Basic and Applied Herpetology 31 (2017) 117-123

The diurnal aggregation behavior in cochranae tadpoles (Anura: )

Thiago Augusto Leão-Pires1,*, Ariovaldo Giaretta2, Ricardo Jannini Sawaya3

1 Instituto de Biologia, Universidade Estadual de Campinas. Cidade Universitária Zeferino Vaz - Barão Ge- raldo, 13083970, Campinas - São Paulo, Brazil. 2 Laboratório de Taxonomia, Sistemática e Ecologia Comportamental de Anuros Neotropicais, Faculdades Integradas do Pontal, Universidade Federal de Uberlândia. Rua João Naves de Avila, 2121, 38408100, Uberlândia - Minas Gerais, Brazil. 3 Departamento de Ciências Biológicas, Universidade Federal de São Paulo, Campus Diadema. Rua Prof. Artur Riedel 275, 09972270, Diadema - São Paulo, Brazil.

*Correspondence: Phone: +55 19 35216381, Fax: +55 19 35216374, E-mail: [email protected]

Received: 21 September 2016; returned for review: 13 November 2016; accepted 20 January 2017.

We investigated schooling behavior of Phasmahyla cochranae including its periodicity based on period- ic regression models. The school structure and differences between day and night were discussed. We found that tadpoles formed aggregative schools, which were significantly more frequent dur- ing the day than at night. During the day, from 06:30 to 18:00 h, tadpoles formed one or two polar- ized schools at the water surface. Based on these results and on observations of specific behaviors, we suggest that daylight may be a significant environmental factor related to schooling behavior in P. cochranae, although this hypothesis needs to be further investigated.

Key words: ; cyclic data; diel preference; gregarious behavior; schools.

Many species show gregari- iations in water temperature (Brattstrom, ous behavior during the larval stage in 1962) and daylight (Brattstrom, 1962; aquatic environments (McDiarmid Al- Katz et al., 1981; Wassersug et al., 1981; tig, 1999). In fact, there are at least nine Branch, 1983). families of anurans, including Phyllome- Daylight has been shown to trigger dusidae, in which tadpoles form aggrega- aggregative behavior (Beiswenger, 1977; tions (Wells, 2007). This aggregation be- Branch, 1983; Eterovick Sazima, 1999; havior can exhibit irregular distribution of Surova, 2006) and to influence orientation individuals in constant rotation, or large of tadpoles in ponds (Katz et al., 1981; compact polarized groups usually called Wassersug et al., 1981). Low water visibility “schools” (Wassersug et al., 1981). School- in ponds caused by diminishing of day- ing behavior may be the result of individu- light or by increased water turbidity nega- al responses to the presence of other tad- tively affects tadpole aggregations, and poles and / or of other external stimuli may even cause dispersal of tadpoles (Wassersug Hessler, 1971; Beiswenger, (Beiswenger, 1977; Branch, 1983). In- 1975), such as cannibalism or predation creased visibility under high light condi- (Brattstrom, 1962; Beiswenger, 1977), var- tions may favor visually-oriented aquatic

