Terrapene coahuilaCoahuilan box turtle

Geographic Range

Coahuila box turtles (Terrapene coahuila) are native to the southernmost part of the Nearctic region, and endemic to the Cuatro Ciénegas basin in the state of Coahuila. This basin is in an area encompassing 840 km^2. Disjunct turtle populations in this basin total 360 km^2. They are south of Ocampo, north of El Hundido, east of Corral de Barrancas, and west of Monclova. (Brown, 1971; Contreras-Balderas, 1984; Howeth, et al., 2008; Milstead, 1967; Minx, 1996; van Dijk, et al., 2007; Webb, et al., 1963)

Habitat

Coahuila box turtles inhabit wetlands in the Cuatro Ciénegas basin. This area has an average elevation of 720 m. These fully aquatic turtles are found in shallow freshwater areas with slow-moving currents. The main part of the Cuatro Ciénegas basin is marshy, with water depths averaging 0.6 m. Coahuila box turtles tend to move through rivers, lagunas, and pozas. They are commonly found around dense vegetation such as green algae genus Chara, cattails genus Typha, sedges genus Carex, swamp sawgrass Cladium mariscus, desert saltgrass Distichlis stricta, beaked spikerush Eleocharis rostellata. These turtles are found in waters that are, on average, 27 to 29°C. (Dodd, 2002; Howeth, et al., 2008; Iverson, 1982; van Dijk, et al., 2007; Webb, et al., 1963)

  • Aquatic Biomes
  • rivers and streams
  • Average elevation
    720 m
    2362.20 ft
  • Average depth
    0.6 m
    1.97 ft

Physical Description

Coahuila box turtles have rough, bumpy skin and their bodies are covered in rounded shells. They usually have algae growing on the top part of their shells, known as the carapaces. Their skin is brown, black, or grey, typically with tiny black spots. They have a pale-yellow color on their carapaces. They are ectotherms, which means they rely on their environment to regulate their body temperature.

There are a few differences between males and females. Males have brown eyes and females have pale grey eyes. Males have longer and thicker tails as well as bigger shells. Male coahuila box turtles can reach carapace lengths of 16.8 cm, while females average carapace lengths of about 15 cm. Males have a plastral concavity, which helps with mating, but this cavity is absent in females. The difference in shell depth to carapace length is more apparent in females. Another difference is that males have a notched beak, while females do not. Adults on average weigh 568 g.

Hatchlings have an average length of 33.4 mm and an average width of 16.8 mm. They weigh, on average, 5.61 g. Hatchlings are generally a brighter yellow color and they dull with age. (Brinkman, et al., 2013; Legler, 2013; Milstead, 1967; Minx, 1996; Webb, et al., 1963)

  • Sexual Dimorphism
  • male larger
  • sexes shaped differently
  • Average mass
    568 g
    20.02 oz
  • Average length
    15 cm
    5.91 in

Development

Hatchlings have an average length of 33.4 mm and an average width of 16.8 mm. They weigh, on average, 5.61 g. Coahuilan box turtles go through indeterminate growth, meaning they continue to grow throughout their life. Males grow at a faster rate than females. From the ages of 10 to 14, they have the highest rate of growth. After the age of 14, their growth slows. As males grow, their plastron becomes more concave than that of females. (Brown, 1971; Milstead, 1967; Webb, et al., 1963)

Reproduction

Male Coahuilan box turtles pursue potential female mates. The males extend their heads and bump females using their carapaces. Females will often try to swim or run away. Sometimes, multiple males will pursue a single female. Whichever male reaches the female and is able to get on top of her shell first becomes her mate. Mating can occur in or out of the water and will usually last around 30 minutes. Females are able to store sperm from several males during a mating season, and can store it for up to three years. These turtles are polygynandrous, which means that both sexes have multiple mates. (Brown, 1971; Legler, 2013)

Coahuilan box turtles have a mating season that typically spans from September to June, with mating events occuring mostly in spring. Females lay their eggs between May and September and usually their clutches have 2 to 3 eggs. Coahuilan box turtles usually mate in shallow waters instead of on land.

Clutch size has been reported to vary. A single clutch in the wild may have 2 to 7 eggs, averaging 4. In captivity, clutch size ranges from 3.8 to 5.0. They can produce up to three clutches per year, but the total number of eggs per year maxes out at 11. Most females lay fewer than 11 per year; in one study, 33% of females averaged 6.8 eggs for the entire year.

