Diamondback terrapin

Diamondback terrapin
hand-colored lithograph from Holbrook's North American Herpetology (1842)
Conservation status
Near Threatened (IUCN 2.3) [1]
Scientific classification
Kingdom:	Animalia
Phylum:	Chordata
Subphylum:	Vertebrata
Class:	Reptilia
Subclass:	Anapsida
Order:	Testudines
Suborder:	Cryptodira
Superfamily:	Testudinoidea
Family:	Emydidae
Subfamily:	Deirochelyinae
Genus:	Malaclemys Gray, 1844 [2]
Species:	M. terrapin
Binomial name
Malaclemys terrapin (Schoepff, 1793) [2]
Synonyms
Testudo terrapin Schoepff, 1793 Testudo concentrica Shaw. 1802 Testudo ocellata Link Testudo concentrata - Kuhl, 1820 (ex errore) Emys concentrica - Duméril & Bibron, 1835 Emys terrapin - Holbrook, 1842 Emys macrocephalus Gray, 1844 Malaclemys concentrica - Gray, 1863 Malacoclemmys terrapen - Boulenger, 1889 (ex errore) Malaclemys terrapin - Bangs, 1896 Malaclemys centrata concentrica - Cochran, 1932 Malaclemys terrapin - Conant, 1975[3]

The diamondback terrapin (Malaclemys terrapin) or simply terrapin, is a species of turtle native to the brackish coastal swamps of the eastern and southern United States. It belongs to the monotypic genus, Malaclemys.  It is has one of the largest ranges of all  turtles in North America, stretching from the Florida Keys to Cape Cod.^[4]

Naming

The name "terrapin" is derived from the Algonquian word torope.^[5] It applies to Malaclemys terrapin in both British English and American English. The name originally was used by early European settlers in North America to describe these brackish-water turtles that inhabited neither freshwater habitats nor the sea. It retains this primary meaning in American English.^[5] In British English, however, other semi-aquatic turtle species, such as the red-eared slider, might be called a terrapin.

Description

photograph of a diamondback terrapin, showing the diamond pattern

The common name refers to the diamond pattern on top of its shell (carapace), but the overall pattern and coloration vary greatly.  The shell is usually wider at the back than in the front and from above its appears wedge shaped. Its shell coloring can vary from browns to greys, and its body color can be grey, brown, yellow, or  white. All have a unique pattern of wiggly, black markings or spots on their body and head. The diamondback terrapin have large webbed feet.^[6] The species is sexually dimorphic in that the males grow to approximately 5 inches (130 mm), while the females grow to an average of around 7.5 inches (190 mm), though they are capable of growing larger. The largest female on record was just over 9 inches (230 mm) in length. Specimens from regions that are consistently warmer in temperature tend to be larger than those from cooler, more northern areas.^[7]

Adaptations to their environment

Terrapins look much like their freshwater relatives, but are well adapted to the near shore marine environment.  They have several adaptations that allow them to survive in varying salinities. They can live in full strength salt water for extended periods of time,^[8] and their skin is largely impermeable to salt.  Terrapins have lachrymal salt glands,^[9][10] not present in their relatives, which are used primarily when the turtle is dehydrated.  They can distinguish between drinking water of different salinities.^[11]  Terrapins also exhibit unusual and sophisticated behavior to obtain fresh water, including drinking the freshwater surface layer that can accumulate on top of salt water during rainfall and raising their heads into the air with mouths open to catch falling rain drops,.^[11][12]  

Terrapins are strong swimmers.  They have strongly webbed hind feet, but not flippers as do sea turtles.  Like their relatives (Graptemys), they have strong jaws for crushing shells of prey, such as clams and snails.  This is especially true of females, who have larger and more muscular jaws than males.^[13]

Subspecies

Seven subspecies are recognized including the nominate race.