DOI: http://dx.doi.org/10.11160/bah.55 SHORT NOTES predators (Morin, 1983; Wilbur et al., 46˚30’18’’ W), Atibaia municipality, São 1983; Lima Dill, 1990). With reduced Paulo. This is a reserve with a total area of sunlight at dusk, predation risks probably approximately 10 000 ha, and occupies decrease because of low prey detectability, part of the municipalities of Mairiporã, and therefore sunlight could have a direct Nazaré Paulista, Atibaia and Bom Jesus and indirect influence on tadpole behav- dos Perdões, in a mountainous region with ior. elevations ranging between 900 and 1400 Aggregation behavior in tadpoles has m and annual rainfall from 1400 to 1700 been well studied in numerous species, mm. The vegetation type is high elevation, including bufonids (Anaxyrus americanus, semi-deciduous forest (Neto et al., 1989; Bufo bufo, B. woodhousei), ranids (Rana cas- Grombone et al., 1990). Natural water bod- cadae, R. temporaria), or pipids (Xenopus ies include ponds, lakes and forest laevis) (Blaustein O’Hara, 1987; Surova streams. Focal observations were conduct- et al., 2009). Within the family Phyllomedusi- ed in a rock pond with approximately 4 m dae, this behavior has been described in of diameter formed within a stream (Fig. some species from the subfamily Phyl- 1b). The specimens were identified by au- lomedusinae (Branch, 1983; Brandão et thors in accordance with species descrip- al., 2009), and more specifically in the genus tion (Fig.1a; Bokermann, 1966). Phasmahyla (Lutz Lutz, 1939; Boker- The studied pond was limited by a rock mann Sazima, 1978), although no report -strewn formation that restricted the water existed so far about the presence of this flow, forming an ovoid pool. A grid built behavior in Phasmahyla cochranae with PVC frames and nylon twine delimit- (Bokermann, 1966). In the present study, ing 252 squares (10 x 10 cm) identified we tested the aggregation behavior of P. with letters and numbers was installed cochranae tadpoles and the diel preference for above this pool (Fig. 1b). We observed the displaying such behavior. swimming behavior and location of indi- Phasmahyla cochranae is a small-sized viduals in the grid from a stationary obser- species (adult snout-vent length: 29.0-45.5 vation point (adjacent, 4 m above the mm, tadpole maximum total length: 55.0 pool), with assistance of binoculars and mm; Bokermann, 1966). Tadpoles (Fig. 1a) artificial light. We started sampling at inhabit small ponds formed in lotic envi- 16:30 h on February 23rd and finished at ronments, such as creeks and streams. It 16:00 h the following day, with a total of occurs in the states of São Paulo, Rio de 48 records made at regular intervals of 30 Janeiro and Minas Gerais in southeastern minutes. For each observation, we record- Brazil, generally in coastal mountain rang- ed the number of tadpoles in each square es such as Serra da Bocaina, Serra do Mar of the grid, and whether individuals were and Serra da Mantiqueira (Cruz Car- polarized (i.e. oriented in the same direc- valho-e-Silva, 2004; Rossa-Feres et al., tion) or not. 2011). Our study was conducted on Febru- To verify if tadpoles exhibited gregari- ary 23rd and 24th, 1995 in the Parque Mu- ous behavior, and if this behavior was var- nicipal do Itapetinga (23˚14’23’’ S, iable during the 24-h sampling period, we

118 SHORT NOTES defined an index of aggregation as the ra- we employed a periodic regression model tio between the number of tadpoles and (Batschelet, 1981). This analytical tool fit the approximate area that they occupied. observed data to a period model, assessing This calculation was achieved by dividing its possible periodicity. The model gener- the number of observed individuals ates a cosine function given by the equa- (minimum = 4, maximum = 8) by the sum tion of squares occupied by at least one indi- y = M + A cos ω (t – θ) vidual and the number of empty squares where t represents the independent varia- located between two occupied squares. ble time, M represents the mean values of In order to evaluate the aggregation the dependent variable (aggregation in- behavior and the periodicity of the data, dex), A is the amplitude, or the range be-

Figure 1: (a) Tadpole of Phasmahyla cochranae (Gosner stage 35, total length 41.12 mm). Author: Mario Sacramento. (b) Grid built with PVC frame and nylon twine delimiting numbered squares of 10 x 10 cm in the studied pond at Parque Estadual de Itapetinga, Atibaia municipality, São Paulo state, Brazil. Author: Ricardo J. Sawaya.

