You are what, where, and when you eat: seasonal and ontogenetic changes in a tropical tadpole’s diet

in Amphibia-Reptilia

Abstract

Tadpole diet is likely to vary in response to environmental conditions and nutritional needs throughout growth and development. We investigated seasonal variation in diet composition of Bokermannohyla saxicola tadpoles and compared diets between two developmental stages with a significant difference in size. We found that the diet of B. saxicola tadpoles was dominated by periphytic algae, in accordance with their benthic habits. Considering number of cells ingested, tadpole trophic niches were broader in more advanced developmental stages. Tadpole trophic niches were narrower during the summer (wet season) than during the winter (dry season), which may reflect increased consumption of more energetic food items during the warm period when primary productivity is expected to be higher. Tadpole metabolism is likely to be higher in the summer and increased energetic needs might be supplied in this manner. However, results differed when biovolume was considered instead of number of cells ingested, with larger items assuming a greater importance and niches being usually larger in the summer. In these cases, the increased ingestion of diatoms (likely to be more nutritive) in the summer may decrease the relative importance of large algae (e.g., Mougeotia sp.) that form the bulk of the diet. Both food availability/accessibility and tadpole feeding behaviour driven by nutritional needs may influence patterns of food acquisition. Given the importance of biofilms to tadpole diet, studies on the mechanisms by which tadpole nutritional needs and environmental conditions interact are likely to provide important insights into the dynamics of aquatic food webs.

Abstract

Tadpole diet is likely to vary in response to environmental conditions and nutritional needs throughout growth and development. We investigated seasonal variation in diet composition of Bokermannohyla saxicola tadpoles and compared diets between two developmental stages with a significant difference in size. We found that the diet of B. saxicola tadpoles was dominated by periphytic algae, in accordance with their benthic habits. Considering number of cells ingested, tadpole trophic niches were broader in more advanced developmental stages. Tadpole trophic niches were narrower during the summer (wet season) than during the winter (dry season), which may reflect increased consumption of more energetic food items during the warm period when primary productivity is expected to be higher. Tadpole metabolism is likely to be higher in the summer and increased energetic needs might be supplied in this manner. However, results differed when biovolume was considered instead of number of cells ingested, with larger items assuming a greater importance and niches being usually larger in the summer. In these cases, the increased ingestion of diatoms (likely to be more nutritive) in the summer may decrease the relative importance of large algae (e.g., Mougeotia sp.) that form the bulk of the diet. Both food availability/accessibility and tadpole feeding behaviour driven by nutritional needs may influence patterns of food acquisition. Given the importance of biofilms to tadpole diet, studies on the mechanisms by which tadpole nutritional needs and environmental conditions interact are likely to provide important insights into the dynamics of aquatic food webs.

Introduction

The anuran larval phase is subject to strong selective pressures imposed by predators, competitors, and other factors (Heyer, 1979; Wells, 2007). Tadpole diets are an important component of tadpole success because they can vary in amounts of carbohydrates, proteins, and lipids, which influence growth, development, and metamorphosis (Kupferberg, 1997a; Richter-Boix et al., 2007). For instance, a high quality diet can decrease time to metamorphosis (Kupferberg, 1997a) and consequently time exposed to aquatic predators (Heyer et al., 1975). On the other hand, predator presence may limit tadpole activity (Nomura et al., 2011) and access to microhabitats with better foraging opportunities (high quality food; Kupferberg, 1998).

Tadpoles can eat a variety of items that include attached algae or biofilms essentially composed of green algae, cyanobacteria, diatoms, and bacteria (Dickman, 1968), as well as organic matter, protozoans, pollen (Diaz-Paniagua, 1985), insects, and even other tadpoles or anuran eggs (Alford, 1999; Schiesari et al., 2009; Jefferson et al., 2014). Diatoms and other algae, as well as cyanobacteria, are rich in protein; green algae (Chlorophyta) also store high quantities of carbohydrates (Bold and Wynne, 1985) and represent important resources for tadpoles, especially those with a long larval stage (Kupferberg, 1997a). Diatoms are also especially important for larval nutrition due to their high lipid content (Gordon et al., 2006). Increased algae ingestion is likely to increase growth of consumers (Bowen et al., 1995), which, on the other hand, influence the dynamics of algae populations and aquatic food webs (Dickman, 1968; Kupferberg, 1997b).

Many aspects of the trophic ecology of tadpoles remain understudied, such as food selection, nutritional demands throughout ontogeny and even their actual trophic level in aquatic communities (Dutra and Callisto, 2005; Schiesari et al., 2009). Tadpoles have varied morphologies that enable them to forage in different microhabitats and likely consume different diets (Altig and Johnston, 1989; Altig and McDiarmid, 1999). Tadpoles are known to select microhabitats (Eterovick and Barata, 2006) and may alter their microhabitat use/selection throughout the year. However, assessed predation risk or microhabitat availability did not explain changes in microhabitat use, the causes of which remain to be understood (Eterovick et al., 2010). A recent study showed the availability of items consumed by tadpoles (unicellular and filamentous Zygnematophyceae and Bacillariophyceae, Cyanophyceae, pollen and testate amoebae) to vary among different types of microhabitats in streams (including the stream where the present study was conducted) and influence the diets of species using these microhabitats (JSK, CCF, and PCE, unpublished data). Diet is also likely to change with tadpole developmental stage (Souza-Filho et al., 2007). On the other hand, food items differ in digestibility, as well as in susceptibility to foraging consumers (Peterson and Jones, 2003). Thus, comprehensive studies on tadpole diet need to account for spatial and temporal variation in food consumption and take digestibility into account in order to understand the trophic status and ecological roles of tadpoles.

We chose the tadpole of Bokermannohyla saxicola (Bokermann, 1964) as a model to study diet composition and variation throughout the year of two different developmental stages. At four periods throughout the year, we selected five tadpoles in each of developmental stages 25 and 30 (sensu Gosner, 1960) to represent an initial stage and a more advanced stage (with developing hindlimbs), respectively. We assumed our stage 25 tadpoles were demanding a lot of energy for growth, while stage 30 tadpoles were investing more in limb development. We aimed to test the hypotheses that (1) tadpole diets will vary between the two developmental stages, which will likely differ in size and nutritional needs, and (2) tadpole diets will vary throughout the year due to expected changes in food availability (Ferragut et al., 2010) and patterns of microhabitat use by tadpoles (Eterovick et al., 2010). We expected tadpoles to prioritize consumption of items of higher nutritional value in the rainy, warm season, when productivity/food availability is likely to increase, which would result in narrower niches and greater niche overlap. On the other hand, we expected tadpole consumption to be less specific in the dry, cold season, when productivity/food availability decreases, or at larger sizes, due to constraints to attend the greater demands of a large body. We also expected niche overlaps to be greater within developmental stages than between them.

