Diamondback terrapins in Maryland: Research and conservation

Beate Pfau & Willem M. Roosenburg Beate Pfau and Willem M. Roosenburg Diamondback terrapins in Maryland: Research and conservation Introduction Diamondback terrapins (Malaclemys terrapin) appeal to humans because of their dark eyes, wide smiling lips and attractive, often contrasting black and light grey skin pattern. Their vernacular name derives from the sculptured carapace, which often resembles cut diamonds (Fig. 2). The coloration is quite variable, even within a local population. Figs. 3 and 4 illustrate two color pattern variants of the Northern Diamondback terrapin (M. t. terrapin). Diamondback terrapins owners easily recognize individuals because of the unique color patterns. These color patterns remain distinct in adults. However, as the turtles grow the pattern and coloration changes and thus cannot be used to recognize individuals in population studies. Therefore, terrapin researchers mark individuals by other means, e.g. passive integrative transponders (PIT tags) and/or notching certain marginal scutes (Cagle, 1939; see below). Male and female terrapins differ in their maximum size. Males are smaller and can attain a maximum carapace length of 16 cm, females get much larger and may attain a maximum carapace length of 26 cm. At 10 cm carapace length and larger, external characters distinguish males from females. Males have longer and thicker tails (Fig. 5). Older females are much larger and have enlarged heads with strong jaws adapted for crushing their hard-shelled prey (see below). Because diamondback terrapins are cute and do not get too large, they are popular among pet keepers. Unfortunately, they are very sensitive to inferior housing, particularly to poor water quality, and therefore they are recommended as pets for only skilled keepers. Sachsse was one of the first Europeans who was able to breed diamondback terrapins regularly (Sachsse 1984), and Szymanski (2005) published a detailed report on keeping and breeding terrapins. During the 19 th and early 20 th century, Diamondback terrapins were in high demand in the United States as a gourmet food. By 1900, there were experimental breeding farms to evaluate the potential to supply food market with diamondback terrapins (Coker 1906, Barney 1922). However, the labour intensive nature of raising terrapins led to a collapse of the early terrapin farming. Currently, several diamondback terrapin breeders in the US provide hatchlings for the pet market. Hobbyists have bought some of the most attractively patterned terrapins from the commercial markets and established breeding pairs in their homes presumably already in the early years of the 20 th century. Demand from terrapin flesh from China has prompted at least one renewed attempt at terrapin farming in Maryland. This farmer still produces turtles and exports them to Asian food and pet markets (Pelton 2006). The farmer dug several ponds (1+ hectare) in a corn field and stocked them with approximately 2,200 diamondback terrapins (among other species). He collects their eggs after the female nests and artificially incubates thousands of hatchlings that are exported to China. The colourful ones are RADIATA 19 (1), 2010

Diamondback terrapins in Maryland sold in the pet trade where individual terrapins can bring as much as $150 apiece and other are sent to turtle farms where they are reared for breeding stock and food. It is difficult to imagine that this business can be profitable and self-sustaining because of the water quality requirements of terrapins. Hopefully, regulatory authorities will maintain keen oversight to ensure a healthy environment for the terrapins. Terrapins are specialized brackish water turtles and are frequently mentioned in scientific and popular articles on US estuarine habitats. Despite their fame, popularity, and charismatic nature; there is much that remains to be learned about this salt marsh denison. Threatened by over-exploitation, nutrient loading, pollution and habitat loss, the diamondback terrapins have become a symbol for the conservation efforts for estuaries within the USA. Education programs use the active and friendly terrapin as a focal species in conservation and education programs to effectively promote environmental awareness and stewardship. The key to understanding terrapin conservation and management, as with almost all turtles, lies in long-term, mark-recapture data sets. One of us, Willem Roosenburg conducts such long term research on Maryland s diamondbacks and his findings contribute to sound terrapin conservation. Beate Pfau followed Willem during the summer of 2007 while in Maryland to learn of his work and discuss the fundamentals of terrapin biology with Willem and some of his colleagues. Herein, we describe what we learned and experienced during that time. Natural history of Diamondback terrapins Diamondback terrapins live in estuarine, brackish water habitats. The salinity they experience may vary considerably with Fig. 1. Will Williams and Melanine Heckman measuring a head-started terrapin. Photo: B. Pfau. RADIATA 19 (1), 2010

Beate Pfau & Willem M. Roosenburg Fig. 2. Carapace view of a Northern Diamondback terrapin. Photo: B. Pfau. RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 3. Malaclemys terrapin terrapin female with a skin pattern of small spots. Photo: B. Pfau. Fig. 4. Malaclemys terrapin terrapin female with a skin pattern of bold stripes and dots. Photo: B. Pfau. Fig. 5. Male (left) and female (right) terrapins show the difference in tail shape. Photo: B. Pfau. RADIATA 19 (1), 2010

