578 J.J. McDermott 22001133 NORTNHorEthAeSaTsEteRrNn NNaAtTuUraRliAstLIST 2V0(o4l). :2507,8 N–5o8. 64 The Distribution of Ocypode quadrata, Atlantic Ghost Crab (Decapoda: Brachyura: Ocypodidae) Megalopae, beyond the Presumptive Northern Boundary of Adult Populations in the Northwest Atlantic John J. McDermott* Abstract - Previous observations on the occurrence of the megalopae of Ocypode quadrata (Atlantic Ghost Crab) along the inshore waters of the northeastern coast of the US from New Jersey to southern Massachusetts and the offshore waters of southwestern Nova Scotia, dating back to the end of the 19th century to recent findings in the 21st century, are reviewed. Although megalopae were found for the first time north of Cape Cod in plankton samples from Nova Scotia (1977–1978), they are reported here for the first time on beaches north of Cape Cod along the east coast of Massachusetts and as far north as Kennebunkport, ME. The nearest populations of adult Atlantic Ghost Crabs are located along the southeast coast of Massachusetts. Thus, zoeae larvae and megalopae originating below Cape Cod must migrate northward around the Cape or via Buzzards Bay through the Cape Cod Canal. Likewise, megalopae reported from southwestern Nova Scotian waters must have originated from adult populations to the south. The incidence of megalopae from New Jersey northward along the coast suggests a recruitment period from late summer into early fall for Atlantic Ghost Crabs on the northern edge of their range. Introduction Ocypode quadrata (Fabricius) (Atlantic Ghost Crab) inhabits burrows on sandy beaches from Block Island, RI to Santa Catarina, Brazil, and the species has also been reported from the islands of Bermuda and the Fernando de Noronha archipelago, Brazil (Williams 1984). Atlantic Ghost Crabs populate beaches of the islands of Martha’s Vineyard, Nantucket, Muskeget, and Tuckermuck off the southeast coast of Massachusetts, and Monomoy and Chatham at the elbow of Cape Cod (L. Johnson, Biodiversity Works, Edgartown, MA and T. Simmons, Natural Heritage and Endangered Species Program, West Boylston, MA, pers. comm.). Simmons first recorded crabs at some of the above-mentioned locations beginning in 1985, but had not found them north of Cape Cod (i.e., Cape Cod Bay; Fig. 1). Based on the known distribution of Atlantic Ghost Crab populations in 1870, Verrill (1873) suggested that these crabs “… may be looked for on the beaches of Nantucket and Martha’s Vineyard.” All members of this semi-terrestrial genus inhabit sandy beaches worldwide (Ng et al. 2008). Knowledge of the biology of Atlantic Ghost Crab is mainly based on populations from more southern latitudes. Both the size of Atlantic Ghost Crab populations and mean carapace width (CW) are greater south of Delaware Bay than north of it (J.J. McDermott, unpubl. data). Crabs venture into the surf zone to feed and release their *Department of Biology, Franklin and Marshall College, Lancaster, PA 17604-3003; john. mcdermott@fandm.edu. Northeastern Naturalist Vol. 20, No. 4 J.J. McDermott 2013 579 first zoeae during the reproductive period. They scavenge beach wrack; feed on a great diversity of aquatic sympatric invertebrates (e.g., mollusks and crustaceans) (Wolcott 1978); consume vertebrates, such as shore bird and turtle hatchlings (Knott 2005, Williams 1984); and they deposit-feed at times (Robertson and Pfeiffer 1982). In New Jersey, crabs probably become ovigerous in late spring or early summer, and some females still carry broods in July (Milne and Milne 1946). Farther south, in North Carolina, Atlantic Ghost Crabs are ovigerous from approximately April to July (Williams 1984), while those along the Texas coast have an extended reproductive period with two broods, the second of which produces first crab stages in late October (Haley 1972). Embryos of Atlantic Ghost Crabs are hatched as first zoeae in the shallow surf of sandy beaches, molt through four more planktonic zoeal stages, and finally metamorphose into megalopae that return to suitable beaches where they metamorphose into the first crab stage (Diaz and Costlow 1972). Measurements of Atlantic Ghost Crabs collected during surf-zone research in New Jersey in the late 1970s and early 1980s, showed that the largest male and female crabs were 43.3 mm and 44.2 mm CW, respectively (J. McDermott, unpubl. data). Milne and Milne (1946) recorded a 48-mm specimen near Townsends Inlet, just north of Cape May, NJ (sex of crab and number measured were not given). Atlantic Ghost Crab numbers are small in northeastern New Jersey (e.g., Sandy Hook at the entrance to New York harbor), but populations become