The genus Lithodytes Fitzinger, 1843 includes only one species, the ant frog L. lineatus (Schneider, 1799)

(Fig. 1), which is widely distributed in the Amazonian and Orinocoan basins. When re-evaluating amphibian phylogenetic relationships Frost et al. (2006) placed the genus Lithodytes (and Adenomera) as a synonym of Leptodactylus thus recognizing the clade Lithodytes plus Adenomera as a subgenus called Lithodytes. �e S�� et al.�e S�� et al. (2005), Fouquet et al. (2007), and Ponssa et al. (2007)(2007) treated both as valid genera. We agree with both author teams in recognizing Lithodytes as a distinct genus until broader taxon sampling challenge the taxonomic arrangement proposed by Frost et al. (2006). Knowledge

Herpetology Notes, volume 2: 101-105 (2009) (published online on 19 July 2009)

Use of an active nest of the leaf cutter ant Atta cephalotes (Hymenoptera: Formicidae) as a breeding site of Lithodytes lineatus

(Anura: Leptodactylidae)Andreas Schlüter1*, Petra Löttker2 and Konrad Mebert3

Abstract. Herein, we report for the first time the use of an Atta cephalotes ant nest as a breeding site of the frog Lithodytes lineatus. We suggest that apart from using Atta nests as breeding sites the frogs may benefit from their association with the ants by obtaining hiding places and experiencing stable microclimate. The frogs feeding on predatory insects as assassin bugs may be relevant for the ants. We also present an advertisement call of Lithodytes lineatus vocalisation, from the interior of an ant nest.

Keywords. Amphibia, Lithodytes lineatus, reproduction, life history, Formicidae, Atta cephalotes, Tambopata, Madre de �íos, Peru.

Figure 1. Adult Lithodytes lineatus from Madre Selva, Loreto, Peru. Photo: K. Mebert.

1 Staatliches Museum für Naturkunde, Rosenstein 1, �-70171 Stuttgart, Germany;

e-mail: schlueter.smns@naturkundemuseum-bw.de2 Light & Shadow GmbH, Badestr. 19a, �-48149 Münster,

Germany 3 Alte Obfelderstrasse 44, CH-8910 Affoltern am Albis,

Switzerland * corresponding author

Andreas Schlüter et al.102

of the ecology of Lithodytes lineatus is minimal with the exception of its association with leaf cutter ants (e.g. Schlüter, 1980; Schlüter and Regös, 1981; Lamar and Wild, 1995).

A few associations between amphibians and reptiles with invertebrates are known, such as that of the worm snake Leptotyphlops dulcis living together with its prey, the army ant Neivamyrmex nigrescens (Watkins et al., 1969), or different North American snake species (Virginia valeriae, Diadophis punctatus, Carphophis vermis, Storeria dekayi) using active ant nests as hibernaculum (Pisani, 2009). Relationships between frogs and tarantula spiders have been reported by Blair (1936), Powell et al. (1984), Foelix (1982), and Cocroft and Hambler (1989). Associations between frogs and ants, however, are rarely documented (e.g. Gallardo, 1964; Weber, 1972; Schlüter and Regös, 1981, 1996; Hoogmoed, 1986; �ejean and Amiet, 1992; Lamar and

Wild, 1995; Rödel and Braun, 1999) but the use of an active ant nest as a breeding site for a frog species has never been reported. The association of L. lineatus with the leaf cutter ant Atta cephalotes (Linnaeus, 1758) was first mentioned by Schlüter (1980), who recorded advertisement calls emanating from the interior of an ant nest in the biological field station Panguana, Rio Llullapichis drainage, �epartment Hu��nuco, Peru (9°35´S, 74°56´W, about 250 m asl). Based on additional observations on the frog’s association with A. cephalotes Schlüter and Regös (1981) suggested a mutual relationship (‘true symbiosis’?) between the ants and frogs. Furthermore, additional biological aspects of L. lineatus such as different call types, foam-nest building behavior in captivity, and tadpoles of captive-raised individuals were reported (Regös and Schlüter, 1984). Subsequently, Hoogmoed (1986), �e la Riva (1993), M��rquez et al. (1995), and Lamar and Wild

Figure 2. Oscillogram (above) and spectrogram of the advertisement call of a male Lithodytes lineatus calling from the interior of an active nest of Atta cephalotes at the Tambopata National Reserve, Peru.

Use of Atta cephalotes nest as a breeding site 103

(1995) confirmed the frog’s association with leaf cutter ants.