• M. t. centrata (Latreille, 1801) – Carolina diamondback terrapin (Georgia, Florida, North Carolina, South Carolina) ^[2]
• M. t. littoralis (Hay, 1904) – Texas diamondback terrapin (Texas) ^[2]
• M. t. macrospilota (Hay, 1904) – Ornate diamondback terrapin (Florida) ^[2]
• M. t. pileata (Wied, 1865) – Mississippi diamondback terrapin (Alabama, Florida, Louisiana, Mississippi, Texas) ^[2]
• M. t. rhizophorarum Fowler, 1906 – Mangrove terrapin (Florida) ^[2]
• M. t. tequesta Schwartz, 1955 – Eastern Florida terrapin (Florida) ^[2]
• M. t. terrapin (Schoepff, 1793) – Northern diamondback terrapin (Alabama, Connecticut, Delaware, Florida, Georgia, Louisiana, Maryland, Massachusetts, Mississippi, New Jersey, New York, North Carolina, Rhode Island, South Carolina, Texas, Virginia) ^[14][15]

Distribution and habitat

Diamondback terrapins live in the very narrow strip of coastal habitats on the Atlantic and Gulf coasts of the United States, from as far north as Cape Cod, Massachusetts to the southern tip of Florida and around the Gulf Coast to Texas. In most of their range terrapins live in Spartina marshes that are flooded at high tide, but in Florida they also live in mangrove swamps.^[16]  This turtle can survive in freshwater as well as full strength ocean water but adults prefer intermediate salinities. They have no competition from other turtles, although snapping turtles do occasionally make use of salty marshes.^[17] It is unclear why terrapins do not inhabit the upper reaches of rivers within their range, as in captivity they tolerate fresh water.  It is possible they are limited by the distribution of their prey.^[18]  Terrapins live quite close to shore, unlike sea turtles, which wander far out to sea.  Terrapins tend to live in the same areas for most or all of their lives, and do not make long distance migrations,^[19][20],.^[21]

Life cycle

Adult diamondback terrapins mate in the early spring, and clutches of 4-22^[22] eggs are laid in sand dunes in the early summer. They hatch in late summer or early fall. Maturity in males is reached in 2–3 years at around 4.5 inches (110 mm) in length; it takes longer for females: 6–7 years (8–10 years for northern diamondback terrapins) at a length of around 6.75 inches (171 mm).

Reproduction

Like all reptiles, terrapin fertilization occurs internally. Courtship has been seen in May and June, and is similar to that of the closely related red-eared slider (Trachemys scripta).^[23]  Female terrapins can mate with multiple males and store sperm for years,^[24] resulting in some clutches of eggs with more than one father. 

Like many turtles, terrapin have temperature dependent sex determination, meaning that the sex of hatchlings is the result of incubation temperature.  Females can lay up to three clutches of eggs/year in the wild,^[25] and up to five clutches/year in captivity.^[26]  It is not known how often they may skip reproduction, so true clutch frequency is unknown.  

Females may wander considerable distances on land before nesting.  Nests are usually laid in sand dunes or scrub vegetation near the ocean^[27] in June and July, but nesting may start as early as late April in Florida.^[28]  Females will quickly abandon a nest attempt if they are disturbed while nesting.  Clutch sizes vary latitudinally, with average clutch sizes as low as 5.8/eggs/clutch in southern Florida^[29] to 10.9 in New York.^[25]  After covering the nest, terrapins quickly return to the ocean and do not return except to nest again.

The eggs usually hatch in 60–85 days, depending on the temperature and the depth of the nest. Hatchlings usually emerge from the nest in August and September, but may overwinter in the nest after hatching.^[30]  Hatchlings sometimes stay on land in the nesting areas in both fall and spring, and they may remain terrestrial for much or all of the winter in some places,.^[28][31] Hatchling terrapins are freeze tolerant,^[30] which may facilitate overwintering on land.  Hatchlings have lower salt tolerance than adults, and Gibbons et al.^[19] provided strong evidence that one- and two-year old terrapins use different habitats than do old individuals.

Growth rates, age of maturity, and maximum age are not well known for terrapins in the wild, but males reach sexual maturity before females, because of their smaller adult size.  In females at least, sexual maturity is size rather than age dependent.^[32]  Estimations of age based on counts of growth rings on the shell are untested, so it not clear how to determine the ages of wild terrapins.