Materials and methods

Study site

The study was conducted at a third-order section (sensu Strahler, 1957) of Água Escura stream (19°16′1.2″S; 43°32′48.5″W, 1200 m alt., datum WGS 84). The stream is located inside the Parque Nacional da Serra do Cipó (PNSC), Brazil, and belongs to the Doce river basin. The stream has dissolved oxygen saturation from 77 to 137%, conductivity between 5.5 and 6.4 μS/cm, total alkalinity of 0.03 mEq/l and low nutrient concentrations, being characterized as oligotrophic (Mendes, 2003). Total phosphorus concentration is 15μg/l, and pH is between 4.23 and 6.88, corresponding to Type 4 in the classification of acidic streams proposed by Coring (1996). The stream bottom is mainly rocky with sand deposits, pebbles, or debris and some patches of aquatic vegetation. The climate presents cyclic seasonality, with a dry, cold season from April to September and a wet, warm season from October to March. Mean air temperature is 21.1°C and mean annual rainfall is 1622 mm (Eterovick and Sazima, 2004). The historical mean minimum and maximum temperatures in the sampling months, October, February, May and June (see next section), are 17 and 27°C, 18 and 27°C, 13 and 24°C, 11 and 24°C, respectively. Most of the rainfall is concentrated between October and February, with usually much less than 50 mm or no rainfall in May and June together (ICMBio, 2009).

Tadpole sampling

Tadpoles of Bokermannohyla saxicola (Anura, Hylidae) are present year-round in permanent streams, which makes them suitable for this study. The tadpoles take at least five months to develop (Eterovick and Brandão, 2001). They are benthic, mostly nocturnal and usually rest on rocks (Eterovick and Sazima, 2004). These tadpoles remain on the stream bottom (Eterovick and Sazima, 2004) and have eight (most commonly) to 11 denticle rows (Eterovick and Brandão, 2001) that enable them to scrape food items from surfaces of rocks, pebbles, and other substrates (see Altig and Johnston, 1989). The great number of denticle rows may enable them to eat even small diatoms of difficult access that remain closely attached to the substrate.

We collected tadpoles twice during the rainy season (October 2012 and February 2013) and twice during the dry season (May and June 2013). We expected the sampling months to represent the onset (October and May) and ongoing (February and June) periods of the rainy and dry seasons, respectively. From now on we refer to these periods as OW (onset wet: October), MW (middle wet: February), OD (onset dry: May), and MD (middle dry: June).

Bokermannohyla saxicola tadpoles hatch in stage 25 which has a relatively long duration (Eterovick and Brandão, 2001), and is when most growth takes place. We thus collected tadpoles within a size range that would probably be reached about one month after hatching (PCE, pers. obs.), thus avoiding recently hatched tadpoles that could have not filled their guts yet. We collected tadpoles with a dipnet, immediately euthanized them with 10% lidocaine, and preserved them in 5% formalin.

Data analyses

We measured tadpole total length, tail length, tail width, body length, and mouth width according to Altig and McDiarmid (1999). We performed t-tests to check for size differences in these measurements between the developmental stages considered when normality was observed in the dataset. For data violating assumptions of parametric tests, we performed Mann-Whitney tests. In order to make sure our sample was standardized throughout the year or account for increased growth at any specific sampling period, we conducted Kruskal-Wallis tests separately for stages 25 and 30 to compare tadpole dimensions among the four sampling periods. These analyses were performed in the software Systat (SYSTAT 12 for Windows. SYSTAT Software Inc., USA; https://systatsoftware.com).

We analyzed separately three segments of equal size (anterior, median, and posterior) of the digestive tract in order to account for digestion level throughout the gut. The anterior segment corresponded to the manicotto and most of the anterior small intestine; the median segment corresponded to the final portion of the anterior small intestine, inflection and the initial portion of the posterior small intestine; and the posterior segment corresponded to the rest of the posterior small intestine, colon and rectum (sensu Pryor and Bjorndal, 2005).

We macerated each segment, diluted its contents in 1 ml of distilled water and counted food items in a Sedgewick-Rafter counting chamber under a microscope with 10× magnification. We previously identified food items in a microscope with 100× magnification in order to be able to identify them correctly at the smaller magnification used with the counting chamber. We used diatoms to compare breakage/digestion level in different segments of tadpole guts because they were the most abundant food items and their frustules are resistant enough to be found in all portions of the gut, whereas other food items may suffer fast breakage/digestion and leave no traces. We quantified only intact diatoms (we considered empty frustules as digested diatoms). According to Altig et al. (2007), it is also possible that tadpoles may accidentally ingest empty diatom frustules while foraging on a substrate where these are abundant. We identified ingested items according to Bicudo and Menezes (2005) and Moresco et al. (2011). We used data from the anterior segment of the gut in subsequent analyses.

We represented tadpole diets based on the quantification of (1) number of cells and (2) biovolume of each food type ingested by each tadpole in two non-metric multidimensional scalings (NMDSs) with the package Vegan (Oksanen et al., 2016) in R (R Core Team, 2016). We used the same data to test for significance of developmental stage (25 or 30) and sampling period (OW, MW, OD, and MD) as well as their interactions to explain variation in diet composition with a PERMANOVA in the Vegan package. We calculated biovolume in μm3 based on Hillebrand et al. (1999), and estimated ingested biovolume as μm3/ml.

We tested our predictions on tadpole dietary niche breadth variation based on the number of cells and biovolume. We calculated niche breadth for each sampling period and each tadpole developmental stage using the Probability of Interspecific Encounter (PIE) diversity index in EcoSim 7.0 (Gotelli and Entsminger, 2001). The value of the PIE index ranges from 0 to 1 and can be interpreted as the probability that two randomly picked items (cells or μm3, respectively) from the sample represent two different items. We applied the index to food item diversity in the guts. We considered as significantly different niche breadths that did not overlap within the 95% range of estimated values (based on 1000 simulations).

Figure 1.

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Figure 1.

Material recorded in the anterior portion of Bokermannohyla saxicola tadpole guts at developmental stages 25 (black bars) and 30 (grey bars) throughout the year considering number of cells (A, C, E, G) and biovolume (B, D, F, H). A and B: Onset wet, C and D: middle wet, E and F: onset dry, G and H: middle dry (see text for details).

Citation: Amphibia-Reptilia 39, 4 (2018) ; 10.1163/15685381-17000209

To test our predictions on niche overlap, we calculated niche overlap (Ojk) between developmental stages and among the four sampling periods using Pianka’s (1973) index in EcoSim 7.0 (Gotelli and Entsminger, 2001). Estimates were obtained based on 1000 simulations and data from different stages/periods were compared through rarefaction considering the smallest number of food items as reference to standardize sample size. Values of p were adjusted through Bonferroni correction to minimize chances of type I error (Rice, 1989).

