequently disturbed by human activities such as clam harvesting and farming, kite surfing, and seal rookery observation (USFWS 2011b, p. 29). With the increasing popularity of ecotourism, more visitors from around the world come to the shores of the Bay of Fundy in Canada, but existing infrastructure is insufficient to minimize disturbance to roosting shorebirds during high-tide periods. In addition, access to the shoreline is increasing due to ORV use (WHSRN 2012).
   Areas of South America also have documented red knot disturbance. In Tierra del Fuego, wintering red knots are often disturbed around Rio Grande City, Argentina, by ORVs, motorcycles, walkers, runners, fishermen, and dogs (Niles et al. 2008, p. 107; COSEWIC 2007, p. 36). The City of Rio Grande has recently grown extensively towards the sea and river margins. Escudero et al. (2012, p. 358) reported that pedestrians, ORVs, and unleashed dogs on the gravel beach during high tide caused red knots to fly from one spot to another or to move farther away from feeding areas. During outgoing tides, as prime intertidal foraging habitats became exposed, red knots were disturbed and were flushed continuously by walkers, ORVs, and dogs (Escudero et al. 2012, p. 358).
   In Patagonian Argentina, disturbance of migrating red knots has been reported from shorebird reserve areas at Rio Gallegos, Peninsula Valdes, Bahia San Antonio (San Antonio Oeste), and Bahia Samborombon (WHSRN 2012; Niles et al. 2008, p. 107). Coastal urban growth at Rio Gallegos has increased disturbances to shorebirds, especially during high tide when they gather in a limited number of spots very close to shore. Dogs and people frequently interrupt the birds' resting and feeding activities. Various recreational activities, including boating, sport fishing, hiking, and dog walking, take place at urban sites near the coast and on the periphery of the city. These seasonal activities are concentrated in the austral spring and summer (WHSRN 2012), when red knots are present.
   Both shorebirds and people are attracted to the pristine beaches in Bahia San Antonio, Argentina. For example, Las Grutas Beach draws 300,000 tourists every summer, a number that has increased 20 percent per year over the past decade, and the timing of which corresponds with the red knot's wintering use. New access points, buildings, and tourist amusement facilities are being constructed along the beach. Lack of planning for this rapid expansion has resulted in uncontrolled tourist disturbance of crucial roosting and feeding areas for migratory shorebirds, including red knots (WHSRN 2012).
   Management efforts have begun to mitigate disturbance at some South American sites. Campaigns to build alternative ORV trails away from shorebird areas, and to raise public awareness, have helped reduce disturbance in Tierra del Fuego, Rio Gallegos, and Bahia San Antonio (
Disturbance--Precluded Use of Preferred Habitats
   Where shorebirds are habitually disturbed, they may be pushed out of otherwise preferred roosting and foraging habitats (Colwell et al. 2003, p. 492; Lafferty 2001a, p. 322; Luis et al. 2001, p. 72; Burton et al. 1996, pp. 193, 197-200; Burger et al. 1995, p. 62). Roosting knots are particularly vulnerable to disturbance because birds tend to concentrate in a few small areas during high tides, and availability of suitable roosting habitats is already constrained by predation pressures and energetic costs such as traveling between roosting and foraging areas (L. Niles pers. comm.
   Exclusion of shorebirds from preferred habitats due to disturbance has been noted throughout the red knot's nonbreeding range. For example, Pfister et al. (1992, p. 115) found sharper declines in red knot abundance at a disturbed site in Massachusetts than at comparable but less disturbed areas. On the Atlantic coast of New Jersey, findings by Mizrahi (2002, p. 2) generally suggest a negative relationship between human and shorebird densities; specifically, sites that allowed swimming had the greatest densities of people and the fewest shorebirds. At two sites on the Atlantic coast of New Jersey, Burger and Niles (in press) found that disturbed shorebird flocks often did not return to the same place or even general location along the beach once they were disturbed, with return rates at one site of only eight percent for monospecific red knot flocks. In
   Although not specific to red knot, Forgues (2010, p. ii) found the abundance of shorebirds declined with increased ORV frequency, as did the number and size of roosts. Study sites with high ORV activity and relatively high invertebrate abundance suggest that shorebirds may be excluded from prime food sources due to disturbance from ORV activity itself (Forgues 2010, p. 7). Tarr (2008, p. 133) found that disturbance from ORVs decreased shorebird abundance and altered shorebird habitat use. In experimental plots, shorebirds decreased their use of the wet sand microhabitat and increased their use of the swash zone in response to vehicle disturbance (Tarr 2008, p. 144).
Disturbance--Effects to Energy Budgets
   Disturbance of shorebirds can cause behavioral changes resulting in less time roosting or foraging, shifts in feeding times, decreased food intake, and more time and energy spent in alert postures or fleeing from disturbances (Defeo et al. 2009, p. 3; Tarr 2008, pp. 12, 134; Burger et al. 2007; p. 1164; Thomas et al. 2003, p. 67; Lafferty 2001a, p. 315; Lafferty 2001b, p. 1949; Elliott and Teas 1996, pp. 6-9; Burger 1994, p. 695; Burger 1991, p. 39; Johnson and Baldassarre 1988, p. 220). By reducing time spent foraging and increasing energy spent fleeing, disturbance may hinder red knots' ability to recuperate from migratory flights, maintain adequate weights, or build fat reserves for the next phase of the annual cycle (Clark in Farrell and Martin 1997, p. 24; Burger et al. 1995, p. 62). In addition, stress such as frequent disturbance can cause red knots to stop molting before the process is complete (Niles 2010b), which could potentially interfere with the birds' completion of the next phase of their annual cycle.
   Although population-level impacts cannot be concluded from species' differing behavioral responses to disturbance (Stillman et al. 2007; p. 73; Gill et al. 2001, p. 265), behavior-based models can be used to relate the number and magnitude of human disturbances to impacts on the fitness of individual birds (Goss-Custard et al. 2006, p. 88; West et al. 2002, p. 319). When the time and energy costs arising from disturbance were included, modeling by West et al. (2002, p. 319) showed that disturbance could be more damaging than permanent habitat loss. Modeling by Goss-Custard et al. (2006, p. 88) was used to establish critical thresholds for the frequency with which shorebirds can be disturbed before they die of starvation. Birds can tolerate more disturbance before their fitness levels are reduced when feeding conditions are favorable (e.g., abundant prey, mild weather) (Niles et al. 2008, p. 105; Goss-Custard et al. 2006, p. 88).
   At one California beach, Lafferty (2001b, p. 1949) found that more than 70 percent of birds flew when disturbed, and species that forage lower on the beach were disproportionally affected by disturbance because contact with people was more frequent. This finding would apply to red knots, as they forage in the intertidal zone. At two Atlantic coast sites in New Jersey, Burger and Niles (in press) found that 70 percent of shorebird flocks with red knots flew when disturbed, whether the flocks were monospecific or contained other species as well. In two New Jersey bays, Burger (1986, p. 125) found that 70 percent of shorebirds, including red knots, flew when disturbed, including 25 (
   In Florida, sanderlings ran or flew to new spots when people moved rapidly toward them, or when large groups moved along the beach no matter how slow the movement. The number of people on the beach contributed significantly to explaining variations in the amount of time sanderlings spent feeding, and active feeding time decreased from 1986 to 1990 (Burger and Gochfeld 1991, p. 263). Along with reduced size of prey items, disturbance was a key factor explaining sharp declines in red knot food intake rates at Rio Grande, Argentina, on Tierra del Fuego (Escudero et al. 2012, p. 362). Comparing conditions in 2008 with earlier studies, total red knot feeding time was 0.5 hour shorter due to continuous disturbance and flushing of the birds by people, dogs, and ORVs during prime feeding time just after high tide (Escudero et al. 2012, pp. 358, 362). Studying another Calidris canutus subspecies in Australia, Rogers et al. (2006b, p. 233) found that energy expenditure over a tidal cycle was sensitive to the amount of disturbance, and a relatively small increase in disturbance can result in a substantial increase in energy expenditure. Shorebirds may be able to compensate for these costs to some extent by extending their food intake, but only to a degree, and such compensation is dependent upon the availability of adequate food resources. The energetic costs of disturbance are greatest for heavy birds, such as just before departure on a migratory flight (Rogers et al. 2006b, p. 233).
   Both modeling (West et al. 2002, p. 319) and empirical studies (Burger 1986, pp. 126-127) suggest that numerous small disturbances are generally more costly than fewer, larger disturbances. Burger et al. (2007, p. 1164) found that repeated disturbances to red knots and other shorebirds may have the effect of increasing interference competition for foraging space by giving a competitive advantage to gull species, which return to foraging more quickly than shorebirds following a response to vehicles, people, or dogs.
   Tarr (2008, p. 133) found that vehicle disturbance decreased the amount of time that sanderlings spent roosting and resting. Forgues 2010 (pp. 39, 55) found that shorebirds spent significantly less time foraging and more time resting at sites with ORVs, and suggested that the increased amount of time spent resting may be a compensation method for energy lost from decreased foraging.
   Shorebirds are more likely to be flushed by dogs than by people (Thomas et al. 2003, p. 67; Lafferty 2001a, p. 318; Lord et al. 2001, p. 233), and birds react to dogs from greater distances than to people (Lafferty 2001a, p. 319; Lafferty 2001b, pp. 1950, 1956). Pedestrians walking with dogs often go through flocks of foraging and roosting shorebirds, and unleashed dogs often chase the birds and can kill them (Lafferty 2001b, p. 1955; Burger 1986, p. 128). Burger et al. (2007, p. 1162) found that foraging shorebirds in migratory habitat do not return to the beach following a disturbance by a dog, and Burger et al. 2004 (pp. 286-287) found that disturbance by dogs is increasing in
Disturbance--Summary
   Red knots are exposed to disturbance from recreational and other human activities throughout their nonbreeding range. Excessive disturbance has been shown to preclude shorebird use of otherwise preferred habitats and can impact energy budgets. Both of these effects are likely to exacerbate other threats to the red knot, such as habitat loss, reduced food availability, asynchronies in the annual cycle, and competition with gulls (see Cumulative Effects below).
