Diet of Amazon river turtles (Podocnemididae): a review

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Diet of Amazon river turtles (Podocnemididae): a review of the effects of body size, phylogeny, season and habitat
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[Cowboy_Ken]

Diet of Amazon river turtles (Podocnemididae): a review of the effects of body size, phylogeny, season and habitat
You can use the link below to download the final version the article on ScienceDirect for free until April 19, 2017:

http://www.sciencedirect.com/science/article/pii/S0944200616300666

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Zoology
February 2017, Vol.120:92–100, doi:10.1016/j.zool.2016.07.003
Review
Diet of Amazon river turtles (Podocnemididae): a review of the effects of body size, phylogeny, season and habitat
Carla C. EisembergStephen J. ReynoldsRichard C. Vogt
Show more
Highlights
•
Diet among the Amazon podocnemidids varies depending on species, sex, season and location.
•
There is no relationship between maximum carapace length and vegetable matter consumed.
•
Habitat (water type) indirectly influences the average volume of total vegetable matter consumed.
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Species with no specialised stomach adaptations consume vegetable matter less hard to digest.
•
Plant secondary metabolites most effectively prevent consumption by turtles that lack adaptations to herbivory.
Abstract
Amazon rivers can be divided into three groups (black, white and clear waters) according to the origin of their sediment, dissolved nutrient content, and vegetation. White water rivers have high sediment loads and primary productivity, with abundant aquatic and terrestrial plant life. In contrast, black water rivers are acid and nutrient-poor, with infertile floodplains that support plant species exceptionally rich in secondary chemical defences against herbivory. In this study, we reviewed available information on the diet of Amazon sideneck river turtles (Family Podocnemididae). Our aim was to test the relationship between water type and diet of podocnemidids. We also took into account the effects of season, size, age, sex and phylogeny. Based on our review, turtles of this family are primarily herbivorous but opportunistic, consuming from 46 to 99% (percent volume) of vegetable matter depending on species, sex, season and location. There was no significant correlation between the maximum carapace size of a species and vegetable matter consumed. When the available information on diet, size and habitat was arranged on the podocnemidid phylogeny, no obvious evolutionary trend was evident. The physicochemical properties of the inhabited water type indirectly influence the average volume of total vegetable matter consumed. Species with no specialised stomach adaptations for herbivory consumed smaller amounts of hard to digest vegetable matter (i.e. leaves, shoots and stems). We propose that turtles with specialized digestive tracts may have an advantage in black water rivers where plant chemical defences are more common. Despite limitations of the published data our review highlights the overall pattern of diet in the Podocnemididae and flags areas where more studies are needed.

Keywords
PodocnemisPeltocephalusHerbivoryFloodplainsFood availability
1 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 and 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 and 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 and 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 and Parmenter and Avery, 1990). These hypotheses have also been extended to explain ontogenetic dietary shifts in several species of freshwater turtles (Moll, 1976 and 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 and 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 and 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 and 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 and 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 and Piedade et al., 1992).


Fig. 1. Main rivers from Amazon and Orinoco basins (adapted from Goulding et al., 2003 and Rodríguez et al., 2007) with water types (white, black, clear) specified. Letters represent study locations: A = Yagua and Atacavi rivers; B = Negro/Itú/Jau rivers; C = Ayanã River; D = Guaporé River; E = Caquetá River; F = Trombetas River; G = Prado River; H = Depresión Momposina; I = Middle-Solimões/Japurá River; J = Azupizu River; K = Los Llanos.

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 and 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 and 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 and 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 and Bock et al., 2001), all species have distinct distributions and habitat preferences (Pritchard and Trebbau, 1984, Rueda-Almonacid et al., 2007 and 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 and 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.

2 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 matter, frequency of occurrence and percent volume were also noted. We determined if the study recorded differences in diet among distinct periods of the year, areas or habitats, animal sizes and sex. Sampling methodologies were assessed according to sample size and period of study.

The relationship of species size with diet and habitat was examined by plotting maximum (linear) carapace length (LCLmax; according to Ernst and Barbour, 1989), average volume of vegetable matter consumed (obtained in the diet literature review) and habitat in regard to water type (predominantly black, white or both). Only diet studies on white and black waters were used in these analyses. We also used a Spearman correlation to test the relationship between size and the mean volume of difficult to digest plant matter (leaves, shoots and stems) after removing the probable confounding effect of fruits and seeds. We plotted LCLmax, habitat, and diet and merged this information with the most recent phylogeny (Vargas-Ramírez et al., 2008). Statistical analyses were performed using the package Agricolae, R v.3.0 (R Core Team, 2015).