Results

Based on counts of cells, tadpole gut contents were dominated by diatoms (Bacillariophyceae) from five genera: Cymbella, Eunotia, Navicula, Nitzschia, and Sellaphora. Together, diatoms represented 86% and 80.9% of all cells ingested by stage 25 and stage 30 tadpoles, respectively (fig. 1). Other algae were also present, including Zygnemataceae (Mougeotia), Desmidiaceae (Actinotaenium, Bambusina, Cosmarium, Euastrum, Xanthidium), Mesotaeniaceae (Cylindrocystis), and Cyanobacteria (Phormidium) (fig. 1A, 1C, 1E, 1G). Each genus was represented by a single species, except for Euastrum, which was represented by five different species, and Xanthidium, which was represented by two. We also recorded pollen and testate amoebae (Arcella sp.), vegetal remains, sand grains, eggs, and limbs and antennae of aquatic invertebrates and microcrustaceans (whose digestion level impaired identification). When we evaluated biomass instead of number of cells, Bambusina and Mougeotia (Zygnematophyceae) accounted for most of the volume in gut contents due to their large cells (60.9% of volume in stage 25 and 65.1% in stage 30 tadpoles); this was not the case for some small Zygnematophyceae, such as Euastrum, Cosmarium, Cylindrocystis, Actinotaenium and Xanthidium. Large non-photosyntesizing items such as testate amoebae (Rhizopoda) and pollen represented together 17.9% and 12.6% of ingested volume in stage 25 and 30 tadpoles, respectively (fig. 1B, 1D, 1F, 1H). On the other hand, diatoms represented only 12.8% and 10.7% of the volume ingested by stage 25 and stage 30 tadpoles, respectively.

The amount and variety of food items was markedly greater in the anterior segment of tadpole guts compared to median and posterior segments, so we conducted all the subsequent analyses based only on the anterior segment. The only remaining identifiable items in median and posterior gut segments were diatoms, while all the other items seemed to be digested before they reached these segments. Tadpoles in developmental stage 25 were significantly smaller than tadpoles in stage 30 (table 1). However, tadpole dimensions did not differ significantly among sampling periods for stages 25 or 30 (results not shown).

Table 1.

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Table 1.

Measurements of Bokermannohyla saxicola tadpoles in developmental stages 25 (n = 20) and 30 (n = 20) (sensu Gosner, 1960). Data is presented as mean ± SD. Stages were compared with Mann-Whitney or t-tests for non-normal and normal data, respectively (significance level considered as p < 0.05).

Citation: Amphibia-Reptilia 39, 4 (2018) ; 10.1163/15685381-17000209

Tadpoles differed in their diets between developmental stages 25 and 30 considering number of cells (MS = 0.325, F = 3.950, df = 1, p = 0.002) but not biovolume (MS = 0.254, F = 1.175, df = 1, p = 0.284) of food types. On the other hand, tadpoles differed in their diets among sampling periods considering both number of cells (MS = 0.536, F = 6.505, df = 3, p = 0.001) and biovolume (MS = 0.461, F = 2.135, df = 3, p = 0.022) of food types. The interactions between developmental stage and sampling periods were significant considering both number of cells (MS = 0.374, F = 4.544, df = 3, p = 0.001) and biovolume (MS = 0.482, F = 2.233, df = 3, p = 0.009) of food types. The NMDSs provided a reasonable spatial representation of the data considering that it included 20 dimensions, each one represented by a food type (number of cells: stress = 0.233, rmse = 0.035, max. resid. = 0.125; fig. 2A; biovolume: stress = 0.234, rmse = 0.001, max. resid. = 0.005; fig. 2B).

Figure 2.

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Figure 2.

NMDS showing classification of tadpole diets based on number of cells (A) and biovolume (B) of food items for eight groups given by the combination of two developmental stages (25 and 30 sensu Gosner, 1960) and four sampling periods (OW = onset wet, MW = middle wet, OD = onset dry, MD = middle dry; see text for additional details). Species included in the polygon representing each group are those consumed more by that group than by other groups. Each dot represents one tadpole, and colors correspond to groups (stage × sampling period). Sampling periods within the wet season are marked in green for stage 25 tadpoles and in orange for stage 30 tadpoles. Sampling periods within the dry season are marked in blue for stage 25 tadpoles and in yellow for stage 30 tadpoles.

Citation: Amphibia-Reptilia 39, 4 (2018) ; 10.1163/15685381-17000209

Tadpole dietary niches based on number of cells ingested were broader during the dry season (OD and MD) than during the wet season, and differed among all sampling periods, except for stage 30 tadpoles between OD and MD (table 2). Niches were always broader for stage 30 compared to stage 25 tadpoles within the same period (table 2). Niche overlap was higher than expected by chance among sampling periods for both stage 25 (Ojk = 0.895, p < 0.0001) and stage 30 tadpoles (Ojk = 0.766, p < 0.0001). Niche overlap was also higher than expected by chance between the tadpole developmental stages considered in the middle of both seasons (MW: Ojk = 0.974, p < 0.0001; MD: Ojk = 0.972, p < 0.0001). In the onset of both seasons niche overlap between tadpole stages did not differ from random (OW: Ojk = 0.501, p = 0.052; non-significant after Bonferroni correction; OD: Ojk = 0.799, p = 0.258).

Table 2.

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Table 2.

Estimatives of niche breadth based on (1) number of cells and (2) biovolume of food types for Bokermannohyla saxicola in developmental stages 25 and 30 (sensu Gosner, 1960) throughout the year: OW = onset wet, MW = middle wet, OD = onset dry, MD = middle dry (see text for further details). Estimatives were obtained based on 1000 simulations and data from different stages/periods were compared through rarefaction considering the smallest number of items/biovolume ingested (n = 18 440 and n = 1 213 210.2 μm3/ml, respectively) as reference. Different letters (last column) indicate significantly different results (p < 0.05) within the analyses (number of cells or biovolume).

Citation: Amphibia-Reptilia 39, 4 (2018) ; 10.1163/15685381-17000209

Tadpole dietary niches showed a different pattern when biovolume was considered instead of number of cells. Niches were broader during the wet season, except for stage 25 tadpoles in MW, whose niches were the narrowest. Niches were broader for stage 25 than stage 30 tadpoles, except for MW, when stage 30 tadpoles had broader niches than stage 25 tadpoles. Niche overlap was still higher than expected by chance among sampling periods for both stage 25 (Ojk = 0.604, p < 0.0001) and stage 30 tadpoles (Ojk = 0.966, p < 0.0001). Niche overlap was higher than expected by chance between tadpole developmental stages considered in the middle of the wet season (MW: Ojk = 0.977, p < 0.0001) and at the onset of both seasons (OW: Ojk = 0.808, p < 0.0001; OD: Ojk = 0.934, p = 0.006), but not in the middle of the dry season (MD: Ojk = 0.375, p = 0.113).

Discussion

The prevalence of pennate diatoms, Zygnemataceae and Desmidiaceae in tadpole guts suggests reliance of Bokermannohyla saxicola tadpoles on biofilms for feeding. Thus, the diet of Bokermannohyla saxicola tadpoles seems to be in accordance with their ecomorphological type (benthic tadpoles, sensu Altig and Johnston, 1989). Biofilm algae are important primary producers in several aquatic habitats, including rivers (Stevenson, 1996; Vadeboncoeur et al., 2008; Pellegrini and Ferragut, 2012), and are affected by light, nutrient availability (Stevenson, 1996; Boëchat et al., 2011; Pellegrini and Ferragut, 2012) and pH (Müller, 1980). The low pH of the studied stream was likely favoring a high abundance of diatoms (JSK, CCF and PCE, unpublished data). Diatoms are small planktonic or periphytic autotrophic unicellular organisms that possess a cell wall (frustule) composed of two silicate shells. Under experimental conditions, they dominated under low pH values (Müller, 1980). They are very abundant in aquatic systems and important in the diets of other trophic levels, such as zooplankton (Liu and Wu, 2016) and tadpoles (Souza-Filho et al., 2007; Santos et al., 2016).