larger from Atlantic City south to Cape May (Grant 1983, Milne and Milne 1946). T. Simmons (pers. observ. and unpubl. data) also found that crabs inhabiting the islands of southeastern Massachusetts are smaller than those he has seen from New Jersey and North Carolina. Most were less than 30 mm CW, but some reached 41 mm CW. On Delaware shores, Morris (1957) noted that adults were >45 mm CW (no other data given). Atlantic Ghost Crabs farther south and into the Gulf of Mexico reach a maximum CW of >50 mm: e.g., 50 mm in South Carolina (Ruppert and Fox 1988); and male and female crabs from the Texas coast reach 53.5 mm and 52.0 mm CW, respectively (Haley 1969). I recently reviewed the literature regarding Atlantic Ghost Crab megalopae and reported our current knowledge of their occurrence and distribution in the western Atlantic, their distinctive morphology and large size, and comparisons with those of other species within the genus (McDermott 2009). At the time I was unaware of a survey of brachyuran larvae and megalopae conducted in the offshore waters of southwestern Nova Scotia in the summers of 1977 and 1978, during which Atlantic Ghost Crab megalopae were found (Roff et al. 1984). The authors of the study collected larvae of 35 crab species from 3055 plankton samples, accounting for 48 of >600,000 specimens. While many aspects of Atlantic Ghost Crab biology and ecology, as well as of the Ocypodidae in general are known (Knott 2005, Williams 1984), relatively little information exists on larval distribution and the occurrence and behavior of megalopae, the most important stage in the species’ recruitment to sandy beaches. The purpose of this paper is to present recent information on the occurrence of Atlantic Ghost Crab megalopae found north of New Jersey and particularly north 580 J.J. McDermott 2013 Northeastern Naturalist Vol. 20, No. 4 of Cape Cod. I also discuss factors that might be involved in a possible range expansion of this species. Methods This study involves a review of previous published data on the occurrence of Atlantic Ghost Crab megalopae on sandy beaches from New Jersey to Long Island Sound (McDermott 2009; Smith 1873a, 1873b, 1880; Williams 1984). Data on Atlantic Ghost Crab megalopae obtained in a survey of brachyuran plankton from waters off Nova Scotia (Roff et al. 1984) are involved in this review. Finally, I present recent unpublished data regarding the occurrence of Atlantic Ghost Crab megalopae from coastal beaches north of Cape Cod, in Massachusetts and Maine. I examined specimens and/or photographs from these sources, confirmed identifications, and obtained measurements for comparisons with megalopae from New Jersey. Carapace width and carapace length (CL) were measured in millimeters with an ocular micrometer, and I used these values to calculate the ratio CW/CL. Results Atlantic Ghost Crab megalopae have been recorded in very small numbers along sandy beaches from New Jersey northward to the southern coast of Massachusetts (Vineyard Sound) (Table 1, Fig. 1). Populations of adult Atlantic Ghost Crabs inhabit these waters. In the colder waters north of Cape Cod, where adult populations have not been documented, megalopae of these crabs have been collected on beaches as far north as Maine during the last few years of this century (Table 1). Table 1. Seasonal sightings of Ocypode quadrata megalopae from New Jersey to Maine from the 1870s to 2012. Each date refers to the collection of one specimen except where more than one is indicated. Location Date Reference New Jersey (Cape May County 6 Sep 1980 McDermott (2009) at two locations) 19 Sep 1981 13 Sep 1985 7 Sep 1999 6 Oct 2000 New York (Long Island, south late Aug 1870 Smith (1873a, b) shore)* Rhode Island (Block Island)* Aug 1870 Smith (1873a, b) Massachusetts (Vineyard Sound)* Sep 1875 (early) Smith (1880) Massachusetts (Gloucester) 26 Aug 2012 O’Connor (pers. comm.) Massachusetts (Plum Island)** 21 Sep 2012 Hutchings (pers. comm.) Maine (Kennebunkport) 31 Aug 2010 Kraeuter (pers. comm.) Maine (Kennebunk) 31 Aug 2012 Miller (pers. comm..) *= Supposedly numerous, but no exact number given. **= 2 specimens. Northeastern Naturalist Vol. 20, No. 4 J.J. McDermott 2013 581 Two megalopae were collected at Sandy Point State Reservation, Plum Island, MA (information and photos provided by Lisa Hutchings, Education Coordinator, Joppa Flats Education Center, Newburyport, MA, pers. comm.). One measured 5.05 mm CW, 6.25 mm CL, CW/CL = 0.81, and although the carapace of the other crab was damaged, photos and microscopic examination revealed that it was close to the same size. A single megalopa was collected by William