Many turtle populations make or made significant contributions to the biomass of their environment, as first noted by Iverson Turtle standing crop biomass is generally very high in comparison with other vertebrates figure 1 , often surpassing that of all other reptiles.
Biomass values for turtles are typically at least an order of magnitude higher than those of other reptiles and similar to those of large schools of fish. The high biomass of turtles is related largely to the high population densities they are capable of achieving.
For example, two centuries ago, sea turtles were estimated to number in the tens of millions in the Caribbean Sea alone. More recently, their numbers were estimated in the tens of thousands Jackson et al. Maximum biomass estimates for several major vertebrate assemblages represented with generic silhouettes , subdivided into dietary groups, such as herbivorous, omnivorous, and carnivorous species.
The top image is an inset displaying biomass estimates that were less than 10 kilograms per hectare kg per ha and difficult to display on the bottom image. All estimates are from Iverson , except for omnivorous turtles Congdon et al. The highest accepted biomass for an aquatic turtle is kilograms per hectare kg per ha; Congdon et al. At a minimum of kg per ha, the Aldabra tortoise Aldabrachelys gigantea achieves the highest undisputed standing crop biomass for tortoises Coe et al.
Aquatic species such as the Mexican mud turtle Kinosternon integrum and the Llanos sideneck turtle Podocnemis vogli are reported to achieve standing crop biomasses of kg per ha and 15, kg per ha, respectively, although these values represent temporary aggregations or exaggerations Iverson Mass nesting arribadas of sea turtles are classic examples of temporary aggregations and exceptional concentration of biomass on nesting beaches Ernst and Lovich The numbers reported above are truly remarkable biomass figures, surpassing even the maximum value kg per ha reported by Coe and colleagues for herds of large herbivores on the African plains!
At these historically high densities and biomasses, turtles had a major impact in their ecosystems, especially as consumers but also as prey. Therefore, extirpation or population declines of turtles can result in alteration of ecosystem structure and function as described in the sections below.
Turtles also contribute substantially to secondary productivity in some ecosystems. Estimates of annual biomass production growth of individuals plus egg production range from 7. As a consequence of their overall secondary productivity and biomass, turtles have a disproportionate influence on processes in many wetland and terrestrial environments, as described further in the sections below.
Even more diverse turtle communities exist in biodiversity hotspots, such as the southeastern United States Buhlmann et al. What conditions allow some turtle species to attain such extraordinarily high standing crop biomasses? In a review of the role of desert vertebrates in the ecosystem, Brown noted several factors that contribute to the diversity and high biomass of desert reptiles. First, habitats that could support only a small number of endothermic, or warm-blooded, birds or mammals can support a much larger population of reptiles, such as turtles.
The available data suggest that reptiles are at least an order of magnitude more energetically efficient than endotherms, converting a higher proportion of assimilated energy into biomass and making it available to predators at higher trophic levels Vitt and Caldwell Herbivorous turtles may even expend energy at a slower rate for their body mass than some other herbivorous reptiles Jodice et al.
Second, reptiles can become dormant during long periods of low resource availability. Therefore, the abundance of some desert reptiles can be partially attributed to low productivity in the desert ecosystem that favors organisms with low metabolic requirements and the ability to become dormant during lean times.
Endotherms that lack the ability to remain inactive under adverse conditions must migrate to other areas. All of the Aldabra tortoise's close relatives i.
Unfortunately, most of these species have been driven to extinction Turtle Extinctions Working Group Similar to the ecosystem effects of Aldabra tortoises, these extinct tortoises modified the landscape through heavy grazing and soil disturbance terraforming but also through seed dispersal of endangered plants Hansen et al. Without the ecosystem services provided by these tortoise species, many of these island ecosystems have become degraded.
The history of tortoises on these and other islands provides a cautionary tale of how important turtles can be in their ecosystems. Because turtles contribute a significant portion of the overall biomass to an ecosystem, turtles are strongly linked to ecosystem health and function through resource subsidies, mineral cycling, top-down food web effects, seed dispersal and germination enhancement, and bioturbation.
All of these topics are discussed in the following sections. Production of organic matter in living organisms requires harvesting food resources, and turtles certainly play a role in the energy flow of their immediate and surrounding environment. The dried contents of turtle eggs are almost entirely protein and lipids Booth A detailed example of this energy transfer from marine to terrestrial environments was provided for nesting sea turtles on a beach in Florida Bouchard and Bjorndal Loggerhead sea turtles Caretta caretta deposited 14, nests, with an estimated 1.