Beate Pfau & Willem M. Roosenburg fluctuations in rainfall and the stage of the tide. Terrapins are adapted to these fluctuations and can tolerate a certain range of ion concentrations in their body fluids, but the composition of their intracellular fluids remains fairly constant (Robinson & Dunson 1976). If the salinity of the water is high for several days, then terrapins may try to access fresh water. They will wander onto land and drink water from puddles or even from a thin water film on the soil. In rainy weather, they can obtain water that runs off their carapace (Davenport & Macedo 1990). Terrapins do have lachrymal glands which lie behind the eye, but these glands are not effective in regulating the osmotic pressure of their body fluids (Cowan 1990). Unfortunately, most estuaries along the east and Gulf coast of the United States are major agricultural, industrial, and urban areas and thus suffer from a variety of anthropogenic disturbance including pollution, habitat destruction, and interaction with fishing gear. Naturally, diamondback terrapins, like other estuarine organisms, are affected by the pollution. Heavy metals, including mercury, accumulate in the tissues of turtles (see for example Burger 2002). Blainvillain et al. (2007) suggested that diamondback terrapins can be used to monitor pollution, because they bioaccumulate toxic substances which they obtain via the food chain. Organic contaminants also harm terrapins. Diamondback terrapins exposed to PCB show higher stress hormone levels, slower growth and reduced bone density than controls (Ford 2005). Oil spills in coastal areas affect diamondback terrapins directly by oiling and drowning the animals and indirectly by contaminating their nesting beaches. The short-term impacts of the oil spill from a leak in an underground oil pipeline near Chalk Point, Maryland, are rather well documented (NOAA 2000). Research showed that not only the terrapins themselves, but also hatchlings from nests in polluted sand were severely affected (Roosenburg et al. 2001). Regrettably, and as usual, there has been no long-term Fig. 6. Female Malaclemys terrapin. Photo: B. Pfau. RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 7. Female Malaclemys terrapin. Photo: B. Pfau. survey of the impacts of this oil pollution on the Diamondback terrapins and other organisms. Terrapins are predominantly molluscivores feeding mostly on snails, barnacles, and clams. Adults also will eat crustaceans and fishes when they can catch them. Juveniles prey on soft-bodied animals including small crustaceans and insects, for example amphipods (Amphipoda) or green crabs (Carcinus maenas; King 2007). Larger female terrapins are specialized; they mainly feed on hardshelled prey because of their ability to crush the shells of many gastropods and bivalves. Diet varies depending on the availability of prey, in areas where snails are uncommon terrapins feed mostly on soft-shelled clams (Mya arenaria) and mussels (Mytilus sp.), but where snails are abundant they are included in the diet. In the southern parts of the range they prey on the Marsh periwinkle (Littorina irrorata; see Tucker & FitzSimmons 1992, Tucker et al. 1995). This snail feeds on bacteria that grow on ecologically important cordgrass (Spartina alterniflora) and heavy grazing by the snails damages the stems. Spartina plays an important role in shoreline stabilization and its loss increases erosion rates. Conservationists appreciate the ecologically important role of the terrapins as periwinkle predators. The terrapins walk or swim between the cordgrass and pluck the snails, and crush their shells with and audible popping noise (see for example Conant & Newman 1993). Similar to females of some Graptemys species, the sister genus of Malaclemys, female terrapins have enlarged heads and broad crushing surfaces of their jaws adapted to their hard-shelled prey (Lamb & Osentoski 1997). Fully grown male terrapins do not show head enlargement, and they are not able to crush molluscs with heavier shells (Tucker et al. 1995). RADIATA 19 (1), 2010

G St La Beate Pfau & Willem M. Roosenburg Boston Chicago New York WASHINGTON St Louis Memphis Atlanta Dallas Austin Houston Columbia New Orleans Gulf of Mexico Miami Fig. 8. Distribution map of the subspecies of Malaclemys terrapin (after Ernst et al. 1994). Diamondback terrapins also eat crustaceans, particularly fiddler crabs (Uca pugnax and other Uca species), marsh crabs (Sesarma reticulatum) and blue crabs (Callinectes sapidus; Tucker et al. 1995). Because larger crabs have hard chitin exoskeletons, Mid will eat only the crab s terrapins sometimes dlelower nutritional value. legs, despite their A To crop a crab leg, themterrapin attacks the er crab from behind and takesicathe leg farthest T from the pinching chelipeds, reand tries to n trick the crab into dropping it (Dcavenport et al. 1992). Terrapins also prefer blue crabs when their shells are soft after molting. Age and size at maturity throughout the terrapins range varies considerably. In general, both age and size at maturity correlates positively with latitude. In Chesapeake Bay male terrapins mature at 4-5 years of age, 10 cm straight plastron length (SPL) and a weight of 300 g. Females start laying eggs at about 8 years of age and a SPL of 16.5 cm, and a weight of at least 1,100 g (R oosenburg 1996). There is considerable variation in the reproductive output of terrapins throughout CARIBBEAN SEA their range. In general, females mature later and at a larger body size, produce larger clutches of smaller eggs, and have a shorter nesting season as one goes north. Panama The Canal variation is considerable when one compares populations in Florida to those in Massachusetts (R oo senburg 1994). Fundamental data on terrapin reproduction in Maryland has been gathered from both the Patuxent River and the Poplar Island research project (see below). Like most other chelonians, Diamondbacks exhibit temperature dependent sex determination (TSD; Jeyasuria et al., 1994). When incubated at constant conditions, the temperature during the middle third of incu- RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 9. Diamondback terrapin nesting beach. Photo: B. Pfau. Fig. 10. Former Diamondback terrapin nesting beach, now with houses and gardens. Photo: B. Pfau. RADIATA 19 (1), 2010