3 Species summaries
Peltocephalus dumerilianus is the most omnivorous species (Pérez-Emán and Paolillo, 1997 and 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 and Rueda-Almonacid et al., 2007).

Podocnemis erythrocephala is mainly a black water species and is found commonly in small streams and lakes, although it can also inhabit clear water tributaries (Mittermeier et al., 2015). There is no consensus on the main dietary items for this species (Silva, 2007, Souza and Vogt, 2008 and Santos-Júnior, 2009). Vogt (2001) found primarily filamentous algae in their stomachs, while Thomé-Sousa (2005) and Santos-Júnior (2009) found allochthonous plant material from the flooded forest. However, P. erythrocephala studies are difficult to compare since they differ in season, methodology and circumstances. For example, the study of Vogt (2001) was undertaken after a forest fire, when there was a high incidence of light and thus algae production (Thomé-Sousa, 2005).

Podocnemis expansa lives in all three Amazon water types (Ernst and Barbour, 1989). This species is mainly herbivorous, with a minimum of 89% of the stomach contents consisting of vegetable matter (Ojasti, 1971, Fachín-Terán et al., 1995, Costa, 2012 and Figueroa et al., 2012). It feeds on fruits and seeds that fall from riparian trees, and stems, leaves, and roots of floodplain plants (Pritchard, 1979, Soini, 1984, Almeida et al., 1986, Soini et al., 1989, Rodrigues et al., 2004, Rueda-Almonacid et al., 2007 and Vogt, 2008). Studies in captivity suggest that P. expansa can be opportunistic and omnivorous, consuming animal foods when they are available (Alho et al., 1979, Alho and Padua, 1982, Acosta et al., 1995, Duarte, 1998 and Malvasio et al., 2003). Sub-adults especially prefer beef and fish (Ojasti, 1971).

Podocnemis sextuberculata is found in white and clear water rivers (Ernst and Barbour, 1989). The only systematic study of this species concluded that all life stages are mostly herbivorous, feeding mainly on seeds and fruits throughout the year. Other plant parts, such as leaves and rhizomes, are consumed only when the animal reaches a size of at least 15 cm (Fachín-Terán, 1999). Anecdotal reports from other rivers consider this species omnivorous, feeding primarily on snails (Rueda-Almonacid et al., 2007 and Vogt, 2008). In captivity, it is predominantly carnivorous, especially hatchlings and young adults (Malvasio et al., 2003). In the Trombetas River, females marked with transmitters at a nesting beach in three different years were found feeding on molluscs in a mud flat 97 km from the nesting beach (Vogt, personal observation).

Podocnemis unifilis is widely distributed in white, black and clear water rivers of the Orinoco and Amazon basins (Ernst and Barbour, 1989, Rueda-Almonacid et al., 2007 and Vogt, 2008). Only plant material was found in the stomachs of P. unifilis by Medem (1964) and Almeida et al. (1986). Detailed studies found that no less than 80% of the volume of the stomachs consisted of vegetable matter (Fachín-Terán et al., 1995, Balensiefer and Vogt, 2006, Figueroa et al., 2012 and Ferronato et al., 2013). Many studies report the aquatic plant Eichhornia as a particularly abundant food item (Mondolfi, 1955, Medem, 1964, Almeida et al., 1986 and Ushinhahua and Del Aguila, 1986). However, P. unifilis rarely feeds on this aquatic plant in the Guaporé River, although Eichhornia is abundant there throughout the year. Plant species from 21 families were identified as part of the diet of P. unifilis (Portal et al., 2006). In captivity, P. unifilis can easily adapt to animal and vegetable items (Malvasio et al., 2003). According to Ferronato et al. (2013), differences in the variety of plant species recorded can be due to differences in the number of sampled sites, habitats, and animals. Fruits and seeds were important items on black water rivers (Fachín-Terán et al., 1995), but they were not as important in white water (Balensiefer and Vogt, 2006) and clear water rivers (Ferronato et al., 2013).

