Resumen de Ecología poblacional de tortugas de agua dulce en áreas urbanas del sur de brasil
1. Introducción o motivación de la tesis The urban areas still lodging wild species through forest remnants, such as parks, riparian vegetation, and squares (e.g. Slabbekoorn & Peet 2003; Ryan et al. 2014; Viana et al. 2017). Birds, mammals, amphibians and reptiles are some of the animals that can persist at these areas (Hunt et al. 2013; Villaseñor et al. 2017; Beaugeard et al. 2019; Santini et al. 2019). Even lodging biodiversity, urban environments suffer with some impacts related to fragmentation and degradation of riparian vegetation, channeling of water bodies, and as a consequence, the silting of rivers. Other regular disturbance are regarding to urban noise, recreational activities (e.g. fishing), wild-feeding, and introduction of alien species (Slabbekoorn & Peet 2003; Green & Giese 2004; Hunt et al. 2013; Ciccheto et al.. 2018; Rocha et al. 2018). Since these changes may affect the biodiversity and their ecology, such as survival, movement pattern, distribution (Ryan et al. 2008; Rees et al. 2009; Cosentino et al. 2010; Hill & Vodopich 2013) is important to evaluate how environmental pressures is affecting wild populations.
Recreational fishing, for example, is a common activity in the Brazilian culture and it is often recorded in urban places, even in protected areas. However, this activity may damage the aquatic native fauna (Nemoz et al. 2004; Steen et al. 2014), such as turtles which remain in these areas. This type of incidents occurs because the freshwater turtles are usually opportunistic scavengers and feed on living prey, therefore they are attracted by baited traps and hooks (Borkowski 1997). There are many records about incidents with freshwater turtles regarding to ingestion of fishing sinkers, hooks, as well as monofilament lines, and it can lead to problems in the digestive tract in general and ultimately to death (Larocque et al. 2012; Steen et al. 2014). In the urban area studied (Maringá City) a case of mortality of the native freshwater turtle Phrynops geoffroanus (Schweigger 1812) was recorded due to fishing activity, and this reflects the human impact on the environment (Rocha et al. 2018). Even our record being the first causality for Brazilian freshwater turtles, this type of accident is well known among fishermen, and reflects the lack of knowledge regarding the turtle populations. Phrynops geoffroanus is not a threatened species, however this type of urban impact can cause a population decrease and eventual local extinction of the specie (Steen et al., 2014; Rocha et al. 2018). Therefore, the monitoring of wild native species should be considered in urban environments management plans.
The introduction of alien species is other problem faced by urban areas. According to the Convention on Biological Diversity - CBD (2006), the designation of alien species is related to a particular species, subspecies or inferior taxon introduced in the past or in the present, outside of its natural area of distribution. It includes any structure of this organism (e.g. gamete, seeds, eggs or propagule) that can survive and posteriorly reproduce. Since one species is introduced it should exceed the environmental barrier to survive, such as predators, diseases, and climatic conditions. Whether this species can overcome these barriers and start to reproduce, and maintain a self-regenerating population, then it is consider an established species (Ziller & Zalba 2007). The next barrier to be crossed is the geographic one, which is closely related to the capacity of dispersion of this species. Exceeding the point where it was introduced, and therefore reaching large areas, through physical ways (e.g. wind, dispersers, by human indirect help) or by them own means. The species then is considered an invasive one. Finally, if this species is introduced in many different and separated areas, the invasions increase (Ziller & Zalba 2007).
There are different reasons which can contribute to the flow of alien species, such as the trade of pets, which move millions of individuals annually worldwide (Kraus 2003). In particular, the introduction of amphibian and reptiles started to rise on the 1960s (Kraus 2003). The United States and European Union were the pioneers to trade reptiles and amphibian pets (Tapley et al. 2011; Romagosa 2015). The problem with this activity starts with the fact that many pet's owners receive erroneous or no information regarding to the biology of the animal (e.g. body size that they can reach, longevity, etc.). This lack of information lead owners to introduce intentionally unwanted animals into the wild (Romagosa 2016). In Brazil, exists an additional source of introductions of pets: the release done by authorities after seizure of illegal animals, usually birds and reptiles (Destro et al. 2012). This occurs due to the savage condition of the animals, as well as the lack of places to keep them in captivity (pers. obs). On the other hand, some pets can be introduced accidentally, because of their capacity to escape easily (Pysek et al. 2010). As a consequence, the alien invasion can threaten the local biodiversity, its ecosystem and local economy, being this the second cause of biodiversity loss around the world (Lowe et al. 2000; Ziller & Zalba 2007). It may affect the biodiversity by changing communities organization and functionality, modifying the process of animals foraging, spreading pathogens and inducing the exclusion by competition ( Lowe et al. 2000; Ziller & Zalba 2007; Ferronato et al. 2009). Considering the pressures of urban environment on wild species, the overall goal of the present study was to investigate the influence of urban habitat on population parameters and movement pattern of freshwater turtles.