Beate Pfau & Willem M. Roosenburg Fig. 11. Female Malaclemys terrapin. Photo: B. Pfau. Fig. 12. Female Malaclemys terrapin, portrait. Photo: C. Pfau. Fig. 13. Female Malaclemys terrapin. Photo: B. Pfau. 10 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland bation determines sex. Warm temperatures produce females, cool temperatures produce males and 29.1 C produces a mixed sex ratio (Jeyasuria et al., 1994). The threshold range that results in mixed sex ratios is only about 3 C wide. Female terrapins will place larger eggs in warmer environments more likely to produce females and smaller eggs in cooler sites. Coupled with the sexual dimorphism in terrapins the behaviour is potentially adaptive because female offspring from larger eggs grow faster and mature earlier than those from small eggs whereas males do not realize a difference in growth or age at maturity attributable to egg size (Roosenburg & Kelley 1996). Therefore it is advantageous (adaptive) for females to lay larger eggs in warmer sites (Roosenburg 1996). Furthermore, these finding suggest that a variety of beach habitats are needed to maintain a functional male-to-female ratio in a given population. For example, if only south facing, warmer beaches that are female biased, are protected, then sex ratio skew may occur (Roosenburg & Place 1995). The minimum incubation time in the laboratory is 40 days (Roosenburg & Kelley 1996). In the wild incubation times range from 50 days, to well over 200 days as some hatchlings, mainly from late nests, are able to overwinter in the nest. Overwintering nests hatch in the fall and hatchlings remain in the natal nest until the following spring when they emerge. There they can experience subzero temperatures in the nests but they have the ability to survive the sub-zero temperatures (Costanzo et al. 2006). However, severe cold and prolonged freezing will increase the mortality of overwintering hatchlings. Diamondback terrapins are vulnerable to a variety of predators throughout their life cycle. Nests are depredated by several species of mammals including racoons, foxes, skunks, and otters that eat the eggs. Avian predator (sea gulls, crows, and willets (Catoptrophorus semipalmatus, Roosenburg personal observation) also prey on terrapin nests. Additionally, king snakes (Lampropeltis getulus, Roosenburg personal observation) eat terrapin eggs. On several beaches crows have learned to watch nesting females and eat their eggs, sometime while the female is still laying. Even plant roots can be dangerous to terrapin eggs and embryos. They are attracted to the moisture and nutrients and surround the eggs tightly and absorb all the moisture from the egg and in some cases the roots entrap a hatchling and prevent it from emerging (Roosenburg 1992, Giambanco 2003, Butler et al. 2004). Abiotic factors, including flooding during storms and prolonged drought, may also lead to nest failures. Hatchlings are also vulnerable to predation. Some nests are attacked by ants and after leaving the nest hatchlings are eaten by many predators, including gulls, herons, cormorants, crows, raccoons, foxes, otters and rats. Reaching the water, they face more predators such as large fish and crabs (which they in turn like to eat when grown up). To avoid predation the smaller terrapins live in marshes near the shoreline hidden in shallow water with plenty of cover and vegetation (see Roosenburg et al. 1999). Adult diamondbacks have fewer natural enemies. Unfortunately, some racoons have learned to wait for females coming ashore to nest. They kill them by severing the head and then disemboweling them through the inguinal opening of the shell to get to the eggs. Terrapins shells also can be found near the nests of the USA s national emblem; the bald eagle (Haliaeetus leucocephalus) will eat males and half grown female terrapins (Clark 1982), but it is unknown if these terrapins are killed or scavenged. RADIATA 19 (1), 2010 11

Beate Pfau & Willem M. Roosenburg Diamondback terrapin subspecies and distribution Diamondback terrapins, Malaclemys terrapin (Schoepff 1793), occur along the Atlantic and Gulf coasts from the New England states to southern Texas. Traditionally they have been divided into seven subspecies throughout their range (Carr 1952, Ernst et al. 2000, Fig. 8). However, recent molecular studies suggest the distinction between the subspecies is not clear (see for example Chan et al. 2006). The traditional subspecies based on morphological characteristics include the following. Malaclemys terrapin terrapin (Schoepff 1793), Northern Diamondback terrapin, ranges along the Atlantic coast from Cape Cod to Cape Hatteras. Its medial keel does not bear terminal knobs on each scute, and the sides of the carapace diverge posteriorly. Malaclemys terrapin centrata (Latreille 1802), Carolina Diamondback terrapin, ranges from Cape Hatteras south along the coast to northern Florida. Its medial keel bears no terminal knobs on each scute, the sides of the carapace are nearly parallel, and the marginals curl upwards. Malaclemys terrapin tequesta (Schwartz 1955), the Florida East Coast terrapin occurs along the Atlantic coast of Florida. Its medial keel bears posteriorly facing tubercles or knobs. The carapace is dark or tan with no pattern of concentric light circles. M a l a c l e m y s terrapin rhizophorarum (Fowler 1906), the Mangrove terrapin is restricted to the Florida Keys. Its medial keel bears bulbous terminal knobs and its shell is strongly oblong. The ventral seam of the marginal and plastral scutes are often outlined with black. Spots on the neck frequently fuse to form a streaked pattern, and the hind legs may be striped. Malaclemys terrapin macrospilota (Hay 1904) the Ornate Diamondback terrapin ranges along the Gulf coast from Tampa Bay to the panhandle. Its medial keel has terminal, often bulbous, knobs and the carapacial scutes show orange or yellow centers. Malaclemys terrapin pileata (Wied-Neuwied 1865), the Mississippi Diamondback terrapin ranges along the Gulf coast from the Florida Panhandle to western Louisiana. Its medial keel has terminal tuberculate knobs. The scutes of the oval carapace lack light centres. The upturned edges of the marginals are orange or yellow, and the plastron is yellow and often dusky. Top of the head, upper lip, neck, and limbs are black or dark brown. Malaclemys terrapin littoralis (Hay 1904), the Texas Diamondback terrapin occurs along the Gulf coast from western Louisiana to Texas and has a medial keel with terminal knobs on its deep carapace. Its carapacial shields lack distinct light centres, the plastron is pale or white, the upper lip and top of head are whitish, and the neck and legs are greenish gray with heavy black spotting. Fig. 14. A large Horseshoe crab (Limulus polyphemus). Photo: C. Pfau. 12 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 15. Old barn near the Patuxent river. The laboratory for Diamondback terrapin research is in the ground floor. Photo: B. Pfau. Fig. 16. Fyke net. The back end of it is always above the water level. Photo: C. Pfau. Fig. 17. Blue crab (Callinectes sapidus). Photo: B. Pfau. RADIATA 19 (1), 2010 13