Tadpoles can also be opportunistic and exploit nutritious food items that become available to them at different periods or habitats (Petranka and Kennedy, 1999; Schiesari et al., 2009). For instance, benthic tadpoles are also likely to exploit other microhabitats for food, such as the water surface for pollen (Wagner, 1986), known to be a nutritive food for several groups of organisms (Filipiak, 2016). Bokermannohyla saxicola ingested pollen (from plants of the family Asteraceae) in both seasons and in both developmental stages considered in the present study. Alternatively, pollen could have sank and become available for them on the bottom. Sand grains were also present in the guts and could have been ingested accidentally or intentionally, to take advantage of the film of bacteria covering them or to physically improve the breakage of food in the gut (Sousa-Filho et al., 2007).

Some previous studies have analyzed the entire digestive tract of tadpoles (e.g., Sousa-Filho et al., 2007), which may overestimate items that are difficult to digest. Rossa-Feres et al. (2004) used the initial portion of tadpole intestines to analyze diet and stated that they observed no differences in food quantity and composition throughout the entire intestine, although they provided no data or detailed information on how this comparison was done. Our comparison of level of digestion (i.e. food breakage) throughout the gut had to be based on diatoms due to their predominance in the diet of B. saxicola, but showed high digestibility of these algae. Although our results were based only on diatoms, we recommend that tadpole diet studies use the anterior portion of the gut in order to minimize the problem of overlooking small easily digested items (see Hoff et al., 1999). This problem is corroborated by the fact that we only observed other food items (likely to be more easily broken/digested) in the initial portion of the gut.

Bokermannohyla saxicola tadpoles in both developmental stages exhibited a narrower trophic niche (considering number of cells) during the rainy season than during the dry season, as we expected. That is, increased algae productivity and diversity (e.g. Souza et al., 2015) may favor increased consumption of more energetic items, as we predicted. However, considering biovolume, stage 25 tadpoles had the narrowest niches in MW, otherwise niches were broader in the rainy season. Mougeotia is one of the diet components with the largest total volume, thus the increased ingestion of more nutritive items (like diatoms) during the rainy, warm season may reduce the dominance of Mougeotia and other large items in biovolume, explaining the increase in niche breadth. Higher tadpole metabolism during the rainy, warm season would explain an increased consumption of energetic food items, like diatoms (see fig. 1A, 1C). Diatoms are an important source of organic nutrients, mainly lipidic compounds such as PUFA (polyunsaturated fatty acids) and EPA (eicopentaenoic acid; Napiórkowska-Krzebietke, 2016). Diets enriched with diatoms can boost development and allow tadpoles to metamorphose into larger froglets (Kupferberg, 1997a).

Changes in tadpole diet are likely favored by the dynamics of benthic communities and availability of food items, which show temporal variations (Sandefur et al., 2011; Souza et al., 2015). Tadpoles can ingest high amounts of carbohydrates and lipids to capitalize growth (Richter-Boix et al., 2007) and development. Food types vary in nutrient content and can contribute to complement nutritional needs of tadpoles (Gordon et al., 2006). Knowledge on the dynamics of benthic communities on natural substrates is rare in general, but seasonal changes have been shown to occur (Ferragut et al., 2010; Pellegrini and Ferragut, 2012). For instance, periphyton algae biovolume, biomass and species richness are likely to be higher in the summer (Souza et al., 2015). The initial development of periphyton includes colonization of exposed substrates and development of a diatom biofilm. Filamentous algae will then colonize mature communities that may lose fragments due to stream current and allow recolonization (Sigee, 2005). Filamentous green algae, like Mougeotia and Bambusina, usually grow in clouds in microhabitats with slow flowing water because they usually lack structures to attach themselves to the bottom (CCF, pers. obs.). On the other hand, periphyton consumers are expected to change the composition of this benthic community due to direct consumption or nutrient enrichment via excretion (Furey et al., 2012). Periphyton grazers may also promote stability by avoiding excessive growth and thus reducing susceptibility of the thin biofilm to removal by currents (Pringle and Hamazaki, 1997).

We consider that the consumption of diatoms by tadpoles of B. saxicola in this study seems indeed to be greater at the onset of the rainy season, when diatoms would be expected to colonize substrates scoured by heavy rains (Sigee, 2005). The consumption of Mougeotia subsequently increased, probably with its availability, as periphyton succession progressed. We noticed the filamentous green algae Mougeotia to be most consumed by tadpoles of both stages in the middle of the wet season and at the onset of the dry season. Mougeotia was present in large amounts in the diet of B. saxicola tadpoles (present study) and has been detected in the diets of tadpoles of other species as well (Dickman, 1968; Huckembeck et al., 2016), despite having low nutritional value (Kupferberg et al., 1994).

Bokermannohyla saxicola tadpoles in stage 30 were larger and had broader niches than tadpoles in stage 25, considering number of food items, as we expected. Increased size and developmental stage also resulted in a more diversified diet in tadpoles of Scinax angrensis (Sousa-Filho et al., 2007). Schiesari et al. (2009) detected ontogenetic shifts in the diets of Lithobates species as well. Mouth size alone may not explain the variation in tadpole diet during different developmental stages because tadpoles are usually efficient in consuming a broad array of food items of different sizes (Alford, 1999). However, increased size and experience may enable tadpoles to move more and explore microhabitats with different food availability. The gut of B. saxicola tadpoles in developmental stage 30 had a 14.6% increase in length compared to stage 25, which could also influence the amount of ingested items stored in the intestine, contributing to the characterization of a broader dietary niche. The qualitative compositions of diets of stage 25 and stage 30 tadpoles were similar (see fig. 1), but the relative amounts of each food item ingested changed between stages and among sampling periods. We did not notice an increase in consumption by stage 30 tadpoles of food items that are hard to digest and would require a longer gut to be efficiently broken and digested. Actually, developmental stages did not differ considering volume of food items ingested. Gut size is likely to present allometric variation with tadpole size, and the associated changes in diet composition/digestion deserve further study.

Niche overlaps (based on number of cells) between tadpole developmental stages were higher than expected in the middle of both seasons but did not differ from random at the onset of either season. The onset of seasons may represent a transition period, before the patterns of food availability and consumption of the season are well established. Considering biovolume, however, the pattern changed, with niches overlapping more than expected by chance between tadpole developmental stages in all sampling periods but MD. The similarities or differences in the consumption of a few large food items (e.g. Mougeotia sp., Bambusina sp., testate amoebae) are likely responsible for the observed pattern. We recommend that biovolume is also considered when studying tadpole diets, since food items vary greatly in size. The niche analyses based on biovolume seemed to be highly influenced by the consumption of Mougeotia sp. (see fig. 1B, 1D, 1F, 1H), which is by far the largest food item (5457.9 μm3). The remaining food items varied from 5.1 μm3 (Eunotia) to 982 μm3 (Actinotaenium).

Tadpoles of the same stage showed higher than expected dietary niche overlap across all sampling periods, considering both number of cells and biovolume, despite any eventual seasonal changes in food availability (not measured). Besides, stage 30 tadpoles did not differ in size throughout the year, showing ability to grow equally in likely different temporal contexts of food availability. These results indicate an ability to exploit available resources based on the nutritional needs of each developmental stage (Richter-Boix et al., 2007). Although we found the same result for size of stage 25 tadpoles, this should be a methodological artifact because we made an effort to standardize tadpole size when sampling this developmental stage (that encompasses a great size range).