On average, each nest transferred grams g of organic matter, 18, kilojoules kJ of energy, g of lipids, 72 g of nitrogen, and 6. In their review, Bouchard and Bjorndal concluded that the energy and nutrients introduced by turtles in this fashion are comparable to the quantities moved by other cross-ecosystem transport systems involving birds. By introducing nutrients into beach ecosystems, sea turtles may help maintain stable dune systems that are critical to their reproductive success.
In another example of nutrient transfer, American beach grass Ammophila breviligulata , which stabilizes dune nesting habitat for turtles, is capable of absorbing nutrients directly from the eggs of diamond-backed terrapin Malaclemys terrapin nests Stegman et al. In addition, nutrients from the eggs in sea turtle nests influence the beach meiofauna, especially nematodes Diane et al.
Energy in nutrients transferred from marine to terrestrial environments by nesting sea turtles is now greatly diminished with worldwide reductions in sea turtle populations. This figure shows the projected transfer of energy from 14, loggerhead sea turtle Caretta caretta nests with an estimated 1.
Note that only about one quarter of total energy transferred to beaches returned to the marine environment in hatchlings. The second reason supporting the importance of turtles in energy flow relates to their role as consumers, particularly as scavengers. Thompson studied a riverine community of three turtle species in Australia. Making a variety of assumptions on population densities and distribution of the species, he estimated their standing crop biomass as Additional information on the role of turtles as consumers is summarized in the section on trophic status.
The scavenging value of turtles even has profound importance in the cleanup of rivers polluted by humans Sinha The Ganges River in India is badly polluted with, among other things, the partially cremated corpses of humans on the ghats , or stairs, along the river. In in Varanasi alone, officials estimated that 20,—30, human bodies were cremated annually.
About 24, turtles were raised and released into the Ganges since the program was initiated in Anderson It is estimated that a fully grown turtle can eat about one pound of meat per day. Whether turtles are making a difference is subject to local debate.
Mineral cycling involves the transfer of life-essential nutrients and elements from the environment to organisms and back to the environment, from birth to death. However, the role of turtles in calcium and phosphorus cycling is virtually unknown. Radioecological studies with an isotope of strontium 90 Sr , a bone-seeking calcium analog, provide a glimpse of the potential role turtles play in the calcium cycle Hinton and Scott These researchers found that turtles are similar to other organisms in their ability to concentrate 90 Sr, but herbivorous species such as the gopher tortoise Gopherus polyphemus may accumulate higher concentrations than other turtles do because of their trophic position.
This is because levels of 90 Sr tend to be higher in vegetation than at higher trophic levels occupied by omnivorous or carnivorous turtles. However, a significant difference between turtles and other aquatic organisms is the concentration ratio between the animal and its environment.
Concentration ratios are useful for comparing organisms because they normalize for variations in the radionuclide concentration of the environment e. Concentration ratios for turtles are very high relative to other organisms, showing their propensity to accumulate 90 Sr as a calcium analog in the periodic table.
High concentration ratios can be associated with low availability of the nutrient element analog calcium , longevity, high assimilation, long retention time, or some combination thereof. The long lifespan of many turtles Gibbons , their high percentage of slowly developing bone, and their high assimilation rates make them a potentially important link in the calcium cycle of some ecosystems Hinton and Scott These episodes, known as geophagy , have only been observed in sexually mature females during the nesting season, a time when females may experience calcium stress due to egg production Marlow and Tollestrup Osteophagy , or the consumption of bones, has also been observed in G.
A bizarre case of mineral cycling and subsequent disease transmission among tortoises and ungulates in Ethiopia was reported by Mengiste and colleagues Bovine botulism in southern Africa has long been associated with the consumption of dead tortoises by cattle Fourie Mengiste and his colleagues suggested that soil in the affected area was deficient in phosphorus, forcing cattle to consume dead tortoises as a source of that element, ultimately infecting them with botulism bacteria that originated in the rotting carcasses.
The role of turtles in mineral cycles also makes them excellent environmental indicators for chemicals of concern to human health. Because of the long lives and relatively high trophic position of omnivorous and carnivorous species in aquatic environments, they have the potential to accumulate significant levels of some pollutants e.
North American turtles have been shown to be effective for monitoring mercury contamination Golet and Haines and even radioactivity in aquatic systems Hinton and Scott The trophic position of an organism in a food web can have important direct effects on community structure through top-down or bottom-up cascades.
As a group, turtles occupy trophic positions as herbivores, carnivores, and omnivores and play important, even dominant, roles Hastings et al. Perusal of the feeding habits of the turtle species recognized at the time by Ernst and Barbour shows that the natural diets of about species are known with some degree of confidence. Of these, roughly a third each are omnivores, carnivores, and herbivores.
