Explosion into the canyon: an insight into the breeding aggregation of Scaphiophryne gottlebei Busse & Böhme, 1992

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1 NORTH-WESTERN JOURNAL OF ZOOLOGY 7 (2): NwjZ, Oradea, Romania, 2011 Article No.: Explosion into the canyon: an insight into the breeding aggregation of Scaphiophryne gottlebei Busse & Böhme, 1992 Gonçalo M. ROSA 1,2*, Vincenzo MERCURIO 3, Angelica CROTTINI 4,5,6 and Franco ANDREONE 7 1. Centro de Biologia Ambiental, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Bloco C2, Campo Grande, Lisboa, Portugal. 2. Department of Anthropology, Durrell Institute of Conservation and Ecology, University of Kent, Canterbury, Kent, UK. 3. Museum für Naturkunde, Leibniz-Institut für Evolutions-und Biodiversitätsforschung an der Humboldt-Universität zu Berlin, Germany 4. Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Mendelssohnstraße, 4, 38106, Braunschweig, Germany 5. Universitá degli Studi di Milano, Dipartimento di Biologia, Sezione di Zoologia e Citologia, Via Celoria 26, Milano, Italy 6. Current address: CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, R. Padre Armando Quintas, Vairão, Portugal. 7. Museo Regionale di Scienze Naturali, Via G. Giolitti, 36, I-10123, Torino, Italy. * Corresponding author, goncalo.m.rosa@gmail.com Received: 15. December 2010 / Accepted: 19. July 2011 / Available online: 21.July 2011 Abstract. We describe the explosive breeding aggregation event in the rainbow toad, Scaphiophryne gottlebei, an endemic frog of Isalo Massif, south-central Madagascar. The frogs were observed just after the first seasonal rainfall (early November 2009). Males and females aggregated in pools formed within the narrow canyons where they live. The breeding event lasted for three nights, with males mating with females in inguinal amplexus. Males were much more abundant than females, with a tertiary sex ratio of about 34.5% of females. Significant correlation was observed between the snout-vent length and body mass for both sexes. Keywords: Anura; reproduction, canyon; Isalo; Madagascar; microhylids, sex ratio. Nine species are currently ascribed to the microhylid genus Scaphiophryne from Madagascar (Glaw & Vences 2007, Vieites et al. 2009). The rainbow frog S. gottlebei, endemic of the sandstone Isalo Massif (south-central Madagascar), is well-known for its attractive colour pattern with white, greenish, pinkish-red and black blotches, that makes of it one of the most requested Malagasy frogs for the pet trade (Andreone et al. 2005a, 2005c, 2006). The species is currently listed as CITES II and assessed as Endangered according to IUCN (2010). The adults live inside and around the narrow canyons that cross the massif. They usually hide in the sandy substrate, or climb up the canyon wall hiding in small crevices and cavities caused by pebble falling (Mercurio & Andreone 2006, Glaw & Vences 2007). The psammo-nektonic larvae develop in pools of lentic water within the canyons, burying in the sand of the bottom during the day, and swimming in the water column during the night (Mercurio & Andreone 2006). Previous papers were focused on the species (see Andreone et al. 2005b, Mercurio & Andreone 2006, Crottini et al. 2008), but almost nothing was known of the breeding habits and natural history requirements; as this is missing information for defining conservation programs (Andreone et al. 2005a, Mercurio et al. 2008), we here provide the first description of the breeding aggregation in S. gottlebei and other aspects of its reproductive biology. The aggregation event of S. gottlebei was recorded in 2009 in an area known as Zahavola (22 37'17.54"S '41.49"E, 850 m a.s.l.), which lies just outside the administrative borders of the Parc National de l Isalo (PNI). In Isalo, rare but intense rainfalls usually take place from late October to February (Projet ZICOMA 1999). The Zahavola site is a small basin (4x3 m width) within a narrow and cave-like canyon (Andreone et al. 2005b), with sandy substrate on the bottom (Fig. 1). The breeding aggregation was recorded between 1 st -3 rd of November 2009 after the first intense rains (max. daily precipitation of 70 mm; recorded air temperature ranged º C). This was the only rainfall event documented during all the survey from 1 st -14 th November, Snoutvent length (SVL) of males and females was measured with a vernier caliper (precision of 0.1 mm), and body mass with an electronic balance (precision of 0.1 g). The breeding activity, stimulated by the rainy precipitation, likely started between the