Podocnemis lewyana, a species endemic to white water rivers in Colombia (Rueda-Almonacid et al., 2007 and Páez et al., 2009), is primarily herbivorous, with vegetable matter comprising 92–99% of the stomach contents (Cano, 2007, Páez et al., 2009 and González-Zárate, 2010).

Podocnemis vogli is a small species (LCLmax 36 cm) that inhabits the grassland areas (llanos) of the Orinoco drainage in Venezuela and Colombia (Pritchard and Trebbau, 1984). Its diet includes aquatic plant stems, leaves and seeds, but also insects, molluscs, crustaceans, fish and carrion (Alarcón Prado, 1969 and Ramo, 1982). This is the only podocnemidid known to graze outside the water, which it does on young grasses during low water (Ramo, 1982).

The Madagascan Erymnochelys madagascariensis is the only species from the family outside South America. This species has a LCLmax of 44 cm and it is found in slow-flowing rivers, streams, swamps, lagoons and marshes (Ernst and Barbour, 1989). Although E. madagascariensis was not included in our analyses, it is important to note that it presents an omnivore and opportunistic diet, with plant material being less representative in the gut analyses of juveniles (41%) and adults (72%) than in the Amazon species (Garcia and Lourenco, 2007).

4 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 role in structuring diet within this family (Snell et al., 1984).


Fig. 2. Diet, size (maximum carapace length; Ernst and Barbour, 1989) and habitat type merged with the Podocnemididae phylogeny (according to Vargas-Ramírez et al., 2008; note that the illustrated topology shows clades but not divergence times). Dimensions of the squares represent species size, circle backgrounds indicate species diet (percentage of vegetable and animal matter) and square backgrounds, habitat (mostly black water, white water or both) for studied species from South America. There are no details shown for Podocnemis vogli because there was no data on volume of vegetable matter consumed for this species; it lives in white water ponds and is similar in size to P. sextuberculata.

5 Amazon floodplains
Most freshwater turtles are omnivorous and opportunistic (Legler, 1993 and 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 and Metzger and Herrel, 2005). The capacity of opportunistic omnivorous species to exploit a variety of food items acts as a buffer against adverse conditions (Teixeira et al., 2005). In the Amazonian floodplain, opportunistic fishes adjust their diet to the food items available in the different phases of the hydrological cycle (Pereira et al., 2011). The floodplain forest is flooded from four to eight months of the year and during the dry season can shrink to less than 20% of maximum area (Junk, 1985). To guarantee optimum exploitation of the available resources, turtles and fishes need to be highly mobile and flexible in their food choices (Junk et al., 1997).

In the Amazon floodplain, there are at least 40 trees per hectare (from 42 different species in the area) that produce edible fruits and seeds for fishes (reviewed by Araujo-Lima et al., 1995) and probably for turtles as well. In return, podocnemidid turtles might be important seed dispersers, since they ingest a large number of fruits without damaging the seeds (Ojasti, 1971, De La Ossa et al., 2011 and Figueroa et al., 2012). The importance of chelonians as seed dispersers has been suggested for a number of species (MacDonald and Mushinsky, 1988, Vogt and Guzman, 1988, Moskovits and Bjorndal, 1990 and Moll and Moll, 2004). Costa (2012) found no evidence of P. expansa being a seed disperser, although the sample size (n = 7) was small. More research is needed in this area, particularly in regard to the role of turtles in the dynamics of Amazonian floodplain ecosystems and the redistribution of nutrients (Pérez-Emán and Paolillo, 1997).

6 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, Huntingford et al., 2001 and dos Santos et al., 2008). During low water the (relatively uniform) open water is the only habitat available. As a consequence, food intake is reduced (Goulding, 1980), and non-predatory vertebrates rely on body fat reserves as food becomes scarce (Junk, 1985).

Seven studies collected data in more than one season, and in most cases (57%) there were differences among seasons (Table 1). Fachín-Terán et al. (1995) and De La Ossa et al. (2011) did not find differences between seasons for P. dulmerilianus and P. unifilis. In some cases, seasonality was the main factor responsible for dietary intraspecific variation (Pérez-Emán and Paolillo, 1997). P. vogli and P. sextuberculata consumed more animal matter during falling waters (Ramo, 1982 and Fachín-Terán, 1999), while P. unifilis and P. expansa had a higher consumption of fruits at high and rising water (Figueroa et al., 2012).