Beate Pfau & Willem M. Roosenburg Fig. 18. This Snapping turtle (Chelydra serpentina) was immediately released. Photo: C. Pfau. 14 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland A comprehensive, well illustrated synopsis of the Florida subspecies of Malaclemys terrapin is given by Butler et al. (2006). Diamondbacks terrapins also occur in Bermuda (Davenport et al. 2005). Parham et al. (2008) tested the origin of these terrapins using a combination of paleontological and genetic data. They conclude that the terrapins are recent natural colonizers, between 3,000 and 400 years ago. The subspecies of the Bermuda terrapins is not given but they suggest that it is either M. t. terrapin or M. t. centrata. Terrapins were introduced in California in 1886 and again in 1943 but these populations disappeared shortly after introduction (Brown 1971). Diamondback terrapins of unknown origin cannot be reliably identified to subspecies as based on their external characteristics. However, genetic analysis can identify populations and have been used to identify the source of terrapins from the markets in New York City (Lester 2007). Because terrapins have been traded since the 1800 s and there are know escapes and releases throughout their range, it is possible that many populations contain subspecific hybrids. Threats to Diamondback terrapins Numerous authors have described threats to terrapin populations throughout their range (Florida, Butler et al. 2006; Maryland, Roosenburg 1991; New Jersey, Wood & Herlands 1997; and range wide, Seigel & Gibbons 1995). These threats include commercial harvesting, bycatch mortality in commercial crab pots, loss of nesting habitat, impacts by cars and motor boats, pollution, and the increase in predation of nests by growing raccoon populations. Crab pots Perhaps the biggest threat to terrapins throughout their range is the interaction with the commercial blue crab (Callinectes sapidus) fishery. The most popular mechanism to catch crabs in most states is the crab pot. Crab pots function similar to turtle traps, however because they fish submerged, entrapped turtles most often drown. Other mechanisms to catch crabs include bank traps, trot lines, and crab traps. However, if fished properly these techniques do not lead to terrapin mortality in a similar manner to crab pots. Because crab pots are the primary commercial way to harvest crabs, trapping effort can be concentrated and occur in shallow waters where terrapins occur. Furthermore, pots are baited with fish which attract terrapins, and at times clams are sued a bait which are a preferred food of terrapins. Roosenburg et al. (1997) examined the impact of crab pots in the Chesapeake Bay. They estimated that 15-78% of the local terrapin populations can be captured in crab pots in a single year. Because the entrance of the pots is too small for mature females, most of the victims are males and similarly sized females. Very small terrapins can escape the pots through the wire mesh. Because of the selective mortality of males in crab pots, the terrapin sex ratio in Chesapeake bay is 1:2 to 1:3 (m:f). Thus, crab pots have an effect on the population structure and long-term impacts on the population dynamics. Roosenburg et al. (1997) designed a new, larger, crab pot that maintained permanent access to air and prevented the drowning of terrapins. They compared the catch rates of the new pots to the traditional size and actually caught more crabs in their new design. Nevertheless the higher costs and cumbersome size of the modified pots prevented their commercial success. RADIATA 19 (1), 2010 15

Beate Pfau & Willem M. Roosenburg The next device to be tested was the bycatch reduction device (BRD) that prevents terrapins from entering the pots (Wood & Herlands, 1997). Several authors have tested BRDs of various sizes and in a variety of states (reviewed in Roosenburg 2004). All studies have been able to pinpoint the dimensions of a BRD that greatly reduces terrapin catch without reducing crab catch, e.g. Roosenburg & Green (2000), Butler & Heinrich (2007) and Cole & Helser (2001). In Maryland, the most effective bycatch reduction devices are rectangular frames of wire or plastic material with openings of 4.5 cm by 12.0 cm, which are fitted horizontally into the pot entrance. The devices reduced the terrapin bycatch by 82% and did not affect the crab numbers or size of the commercially valuable crabs (see for example Roosenburg & Green 2000, Radzio & Roosenburg 2005, Butler & Heinrich 2007). Habitat loss Female terrapins prefer sandy substrates for nesting (Fig. 9). Coastal populations prefer to nest on sand dunes (Burger & Montevecchi 1975) while females from inland populations, where dunes are absent, nest on beaches and sandy fringes of the estuary. These nests are usually less than 10 m from the mean high tide mark and in some cases can be inundated by wind driven, higher than normal tides. Unfortunately, waterfront property is in high demand throughout out much of the terrapin s range. Landowners resort to bulk heading and the use of riprap to prevent loss of their property. These structures form barriers that prevent terrapins from reaching their preferred nesting areas and results in the loss of nesting habitat (Roosenburg 1991, Roosenburg & Place 1995). Furthermore, Fig. 20. Measuring carapace length. Photo: B. Pfau. Fig. 19. Palpating a female Diamondback terrapin for eggs. Photo: C. Pfau. Fig. 21. Measuring the length of the suture of the third plastron shield on the richt side of the terrapin. Photo: B. Pfau. 16 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 22. Female terrapins have enlarged heads. Photo: B. Pfau. Fig. 23. Marking of a terrapin which was caught for the first time. The wounds which are caused by boring the marginal shields will heal up quickly. Photo: B. Pfau. Fig. 24. The terrapin is released carefully... Photo: C. Pfau. RADIATA 19 (1), 2010 17

