POTENTIAL ADVERSE EFFECTS OF NEAR-SHORE INTERTIDAL OYSTER AQUACULTURE ON SHOREBIRDS AND HORSESHOE CRABS: A CRITICAL NEED FOR ASSESSMENT

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1 POTENTIAL ADVERSE EFFECTS OF NEAR-SHORE INTERTIDAL OYSTER AQUACULTURE ON SHOREBIRDS AND HORSESHOE CRABS: A CRITICAL NEED FOR ASSESSMENT Prepared for The New Jersey Endangered and Nongame Species Advisory Committee Prepared by David Mizrahi PhD, New Jersey Audubon (ENSAC member) Richard Lathrop PhD, Rutgers University (ENSAC member) Joanna Burger PhD, Rutgers University ENSAC member Joseph Smith PhD, American Littoral Society & LJ Niles Associates Lawrence Niles PhD, American Littoral Society & LJ Niles Associates July 15, 2015

2 EXECUTIVE SUMMARY The Endangered and Nongame Species Committee (ENSAC) recommends that expansion of near-shore intertidal oyster aquaculture along New Jersey's Delaware Bay shore be delayed in areas of moderate and high Red Knot use until there is a thorough evaluation of the risks to Red Knots, other shorebirds, and spawning horseshoe crabs. The Red Knot was recently designated as "threatened" under the US Endangered Species Act. Several factors must be thoroughly evaluated before expansion can be considered. These include displacement of Red Knots and other shorebirds from crucial foraging areas and direct disturbance to foraging or roosting Red Knots and other shorebirds, both of which could have significant adverse effects on foraging efficiency. Potentially adverse effect to horseshoe crabs, such as displacement from preferred feeding habitats direct impacts to their prey and impingement on oyster aquaculture gear must also be assessed. Oyster culturing in Delaware Bay has important societal and economic benefits, but expansion of the industry should only be undertaken after explicitly designed research has documented potential impacts and strategies are developed to mitigate adverse effects so that the long-term viability of Red Knot and other shorebird populations can be ensured. The Committee s reasons for this recommendation are as follows: 1. There is considerable evidence that Red Knots, recently listed on US Endangered Species List, have declined, and their populations are threatened. 2. Red Knots, and other shorebirds that have also declined, are dependent upon excess eggs of Horseshoe Crabs as their food source to gain weight for their northward migration in May. 3. Excess eggs are available to Red Knots only when the spawning horseshoe crab population is sufficiently large to result in females digging up the nests of other crabs. 4. Several studies have indicated that shorebirds, including the Red Knot, are adversely impacted by the presence of many human activities. 5. When foraging or roosting Red Knots and other shorebirds are disrupted by human activities, they often stop feeding, fly away, and do not return, making it difficult to gain sufficient weight to migrate successfully to the Arctic. 6. Foraging Red Knots and other shorebirds may avoid beaches with near-shore intertidal oyster aquaculture rack structures and the activities associated with their maintenance, thereby reducing their options for foraging during a critical migratory staging period in Delaware Bay. 7. Certain types of near-shore intertidal oyster aquaculture activity (e.g., access to racks and bags using all-terrain vehicles to conduct daily maintenance) may disrupt or prevent horseshoe crabs from coming to beaches to spawn, thus reducing eggs available for foraging Red Knots. 8. Prior to the initiation of near-shore intertidal oyster aquaculture at the Rutgers Cape Shore, Laboratory, there were large horseshoe crab spawning concentrations at the site. This was not the case following installation of rack and bag aquaculture structures and associated oyster aquaculture activities. In the following document, these issues are discussed and evaluated in light of studies published in the refereed literature. Considerable effort has been made by the Atlantic States Marine Fisheries Council, the State of New Jersey, conservation organizations and volunteers to enhance Red Knot and other shorebird populations by: (1) reducing the harvest of Delaware Bay horseshoe crabs, (2) restricting access to important shorebird beaches during the spring migration staging period, (3) restoring horseshoe crab spawning and shorebird foraging habitat and (4) extensive multi-state, multi-national studies to understand the system and the importance of Delaware Bay to the long-term persistence of Red Knots. 2