Females lay eggs in soft soil, about 10 cm under vegetation or rocks to protect the eggs. Gestation periods average 70 days (range: 65 to 90 days). As soon as eggs hatch, they are fully independent. When they hatch, their average weight is 5.61 g. Males reach sexual maturity at six years, and females at eight. (Brown, 1971; van Dijk, et al., 2007)

  • Breeding interval
    Breed usually three times a breeding season
  • Breeding season
    September to June
  • Range number of offspring
    2 to 7
  • Average number of offspring
    4
  • Range gestation period
    65 to 90 days
  • Average gestation period
    70 days
  • Range time to independence
    0 to 0 minutes
  • Average age at sexual or reproductive maturity (female)
    8 years
  • Average age at sexual or reproductive maturity (male)
    6 years

Males provide no parental investment, leaving females as soon as they are finished mating. Females carry their eggs internally until they are laid. Female Coahuilan box turtles lay their eggs in a safe space, such as under vegetation or under a log or rock (female pre-hatching parental investment). Once eggs are laid, females leave their nest sites. Newborn Coahuilan box turtles are fully independent. The mortality rate of egg clutches is very high because of the lack of post-laying parental investment. (Minckley, 1966; Webb, et al., 1963)

  • Parental Investment
  • pre-hatching/birth
    • protecting
      • female

Lifespan/Longevity

The longest recorded lifespan of Coahuilan box turtles living in captivity is 18.8 years, whereas the longest known lifespan in the wild is 9.4 years. This shorter lifespan in the wild is due to predation and habitat loss. The expected lifespan in the wild is 8.7 years. The expected lifespan in captivity is 17.4 years, with most living at least 5 years in captivity. (van Dijk, et al., 2007)

  • Average lifespan
    Status: wild
    9.4 years
  • Average lifespan
    Status: captivity
    18.8 years
  • Average lifespan
    Status: wild
    8.7 years
  • Typical lifespan
    Status: captivity
    5 (low) years
  • Average lifespan
    Status: captivity
    17.4 years

Behavior

Coahuilan box turtles tend to bury themselves in mud to hide or to keep their body temperatures stable. These turtles usually stay in the general area in which they hatched. There is typically no territorial social hierarchy within an area with one exception: brighter colored males tend to be territorial. These males may violently combat each other to protect their territories. They will ram and bite other turtles.

Coahulian box turtles are mostly aquatic, spending 90% of their time in the water. They tend to be less active in the winter. When temperatures drop, they bury themselves under the mud at a depth of 0.15 m. Their typical stable body temperature ranges from 20 to 25°C. From December to February, they bury themselves at night and are less active during the day. They are considered to be social and colonial because they live in groups. (Brown, 1971; Dodd, 2002; Milstead, 1967; Webb, et al., 1963)

  • Range territory size
    20 to 30 m^2
  • Average territory size
    25.6 m^2

Home Range

The density of Coahuilan box turtle populations depends on food availability. The more food there is, the higher the population density. Their strong sense of smell helps them search for food in their territory. They typically live in shallow waters, such as streams, so they can get in and out of the water easier. Their territories are anywhere from 20 to 30 m^2 but average 25.6 m^2. (Brown, 1971; Iverson, 1989)

Communication and Perception

Coahuilan box turtles use their vision during the day and at night. They do not have external ears, but they have an inner ear system that can hear low-frequency sounds from 50 to 1,500 Hz. These sounds allow them to “hear” water vibrations. Their inner ear structures are mainly used for balance more so than for hearing. Their sense of smell helps them find food sources and other members of their species through pheromones. They are also able to vocally communicate by making small screeching noises. Their vision helps them to look for mates as well as predators. (Brinkman, et al., 2013; Dodd, 2002; Legler, 2013; Milstead, 1967; Minx, 1996)

Food Habits

Coahuilan box turtles are opportunistic omnivores. Brown (1971) found that they have diets consisting of 45.6% plant matter and 50.7% aquatic insects. The types of insects they consume include fly larvae, beetles, and dragonfly nymphs. The plant types they eat are green algae (genus Chara) and spikerush (Eleocharis rostella). They also consume mushrooms. Less than 1% of their diet consists of spiders, fish, and crustaceans. There are also seasonal differences in their diets. (Brinkman, et al., 2013; Brown, 1971)

  • Animal Foods
  • fish
  • insects
  • terrestrial non-insect arthropods
  • terrestrial worms
  • aquatic or marine worms
  • aquatic crustaceans
  • Plant Foods
  • algae
  • Other Foods
  • fungus

Predation

Coahuilan box turtle egg predators include raccoons (Procyon lotor) and copperheads (Agkistrodon contortrix). Copperheads will swallow eggs whole if they find them.

Raccoons also prey on Coahuilan box turtles as hatchlings and adults. In order to protect themselves, these turtles have a hard and dull shell that they are able to retreat into if they feel threatened. This behavior is known as the freezing state. The dark colors on their shells help them blend in with mud or logs in their environment. They can escape to the water if a potential predator is on land. Virginia opossums (Didelphis virginiana) and striped skunks (Mephitis mephitis) are also predators of Coahuilan box turtles.