Beate Pfau & Willem M. Roosenburg the houses are usually built near the shore (Fig. 10), or the owners create lawns or ornamental gardens that alter the incubation environment and are maintained intensively resulting in the death of many terrapin hatchlings. Additionally the access roads to coastal developments are often built on high ground that is terrapin nesting habitat creating perils for nesting females, particularly if they choose the road embankment as a nest site (Wood & Herlands 1997 or Szerlag & McRobert 2006). Additionally racoon populations (and in some places also fox populations) thrive with increasing human populations because our garbage provides a dependable food source year round. The concentration of nests as nesting habitat becomes limited combined with increasing raccoon populations results in high predation rates on nesting beaches, frequently over 90%. Racoons and foxes are excellent at finding and depredating turtle nests resulting in very low recruitment in areas where these predators occur. Commercial exploitation Up until the beginning of the 20 th century, Diamondback terrapins were in great demand by gourmet restaurants in major metropolitan areas of the US. Haramis et al. (2006) detail the most effective method of harvesting Diamondback terrapins, dredging or scraping in hibernacula where terrapins congregate during the winter. Harvest rates using this technique can be as high as 200 adult terrapins per hour. Terrapins congregate in large numbers in shallow, sheltered creeks in Chesapeake Bay to hibernate in areas where they can be harvested easily with special dredges. Test dredgings revealed that most of the animals caught were adult females, suggesting a significant reduction in the population s reproductive potential. During the terrapin s active period, fyke nets are the most effective harvesting method. In 1920, the prohibition led to a decline in the demand for terrapin flesh because a key ingredient of terrapin soup was sherry. This contributed to the recovery of terrapin populations as the market demand evaporated (compare the chapter A Clear and Present Danger in Brennessel 2006). Nevertheless, the harvest continued on a smaller scale and the terrapin stews were cooked according to different recipes, but in the U.S. the terrapin slowly decreased in value as food, and no longer was considered a delicacy. During the 80 s, a rising demand for terrapins in the Chinatowns of the larger US and Canadian cities fuelled incentive for fishermen to again pursue the terrapin. Furthermore, in 1989 China opened its markets for the international trade and the terrapin fishery began to increase conspicuously. Animals were exported live in great quantities. One single fisherman reported that he had caught and sold 5,000 in 2006, and that half of those were exported to China. Another exporter advertised that he could deliver one ton of diamondbacks per month to China (Chesapeake Terrapin Alliance, see Internet resources). In 2007, the last two US states, Maryland and Texas, that permitted large scale harvest passed laws stopping the commercial harvest of wild terrapins for both food and the pet trade (see below). Diamondback terrapins are still in great demand as pets for turtle aficionados. Terrapin enthusiasts and the pet trade recognize that captive bred terrapins are superior pets because they are less prone to diseases than wild animals. Additionally, prohibition on commercial harvest limits the availability of wild animals for the pet industry. In the USA, there are some speciality terrapin breeders for the pet market. In Europe, there are only few Malaclemys groups 18 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland being kept, and accordingly few breeders regularly hatch them, but they are available through some sources. Diamondback terrapin conservation Legislation In 1994, the diamondback terrapin became Maryland s official State reptile and for 70 years has been the University of Maryland s mascot. The Maryland Department of Natural Resources is responsible for controlling research and promoting terrapin conservation and management. In the last 10 years, declining terrapin populations and continued commercial harvest spawned a renewed public awareness of diamondback terrapins focused on closing the commercial harvest and improving conservation. For the most part, the public was unaware of the exploitation of natural terrapin populations. Finally, in July 2007, Maryland banned the commercial harvest of diamondback terrapins. The governor of Maryland signed the Terrapin Bill, and only Texas remained as the one state in the range of Malaclemys terrapin where terrapins could be harvested. Texas adopted similar legislation banning the commercial harvest most species of turtles including terrapins about one month later. New Jersey, Maryland, and Delaware have laws and regulations requiring the use of BRDs on crab pots. However, most states in the terrapins range do not have regulations that protect terrapins from the crab pots. New Jersey and Georgia require rapidly decaying panels made of fast rusting metals) to allow escape from lost traps (ghost pots). Ghost pots continue to catch terrapins and have frequently been found with more then 50 terrapins in a single trap (Roosenburg 1991). An overview of the laws and regulations for crab pots are given by Watters (2004). Publicity Diamondback terrapins are an excellent hallmark species for the protection of the fragile estuarine environments. Young children are drawn to hatchlings and will engage themselves for their protection and, if well informed, will involve their families and friends. This is effective because nobody will act directly against the will of an angry child! Therefore conservation efforts often include children. Of special importance for Diamondback terrapin protection was the printing of the children s book Turtles in my sandbox, by Jennifer Keats Curtis (2007). The author depicts how a little girl learns to observe terrapins hatching from eggs that she had found in her sandbox. The story describes how she develops, with the help of a neighbour, into an engaged terrapin conservationist. Children also desire to be actively involved. Conservation projects that involve head-starting and releasing terrapins at larger body sizes are a good opportunity to work with school children. The children care for terrapins in their classrooms, and collect data on their behaviour and growth as part of a curriculum to teach environmental biology. Used correctly, these terrapins engage children in the broader context of environmental stewardship and environmental awareness. Raising terrapin hatchlings accelerates growth to a larger, body size while the children incorporate terrapin themes in their curriculum. The children frequently project their enthusiasm for terrapin conservation to friends and family. Precautions are necessary when children work with turtles because they can carry Salmonella or other bacteria. Therefore, detailed instructions on terrapin husbandry were developed and some of the tasks are carried out only by adults. Children are RADIATA 19 (1), 2010 19