Factor E--Competition With Gulls
   Gulls foraging on the beaches of
   Aerial surveys of breeding gull species on the Atlantic coast of New Jersey from 1976 to 2007 show that herring and greater black-backed gull populations were relatively stable. Greater black-backed gulls showed a slight increase in 2001 that had subsided by 2004. Laughing gull populations grew steadily from 1976 (fewer than 20,000 birds) to 1989 (nearly 60,000 birds). Following a dip in 1995, laughing gull numbers spiked in 2001 to nearly 80,000. From 2004 to 2007, laughing gull numbers returned to approximately the same levels that predominated in the 1980s (50,000 to 60,000 birds) (Dey et al. 2011b, p. 24).
   From 1992 to 2002, the number of gulls recorded in single-day counts on
   Burger et al. (1979, p. 462) found that intraspecific (between members of the same species) aggressive interactions of shorebirds were more common than interspecific (between members of different species) interactions. Negative interactions between red knots and laughing gulls that resulted in disruption of knot behavior were no more prevalent than interactions with other shorebird species. However, larger-bodied species (like gulls) tended to successfully defend areas against smaller species. Total aggressive interactions increased as the density of birds increased in favored habitats, which indicated some competition for food resources (Burger et al. 1979, p. 462).
   Sullivan (1986, pp. 376-377) found that aggression in ruddy turnstones increased as experimentally manipulated food resources (horseshoe crab eggs) changed from an even distribution to a more patchy distribution. Horseshoe crab eggs are typically patchy on
   Following up on earlier studies, Burger (undated, p. 9) studied foraging behavior in shorebirds and gulls on the New Jersey side of
   Despite the observed competitive behaviors between gulls and red knots, Karpanty et al. (2011, p. 992) did not observe red knots to be excluded from foraging by aggressive interactions with other red knots, other shorebirds, or gull species in experimental sections of beach in 2004 and 2005. These authors did observe knots foraging in plots with high egg densities and knots foraging throughout the tidal cycle in all microhabitats. Thus, red knots did not appear to be substantially affected by interspecific or intraspecific interference competition during this study.
   Burger et al. (2007, p. 1162) found that gulls are more tolerant of human disturbance than shorebirds are. When disturbed by humans, gull numbers returned to pre-disturbance levels within 5 minutes. Even after 10 minutes, shorebird numbers failed to reach predisturbance levels. Repeated disturbances to red knots and other shorebirds may have the effect of increasing interference competition for foraging space by giving a competitive advantage to gull species, which return to foraging more quickly than shorebirds following a flight response to vehicles, people, or dogs (Burger et al. 2007, p. 1164). The size and aggression of gulls, coupled with their greater tolerance of human disturbance, give gulls a competitive advantage over shorebirds in prime feeding areas (Niles et al. 2008, p. 107).
   Reduction of available horseshoe crab eggs or consolidation of spawning horseshoe crabs onto fewer beaches can increase interference competition among egg foragers. Karpanty et al. (2006, p. 1707) found a positive relationship between laughing gull numbers and red knot presence (i.e., more laughing gulls were present when red knots were also present), concluding that this correlation was likely due to the use by both bird species of the sandy beach areas with the highest densities of horseshoe crab eggs for foraging. Competition for horseshoe crab eggs increases with reduced egg availability, and the ability of shorebirds to compete with gulls for food decreases as shorebird flock size decreases (Breese 2010, p. 3; Niles et al. 2005, p. 4).
   Competition between shorebirds and laughing gulls for horseshoe crab eggs increased in the 2000s as the decline in the horseshoe crab population concentrated spawning in a few favored areas (e.g.,
   In summary, competition with gulls can exacerbate food shortages in
   Gull competition has not been reported as a threat to red knots outside of
Factor E--Harmful Algal Blooms (HABs)
   A harmful algal bloom (HAB) is the proliferation of a toxic or nuisance algal species (which can be microscopic or macroscopic, such as seaweed) that negatively affects natural resources or humans (
HABs--Impacts to Shorebirds
   Large die-offs of fish, mammals, and birds can be caused by HABs. Wildlife mortality associated with HABs can be caused by direct exposure to toxins, indirect exposure to toxins (i.e., as the toxins accumulate in the food web), or through ecosystem impacts (e.g., reductions in light penetration or oxygen levels in the water, alteration of food webs due to fish kills or other mass mortalities) (Woods Hole 2012; Anderson 2007, p. 5; FAO 2004, p. 1). Wildlife can be exposed to algal toxins through aerosol (airborne) transport or via consumption of toxic prey (FFWCC 2011; Steidinger et al. 1999, p. 6). Exposure of wildlife to algal toxins may continue for weeks after an HAB subsides, as toxins move through the food web (Abbott et al. 2009, p. 4).
   Animals exposed to algal toxins through their diets may die or display impaired feeding and immune function, avoidance behavior, physiological dysfunction, reduced growth and reproduction, or pathological effects (Woods Hole 2012). A poorly defined but potentially significant concern relates to sublethal, chronic impacts from toxic HABs that can affect the structure and function of ecosystems (Anderson 2007, p. 4). Chronic toxin exposure may have long-term consequences affecting the sustainability or recovery of natural populations at higher trophic levels (e.g., species that feed higher in the food web). Ecosystem-level effects from toxic algae may be more pervasive than yet documented by science, affecting multiple trophic levels, depending on the ecosystem and the toxin involved (Anderson 2007, pp. 4-5).
   For both humans and shorebirds, shellfish are a key route of exposure to algal toxins. When toxic algae are filtered from the water as food by shellfish, their toxins accumulate in those shellfish to levels that can be lethal to humans or other animals that eat the shellfish (Anderson 2007, p. 4). Several shellfish poisoning syndromes have been identified according to their symptoms. Those shellfish poisoning syndromes that occur prominently within the range of the red knot include Amnesic Shellfish Poisoning (ASP) (occurring in Atlantic Canada, caused by Pseudo-nitzchia spp.); Neurotoxic Shellfish Poisoning (NSP, also called "red tide") (occurring on the U.S. coast from Texas to North Carolina, caused by Karenia brevis and other species); and Paralytic Shellfish Poisoning (PSP) (occurring in Atlantic Canada, the U.S. coast in New England, Argentina, and Tierra del Fuego, caused by Alexandrium spp. and others) (Woods Hole 2012; FAO 2004, p. 44). The highest levels of PSP toxins have been recorded in shellfish from Tierra del Fuego (
   Algal toxins may be a direct cause of death in seabirds and shorebirds via an acute or lethal exposure, or birds can be exposed to chronic, sublethal levels of a toxin over the course of an extended bloom. Sub-acute doses may contribute to mortality due to an impaired ability to forage productively, disrupted migration behavior, reduced nesting success, or increased vulnerability to predation, dehydration, disease, or injury (VanDeventer 2007, p. 1). It is commonly believed that the primary risk to shorebirds during an HAB is via contamination of shellfish and other invertebrates that constitute their normal diet. Coquina clams (Donax variabilis) and other items that shorebirds feed upon can accumulate marine toxins during HABs and may pose a risk to foraging shorebirds. In addition to consuming toxins via their normal prey items, shorebirds have been observed consuming dead fish killed by HABs (VanDeventer 2007, p. 11). VanDeventer et al. (2011, p. 31) observed shorebirds, including sanderlings and ruddy turnstones, scavenging fish killed during a 2005 red tide along the central west coast of Florida. Brevetoxins (discussed below) were found both in the dead fish and in the livers of dead shorebirds that were collected from beaches and rehabilitation centers (VanDeventer et al. 2011, p. 31). Although scavenging has not been documented in red knots, clams and other red knot prey species are among the organisms that accumulate algal toxins.
   Sick or dying birds often seek shelter in dense vegetation; thus, those that succumb to HAB exposure are not often observed or documented. Birds that are debilitated or die in exposed areas are subject to predation or may be swept away in tidal areas. When extensive fish kills occur from HABs, the carcasses of smaller birds such as shorebirds may go undetected. Some areas affected by HABs are remote and rarely visited. Thus, mortality of shorebirds associated with HABs is likely underreported.
HABs--Gulf of Mexico
   Algal blooms causing massive fish kills in the Gulf of Mexico have been reported anecdotally since the 1500s, but written records exist only since 1844. The dinoflagellate Karenia brevis has been implicated in producing harmful red tides that occur annually in the Gulf of Mexico. Red tides cause extensive marine animal mortalities and human illness through the production of highly potent neurotoxins known as brevetoxins (FFWCC 2011). Brevetoxins are toxic to fish, marine mammals, birds, and humans, but not to shellfish (FAO 2004, p. 137). Karenia brevis has come to be known as the Florida red tide organism and has also been implicated in HABs in the Carolinas, Alabama, Mississippi, Louisiana, and Texas in the United States, as well as in Mexico (
   A red tide event occurred in
   Another Texas red tide event was documented by shorebird biologists in
   Although no HAB-related red knot mortality has been reported from Florida, HABs have become a common feature of Florida's coastal environment and are associated with fish, invertebrate, bird, manatee, and other wildlife kills (Abbott et al. 2009, p. 3; Steidinger et al. 1999, pp. v, 3-4). Red tides occur nearly every year along Florida's Gulf coast, and may affect hundreds of square miles (FFWCC 2011). Red tides are most common off the central and southwestern coasts of Florida between Clearwater and
HABs--Uruguay
   In
HABs--Causes and Trends
   During recent decades, the frequency, intensity, geographic distribution, and impacts of HABs have increased, along with the number of toxic compounds found in the marine food chain (Anderson 2007, p. 2; FAO 2004, p. 2). Coastal regions throughout the world are now subject to an unprecedented variety and frequency of HAB events. Many countries are faced with a large array of toxic or harmful species, as well as trends of increasing bloom incidence, larger areas affected, and more marine resources impacted. The causes behind this expansion are debated, with possible explanations ranging from natural mechanisms of species dispersal and enhancement to a host of human-related phenomena including climate change (Anderson 2007, pp. 3, 13; FAO 2004, p. 2). The influence of human activities in coastal waters may allow HABs to extend their ranges and times of residency (Steidinger et al. 1999, p. v).