3 INTRODUCTION There is considerable evidence suggesting that horseshoe crab (Limulus polyphemus, [Linnaeus].)spawning on Delaware Bay beaches have experienced marked declines in since the increase in crab harvest, which began in the 1990s (Smith et al. 2009). In the same period there has been a decline in numbers of migrating shorebirds in Delaware Bay (Baker et al. 2004, Niles et al. 2009). This decline has led to the Red Knot being listed as Threatened on the Federal Endangered Species list. A number of studies have shown that many types of human activities disrupt the foraging behavior of shorebirds (Burger and Niles 2013), including Red Knots (Burger et al. in revision). There is now considerable interest in expanding oyster aquaculture in southern New Jersey, including high-use shorebird areas in Delaware Bay. The potential for new oyster aquaculture development to affect achieving shorebird conservation goals adversely is important to understand and consider because of the recent listing of the Red Knot as threatened under the Endangered Species Act (ESA). To determine the compatibility of the proposed expansion of near-shore intertidal aquaculture on Delaware Bay with protection of the Red Knot and its critical habitat under provision of the ESA, we recommend that the impact of existing aquaculture activities on Red Knots and horseshoe crabs. Research approaches, such as Before-After-Control-Impact; aka BACI; Smith et al. 1993) should be initiated to assess potential adverse effects of near-shore intertidal oyster aquaculture and associated activities on shorebirds and horseshoe crabs and must be completed before any new development is approved. It is our understanding that such research efforts are beginning with a grant to research faculty at Rutgers Cooperative Extension (Maslo et al. personal communication). In this brief, we discuss background on the issue of near-shore intertidal oyster aquaculture, ESA implications, potential impacts on shorebirds and horseshoe crabs, and recommendations to avert them. This brief was developed by a sub-committee of the Endangered and Nongame Species Committee (ENSAC, Mizrahi [chair], Lathrop, Burger), with technical assistance from Joseph Smith (Niles and Associates, LLC) and Lawrence Niles (Niles and Associates, LLC, former Chief of the Endangered and Nongame Species Program [ENSP]). The document is intended to address the possible impacts (negative or positive) to Red Knots and the Red Knot-horseshoe crab interaction, which is within the purview of the ENSAC's responsibilities. The Committee recognizes the importance of oyster aquaculture to the economy and culture of Delaware Bay, and the potential positive effects of the industry. POTENTIAL IMPACT OF EXPANDED AQUACULTURE DEVELOPMENT Overview Although the effects of current near-shore intertidal oyster aquaculture infrastructure and activity has, to date, not been studied specifically, disturbance phenomena and adverse effects on Red Knot behavior and feeding that are related to some human activities within Red Knot utilization areas have been reported (Burger et al. in review, Burger and Niles 2013, 2014). Additionally, data from Rutgers Cape Shore Laboratory, the one area of the Delaware Bay shore where there is ongoing intensive near-shore intertidal oyster aquaculture suggests that shorebird use there has decreased (Niles et al. 2008, 2013) since the early 2000s. Furthermore, horseshoe crab egg densities decreased from the highest among New Jersey beaches to one of the lowest (Dey et al. 2012, Pooler et al. 2003, Shuster and Botton 1985). With the listing of the Red Knot under the ESA, a comprehensive assessment is essential. There are several potential ways that near-shore intertidal oyster aquaculture may influence Red Knot use of beach habitat and/or degrade feeding habitat quality. 3

4 First, human activity and machine noise associated with aquaculture activities may disturb Red Knots so that they avoid beaches that are critical feeding habitat ("Harass"). Second, aquaculture structures alone (no humans or machines present) may preclude Red Knots from foraging between or near structures ("Harm"). Third, near-shore intertidal aquaculture rack and bag arrays adjacent to key horseshoe crab spawning beaches may obstruct their movement and/or access to feeding areas in the intertidal flats, resulting in a net decrease in horseshoe crab egg availability for Red Knots. If new near-shore intertidal oyster aquaculture leases are approved following USFWS guidelines (see Appendix 1), oyster racks and bags could significantly reduce the amount of New Jersey's Delaware Bay shore habitats crucial to Red Knots and horseshoe crabs. If any of these potential impacts to Red Knots and horseshoe crabs described above are documented through the evaluation we recommend, then nearshore intertidal oyster aquaculture could have considerable cumulative impacts. We recommend caution moving near-shore intertidal oyster aquaculture forward and that each of the potential adverse effects we describe be evaluated critically to ensure future development of the industry can proceed while reducing and mitigating potential impacts to shorebirds and horseshoe crabs. Our understanding of the need for caution comes partly from the USFWS Aquaculture Recommendations of December 11, 2014 (see Appendix 1). "Pursuant to Section 7 of the Endangered Species Act (ESA), the Service recommends the following conservation measures to avoid adverse effects to Red Knots from native shellfish aquaculture activities on the New Jersey side of Delaware Bay. Projects that are not likely to adversely affect listed species must not result in take, which includes harass, harm, pursue, hunt, shoot, wound, kill, trap, capture, and collect. Harm is defined to include significant habitat modification or degradation that results in death or injury to listed species by significantly impairing behavioral patterns such as breeding, feeding, or sheltering. Harass is defined as actions that create the likelihood of injury to a listed species by annoying it to such an extent as to significantly disrupt normal behavior patterns including, but not limited to, breeding, feeding, or sheltering. Specific to Red Knots, unimpeded feeding on horseshoe crab eggs along key portions of the Delaware Bay shoreline is essential to their gaining adequate weight for successful migration and subsequent breeding upon arrival in their Arctic breeding ground, while roosting above the water line constitutes sheltering." Our concern for a slow and careful approach to expanding near-shore intertidal aquaculture in the proposed development areas is based on several important considerations. Several scientific publications indicate that the stretch of New Jersey s Delaware Bay shoreline likely to be considered for aquaculture expansion represents among the most important migratory shorebird staging habitats in the world (Atkinson et al. 2007, Baker et al. 2004, Botton et al. 1994, Clark et al. 1993, Gillings et al. 2007, 2009, Haramis et al. 2007, Karpanty et al. 2006, Mizrahi and Peters 2009, Niles et al. 2008, 2009, Robinson et al. 2003, Tsipoura and Burger 1999), supporting 50-80% of the world s population of the rufa Red Knot each spring (Brown et al. 2000). This is primarily because this same stretch of coastline is part of the largest spawning aggregation of horseshoe crabs in the world (Shuster and Sekiguchi 2009). Similarly well-documented is the decline of Red Knot and horseshoe crab populations in the Delaware Bay (Morrison et al 2004, Niles et al. 2009, Department of Interior 2013). Beyond ESA listing of the Red Knot, significant efforts are underway to reverse these declining population trends through beach access management by the public during the spring migration season (Isaacs 2012), horseshoe crab habitat restoration in the Delaware Bay (Niles et al. 2013), and through more restrictive harvest management of Delaware Bay horseshoe crabs (McGowan et al. 2011, Niles et al. 2009). 4