In conclusion, biofilm communities are important for B. saxicola tadpole development, since they constitute the main source of food for these tadpoles. We have shown that proportions of ingested food items are likely to change throughout the year and interact with developmental stages. That is, where and when tadpoles eat determine what they eat. The causes could be food availability/accessibility through time and space, behavioral adjustments to changing nutritional needs, or a combination of both, which remains to be investigated. Knowledge of tadpole diet is important for understanding aquatic food webs (Kupferberg, 1997b; Dutra and Callisto, 2005; Schiesari et al., 2009) and understanding the ecological consequences of the extinction of these grazers in ecosystems (Ranvestel et al., 2004; Altig et al., 2007). We believe there is a need for more studies on the diet of tropical tadpoles, as well as internal (e.g. food preference, nutritional needs) and external (e.g. food availability, microhabitat use vs. predator avoidance) factors that control its composition. Then we will make progress in understanding how impacts on aquatic habitats and periphyton communities affect tadpole diet and development.

Corresponding author; e-mail: pceterovick@gmail.com

Acknowledgements

We are grateful to G. Rodrigues and I. Moreira for help during field work; to Sarah Kupferberg, Dale Jefferson and two anonymous reviewers for comments on a previous version of the manuscript; to Erik R. Wild for revision of the English; to the Parque Nacional da Serra do Cipó staff for logistic support; to Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig) and Pontifícia Universidade Católica de Minas Gerais for finantial support; and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a Research Productivity grant (304422/2014-2) provided to P. C. Eterovick. Collection permits were provided by Sisbio/ICMBio (31398-1).

References

  • AlfordR.A. (1999): Ecology. Resource use, competition, and predation. In: Tadpoles. The Biology of Anuran Larvae p. 240-278. McDiarmidR.W.AltigR. Eds The University of Chicago PressChicago, IL.

  • AltigR.JohnstonG.F. (1989): Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol. Monogr. 3: 81-109.

  • AltigR.McDiarmid R.W. (1999): Diversity: familial and generic characterizations. In: Tadpoles. The Biology of Anuran Larvae p. 295-337. McDiarmidR.W.AltigR. Eds The University of Chicago PressChicago, IL.

  • AltigR.WhilesM.R.Taylor C.L. (2007): What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshw. Biol. 52: 386-395.

  • BicudoC.E.M.MenezesM. (2005): Gêneros de Algas Continentais do Brasil. Rima EditoresSão Carlos, Brazil.

  • BoëchatI.G.KrügerA.GianiA.FigueredoC.C.GückerB. (2011): Agricultural land use affects the nutritional quality of stream microbial communities. FEMS Microbiol. Ecol. 77: 568-576.

  • BokermannW.C.A. (1964): Dos nuevas especies de Hyla de Minas Gerais y notas sobre Hyla alvarengai. (Amphibia, Salientia, Hylidae). Neotropica 10: 67-76.

  • BoldH.C.Wynne M.J. (1985): Introduction to the Algae: Structure and Reproduction. Prentice-HallEnglewood Cliffs, NJ.

  • BowenS.H.LutzE.V.AhlgrenM.O. (1995): Dietary protein and energy as determinants of food quality: trophic strategies compared. Ecology 76: 899-907.

  • CoringE. (1996): Use of diatoms for monitoring acidification in small mountain rivers in Germany with special emphasis on “diatom assemblage type analysis”. In: Use of Algae for Monitoring Rivers II p. 7-16. WhittonB.A.RottE. Eds Institut for Botanik, Universitat InnsbruckInnsbruck, Austria.

  • Diaz-PaniaguaC. (1985): Larval diets related to morphological characters of five anuran species in the biological reserve of Donana (Huelva, Spain). Amphibia-Reptilia 6: 307-322.

  • DickmanM. (1968): The effect of grazing by tadpoles on the structure of a periphyton community. Ecology 49: 1188-1190.

  • DutraS.L.CallistoM. (2005): Macroinvertebrates as tadpole food: importance and body size relationships. Rev. Bras. Zool. 22: 923-927.

  • EterovickP.C.BarataI.M. (2006): Distribution of tadpoles within and among Brazilian streams: the influence of predators, habitat size and heterogeneity. Herpetologica 62: 365-377.

  • EterovickP.C.BrandãoR.A. (2001): A description of the tadpoles and advertisement calls of members of the Hyla pseudopseudis group. J. Herpetol. 35: 442-450.

  • EterovickP.C.SazimaI. (2004): Amphibians From the Serra do Cipó Minas Gerais Brazil. Editora PUC MinasBelo Horizonte, Brazil.

  • EterovickP.C.LazarottiI.FrancoB.P.DiasC.J. (2010): Seasonal variation of tadpole spatial niches in permanent streams: the roles of predation risk and microhabitat availability. Austral. Ecol. 35: 879-887.

  • FerragutC.RodelloA.F.BicudoC.E.M. (2010): Seasonal variability of periphyton nutrient status and biomass on artificial and natural substrates in a tropical mesotrophic reservoir. Acta Limnol. Bras. 22: 397-409.

  • FilipiakM. (2016): Pollen stoichiometry may influence detrital terrestrial and aquatic food webs. Front. Ecol. Evol. 4: 138.

  • FureyP.C.LoweR.L.Power M.E.Campbell-CravenA.M. (2012): Midges, Cladophora, and epiphytes: shifting interactions through succession. Freshw. Sci. 31: 93-107.

  • GordonN.NeoriA.ShpigelM.LeeJ.HarpazS. (2006): Effect of diatom diets on growth and survival of the abalone Haliotis discus hannai postlarvae. Aquaculture 252: 225-233.

  • GosnerK.L. (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183-190.

  • GotelliN.J.Entsminger G.L. (2001): EcoSim: null models software for ecology. Version 7.0. Acquired Intelligence Inc. and Kesey Bear Jericho VT [cited 2012 July 10]. Available from: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html.

  • HeyerW.R. (1979): Annual variation in larval amphibian populations within a temperate pond. J. Wash. Acad. Sci. 69: 65-74.

  • HeyerW.R.McDiarmid R.W.Weigmann D.L. (1975): Tadpoles, predation and pond habitats in the tropics. Biotropica 7: 100-111.

  • HillebrandH.DürselenC.-D.KirschtelD.PollingherU.ZoharyT. (1999): Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35: 403-424.

  • HoffK.S.BlausteinA.R.McDiarmidR.W.AltigR. (1999): Behavior: interactions and their consequences. In: Tadpoles. The Biology of Anuran Larvae p. 215-239. McDiarmidR.W.AltigR. Eds The University of Chicago PressChicago, IL.

  • HuckembeckS.AlvesL.T.LoebmannD.GarciaA.M. (2016): What the largest tadpole feeds on? A detailed analysis of the diet composition of Pseudis minuta tadpoles (Hylidae, Dendropsophini). An. Acad. Bras. Ciênc. 88: 1397-1400.