   Some new bloom events reflect indigenous algal populations discovered because of better detection methods and more observers. Several other "spreading events" are most easily attributed to natural dispersal via currents, rather than human activities (Anderson 2007, p. 11). However, human activities have contributed to the global HAB expansion by transporting toxic species in ship ballast water (Anderson 2007, p. 13). Another factor contributing to the global expansion in HABs is the substantial increase in aquaculture activities in many countries (Anderson 2007, p. 13), and the transfer of shellfish stocks from one area to another (FAO 2004, p. 2). Changed land use patterns, such as deforestation, can also cause shifts in phytoplankton species composition by increasing the concentrations of organic matter in land runoff. Acid precipitation can further increase the mobility of organic matter and trace metals in soils (FAO 2004, p. 1), which contribute to creating environmental conditions suitable for HABs.
   Of the causal factors leading to HABs, excess nutrients often dominate the discussion (Steidinger et al. 1999, p. 2). Coastal waters are receiving large and increasing quantities of industrial, agricultural, and sewage effluents through a variety of pathways. In many urbanized coastal regions, these anthropogenic inputs have altered the size and composition of the nutrient pool which may, in turn, create a more favorable nutrient environment for certain HAB species (Anderson 2007, p. 13). Shallow and restricted coastal waters that are poorly flushed appear to be most susceptible to nutrient-related algal problems. Nutrient enrichment of such systems often leads to excessive production of organic matter (a process known as eutrophication) and increased frequencies and magnitudes of algal blooms (Anderson 2007, p. 14).
   On a global basis, Anderson et al. (2002, p. 704) found strong correlations between total nitrogen input and phytoplankton production in estuarine and marine waters. There are also numerous examples of geographic regions (e.g.,
   Although important, eutrophication is not the only explanation for algal blooms or toxic outbreaks (Anderson et al. 2002, p. 704). The link is clear between nutrients and nontoxic algal blooms, which can cause oxygen depletion in the water, fish kills, and other ecosystem impacts (Woods Hole 2012; Anderson 2007, p. 5; Anderson et al. 2002, p. 704; Steidinger et al. 1999, p. 2). However, the connection with excess nutrients is less clear for algal species that produce toxins, as toxic blooms can begin in open water miles away from shore or the immediate influence of human activities (Steidinger et al. 1999, p. 2). Many of the new or expanded HAB problems have occurred in waters with no influence from pollution or other anthropogenic effects (Anderson 2007, pp. 11, 13).
   The overall effect of nutrient overenrichment on harmful algae is species specific. Nutrient enrichment has been strongly linked to stimulation of some harmful algal species, but for others it has apparently not been a contributing factor (Anderson et al. 2002, p. 704). There is no evidence of a direct link between Florida red tides and nutrient pollution (FFWCC 2011). Elevated nutrients in inshore areas do not start these blooms but, in some instances, can allow a bloom to persist in the nutrient-rich environment for a slightly longer period than normal (Steidinger et al. 1999, p. 2). For those regions and algal species where nutrient enrichment is a causative or contributing factor, increased coastal water temperatures and greater spring runoff associated with global warming may increase the frequency of HABs (USGCRP 2009, pp. 46, 150).
   Coastal managers are working toward mitigation, prevention, and control of HABs. Mitigation efforts are typically focused on protecting human health (Anderson 2007, p. 15), and are thus unlikely to prevent exposure of red knots. Several challenges hinder prevention efforts, including lack of information regarding the factors that cause blooms and limitations on the extent to which those factors can be modified or controlled (Anderson 2007, p. 16). Bloom control is the most challenging and controversial aspect of HAB management. Control refers to actions taken to suppress or destroy HABs, directly intervening in the bloom process. There are five categories or strategies that can be used to combat or suppress an invasive or harmful species, consisting of mechanical, biological, chemical, genetic, and environmental control. Several of these methods have been applied to HAB species (Anderson 2007, p. 18). However, the science behind HAB control is rudimentary and slow moving, and most control methods are currently infeasible, theoretical, or only possible on an experimental scale (Anderson 2007, pp. 18-20). It is likely that HABs will always be present in the coastal environment and, in the next few decades at least, are likely to continue to expand in geographic extent and frequency (Anderson 2007, p. 2).
HABs--Summary
   To date, direct impacts to red knots from HABs have been documented only in Texas, although a large die-off in Uruguay may have also been linked to an HAB. We conclude that some level of undocumented red knot mortality from HABs likely occurs most years, based on probable underreporting of shorebird mortalities from HABs and the direct exposure of red knots to algal toxins (particularly via contaminated prey) throughout the knot's nonbreeding range. We have no documented evidence that HABs were a driving factor in red knot population declines in the 2000s. However, HAB frequency and duration have increased and do not show signs of abating over the next few decades. Combined with other threats, ongoing and possibly increasing mortality from HABs may affect the red knot at the population level.
Factor E--Oil Spills and Leaks
   The red knot has the potential to be exposed to oil spills and leaks throughout its migration and wintering range. Oil, as well as spill response activities, can directly and indirectly affect both the bird and its habitat through several pathways. Red knots can be exposed to petroleum products via spills from shipping vessels, leaks or spills from offshore oil rigs or undersea pipelines, leaks or spills from onshore facilities such as petroleum refineries and petrochemical plants, and beach-stranded barrels and containers that can fall from moving cargo ships or offshore rigs. Several key red knot wintering or stopover areas also contain large-scale petroleum extraction, transportation, or both activities. With regard to potential effects on red knot habitats, the geographic location of a spill, weather conditions (e.g., prevailing winds), and type of oil spilled are as important, if not more so, than the volume of the discharge.
   Petroleum oils are complex and variable mixtures of many chemicals and include crude oils and their distilled products that are transported globally in large quantities. Overwhelming evidence exists that petroleum oils are toxic to birds (Leighton, 1991, p. 43). Acute exposure to oil can result in death from hypothermia (i.e., from loss of the feathers' waterproofing and insulating capabilities), smothering, drowning, dehydration, starvation, or ingestion of toxins during preening (Henkel et al. 2012, p. 680; Peterson et al. 2003, p. 2085). In shorebirds, oil ingestion by foraging in contaminated intertidal habitats and consumption of contaminated prey may also be a major contamination pathway (Henkel et al. 2012, p. 680; Peterson et al. 2003, p. 2083). Mortality from ingested oil is primarily associated with acute toxicity involving the kidney, liver, or gastrointestinal tract (Henkel et al. 2012, p. 680; Leighton 1991, p. 46). In addition to causing acute toxicity, ingested oil can induce a variety of toxicologically significant systemic effects (Leighton 1991, p. 46). Since shorebird migration is energetically and physiologically demanding, the sublethal effects of oil may have severe consequences that lead to population-level effects (Henkel et al. 2012, p. 679). Oil can have long-term effects on populations through compromised health of exposed animals and chronic toxic exposures from foraging on persistently contaminated prey or habitats (Peterson et al. 2003, p. 2085).
   Oiled birds may also experience decreased foraging success due to a decline in prey populations following a spill or due to increased time spent preening to remove oil from their feathers (Henkel et al. 2012, p. 681). Shorebirds oiled during the 1996 T/V Anitra spill in
   Finally, efforts to prevent shoreline oiling and cleanup response activities can disturb shorebirds and their habitats (USFWS 2012a, p. 36; Burger 1997a, p. 293; Philadelphia Area Committee 1998, Annex E). Movement of response personnel on the beach and vessels in the water can flush both healthy and sick birds, causing disruptions in feeding and roosting behaviors (see Human Disturbance, above). In addition to causing disturbance, post-spill beach cleaning activities can impact habitat suitability and prey availability (see Factor A--Beach Cleaning, above). And lastly, dispersants used to break up oil can also have health effects on birds (NRC 2005, pp. 254-257).
Oil Spills--Canada
   The shorebird habitats of the Mingan Islands in the Gulf of St. Lawrence (Province of Quebec) are at risk from oil impacts because of their proximity to ships carrying oil through the archipelago to the Havre-Saint-Pierre harbor (Niles et al. 2008, p. 100). In
Oil Spills--
   
   The farthest upstream areas of
   The narrow channel and frequent occurrence of strong wind and tide conditions increase the risk of oil spills in the
   Although there have been several thousand spills reported in the
Table 10--Oil Spills Greater Than 10,000 Gallons (37,854 Liters) in theDelaware River and Bay Since 1985 [NOAA 2013d] Vessel Date Volume Location Approximate (gallons) river miles from Red Knot habitat M/V Athos 1 11/12/2004 265,000 Paulsboro, NJ 45 T/V Anitra 5/9/1996 42,000 Big Stone 0 Anchorage, DE T/V Presidente 6/24/1989 306,000 Marcus Hook, 40 Rivera NJ T/V Grand 9/28/1985 435,000 Marcus Hook, 40 Eagle NJ T/V Mystra 9/18/1985 10,000 Delaware Bay 0
   Although the Anitra spill occurred in May near red knot habitat, environmental conditions caused the oil to move around the
   Large spills upriver, or moderate spills in the upper bay, have the potential to contact a significant portion of the shorebird concentration areas. Although the migration period when crabs and shorebirds are present is short, even a minor spill (i.e., less than 1,000 gal (3,785 L)) could, depending on the product spilled, affect beach quality for many years. Both New Jersey and Delaware officials work closely with Emergency Response managers and the USCG in planning for such an occurrence (Kalasz 2008, pp. 39-40; Clark in Farrell and Martin 1997, p. 24).
Oil Spills--Gulf of Mexico
   As of 2010, there were 3,409 offshore petroleum production facilities in Federal waters within the Gulf of Mexico Outer Continental Shelf (OCS), down from 4,045 in 2001 (
   The BSEE tracks spill incidents of one barrel or greater in size of petroleum and other toxic substances resulting from Federal OCS oil and gas activities (BSEE 2012). Table 11 shows the number of spills 50 barrels (2,100 gal (7,949 L)) or greater in the Gulf of Mexico since 1996. These figures do not include incidents stemming from substantial extraction operations in State waters. Crude oil production in 2012 was an estimated 4.9 million barrels in Louisiana State waters (
Table 11--Federal Outer Continental Shelf Spill Incidents 50 Barrels (2,100 Gallons (7,949 liters)) or Greater, Resulting From Oil and Gas Activities, 1996 to 2012 [BSEE 2012] Year Number of incidents 2012 8 2011 3 2010 5 2009 11 2008 33 2007 4 2006 14 2005 49 2004 22 2003 12 2002 12 2001 9 2000 7 1999 5 1999 9 1997 3 1996 3
   Nationwide, spill rates (the number of incidents per billion barrels of crude oil handled) in several sectors decreased or remained stable over recent decades. From 1964 to 2010, spill rates declined for OCS pipelines, and spill rates from tankers decreased substantially, probably because single-hulled tankers were largely phased out (see the "International Laws and Regulations" section of the Factor D supplemental document). Looking at the whole period from 1964 to 2010, nationwide spill rates for OCS platforms were unchanged for spills 1,000 barrels or greater, and decreased for spills 10,000 barrels or greater. However, spill rates at OCS platforms increased in the period 1996 to 2010 relative to the period 1985 to 1999, as the later period included several major hurricanes (e.g., Hurricane Katrina and Hurricane Rita) and the Deepwater Horizon spill (Anderson et al. 2012, pp. iii-iv). Generally decreasing spill rates were partially offset by increasing production, as shown in Table 12.
