Herpetology Notes, volume 14: 231-237 (2021) (published online on 01 February 2021)

Diet composition of nitoi (Barrio, 1973) in Chilean Patagonia

Nicza Alveal1,2,*, and Helen Díaz-Páez1

Abstract. The availability of data on the diet of a can be of great importance in understanding its basic biology, as well as contributing to conservation and management. The genus Atelognathus contains five species distributed in the Patagonia region of Chile and Argentina; only A. nitoi occurs in Chile. There are reports on the diet of species of Atelognathus in Argentina, however for A. nitoi studies have focused mainly on and systematics. The objective of this study is to provide information on the diet composition of A. nitoi in Chile. A total of 21 specimens of A. nitoi were collected from four localities in Chilean Patagonia during the spring-summer seasons in 2007 and 2010: La Tapera (44°38’S, 71°41’W), Chile Chico (46°32’S, 72°00’W), Cerro Castillo (45°59’S, 71°52’W) and Reserva Nacional Lago Jeinimeni (46°50’S, 71°59’W), XI Región, Chile. We analysed the diet by dissecting the stomach between the cardias and the pylorus. Stomach contents were examined under a stereo microscope and the prey items identified to order or family. Twenty items were determined in 12 taxonomic categories. The highest relative importance index was represented by Dytiscidae, Sylvanidae, Curculionidae and Elateridae, all of the order Coleoptera. The data show that A. nitoi consume a variety of prey, adult and larval coleopterans of both terrestrial and aquatic species. Dietary information is key to understanding life history and ecological strategies of little- known species, especially for their interactions with ecosystems which still remain pristine; it is important for the conservation of nature.

Keywords. Diet, Prey, Ranita del Challhuaco, South America

Introduction considered endemic to the province of Río Negro, Argentina, is found in Chile (Barrazo and Basso, 2018). The genus Atelognathus described by Lynch in A. nitoi inhabits temperate in the transition from 1978 was long recognised as a genus with distribution high prairie to lenga . are found under restricted to Chilean and Argentine Patagonia (Basso, 1998). There have been only a few studies stones quite far from the water in open areas above the on the biology of the genus Atelognathus, mainly forest and among forest vegetation under sticks and concerning systematic and morphological aspects. New leaves, usually near lagoons or streams (Meriggio et morphological and molecular approaches have reduced al., 2004; Díaz-Páez et al., 2011). In Lake Jeinimeni the number of species recognised in this genus from A. nitoi cohabits with bufonina Bell 1843 seven to five species: A. patagonicus Gallardo 1962; (Basso, 1998; Meriggio et al., 2004). The preferred A. praebasalticus Cei and Roig, 1968; A. reverberrii microhabitats of adults and juveniles are the most humid Cei, 1969; A. solitarius Cei, 1970 and A. nitoi Barrio, areas of the forest. 1973 (Barrazo and Basso, 2018). Most of these species The reproductive period extends from spring through are present in Argentina; only A. nitoi, which was long late summer (Meriggio et al., 2004). Release calls, an acoustic signal type in this species, seem to be strongly related only to the reproductive season. Reproduction and larval development occur in lentic environments 1 Laboratorio de Ecofisiología y Conservación de Herpetozoos, (Úbeda, 1999); after metamorphosis they quickly seek Departamento de Ciencias Básicas, Escuela de Educación, a wet shelter. As they grow, the juveniles disperse to Universidad de Concepción, Campus Los Ángeles, Casilla 341, Los Ángeles, Chile. new areas with similar characteristics, enduring greater 2 Departamento de Zoología, Facultad de Ciencias Naturales dryness (Meriggio et al., 2004). y Oceanográficas, Universidad de Concepción, Campus feeding behaviour has been the focus of Concepción, Casilla 160-C, Concepción, Chile. numerous papers and has defined their role in terrestrial * Corresponding author. E-mail: [email protected] and aquatic ecosystems (Muñoz-Guerrero, 2007; © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Arroyo, 2008), where they act as predators capable of 232 Nicza Alveal & Helen Díaz-Páez controlling many populations, especially invertebrates with greater relative importance for the aquatic form (Wells, 2007; Toledo et al., 2007). Multiple factors were odonate naiads and amphipod crustaceans. For the influence diet composition, including environmental littoral morph all prey were adult terrestrial arthropods changes (Solé et al., 2009), individual body size (Cuello et al., 2006). (Lima, 1998; Batista et al., 2011; Sugai et al., 2012), Our objective is to obtain basic knowledge about seasonality (Maragno and Souza, 2011) and hunting the diet composition of A. nitoi in Chile, including strategies (Maneyro et al., 2004). The trophic niche is identification of prey items, determination of abundance an important component of the natural history of species (N), frequency of occurrence (F) and relative importance and suggests ecological consequences (Anderson and index (IRI). Mathis, 1999), and there is a direct relationship between environmental conditions, alterations and prey Materials and Methods distribution (Parker and Goldstein, 2004). Based on this environmental link, information about the trophic Our study took place in 2007 and 2010 spring-summer niche of the species can help to establish conservation seasons. 21 specimens of Atelognathus nitoi were strategies (Batista et al., 2011). collected from localities around lagoons in Chilean Trophic biology in the genus Atelognathus has Patagonia (Fig. 1), with permission from the Servicio only been reported in A. partagonicus, where two Agrícola y Ganadero (N° 6494, 27 December 2006). morphotypes have been documented for the species, The material analysed comes from four Patagonian a littoral morph and an aquatic morph, indicating a localities: La Tapera (44°38’S, 71°41’W; 1,041 m relationship between habitat and diet type. The items a.s.l.), Chile Chico (46°32’S, 72°00’W; 423 m a.s.l.),