2.Contenido de la investigación Considering the pressures of urban environment on wild species, the overall goal of the present study was to investigate the influence of urban habitat on population parameters and movement pattern of freshwater turtles. Specifically in Chapter I, we presented the populations parameters (i.e. population size, density, sex ratio and recapture rates) of three species of freshwater turtles in an urban area, being one native (Geoffroy’s slide-necked turtle - Phrynops geoffroanus) and two alien species: D'Orbigny's slider - Trachemys dorbigni dorbigni (Duméril & Bibron, 1835), and Red-eared slider - Trachemys scripta elegans (Thunberg in Schoepff, 1792); as well as information regarding to the home range, distance ranged and the influence of urban features in the habitat selection of species. After 61 capture-recapture sessions of turtles between July 2016 and August 2018 in a park of Paraná state (Brazil), we sampled 41 Phrynops geoffroanus (PG), 35 Trachemys dorbigni dorbigni (TDD), and 20 Trachemys scripta elegans (TSE). The rate of recapture was high: 42%, 65%, and 70%, respectively. Population size (±SE) was estimated as 59 ± 7.6 (PG), 36 ± 1.4 (TDD), and 20 ± 0.5(TSE) individuals, and density (±SE) was 1.36 (0.34), 1.72 (0.36), and 0.87 (0.25) turtle/ha respectively. Sex ratio was female-biased for the two sliders. Urban features, mainly walkways, were highly preferred by the three species, likely due to wild animals feeding by the park users. In addition, the body size influenced the total movement ranged by alien species.
In Chapter II, we described the spatial ecology of the alien species D'orbigni's slider, presenting for the first time data related to this species outside of its natural distribution range. Our results revealed a mean home range of 1.90 ha (KDE 95%) and 3.39 ha (MPC 100%), and this was dependent to body size. Studied turtles selected habitats with urban features, in particular with presence of feeders. Our study is the first to analyze population ecology of native and alien species of freshwater turtles coexisting in Brazil. Long term monitoring of turtles which coexist in that park should be considered, to continue analyzing the populations. In addition, considering that the water body inside and outside are connected, this area structurally is like a matrix of biological invaders. Since the park protects river sources which flow into larger rivers, the water bodies can lead the associated fauna (i.e. D'Orbigny's slider). Finally, an environment education is needed in this park to inform the local people about the problems associated with the alien species (i.e. disease, resource competition with native species) and avoid future pet releases. In Brazil we do not have information about the problems that this species is bringing around the ten states where it has been introduced. Nevertheless, based on the huge impact caused by the congeneric Red-eared turtle (T. scripta) around the world (Lowe et al. 2000), it is necessary to carried out actions to avoid similar problems with this slider in Brazil. Failure to act may facilitate future invasions, and therefore, losing the opportunity to solve this problem before hand.
3.Conclusión At urban areas, our results revealed that anthropic features is influencing the movement of Phrynops geoffroanus (Geoffroy’s slide-necked turtle) , Trachemys dorbigni dorbigni (D'Orbigny's slider) and Trachemys scripta elegans (Red eared turtle). The data recorded by radio telemetry demonstrated more accuracy and supported more detailed monitoring of turtles. Our results proved that the sliders may live long period in the park, at least two years. Even with similar demographic parameters, the presence of two alien species (Red eared turtle and D'Orbigny's slider) seems to be able to bring future problems regarding to its potential of invasion. Special attention should be given to the alien D'Orbigny's slider, which showed characteristics that support its high cognitive capacity.
We strongly suggest long term monitoring of the three species to continue analyzing the dynamic of the population, mainly with the alien species T. d. dorbigni. In addition, social programs should be developed to avoid future introductions of alien species (pet release). Our data should be used as a framework for management of wild urban species.
4. Bibliografía Beaugeard E, Brischoux F, Henry P Y, Parenteau C, Trouvé C & Angelier F. 2019. Does urbanization cause stress in wild birds during development? Insights from feather corticosterone levels in juvenile house sparrows (Passer domesticus). Ecology and Evolution 9(1): 640-652.
Borkowski RDVM. 1997. Lead Poisoning and Intestinal Perforations in a Snapping Turtle (Chelydra serpentina) due to fishing gear ingestion. Journal of Zoo and Wildlife Medicine 28(1): 109-113.
Ciccheto JRM, Grou CEV & Rocha SB. 2018. Novos registros de ocorrência de Trachemys dorbigni no Brasil. In: Estudo Da Herpetofauna Brasileira (Ed. DP Oldiges), pp. 42-50. Atena Editora, Ponta Grossa.
Cosentino BJ, Schooley RL & Phillips CA. 2010. Wetland hydrology, area, and isolation influence occupancy and spatial turnover of the painted turtle, Chrysemys picta. Landscape Ecology 25(10): 1589-1600.