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Figure 2: Circular-linear plot of the aggregation index of Phasmahyla cochranae during 24 hours of observation. The blue bars represent the ag- gregation index values and the black line represents the mean time of the day for the observed aggregations.

tween minimum and maximum values of and generally polarized schools at the wa- the dependent variable, ω represents the ter surface, with stationary positions and angular frequency, and θ represents the heads directed towards the water flow. acrophase or time of maximum peak of the Individuals were distributed leaving small dependent variable. With the aim of test- distances among them (usually < 20 mm), ing if the periodicity variable (time) was but not in physical contact, and the aggre- significant in the model, we used an analy- gate shape was either two small groups or sis of the variance (ANOVA) to compare one large group of eight individuals. Dur- the model with time and the model with- ing the night (18:30-06:00 h), individuals out time as independent variable. dispersed to the bottom of the pond, with We found that tadpoles of P. cochranae greater distances among them (usually > exhibited a periodic gregarious behavior 30 mm) and no evidence of aggregation (F = 21.42, P < 0.001; Fig. 2), in which up to (Fig. 2). seven tadpoles occupied the same 100 cm2 Additionally, we observed four specific square. The amplitude value was A = 1.20 types of behaviors in tadpoles during the and acrophase was θ = -3.00 in radians or monitoring: 1) all tadpoles swimming at 12:30 in hours, indicating that the highest the surface in a polarized form, with values of the aggregation index happened mouth parts on the water surface, suppos- approximately in the middle of the day. edly for foraging, and generally motion- According to our results and field ob- less except for tail tip movements; 2) float- servations, during the day (from 06:30 to ing at mid-water, motionless and polar- 18:00 h), tadpoles often formed cohesive ized, with the head facing upward at an

120 SHORT NOTES angle of about 45˚ and tail tip moving; 3) influence tadpole behavior (Branch, 1983; swimming alongside each other, but stop- Wollmuth et al., 1987). Water transparency, ping and / or changing their position in the for instance, explained most of the varia- grid; and 4) individuals swimming and bility in aggregation size of tadpoles of making series of short displacements (a Phrynomantis microps (Spieler, 2003). Tad- few centimeters) with intervals of short poles of Phyllomedusa vaillanti (Branch, stops and direction changes, presumably 1983) and A. americanus (Beiswenger, not polarized but always staying close to 1977) formed exclusively diurnal schools. each other. Although schooling behavior Experiments including the effects of light was not directly tested, these behaviors in tadpoles of P. vaillanti showed that be- often shown by tadpoles of P. cochranae havior could shift when exposed to light, are related to the description of schooling rather than because of other stimuli behavior made by Caldwell (1989). (Spieler, 2003). We also observed a strong Our results demonstrate that P. association between daytime and aggrega- cochranae tadpoles may show aggregation tion behavior in this study. Our results behavior, particularly during the day, and seem to support the patterns observed in contrast with the description by Boker- other studies, suggesting that daylight mann (1966), who describe this species could be a factor related to aggregation tadpoles as with nocturnal activity and behavior. However, other anuran species surface foragers, while during the day such as Scaphiopus hurterii aggregate at they hid under stones and debris. Thus, night (Bragg, 1948). although our results point out to a diurnal This study represents the first record of activity preference, this should be con- aggregation behavior and the diurnal pref- firmed by means of further research on erence of such behavior in P. cochranae. spatial and temporal replicates. During the Although this first record is still not day, P. cochranae tadpoles were often rec- enough to generalize for all populations of orded in diurnal schools, polarized, mov- the species, our observations agree with ing slowly through the water surface, and other studies conducted on other species swimming near and alongside each other of Phyllomedusinae, such as P. vaillanti, in the same direction. Such type of aggre- and even on other species of the genus gation behavior, although in different dis- Phasmahyla like P. guttata and P. jandaia play forms, has been described in different (Lutz Lutz, 1939; Branch, 1983; Etero- anuran families such as Bufonidae, vick Sazima, 1999; Surova, 2006; Costa Ranidae, Pipidae and Phyllomedusidae Carvalho-e-Silva, 2008), supporting the (e.g. Waldman, 1981, 1982; Foster existence of schooling behavior in P. McDiarmid, 1982), including the subfami- cochranae. ly Phyllomedusinae (Branch, 1983), which Acknowledgement indicates that this is a relative widespread We thank to the two anonymous refer- behavior in anuran tadpoles. ees who carefully reviewed the manu- Experimental observations suggest that script and provide valuable criticism and temperature and light levels in ponds may corrections. TALP thanks Coordenação de