5 Under the ESA, ongoing or expanded near-shore intertidal aquaculture activities should not diminish Red Knot numbers, reproduction, or distribution so that the likelihood of survival and recovery in the wild is appreciably reduced. Furthermore, activities also cannot result in direct or indirect "take" of Red Knots by causing disturbance or adverse habitat modification that actually kills or injures them or that impairs their essential behavioral patterns including breeding, feeding, or sheltering. Impacts to horseshoe crab populations that could adversely affect Red Knots could constitute such a "take". The potential for nearshore intertidal aquaculture to violate provisions of the ESA can only be understood by implementing a comprehensive assessment to determine effects from existing and expanded oyster aquaculture operations on Red Knots and the horseshoe crabs on which they depend. INTERTIDAL OYSTER AQUACULTURE Rack and bag oyster aquaculture (Forrest et al. 2009) structures were first established at the Rutgers Cape Shore Laboratory in the late 1990s, with a marked increase in the project footprint in the mid-2000s. Rack and bag arrays are generally arranged in 100-foot long segments and extend feet offshore. They typically are arranged in twin rows, three feet apart, with six-foot aisles between rows for ATV passage (Figure 1). Racks can be as low as three to four inches off the intertidal flat Figure 1. Aerial photograph of Cape Shore core rack and bag array. Rows within the array are approximately 600 feet long and 300 feet wide. 5

6 Figure 2. Near-shore intertidal rack and bag oystercatcher arrays at Rutgers Cape Shore Laboratory. Photo taken May (Gaine 2012) (Figure 2). The aquaculture structures are accessed from the shore, with daily movements across the beach and intertidal flats by workers on all-terrain vehicles (ATVs). The primary purpose of daily maintenance activities is the removal of Polydora worms (Maurer and Watling 1973) from oysters using gas-powered, high-pressure washers (Gaine 2012). Floating aquaculture structures may also be used in the intertidal zone, but are not likely to remain floating during mid-to-low tidal stages. Our understanding is that there is a great deal of variation in how these activities are conducted, in both frequency and intensity, which may allow modification to reduce potentially adverse effects on shorebirds. POTENTIAL ADVERSE EFFECTS OF INTERTIDAL OYSTER AQUACULTURE The following sections further describe the potential impacts of near-shore intertidal oyster aquaculture on Red Knots and other migratory shorebirds. Research efforts specifically directed at these issues will clarify the extent of these potential impacts, and provide data for all parties concerned. 6

7 Possible Geographic Scope of Intertidal Oyster Aquaculture Over 8.5 miles of Delaware Bay shoreline is presently leased and potentially could be considered for rack and bag-style intertidal oyster aquaculture (Figure 3). This includes the shoreline from Rutgers Cape Shore Laboratory to north of Reeds Beach, as well as sections of Moore s Beach, Heislerville and Egg Island Wildlife Management Areas. We presently do not know how many and which of these lease areas are under active consideration. Figure 3. Map of oyster aquaculture lease areas on New Jersey's Delaware Bay shore with intertidal leases highlighted. To examine the potential footprint that intertidal oyster aquaculture might represent, we undertook a build-out analysis based on the USFWS guidelines for the stretch of shoreline from the Cape Shores Lab to Kimble's Beach (Figure 4). These guidelines specify a 500 buffer around creek mouths, a 300 7