  • ICMBio (2009): Plano de Manejo. Parque Nacional da Serra do Cipó e Área de Proteção Ambiental Morro da Pedreira. Instituto Chico Mendes Brasília Brazil.

  • JeffersonD.M.Hobson K.A.Demuth B.S.Ferrari M.C.Chivers D.P. (2014): Frugal cannibals: how consuming conspecific tissues can provide conditional benefits to wood frog tadpoles (Lithobates sylvaticus). Naturwissenschaften 101: 291-303.

  • KupferbergS.J. (1997a): The role of larval diet in anuran metamorphosis. Am. Zool. 37: 146-159.

  • KupferbergS.J. (1997b): Facilitation of periphyton production by tadpole grazing: functional differences between species. Freshw. Biol. 37: 427-439.

  • KupferbergS.J. (1998): Predator mediated patch use by tadpoles (Hyla regilla): risk balancing or consequence of motionlessness? J. Herpetol. 32: 84-92.

  • KupferbergS.J.MarksJ.C.PowerM.E. (1994): Effects of variation in natural algal and detrital diets on larval anuran (Hyla regilla) life history traits. Copeia 1994: 446-457.

  • LiuH.WuC.J. (2016): Effect of the silica content of diatom prey on the production, decomposition and sinking of fecal pellets of the copepod Calanus sinicus. Biogeosciences 13: 4767-4775.

  • MendesR.S. (2003): Experimentos de enriquecimento in situ: respostas de algas bentônicas a adição de nutrientes em um córrego de Altitude da Serra do Cipó – MG. Master’s Thesis Federal University of Minas Gerais Brazil.

  • MorescoC.Tremarin P.I.LudwigT.A.V.RodriguesL. (2011): Diatomáceas perifíticas abundantes em três córregos com diferentes ações antrópicas em Maringá, PR, Brasil. Rev. Bras. Bot. 34: 359-373.

  • MüllerP. (1980): Effects of artificial acidification on the growth of periphyton. Can. J. Fish. Aquat. Sci. 37: 355-363.

  • Napiórkowska-KrzebietkeA. (2016): Phytoplankton as a basic nutritional source in the diet of fish. J. Elementol. 22: 831-841.

  • NomuraF.PradoV.H.M.SilvaF.R.BorgesR.E.DiasN.Y.N.Rossa-FeresD.C. (2011): Are you experienced? Predator type and predator experience trade-offs in relation to tadpole mortality rates. J. Zool. 284: 144-150.

  • OksanenJ.BlanchetF.G.FriendlyM.KindtR.LegendreP.McGlinnD.MinchinP.R.O’HaraR.B.SimpsonG.L.SolymosP.HenryM.StevensH.SzoecsE.WagnerH. (2016): Vegan: community ecology package. R package version 2.4-1. Available from: https://CRAN.R-project.org/package=vegan.

  • PellegriniB.G.FerragutC. (2012): Variação sazonal e sucessional da comunidade de algas perifíticas em substrato natural em um reservatório mesotrófico tropical. Acta Bot. Bras. 26: 810-821.

  • PetersonC.G.Jones T.L. (2003): Diatom viability in insect fecal material: comparison between two species, Achnanthidium lanceolatum and Synedra ulna. Hydrobiologia 501: 93-99.

  • PetrankaJ.W.Kennedy C.A. (1999): Pond tadpoles with generalized morphology: is it time to reconsider their functional roles in aquatic communities? Oecologia 120: 621-631.

  • PiankaE.R. (1973): The structure of lizard communities. Ann. Rev. Ecol. Syst. 4: 53-74.

  • PringleC.M.HamazakiT. (1997): Effects of fishes on algal response to storms in a tropical stream. Ecology 78: 2432-2442.

  • PryorG.S.BjorndalK.A. (2005): Symbiotic fermentation, digesta passage, and gastrointestinal morphology in bullfrog tadpoles (Rana catesbeiana). Physiol. Biochem. Zool. 78: 201-215.

  • R Core Team (2016): R: a Language and Environment for Statistical Computing. The R Foundation for Statistical ComputingVienna, Austria. Version 3.2.4. Available from: https://cran.r-project.org/.

  • RanvestelA.W.LipsK.R.PringleC.M.WhilesM.R.BixbyR.J. (2004): Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshw. Biol. 49: 274-285.

  • RiceW.R. (1989): Analyzing tables of statistical tests. Evolution 43: 223-225.

  • Richter-BoixA.LlorenteG.A.MontoriA.GarciaJ. (2007): Tadpole diet selection varies with the ecological context in predictable ways. Basic Appl. Ecol. 8: 464-474.

  • Rossa-FeresD.C.JimJ.FonsecaM.G. (2004): Diets of tadpoles from a temporary pond in southeastern Brazil (Amphibia, Anura). Rev. Bras. Zool. 21: 745-754.

  • SandefurH.N.MatlockM.D.CostelloT.A. (2011): Seasonal productivity of a periphytic algal community for biofuel feedstock generation and nutrient treatment. Ecol. Eng. 37: 1476-1480.

  • SantosF.J.M.ProtázioA.S.MouraC.W.N.JuncáF. (2016): Diet and food resource partition among benthic tadpoles of three anuran species in Atlantic Forest tropical streams. J. Freshw. Ecol. 31: 53-60.

  • SchiesariL.WernerE.E.KlingG.W. (2009): Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology. Freshw. Biol. 54: 572-586.

  • SealeD.B. (1980): Influence of amphibian larvae on primary production, nutrient flux, and competition in a pond ecosystem. Ecology 61: 1531-1550.

  • SigeeD.C. (2005): Freshwater Microbiology: Biodiversity and Dynamic Interactions of Microorganisms in the Aquatic Environment. WileyChichester.

  • Sousa-FilhoI.F.BrancoC.C.TellesM.P.SilvaG.R.SabaghL.T. (2007): The diet of Scinax angrensis (Lutz) tadpoles in an area of the Atlantic Florest (Mangaratiba, Rio de Janeiro) (Amphibia, Anura, Hylidae). Rev. Bras. Zool. 24: 965-970.

  • SouzaM.L.PellegriniB.G.FerragutC. (2015): Periphytic algal community structure in relation to seasonal variation and macrophyte richness in a shallow tropical reservoir. Hydrobiologia 755: 183-196.

  • StevensonJ.R. (1996): An introduction to algal ecology in freshwater benthic habitats. In: Algal Ecology: Freshwater Benthic Ecosystems p. 3-30. StevensonR.J.BothwellM.L.LoweR.L. Eds Academic PressSan Diego, CA.

  • StrahlerA.N. (1957): Quantitative analysis of watershed morphology. Trans. Amer. Geophys. Union 38: 913-920.

  • VadeboncoeurY.PetersonG.JakeM.ZandenV.KalffJ. (2008): Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89: 2542-2552.

  • WagnerW.E. (1986): Tadpoles and pollen: observations on the feeding behavior of Hyla regilla larvae. Copeia 1986: 802-804.

  • WellsK.D. (2007): The Ecology and Behavior of Amphibians. The University of Chicago PressChicago, IL.

Associate Editor: Julian Glos.

If the inline PDF is not rendering correctly, you can download the PDF file here.

