Sewer Turtles

Yes, really.

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Turtles are in serious trouble. The IUCN Red List investigated 207 out of ~300 species and arrived at these assessments:

Click to enlarge. This is an unofficial chart of my own construction - for a prior version see the Turtle Conservation Fund. The number of unassessed species is estimated.

95 of the species were last assessed over 10 years ago and are in need of updates (IUCN 2010); this unfortunately suggests the present situation could be worse than illustrated above. It also needs to be pointed out that 'Unassessed' is not necessarily synonymous with 'Least Concern'. For instance, the unassessed Common Snapping Turtle (Chelydra serpentina) is unprotected throughout most of its range and commonly assumed to be in no danger, but in reality requires conservation effort (Ernst and Lovich 2009).


With the situation looking grim, it then comes as a shock that some turtles not only survive in anthropogenically-altered environments, but thrive.

Geoffroy's side-necked turtle (Phrynops geoffroanus) is a moderately-large (max SCL = 35 cm, 13.8") pleurodire which lives east of the Andes in the Orinoco, Amazonas, São Francisco, and Paraná rivers basins ('Turtles of the World', Baldo et al. 2007). Souza (2005), however, interprets the distribution as patternless, and coupled with the diversity of habitat, reiterated a prior suggestion that P. geoffroanus is a complex of sister species. For the sake of not having to construct awkward sentences for the rest of this article, I'll refer to whatever complex may exist as a single species. P. geoffroanus inhabits streams, rivers, lakes and lagoons* with soft bottoms and abundant vegetation ('Turtles of the World', Bonin et al. 2006). The diet is strongly carnivorous, including fish, aquatic insects, snails, and other invertebrates ('Turtles of the World', Bonin et al. 2006). The turtles are shy and flee from humans whom are less than 50 meters (165 feet) away (Bonin et al. 2006). They have been spared from large-scale hunting due to being generally unpalatable, but large numbers are still collected for the pet trade (Bonin et al. 2006). The IUCN does not list the species.


*Making this one of a surprisingly large number of turtles tolerant of saline conditions.

Phrynops geoffroanus from Wikipedia Commons. Phrynops species are commonly called Toad-Head Turtles thanks to their wide dorso-ventrally compressed head.

Souza and Abe (2000) investigated P. geoffroanus populations in Ribeirão Preto Stream, which runs through a town of over half a million and as a result receives an estimated 25-28 tons of sewage per day, as well as dead animals, pesticides, and assorted domestic waste including food scraps, furniture, and tires. The stream is muddy to the degree that at a 30 cm (1 foot) depth, the bottom cannot be seen. Only around 1 kilometer out of the 40 km stretch (0.6 out of 25 miles) is canalized, allowing the grass Panicum maximum to dominate the banks. Up to 75 turtles were present in a 0.1 hectare (0.25 acre) area surveyed; median figures gave a more modest 170-230 turtles/hectare (420-569/acre) or a biomass of 255-345 kg/hectare (1388-1878 lbs/acre). Thus, the 40 km stretch averaging 10 m (33 feet) wide has a population of around 3000 turtles. Surprisingly, neotropical turtles living in lakes may have much higher densities, but in comparison with other streams, the Ribeirão Preto turtles are extremely abundant. It is unfortunate Souza and Abe (2000) did not survey P. geoffroanus in unaltered streams to determine differences in abundance and life history.


So how were the turtles apparently thriving in what essentially amounts to an open-air sewer? Terrestrial prey such as snails and cockroaches were taken, along with carrion and items such as (chicken?) meat and rice from human residences. However, the chironomid Chironomus plumosus was found in 100% of the stomachs surveyed and appears to make up the bulk of the diet. Juvenile turtles - which have a more varied diet than adults - primarily consumed pupal C. plumosus, whereas adult turtles consumed the larvae, suggesting niche partitioning. Due to almost none of the original vegetation remaining in the region, the river otters that would typically prey on the turtles are either locally extinct or scare. Piranhas have been observed to mutilate P. geoffroanus at the stream mouth, but turtles with severe wounds, including damaged or absent forelimbs, can still apparently survive on carrion and/or their small insect prey.


Living in a polluted stream is obviously not without its risks. Souza and Abe (2000) warn that further pollution will eventually kill off C. plumosus and that future canalization will destroy nesting habitat - although it is unlikely the whole 40 km stretch will be so modified. Turtles from the urbanized Anhanduizinho River were found to have a huge mortality rate from roadways (Souza et al. 2008). Chironomid larvae have been observed to live on (and in?) turtles in polluted streams (Marques et al. 2008), but it is not clear what sort of impact this has. Urban P. geoffroanus were found to have a high rate of leech parasitism compared to those from agricultural areas (with no leeches) (Brites and Rantin 2003); another study found that individuals parasitized by leeches and injured by boat strikes showed no sign of disease, although it was suspected they were sub-clinical (Ferronato et al. 2009). Piña et al. (2009) studied P. geoffroanus individuals from the Piracicaba River and found the highest blood serum levels of Cu and Pb for any studied reptile, which was remarkable since there were no obvious clinical or reproductive impacts. The authors warned that the contamination may have been recent enough that any impact, which will likely disrupting reproduction, may eventual appear within a few years.