O’Connor (Gloucester, MA, unpub. data) from Wanson Cove, Gloucester, MA. Unfortunately the specimen was discarded, but I identified it as an Atlantic Ghost Crab megalopa from its photograph. Figure 1. Map showing locations (black circles) where megalopae of Ocypode quadrata were collected from the 19th to 21st centuries along the northeast coast of the United States from New Jersey to Maine. Populations of adult crabs are found only south of Cape Cod. The sites are labeled as follows: CM = Cape May region (two locations, Delaware Bay west and barrier beaches east on the peninsula); LI = Long Island south shore; BI = Block Island; VS = Vineyard Sound; G = Gloucester; PI = Plum Island; K = Kennebunk – Kennebunkport area (two nearby locations). DE = Delaware, RI = Rhode Island. 582 J.J. McDermott 2013 Northeastern Naturalist Vol. 20, No. 4 One megalopa was collected 31August 2010 by John N. Kraeuter (Haskin Shellfish Research Laboratory, Rutgers University, Port Norris, NJ, pers. comm.) in sand near the high tide line at Goose Rocks Beach, Kennebunkport, ME (5.85 mm CW, 6.68 mm CL, CW/CL = 0.88). From photographs, I identified a megalopa collected 31 August 2012 at Parsons Beach, Kennebunk, ME ≈10.4 km south of Goose Rocks Beach, as Atlantic Ghost Crab (J. Miller, Wells National Estuarine Research Reserve, Wells, ME, pers. comm.). The crab was released before I could make measurements. Thus, the megalopae of Atlantic Ghost Crabs have been reported ≈190 km beyond any adult populations (distance measured from the eastern end of the Cape Cod Canal, MA to Kennebunkport, ME (Fig. 1). Discussion Twelve Atlantic Ghost Crab megalopae have been collected from nine locations on twelve dates from New Jersey to Maine (Table 1). These dates ranged from late summer to early fall (26 August 2012, in Gloucester, MA to 6 October 2000 at Stone Harbor, NJ). The other ten collections, dating back to the 1870s (Smith 1873a, 1873b, 1880) were in August and September. These data on megalopae, while very few, suggest a late summer to early fall recruitment period for Atlantic Ghost Crab in its northernmost range, i.e., New Jersey to Maine. My two decades of observations of southern New Jersey’s sandy beach surf-zone invertebrate fauna support this suggestion (McDermott 1983, 1987, 2001, 2005). Adult Atlantic Ghost Crab populations along the southeast coast of New England and the islands of Martha’s Vineyard and Nantucket are smaller than those of southern Long Island and New Jersey, and the latter two populations are considerably smaller than those on the barrier beaches of the Carolinas (L. Johnson and T. Simmons , pers. comm.; J. McDermott, pers. observ.). Cape Cod is recognized as a major barrier to the northern migration of southern fauna, and the colder water of Cape Cod Bay is thought to prevent northward movement by some crab species (Smith 1873a, b; Verrill 1873). The Western Gulf of Maine Coastal Current flows from the northeast into the Bay before branching and apparently continuing southward offshore of Cape Cod. These topographical and thermal barriers obviously do not completely impede the migration of Atlantic Ghost Crab zoeae and megalopae from moving north. Those zoeae and megalopae that traverse the outer Cape or are carried from Buzzards Bay through the Cape Cod Canal at the shoulder of Cape Cod might survive long enough to burrow into a sandy beach, and if competent and tolerant to the colder water, may even molt into the first crab stage. Warm core eddies off the Gulf Stream may be instrumental in transporting southern fauna beyond Cape Cod (Lalli and Parsons 1991). At this point in geological time, however, colder water north of Cape Cod is not conducive to the establishment of adult populations of Atlantic Ghost Crab. In recent years, these barriers did not inhibit the establishment of populations of the introduced Hemigrapsus sanguineus (De Haan) (Asian Shore Crab). First recorded in New Jersey in 1988, it reached the waters of Maine by 2002 (McDermott 1991, 1998; Stephensen et al. 2009; Williams and McDermott 1990). This colonization was Northeastern Naturalist Vol. 20, No. 4 J.J. McDermott 2013 583 predicted from its tolerance to a wide range of water temperatures, as documented in the in the northwest Pacific (McDermott 1998). Records for the occurrence of Atlantic Ghost Crab megalopae on Atlantic coastal beaches of the US are extremely rare, and when megalopae are encountered they are usually not numerous. Megalopae of the sympatric Indian species of ghost crab, Ocypode platytarsis H. Milne Edwards and O. cordimanus Latrielle, occurred in greater numbers on beaches than Atlantic Ghost Crab so