Beate Pfau & Willem M. Roosenburg not allowed to touch the terrapins this is good training for handling any wildlife. Children change the water and clean the filters according to specific instructions. Only on the release day may the children handle their terrapin when they let it go (and wash hands immediately thereafter). Terrapin attract considerable media attention in local newspapers and on TV. Children with animals always have great public appeal; see for example Gvozdas (2007a, b). The children sensitize the public to terrapin conservation and they contributed to raising public awareness about the bill banning commercial harvest in Maryland (see above). In Maryland, one head-starting project is coordinated by Will Williams and Steve Barry (Fig. 1) at the Arlington Echo Outdoor Education Centre. Terrapin hatchlings from Poplar Island are used in their program (see below). Teachers submit weekly reports on the terrapins measurements to Will who maintains the database. The project gets public funding from the Chesapeake Bay Trust which pays for aquaria, food, and measuring tools. Will organizes buses and boat trips that bring the children to Poplar Island for the release of their terrapins. Since 1932, the diamondback terrapin, Testudo has been the official mascot of the University of Maryland. The University of Mayland Terrapins, or Terps play under the motto Fear the Turtle. Since 2002, the university contributes 15% of the proceeds derived from the sales of materials bearing the Fear the Turtle logo to terrapin conservation and education. These funds are used to fund terrapin research and interns working on terrapin conservation. Fig. 25. and swims away as rapidly as it can. Photo: B. Pfau. 20 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland The projects undertaken in this research are comprehensive. The cornerstone of the terrapin research is the demographic work that has developed a 23 year database of over 10,000 terrapins and more than 31,000 captures. Fig. 26. This bald eagle has its nest very near to the laboratory. Photo: C. Pfau. Scientific research on Diamondback terrapins in Maryland In 1987, prior to becoming Maryland s state reptile, Willem Roosenburg started his research on Malaclemys terrapin terrapin in the Maryland waters of Chesapeake Bay. He spends his springs and summers studying terrapins on the lower Patuxent River and living in a small house on Cremona Farm. Several students work with him each year continuing his mark-recapture study and completing their own research projects under his supervision. The students live in primitive bunk houses on Cremona that are part of the research facility. A ground floor room in an old east-coast barn serves as a laboratory for processing terrapins (Fig. 15). Long-term research of the lower Patuxent River Diamondback terrapin population Terrapins are caught in variety of traps, but most are caught in unbaited fyke nets that are set near the shore (Fig. 16). A float holds the cod end above water, maintains an airspace that will adjusts with the tide so the entrapped terrapins will not drown. The nets are checked daily to avoid harming the terrapins. The nets also catch a host of estuarine organisms, including a variety of fishes, horseshoe crabs (Limulus polyphemus, Fig. 14), blue crabs (Callinectes sapidus, Fig. 17) and snapping turtles (Chelydra serpentina, Fig. 18). The bycatch is released immediately. Female diamondbacks are immediately palpated for eggs (Fig. 19), and if gravid they are separated from the others in case they start to lay their eggs before being released. The terrapins are held in numbered laundry bags and the location of the trap and bag number are recorded to ensure that Fig. 27. Juvenile female terrapin from Poplar Island with carapace anomalies. Photo: B. Pfau. RADIATA 19 (1), 2010 21