Figure 1. Habitat of the species of A. nitoi. A. La Tapera B. Cerro Castillo C. Chile Chico and D. Lago Jeinimeni. Diet composition of Atelognathus nitoi in Chilean Patagonia 233

Cerro Castillo (45°59’S, 71°52’W; 994 m), and Reserva mL precision test tube. With these data we calculated Nacional Lago Jeinimeni (46°50’S, 71°59’W; 730 m the aggregate percentage of volume and the number of a.s.l.) XI Región, Chile (Fig. 2). The environmental items consumed for each species (Litvaitis et al., 1994). conditions where we collected the specimens were We then determined an Index of Relative Importance similar, and due to the low number of individuals, we (IRI) (Powell et al., 1990) for each invertebrate taxon, grouped them without differentiating between locality for which we used the following formula: IRI = (%N + of origin to perform the trophic analyses. We captured %F + %V )/ 3, where %N is the aggregate numerical the between 13:00 h and 17:00 h. All percentage, %V is the aggregate percentage volume individuals were euthanised with 1% benzocaine and and %F is the percentage frequency of occurrence. This fixed in 10% formalin for subsequent preservation index allows comparing the relative importance that in 70% ethanol. All specimens were deposited in the each item represents in the total diet of the predatory Zoology Museum of the Universidad de Concepción species. (MZUC 36572–36575; 36577–36580; 36584–36586; The IRI values allowed establishing three categories 36589; 36404–36408; 36410–36411; 36414; 36418; of food importance: primary, secondary and tertiary, 36770–36772; 36763; 36767). We analysed the diet where the highest values of the index indicate the by dissecting the stomach between the cardias and the greatest importance of the food item. Since these are pylorus. We observed the stomach contents under a not continuous variables, the value of the median (2.73) stereo microscope and identified the different items to was prioritised over the value of the mean (3.67 ± 2.75) order or family. For each food item we recorded the total added to the standard deviation (Díaz-Páez and Ortiz, number and determined the volumetric valuation (V) 2003) in order to set the limits of each category (Table by calculating the volume of liquid displaced in a 0.01 1).