Table 1. Information on diet and maximum carapace length (in parentheses, according to Ernst and Barbour, 1989) for species of South American Podocnemididae, and study location, water type and period of year. Letters A–K denote locations in Fig. 1. VM = vegetable matter consumed; FS = fruits and seeds consumed; PV = percent volume; FO = frequency of occurrence; NS = not studied; AV = average. * = studies where sample size was ≥ 20 individuals.

Species Location Water
type VM (%)
FS (%)
Differences in diet by
Sampling Reference PV FO PV FO Period Area Size Sex Peltocephalus dumerilianus (68 cm) A. Yagua and Atacavi rivers (Amazonas, Venezuela) Black 45.8 NS 36 56.5 NS Yes No Yes Two rivers in distinct seasons* Pérez-Emán and Paolillo, 1997 B. Negro River Igapós (Amazonas, Brazil) Black 76.2 59 AV NS NS No NS NS Yes One year* De La Ossa et al., 2011 Podocnemis erythrocephala (32 cm) C. Ayanã River (Amazonas, Brazil) Black 66 89 50 NS NS NS NS NS Low water season Silva, 2007 B. Itú River (Amazonas, Brazil) Black 88 NS NS NS NS NS NS NS Low water season* Souza and Vogt, 2008 B. Jau River Igapós (Amazonas, Brazil) Black 97.9 100 47.7 98 NS NS NS No High water season* Santos-Júnior, 2009 Podocnemis expansa
(107 cm) D. Guaporé River (Rondônia, Brazil) Black 97.6 NS NS NS NS NS NS NS Three individuals, low water season Fachín-Terán et al., 1995 E. Caquetá River (Amazonas, Colombia) White 94 AV NS 63 AV NS Yes NS NS NS Nine individuals,
> one year sampling Figueroa et al., 2012 F. Trombetas River (Pará, Brazil) Clear 89.2 NS 23 NS NS NS No No Low water season* Costa, 2012 Podocnemis lewyana (45 cm) G. Prado River (Tolima, Colombia) White 92 NS NS NS NS NS NS NS Low water season, four different areas* González-Zárate, 2010 H. Depresión Momposina (North Colombia) White 99 NS NS NS NS NS NS NS Seven females, low water season Cano, 2007 Podocnemis sextuberculata (34 cm) I. Middle-Solimões/Japurá River (Amazonas, Brazil) White 96 NS 91 87 Yes Yes Yes Yes 17 months* Fachín-Terán, 1999 Podocnemis unifilis (68 cm) J. Azupizu River (Pasco, Peru) Clear 95 62.9 85 29.6 No No No No Low water season* Ferronato et al., 2013 D. Guaporé River (Rondônia, Brazil) Black 90 NS 39 93 No Yes Yes Yes One year, three different habitats* Fachín-Terán et al., 1995 I. Middle-Solimões/Japurá River (Amazonas, Brazil) White 79.7 100 49.5 61.5 NS NS No No Low water season* Balensiefer and Vogt, 2006 E. Caquetá River (Amazonas, Colombia) White 97 AV NS 71
AV NS Yes NS NS Yes Nine individuals, over one year Figueroa et al., 2012 Podocnemis vogli (36 cm) K. Los Llanos (Apure, Venezuela) White NS 94.7 NS NS Yes Yes Yes Yes One year, two different areas* Ramo, 1982
Independent of the study region, more vegetable matter was consumed during high water (Fachín-Terán et al., 1995, Malvasio et al., 2003 and Figueroa et al., 2012). This might reflect food item availability (Tucker et al., 1995), because a greater spectrum of foods becomes accessible during high water when the floodplains are inundated (Gottsberger, 1978, Junk et al., 1997 and de-Mérona and Rankin-de-Mérona, 2004). Although fruiting occurs at different times of year, maximum fruiting is usually associated with high water (Ayres, 1993, Kubitzki and Ziburski, 1994 and Junk et al., 1997). Most Amazon fishes are omnivorous on a seasonal basis, with predation playing a major role during the rising and high water periods in black water and during the falling and low water periods for white water (Junk et al., 1997).