Beate Pfau & Willem M. Roosenburg animals are returned to the same location. After checking all the nets, the terrapins are brought back to the laboratory for processing. Researchers measure carapace length (Fig. 20), carapace width, carapace height, plastron length, length of the 3 rd midline seam of the left pectoral scute (Fig. 21) and head width (Fig. 22). Researchers count growth annuli to age the terrapin and the terrapin is weighed. Finally, students determine the gender of terrapins greater than 10 cm carapace length. If the terrapin has already been marked the ID is read and checked in the database, otherwise the animal is marked using the traditional notching of marginal scutes (Cagle, 1939; Fig. 23). Upon completion of processing the days catch, the terrapins are brought back and released where they were caught (Figs. 24 and 25). They swim only a short distance, then dive down and a few seconds later they resurface for a breath and a seeming orientation of their whereabouts. The diamondbacks in the research area have been recaptured on average three times. The oldest terrapin caught in 2007 was 32 years, a female first caught in 1987 when she was twelve years old. Terrapins can be aged until about 10-15 years after which the annuli fade because they shed the scutes that reveal the rings. This female was still healthy when caught in 2007 and was perhaps on her way to a nesting beach. The maximum age of wild Diamondback terrapins is not yet known; only the continuing studies will reveal the potential longevity of terrapins. However, it is reasonable to assume that some female terrapins in the Patuxent River are more than 50 years old. Most of the terrapins caught in the fyke nets are females (sex ratio 3-3.5:1). Other population studies in the Chesapeake Bay have similar results and reveal that there are considerably more females than males. The terrapin nesting season in Chesapeake Bay begins in the end of May (Memorial Day is a good reminder) and continues until the end of July. On rare occasions, nests have been discovered in August. The average clutch size in the middle Chesapeake is 13 eggs and females will nest up to 3 times per year (Roosenburg & Dunham 1997). The long-term study also benefits from serendipitous observations. For example, the shells of marked terrapins have been recovered under an active bald eagle nest that is near the laboratory (Fig. 26). The long-term research reveals some interesting findings. Diamondbacks move little among regions of the bay. Recapture rates of adults are high and females show a high degree of philopatry to nesting areas. The limited movement may contribute to morphological differences among populations throughout the bay, e.g. female terrapins on Smith Island have broader heads and smaller body sizes suggesting that the populations their may have larger beaks because they feed on harder shelled snails then the clams preferred in the Patuxent River. A detailed analysis is needed to confirm the divergence between these nearby populations. Regrettably Roosenburg s long-term study documents a decline in the terrapin population in the Patuxent River since 1996. Because of the comprehensive and reliable documentation, this result cannot be denied by the lobbyists of the commercial turtle harvesters or the industries that pollute the habitat. Only prudent environmental legislation protecting terrapins and their habitat and stringent enforcement coupled with public awareness could perhaps reverse the decline of the terrapins and other organisms in the fragile estuarine habitat. Although some progress toward this goal has been accomplished, much remains to be implemented to ensure terrapin populations for future generations. 22 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Diamondback terrapin habitat restoration on Poplar Island Sandy islands, ideal nesting beaches for terrapins, were once common throughout the Chesapeake Bay. However, in the last century a combination of development, erosion, and increasing water levels have diminished these islands throughout the bay. During the last century mean high water marks have changed as much as 40 cm in some areas. The accompanying loss of marsh habitats has been particularly well documented for the Blackwater National Wildlife Refuge in Maryland (USGS 2004). Poplar Island lies approximately 50 miles south of Baltimore near the eastern shore of the bay. When originally mapped in 1847, Poplar Island was more than 400 hectares. Because of its isolation and beauty, the island became a weekend retreat for prominent politicians in 1930s and therefore gained notoriety. By 1999 less than 5 acres remained. The availability of dredged material from the shipping channel and Baltimore Harbour approach provided a potential source to rebuild the island. An interagency group, including the U.S. Army Corps of Engineers, the Maryland Port Administration, and Federal and State environmental agencies decided in 1994 to re-build Poplar Island to its original size using dredged material. In 1999 the task began and will be completed in 2016. A summary of this project is given on the internet site of the US Army Corps of Engineers (USACE w.y.). The restoration project is monitored closely, including detailed analysis of water quality, dredge material, and the impact on local wildlife. As the project progresses the impacts on the islands flora and fauna are carefully monitored to assure the creation of high quality habitat. Like many other wildlife species, terrapins started using Poplar Island as soon as the first dikes were constructed. It remains unknown whether these were old resident females native to the archipelago and nested on the islands beaches in previous years, or whether they came from the mainland and discovered the new beaches. The hatching success on the new beaches is exceptionally high. However, the terrapins are nesting in sand mined from the site and not in dredge material. Although the engineers who would have preferred that the terrapins wait until the island was completed, and measure were necessary to keep terrapins from entering areas still under construction. For the terrapins, the island is a tremendous source of recruitment because nest predators, racoons and foxes, have not colonized the island. Therefore, over 70% of terrapin nests survive. Only the fish crows, Corvus ossifragus, gulls, Larus spp., egrets, Egretta spp., and herons Ardea spp. are still a threat to the nests and hatchlings. Diamondback terrapins inhabited Poplar Island in the past. But as the island eroded, the terrapin population probably declined because the nesting beaches were successively lost and the shallow water habitats were flooded. One of the most important goals of the project has become the restoration of the resident terrapin population. Poplar Island is surveyed annually by terrapin specialists (see for example Roosenburg & Allman 2003, Roosenburg et al. 2003, 2004, 2007). In summer 2002, the study team found 50 terrapin nests and recovered 323 hatchlings. In 2006, more than 280 nests were discovered and 1616 hatchlings were produced on the island (Roosenburg et al. 2007 and Roosenburg 2007, see Internet resources). The increase in nesting observed during the last five years suggests that the island is good nesting habitat that may be limiting in other areas of the bay because of shoreline development. At the Patuxent River site, terrapins average 13 eggs per nest (Roosenburg & RADIATA 19 (1), 2010 23

Beate Pfau & Willem M. Roosenburg Fig. 28. The endoscope is inserted trough a slit which had been cut into the inguinal opening. The light of the endoscope shines through the carapace approximately at the location of the gonads. Photo: B. Pfau. Fig. 29. Willem Roosenburg sexes a terrapin. Photo: B. Pfau. 24 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 30. The juvenile terrapins are raised in standardized terraria. Photo: B. Pfau. Fig. 31. A transponder is inserted. Photo: B. Pfau. Fig. 32. The terrapin remains in a dry place until the wound has closed sufficiently. Photo: B. Pfau. RADIATA 19 (1), 2010 25