8 Figure 4. Potential build-out in current aquaculture leases of intertidal rack and bag oyster aquaculture based on guidelines developed by the USFWS. 8

9 buffer from Mean High Water and an overall 10% area coverage per lease of rack and bag structures. Each red line represents a double row of racks and bags 100 long with racks 2.5 wide and spaced 2 apart. Double rows are mapped in arrays of ten. This build-out analysis represents only one layout scenario with the rack and bag structures clustered together. Other layouts might disperse the individual rack and bag structures over a wider area. While the USFWS guidelines specify that an overall 10% of the lease area be covered by rack and bag structures, it does not include the area between rack structures or the travel lanes. When the area of these features are included, our potential build-out suggests that upwards of 20% to 30% of the lease area should be considered as part of the broader footprint for the intertidal aquaculture structures as well as associated activities. Adding the area of travel lanes from the Mean High Water line out to the rack and bag structures (not included in the build-out analysis) would further increase the footprint area. Disturbance of birds and foraging habitat displacement Previous research on Delaware Bay (Burger et al. in revision) and Atlantic Coast (Burger and Niles 2013) beaches has demonstrated that among all shorebirds, Red Knots appear to be the most sensitive to human disturbance. Furthermore Red Knot flocks have a low likelihood of returning to an area immediately after disturbance (Burger and Niles 2014). This is a particular problem because gulls return immediately after disturbance, occupying most available space and preventing the knots from foraging if and when they do return (Burger et al. 2007). Interspecific interference competition has been well documented for other shorebird species (Triplet et al.1999, Yates et al.2000, Vahl et al. 2005), Since 2003, considerable effort has been made on New Jersey Delaware Bay beaches to reduce disturbance through seasonal beach access restrictions during Red Knot migration staging periods (i.e., May 7 June 7) each year. A beach steward program implemented by volunteers at key beach entry points helps enforce access restrictions and educate visitors about the horseshoe crab and shorebird phenomenon on Delaware Bay (Isaacs 2012, A. Dey personal communication). Currently under consideration is an expansion of near-shore intertidal oyster aquaculture from Rutgers Cape Shore Laboratory to South Reeds Beach. This stretch of shoreline has optimal horseshoe crab spawning habitat (Latham et al. 2006) and has been the focus of horseshoe crab habitat restoration efforts in 2013 and 2014 (Niles et al. 2013). Furthermore, the area has supported a significant percentage of the bay-wide population of Red Knots during the period of 2002 to 2014 (Figure 5). In 2013 and 2014, an even greater percentage of the bay-wide population of Red Knots was documented in the area (23% and 38% respectively, NJDFW, A. Dey unpublished data). If disturbance-sensitive Red Knots, are displaced from preferred feeding areas, either by the placement of rack and bag arrays or the potential disturbance related to maintaining them (e.g., daily foot and ATV access during the low tide foraging periods, power-washing, see previous section "Intertidal Oyster Aquaculture"), this may impair weight gain during the crucial DE Bay staging period. 9

10 Figure 5. Map of Red Knot use on stretch of shoreline from the Aquaculture Development Zone (ADZ) to Cook s Beach. 10

11 Disrupting passage of horseshoe crabs to and from spawning beaches The Committee s main responsibility is Endangered and Nongame species. However, the relationship between shorebirds and horseshoe crabs during spring migration staging periods are inextricable. This relationship underpins the ability of Red Knots to gain sufficient weight to reach the Arctic in good breeding condition and survive until food resources become available after snowmelt (Morrison and Hobson 2004). Horseshoe crabs make precisely timed movements from offshore wintering areas to beaches during the spawning season. Aquaculture infrastructure may disrupt the free movement of horseshoe crabs to and from spawning beaches. Fewer horseshoe crabs may then be able to reach the beach, they may be unable to reach the beach at the optimal time during the spawning season or at optimal periods of the tidal cycle, or crabs may be unable to return to the bay, leaving them exposed to gull predation (Botton and Loveland 1989). In some cases, oyster culturing rack and bag arrays are only 3-4 inches off the sand surface (Gaine 2012), preventing horseshoe crab passage underneath. Even racks that are 12 inches above the sand surface may be avoided by horseshoe crabs because of their apparent aversion to overhead objects. Barlow (2009) found that horseshoe crabs avoided underwater shadows cast by overhead objects, presumed to be a predator avoidance behavior. The effect of racks on horseshoe crab movement needs to be examined. If rack and bag arrays either prevent some crabs from accessing beaches or alter their timing of arrival on beaches, this could result in a net reduction in horseshoe crab eggs on the beach and available to Red Knots and other shorebirds. As noted previously, the Rutgers Cape Shore Laboratory site had among the greatest horseshoe crab egg densities along New Jersey s Delaware Bay shore in the 1980s, but now ranks among the lowest (Table 1). This finding emphasizes the need to evaluate the degree that horseshoe crabs may be impeded by aquaculture structures to rule out the possibility that they were in some way associated with the decline horseshoe crab egg densities at Cape Shore. Currently, no data exist to evaluate the potential effects of near-shore intertidal oyster aquaculture on horseshoe crab movements. Consequently, a comprehensive understanding derived from explicitly designed research is critical to developing strategies to minimize potentially adverse effects. Potential impacts of foraging habitat displacement and reduction in food availability for horseshoe crabs during the spawning period Rack and bag aquaculture arrays may potentially displace crabs from feeding areas on intertidal flats. Racks are either too low for crabs to move beneath them to feed or racks may trigger crab avoidance because of their aversion to passing under overhead structures. Furthermore, ATV use to access racks could cause sediment compaction, thus may negatively affect bivalves living just below the sand surface, which horseshoe crabs feed. Research conducted at the Rutgers Cape Shore Laboratory before initiation of intertidal aquaculture suggests that horseshoe crabs significantly reduced the abundance of benthic bivalves (Botton 1984) and increased the depth of sediment mixing when compared with areas where crabs were excluded (Kraeuter and Fegley 1994). These findings strongly suggest that Delaware Bay's intertidal flats represent an important feeding resource for horseshoe crabs spawning each spring. Access to prey during the spawning season may be a key aspect of beach suitability for spawning crabs, and consequently, for shorebird foraging. 11