Some species are highly specialized, and others are more opportunistic, each playing a role in their trophic niche. The leatherback sea turtle Dermochelys coriacea feeds almost exclusively on jellyfish. This is a niche occupied by few other large marine predators, with the exception of the ocean sunfish Mola mola ; Ernst and Lovich The hawksbill turtle Eretmochelys imbricata also has a specialized diet, feeding almost exclusively on sponges Meylan In contrast, many other species, such as adult slider turtles, are opportunistic omnivores with a very catholic diet Parmenter and Avery In turn, turtles and their eggs are prey to an incredibly diverse array of predators including both invertebrates and vertebrates see Ernst and Lovich for numerous examples.
Evidence of turtles as prey species dates to at least the lower Cretaceous of Australia, when prehistoric ichthyosaurs Platypterygius longmani consumed this food source Kear et al. Aldabra giant tortoise populations on Aldabra Atoll form what is potentially the largest tortoise concentration on Earth in perhaps the only terrestrial ecosystem dominated by a reptilian herbivore Stoddart and Serge Tortoises of average mass 20—30 kg on Aldabra may eat as much as 79 kg of forage per year Coe et al.
With an estimated population of , animals in The environmental impact of that many tortoises results in landscape-level changes, including modification of the plant community from coastal, maritime, scrub-tussock vegetation to one of short, turf grassland Hnatiuk et al.
Another tortoise species endemic to Madagascar, the radiated tortoise Astrochelys radiata , formerly achieved estimated population densities of up to per km 2 Leuteritz et al. The loss of turtles from an ecosystem can lead to significant environmental consequences. For example, populations of small estuarine diamond-backed terrapins Malaclemys terrapin are members of a guild of top-down predators that regulate grazing species, such as salt-marsh periwinkle snails Littorina irrorata.
Without the effect of these predators, periwinkle snails can convert productive grasslands in salt marshes to barren mudflats in 8 months under experimental conditions Silliman and Bertness Other descriptions of the effects that turtles have on ecosystems are described in the section on ecosystem restoration. Predators e. Turtles assume all the traditional trophic positions of consumers; therefore, the removal or extirpation of turtles could have profound effects on the structure and function of terrestrial, freshwater, and marine communities.
For instance, the removal or diminished role of turtles in the wild can be far-reaching and create trophic cascades, altered biomass structure, loss of community function, and invasive species resilience, all of which are critical to maintaining healthy ecosystems. Unfortunately, empirical data reporting these top-down effects caused by turtles are scarce in the scientific literature. The top-down effects of sea turtles on seagrass meadows and coral reefs are relatively well known.
Green turtles Chelonia mydas can alter the physical structure and flowering of seagrass meadows by heavy, sustained grazing Lal et al. In addition, green turtles directly alter the vegetation community composition of the seagrass meadows, which indirectly diminishes prey refugia and recruitment see Lal et al.
Furthermore, hawksbill turtles Eretmochelys imbricate often provide top-down indirect effects on coral reef ecosystems.
These sea turtles directly consume sponges, which are competitively superior to coral, thus reducing competition for space within the coral reef and increasing coral species richness and health. The roles of sea turtles are now greatly diminished because of years of global overexploitation Jackson et al. As freshwater predators, aquatic and semiaquatic freshwater turtles may have strong direct effects on prey abundance but also indirect effects that shape communities as well.
For example, the presence of a common freshwater species, the slider turtle, significantly altered environmental characteristics e. In addition, the increased nutrient load associated with turtle presence in the experimental ponds drove a significant increase in invertebrate abundance and density in the system. Similarly, in ephemeral freshwater ponds, increased nutrient influx provided by the common snapping turtle Chelydra serpentina positively affected the lowest trophic position of the food web, phytoplankton Wilbur In aquatic ecosystems, in which turtles occupy the highest trophic position, as apex predators, their long-term or temporary presence can have strong effects on ecosystem dynamics.
For example, in freshwater mesocosms, common snapping turtles directly altered amphibian community compositions and body condition of prey Garig Altered dynamics of lower trophic levels in these mesocosms exposed to turtles were documented over several weeks, even though the turtles were introduced and removed over a 4-day period, demonstrating short- and potentially long-term e.
Consequently, the extirpation or a diminished role of turtles in a freshwater community could have cascading effects at multiple trophic levels and environmental conditions, shifting short- and long-term ecosystem processes. The majority of temperate and tropical woody plants depend on vertebrates for seed dispersal Howe and Smallwood Therefore, this ecosystem service is vital for maintenance of terrestrial ecosystems globally Wang and Smith Turtles have long been overlooked as important seed dispersers; however, several species have been identified as important agents for seed dispersal and germination enhancement of plants.