Table 12--Nationwide Outer Continental Shelf Petroleum Production, and Spills 1 Barrel or Greater, 1964 to 2009 * [Anderson et al. 2012, p. 10] Barrels spilled by Number of spills by spill size spill size Year Barrels Billions Total 1 to 1,000 Total 1 to 1,000 spilled of 999 Barrels 999 Barrels per barrels Barrels or barrels or billion produced greater Greater barrels produced 1964-1970 255,280 1.54 394,285 3,499 390,786 33 23 10 1971-1990 16,682 6.79 113,307 21,415 91,892 1,921 1,909 12 1991-2009 6,427 9.2 59,142 28,144 30,998 853 843 10 1964-2009 32,329 17.53 566,734 53,058 513,676 2,807 2,775 32 * Spill data for 1964 to 1970 are for spills of 50 barrels or greater. Barrels of production or spillage may not add due to rounding of decimals not shown. One barrel equals 42 gallons (159 liters).
   In the Gulf of Mexico, threats from oil spills are primarily from the high volume of shipping vessels, from which most documented spills have originated, traveling offshore and within connected bays. In addition to the risk of leaks and spills from offshore oil rigs, pipelines, and petroleum refineries, there is a risk of leaks from oil-filled barrels and containers that routinely wash up on the Texas coast. Federal and State land managers have protective provisions in place to secure and remove the barrels, thus reducing the likelihood of contamination (M. Bimbi pers. comm.
   Chronic spills of oil from rigs and pipelines and natural seeps in the Gulf of Mexico generally involve small quantities of oil. The oil from these smaller leaks and seeps, if they occur far enough from land, tend to wash ashore as tar balls. In cases such as this, the impact is limited to discrete areas of the beach, whereas oil slicks from larger spills coat longer stretches of the shoreline. In late July and early
   On
Oil Spills--South America
South America--Brazil and Patgonia
   Threats to red knot habitat in Maranhao, Brazil include oil pollution as well as habitat loss (see Factor A above) from offshore petroleum exploration on the continental shelf (WHSRN 2012; Niles et al. 2008, p. 97; COSEWIC 2007, p. 37).
   Oil pollution is also a threat at several red knot wintering and stopover habitats along the Patagonian coast of Argentina including Peninsula Valdes and Bahia Bustamante; at the latter site, 15 percent of red knots were polluted with oil during a study in 1979 (Niles et al. 2008, p. 98). Further south in Argentina, at a shorebird reserve and red knot stopover area in Rio Gallegos near Tierra del Fuego, the main threat comes from oil and coal transport activities. Crude oil and coal are loaded onto ships at a hydrocarbon port where the estuary empties into the sea adjacent to the salt marsh zone. This area has a history of oil tankers running aground because of extreme tides, strong winds, tidal currents, and piloting errors. A shipwreck at Rio Gallegos could easily contaminate key areas used by shorebirds, including red knots (WHSRN 2012; Niles et al. 2008, p. 98; Ferrari et al. 2002, p. 39). However, oil pollution has decreased significantly along the Patagonian coast (Niles et al. 2008, p. 98).
South America--Tierra del Fuego
   The risk of an oil spill is a primary threat to the largest red knot wintering areas in both the Chilean and Argentinean portions of Tierra del Fuego (WHSRN 2012; Niles et al. 2008, pp. 98-99; COSEWIC 2007, p. 36) due to the proximity of large-scale oil operations close to key red knot habitats. In recent years, oil operations have been decreasing in Chile around Bahia Lomas, but increasing along the Argentinean coast of Tierra del Fuego (Niles et al. 2008, p. 98; COSEWIC 2007, pp. 36-37).
   The region of Magellan, Chile, has traditionally been an important producer of oil and natural gas since the first oil discovery was made in 1945 within 6.2 mi (10 km) of the bayshore, in Manantiales. Production continues, although local oil activity has diminished over the last 20 years. Oil is extracted by drilling on land and offshore, the latter with no new drillings between 2000 and 2008. The largest single red knot wintering site, Bahia Lomas, has several oil platforms. Most are static, and several were closed around 2007 as the oil resource had been depleted (Niles et al. 2008, p. 98). However, the red knot area at Bahia Lomas remains at risk from a spill or leak from the remaining oil extraction facilities.
   Exposure of red knots to hydrocarbon pollution at Bahia Lomas could also come from shipping accidents, as the site is located at the eastern end of the
   In 10 of the 12 years since 2000 for which survey data are available, Bahia Lomas supported over half of the total Argentina-Chile wintering population of red knots, rising to over 90 percent from 2010 through 2012 (G. Morrison pers. comm.
   On the nearby
   Farther south on Tierra del Fuego, the area near the shorebird reserves at Rio Grande, Argentina, is important for onshore and offshore oil production, which could potentially contribute to oil pollution, especially from oil tankers loading around Rio Grande City. No direct evidence exists of red knots being affected by oil pollution, but it remains a risk (Niles et al. 2008, pp. 98-99).
Oil Spills--Summary
   Red knots are exposed to large-scale petroleum extraction and transportation operations in many key wintering and stopover habitats including Tierra del Fuego, Patagonia, the Gulf of Mexico,
Factor E--Environmental Contaminants
   Environmental contaminants can have profound effects on birds, acting from the molecular through population levels (Rattner and Ackerson 2008, p. 344). Little experimental work has been done on the toxic effects of organochlorines (e.g., polychlorinated biphenyls (PCBs); pesticides such as DDT (dichloro-diphenyl-trichloroethane), dieldrin, and chlordane) or trace elements (e.g., mercury, cadmium, arsenic, selenium) in shorebirds, but adult mortality due to organochlorine poisoning has been recorded (Braune and Noble 2009, pp. 200-201).
Contaminants--Canada
   In 1991 and 1992, Braune and Noble (2009, p. 185) tested 12 shorebird species (not including Calidris canutus) from 4 sites across Canada (including 2 red knot stopover areas) for PCBs, organochlorine pesticides, mercury, selenium, cadmium, and arsenic. Contaminant exposure among species varied with diet, foraging behavior, and migration patterns. Diet composition seemed to provide a better explanation for contaminant exposure than bill length or probing behaviors. Based on the concentrations measured, researchers found no indication that contaminants were adversely affecting the shorebird species sampled in this study (Braune and Noble 2009, p. 201).
   Heavy shipping traffic in the Gulf of St. Lawrence (Province of Quebec) presents a risk of environmental contamination, as well as possible oil spills (which were discussed above). Red knot habitats in the Mingan Islands are particularly at risk because large ships carrying titanium and iron navigate through the archipelago to the Havre-Saint-Pierre harbor throughout the year (COSEWIC 2007, p. 37).
   At another red knot stopover area, the Bay of Fundy, chemicals such as herbicides and pesticides originate from farming activities along tidal rivers and accumulate in intertidal areas. These contaminants build up in the tissues of intertidal invertebrates (e.g., the burrowing amphipod Corophium volutator and the small clam Macoma balthica) that are, in turn, ingested by shorebirds, but with unknown consequences (WHSRN 2012).
Delaware Bay
   
   Burger et al. (1993, p. 189) examined concentrations of lead, cadmium, mercury, selenium, chromium, and manganese in feathers of shorebirds, including red knots migrating north through
   Burger (1997b, p. 279) measured lead, mercury, cadmium, chromium, and manganese concentrations in the eggs of horseshoe crabs from 1993 to 1995, and from leg muscle tissues in 1995, in
   Burger et al. (2002, p. 227) examined the levels of arsenic, cadmium, chromium, lead, manganese, mercury, and selenium in the eggs and tissues of 100 horseshoe crabs collected at 9 sites from Maine to Florida, including
   Revisiting the 1997 study specific to
   Botton et al. (2006, p. 820) found no significant differences in the percentage of horseshoe crab eggs that completed development when cultured using water from
   The USFWS (2007b, p. ii) examined embryonic, larval, and juvenile horseshoe crab responses to a series of exposures (from 0 to 100 ppb) of methoprene, a mosquito larvicide (a pesticide that kills specific insect larvae). The results provided no evidence that a treatment effect occurred, with no obvious acute effects of environmentally relevant concentrations of methoprene on developing horseshoe crab embryos, larvae, or first molt juveniles. The study results suggested that exposure to methoprene may not be a limiting factor to horseshoe crab populations. However, horseshoe crab life stages after the first molt were not tested for methoprene effects, which have been found in other marine arthropod species. Walker et al. (2005, pp. 118, 124) found that methoprene was toxic to lobster (Homarus americanus) stage II larvae at 1 ppb, and that stage IV larvae were more resistant but did exhibit significant increases in molt frequency beginning at exposures of 5 ppb. However, we do not have information on how or to what extent these levels of methoprene may affect horseshoe crab populations or red knots, through their consumption of exposed horseshoe crab eggs.