Seasonal activities

Because nesting is the only terrapin activity that occurs on land, most other aspects of terrapin behavior are poorly known. Limited data suggest that terrapins hibernate in the colder months in most of their range, in the mud of creeks and marshes.^[33]

Diet

Diamondback terrapin diets are not generally well studied, and almost all work on diets has been done in the southeastern part of their range.  They eat shrimp, clams, crabs, mussels, and other marine invertebrates,^[20] especially periwinkle snails.^[34] At high densities they may eat enough invertebrates to have ecosystem-level effects, partially because periwinkles can themselves overgraze important marsh plants.^[35]

Conservation

Status

In the 1900s the species was once considered a delicacy to eat and was hunted almost to extinction. The numbers also decreased due to the development of coastal areas and, more recently, wounds from the propellors on motorboats. Another common cause of death is the trapping of the turtles under crabbing and lobster nets. Due to this, it is listed as an endangered species in Rhode Island, is considered a threatened species in Massachusetts, and is considered a "species of concern" in Georgia, Delaware, Alabama, Louisiana, North Carolina, and Virginia. In Connecticut there is no open hunting season for this animal. However, it holds no federal conservation status.^[6]

Diamondback terrapin, Malaclemys terrapin

Conservation research

Diamondback terrapins are decreasing in much of their range. There is limited protection for terrapins on a state-by-state level throughout its range; it is listed as Endangered in Rhode Island and Threatened in Massachusetts.  Check with the Diamondback Terrapin Working Group ^[36] for a recent review of state-by-state laws. There is no national protection except through the Lacey Act, and little international protection. 

Numerous scientists, conservation organizations, and private individuals are conducting research and working to help terrapins.  The Diamondback Terrapin Working Group^[36]

Threats

The major threats to diamondback terrapins are all associated with humans, and probably differ in different parts of their range.  People tend to build their cities on ocean coasts near the mouths of large rivers, and in doing so they have destroyed many of the huge marshes terrapin inhabited.^[37]  Nationwide, probably >75% of the salt marshes where terrapins lived have been destroyed or altered.  Currently, ocean level rise threatens the remainder. 

Traps used to catch crabs both commercially and privately have commonly caught and drowned many diamondback terrapins,^[19] which can result in male-biased populations and local population declines and even extinctions,.^[20][38]  When these traps are lost or abandoned (= “ghost traps”), they can kill terrapins for many years.  Terrapin-excluding devices are available to retrofit crab traps, these reduce the number of terrapins captured while having little or no impact on crab capture rates.^[39][40]  In some states (NJ, DE, MD), these devices are required by law.

Nests, hatchlings, and sometimes adults,^[41] Burke unpub. data) are commonly eaten by raccoons, foxes, rats,^[25][42][43] and many species of birds, especially crows and gulls,.^[28][44] Density of these predators are often increased because of their association with humans.  Predation rates can be extremely high; predation by raccoons on terrapin nests at Jamaica Bay Wildlife Refuge in New York varied from 92-100% each year from 1998–2008,^[25] Burke unpubl. data).

Terrapins are killed by cars when nesting females cross roads,^[45] and mortality can be high enough to seriously impact populations.^[46]  Terrapins are still harvested for food in some states. Terrapins may be affected by pollutants such as metals and organic compounds,^[47] but this has not been demonstrated in wild populations.

There is an active casual and professional pet trade in terrapins, and it is unknown how many are removed from the wild for this purpose.  Some people breed the species in captivity (e.g.,,^[48] and some color variants are considered especially desirable.  In Europe, Malaclemys are widely kept as pets as are many closely related species.

Relationship with humans

In Maryland, diamondback terrapins were so plentiful in the 18th century that slaves protested the excessive use of this food source as their main protein. Late in the 19th century, demand for turtle soup claimed a harvest of 89,150 pounds from Chesapeake Bay in one year. In 1899, terrapin was offered on the dinner menu of Delmonico's Restaurant in New York City as the third most expensive item on the extensive menu. A patron could request either Maryland or Baltimore terrapin at a price of $2.50. Although demand was high, over capture was so high by 1920, the harvest of terrapins reached only 823 pounds for the year.^[49]

According to the FAA National Wildlife Strike Database, a total of 18 strikes between diamondback terrapins and civil aircraft were reported in the US from 1990 to 2007, none of which caused damage to the aircraft.^[50] On July 8, 2009, flights at John F. Kennedy Airport in New York City were delayed for up to one and a half hours as 78 diamondback terrapins had invaded one of the runways. The turtles, which according to airport authorities were believed to have entered the runway in order to mate, were removed and released back into the wild.^[51] A similar incident happened on June 29, 2011, when over 150 turtles crossed runway four, closing the runway and disrupting air traffic. Those terrapins were also relocated safely.^[52]