Figure 2. Locations of A. nitoi in Chile included in the study: 1. La Tapera, 2. Cerro Castillo, 3. Chile Chico and 4. Reserva Nacional Lago Jeinimeni.

234 Nicza Alveal & Helen Díaz-Páez

Table 1. AbundanceTable 1.and Abundance frequency andof prey frequency items offound prey in items the stomach found in contents the stomach of eight contents A. nitoi of eight(out ofA. 21 nitoi examined). (out of 21 % N: examined). % N: Numerical percentage, f frequency of stomachs that had that prey, % F: Frequency of Numerical percentage,occurrence f frequencypercentage, of %V: stomachs Volumetric that hadpercentage that prey, and % RII: F: IndexFrequency of Relative of occurrence Importance. percentage, %V: Volumetric percentage and RII: Index of Relative Importance.

Prey Item N f % V %F IRI Category Hexapods

1.1 Coleoptera

Curculionidae 4 1 10 7.14 5.78 Primary Elateridae 4 2 8 14.28 7.49 Primary Carabidae (larva) 1 1 0.2 7.14 2.46 Tertiary Silvanidae (larva) 1 1 9 7.14 5.39 Secondary Tenebrionidae 1 1 1 7.14 2.73 Tertiary Scarabaeidae 1 1 5 7.14 4.06 Secondary Dytiscidae 2 2 16 14.28 10.12 Primary 1.2 Diptera

Undetermined Diptera 1 1 0.5 7.14 2.56 Tertiary Tipulidae 1 1 1 7.14 2.73 Tertiary 1.3 Hymenoptera

Ichneumonoidea 2 1 1 7.14 2.74 Secondary Crustacea 1 1 1 7.14 2.73 Tertiary Arachnida 1 1 0.5 7.14 2.56 Tertiary

Results the OTUs Dytiscidae (10.12), Curculionidae (5.78) and Elateridae (7.49), all of the order Coleoptera. Eight of the 21 specimens (38%) of A. nitoi analysed Prey of the order Coleoptera were recognised without had stomach contents. Twenty prey items of 12 major problem since specimens of this order have body taxonomic categories were detected and determined structures that are slowly degraded, unlike prey of the (Table 1). We considered each taxon identified as an order Diptera, which were only determined to order, Operational Taxonomic Unit (OTU). We identified although the tipulids could be identified to family. the following prey OTUs: Curculionidae, Elateridae, The prey of the subphylum Crustacea and the class Carabidae, Silvanidae, Tenebrionidae, Scarabaeidae, Arachnida were not determined to order since they were Dytiscidae, indeterminate Diptera, Tipulidae, in a state of degradation that prevented their recognition. Ichneumonoidea, Crustacea and Arachnida. We found insignificant consumption of detritus and Our results show that A. nitoi consumes mostly vegetable remains, which were not identified, so they prey, among which the coleopteran families Elateridae (N were not considered in Table 1. The detritus consisted of = 4) and Curculionidae (N = 4) were the most abundant small granules of minerals and the plant parts included (Fig. 3). Dytiscidae and Elateridae contributed 14.28% pieces of stems, leaves and small undetermined seeds. each to the percentage of frequency of occurrence; we found both in individuals from the northernmost locality Discussion La Tapera and in the southernmost localities (Table 1). The prey items with the highest volume were Dytiscidae Ecological traits are especially relevant in the study of (0.16 ml), Curculionidae (0.1 ml) and Silvanidae (0.09 communities and species, even more so in the face of ml). In addition to adult prey, we recorded one larva climate change and the loss of biodiversity. Amphibians of the family Carabidae and one larva of the family areI abundant in many terrestrial and freshwater Silvanidae (Fig. 3). ecosystems, where they perform important ecosystem The contribution of each food category to the diet of functions (Hocking and Babbitt, 2014). Freire et al. the species obtained by the application of the relative (2017) indicated the need to increase knowledge about importance index (IRI) showed the highest values in natural history traits in amphibians. These data are still Diet composition of Atelognathus nitoi in Chilean Patagonia 235

