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Phyllomedusa 1(1):31-40, 2002 @ 2002 Melopsittacus Publicações Científicas ISSN 1519-1397

Why do breeding colonize some puddles more than others?

Paula Cabral Eterovick and Geraldo Wilson Fernandes

Ecologia Evolutiva de Herbívoros Tropicais, Caixa Postal 486, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. 30123-970. Belo Horizonte, MG, Brasil. E-mail: [email protected]

Abstract The composition of anuran communities at the Serra do Cipó (southeastern Brazil) was studied to familiarize ourselves with the species that breed in natural puddles. An experiment with artificial puddles was conducted to investigate the relationship of several physical properties of puddles to the pattern of their colonization by breeding anurans; the factors included were puddle size. permanency. pH, distance from a colonizing source, and abundance and richness of potential tadpole predators. Estimates of anuran species richness wet"e based on records of tadpoles and calling ma- les; species richness was higher in puddles with more types of tadpole predators. The number of species of tadpoles was higher in less ephemeral puddles with more predator types, and the number of species of calling males was higher in puddles having greater abundances of tadpole predators. Males may not be sensitive to tadpole-predation risk when they select calling sites, and the same physical characteristics of the puddles may attract both tadpole predators and anurans. For éxample, puddle permanency probably is such a feature, because in the less ephemeral puddles there were more species of tadpoles. as well as greater numbers and species richness of predators.

Keywords: Anura selection, tadpole predators, puddle permanency, southeastem Brazil.

Introduction larger scales, factors such as local extinction and recolonization, and pond succession probably At a relatively small spatial scale, the spatial are important (Marsh and Borrell, 2001). and temporal distribution of anuran populations Behavior associated with se1ection of and species during reproductive activities may oviposition site contributes to spatial and tempo- be influenced by choice of oviposition site; at ral variation in patterns of abundance or population dynamics, and is influenced by habitat quality and interactions with conspecifics

Received 23.05.2001 or predators (Resetarits and Wilbur, 1989; Accepted 02.10.2001 Marsh and Borrell. 2001 ). Some environmental .

Phyllomedusa 111.Jonuorv 2002 Eterovirk nnd Fernand",

factors known to influence habitat selection by occur every year. Anuran species richness may reproducing anurans are leaf litter availability, be determined by site selectivity by the surface area, depth of water (Marsh and Borrell, colonizers (which may be sensitive to variables 2001), shade (Wemer and Glennemeier, 1999), such as pool size or potential permanency) and and water chemistry and transparency (Leuven their ability to reach a given puddle and cope et al., 1986; Evans et al., 1996). with the prevailing environmental conditions. Isolation of water bodies is a major factor We determined the composition of anuran influencing anuran distribution, especial1y in assemblages in natural temporary puddles and species with limited dispersal abilities or in then tested whether puddle size, permanency, species that rely on breeding that vary pH, distance from a colonizer source, and in space and time, such as temporary puddles abundance. and richness of potential tadpole (Marsh et al., 1999). The time taken by Tungara predators influenced anuran species richness in frogs ( pustulosus) to colonize artificial puddles. available ponds increased with pond isolation at Barro Colorado Island (Marsh et al., 1999), and Methods in areas with isolated water bodies, may not be able to avoid oligotrophic and acid Study site waters by means of habitat selection as they do The study was conducted at the montane at less isolated oviposition sites (Leuven et al., meadows of the Serra do Cip6 (19°12'-19°20'S, 1986). 43°30'-43°40'W, 1095-1485 m e]evation), Mi- At larger spatial scales, species distribution nas Gerais, southeastem Brazi]. Many temporary depends on colonization abilities and successful wet]ands and some pudd]es appear during the establishment of species. Factors such as rainy season at the site and are used by anurans landscape pattems and proximity of suitable during reproductive activities. The rainy season habitats may facilitate dispersal, whereas factors starts in October or November and ends in such as pond chemistry and predation pressure March. may cause environmental resistance and prevent tecruitment (Bunnell and Zampella, 1999). Once Field activities colonization occurs, interspecific competition, We studied six natural puddles (Table 1) predation, and pond drying may interact to from November 1998 to March 2000. We produce pattems of distribution and composition sampled tadpoles and ca1ling males monthly of tadpole assemblages (Morin, 1983; Skelly, during the rainy season and bimonthly during 1996). In southeastem Michigan, Skel1y (1996) , the dry season. One man-made puddle (Puddle found that more permanent ponds had morea., 3) near the upper entrance of the National Park predators of larger sizes and greater taxonomic of the Serra do Cip6 is used by some diversity than did less permanent ponds. species and functions as a natural puddle. Differences in the ability of tadpoles to gamer Tadpoles that could not be identified in the field resources and avoid predation were reflected in were co1lected and identified by comparison their distributions among pond sizes: tadpoles with specimens housed in the co1lections of the from smal1, temporary sites spend more time Universidade Federal de Minas Gerais (UFMG), feeding and cah develop faster than tadpoles MG, Brazil, and Museu de Hist6ria Natura1 Uni- from large, permanent sites, where the larvae versidade Estadual de Campinas (ZUEC), Cam- must spend more time hiding from predators pinas, SP, Brazil. Specimens co1l~cted during . and, as a consequence, develop more slowly this study were deposited in the herpetological (Skel1y, 1997). co1lection of the Departmento de Zoologia of In temporary puddles, colonization must the UFMG.