You are what, where, and when you eat: seasonal and ontogenetic changes in a tropical tadpole’s diet

in Amphibia-Reptilia

Sections

References

  • AlfordR.A. (1999): Ecology. Resource use, competition, and predation. In: Tadpoles. The Biology of Anuran Larvae p. 240-278. McDiarmidR.W.AltigR. Eds The University of Chicago PressChicago, IL.

  • AltigR.JohnstonG.F. (1989): Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol. Monogr. 3: 81-109.

  • AltigR.McDiarmid R.W. (1999): Diversity: familial and generic characterizations. In: Tadpoles. The Biology of Anuran Larvae p. 295-337. McDiarmidR.W.AltigR. Eds The University of Chicago PressChicago, IL.

  • AltigR.WhilesM.R.Taylor C.L. (2007): What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshw. Biol. 52: 386-395.

  • BicudoC.E.M.MenezesM. (2005): Gêneros de Algas Continentais do Brasil. Rima EditoresSão Carlos, Brazil.

  • BoëchatI.G.KrügerA.GianiA.FigueredoC.C.GückerB. (2011): Agricultural land use affects the nutritional quality of stream microbial communities. FEMS Microbiol. Ecol. 77: 568-576.

  • BokermannW.C.A. (1964): Dos nuevas especies de Hyla de Minas Gerais y notas sobre Hyla alvarengai. (Amphibia, Salientia, Hylidae). Neotropica 10: 67-76.

  • BoldH.C.Wynne M.J. (1985): Introduction to the Algae: Structure and Reproduction. Prentice-HallEnglewood Cliffs, NJ.

  • BowenS.H.LutzE.V.AhlgrenM.O. (1995): Dietary protein and energy as determinants of food quality: trophic strategies compared. Ecology 76: 899-907.

  • CoringE. (1996): Use of diatoms for monitoring acidification in small mountain rivers in Germany with special emphasis on “diatom assemblage type analysis”. In: Use of Algae for Monitoring Rivers II p. 7-16. WhittonB.A.RottE. Eds Institut for Botanik, Universitat InnsbruckInnsbruck, Austria.

  • Diaz-PaniaguaC. (1985): Larval diets related to morphological characters of five anuran species in the biological reserve of Donana (Huelva, Spain). Amphibia-Reptilia 6: 307-322.

  • DickmanM. (1968): The effect of grazing by tadpoles on the structure of a periphyton community. Ecology 49: 1188-1190.

  • DutraS.L.CallistoM. (2005): Macroinvertebrates as tadpole food: importance and body size relationships. Rev. Bras. Zool. 22: 923-927.

  • EterovickP.C.BarataI.M. (2006): Distribution of tadpoles within and among Brazilian streams: the influence of predators, habitat size and heterogeneity. Herpetologica 62: 365-377.

  • EterovickP.C.BrandãoR.A. (2001): A description of the tadpoles and advertisement calls of members of the Hyla pseudopseudis group. J. Herpetol. 35: 442-450.

  • EterovickP.C.SazimaI. (2004): Amphibians From the Serra do Cipó Minas Gerais Brazil. Editora PUC MinasBelo Horizonte, Brazil.

  • EterovickP.C.LazarottiI.FrancoB.P.DiasC.J. (2010): Seasonal variation of tadpole spatial niches in permanent streams: the roles of predation risk and microhabitat availability. Austral. Ecol. 35: 879-887.

  • FerragutC.RodelloA.F.BicudoC.E.M. (2010): Seasonal variability of periphyton nutrient status and biomass on artificial and natural substrates in a tropical mesotrophic reservoir. Acta Limnol. Bras. 22: 397-409.

  • FilipiakM. (2016): Pollen stoichiometry may influence detrital terrestrial and aquatic food webs. Front. Ecol. Evol. 4: 138.

  • FureyP.C.LoweR.L.Power M.E.Campbell-CravenA.M. (2012): Midges, Cladophora, and epiphytes: shifting interactions through succession. Freshw. Sci. 31: 93-107.

  • GordonN.NeoriA.ShpigelM.LeeJ.HarpazS. (2006): Effect of diatom diets on growth and survival of the abalone Haliotis discus hannai postlarvae. Aquaculture 252: 225-233.

  • GosnerK.L. (1960): A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183-190.

  • GotelliN.J.Entsminger G.L. (2001): EcoSim: null models software for ecology. Version 7.0. Acquired Intelligence Inc. and Kesey Bear Jericho VT [cited 2012 July 10]. Available from: http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html.

  • HeyerW.R. (1979): Annual variation in larval amphibian populations within a temperate pond. J. Wash. Acad. Sci. 69: 65-74.

  • HeyerW.R.McDiarmid R.W.Weigmann D.L. (1975): Tadpoles, predation and pond habitats in the tropics. Biotropica 7: 100-111.

  • HillebrandH.DürselenC.-D.KirschtelD.PollingherU.ZoharyT. (1999): Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35: 403-424.

  • HoffK.S.BlausteinA.R.McDiarmidR.W.AltigR. (1999): Behavior: interactions and their consequences. In: Tadpoles. The Biology of Anuran Larvae p. 215-239. McDiarmidR.W.AltigR. Eds The University of Chicago PressChicago, IL.

  • HuckembeckS.AlvesL.T.LoebmannD.GarciaA.M. (2016): What the largest tadpole feeds on? A detailed analysis of the diet composition of Pseudis minuta tadpoles (Hylidae, Dendropsophini). An. Acad. Bras. Ciênc. 88: 1397-1400.

  • ICMBio (2009): Plano de Manejo. Parque Nacional da Serra do Cipó e Área de Proteção Ambiental Morro da Pedreira. Instituto Chico Mendes Brasília Brazil.

  • JeffersonD.M.Hobson K.A.Demuth B.S.Ferrari M.C.Chivers D.P. (2014): Frugal cannibals: how consuming conspecific tissues can provide conditional benefits to wood frog tadpoles (Lithobates sylvaticus). Naturwissenschaften 101: 291-303.

  • KupferbergS.J. (1997a): The role of larval diet in anuran metamorphosis. Am. Zool. 37: 146-159.

  • KupferbergS.J. (1997b): Facilitation of periphyton production by tadpole grazing: functional differences between species. Freshw. Biol. 37: 427-439.

  • KupferbergS.J. (1998): Predator mediated patch use by tadpoles (Hyla regilla): risk balancing or consequence of motionlessness? J. Herpetol. 32: 84-92.

  • KupferbergS.J.MarksJ.C.PowerM.E. (1994): Effects of variation in natural algal and detrital diets on larval anuran (Hyla regilla) life history traits. Copeia 1994: 446-457.

  • LiuH.WuC.J. (2016): Effect of the silica content of diatom prey on the production, decomposition and sinking of fecal pellets of the copepod Calanus sinicus. Biogeosciences 13: 4767-4775.

  • MendesR.S. (2003): Experimentos de enriquecimento in situ: respostas de algas bentônicas a adição de nutrientes em um córrego de Altitude da Serra do Cipó – MG. Master’s Thesis Federal University of Minas Gerais Brazil.

  • MorescoC.Tremarin P.I.LudwigT.A.V.RodriguesL. (2011): Diatomáceas perifíticas abundantes em três córregos com diferentes ações antrópicas em Maringá, PR, Brasil. Rev. Bras. Bot. 34: 359-373.