Many human activities threaten the safety of daimondback terrapins. The terrapins get caught and drown in crab nets that humans put out, are suffocated by pollution that humans greatly contribute to, and lose their marsh and estuarine habitats because of urban development.^[53]

History as a delicacy

Diamondback terrapins were heavily harvested for food in colonial America, and probably before that by native Americans. Terrapins were so abundant and easily obtained that slaves and even the Continental Army ate large numbers of terrapins. Terrapins become a fashionable delicacy and sold for as much as $5 each in 1917.^[42]  Huge numbers of terrapins were harvested from marshes and marketed in cities. By the early 1900s populations in the northern part of the range were severely depleted, and the south was greatly reduced as well.^[34]  As early as 1902 the U.S. Bureau of Fisheries (which later became the U.S. Fish and Wildlife Service) recognized that terrapin populations were declining and started building large research facilities in South Carolina to investigate methods for captive breeding terrapins for food.  People tried (unsuccessfully) to establish them in many other locations, including San Francisco.^[54]

Use as a symbol

Maryland named the diamondback terrapin its official state reptile in 1994. The University of Maryland, College Park has used the species as its nickname (the Maryland Terrapins) and mascot (Testudo) since 1933. The athletic teams are often referred to as "Terps" for short.^[55]

References

1. ^ IUCN Red List: Malaclemys terrapin IUCN Red List: Malaclemys terrapin
2. ^ ^{a b c d e f g h} (Rhodin et al. 2010, p. 000.101)
3. ^ Malaclemys terrapin (SCHOEPFF, 1793) - The Reptile Database
4. ^ Seigel, Richard A.. "Nesting Habits of Diamondback Terrapin (Malaclemys terrapin) on the Atlantic Coast of Florida". Department of Biological Studies, University of Central Florida. http://www.jstor.org/pss/3628414. Retrieved 2011-10-25. 
5. ^ ^{a b} "Terrapin" at m-w.com
6. ^ ^{a b} "Northern Diamondback Terrapin Malaclemys t. terrapin". http://www.ct.gov/dep/lib/dep/wildlife/pdf_files/outreach/fact_sheets/dmbkterp.pdf. Retrieved 25 October 2011. 
7. ^ Davenport, John (1992)."The Biology of the Diamondback Terrapin Malaclemys Terrapin (Latreille)", Tetsudo, 3(4)
8. ^ Bentley, P.J., Bretz, W.L., and K. Schmidt-Nielsen.  1967.  Osmoregulation in the diamondback terrapin, Malaclemys terrapin cetrata.  Journal of Experimental Biology. 46:161-167
9. ^ Cowan, F.B.M.  1971.  The ultrastructure of the lachrymal “salt” gland and the Harderian gland in the euryhaline Malaclemys and some closely related stenohaline emydids.  Canadian Journal of Zoology 49:691-687
10. ^ Cowan, F. B. M. 1981. Effects of salt loading in salt gland function in the euryhaline turtle, Malaclemys terrapin. Journal of Comparative Physiology 145:101-108
11. ^ ^{a b} Davenport, J. and E. A. Macedo. 1990. Behavioral osmotic control in the euryhaline diamondback terrapin Malaclemys terrapin: responses to low salinity and rainfall. Journal of Zoology 220:487-496
12. ^ , V.L., Davenport, J., and S. Renous.  1995.  Drinking and water expulsion in the diamondback terrapin Malaclemys terrapin.  Journal of Zoology (London) 236:483-497
13. ^ Tucker, A. D., N. N. Fitzsimmons, J. W. Gibbons. 1995. Resource partitioning by the estuarine turtle Malaclemys terrapin: trophic, spatial and temporal foraging constraints. Herpetologica 51:167-181
14. ^ (Conant 1975)
15. ^ (Smith 1982)
16. ^ Hart, K. M., C. C. McIvor. 2008. Demography and Ecology of Mangrove Diamondback Terrapins in a Wilderness Area of Everglades National Park, Florida, USA. Copeia 2008:200-208