Figure 3. %N (Relative Abundance) in black and %V (Percentage Volume) in gray of the 12 OTUs (Operational Taxonomic Units) determined. scarce for many taxa. Amphibians are also the most the consumption of taxa from terrestrial or aquatic threatened group of vertebrates in the world, with many organisms between the different food items detectable. species on the brink of extinction. However, in the absence of data on relative abundance Dietary data constitute a first contribution to our of prey, it is not possible to infer selection of the food knowledge of aspects of the biology of A. nitoi. The items determined to have the highest importance values use of IRI is a valuable alternative to single index (Whittaker, 1977; Anderson et al., 1999). measures; it is a composite measure that reduces bias The relative importance of Dytiscidae in the diet in descriptions of animal dietary data. Although its indicates that some prey are captured in an aquatic use has been limited, this index allows us to provide environment, as is the case for the aquatic form of A. a percentage approach to describe the diets of patagonicus (Cuello et al., 2006). As in other anurans (Hart et al., 2002). (Pincheira-Donoso, 2002a, b; Díaz-Páez and Ortiz, A. nitoi is the only species of the genus Atelognathus 2003; Bello et al., 2005; Cuello et al., 2006; Gutiérrez in Chilean Patagonia; the main focus of studies has et al., 2008), there was a great variety of coleopteran been clarifying its taxonomic status (Barrazo and prey items. Most frequently, adult individuals were Basso, 2018). Knowledge of this taxon in extreme found of the families Curculionidae and Elateridae and environments is scarce, probably due to the difficult larvae of the families Carabidae and Silvanidae. This access to multiple sites, which has generated few data majority consumption of Coleoptera is probably due on its ecology (Meriggio et al., 2004; Díaz-Páez et al., to the fact that they are large prey and occupy virtually 2011). every terrestrial habitat (Lawrence and Newton, 1995; The diet data allow us to understand better basic Elgueta, 2000). Most of them are agile, making them aspects of the ecology of this species (Stebbins and ideal prey for the anurans, which are visual hunters that Cohen, 1995; Wells, 2007). The results of our study react to their movement (Ewert, 1987; Browne, 2009). showed a high rate of empty stomachs, a result that The consumption of tipulids is principally due to the we believe could be influenced by the capture of the fact that they are large and nocturnal, which coincides individuals in the afternoon, when the food consumed with the period of activity of this species (Meriggio et the previous night might already have been digested. al., 2004). However, these results constitute a first record of the According to presence records, A. nitoi cohabits with ecological traits of A. nitoi. P. bufonina (Basso, 1998; Meriggio et al., 2004), which The food analysis of A. nitoi showed no trend towards has a similar diet in terms of coleopteran consumption. 236 Nicza Alveal & Helen Díaz-Páez

Both species also consume Hymenoptera; P. bufonina Batista, R.C., De–Carvalho, C.B., Freitas, E.B., Franco, S.C., has a majority consumption of Formicidae (Pincheira- Batista, C.C., Coelho, W.A., Faria, R.G. (2011): Diet of Rhinella Donoso, 2002a; Bello et al., 2005) and A. nitoi of schneideri (Werner, 1894) (Anura: Bufonidae) in the Cerrado, Central Brazil. Herpetology Notes 4: 17–21. Ichneumonoidea. Bello, M.T., Hougham, V., Úbeda, C.A., Cuello, M.E. (2005): The intake of detritus and plant remains is common Pleurodema bufoninum (NCN). Diet. Herpetological Review in anurans (Camera et al., 2014). However, due to its 36: 303–304. low consumption it was not possible to determine in this Browne, R.K. (2009): Amphibian diet and nutrition. AArk Science study a likely role of this food item. The intake could and Research. be a bycatch during food intake (Whittaker, 1977), or Camera, B., Krinski, D., Calvo, I. 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Accepted by Andrew Durso