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For anyone disappointed about a more literal Sewer Turtle not showing up, there's hope. Actinemys marmorata, a vulnerable species, has lost habitat due to urbanization and other anthropic changes, but thrives in sewage treatment plants (Germano 2010). The author suggested the facilities could be used to stock up populations to re-introduce to more natural environments. I wish I have access to this one...






References:


Baldo, D., Martinez, P., Boeris, J. M., Giraudo, A. R. (2007). Reptilia, Chelonii, Chelidae, Phrynops geoffroanus Schweigger, 1812 and Mesoclemmys vanderhaegei (Bour, 1973): Distribution extension, new country record, and new province records in Argentina. Check List 3 (4), 348-352. Available. 


Bonin, F., Devaux, B. Dupré, A. (2006). Turtles of the World. Baltimore, Maryland: John Hopkins University Press. Partially Available.


Brites, V. L. C. and Rantin, F. T. (2003). The Influence of Agricultural and Urban Contamination on Leech Infestation of Freshwater Turtels, Phrynops geoffroanus, taken from Two Areas of the Uberabinha River. Environmental Monitoring and Assessment 96(1-3), 273-281. DOI: 10.1023/B:EMAS.0000031733.98410.3c


Ernst, C. H., and Lovich, J. E. (2009). Turtles of the United States and Canada. John Hopkins University Press: Baltimore, Maryland. ISBN 13:978-0-8018-9121-2

Ernst, C. H., Altenburg, R. G. M., and Barbour, R. W. "Phrynops geoffroanus". Turtles of the World.
http://nlbif.eti.uva.nl/bis/turtles.php?selected=beschrijving&menuentry=soorten&record=Phrynops%20geoffroanus

Ferronato, B. O., Genoy-Puerto, A., Piña, C. I., Souza, F. L., Verdade, L. M., and Matushima, E. R. (2009). Notes on the hematology of free-living Phrynops geoffroanus (Testudines: Chelidae) in polluted rivers of Southeastern Brazil. Zoologia (Curitiba, Impresso) 26(4). doi: 10.1590/S1984-46702009000400027


IUCN 2010. IUCN Red List of Threatened Species. Version 2010.4. www.iucnredlist.org


Germano, D. J. (2010). Ecology of Western Pond Turtles (Actinemys marmorata) at Sewage-Treatment Facilities in the San Joaquin Valley, California. The Southwestern Naturalist 55(1), 89-97.

doi: 10.1894/GC-196.1

Marques, T. S., Ferronato, B. O., Guardia, I., Longo, A. L. B., Trivinho-Strixino, S., Bertoluci, J., and Verdade, L. M. (2008). First record of Chironomus inquinatus larvae Correia, Trivinho-Strixino & Michailova (Diptera, Chironomidae) living on the shell of the side-necked turtle Phrynops geoffroanus Schweigger (Testudines, Chelidae). Biota Neotropica 8(4). doi: 10.1590/S1676-06032008000400019. 

Piña, C. I., Lance, V. A., Ferronato, B. O., Guardia, I., Marques, T. S., and Verdade, L. M. Heavy Metal Contamination in Phrynops geoffroanus (Schweigger, 1812) (Testudines: Chelidae) in a River Basin, Sao Paulo, Brazil. Bulletin of Environmental Contamination and Toxicology 83, 771-775. Available.


Souza, F. L., Raizer, J., da Costa, H. T. M., and Martins, F. I. (2008). Dispersal of Phrynops geoffroanus (Chelidae) in an Urban River in Central Brazil. Chelonian Conservation and Biology 7(2), 257–261. Available.


Souza, F. L. (2005). Geographical distribution patterns of South American side-necked turtles (Chelidae), with emphasis on Brazilian species. Revista Española de Herpetología 19, 33-46. Available.


Souza, F. L., and Abe, A. S. (2000). Feeding ecology, density and biomass of the freshwater turtle, Phrynops geoffroanus, inhabiting a polluted urban river in south-eastern Brazil. Journal of Zoology 252, 437-446. DOI: 10.1111/j.1469-7998.2000.tb01226.x

Turtle Conservation Fund. (2002). A global action plan for conservation of tortoises and freshwater turtles. Strategy and funding prospectus 2002–2007. Washington, DC: Conservation International and

Chelonian Research Foundation. Available.