Contaminants--Florida
   A piping plover was found among dead shorebirds discovered on a sandbar near
Contaminants--South America
   Blanco et al. (2006, p. 59) documented the value of South American rice fields as an alternative feeding habitat for waterbirds. Agrochemicals are used in the management of rice fields. Although shorebirds are not considered harmful to the rice crop, they are exposed to lethal and sublethal doses of toxic products while foraging in these habitats. Rice fields act as important feeding areas for migratory shorebirds but can become toxic traps without adequate management (Blanco et al. 2006, p. 59). In rice field surveys from
   Threats to red knot habitat in Maranhao, Brazil, include iron ore and gold mining, which can cause mercury contamination (WHSRN 2012; Niles et al. 2008, p. 97; COSEWIC 2007, p. 37). The important migration stopover area at San Antonio Oeste, Argentina faces potential pollution from a soda ash factory built in 2005, which could release up to 250,000 tons of calcium chloride per year, affecting intertidal invertebrate food supplies. Garbage and port activities are additional sources of pollution in this region (WHSRN 2012; Niles et al. 2008, p. 98; COSEWIC 2007, p. 37).
   At the southern Argentinean stopover of Rio Gallegos, a trash dump adjoins the feeding and roosting areas used by shorebirds. Garbage is spread quickly by the strong winds characteristic of the region and is deposited over large parts of the estuary shore. This trash diminishes habitat quality, especially when plastics, such as polythene bags, cover foraging or roosting habitats (Niles et al. 2008, p. 98; Ferrari et al. 2002, p. 39). Pollution at Rio Gallegos also stems from untreated sewage, but a project is under way to carry the waste offshore instead of discharging it into the shorebird habitats (WHSRN 2012) (see Factor A--Coastal Development--Other Countries).
   In the past, organic waste from the City of Rio Grande (in Argentinean Tierra del Fuego, population approximately 50,000), including that from a chicken farm, has been released at high tide over the flats where red knots feed (Atkinson et al. 2005, p. 745). We have no direct evidence of red knots having been affected by organic waste, but it remains a potential source of contamination risk (e.g., nutrients, trace metals, pesticides, pathogens, pharmaceuticals, endocrine disruptors) (Fisher et al. 2005, pp. iii, 4, 34) to the knots and their wintering habitat. As at Rio Gallegos, wind-blown trash from a nearby landfill degrades shorebird habitats at one location in Rio Grande, but the City is working to relocate the landfill. In addition, a methanol and urea plant and two seaports are in development (WHSRN 2012), which could also increase pollution.
Contaminants--Summary
   Although red knots are exposed to a variety of contaminants across their nonbreeding range, we have no evidence that such exposure is impacting health, survival, or reproduction at the subspecies level. Exposure risks exist in localized red knot habitats in Canada, but best available data suggest shorebirds in Canada are not impacted by background levels of contamination. Levels of most metals in red knot feathers from the
   Horseshoe crab reproduction does not appear impacted by the mosquito control chemical methoprene (at least through the first juvenile molt) or by ambient water quality in mid-Atlantic estuaries. Shorebirds have been impacted by pesticide exposure, but use of the specific chemical that caused a piping plover death in Florida has subsequently been banned in the United States. Exposure of shorebirds to agricultural pollutants in rice fields may occur regionally in parts of South America, but red knot usage of rice field habitats was low in the several countries surveyed. Finally, localized urban pollution has been shown to impact South American red knot habitats, but we are unaware of any documented health effects or population-level impacts. Thus, we conclude that environmental contaminants are not a threat to the red knot. However, see Cumulative Effects, below, regarding an unlikely but potentially high-impact synergistic effect among avian influenza, environmental contaminants, and climate change in
Factor E--
   Within the red knot's U.S. wintering and migration range, substantial development of offshore wind facilities is planned, and the number of wind turbines installed on land has increased considerably over the past decade. The rate of wind energy development will likely continue to increase into the future as the United States looks to decrease reliance on the traditional sources of energy (e.g., fossil fuels). Wind turbines can have a direct (e.g., collision mortality) and indirect (e.g., migration disruption, displacement from habitat) impact on shorebirds. We have no information on wind energy development trends in other countries, but risks of red knot collisions would likely be similar wherever large numbers of turbines are constructed along migratory pathways, either on land or offshore.
Wind Energy--Offshore
   In 2007, the
   In addition to these Federal efforts, several States are considering installation of offshore wind turbines in their jurisdictional ocean waters (i.e., up to 3 nautical miles (5.6 km) off the Atlantic coast; variable distances in the Gulf of Mexico) (DOE 2013;
   To date, no offshore wind facilities have been installed in the United States. However in 2010, BOEM issued the first lease to build a wind facility in Federal waters, authorizing the
   Analysis by the DOE shows the potential for wind energy, and offshore wind in particular, to reduce greenhouse gas emissions in a rapid and cost-effective manner (DOE and BOEMRE 2011, p. 5). However, large-scale installation of offshore wind turbines represents a potential collision hazard for red knots during their migration (Burger et al. 2012c, p. 370; Burger et al. 2011, p. 348; Watts 2010, p. 1), and offshore wind resources within the U.S. range of the red knot show high potential for wind energy development (DOE and BOEMRE 2011, pp. 5-6). Avian collision risks are related to both the total number of turbines and the height of the turbines (Kuvlesky et al. 2007, p. 2488; NRC 2007, p. 138; Chamberlain et al. 2006, p. 198). Increasing power output per turbine is key to reducing the cost of offshore wind energy generation, necessitating the development of larger turbines (DOE and BOEMRE 2011, p. 15). As approved, the
   Buildout (when all available sites are either developed or restricted) of the wind industry along the Atlantic coast will result in the largest network of overwater avian hazards ever constructed, adding a new source of mortality to many bird populations (Watts 2010, p. 1), some of which can little tolerate further reductions before realizing population-level effects. Watts (2010, p. 1) used a form of harvest theory called Potential Biological Removal to develop a population framework for estimating sustainable limits on human-induced bird mortality. Enough information was available from the literature for 46 nongame waterbird species to allow for estimates of sustainable mortality limits from all human-caused sources. Among these 46 populations, red knot stood out as having particularly low mortality limits (Watts 2010, p. 1).
   Using an estimated rangewide population size of 20,000 red knots, Watts (2010, p. 39) estimated that human-induced direct mortality exceeding 451 birds per year would start to cause population declines. This estimate of 451 birds per year could increase with the use of updated estimates of population size (see the "Population Surveys and Estimates" section of the Rufa Red Knot Ecology and Abundance supplemental document) and survival (e.g., Schwarzer et al. 2012, p. 729; McGowan et al. 2011a, p. 13). While the Watts (2010, p. 39) model underscores the vulnerability of red knot populations to direct human-caused mortality from any source (see also Oil Spills and Leaks, Harmful Algal Blooms, and Factor B, above), we have only preliminary information on the actual red knot collision risk posed by offshore wind turbines (e.g., based on collision rates in other countries, the effects of weather and artificial lighting, behavioral avoidance capacity, flight altitudes, migration routes). Best available data regarding these risk factors are presented below, but are currently insufficient to estimate the likely annual mortality of red knots upon buildout of offshore wind infrastructure.
   Research from Europe, where several offshore wind facilities are in operation, suggests that bird collision rates with offshore turbines may be higher than for turbines on land. For various waterbird species, annual collision rates from 6.7 to 19.1 birds per turbine have been reported (Kuvlesky et al. 2007, p. 2489). Collision risks depend on turbine design and configuration, geography, attractiveness of the habitat, behavior and ecology of the species, habitat and spatial use, and ability of the birds to perceive and avoid wind turbines at close range (Burger et al. 2011, p. 340; Kuvlesky et al. 2007, p. 2488; NRC 2007, p. 138).
   A number of studies from Europe also suggest that wind facilities could displace migrating waterfowl and shorebirds, create barriers to migration, and alter flight paths between foraging and roosting habitats (Kuvlesky et al. 2007, p. 2489). Such effects are thought to extend at least 1,969 ft (600 m) from the wind facility, but could extend 1.2 to 4.5 mi (2 to 4 km) for some species (Kuvlesky et al. 2007, p. 2490). Avoidance of wind energy facilities varies among species and depends on site, season, tide, and whether the facility is in operation. Disturbance tends to be greatest for migrating birds while feeding and resting (NRC 2007, p. 108). As with the potential for increasing hurricane frequency or severity (discussed under Asynchronies--Fall Migration, above), extra flying to avoid obstacles during migration represents additional energy expenditure (Niles et al. 2010a, p. 129), which could impact survival as well as the timing of arrival at stopover areas (see Asynchronies, above). However, displacement of birds from habitats around wind facilities somewhat reduces the risks of turbine collisions.
   Although little shorebird-specific information is available, the effect of weather on migrating bird flight altitudes has been well documented through the use of radar and thermal imagery. Numerous studies indicate that the risk of bird collisions with wind turbines (including offshore turbines) increases as weather conditions worsen and visibility decreases (Drewitt and Langston 2006, p. 31; Hueppop et al. 2006, pp. 102, 105-107; Exo et al. 2003 p. 51). If birds are migrating at high altitudes and suddenly encounter fog, precipitation, or strong head winds, they may be forced to fly at lower altitudes, increasing their collision risks if they fly in the rotor (i.e., turbine blade) swept zone (Drewitt and Langston 2006, p. 31). Avoidance behavior is likely to vary according to conditions. It is reasonable to expect that avoidance rates would be much reduced at times of poor visibility, in poor weather, at night (Chamberlain et al. 2006, p. 199), and under varying structure illumination conditions (Drewitt and Langston 2006, p. 31; Hueppop et al. 2006, p. 105). The greatest collision risk occurs at night, particularly in unfavorable weather conditions. Behavioral observations have shown that most birds fly closer to the height of turbine rotor blades at night than during day, and that more birds collide with rotor blades at night than by day (Exo et al. 2003, p. 51).
   Burger et al. (2011, pp. 341-342) used a weight-of-evidence approach to examine the risks and hazards from offshore wind development on the OCS for three species of coastal waterbirds, including red knot. Three levels of exposure were identified: Micro-scale (whether the species is likely to fly within the rotor swept area, governed by behavioral avoidance abilities); meso-scale (occurrence within the rotor swept zone or hazard zone, governed by flight altitude); and macro-scale (occurrence of species within the geographical areas of interest). Regarding micro-scale exposure, little is known about the red knot's abilities to behaviorally avoid turbine collisions (Burger et al. 2011, p. 346), an important factor in determining collision risk (Chamberlain et al. 2006, p. 198). The red knot's visual acuity and maneuverability are known to be good, but no actual interactions with wind turbines have been observed. The red knot's ability to avoid turbines, even if normally good, could be reduced in poor visibility, high winds, or inclement weather.