Beate Pfau & Willem M. Roosenburg Fig. 33. Willem Roosenburg digs up the nest. Photo: B. Pfau. Dunham 1997) but at the Poplar Island site females average almost 14 eggs per nest (Roosenburg et al. 2007). Researchers do not understand the differences between these two populations that are separated by less than 50 km but future studies will explore why the differences exist and the environmental factors that underlie them. The hatchlings from Poplar Island are same size as terrapin hatchlings from other beaches in Maryland. Scute anomalies (irregular carapacial scutes, see for example Fig. 27) are more common on Poplar Island and may be due higher incubation temperatures because the island lacks shade producing vegetation. High incubation temperatures cause more carapacial anomalies in many chelonian species (compare to Jasser-Häger & Winter 2007), and also in terrapins (Herlands et al. 2003). There is no evidence that these anomalies reduce the turtles fitness. During the initial stages of the Poplar Island Restoration Project, wetlands where juvenile terrapins spend the first years were limited. Nevertheless, the 2002 and 2003 hatchlings were released into the best habitat available. Since 2003, hatchlings from the island are released into newly constructed wetland cells that are remarkable restorations of the estuarine salt marsh. Since 2005, school classes through Arlington Echo (see above) have head- started approximately 450 terrapin hatchlings from Poplar Island. These hatchlings attain the size of 4-5 year olds by spring because they are fed and kept in warm conditions throughout the winter. This headstarting method has been used successfully for certain (not all) turtle species. The teachers are trained and the rearing conditions are standardized. The terrapins live in special aquaria with 80 40 cm base and 10 cm water depth. Foam filters clean and agitate the water. A stone basking 26 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland platform sits under full spectrum fluorescent light and a ceramic heat bulb (Fig. 30). The terrapins start with special pelleted food and graduate to natural prey before release. The water temperature is kept high intentionally to accelerated growth over the winter. The teachers bring the terrapins to the laboratory in May for an overall examination and for sexing by endoscopy (Figs. 28 and 29). The terrapins are marked individually with an internal PIT (Passive Integrated Transponder) tag (Fig. 31) and additional growth data are collected. Following surgery and tag implantation, the terrapins are kept dry for 12 hours (Fig. 32) to allow the 2 mm incision in the inguinal region to heal. The teachers pick up their terrapins 48 hours after drop off. The school children wean the terrapins to natural, live food, to teach the terrapins to forage in the wild. Crab and shrimp are forbidden because the young terrapins get addicted to this food and will not practice catching worms, snails and other animals. During the last days of school year, the children come to Poplar Island to release the head-started terrapins (see above, Publicity ). These diamondbacks are no longer dependent on the shallow water habitats and they are too large for most of the natural predators. Because they carry the PIT tags with an individual code their survival can be monitored in the future. Hopefully, some of these turtles will nest on the beaches where they originated. Electric fencing of nesting areas As described above, the extensive development along beaches has reduced suitable nesting habitat, but also indirectly increased the number of racoons and foxes, predators of terrapin nests. Roosenburg (1991) found that 35 of 1,314 terrapin nests hatched over a 4 year period. Most of the unsuccessful nests were eaten by mammalian predators. A more detailed analysis indicated that predation rates were higher on the beach with a higher nest density (Roosenburg & Place 1995) suggesting that nests predation rates may be density dependent. If nest predation is density dependent, then continued development and loss of nesting habitat could result in greater than normal rates of nest predation and ultimately population decline. Several techniques have been used to protect chelonian nests including wire cages, transplanting nests, and chemicals to deter mammalian predators. Most of these techniques are laborious and expensive. Transplanting eggs runs the risk of disrupting development and therefore is only suggested for critically endangered species. In collaboration with Willem Roosenburg, undergraduate students from the University of Maryland s Gemstone Scholar program are experimenting with the use of electric fencing to exclude mammalian predators from nesting areas. The researchers selected a recently restored nesting beach that formerly was a known terrapin nesting area (Fig. 36). The restoration used sand with higher gravel content than found on the typical nesting beaches, but terrapins are still nesting on the site. Spartina patens was planted sparsely on the nesting area. Marjorie Clemens, one of the students, surveys the newly built beach daily for signs of nesting activity. The beach segment chosen by Marjorie and her colleagues partitioned the beach into alternating protected and unprotected 5 5 m squares. An electric fence about 1 m high protects the experimental plots on the beach (Fig. 39). Rigid poles are placed on each corner of a plot and one support pole between each corner. The lowest wire is 10 cm above the ground so nesting female terrapins can pass below without touching it. Walking or even crawling foxes and racoons will get RADIATA 19 (1), 2010 27

Beate Pfau & Willem M. Roosenburg Fig. 34. Track of a Diamondback terrapin. Photo: B. Pfau. Fig. 35. The tracks of Snapping turtles show dragging marks of the tail. Photo: B. Pfau. an electric shock when they touch the wire when trying to get into the protected area. The top wires, approximately 1 m above the ground prevent mammals from jumping the fence. The voltage is similar to that used in horse pastures because weak currents will not deter a determined racoon. Of course, signs warn humans about the danger of the electric fence colored flags clearly mark corners of the fenced squares. During the nesting season, the students inspect the beach daily for nesting activity. Occasionally, snapping turtles, Chelydra serpentina, will wander onto the beach but their tracks are easily distinguished from terrapins (Fig. 34) by the long toenail marks and the large tail drag (Fig. 35). At the end of the track from the river, the nest can be found where the female terrapin has concealed the nest cavity with turning movements (Fig. 37). Marjorie Clemens gets the exact nest location using a handheld Geographic Positioning System (GPS) unit (Fig. 40). Normally the nest is left undisturbed, but Willem digs up the nest to show us the eggs (Fig. 33). The eggs are about 10 cm below surface, fresh eggs are translucent (Fig. 38) and they become chalky white as they age. Of course, the eggs were reburied afterwards and the nest was closed carefully. Not all the turtle tracks lead to nests. Some females returned to the water because they were disturbed or they did not find a favourable nesting site. Regrettably, Marjorie Clemens also finds depredated terrapin nests, but these are not in the area protected by the fence (Fig. 41). 28 RADIATA 19 (1), 2010

Diamondback terrapins in Maryland Fig. 36. The artificial nesting beach with young plants. Photo: B. Pfau. Fig. 39. The wires of the electric fencing are fastened in different heights above the ground. Photo: B. Pfau. Fig. 37. The female Diamondback terrapin has closed its nest by turning movements. Photo: B. Pfau. Fig. 40. Marjorie Clemens takes the geographical coordinates of the nest using a GPS handy. Photo: B. Pfau. Fig. 38. Freshly laid terrapin eggs are somewhat translucent. Photo: B. Pfau. Fig. 41. This unprotected nest of a Snapping turtle has been raided. Only shrunken eggshells remain. Photo: B. Pfau. RADIATA 19 (1), 2010 29