Destro GFG, Pimentel TL, Sabaine RM, Borges RC & Barreto R. 2012. Efforts to combat wild animals trafficking in Brazil. In: Biodiversity enrichment in a diverse world according (Ed. GA Lameed), pp. 421–436. Intech Open, London.
Ferronato BO, Marques TS, Souza FL, Verdade LM & Matushima ER. 2009. Oral bacterial microbiota and traumatic injuries of free-ranging Phrynops geoffroanus (Testudines, Chelidae) in southeastern Brazil. Phyllomedusa 8(1): 19-25.
Green R & Giese M. 2004. Negative Effects of Wildlife Tourism on Wildlife. In: Wildlife Tourism: Impacts, Management and Planning (Ed K Higginbottom), pp. 81-93. Common Ground Publishing Pty Ltd, Melborne.
Hill SK & Vodopich DS. 2013. Habitat use and basking behavior of a freshwater turtle community along an urban gradient. Chelonian Conservation and Biology 12(2): 275-282.
Hunt SD, Guzy JC, Price SJ, Halstead BJ, Eskew EA & Dorcas ME. 2013. Responses of riparian reptile communities to damming and urbanization. Biological Conservation 157: 277–284.
Kraus F. 2003. Invasion pathways for terrestrial vertebrates. In Invasive species: vectors and management strategies (Eds. RMJ Carlton & G Ruiz), pp. 68–92. Island Press, Washington DC.
Larocque SM, Colotelo AH, Cooke SJ, Blouin-Demers G, Haxton T & Smokorowski KE. 2012. Seasonal patterns in bycatch composition and mortality associated with a freshwater hoop net fishery. Animal Conservation 15(1): 53-60.
Lowe S, Browne M, Boudjelas S & De Poorter M. 2000. 100 of the World’s Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG), Auckland, 12 pp.
Nemoz M, Cadi A & Thienpont S. 2004. Effects of recreational fishing on survival in an Emys orbicularis population. Biologia 59(Suppl. 14): 185-189.
Pysek P, Jarosik V, Hulme PE et al. 2010. Disentangling the role of environmental and human pressures on biological invasions across Europe. Proceedings of the National Academy of Sciences 107(27): 12157–12162.
Santini L, González-Suárez M, Russo D, Gonzalez-Voyer A., Von Hardenberg A & Ancillotto L. 2019. One strategy does not fit all: determinants of urban adaptation in mammals. Ecology Letters 22(2): 365–376.
Steen DA, Hopkins BC, Dyke JUV & Hopkins WA. 2014. Prevalence of ingested fish hooks in freshwater turtles from five rivers in the southeastern United States. Plos one 9(3): 1–6.
Rees M, Roe JH & Georges A. 2009. Life in the suburbs: Behavior and survival of a freshwater turtle in response to drought and urbanization. Biological Conservation 142: 3172-3181.
Ryan TJ, Conner CA, Douthitt BA, Sterrett SC & Salsbury CM. 2008. Movement and habitat use of two aquatic turtles (Graptemys geographica and Trachemys scripta) in an urban landscape. Urban Ecosystems 11: 213-225.
Ryan TJ, Peterman WE, Stephens JD & Sterrett SC. 2014. Movement and habitat use of the snapping turtle in an urban landscape. Urban Ecosystems 17: 613-623.
Rocha SB, Grou CEV., Takemoto RM & Ferreira VL. 2018. Phrynops geoffroanus (Geoffroy’s Side-necked Turtle). Mortality from fishing hook. Herpetological Review 49(2): 321-322.
Romagosa CM. 2015. Contribution of the live animal trade to biological invasions. In: Biological Invasions in Changing Ecosystems - Vectors, Ecological Impacts, Management and Predictions (Ed. J Canning-Clode), pp. 116-134. De Gruyter Open, Berlim.
Tapley B, Griffiths RA & Bride I. 2011. Dynamics of the trade in reptiles and amphibians within the United Kingdom over a ten-year period. Herpetological Journal 21: 27-34.
Slabbekoorn H & Peet M. 2003. Birds sing at a higher pitch in urban noise. Nature 424-267.
Viana IR, Prevedello JA & Zocche JJ. 2017. Effects of landscape composition on the occurrence of a widespread invasive bird species in the Brazilian Atlantic Forest. Perspectives in Ecology and Conservation 15(1): 36–41.
Villaseñor NR, Driscoll DA, Gibbons P, Calhoun AJK & Lindenmayer DB. 2017. The relative importance of aquatic and terrestrial variables for frogs in an urbanizing landscape: Key insights for sustainable urban development. Landscape and Urban Planning 157: 26-35.
Ziller SR & Zalba S. Propostas de ação para prevenção e controle de espécies exóticas invasoras. Natureza e Conservação 5(2): 8-15.