   Avoidance may be more difficult upon descent after long migratory flights than on ascent (Burger et al. 2011, p. 346). Lighting on tall structures has been shown to be a significant risk factor in avian collisions (Kuvlesky et al. 2007, p. 2488; Manville 2009; entire). Particularly during inclement weather, birds become disoriented and entrapped in areas of artificially lighted airspace. Although the response of red knots to lighting is not known, red knots are inferred to migrate during both night and day, based on flight durations and distances documented by geolocators (
   Regarding meso-scale exposure, the migratory flight altitude of red knots remains unknown (
   Regarding macro-scale exposure, red knot migratory crossings of the Atlantic OCS are likely to occur broadly throughout this ocean region, with possible concentrations south of
   South of the Atlantic coast stopovers, red knots' migratory pathways may be either coast-following, OCS-crossing, or a mixture of both (
   Although exposure of red knots to collisions with offshore wind turbines is broad geographically, exposure is much more restricted temporally, occurring mainly during brief portions of the spring and fall migration when long migratory flights occur over open water (
   Taking advantage of the limited temporal exposure of migrating birds to offshore turbine collisions, the authorization for one offshore wind facility in New Jersey's State waters includes operational shutdowns during certain months when red knots and two federally listed bird species (piping plovers and roseate terns) may be present. The shutdowns would occur only during inclement weather conditions (USFWS 2012d, p. 3) that may prompt lower migration altitudes and hinder avoidance behaviors.
Wind Energy--Terrestrial
   The number of land-based wind turbines installed within the U.S. range of the red knot has increased substantially in the past decade (table 13). As of 2009, estimates of total avian mortality at U.S. turbines ranged from 58,000 to 440,000 birds per year, and were associated with high uncertainty due to inconsistencies in the duration and intensity of monitoring studies (Manville 2009, p. 268). In 2008, DOE released a report to investigate the feasibility of achieving 20 percent of U.S. electricity from wind by 2030 (DOE 2008, p. 1), a scenario that would substantially reduce U.S. carbon dioxide emissions (DOE 2008, p. 107). The 20 percent wind scenario envisions 251 GW of land-based generation in addition to 54 GW of shallow-water offshore production (DOE 2008, p. 10). Using an average capacity of 2 MW per turbine (
Table 13--Installed Wind Energy Generation Capacity by State Within theU.S. Range of the Red Knot (Including Interior Migration Pathways), 1999 and 2012 (DOE 2012). [U.S. average turbine size was 1.97 MW in 2011, up from 0.89 MW in 2000 (University of Michigan 2012, p. 1). We divided the megawatts by these average turbine sizes to estimate the numbers of turbines.] 1999 2012 State Megawatts Estimated Megawatts Estimated number of number of turbines turbines Alabama 0.000 0 0 0 Arkansas 0.000 0 0 0 Colorado 21.600 24 2,301 1,168 Connecticut 0.000 0 0 0 Delaware 0.000 0 2 1 Florida 0.000 0 0 0 Georgia 0.000 0 0 0 Illinois 0.000 0 3,568 1,811 Indiana 0.000 0 1,543 783 Iowa 242.420 272 5,137 2,608 Kansas 1.500 2 2,712 1,377 Kentucky 0.000 0 0 0 Louisiana 0.000 0 0 0 Maine 0.100 0 431 219 Maryland 0.000 0 120 61 Massachusetts 0.300 0 100 51 Michigan 0.600 1 988 502 Minnesota 273.390 307 2,986 1,516 Mississippi 0.000 0 0 0 Missouri 0.000 0 459 233 Montana 0.100 1 645 327 Nebraska 2.820 3 459 233 New Hampshire 0.050 0 171 87 New Jersey 0.000 0 9 5 New York 0.000 0 1,638 831 North Carolina 0.000 0 0 0 North Dakota 0.390 1 1,679 852 Ohio 0.000 0 426 216 Oklahoma 0.000 0 3,134 1,591 Pennsylvania 0.130 1 1,340 680 Rhode Island 0.000 0 9 5 South Carolina 0.000 0 0 0 South Dakota 0.000 0 784 398 Tennessee 0.000 0 29 15 Texas 183.520 206 12,212 6,199 Vermont 6.050 7 119 60 Virginia 0.000 0 0 0 West Virginia 0.000 0 583 296 Wisconsin 22.980 26 649 329 Wyoming 72.515 81 1,410 716 Total 828.465 931 45,643 23,169
   Although avian impacts from land-based wind turbines are generally better documented than in the offshore environment, relatively little shorebird-specific information is available. Compiling estimated mortality rates from nine U.S. wind facilities (including four in California), Erickson et al. (2001, pp. 2, 37) calculated an average of 2.19 avian fatalities per turbine per year for all bird species combined, and found that shorebirds constituted only 0.2 percent of the total. Compiling 18 studies around the
   Even in coastal states, most of the wind capacity installed to date is located along interior ridgelines or other areas away from the coast. With operations starting in 2005 (
   Considerable wind facility development has occurred in recent years near the Texas coast, south of Corpus Christi, and in the Mexican State of Tamaulipas; many additional wind energy projects are proposed in this region (Newstead et al. in press). As of 2011, coastal wind installations in Texas totaled more than 1,200 MW, or about 13 to 15 percent of the Statewide total (Reuters 2011). Kuvlesky et al. (2007, pp. 2487, 2492-2493) identified the lower Gulf coast of Texas as a region where wind energy development may have a potentially negative effect on migratory birds. Onshore wind energy development in the area of Laguna Madre may expose red knots to direct and indirect impacts during daily or seasonal movements (Newstead et al. in press). Shorebirds departing the coast for destinations along the central flyway (see the "Migration--Northwest Gulf of Mexico" section of the Rufa Red Knot Ecology and Abundance supplemental document) may be at some risk from wind projects throughout the flyway, but especially those that are adjacent to the coast where birds on a northbound departure may not have reached sufficient altitude to clear turbine height before reaching migration altitude (Newstead et al. in press).
Wind Energy--Summary
   We analyzed shorebird mortality at land-based wind turbines in the United States, and we considered the red knot's vulnerability factors for collisions with offshore wind turbines that we expect will be built in the next few decades. We have no information regarding wind energy development in other countries. Based on our analysis of wind energy development in the United States, we expect ongoing improvements in turbine siting, design, and operation will help minimize bird collision hazards. However, we also expect cumulative avian collision mortality to increase through 2030 as the number of turbines continues to grow, and as wind energy development expands into coastal and offshore environments. Shorebirds as a group have constituted only a small percentage of collisions with U.S. turbines in studies conducted to date, but wind development along the coasts (where shorebirds might be at greater risk) did not begin until 2005.
   We are not aware of any documented red knot mortalities at any wind turbines to date, but low levels of red knot mortality from turbine collisions may be occurring now based on the number of turbines along the red knot's migratory routes (table 13) and the frequency with which red knots traverse these corridors. Based on the current number and geographic distribution of turbines, if any such mortality is occurring, it is likely not causing subspecies-level effects. However, as buildout of offshore, coastal, and inland wind energy infrastructure progresses, increasing mortality from turbine collisions may contribute to a subspecies-level effect due to the red knot's vulnerability to direct human-caused mortality. We anticipate that the threat to red knots from wind turbines will be primarily related to collision or behavioral changes during migratory or daily flights. Unless facilities are constructed at key stopover or wintering habitats, we do not expect wind energy development to cause significant direct habitat loss or degradation or displacement of red knots from otherwise suitable habitats.
Factor E--Conservation Efforts
   There are many components of Factor E, some of which are being partially managed through conservation efforts. For example, the reduced availability of horseshoe crab eggs from the past overharvest of crabs in
   Some threats to the red knot's other prey species (mainly mollusks) are being partially addressed. For example, the Service is working with partners to minimize the effects of shoreline stabilization projects on the invertebrate prey base for shorebirds (e.g., Rice 2009, entire), and management of ORVs is protecting the invertebrate prey resource in some areas. Other likely threats to the red knot's mollusk prey base (e.g., ocean acidification; warming coastal waters; marine diseases, parasites, and invasive species) cannot be managed at this time, although efforts to minimize ballast water discharges in coastal areas likely reduce the potential for introduction of new invasive species.
   Other smaller-scale conservation efforts implemented to reduce Factor E threats include beach recreation management to reduce human disturbance, gull species population monitoring and management in
Factor E--Summary
   Factor E includes a broad range of threats to the red knot. Reduced food availability at the
   In addition, the red knot's life-history strategy makes this species inherently vulnerable to mismatches in timing between its annual cycle and those periods of optimal food and weather conditions upon which it depends. The red knot's sensitivity to timing asynchronies has been demonstrated through a population-level response, as the late arrivals of birds in
   Other threats are likely to exacerbate the effects of reduced prey availability and asynchronies, including human disturbance, competition with gulls, and behavioral changes from wind energy development. Additional threats are likely to increase the levels of direct red knot mortality, such as HABs, oil spills and other contaminants, and collisions with wind turbines. In addition to elevating background mortality rates, these three threats pose the potential for a low-probability but high-impact event if a severe HAB or major oil or contaminant spill occurs when and where large numbers of red knots are present, or if a mass-collision event occurs at wind turbines during migration. Based on our review of the best scientific and commercial data available, the subspecies-level impacts from Factor E components are already occurring and are anticipated to continue and possibly increase into the future.
Cumulative Effects from Factors A through E
   Cumulative means an increase in quantity, degree, or force by successive addition. Synergy means the interaction of elements that, when combined, produce a total effect that is greater than the sum of the individual elements. Red knots face a wide range of threats across their range on multiple geographic and temporal scales. The effects of some smaller threats may act in an additive fashion to ultimately impact populations or the subspecies as a whole (cumulative effects). Other threats may interact synergistically to increase or decrease the effects of each threat relative to the effects of each threat considered independently (synergistic effects).