12 This combination of potential horseshoe crab exclusion and sediment compaction from vehicles could ultimately decrease the amount of benthic foraging habitat and prey availability for horseshoe crabs. If aquaculture expands and reaches build out, it may exclude horseshoe crabs from many prime intertidal feeding areas. Figure 6. Spawning horseshoe crab counts from the late 1970s illustrating that the Rutgers Cape Shore site had the highest spawning densities of crab of all NJ beaches surveyed (from Shuster and Botton 1985). 12

13 HISTORIC TRAJECTORY OF SHOREBIRD AND HORSESHOE CRAB EGG ABUNDANCE AT THE RUTGERS CAPE SHORE LABORATORY SITE The long history of research on shorebirds and horseshoe crabs in the Delaware Bay can provide insight into temporal in habitat quality changes at the Rutgers Cape Shore site. Surveys conducted in May and June 1999 suggested the site had the highest density of horseshoe crab eggs of any Delaware Bay beach in New Jersey (Pooler et al. 2003) (Table 1). This finding was supported by earlier surveys done by Shuster and Botton (1985), who also found the highest spawning horseshoe crab densities on the Rutgers Cape Shore site (NJ Oyster Research Laboratory (NJORL), Figure 6). More recent surveys of horseshoe crab eggs conducted by NJ Division of Fish & Wildlife and Stockton University (Dey et al. 2012, NJ Division of Fish and Wildlife, Endangered and Nongame Species Program 2012), indicate that the site has among the lowest horseshoe crab egg densities of the beaches surveyed in New Jersey (Table 1). Shorebird numbers showed a similar decline at the Rutgers Cape Shore site. Aerial survey results between 2001 and 2005 (Figure 7, from Niles et al. 2008), just prior to the marked increase in intertidal oyster aquaculture at the Cape Shores site, show a relatively even distribution of Red Knots along the Cape May peninsula south to Norbury's Landing, (Warner 2005). More recent aerial and ground-based shorebird surveys in 2013 and 2014 (Figure 8) show that most Red Knot habitat use occurs well north of the Cape Shore site (NJDFW, A. Dey unpublished data, Niles et al. 2013). These results suggest a greater amount of Red Knot use in areas being considered for new, near-shore intertidal oyster aquaculture development. Taken together, these data suggest a decline in horseshoe crab and shorebird use of the Rutgers Cape Shore site during a period that coincided with increased near-shore intertidal oyster aquaculture activity. Clearly, we cannot know if these activities caused the declines in horseshoe crabs and shorebird use of the site. However, we believe they present a possible scenario that prompts us to recommend a precautionary approach to future near-shore intertidal aquaculture development in Delaware Bay. This approach necessitates a thorough and explicitly designed assessment of the potential effects of aquaculture activities on horseshoe crabs and shorebirds. These data can then provide the insight needed to ensure that oyster aquaculture development along New Jersey's Delaware Bay shore is compatible with conservation of the Red Knot. SOCIAL DIMENSIONS Many stakeholders including recreational beach users, sport and commercial fishermen, municipalities, state and federal agencies, non-governmental organizations and conservation volunteers have made considerable effort to achieve effective conservation of Red Knots and horseshoe crabs in the Delaware Bay. This includes restricted beach access to reduce disturbance of shorebirds and a statewide harvest moratorium of horseshoe crabs in New Jersey. Furthermore the Atlantic States Marine Fisheries Commission is engaged in adaptive management of horseshoe crab harvest that is explicitly linked to the health of Red Knot populations (McGowan et al. 2011). Nonetheless, these harvest restrictions have not led to a marked increase in the bay s spawning horseshoe crab population more than 15 years after harvest restrictions were put in place (Smith and Robinson 2015). 13