17. ^ Kinneary, J. J.  1993.  Salinity relations of Chelydra serpentina in a Long Island estuary. Journal of Herpetology 27: 441-446
18. ^ Coker, R. E. 1906. The natural history and cultivation of the diamond-back terrapin with notes of other forms of turtles. North Carolina Geological Survey Bulletin. 14:1-67
19. ^ ^{a b c} Gibbons, J. W., J. E. Lovich, A. D. Tucker, N. N. Fitzsimmons and J. L. Greene. 2001. "Demographic and ecological factors affecting conservation and management of diamondback terrapins (Malaclemys terrapin) in South Carolina" Chelonian Conservation and Biology 4:66-74
20. ^ ^{a b c} Tucker, A. D., J. W. Gibbons, and J. L. Greene. 2001. Estimates of adult survival and migration for diamondback terrapins: conservation insight from local extirpation within a metapopulation. Canadian Journal of Zoology 79:2199-2209
21. ^ Hauswaldt, J. S. and T. C. Glen. 2005. Population genetics of the diamondback terrapin (Malaclemys terrapin). Molecular Ecology 14:723-732
22. ^ Brennessel, Barbara. "Diamonds in the Marsh," Hanover: University Press of New England, 2006
23. ^ Seigel, R.A. 1980. Courtship and mating behavior of the diamondback terrapin, Malaclemys terrapin tequesta. Journal of Herpetology 14:420-421
24. ^ Barney, R.L.  1922.  Further notes on the natural history and artificial propagation of the diamondback terrapin.  U.S. Bureau of Fisheries.  Economic Circular No. 5, rev.  91-111
25. ^ ^{a b c d} Feinberg, J. A. and R. L. Burke. 2003. Nesting ecology and predation of diamondback terrapins, Malaclemys terrapin, at Gateway National Recreation Area, New York. Journal of Herpetology 37:517-526
26. ^ Hildebrand, S. F. 1928. Review of the experiments on artificial culture of the diamond-back terrapin. Bulletin of the United States Bureau of Fisheries 45:25-70
27. ^ Roosenburg, W. M. 1994. Nesting habitat requirements of the diamondback terrapin: a geographic comparison. Wetlands Journal 6:9-12
28. ^ ^{a b c} Butler, J. A., C. Broadhurst, M. Green and Z. Mullin. 2004. Nesting, nest predation and hatchling emergence of the Carolina diamondback terrapin, Malaclemys terrapin centrata, in Northeastern Florida. American Midland Naturalist 152:145-155
29. ^ Baldwin, J.D., L.A. Latino, B.K. Mealey, G.M. Parks, and M.R.J. Forstner.  2005.  The diamondback terrapin in Florida Bay and the Florida Keys: Insights into Turtle Conservation and Ecology.  Chapter 20 In: In: W. E. Meshaka, Jr., and K. J. Babbitt, eds. Amphibians and Reptiles: status and conservation in Florida. Krieger Publishing Company, Malabar, Florida
30. ^ ^{a b} Baker, P.J., J.P. Costanzo, R. Herlands, R.C. Wood, and R.E. Lee, Jr.  2006.  Inoculative freezing promotes winter survival in hatchling diamondback terrapin, Malaclemys terrapin.  Canadian Journal of Zoology 84:116-124
31. ^ Pilter, R. 1985. Malaclemys terrapin terrapin (Northern diamondback terrapin) Behavior. Herpetological Review 16:82
32. ^ Hildebrand, S. F. 1932. Growth of diamond-back terrapins: size attained, sex ratio and longevity. Zoologica. 9:231-238
33. ^ Yearicks, E. F., R. C. Wood, W . S. Johnson. 1981. Hibernation of the northern diamondback terrapin, Malaclemys terrapin terrapin. Estuaries 4:78-80
34. ^ ^{a b} Coker, R. E. 1931. The diamondback terrapin in North Carolina. In (ed) H. F. Taylor, Survey of Marine Fisheries of North Carolina. University of North Carolina Press, Chapel Hill, NC pp. 219-230
35. ^ Silliman, B. R. and M. D. Bertness. 2002. A Trophic Cascade Regulates Salt Marsh Primary Production. Proceedings of the National Academy of Sciences (USA) 99: 10500-10505