Braun and Brooks fed wild fruits to captive eastern box turtles Terrapene carolina to determine germination potential. Eleven of 15 species germinated, and 5 had higher germination potential following digestion. In fact, the eastern box turtle is the only known seed dispersal agent for the mayapple Podophyllum peltatum.
Mayapple seeds eaten by this turtle species germinate faster and have a higher probability of success than noningested seeds Rust and Roth Fecal samples of the leopard tortoise Geochelone pardalis in South Africa contained 75 plant species belonging to 26 families.
Viable seeds were observed for seven plant families on the basis of germination trials, but data were not presented to indicate enhanced germination following digestion Milton The majority of seedlings that germinated were grasses. Similar dispersal and germination enhancement capabilities were documented for the Greek tortoise Testudo graeca ; Cobo and Andreu , with 6.
Rose and Judd conducted one of the most thorough analyses of germination enhancement in a tortoise. Seeds placed in a solution of hydrochloric acid with a pH of 3.
The authors suggested that seeds passed in fecal pellets have a selective advantage in that they germinate quickly in the presence of water and have a nitrogen source for early development.
Another interesting example of seed dispersal—and, presumably, germination enhancement—involves the declining tambalacoque trees Sideroxylon sessiliflorum and S. The extinction of the dodo bird Raphus cucullatus has been suggested as an explanation for the declining trees, because dodos may have abraded the thick endocarp of the seed and facilitated germination.
However, Iverson provided sufficient evidence to suggest that the extinct tortoises ate the seeds and facilitated germination. Similar scenarios may have existed between extinct tortoises and an extant baobab tree Adansonia rubrostipa in Madagascar Andriantsaralaza et al.
Twenty-eight species of grasses, herbs, and woody plants have been documented to germinate from the feces of Aldabra giant tortoises Hnatiuk The seed dispersal and germination enhancement abilities of turtles and other members of the seed-eating guild can have a strong influence in the composition of plant communities they occupy. The habit of the black wood turtle Rhinoclemmys funerea to emerge and defecate on river banks may contribute to the establishment of certain riparian plant species, and the foraging activity of the furrowed wood turtle Rhinoclemmys annulata may contribute to the distinctive flora of treefall areas in the forest Moll and Jansen Similar roles can be envisioned for other species of turtles such as alligator snapping turtles Macrochelys temminckii that feed on the fruits of riverine plant species including acorns Elbers and Moll Digging and burrowing animals, including some tortoises, can have an enormous impact on soil processes including its formation, function, and maintenance.
Animals living in the soil body and intimately associated with it are considered part of the soil, and animals living above the soil make contributions to it Hole In a major review of the effects of animals on soil, Hole identified 12 effects: mounding, mixing, forming voids, back-filling voids, forming and destroying peds soil particles , regulating soil erosion, regulating movement of air and water, regulating plant litter, regulating animal litter, regulating nutrient cycling, regulating biota, and producing special constituents.
Turtles have a role in many of these processes. Some turtles are prodigious burrowers, including Agassiz's desert tortoise and the gopher tortoise. Their impressive burrows, sometimes over 10 meters m in length for gopher tortoises, qualify them for the title of ecosystem engineers because of the impact of burrows on soil layers, water and gas diffusion, and surrounding vegetation.
The excavated mounds in front of burrows contribute to environmental heterogeneity and increased plant species diversity Kaczor and Hartnett In addition, their burrows are used by over other species figure 3 as symbiotic occupants Johnson et al.
Given the high densities these tortoises previously achieved and their habit of using more than one burrow per year, they exerted a strong influence on soils before their populations declined Ernst and Lovich Catano and Stout concluded that gopher tortoises were keystone species and ecosystem engineers by virtue of their burrowing habit.
Gopher tortoise Gopherus polyphemus burrows provide shelter for over vertebrates and invertebrates Johnson et al. Included are burrowing owls Athene cunicularia , various species of lizards, gopher frogs Lithobates capito , red foxes Vulpes vulpes , bobcats Lynx rufus , rodents, rabbits, and snakes, including other declining species, such as eastern indigo snakes Drymarchon couperi and diamondback rattlesnakes Crotalus adamanteus.
An example of the degree of soil disturbance that turtles are capable of achieving is shown in nesting green turtles and loggerhead sea turtles on Heron Island, Australia.
These species exert a profound effect on the fringing vegetation of the island. Thousands of turtles nest during the period from October to March, affecting a swath of coastal vegetation averaging A single turtle can affect an area of over 2 m in diameter Rogers Loggerhead sea turtles in Moreton Bay, Australia, use an unusual foraging strategy that causes considerable disturbance to the seafloor Preen To gain access to buried food sources, loggerhead sea turtles dig pits up to 1.