14 Table 1. Horseshoe crab egg densities on five New Jersey beaches, , compared to a similar study done in 1999, approximately when near-shore intertidal aquaculture at the Rutgers Cape Shore site started. Recent data are given in eggs/m 2 and site ranks based on egg densities beaches in each survey (i.e., 1 = greatest, 5 = lowest densities). Beach Year Mean Standard 3 year Error average rank* rank** Raybins/Fortescue Reeds Beach Kimble's Beach Highs Beach Cape Shore year average all beaches 3817 *1999 from Pooler P.S., Smith D.R., Loveland R.E., Botton M.L., & Michels S.F. (2003) Assessment of sampling methods to estimate horseshoe crab (Limulus polyphemus (L.) egg density in Delaware Bay. Fish Bull, 101, ** taken from Dey A.D and D. Hernandez 2012 and NJDFW unpublished data SUMMARY CONCLUSION Given that horseshoe crab populations have not increased despite harvest restrictions and that the Red Knot was listed as "threatened" under the Endangered Species Act in early 2015, we recommend that a precautionary approach be undertaken with respect to future near-shore intertidal oyster aquaculture development. The areas likely to be proposed for future development are currently among the most important Red Knot migration staging areas in the Western Hemisphere. Their importance is linked to the high concentrations of horseshoe crab that spawn on the beaches there. We also recommend that future development be evaluated explicitly to determine potential adverse effects on Red Knots, their critical habitats and their primary food source, that is, horseshoe crab eggs. This approach will ensure long-term compatibility between a growing oyster aquaculture industry and the conservation of Red Knots and horseshoe crabs. 14

15 Figure 7. Red Knot distribution average over 5 years 2001 to The distribution shows a marked concentration in the area of the Rutgers Cape Shore site just north of Norbury's Landing (from Niles et al. 2008). 15

16 Figure 8. Simultaneous bay-wide counts of the Red Knot population in the Delaware Bay in 2013 and These figures illustrate Red Knot concentrations along beaches restored in 2013 and These areas coincide with those delineated for potential expansion of near-shore intertidal oyster aquaculture. RECOMMENDATIONS We recommend that no further development of near-shore intertidal oyster aquaculture occur in areas of moderate and high Red Knot use (i.e., as determined by the USFWS guidelines, see Figure 6) until a thorough evaluation of the risks to Red Knots, other shorebirds, and horseshoe crabs has been completed. This evaluation should include all of the potential impacts outlined above, including disturbance to birds foraging habitat displacement, disruption of horseshoe crab passage to and from spawning beaches, displacement of horseshoe crabs from feeding habitat and effects on horseshoe crab prey. Each of these factors must be evaluated using an experimental research design approach, which we believe has the best chance of providing insight to the potential adverse effects on Red Knots from the physical structures and human activities associated with near-shore intertidal oyster aquaculture. This research should also evaluate the potential benefits of oyster aquaculture, such as reduction of wave intensity, which could enhance horseshoe crab spawning and foraging conditions and thus increase in horseshoe crab egg availability for staging Red Knots and other shorebirds. Together, the results of these studies can be used to develop evidence-based recommendations for future development of oyster aquaculture in the Delaware Bay and best management practices to guide aquaculture activities that minimize adverse effects to Red Knots, other shorebirds and horseshoe crabs. 16