   An example of cumulative effects comes from local or regional sources of typically low-level but ongoing direct mortality, such as from hunting, normal levels of parasites and predation, stochastic weather events, toxic HAB events, oil pollution, and collisions with wind turbines. We have no evidence that any of these mortality sources individually are impacting red knot populations, but taken together, the cumulative effect of these threats may potentially aggravate population declines, or slow population recoveries, particularly since modeling has suggested that the red knot is inherently vulnerable to direct human-caused mortality (Watts 2010, p. 39). Red knots by nature flock together within wintering areas and at critical migration stopovers. Surveys indicate that red knot populations using Tierra del Fuego and
   An example of a localized synergistic effect is increased beach cleaning following a storm, HAB event, or oil spill. Red knots and their habitats can be impacted by both the initial event, and then again by the cleanup activities. Sometimes such response efforts are necessary to minimize the birds' exposure to toxins, but nonetheless cause further disturbance and possibly alter habitats (e.g., N. Douglass pers. comm.
   Modeling the effect of winds on migration in Calidris canutus canutus, Shamoun-Baranes et al. (2010, p. 285) found that unpredictable winds affect flight times and that wind is a predominant driver of the use of an intermittently used emergency stopover site. This study points to the interactions between weather and habitat. The somewhat uncertain but nevertheless likely threat to red knots from changing frequency, intensity, geographic paths, or timing of coastal storms could have a synergistic effect with loss or degradation of stopover habitats (e.g., changing storm patterns could intensify the red knot's need for a robust network of stopover sites). Likewise, encounters with more frequent, severe, or aberrant storms during migration might not only exact some direct mortality and the energetic costs (to survivors) of extra flight miles, but also could induce red knots to increase their use of stopover habitats in areas where shorebird hunting is still practiced (Nebel 2011, p. 217).
   Reduced food availability has also been shown to interact synergistically with asynchronies and several other threats. Escudero et al. (2012, p. 362) have suggested that declining prey quality in South American wintering areas may be a partial explanation for the increasing proportion of red knots arriving late in
   While direct predation by peregrine falcons may account for only minor losses of individual birds, observations by shorebird biologists in Virginia, Delaware, and New Jersey have found that the presence of peregrine falcons significantly affects red knot foraging patterns, causing birds to abandon or avoid beaches that otherwise would be used for foraging. During times of limited food availability, this disturbance could reduce the proportion of red knots that can attain sufficient weight for successful migration and breeding in the Arctic. As with predation, human disturbance can also have a synergistic effect with reduced food availability. The combined effects of these two threats (food availability and disturbance) at one key wintering site (Rio Grande, Argentina, in Tierra del Fuego) caused the red knot's energy intake rate to drop from the highest known for red knots anywhere in the world in 2000, to among the lowest in 2008 (Escudero et al. 2012, pp. 359-362). Especially when food resources are limited, human disturbance can also exacerbate competition in
   In
   In mallards, Fereidouni et al. (2009, pp. 1, 6) found that prior exposure to LPAI conferred some immunity to HPAI and could, therefore, increase the risk of mallards transmitting virulent forms of the disease (i.e., they tend to survive the HPAI and, therefore, can spread it). Olsen et al. (2006, p. 388) suggested that many wild bird species may be partially immune to HPAI due to previous exposure to LPAI, enhancing their potential to carry HPAI to previously unaffected areas. The applicability of this finding to shorebirds is unknown, but this finding suggests that species with high rates of LPAI (e.g. ruddy turnstone, mallards (Brown et al. 2013, p. 2)) could be at higher risk of transmitting HPAI, while red knots (with low rates of LPAI) could be more likely to die from HPAI, if exposed. Further, modeling has suggested that, if climate change leads to mismatches between the phenology of ruddy turnstones (the main LPAI carriers) and horseshoe crab spawning, the prevalence of LPAI in turnstones would be projected to increase even as their population size decreased (Brown and Rohani 2012, p. 1). Although the risk of a PCB-mediated HPAI outbreak in
   In the Arctic, synergistic interactions are expected to occur among shifting vegetation communities, loss of sea ice, changing relationships between red knots and their predators and competitors, and the timing of snow melt and insect emergence. Such changes are superimposed on the red knot's breeding season that naturally has very tight tolerances in time and energy budgets due to the harsh tundra conditions and the knot's exceptionally long migration. High uncertainty exists about when and how such synergistic effects may affect red knot survival or reproduction, but the impacts are potentially profound (Fraser et al. 2013, entire; Schmidt et al. 2012, p. 4421; Meltofte et al. 2007, p. 35; Ims and Fuglei 2005, entire; Piersma and Lindstroem 2004, entire; Rehfisch and Crick 2003, entire; Piersma and Baker 2000, entire; Zoeckler and Lysenko 2000, entire; Lindstroem and Agrell 1999, entire). For example, as conditions warm, vegetative conditions in the current red knot breeding range are likely to become increasingly dominated by trees and shrubs over the next century. It is unknown if red knots will respond to vegetative and other ecosystem changes by shifting their breeding range north, where they could face greater energetic demands of a longer migration, competition with Calidris canutus islandica, and possibly no reduction in predation pressure if predator densities also shift north as temperatures warm. Alternatively, red knots may attempt to adapt to changing conditions within their current breeding range, where they could face unfavorable vegetative conditions and a new suite of predators and competitors expanding northward.
Determination
   Section 4 of the Act (16 U.S.C. 1533), and its implementing regulations at 50 CFR part 424, set forth the procedures for adding species to the Federal Lists of Endangered and Threatened Wildlife and Plants. Under section 4(a)(1) of the Act, we may list a species based on (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) Overutilization for commercial, recreational, scientific, or educational purposes; (C) Disease or predation; (D) The inadequacy of existing regulatory mechanisms; or (E) Other natural or manmade factors affecting its continued existence. Listing actions may be warranted based on any of the above threat factors, singly or in combination.
   We have carefully assessed the best scientific and commercial data available regarding the past, present, and future threats to the rufa red knot. We have identified threats to the red knot attributable to Factors A, B, C, and E. The primary driving threats to the red knot are from habitat loss and degradation due to sea level rise, shoreline stabilization, and Arctic warming (Factor A), and reduced food availability and asynchronies in the annual cycle (Factor E). Other threats are moderate in comparison to the primary threats; however, cumulatively, they could become significant when working in concert with the primary threats if they further reduce the species' resiliency. These secondary threats include hunting (Factor B); predation (Factor C); and human disturbance, harmful algal blooms, oil spills, and wind energy development (Factor E). All of these factors affect red knots across their current range.
   Conservation efforts are being implemented in many areas of the red knot's range (see Factors A, B, C, and E). For example, in 2012, the ASMFC adopted the ARM for the management of the horseshoe crab population in the
   Red knots migrate annually between their breeding grounds in the Canadian Arctic and several wintering regions, including the Southeast United States, the Northeast Gulf of Mexico, northern Brazil, and Tierra del Fuego at the southern tip of South America. During both the spring and fall migrations, red knots use key staging and stopover areas to rest and feed. This life-history strategy makes this species inherently vulnerable to numerous changes in the timing of quality food and habitat resource availability across its geographic range. While a few examples suggest the species has some flexibility in migration strategies, the full scope of the species' adaptability to changes in its annual cycle is unknown.
   The Act defines an endangered species as any species that is "in danger of extinction throughout all or a significant portion of its range" and a threatened species as any species "that is likely to become endangered throughout all or a significant portion of its range within the foreseeable future." We find that the rufa red knot meets the definition of a threatened species due to the likelihood of habitat loss driven by climate change and human response to climate change and reduced food resources and further asynchronies in its annual cycle that result in the species' reduced redundancy, resiliency, and representation. While there is uncertainty as to how long it may take some of the climate-induced changes to manifest in population-level effects to the rufa red knot, we find that the best available data suggests the rufa red knot is not at a high risk of a significant decline in the near term. However, should the reduction in redundancy, resiliency, and representation culminate in an abrupt and large loss, or initiation of a steep rate of decline, of reproductive capability or we subsequently find that the species does not have the adaptive capacity to adjust to actual shifts in its food and habitat resources, then the red knot would be at higher risk of a significant decline in the near term, and thus would meet the definition of an endangered species under the Act. We base this determination on the immediacy, severity, and scope of the threats described above. Therefore, on the basis of the best available scientific and commercial data, we propose listing the rufa red knot as a threatened species in accordance with sections 3(6) and 4(a)(1) of the Act.
   Under the Act and our implementing regulations, a species may warrant listing if it meets the definition of an endangered or threatened species throughout all or a significant portion of its range. The rufa red knot proposed for listing in this rule is wide-ranging and the threats occur throughout its range. Therefore, we assessed the status of the subspecies throughout its entire range. The threats to the survival of the subspecies are not restricted to any particular significant portion of that range. Accordingly, our assessment and proposed determination applies to the subspecies throughout its entire range.
Available Conservation Measures
   Conservation measures provided to species listed as endangered or threatened under the Act include recognition, recovery actions, requirements for Federal protection, and prohibitions against certain practices. Recognition through listing results in public awareness and conservation by Federal, State, Tribal, and local agencies, private organizations, and individuals. The Act encourages cooperation with the States and requires that recovery actions be carried out for all listed species. The protection required by Federal agencies and the prohibitions against certain activities are discussed, in part, below.
   The primary purpose of the Act is the conservation of endangered and threatened species and the ecosystems upon which they depend. The ultimate goal of such conservation efforts is the recovery of these listed species, so that they no longer need the protective measures of the Act. Subsection 4(f) of the Act requires the Service to develop and implement recovery plans for the conservation of endangered and threatened species. The recovery planning process involves the identification of actions that are necessary to halt or reverse the species' decline by addressing the threats to its survival and recovery. The goal of this process is to restore listed species to a point where they are secure, self-sustaining, and functioning components of their ecosystems.
   Recovery planning includes the development of a recovery outline shortly after a species is listed and preparation of a draft and final recovery plan. The recovery outline guides the immediate implementation of urgent recovery actions and describes the process to be used to develop a recovery plan. Revisions of the plan may be done to address continuing or new threats to the species, as new substantive information becomes available. The recovery plan identifies site-specific management actions that set a trigger for review of the five factors that control whether a species remains endangered or may be downlisted or delisted, and methods for monitoring recovery progress. Recovery plans also establish a framework for agencies to coordinate their recovery efforts and provide estimates of the cost of implementing recovery tasks. Recovery teams (composed of species experts, Federal and State agencies, nongovernmental organizations, and stakeholders) are often established to develop recovery plans. When completed, the recovery outline, draft recovery plan, and final recovery plan will be available on our Web site (http://www.fws.gov/endangered), or from our New Jersey Fish and Wildlife Office (see FOR FURTHER INFORMATION CONTACT).