At Explorer´s Inn, a lodge in the Tambopata National Reserve in Peru, we observed the use of an active leaf cutter ant nest as breeding site of L. lineatus. Tambopata, Province of the Madre de �íos �epartment, lies at the south-western edge of the Amazon basin near the Andean foothills and encompasses about 36,000 km2 covered primarily by lowland tropical/

subtropical moist forest (Gentry and Leon, 1997; �oan and Ariz��bal, 2002). Recognized as a region of high biodiversity Tambopata has received much attention from a herpetological perspective (e.g., �uellman and Salas, 1991; Rodríguez and Emmons, 1994). �uring a stay in November/�ecember 2005 one of the authors (AS) discovered four nests of the leaf cutter ant Atta cephalotes that were inhabited by calling males of L. lineatus. At one nest vocalizations of frogs were

Figure 3. Water-filled depression in an active nest of Atta cephalotes (red arrows) with tadpoles of Lithodytes lineatus (white arrows). Photo: K. Mebert.

recorded by lowering a slender microphone (Sennheiser) of a tape recorder (SONY-�6C) into a vertical passage (comp. Schlüter and Regös, 1981). Acoustic analyses were performed with Cool Edit software and calls were digitized at a sampling rate of 44.1 kHz (Hamming windowing function set at a resolution of 1024 bands). The calls (Fig. 2) of four L. lineatus males have been recorded, which called synchronously from the interior of the same large nest of A. cephalotes. The call is a continuous series of short whistles repeated at a rate of about 80–90 notes/min. The well-modulated notes are about 0.12 sec long and have three harmonics at 1300, 2600, and 3900 Hz with a dominant frequency at 2600 Hz (comp. Schlüter, 1980; �uellman, 2005).

In February 2009, two of the authors (PL and KM) inspected an Atta nest in the same area discovering one adult L. lineatus and numerous tadpoles in a water filled depression at the end of a system of underwater burrows (Fig. 3). The tadpoles were morphologically similar to those described by Regös and Schlüter (1984), Lamar and Wild (1995), and Schlüter and Regös (1996). A vertical tunnel directly above the pool was around 25 cm in diameter and foam-nests adhered to the roots protruding from the otherwise smooth walls. The channel was frequented by a stream of descending ants. The tadpoles were at different developmental stages reaching from individuals without legs to one metamorphosed juvenile frog. Adult and subadult ant frogs have also been observed along pathways in the forest or sitting in a hollow log without any obvious association to a visible ant nest. It is not clear whether these frogs represent juveniles that have dispersed from the nests or whether they are females or males that are temporarily sexually inactive. Similar observations were reported by Lamar and Wild (1995) and �uellman (2005).

Possible explanations why frogs and ants use the same burrows have been discussed for L. lineatus by Schlüter and Regös (1981, 2005) and for the African frogs Kassina senegalensis (�ejean and Amiet, 1992) and K. fusca and Phrynomantis microps (Rödel and Braun, 1999). Schlüter and Regös (1981) mentioned that all L. lineatus captured at the entrance of Atta nests released an aromatic odour. The authors suggested that this odour might be a chemical disguise or repellent against potential attacks from the ants, which usually try to kill every intruder. The results of Rödel and Braun (1999), who conducted related experiments on West African frog–ant associations, support the hypothesis of chemical communication between the frogs and the ants. In dedicated experiments, in which specimens of

L. lineatus lost this specific odour individuals were immediately killed by the ants (Schlüter and Regös, 1996). We never observed L. lineatus feeding on A. cephalotes. The stomach contents of one L. lineatus specimen caught at the entrance of an Atta nest contained only two nymphs of the predatory insect genus Heza (Reduviidae) (Schlüter and Regös, 2005). Previous reports on stomach contents of two ant frogs contained 19 ants (only 8.1 percent of the food volume), but consisted mostly of crickets, earthworms, isopods, and insect larvae (Parmelee, 1999).

Obviously, the ant frogs - including eggs and larvae - benefit from their association with leaf cutter ants and their nests by (1) obtaining suitable hiding places against potential predation; (2) experiencing a stable microclimate [humidity and temperature, as supposed for Phrynomantis by Rödel and Braun (1999)]; and (3) possibly obtaining food. Further studies are necessary to explore whether the frog’s feeding on predatory insects such as assassin bugs is relevant and a benefit for the ants. Another question concerns the nutrition of tadpoles. Most of captive-raised individuals that were fed with commercial fish food died within a few weeks (Regös and Schlüter, 1984).

Acknowledgments. AS expresses his gratitude to Waltraud Kofer from the �eutsche akademische Austauschdienst (�AA�), Richard P. Korswagen (Instituto de Estudios Ambientales de la PUCP, Lima), Eric Cosio Initiativa Tambopata, Lima), and to Raffael Ernst (�ept. of Biodiversity �ynamics, TU Berlin) for his invitation to the Tambopata Reserve. The observations of PL and KM were made in the context of film shootings for the TV-documention called “Amazon Alive” produced by Light & Shadow GmbH, Germany. We especially thank the Peruvian authorities of INRENA (Instituto National de Recursos Naturales) for their generous cooperation. Our assistants in the field, José Elisban Armas �íaz and Mario Zegarra Catarin, for their invaluable and tireless work and their persistency in finding the frogs. We are grateful to Axel Kwet (SMNS), Mark-Oliver Rödel (Museum für Naturkunde Berlin), and Edgar Lehr (Museum of Zoology, �resden) for valuable suggestions and improvement on the manuscript. Thanks to �r. Lloyd Knutson (United States Department of Agriculture), who managed the identification of arthropods.

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