17 ACKNOWLEDGEMENTS We especially thank Dr. Amanda Dey, Principal Zooologist, NJ Division of Fish and Wildlife, who provided technical advice, data and analyses in her capacity as migratory shorebird biologist for the agency. We also thank members of the Endangered and Nongame Species Advisory Committee for providing helpful comments on earlier drafts of this document. Thanks also to David Jenkins, Chief, Endangered and Nongame Species Program for comments on earlier drafts and providing unpublished data used in this document. We thank Wendy Walsh, US Fish and Wildlife Service, for providing analyses of Red Knot use areas. Thanks also to John Bognar and Michael Ciappi, Rutgers Center for Remote Sensing and Spatial Analysis (CRSSA) for assistance with build-out analyses. LITERATURE CITED Atkinson, P.W., A.J. Baker, K.A. Bennett, N.A. Clark, J.A. Clark, K.B. Cole, A. Dekinga, A. Dey, S. Gillings, P.M. González, and others Rates of mass gain and energy deposition in Red Knot on their final spring staging site is both time-and condition-dependent. Journal of Applied Ecology 44: Baker, A., P. Gonzalez, T. Piersma, L. Niles, I. Nascimento, P. Atkinson, N. Clark, C. Minton, M. Peck, and G. Aarts Rapid population decline in Red Knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proceedings of the royal society of london series b-biological sciences 271: Barlow, R.B Vision in horseshoe crab. Pp , In. Biology and Conservation of horseshoe crab. Springer. Botton, M.L The importance of predation by horseshoe crab, Limulus polyphemus, to an intertidal sand flat community. Journal of Marine Research 42: Botton, M.L., and R.E. Loveland Reproductive risk: high mortality associated with spawning by horseshoe crab (Limulus polyphemus) in Delaware Bay, USA. Marine Biology 101: Botton, M.L., R.E. Loveland, and T.R. Jacobsen Site selection by migratory shorebirds in Delaware Bay, and its relationship to beach characteristics and abundance of horseshoe Crab (Limulus polyphemus) eggs. The Auk 111: Brown, S.C., C. Hickey, B. Harrington, and R. Gill United States shorebird conservation plan. Manomet Center for Conservation Sciences. Burger, J., S.A. Carlucci, C.W. Jeitner, and L. Niles Habitat choice, disturbance, and management of foraging shorebirds and gulls at a migratory stopover. Journal of Coastal Research Burger, J., and L. Niles Shorebirds and stakeholders: Effects of beach closure and human activities on shorebirds at a New Jersey coastal beach. Urban Ecosystems 16: Burger, J., and L.J. Niles Closure versus voluntary avoidance as a method of protecting migrating shorebirds on beaches in New Jersey. Wader Study Group Bulletin 120: Burger, J., L.J. Niles, A.D. Dey, T. Dillingham, S. Gates, and J. Smith. In review. An experimental examination of responses of Red Knots Calidris canutus rufa and other shorebirds to tides, people, and oyster culture at Reed s Beach, Delaware Bay, New Jersey. Wader Study Group Bulletin. Clark, K., L. Niles, and J. Burger Abundance and distribution of migrant shorebirds in Delaware Bay. Condor 95: Department of the Interior Fish & Wildlife Service 50 CFR Part 17 Endangered and Threatened Wildlife and Plants; Proposed Threatened Status for the Rufa Red Knot (Calidris canutus rufa); Proposed Rule.Vol. 78 Monday, No. 189 September 30, 2013 Dey, A.D., K. Kalasz, and D. Hernandez Delaware Bay horseshoe crab egg survey: Report to the Atlantic States Marine Fisheries Commission. 17