As Coahuilan box turtles age, their shells become thicker and harder; this helps protect them from bigger predators. They have a joint called the plastral joint that helps them retreat fully into their shells; they are not able to fully hide in their shells until they are about 5 cm in size.

Coyotes (Canis latrans) are another potential predator, as turtles have been discovered with teeth marks on their carapaces or with limbs missing. (Brown, 1971; Legler, 2013)

  • Anti-predator Adaptations
  • cryptic

Ecosystem Roles

Coahuilan box turtles often dig themselves into the soil to hide or to keep their body temperatures stable, indirectly aerating the soil. Fluke parasites include Telorchis, and monogenean parasites include Polystomoides and unidentified members of the family Oxyuroidae. These box turtles are omnivores, eating insects and plants, and fall prey to a number of mammals and snakes. (Guajardo-Martinez, 1984; Minx, 1996)

Commensal/Parasitic Species

Economic Importance for Humans: Positive

Coahuilan box turtles are sold in the pet trade. Turtle shells are also often sold for money because of their ornate coloring. Coahuilan box turtles, along with other species of box turtles, are the most common turtle to have as a pet, due to them being a smaller size. (Milstead, 1967)

  • Positive Impacts
  • pet trade
  • body parts are source of valuable material

Economic Importance for Humans: Negative

Turtles, such as Coahuilan box turtles, can carry salmonella bacteria. These bacteria can be transmitted to humans. If humans come in direct contact with an infected turtle and then do not wash their hands, they can contract salmonella. (Parlin, et al., 2018)

Conservation Status

Coahuilan box turtles are listed as "Endangered" on the IUCN Red List and the US Federal List. They are an Appendix I species on the CITES list. Appendix I means that commercial trade of this species is banned. Occasional trade could occur if the purpose is purely scientific; even then, a permit is required. These turtles are not listed on the State of Michigan List.

The main reason for Coahuilan box turtle population declines is the loss of their wetland habitats - more specifically, their marshes are drying up. Now-dry marshes are inadequate in sustaining aquatic life. Because these turtles are mostly found in shallow waters, drying marshes make the risk of habitat loss much more prominent. Shallow streams and basins can dry out much faster, leaving Coahuilan box turtles with less habitat. The drop in the water basin prevents the growth of cattails (genus Typha) and sedges (genus Carex). The turtles also have a limit in their geographic range because they are only found in one small basin. van Dijk et al. (2007) recounted 2002 surveys, in which historical, 1960s locations were resurveyed; the turtles were absent from approximately 40% of the surveyed sites in 2002.

Additional threats include road-building, the addition of railroads and pipelines throughout the Cuatro Ciénegas basin, and development to encourage ecotourism. Agricultural use of this basin is increasing, as well. Coahuilan box turtles have been found as roadkill and have also suffered mortality due to fires in the area. Demand for this species in the pet trade also can be a threat.

The National Water Commission of Mexico is putting water pipelines into water basins in the habitats of Coahuilan box turtles. This act seems to be one of the main reasons for the drop in the water table. From 1970 to 1972, scientists started noticing a decrease in Coahuilan box turtle populations. Conservation efforts have been focused on reducing habitat loss. Scientists have also been breeding them in several zoos to help assure colonies in the future. These captive colonies also seem to have removed the pressures from the pet trade, as well.

In 1994, the entire Cuatro Ciénegas basin was designated an IUCN Category IV location. With this designation, the goal is to conserve the habitats and rare species that use them. This does not, however, prevent further development, and conservationists must step in to mitigate development. (Brown, 1971; Howeth, et al., 2008; van Dijk, et al., 2007)

Contributors

McKenzie Harpine (author), Radford University, Lauren Burroughs (editor), Radford University, Layne DiBuono (editor), Radford University, Lindsey Lee (editor), Radford University, Karen Powers (editor), Radford University, Galen Burrell (editor).

Glossary

Nearctic

living in the Nearctic biogeographic province, the northern part of the New World. This includes Greenland, the Canadian Arctic islands, and all of the North American as far south as the highlands of central Mexico.

World Map

acoustic

uses sound to communicate

bilateral symmetry

having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

carnivore

an animal that mainly eats meat

causes disease in humans

an animal which directly causes disease in humans. For example, diseases caused by infection of filarial nematodes (elephantiasis and river blindness).

chemical

uses smells or other chemicals to communicate

colonial

used loosely to describe any group of organisms living together or in close proximity to each other - for example nesting shorebirds that live in large colonies. More specifically refers to a group of organisms in which members act as specialized subunits (a continuous, modular society) - as in clonal organisms.

cryptic

having markings, coloration, shapes, or other features that cause an animal to be camouflaged in its natural environment; being difficult to see or otherwise detect.

ectothermic

animals which must use heat acquired from the environment and behavioral adaptations to regulate body temperature

fertilization

union of egg and spermatozoan

freshwater

mainly lives in water that is not salty.