36. ^ ^{a b} Diamondback Terrapin Working Group
37. ^ Ner, S, and R.L. Burke.  2008.  Direct and indirect effects of urbanization on Diamondback terrapins of New York City: Distribution and predation of terrapin nests in a human-modified estuary.  J.C. Mitchell, R.E. Jung, and B. Bartholomew (eds.).  Pp. 107-117 In: Urban Herpetology.  Herpetological Conservation Vol. 3, Society for the Study of Amphibians and Reptiles
38. ^ Dorcas, M. E., J. D. Wilson, J. W. Gibbons. 2007. Crab trapping causes population decline and demographic changes in diamondback terrapins over two decades. Biological Conservation 137:334-340
39. ^ Guillory, V. and P. Prejean. 1998. Effect of a terrapin excluder device on blue crab, Callinectes sapidus, trap catches. Marine Fisheries Review 60:38-40
40. ^ ,Roosenburg, W.M. and J.P. Green. 2000. Impact of a bycatch reduction device on diamondback terrapin and blue crab capture in crab pots. Ecological Applications 10:882-889
41. ^ Seigel, R.A.  1980.  Predation by raccoons on diamondback terrapins, Malaclemys terrapin tequesta.  Journal of Herpetology 14:87-89
42. ^ ^{a b} Hay, W.P.  1917.  Artificial Propagation of the diamondback terrapin.  Department of Commerce Bureau of Fisheries Economic Circular No. 5, revised.  Pages 3-21
43. ^ Draud, M., M. Bossert, and S. Zimnavoda. 2004. Predation on hatchling and juvenile diamondback terrapins (Malaclemys terrapin) by the Norway rat (Rattus norvegicus). Journal of Herpetology 38:467-470
44. ^ Burger, J.  1977.  Determinants of hatching success in diamondback terrapin, Malaclemys terrapin.  American Midland Naturalist 97:444-464
45. ^ Szerlag, S. and S.P. McRobert.  2006.  Road occurrence and mortality of the northern diamondback terrapin.  Applied Herpetology 3:27-37
46. ^ Avissar, N.G.  2006.  Changes in population structure of diamondback terrapins (Malaclemys terrapin terrapin) in a previously surveyed creek in southern New Jersey.  Chelonian Conservation and Biology 5:154-159
47. ^ Holliday, D. K, A. A. Elskus, and W. M. Roosenburg. 2009. Impacts of multiple stressors on growth and metabolic rate of Malaclemys terrapin. Environmental Toxicology and Chemistry 28:338-345
48. ^ Szymanski, S. 2005. Experience with the raising, keeping, and breeding of the diamondback terrapin (Malaclemys terrapin macrospilota). Radiata 14:3-12
49. ^ Turtletrack.org
50. ^ FAA National Wildlife Strike Database
51. ^ Turtles Delay Flights at JFK at the New York Post website
52. ^ Mating turtles shut down runway at JFK at CNN.com
53. ^ Conant, Therese, Diamondback Terrapin, Division of Conservation Education, N.C. Wildlife Resources Commission, http://www.ncwildlife.org/Portals/0/Learning/documents/Profiles/diamondback_091611.pdf, retrieved October 20, 2011 
54. ^ Brown, P. R. 1971. The story of California diamondbacks. Herpetology 5:37-38
55. ^ "Maryland state reptile—diamondback terrapin". Maryland manual on-line: a guide to Maryland government. Maryland State Archives. March 8, 2010. http://www.msa.md.gov/msa/mdmanual/01glance/symbols/html/reptile.html. Retrieved January 21, 2011. 

Bibliography

• Conant, Roger (1975). A Field Guide to Reptiles and Amphibians of Eastern and Central North America (2nd ed.). Boston: Houghton Mifflin. 
• Smith, Hobart Muir; Brody, E.D. (1982). Reptiles of North America, A Guide to Field Identification. New York: Golden Press. 

External links

• Video of a Diamondback Terrapin in Ocean City, NJ, 20 June 2010.
• Jonathan's Diamondback Terrapin World
• Malaclemys Gallery
• Species Malaclemys terrapin at The Reptile Database