18 Forrest, B.M., N.B. Keeley, G.A. Hopkins, S.C. Webb, and D.M. Clement Bivalve aquaculture in estuaries: Review and synthesis of oyster cultivation effects. Aquaculture 298:1 15. Gaine, E Spraying deterrent stimuli as a treatment method for the prevention of biofouling caused by the mudworm Polydora ligni webster on New Jersey oyster farms. Rutgers University-Camden Graduate School. Gillings, S., P.W. Atkinson, S.L. Bardsley, N.A. Clark, S.E. Love, R.A. Robinson, R.A. Stillman, and R.G. Weber Shorebird predation of horseshoe Crab eggs in Delaware Bay: species contrasts and availability constraints. Journal of Animal Ecology 76: Gillings, S., Philip W. Atkinson, Allan J. Baker, Karen A. Bennett, Nigel A. Clark, Kimberly B. Cole, Patricia M. González, Kevin S. Kalasz, Clive D. T. Minton, Lawrence J. Niles, Ron C. Porter, Inês De Lima Serrano, Humphrey P. Sitters, and Jean L. Woods Staging Behavior in Red Knot (Calidris Canutus) in Delaware Bay: Implications for Monitoring Mass and Population Size. Haramis, G., W. Link, P. Osenton, D. Carter, R. Weber, N. Clark, M. Teece, and D. Mizrahi Stable isotope and pen feeding trial studies confirm the value of horseshoe Crab Limulus polyphemus eggs to spring migrant shorebirds in Delaware Bay. Journal of avian biology 38: Isaacs, J.R Protecting New Jersey s Migratory Shorebirds: A Stewardship Model of Conservation. RAMAPO COLLEGE OF NEW JERSEY. Karpanty, S.M., J.D. Fraser, J. Berkson, L.J. Niles, A. Dey, and E.P. Smith Horseshoe Crab eggs determine Red Knot distribution in Delaware Bay. Journal of Wildlife Management 70: Kraeuter, J.N., and S.R. Fegley Vertical disturbance of sediments by horseshoe crab (Limulus polyphemus) during their spawning season. Estuaries 17: Latham, R.G., M. Allen, and A. Love Mapping and Assessing Critical horseshoe Crab Spawning Habitats of Delaware Bay. Rutgers University Center for Remote Sensing & Spatial Analysis. Maurer, D., and L. Watling The biology of the oyster community and its associated fauna in Delaware Bay. McGowan, C.P., D.R. Smith, J.A. Sweka, J. Martin, J.D. Nichols, R. Wong, J.E. Lyons, L.J. Niles, K. Kalasz, J. Brust, and others Multispecies modeling for adaptive management of horseshoe crab and Red Knots in the Delaware Bay. Natural Resource Modeling 24: Mizrahi, D.S., and K.A. Peters Relationships between sandpipers and Horseshoe Crab in Delaware Bay: A synthesis. Pp , In. Biology and conservation of horseshoe crabs. Springer. Morrison, R. I. G., R. K. Ross, L. J. Niles Declines in wintering populations of red knots in southern South America. The Condor 106(1): Niles, L.J., Jonathan Bart, Humphrey P. Sitters, Amanda D. Dey, Kathleen E. Clark, Phillip W. Atkinson, Allan J. Baker, Karen A. Bennett, Kevin S. Kalasz, Nigel A. Clark, Jacquie Clark, Simon Gillings, Albert S. Gates, Patricia M. GonzÁlez, Daniel E. Hernandez, Clive D. T. Minton, R. I. Guy Morrison, Ronald R. PORTER, R. Ken Ross, and C. Richard Veitch Effects of horseshoe crab harvest in delaware bay on red knots: are harvest restrictions working? Niles, L.J., H.P. Sitters, A.D. Dey, P.W. Atkinson, A.J. Baker, K.A. Bennett, R. Carmona, K.E. Clark, N.A. Clark, C. Espoz, and others Status of the Red Knot (Calidris canutus rufa) in the Western Hemisphere. Cooper Ornithological Society. Niles, L.J., J.A.. Smith, D.F. Daly, T. Dillingham, W. Shadel, A.D. Dey, M.S. Danihel, S. Hafner, and D. Wheeler Restoration of horseshoe crab and migratory shorebird habitat on five Delaware Bay Beaches Damaged by Superstorm Sandy. Report. NJDEP Seasonal Delaware Bay and Atlantic Coast Beach Closure Location Map. Available online at NJ Division of Fish and Wildlife, Endangered and Nongame Species Program Unpublished data, horseshoe Crab egg survey. Pooler, P.S., D.R. Smith, R.E. Loveland, M.L. Botton, and S.F. Michels Assessment of sampling methods to estimate horseshoe Crab (Limulus polyphemus shoe crab (L.) egg density in Delaware Bay. Fish Bull 101:

19 Robinson, R.A., P.W. Atkinson, and N.A. Clark Arrival and weight gain of Red Knot Calidris canutus, Ruddy Turnstone Arenaria interpres and Sanderling Calidris alba staging in Delaware Bay in spring. BTO Research Report. Shuster, C.N., and M.L. Botton A contribution to the population biology of horseshoe crab, Limulus polyphemus (L.), in Delaware Bay. Estuaries 8: Shuster, C.N., and K. Sekiguchi Basic habitat requirements of the extant species of Horseshoe crab (Limulacea). Pp , In. Biology and conservation of horseshoe crab. Springer. Smith, D.R., M.J. Millard, and R.H. Carmichael Comparative status and assessment of Limulus polyphemus with emphasis on the New England and Delaware Bay populations. Pp , In. Biology and conservation of horseshoe crabs. Springer. Smith, D.R., and T.J. Robinson Horseshoe crab spawning activity in Delaware Bay, USA, after harvest reduction: a mixed-model analysis. Estuaries and Coasts Smith, E.P., D.R. Orvos, and J. Cairns Jr Impact assessment using the before-after-control-impact (BACI) model: concerns and comments. Canadian Journal of Fisheries and Aquatic Sciences 50: Triplet, P., R.A. Stillman and J.D. Goss-Custard Prey abundance and the strength of interference in a foraging shorebird. Journal of Animal Ecology 68: Tsipoura, N., and J. Burger Shorebird diet during spring migration stopover on Delaware Bay. Condor 101: Vahl, W.K., van der Meer, J., Weissing, F.J., van Dulleman, D and T. Piersma The mechanisms of interference competition: two experiments on foraging waders. Behavioral Ecology 16: Warner, S The Slow Struggle to Bring Back the Oyster. The New York Times12 June 2005; section New York Region / New York/Region Special. Available online at Accessed March 26, Yates, M.G., R.A. Stillman and J.D. Goss-Custard Contrasting interference functions and foraging dispersion in two species of shorebird (Charadrii). Journal of Animal Ecology 69:

20 APPENDIX 1 U.S. Fish and Wildlife Service Guidelines for Red Knot Conservation Measures in Delaware Bay Related to Near-Shore Intertidal Oyster Aquaculture 20