7 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 rivers (P. unifilis; Fachín-Terán et al., 1995). There were differences in the amount of animal matter consumed by P. sextuberculata in distinct habitats of the middle Solimões river (Fachín-Terán, 1999); animal matter was consumed more frequently by turtles in small channels, while none was consumed by animals close to nesting sandbanks.

P. expansa and P. unifilis are present in both black and white water rivers. Different populations of P. expansa had similar diets. Both black water Guaporé River (Fachín-Terán et al., 1995) and white water Caquetá River (Figueroa et al., 2012) populations consumed 96% of vegetable matter during the low water season. Clear water Trombetas River populations consumed 89% of vegetable matter during the low water season. The proportion of vegetable matter consumed by P. unifilis during low water varied from 80% (white water, Japurá River; Balensiefer and Vogt, 2006) to 82% (black water, Guaporé River; Fachín-Terán et al., 1995), 93% (white water, Caquetá River; Figueroa et al., 2012) and 95% (clear water, Azupizu River; Ferronato et al., 2013). There are no data available for comparisons during high water season.

Dietary differences between populations of the same species are usually related to habitat variation or feeding niche displacement in response to the presence of closely related species (Vogt and Guzman, 1988). These differences can translate into dissimilar patterns of growth (Moll, 1976, Gibbons et al., 1979 and Vogt, 1981). Furthermore, populations from highly productive habitats with no interspecific competition might have a more carnivorous diet and faster growth rates (Vogt and Guzman, 1988).

8 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 females (De La Ossa et al., 2011). Divergent results were found in studies of P. unifilis: Balensiefer and Vogt (2006) found no differences between sexes of P. unifilis in the Japurá River, whereas P. unifilis females in the Guaporé River consumed more seeds and fruits, and males consumed more Poaceae stems (Fachín-Terán et al., 1995). Females of P. sextuberculata fed on insects more frequently than males (Fachín-Terán, 1999).

Differences in male and female diet can be attributed to differential microhabitat use (Plummer and Farrar, 1981), which could reduce direct competition (Mayr, 1963, Moll and Legler, 1971, Vogt, 1981 and Bertl and Killebrew, 1983). Distinctive dietary requirements between sexes, such as females seeking a diet with higher calcium content, necessary for egg formation, is also a possible explanation for dietary preferences between sexes (Moll and Legler, 1971, Vogt, 1981 and Bertl and Killebrew, 1983). According to Ramo (1982), calcium requirement is the reason why P. vogli females consume more molluscs and fish than males.

9 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 and Souza, 2004). These changes can be linked to physiological needs (Plummer and Farrar, 1981, Hart, 1983, Bury, 1986 and Moll, 1990), such as a requirement for a diet rich in calcium, nitrogen and energy to stimulate growth (Moll, 1976, Shealy, 1976, Hart, 1983, White, 1985, Parmenter and Avery, 1990, Congdon et al., 1993 and Bouchard and Bjorndal, 2006). Adults have lower mass-specific nutrient requirements (Hart, 1983, Parmenter and Avery, 1990 and Bjorndal, 1991) but their large body size will result in higher total energy requirements, in which case the costs of pursuing active prey may be too high for large turtles (McCauley and Bjorndal, 1999). It may also involve resource partitioning due to ontogenetic changes in foraging habitat (e.g., adults foraging in deeper waters) (Clark and Gibbons, 1969, Hart, 1983, Moll, 1990 and Arthur et al., 2008).

Ontogenetic and size differences in diet were examined in 44% of the studies. Among those, three studies (43%) found differences in regard to size (Table 1). The consumption of seeds and fruits increased linearly and fish consumption decreased as a function of the carapace length for P. unifilis (Guaporé River; Fachín-Terán et al., 1995). The opposite occurred with P. vogli in Los Llanos, where bigger animals consumed more fish (Ramo, 1982). There were no differences in diet between different size classes in P. dumerilianus and P. unifilis (Pérez-Emán and Paolillo, 1997 and Balensiefer and Vogt, 2006). Frequency of occurrence of seeds decreased in larger P. sextuberculata. Stems, leaves, and rhizomes were only consumed by animals larger than 14 cm and consumption frequency increased with size (Fachín-Terán, 1999).

