ReviewDiet of Amazon river turtles (Podocnemididae): a review of the effects of body size, phylogeny, season and habitat
Introduction
The diet of freshwater turtles reflects factors such as sex, age, size, habitat selection, prey choice and interspecific interactions (Moll, 1976, Tucker et al., 1995, Armstrong and Booth, 2005). However, many turtles feed opportunistically, and the composition of the diet may reflect resource availability (Mahmoud and Klicka, 1979, Moll and Moll, 2004, Souza, 2004). Phylogeny is also important in shaping dietary preferences, which can be influenced by present day interactions and historical influences (Vitt and Carvalho, 1995, Vitt and Zani, 1996, Lindeman, 2000). Closely related species are more likely to be ecologically similar (Ricklefs and Miller, 1999).
Small body size has been viewed as a major constraint to herbivory in reptiles. According to many hypotheses, larger species have a greater absolute capacity for fat storage (enhanced buffer against seasonal variability in food suply), are less able to meet their metabolic requirements on a carnivorous diet, have a favourable ratio of mass-specific energy requirements to gut capacity, and can meet the high mass-specific energy and nutrient requirements on a nutrient-poor plant diet (Clark and Gibbons, 1969, Bell, 1971, Geist, 1974, Wilson and Lee, 1974, Pough, 1983, Penry and Jumars, 1987, Zimmerman and Tracy, 1989, Parmenter and Avery, 1990). These hypotheses have also been extended to explain ontogenetic dietary shifts in several species of freshwater turtles (Moll, 1976, Ernst and Barbour, 1989).
Ecological interactions in tropical rivers are strongly affected by changes in habitat and resource availability associated with seasonal variation in hydrological conditions, particularly annual cycles of flooding and drying (Lowe-McConnell, 1979, Jepsen et al., 1997). Likewise, floodplain forest productivity is influenced by nutrients originating from erosion, flooding, and sedimentation. The chemical composition of leaves, bark, and wood of floodplain trees is influenced by the availability of chemical elements in the water (Irion, 1982, Irion, 1984, Victoria et al., 1989, Junk, 1993). In the Amazon basin there is a synchrony between plant phenology and the inundation pulse. During the high water season there is intense production of seeds and fruits (Goulding et al., 1988, Kubitzki and Ziburski, 1994).
Amazon rivers can be divided into three groups according to the origin of their sediment, dissolved nutrient content and vegetation (Prance, 1979, Klinge et al., 1983, Junk, 1985). White water or ‘muddy’ rivers (i.e., Madeira, Purus, Juruá, Japurá, Magdalena and Amazon; Fig. 1) have a neutral pH and high turbidity, sediment loads and levels of primary production. White water floodplains (Várzea) are rich in dissolved nutrients (especially Ca and Mg) and fertile sediments originating from the Andes. Aquatic and terrestrial herbaceous plants are abundant in white water rivers, as are annual and perennial grasses and aquatic macrophytes which may form floating meadows (Gibbs, 1967, Sioli, 1967, Junk and Howard-Williams, 1984, Martinelli et al., 1989, Piedade et al., 1992).
Tannin-stained black water rivers (i.e., the Negro River and its tributaries) originate from the Guyana and Central Brazilian Shields. The waters are acidic and poor in electrolytes and nutrients, with extremely low sediment loads and low primary production. Their infertile floodplains (Igapó) support forests on extremely impoverished substrates. Herbaceous plants occur in low abundance and aquatic plants are often absent in black water areas (Junk and Howard-Williams, 1984, Junk, 1993).
The third group, clear water rivers, such as the Tocantins, Tapajós and Xingu, have an intermediate nutrient status and are less common than white and black water rivers (Junk, 1993, Goulding et al., 2003). They vary seasonally from crystalline to murky and generally have low sediment loads. The main focus of this review is on turtle diets in black and white water rivers, where the majority of work has been undertaken.
According to Janzen (1974), habitats such as the black water Igapó with a climate favourable to animals, but an environment with extremely low primary productivity, should favour plants rich in secondary chemical defences, or plants that are gregarious and have synchronised (mast) fruiting. Due to the constraint of low nutrient availability, these plants delay leaf replacement and produce a high concentration of toxic alkaloids, phenols and tannins to reduce the incidence of herbivory (Coley and Barone, 1996). This high degree of protection might affect the amount of vegetable matter available which aquatic vertebrates, such as podocnemidid turtles, are able to digest.
The pleurodiran (sideneck) family Podocnemididae is currently represented by three genera and seven species in South America and one in Madagascar (Williams, 1954, Neill, 1965, Rhodin et al., 1978). Six species of Podocnemis and one species of Peltocephalus are found in the Amazon region. Although the two larger species, Podocnemis expansa and Podocnemis unifilis, are sympatric throughout most of the Amazon and Orinoco drainages (Iverson, 1992, Bock et al., 2001), all species have distinct distributions and habitat preferences (Pritchard and Trebbau, 1984, Rueda-Almonacid et al., 2007, Vogt, 2008). Podocnemidids are typically opportunistic, generalistic and omnivorous, tending to herbivory. The proportion of plant and animal matter consumed varies considerably between species, populations and periods (Ojasti, 1971, Mittermeier and Wilson, 1974, Ramo, 1982, Pritchard and Trebbau, 1984, Almeida et al., 1986, Fachín-Terán et al., 1995, Balensiefer and Vogt, 2006, De La Ossa et al., 2011).