   Implementation of recovery actions generally requires the participation of a broad range of partners, including other Federal agencies, States, Tribes, nongovernmental organizations, businesses, and private landowners. Examples of recovery actions include habitat restoration (e.g., restoration of native vegetation), research, captive propagation and reintroduction, and outreach and education. The recovery of many listed species cannot be accomplished solely on Federal lands because their ranges may occur primarily or solely on non-Federal lands. Recovery of these species requires cooperative conservation efforts on private, State, and Tribal lands.
   If this species is listed, funding for recovery actions will be available from a variety of sources, including Federal budgets, State programs, and cost-share grants for non-Federal landowners, the academic community, and nongovernmental organizations. In addition, pursuant to section 6 of the Act, States regularly inhabited by rufa red knots during the wintering or stopover periods would be eligible for Federal funds to implement management actions that promote the protection or recovery of the rufa red knot. Information on our grant programs that are available to aid species recovery can be found at: http://www.fws.gov/grants.
   Although the rufa red knot is only proposed for listing under the Act at this time, please let us know if you are interested in participating in recovery efforts for this species. Additionally, we invite you to submit any new information on this species whenever it becomes available and any information you may have for recovery planning purposes (see FOR FURTHER INFORMATION CONTACT).
   Section 7(a) of the Act requires Federal agencies to evaluate their actions with respect to any species that is proposed or listed as an endangered or threatened species and with respect to its critical habitat, if any is designated. Regulations implementing this interagency cooperation provision of the Act are codified at 50 CFR part 402. Section 7(a)(4) of the Act requires Federal agencies to confer with the Service on any action that is likely to jeopardize the continued existence of a species proposed for listing or result in destruction or adverse modification of proposed critical habitat. If a species is listed subsequently, section 7(a)(2) of the Act requires Federal agencies to ensure that activities they authorize, fund, or carry out are not likely to jeopardize the continued existence of the species or destroy or adversely modify its critical habitat. If a Federal action may affect a listed species or its critical habitat, the responsible Federal agency must enter into formal consultation with the Service.
   Federal agency actions within the species habitat that may require conference or consultation or both as described in the preceding paragraph include management and landscape altering activities on Federal lands administered by the
   The Act and its implementing regulations set forth a series of general prohibitions and exceptions that apply to all endangered wildlife. The prohibitions of section 9(a)(2) of the Act, codified at 50 CFR 17.21 for endangered wildlife, in part, make it illegal for any person subject to the jurisdiction of the United States to take (includes harass, harm, pursue, hunt, shoot, wound, kill, trap, capture, or collect; or to attempt any of these), import, export, ship in interstate commerce in the course of commercial activity, or sell or offer for sale in interstate or foreign commerce any listed species. Under the Lacey Act (18 U.S.C. 42-43; 16 U.S.C. 3371-3378), it is also illegal to possess, sell, deliver, carry, transport, or ship any such wildlife that has been taken illegally. Certain exceptions apply to agents of the Service and State conservation agencies.
   We may issue permits to carry out otherwise prohibited activities involving endangered and threatened wildlife species under certain circumstances. Regulations governing permits are codified at 50 CFR 17.22 for endangered species, and at 17.32 for threatened species. With regard to endangered wildlife, a permit must be issued for the following purposes: For scientific purposes, to enhance the propagation or survival of the species, and for incidental take in connection with otherwise lawful activities.
   Our policy, as published in the
   (1) Unauthorized collecting, handling, possessing, selling, delivering, carrying, or transporting of the species, including import or export across State lines and international boundaries, except for properly documented antique specimens of these taxa at least 100 years old, as defined by section 10(h)(1) of the Act;
   (2) Introduction of nonnative species that compete with or prey upon the rufa red knot, or that cause declines of the red knot's prey species;
   (3) Unauthorized modification of intertidal habitat that regularly support concentrations of rufa red knots during the wintering or stopover periods; and
   (4) Unauthorized discharge of chemicals or fill material into any waters along which the rufa red knot is known to occur.
   (1) The following activities are not likely to result in a violation of section 9 of the Act; this list is not comprehensive: Harvest of horseshoe crabs in accordance with the ARM, provided the ARM is implemented as intended (e.g., including implementation of necessary monitoring programs), and enforced.
   Questions regarding whether specific activities would constitute a violation of section 9 of the Act should be directed to the New Jersey Fish and Wildlife Office (see FOR FURTHER INFORMATION CONTACT). Requests for copies of the regulations concerning listed animals and general inquiries regarding prohibitions and permits may be addressed to the
   Under section 4(d) of the Act, the Secretary has discretion to issue such regulations as he deems necessary and advisable to provide for the conservation of threatened species. Our implementing regulations (50 CFR 17.31) for threatened wildlife generally incorporate the prohibitions of section 9 of the Act for endangered wildlife, except when a "special rule" promulgated pursuant to section 4(d) of the Act has been issued with respect to a particular threatened species. In such a case, the general prohibitions in 50 CFR 17.31 would not apply to that species, and instead, the special rule would define the specific take prohibitions and exceptions that would apply for that particular threatened species, which we consider necessary and advisable to conserve the species. The Secretary also has the discretion to prohibit by regulation with respect to a threatened species any act prohibited by section 9(a)(1) of the Act. Exercising this discretion, which has been delegated to the Service by the Secretary, the Service has developed general prohibitions that are appropriate for most threatened species in 50 CFR 17.31 and exceptions to those prohibitions in 50 CFR 17.32. We are not proposing to promulgate a special section 4(d) rule, and as a result, all of the section 9 prohibitions, including the "take" prohibitions, will apply to the rufa red knot. (As described above, harvest of horseshoe crabs in accordance with the ARM is not likely to result in take under section 9 of the Act.)
   Listing the rufa red knot under the Act would invoke provisions under various State laws that would prohibit take and encourage conservation by State government agencies. Further, States may enter into agreements with Federal agencies to administer and manage areas required for the conservation, management, enhancement, or protection of endangered species. Funds for these activities could be made available under section 6 of the Act (Cooperation with the States). Thus, the Federal protection afforded to these species by listing them as endangered species will be reinforced and supplemented by protection under State law.
   A determination to list the rufa red knot as a threatened species under the Act, if we ultimately determine that listing is warranted, will not regulate greenhouse gas emissions. Rather, it will reflect a determination that the rufa red knot meets the definition of a threatened species under the Act, thereby establishing certain protections for it under the Act. While we acknowledge that listing will not have a direct impact on those aspects of climate change impacting the rufa red knot (e.g., sea level rise, ocean acidification, warming coastal waters, changing patterns of coastal storm activity, warming of the Arctic), we expect that listing will indirectly enhance national and international cooperation and coordination of conservation efforts, enhance research programs, and encourage the development of mitigation measures that could help slow habitat loss and population declines. In addition, the development of a recovery plan will guide efforts intended to ensure the long-term survival and eventual recovery of the rufa red knot.
Required Determinations
Clarity of the Rule
   We are required by Executive Orders 12866 and 12988 and by the Presidential Memorandum of
   (1) Be logically organized;
   (2) Use the active voice to address readers directly;
   (3) Use clear language rather than jargon;
   (4) Be divided into short sections and sentences; and
   (5) Use lists and tables wherever possible.
   If you feel that we have not met these requirements, send us comments by one of the methods listed in the ADDRESSES section. To better help us revise the rule, your comments should be as specific as possible. For example, you should tell us the numbers of the sections or paragraphs that are unclearly written, which sections or sentences are too long, the sections where you feel lists or tables would be useful, etc.
National Environmental Policy Act (42 U.S.C. 4321 et seq.)
   We have determined that environmental assessments and environmental impact statements, as defined under the authority of the National Environmental Policy Act of 1969, need not be prepared in connection with listing a species as an endangered or threatened species under the Endangered Species Act. We published a notice outlining our reasons for this determination in the
References Cited
   A complete list of all references cited in this proposed rule is available on the Internet at http://www.regulations.gov or upon request from the Field Supervisor,
Authors
   The primary authors of this proposed rule are the staff members of the
List of Subjects in 50 CFR Part 17
   Endangered and threatened species, Exports, Imports, Reporting and recordkeeping requirements, and Transportation.
Proposed Regulation Promulgation
   Accordingly, we propose to amend part 17, subchapter B of chapter I, title 50 of the Code of Federal Regulations, as set forth below:
PART 17--[AMENDED]
   1. The authority citation for part 17 continues to read as follows:
   Authority: 16 U.S.C. 1361-1407; 1531-1544; 4201-4245; unless otherwise noted.
   2. In SEC 17.11(h) add an entry for "Knot, rufa red" to the List of Endangered and Threatened Wildlife in alphabetical order under Birds to read as set forth below:
SEC 17.11 Endangered and threatened wildlife.
* * * * *
   (h) * * *
Species Historic range Vertebrate population where endangered or threatened Common name Scientific name * * * * * * * BIRDS * * * * * * * Knot, rufa red Calidris canutus Argentina, Aruba, Entire ssp. rufa Bahamas, Barbados, Belize, Brazil, British Virgin Islands, Canada, Cayman Islands, Chile, Colombia, Costa Rica, Cuba, Dominican Republic, El Salvador, France (Guadeloupe, French Guiana), Guatemala, Guyana, Haiti, Jamaica, Mexico, Panama, Paraguay, Suriname, Trinidad and Tobago, Uruguay, Venezuela, U.S.A. (AL, AR, CT, CO, DE, FL, GA, IA, IL, IN, KS, KY, LA, MA, MD, ME, MI, MN, MO, MS, MT, NE, NC, ND, NH, NJ, NY, OH, OK, PA, RI, SC, SD, TN, TX, VA, VT, WI, WV, WY, Puerto Rico, U.S. Virgin Islands) * * * * * * *
Species Status When Critical Special rules listed habitat Common name * * * * * * * BIRDS * * * * * * * Knot, rufa red T N/A N/A * * * * * * *
   Dated:
Rowan W. Gould,
Acting Director,
[FR Doc. 2013-22700 Filed 9-27-13;
BILLING CODE 4310-55-P
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