Turtles advance through the sediment, eroding the quarry face of the excavation with their front flippers and feeding on invertebrates that are dislocated from their hiding places. Including the lateral sedimentation of spoils from the excavation activity, 8. Preen concluded that foraging disturbance by loggerhead sea turtles had a substantial impact on the biomass, species composition, and dynamics of some seagrass beds and associated fauna. A similar conclusion was reported by Lazar and colleagues for loggerhead sea turtles in the neritic zone of the northern Adriatic Sea.
They stated that foraging behavior by loggerhead sea turtles actively reworks marine sediments and increases the rate of mollusk shell disintegration.
They conservatively estimated that loggerhead sea turtles there bioturbate about 33 metric tons of mollusk shells per year. In addition, infaunal mining of invertebrate prey by loggerhead sea turtles may be important in nutrient transfer in marine ecosystems.
One of the benefits of understanding the functional role of organisms is the potential ability to harness ecological services they provide. For example, failure to recognize the ecological role of turtles in maintaining habitat heterogeneity has resulted in losses of certain habitat features, such as small wetlands, and the extinction or decline of some plant species Iverson , Griffiths et al.
Consider the value of turtles in cleaning rivers polluted with corpses in India or scavenging for carrion, as was discussed previously.
The ability of some turtles to thrive in polluted waterways Moll makes them a tangible benefit. Hundreds of thousands of tortoises were removed from the islands over the centuries MacFarland et al. Since then, tortoise reintroduction efforts are having a positive effect on a rare keystone species of tree-like cactus Opuntia megasperma var.
The selection of tortoise species is important for the success of reintroduction for ecological restoration of some plant species, because not all tortoise species have the same effect or food preferences Hunter et al.
It also eats aquatic plants, snakes, frogs, fish, worms, clams, crayfish and other turtles. All turtles lay eggs. They find a place on land to lay their eggs, dig a nest into the sand or dirt and then walk away. No species of turtle nurtures their young. Turtles reach the age to mate at different times. Some species fight for the right to mate with a female, while others seduce her with a mating ritual. To mate, male and female turtles intertwine their tails so that their shell openings line up perfectly.
Sea turtles travel from the ocean to lay eggs on beaches. Usually, sea turtles lay around eggs in a nest, though the flatback turtle only lays 50 at a time. The temperature of the sand affects the sex of the turtle. The perfect beach temperature produces an equal number of male and female offspring.
Due to rising temperatures, too many sea turtle females are being born, contributing to the decline in species numbers, according to the Sea Turtle Conservancy. According to the International Union for Conservation of Nature IUCN , many turtle species are listed as threatened, endangered or critically endangered. For example, the ploughshare tortoise and radiated tortoise are estimated to be extinct in the next 45 years. The earliest known turtle fossils are from the Triassic Period, about million years ago.
Anatomically, they are nearly identical to modern turtles. Sea turtles have been around for million years , according to a recent analysis. The now-extinct Desmatochelys padillai turtle skeleton was found in Villa de Leyva, Colombia, and is 25 million years older than the Santanachelys gaffneyi turtle from Brazil that previously held the record for the world's oldest sea turtle fossil.
A pair of Russian tortoises went into space. The leatherback was listed in the United States under the Endangered Species Act as endangered in Leatherbacks are seriously declining at all major nesting beaches throughout the Pacific. In contrast, there has been a recent increase in leatherback nesting on the central and south eastern coast of Florida. It is a solitary nester, and thus, population trends or estimates are difficult to determine. The decline of nesting populations is accepted by most researchers.
In , the only known apparently stable populations were in Yemen, northeastern Australia, the Red Sea, and Oman. Although they are found in U. While hawksbills nest on beaches throughout the Caribbean, they are no longer found anywhere in large numbers. In , a Mexican architect filmed an estimated 42, ridleys nesting at Rancho Nuevo in one day.
During , only 1, ridley nests were laid at Rancho Nuevo. Recent good news is that the nesting at Rancho Nuevo seems to be increasing with over 7, nests recorded in ! The increase can be attributed to two primary factors: full protection of nesting females and their nests in Mexico, and the requirement to use turtle excluder devices TEDs in shrimp trawls both in the U. The western North Atlantic Surinam and adjacent areas nesting population has declined more than 80 percent since Declines are also documented for Playa Nancite, Costa Rica, however other nesting populations along the Pacific coast of Mexico and Costa Rica appear stable or increasing.
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