2 330 Figure 1. Temporary water basin inside canyon in Zahavola, Isalo Massif: A. basin completely dried out, before first heavy rainfall (30 th October, 2009); B. overflowing water basin after rainfall (7 th November, 2009); C. almost dried out pool, 40 days after the first rains (10 th December, 2009) (A-B, photos by V. Mercurio; C, photo by G. M. Rosa). Rosa, G.M. et al. night of the 2 nd November, but our observations started on the night of 3 rd November. After the rainfall the pool filled up, with a maximum depth of around 2 m and held the water for the following two months (Fig. 1.B). Twenty-three adult males and 10 adult females were found around the basin and into water. When the monitoring began, nearly all the female individuals already amplected, both in water, on the ground or even within small holes on the canyon s wall (Fig. 2.A-E). Scaphiophryne gottlebei, like other representatives of the genus, lacks nuptial pads (Busse & Böhme 1992), and the amplexus is inguinal, with the male embracing the female at the groin (Fig. 2.A-E). Most females stand still with one or two males on their back. Single males were calling, either from the water or along the water s edge on the bottom of the rocky wall emitting a loud thrilling chorus (Fig. 2.F-H). No egg-laying was observed on the night of 3 rd November. The next morning (4 th November) all paired individuals were still mating and continued with this activity throughout the day. This was the first day without rainfall, but in the evening, most of the individuals were still in the water when the first egg masses were recorded. Small clutches of dark pigmented eggs were attached to submerged tree branches just below the water surface (Fig. 2.I). To safeguard the clutch we did not count the eggs in nature, but we analysed the egg numbers from two preserved individuals captured in 2004, consisting respectively of 196 eggs (FAZC 12866, SVL = mm) and 168 eggs (FAZC 12757, SVL = mm). On 5 th November (at 8 am) several males were still calling but we found only three of them in water (Fig. 2.J). Few and less motivated calls came from the upper part of the canyon, but the great majority of individuals was already burrowed into the sand bank, hidden in crevices and holes in the canyon wall (Fig. 2.K). No breeding activity was recorded on the 6 th November. The first egg clutches hatched on those days, so after three days from deposition (Fig. 2.L- M). Statistical analyses were conducted with STA- TISTICA 9.0 (StatSoft, Tulsa, USA). Morphometrics are provided on Table 1 and Figure 3 and comparisons were performed between sexes: sexual dimorphism in body length (SVL) and body mass was tested using Student s t test. SVL-body mass relationships were described using analysis of covariance, ANCOVA (Day & Quinn 1989, Zar 2009). Body mass was log 10 -transformed, reducing heteroscedasticity which minimises chances of violating the assumptions of the ANCOVA procedure (e.g. Day & Quinn 1989, Ramos-Pallares et al. 2010). The correlation between SVL and body mass is significant (p < 0.01) in both males (r = 0.638) and females (r = 0.956) (Fig. 3) with larger individuals presenting higher weight. Females were also significantly larger and heavier than males (SVL: t = 2.86, p < 0.01; body mass: t = 4.23; p < 0.01), with a different trend between SVL and body mass (AN-

3 Breeding behaviour of Scaphiophryne gottlebei 331 COVA using sex as factor and SVL as covariate): F(1, 36) = 5.501, p = Females also showed a greater body mass compared to males, a difference that can be explained by the presence of eggs in females. Similarly to other anurans, the evolution of larger body in females may result from fecundity advantage, increasing clutch size in larger frogs (Shine 1979, Andersson 1994). The pronounced seasonal climate of Isalo is likely the main responsible cause of the explosive reproductive strategy observed in this species. The reproductive period of S. gottlebei is closely related with the availability of breeding sites and, as we confirmed, as soon as the favourable temporary Table 1. Biometrics from the Scaphiophryne gottlebei population at Isalo (Fianarantsoa Province). Measurements are provided as range, followed by mean, standard deviation and number of sample units (n). Sex SVL (mm) Body mass (g) Males (28.91 ± 1.69, n = 29) (3.46 ± 0.42, n = 29) Females (30.85 ± 2.30, n = 10) (4.50 ± 1.15, n = 10) Figure 2. Mating behaviour and breeding stages on Scaphiophryne gottlebei: A-E. pairs in amplexus; F-H. unpaired calling males; I. mass of eggs attached to a submerged tree branch; J. non-calling male floating; K. individual hidden in a hole in the canyon wall; L. larvae hatching; M. three days tadpole. All photos by V. Mercurio, except for K, by G. M. Rosa.

4 332 aquatic site is established, mating takes place immediately. An explosive breeding behaviour is usually considered a trait of species living in temporary and seasonal habitats. In Madagascar, this is the case, for example, of Laliostominae species and some Scaphiophryne (e.g., S. brevis). Anyhow, a similar reproduction was documented for some other species living in temporary pools within rainforests and deciduous forests, such as Boophis albilabris (G. M. Rosa, pers. obs.), B. tsilomaro (Andreone et al. 2002) and in the genus Aglyptodactylus (Glaw & Vences 2007). Tertiary sex ratio was highly male biased: only 34.5% (n = 39) of breeding individuals were females. Some hypotheses are available to explain this biased sex ratio observed in S. gottlebei. Among these are: an unbalanced sex ratio at birth; a bias in natural history traits, for example it is known that individuals live up to two years and males reach sexual maturity earlier than females, maybe reflecting the smaller body size of the Rosa, G.M. et al. males with respect to the females (Guarino et al. 2010). Nonetheless, the strong male biased sex ratio has been commonly recorded in breeding population of explosive breeders (Wells 1977). Data is also available for Boophis tsilomaro where in a group of about 90 males only one female was found (Andreone et al. 2002). Until now the breeding phenology of S. gottlebei was quite unknown, as well as its overall distribution. Our study work in the last years allowed us to unveil some aspects of its habitat preferences and ecology. Our observations at Zahavola showed that the unpredictability and highly seasonal traits of the Isalo Massif are among the reasons of concentrated breeding activities in S. gottlebei. The peculiar rocky and canyon habitats represent selected breeding habitats for the species, and once again show how the Malagasy frog species evolved specialisation traits that only continuing and long-term studies may allow us to describe. Figure 3. Scatterplots of Log10 body mass (g) against SVL (mm) in males (M, shown by filled triangles) and females (F, shown by open circles) of Scaphiophryne gottlebei population from Isalo Massif. Acknowledgements. For help in the field, we are indebted to our guide Anicet and the collaborators Nirhy H. C. Rabibisoa and Tokihery J. Razafindrabe. The study was carried out in collaboration with Madagascar National Parks and Parc Botanique et Zoologique de Tsimbazaza. We are grateful to the Malagasy authorities, in particular the Ministère de l Environnement et des Eaux et Forêts, for research permits. Fieldwork was funded by Mohamed bin Zayed Species Conservation Fund, Gondwana Conservation and Research, EDGE, and Zoological Society of London. References Andersson, M. (1994): Sexual selection. Princeton: Princeton University Press.

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