that they were sufficient for laboratory experimentation (Raja Bai Naidu 1954). The additional carapace measurements and CW/CL ratios presented here from Atlantic Ghost Crab megalopae collected north of Cape Cod correspond positively with those recorded previously south of the Cape (McDermott 2009). Why were Atlantic Ghost Crab megalopae not reported from the surf zone north of Cape Cod prior to the 21st century? Some might view these recent occurrences as related to the much-discussed warming trend in the oceans. However, because planktonic Atlantic Ghost Crab, and other southern brachyuran larvae were collected in the oceanic waters off southern Nova Scotia (Roff et al. 1984), it is likely that southern currents and eddies have been bringing larvae and megalopae into the cold northern waters for centuries. It has been shown here that some of these megalopae have survived their oceanic journeys and reached sandy beaches along the coastal United States north of Cape Cod. The occurrence of the Atlantic Ghost Crab megalopae on sandy beaches continues to be enigmatic, as I indicated in my scattered observations along the New Jersey coast (McDermott 2009). In order to understand the role of Atlantic Ghost Crab megalopae in recruitment, a concerted effort is needed to explore sandy beaches more intensively and sample quantitatively for megalopae and the first few crab instars, especially during the suggested late summer and early fall recruitment period in northern waters. Studies of ghost crab populations have not emphasized this period in the recruitment of ghost crabs to sandy beaches. Plankton should be sampled for the zoeal stages in the life cycle as well as megalopae (Diaz and Costlow 1972, Roff et al. 1984) in conjunction with exploration for burrowed megalopae in the intertidal zone. Tide stage may be a factor in avoiding predation in that the incoming tide period would land the emerging megalopae nearer the upper beach in preparation for metamorphosis. To my knowledge, all recoveries of megalopae have been in daylight with meager results. Perhaps megalopae tend to invade beaches in greater numbers in the dark, which would be a potential adaptation for avoiding visual predators. Lunar phases could be influencing beach invasions. Addition of information to what little is known of megalopal behavior and strategy at the time megalopae land and explore a sandy beach may provide insight into the factors that influence the success or failure of recruitment (McDermott 2009, Raja Bai Naidu 1994). In addition, results from laboratory studies focused on megalopal behavioral reactions and tolerances to temperature fluctuations should relate to their overall survival in the northern part of their range. Obviously ghost crab megalopae are continually replenishing the sandy beaches of the western Atlantic. John Cushing (Vienna, VA, pers. comm., 2012) reported 584 J.J. McDermott 2013 Northeastern Naturalist Vol. 20, No. 4 finding megalopae, “blueberry crabs”, in August for the last 5 years on the beaches of Duck, NC. He noted that when megalopae “tuck in their legs and tail they look like a little blueberry or a small blue pebble.” Crane (1940) described and illustrated from preserved specimens how the megalopa becomes semispherical and compact as its legs are folded into lateral grooves on the carapace and the abdomen is flattened against the sternum (see McDermott 2009). Cushing observed that megalopae “are hard to find” with only a few of them collected each summer. It is not obvious, therefore, how and when to collect “blueberry crabs” in abundance for experimental study. Acknowledgments I appreciate information on the presence of Atlantic Ghost Crab populations on islands off the southeast coast of MA, provided by Luanne Johnson, Director, Biodiversity Works, Edgartown, MA, and Tim Simmons, Restoration Ecologist, Natural Heritage and Endangered Species Program, West Boylston, MA. David M. Knott, Poseidon Taxonomic Services, Charleston, SC, has been helpful in directing me to recently documented northern populations of crabs. I thank Lisa Hutchings, Education Coordinator, Joppa Flats Education Center, Newburyport, MA, for notifying me and providing photographs and specimens of ghost crab megalopae found on Plum Island, MA. I appreciate the information provided to me by William O’Connor on a megalopa from Gloucester, MA. I am grateful to John N. Kraeuter, Haskin Shellfish Research Laboratory, Rutgers University, Port Norris, NJ, for providing me with a megalopa collected at Kennebunkport, ME, and also for reviewing an earlier draft of this paper. 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