herbivore

An animal that eats mainly plants or parts of plants.

indeterminate growth

Animals with indeterminate growth continue to grow throughout their lives.

induced ovulation

ovulation is stimulated by the act of copulation (does not occur spontaneously)

insectivore

An animal that eats mainly insects or spiders.

iteroparous

offspring are produced in more than one group (litters, clutches, etc.) and across multiple seasons (or other periods hospitable to reproduction). Iteroparous animals must, by definition, survive over multiple seasons (or periodic condition changes).

marsh

marshes are wetland areas often dominated by grasses and reeds.

motile

having the capacity to move from one place to another.

natatorial

specialized for swimming

native range

the area in which the animal is naturally found, the region in which it is endemic.

omnivore

an animal that mainly eats all kinds of things, including plants and animals

oviparous

reproduction in which eggs are released by the female; development of offspring occurs outside the mother's body.

pet trade

the business of buying and selling animals for people to keep in their homes as pets.

pheromones

chemicals released into air or water that are detected by and responded to by other animals of the same species

piscivore

an animal that mainly eats fish

planktivore

an animal that mainly eats plankton

polygynandrous

the kind of polygamy in which a female pairs with several males, each of which also pairs with several different females.

seasonal breeding

breeding is confined to a particular season

sedentary

remains in the same area

sexual

reproduction that includes combining the genetic contribution of two individuals, a male and a female

social

associates with others of its species; forms social groups.

soil aeration

digs and breaks up soil so air and water can get in

swamp

a wetland area that may be permanently or intermittently covered in water, often dominated by woody vegetation.

ultrasound

uses sound above the range of human hearing for either navigation or communication or both

vibrations

movements of a hard surface that are produced by animals as signals to others

References

Brinkman, D., P. Holroyd, J. Gardner. 2013. Morphological variation in the carapace and plastron of Terrapene coahuila Schmidt and Owens 1944. Pp. 535-566 in R Burroughs, C Bell, D Hendrickson, eds. Fossil European Sea Turtles: A Historical Perspective. New York, New York: Springer Science+Business Media Dordrecht.

Brown, W. 1971. Morphometrics of Terrapene coahuila (Chelonia, Emydidae), with comments on its evolutionary status. The Southwestern Naturalist, 16/2: 171-184.

Contreras-Balderas, S. 1984. Environmental impacts in Cuatro Cienegas, Coahuila, Mexico: A commentary. Journal of the Arizona-Nevada Academy of Science, 19/1: 85-88.

Dodd, K. 2002. North American Box Turtles. Norman, Oklahoma: University of Oklahoma Press.

Guajardo-Martinez, G. 1984. Preliminary survey of parasites of Cuatro Cienegas Coahuila, Mexico. Journal of the Arizona-Nevada Academy of Science, 19/1: 81-83.

Howeth, J., S. McGaugh, D. Hendrickson. 2008. Contrasting demographic and genetic estimates of dispersal in the endangered Coahuilan box turtle: A contemporary approach to conservation. Molecular Ecology, 17/19: 4209-4221.

Iverson, J. 1982. Biomass in turtle populations: A neglected subject. Oecologia, 55/1: 69-76.

Iverson, P. 1989. Tortoises and Freshwater Turtles: An Action Plan for Their Conservation. Broadview, Illinois: Kelvyn Press.

Legler, J. 2013. Turtles of Mexico: Land and Freshwater Forms. University of California Press: Berkeley, California.

Milstead, W. 1967. Fossil box turtles (Terrapene) from central North America, and box turtles of eastern Mexico. Copeia, 12/1: 168-179.

Milstead, W., D. Tinkle. 1967. Terrapene of western Mexico, with comments on the species groups in the genus. Copeia, 12/1: 180-187.

Minckley, W. 1966. Coyote predation on aquatic turtles. Journal of Mammalogy, 47/1: 137.

Minx, P. 1996. Phylogenetic relationships among the box turtles, genus Terrapene. Herpetologica, 52/4: 584-597.

Parlin, A., J. Nardone, J. Dougherty, M. Rebein, K. Safi, P. Schaeffer. 2018. Activity and movement of free-living box turtles are largely independent of ambient and thermal conditions. Movement Ecology, 6/1: 1-9.

Webb, R., W. Minckley, J. Craddock. 1963. Remarks on the Coahuilan box turtle, Terrapene coahuila (Testudines, Emydidae). The Southwestern Naturalist, 8/2: 89-99.

van Dijk, P., O. Flores-Villela, J. Howeth. 2007. "Terrapene coahuila (errata version published in 2016)." (On-line). The IUCN Red List of Threatened Species 2007: e.T21642A97428806. Accessed February 06, 2019 at http://dx.doi.org/10.2305/IUCN.UK.2007.RLTS.T21642A9304337.en.