The feeding habits of these turtles have been studied for the last 40 years, yet to our knowledge a review of this information has not been attempted. As is the case with the Amazon fish fauna (Araujo-Lima et al., 1995), many of the studies are unpublised masters and Ph.D. theses or reports in Portuguese and Spanish, and the information has not been summarised for an English language audience. By reviewing the available information, we aim to test the relationship between Amazon environments and the diet of podocnemidids, particularly in relation to habitat (water type). Additionally, size, sex, season, location and phylogenetic relationships may play an important role and should be taken into account (Vargas-Ramírez et al., 2008). Our aim was to review the data available on diet of South American Podocnemididae species in relation to habitat, season, size, age, sex and phylogeny.
Section snippets
Overview
The literature was reviewed to gather information on the diet of Podocnemis erythrocephala, P. expansa, P. lewyana, P. sextuberculata, P. unifilis, P. vogli and Peltocephalus dumerilianus. Diet studies of captive animals or information based solely on interviews with local communities are cited in Section 3 but were not considered in the analyses. The information was categorised by species studied, location of the study and water type (black or white water; Fig. 1). Where available, vegetable
Species summaries
Peltocephalus dumerilianus is the most omnivorous species (Pérez-Emán and Paolillo, 1997, De La Ossa et al., 2011), although it consumes a high proportion of fruits and seeds, which can represent over 85% of its diet (Ojasti, 1971). According to Vogt (2001), P. dumerilianus has a preference for apple snails, when available. This species inhabits preferentially black water rivers, creeks and lakes (Pritchard and Trebbau, 1984, Rueda-Almonacid et al., 2007).
Podocnemis erythrocephala is mainly a
Influence of phylogeny
Information on diet (percentage of animal or vegetable matter), size (LCLmax; Ernst and Barbour, 1989) and habitat (mostly black, white or both) was combined with the family phylogeny assembled by Vargas-Ramirez et al. (2008) in Fig. 2. Neither diet, habitat nor size reflected taxonomic affinities and no clear patterns emerged from the inspection of Fig. 2. This variance in ecologically influenced characteristics is probably an indicator that the evolutionary history might not play an important
Amazon floodplains
Most freshwater turtles are omnivorous and opportunistic (Legler, 1993, Moll and Moll, 2004). The spatial and temporal oscillations of tropical riverine aquatic environments promote the predominance of opportunistic species (Abelha et al., 2008). Omnivory is also common in floodplains with seasonal floral and faunal variations (Cooper and Vitt, 2002, Metzger and Herrel, 2005). The capacity of opportunistic omnivorous species to exploit a variety of food items acts as a buffer against adverse
Seasonal differences
The most frequently studied season was low water (50% of studies). This was largely due to logistical constraints; during low water turtles are easier to find and capture in the reduced habitat available. However, low water studies probably do not account for most energy and nutrient intake. Most feeding takes place during high water, when the turtles move to the flooded forest. Many Amazon aquatic vertebrates depend on the flooded forests to obtain food and accumulate energy (Junk et al., 1997
Regional differences
Few studies (n = 5) compared the diet of a single species between different areas or habitats. As expected (Moll and Moll, 2004), most of these studies (80%) found differences between areas (Table 1). This included the proportion and diversity of fruits, seeds and aquatic plants (P. dumerilianus; Pérez-Emán and Paolillo, 1997), fish and crustaceans in artificial ponds versus streams (P. vogli; Ramo, 1982), and seeds and fruits in flooded forests versus shoots, stems and leaves in oxbow lakes and
Differences between sexes
Ten studies compared diet between sexes. Among those, 60% found dietary differences related to sex (Table 1). Females of P. vogli consumed more fish and mollusks than males (Ramo, 1982), and female P. dumerilianus consumed less Mauritia flexuosa seeds (Pérez-Emán and Paolillo, 1997). There were no differences between the diet of females and males of P. erythrocephala (Jaú River; Santos-Júnior, 2009). Males of P. dumerilianus in the Negro River during high water had lower trophic diversity than
Ontogenetic and size variation
Dietary ontogenetic changes are common in turtles. In many omnivorous species, juveniles are preferentially carnivorous and shift towards herbivory as they grow (Clark and Gibbons, 1969, Moll and Legler, 1971, Moll, 1976, Georges, 1982, Lima et al., 1997, Souza, 2004). These changes can be linked to physiological needs (Plummer and Farrar, 1981, Hart, 1983, Bury, 1986, Moll, 1990), such as a requirement for a diet rich in calcium, nitrogen and energy to stimulate growth (Moll, 1976, Shealy, 1976
Interspecific trends in diet
There was no significant correlation between LCLmax and volume of vegetable matter consumed (ρ(6) = 0.03, p = 0.96; Fig. 3). The two mainly black water species, P. dulmerilianus and P. erythrocephala are more omnivorous in comparison to the other species which inhabit white water or both white and black water habitats. The hydrochemical conditions and fertility of a river ultimately dictate the amount of plant matter available for consumption. White water rivers are more fertile than clear and
Limitations and recommendations for future studies
Of the 16 studies on the diet of South American Podocnemididae, four studies had small sample sizes, which are unlikely to adequately represent the species diet (n < 20; Table 1). Information on P. expansa is particularly problematic due to their small sample size. It is important to note that methods to assess diet differed substantially, which can potentially impact the results. The most common methods used were stomach flushing (e.g., Balensiefer and Vogt, 2006), stomach and digestive tract
Acknowledgements
This study was financed by the National Council for the Scientific and Technological Development (CNPq). C.C.E. was financed by the Science without Borders Program of CNPq (process number 233418/2014-8). We thank Fernando A. Perini, Virginia C. D. Bernardes and Marcia L. Queiroz for help with data collection and analysis.
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