10 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 black water rivers, resulting in abundant aquatic plants and a greater food supply (Junk et al., 1997). In contrast, black water floodplains have a higher percentage of plants rich in secondary chemical defences against herbivory or with gregarious fruiting (Janzen, 1974).


Fig. 3. Non-significant relationship between proportional volume of vegetable matter consumed (average used when there was more than one study of the species), difficult to digest vegetable matter and maximum carapace length (LCLmax; according to Ernst and Barbour, 1989). Podocnemis vogli was excluded because there is no information on volume of vegetable matter consumed.

We also found no significant correlation between LCLmax and volume of hard to digest vegetable matter (ρ(5) = –0.10, p = 0.78; Fig. 3). In this case, the morphology of the digestive tract might be of importance (Hailey, 1997, Franz et al., 2011 and Magalhães et al., 2014). Based on the morphology of the digestive tract, P. dumerilianus and P. sextuberculata should be omnivorous, since they do not have any specialised stomach adaptations for herbivory. They have simple stomachs (Magalhães et al., 2014), similar to the green turtle (Chelonia mydas) and most non-herbivorous vertebrates (George and Castro, 1998 and Magalhães et al., 2010). These two species consumed less leaves, shoots and stems (Fig. 3).

On the other hand, P. expansa, P. unifilis and P. erythrocephala have specialised herbivore stomachs, with two discrete regions. The anterior region functions as a fermentation vat and digestion occurs in the pyloric region (Magalhães et al., 2014). Microbes involved in fermentation may also aid in the detoxification of plant secondary metabolites (Coley and Barone, 1996). This could explain the high consumption of leaves, shoots and stems by P. unifilis and P. erythrocephala in black water. Plant components such as leaves, flowers and roots are present in the diet of Amazon fishes in relatively low amounts (Goulding, 1980, Santos, 1982 and Goulding et al., 1988). This may be due to their low digestibility and high toxicity (Goulding et al., 1988).

Various anatomical and behavioural strategies are utilised by reptiles to increase nutrient uptake from plants (Metzger and Herrel, 2005). Some herbivorous small reptiles (species or juveniles) can offset unfavourable gut capacity and metabolic rate ratios by ingesting smaller food particles, reducing gut transit time, selecting plant parts high in nitrogen and energy, and increasing body temperature to facilitate digestion (Troyer, 1984, Mautz and Nagy, 1987, Bjorndal et al., 1990, Bjorndal and Bolten, 1993 and Wikelski et al., 1993). In regard to digestive performance, herbivorous freshwater turtles do not necessarily outperform omnivorous species, unless they are digesting plant material that is subject to extensive fermentation (Bjorndal and Bolten, 1993).

We propose that turtles with specialised digestive tracts may have an advantage in black water rivers where plant chemical defences are more common. However, more dietary, behavioural and physiological studies are needed to test this hypothesis.

11 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 examination (e.g., De La Ossa et al., 2011), or both (e.g., Pérez-Emán and Paolillo, 1997). However, sieves used to collect and filter food items might not retain small particles and insects, which can be problematic for species that filter small particles on the surface of the water. This feeding behaviour (neustophagia) has been observed in P. expansa, P. erythrocephala, P. unifilis and P. vogli (Belkin and Gans, 1968, Legler, 1976, Rhodin et al., 1981 and González-Zárate, 2010).

Although dietary studies with species of this family have been ongoing for the past 40 years, few studies tested for effects of size, sex, season and habitat. Furthermore, there were major discrepancies between methodologies and statistical tests for differences. Data and results were not presented in a standard format, which is a major issue in comparing dietary studies (Cooper and Vitt, 2002 and Metzger and Herrel, 2005). This was particularly problematic when studies did not identify frequency of occurrence, percent volume or plant parts (e.g. fruits, seeds, leaves, etc.). Fruits have very different nutritional and energetic values, which influence nutrient assimilation and food selection (Parmenter, 1980, Moskovits and Bjorndal, 1990 and Pérez-Emán and Paolillo, 1997). Dietary results might be misinterpreted if fruits are grouped with hard plant parts.

We suggest that future studies on the diet of podocnemidids should consistently present “frequency of occurrence” and “percent volume” and specify the diet items to the lowest possible taxonomic level, as well as the parts of the plant consumed. More comprehensive diet studies should also test for differences in size, sex, season and area using appropriate statistical analyses.

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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