  • MüllerP. (1980): Effects of artificial acidification on the growth of periphyton. Can. J. Fish. Aquat. Sci. 37: 355-363.

  • Napiórkowska-KrzebietkeA. (2016): Phytoplankton as a basic nutritional source in the diet of fish. J. Elementol. 22: 831-841.

  • NomuraF.PradoV.H.M.SilvaF.R.BorgesR.E.DiasN.Y.N.Rossa-FeresD.C. (2011): Are you experienced? Predator type and predator experience trade-offs in relation to tadpole mortality rates. J. Zool. 284: 144-150.

  • OksanenJ.BlanchetF.G.FriendlyM.KindtR.LegendreP.McGlinnD.MinchinP.R.O’HaraR.B.SimpsonG.L.SolymosP.HenryM.StevensH.SzoecsE.WagnerH. (2016): Vegan: community ecology package. R package version 2.4-1. Available from: https://CRAN.R-project.org/package=vegan.

  • PellegriniB.G.FerragutC. (2012): Variação sazonal e sucessional da comunidade de algas perifíticas em substrato natural em um reservatório mesotrófico tropical. Acta Bot. Bras. 26: 810-821.

  • PetersonC.G.Jones T.L. (2003): Diatom viability in insect fecal material: comparison between two species, Achnanthidium lanceolatum and Synedra ulna. Hydrobiologia 501: 93-99.

  • PetrankaJ.W.Kennedy C.A. (1999): Pond tadpoles with generalized morphology: is it time to reconsider their functional roles in aquatic communities? Oecologia 120: 621-631.

  • PiankaE.R. (1973): The structure of lizard communities. Ann. Rev. Ecol. Syst. 4: 53-74.

  • PringleC.M.HamazakiT. (1997): Effects of fishes on algal response to storms in a tropical stream. Ecology 78: 2432-2442.

  • PryorG.S.BjorndalK.A. (2005): Symbiotic fermentation, digesta passage, and gastrointestinal morphology in bullfrog tadpoles (Rana catesbeiana). Physiol. Biochem. Zool. 78: 201-215.

  • R Core Team (2016): R: a Language and Environment for Statistical Computing. The R Foundation for Statistical ComputingVienna, Austria. Version 3.2.4. Available from: https://cran.r-project.org/.

  • RanvestelA.W.LipsK.R.PringleC.M.WhilesM.R.BixbyR.J. (2004): Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshw. Biol. 49: 274-285.

  • RiceW.R. (1989): Analyzing tables of statistical tests. Evolution 43: 223-225.

  • Richter-BoixA.LlorenteG.A.MontoriA.GarciaJ. (2007): Tadpole diet selection varies with the ecological context in predictable ways. Basic Appl. Ecol. 8: 464-474.

  • Rossa-FeresD.C.JimJ.FonsecaM.G. (2004): Diets of tadpoles from a temporary pond in southeastern Brazil (Amphibia, Anura). Rev. Bras. Zool. 21: 745-754.

  • SandefurH.N.MatlockM.D.CostelloT.A. (2011): Seasonal productivity of a periphytic algal community for biofuel feedstock generation and nutrient treatment. Ecol. Eng. 37: 1476-1480.

  • SantosF.J.M.ProtázioA.S.MouraC.W.N.JuncáF. (2016): Diet and food resource partition among benthic tadpoles of three anuran species in Atlantic Forest tropical streams. J. Freshw. Ecol. 31: 53-60.

  • SchiesariL.WernerE.E.KlingG.W. (2009): Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology. Freshw. Biol. 54: 572-586.

  • SealeD.B. (1980): Influence of amphibian larvae on primary production, nutrient flux, and competition in a pond ecosystem. Ecology 61: 1531-1550.

  • SigeeD.C. (2005): Freshwater Microbiology: Biodiversity and Dynamic Interactions of Microorganisms in the Aquatic Environment. WileyChichester.

  • Sousa-FilhoI.F.BrancoC.C.TellesM.P.SilvaG.R.SabaghL.T. (2007): The diet of Scinax angrensis (Lutz) tadpoles in an area of the Atlantic Florest (Mangaratiba, Rio de Janeiro) (Amphibia, Anura, Hylidae). Rev. Bras. Zool. 24: 965-970.

  • SouzaM.L.PellegriniB.G.FerragutC. (2015): Periphytic algal community structure in relation to seasonal variation and macrophyte richness in a shallow tropical reservoir. Hydrobiologia 755: 183-196.

  • StevensonJ.R. (1996): An introduction to algal ecology in freshwater benthic habitats. In: Algal Ecology: Freshwater Benthic Ecosystems p. 3-30. StevensonR.J.BothwellM.L.LoweR.L. Eds Academic PressSan Diego, CA.

  • StrahlerA.N. (1957): Quantitative analysis of watershed morphology. Trans. Amer. Geophys. Union 38: 913-920.

  • VadeboncoeurY.PetersonG.JakeM.ZandenV.KalffJ. (2008): Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89: 2542-2552.

  • WagnerW.E. (1986): Tadpoles and pollen: observations on the feeding behavior of Hyla regilla larvae. Copeia 1986: 802-804.

  • WellsK.D. (2007): The Ecology and Behavior of Amphibians. The University of Chicago PressChicago, IL.

Figures

  • View in gallery

    Material recorded in the anterior portion of Bokermannohyla saxicola tadpole guts at developmental stages 25 (black bars) and 30 (grey bars) throughout the year considering number of cells (A, C, E, G) and biovolume (B, D, F, H). A and B: Onset wet, C and D: middle wet, E and F: onset dry, G and H: middle dry (see text for details).

  • View in gallery

    Measurements of Bokermannohyla saxicola tadpoles in developmental stages 25 (n = 20) and 30 (n = 20) (sensu Gosner, 1960). Data is presented as mean ± SD. Stages were compared with Mann-Whitney or t-tests for non-normal and normal data, respectively (significance level considered as p < 0.05).

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    NMDS showing classification of tadpole diets based on number of cells (A) and biovolume (B) of food items for eight groups given by the combination of two developmental stages (25 and 30 sensu Gosner, 1960) and four sampling periods (OW = onset wet, MW = middle wet, OD = onset dry, MD = middle dry; see text for additional details). Species included in the polygon representing each group are those consumed more by that group than by other groups. Each dot represents one tadpole, and colors correspond to groups (stage × sampling period). Sampling periods within the wet season are marked in green for stage 25 tadpoles and in orange for stage 30 tadpoles. Sampling periods within the dry season are marked in blue for stage 25 tadpoles and in yellow for stage 30 tadpoles.

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    Estimatives of niche breadth based on (1) number of cells and (2) biovolume of food types for Bokermannohyla saxicola in developmental stages 25 and 30 (sensu Gosner, 1960) throughout the year: OW = onset wet, MW = middle wet, OD = onset dry, MD = middle dry (see text for further details). Estimatives were obtained based on 1000 simulations and data from different stages/periods were compared through rarefaction considering the smallest number of items/biovolume ingested (n = 18 440 and n = 1 213 210.2 μm3/ml, respectively) as reference. Different letters (last column) indicate significantly different results (p < 0.05) within the analyses (number of cells or biovolume).

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