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Aperfeiçoamento de Pessoal de Nível Su- : Phyllomedusinae): tadpole and perior, Fundação de Amparo à Pesquisa calls. South American Journal of Herpetolo- de São Paulo (Processos FAPESP n°: gy 4: 61-68. 2008/54472-2. 2014/23677-9) for grants and Brattstrom, B.H. (1962). Thermal control of aggregation behavior in tadpoles. Herpeto- Mario Sacramento for the beautiful photos logica 18: 38-46. kindly provided. AAG thanks Conselho Caldwell, J.P. (1989). Structure and behavior Nacional de Desenvolvimento Científico e of Hyla geographica tadpole schools, with Tecnológico (CNPq) and Fundação de comments on classification of group behav- Amparo à Pesquisa de Minas Gerais for ior in tadpoles. Copeia 1989: 938-948. financial support. RJS thanks CNPq for Costa, P.N. Carvalho-e-Silva, A.M.T. (2008). financial support. Ontogenia e aspectos comportamentais da References larva de (Lutz, 1924) (Amphibia, Anura, Hylidae). Biota Neotro- Batschelet, E. (1981). Circular Statistics in Biolo- pica 8: 219-224. gy. Academic Press, New York, USA. Cruz, C.A.G. Carvalho-e-Silva, S.P. (2004). Beiswenger, R.E. (1975). Structure and function Phasmahyla cochranae. The IUCN Red List of in aggregations of tadpoles of the American Threatened Species, 2004: e.T55814A11369352. toad, Bufo americanus. Herpetologica 31: 222 International Union for Nature Conserva- -233. tion and Natural Resources, Gland, Switzer- Beiswenger, R.E. (1977). Diel patterns of aggre- land. Available at http:// gative behavior in tadpoles of Bufo ameri- www.iucnredlist.org/details/55814/0. Re- canus, in relation to light and temperature. trieved on 15 September 2016. Ecology 58: 98-108. Eterovick, P.C. Sazima, I. (1999). Description Blaustein, A.R. O’Hara, R.K. (1987). Aggre- of the tadpole of Bufo rufus with notes on gation behavior in Rana cascadae tadpoles: aggregative behavior. Journal of Herpetolo- association preferences among wild aggre- gy 33: 711-713. gations and responses to non-kin. Foster, M.S. McDiarmid, R.W. (1982). Study Behaviour 35: 1549-1555. of aggregative behavior of Rhinophrynus Bokermann, W.C.A. (1966). A new Phyllome- dorsalis tadpoles: design and analysis. Herpeto- dusa from southeastern Brazil. Herpetologica logica 38: 395-404. 22: 293-297. Grombone, M.T.; Bernacci, L.C.; Neto, Bokermann, W.C.A. Sazima, I. (1978). Anfí- J.A.A.M.; Tamashiro, J.Y. Filho, H.F.L. bios da Serra do Cipó, Minas Gerais, Brasil. (1990). Estrutura fitossociológica da floresta 4: descrição de Phyllomedusa jandaia sp.n. semidecídua de altitude do Parque Munici- (Anura, Hylidae). Revista Brasileira de Bio- pal da Grota Funda (Atibaia, estado de São logia 38: 927-930. Paulo). Acta Botânica Brasileira 4: 47-64. Bragg, A.N. (1948). Food resources utilized by Katz, L.C.; Potel, M.J. Wassersug, R.J. (1981). tadpoles of Scaphiopus hurterii in tempo- Structure and mechanisms of schooling in rary pools. The Anatomical Record 101: 706. tadpoles of the clawed , Xe no p us lae vis. Branch, L.C. (1983). Social behavior of the tad- Animal Behaviour 29: 20-33. poles of Phyllomedusa vaillanti. Copeia Lima, S.L. Dill, L.M. (1990). Behavioral deci- 1983: 420-428. sions made under the risk of predation: a Brandão, R.A.; Álvares, G.F.R.; Crema, A. review and prospectus. Canadian Journal of Zerbini, G.J. (2009). Natural history of Phyl- Zoology 68: 619-640. lomedusa centralis Bokermann 1965 (Anura: Lutz, A. Lutz, B. (1939). New Hylidae from

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