Phyllomedusa 1 ). Jonuorv 2002 Whv do breedinR froRs colinize some puddles more than others

~ õ' !'! :!I !") "' .. a " ~

Figure 1 Views of Puddle 4, the anuran colonizing source (A) and a 2m-diameter artificial puddle just after lining with a plastic tarpaulin (8).

To investigate the co1onizing abi1ity of quickest after the rainy season remained intact. anurans that use pudd1es to reproduce and their These .were inc1uded as contro1s (Tab1e 2). We preferences regarding puddle size, we dug 18 ar- measured water pH of natural and artificial tificial puddles at increasing distances from a pudd1es containing water on 21 November 1999 natural puddle (Puddle 4; Figure 1A, Table 1) (Tab1es 1,2). that served as a colonizing source. The circular Potentia1 tadpo1e predators were counted puddles were of three different sizes -0.5, 1.0, and identified as one of seven types -Anisoptera and 2.0 m diameter. They had volumes of 0.05, naiads (Odonata), water bugs (Be1ostomatidae), 0.20, and 0.79 m3 respectively, and all were 25 waterscorpions (Nepidae), backswimmers cm deep. We positioned one puddle of each size (Notonectidae), water scavenger beet1es(Hydro- at 5, 10, 20, 40, 80, and 160 m (Table 3) from phi1idae), whir1igig beet1es (Gyrinidae), and the source along three 160-m transects starting spiders (Thaumasia sp., Pisauridae). A11of these at the natural puddle. The angles between taxa can prey upon anuran eggs and 1arvae Transects 1 and 2, and 2 and 3 were about 45° (Borror et al. 1992, Roth and Jackson 1987, and 35°, in order to position them as far apart as Sazimaand Bokermann 1977, Sea1e 1980, A. J. possible and away from a small permanent dos Santos, pers. comm.). Leptodactylus stream that passed about 10 m from the source lab)'rinthicus tadpo1esfeed on eggs and tadpo1es puddle. Frogs that breed in the stream do not of ~ther species of anurans (M. Martins, pers. reproduce in puddles. Therefore, we assumed comm.). A1though these tadpo1es cou1d be that they would not interfere in the experimental considered as an additiona1 predator, we did not colonization process. We visited these puddles inc1ude them in the ana1ysesbecause they on1y once or twice a month during the rainy seasons appeared in the 1ast samp1ing. of 1999/2000 and 2000/2001 until alI the puddles had dried. The most distant artificial Statistical analyses puddles dried quickly; and during the second We used stepwise multiple linear regres- rainy season, we attempted to prolong the sions (Systat, 1998) to relate puddle volume, . duration of these pudd1es by lining the basins permanency (number of months with water per with plastic tarpaulins (Fig. 1B). Most tarpaulins year), pH, distance from the colonizer source, were sto1enand only two of the smallest puddles number of tadpole predator types (richness), and farthest from the source that usually dried total number (abundance) of potential tadpole

Phyllomedusa 1 11 ). Januarv 2002 Eterovick and Fernande.f

Table 1 -Number of anuran species (tadpoles/calling males) found in six natural puddles at the Serra do Cip6. Southeastern Brasil from November 1998 to March 2000. The puddle used as colonizers source in the experiment with artificial pools is marked with an asterisk.

Number Number of Number of Total Number of Volume of months H species of number of (m3) with water p predator Puddle species types calling males per year

8

predators (as independent variables) to the Results number of species of tadpoles, calling males, and species of tadpoles plus cal1ing males (as In the six natural puddles (Table 1), we dependent variables). Separate analyses were found (1) calling males and tadpoles of conducted for tadpoles, cal1ing males, and duartei, S. squalirostris, Leptodactylus jolyi, L. tadpoles plus cal1ing males. We used only the syphax, and Odontophrynus americanus, (2) data from the first rainy season for the plastic- calling males of Leptodactylus cunicularius, L. lined control puddles in this analysis, because furnarius, L. fuscus, and Physalaemus cuvieri; the tarpaulins represent an additional variable. and (3) tadpoles of Leptodactylus camaquara, Had these puddles not remained with the tarpau- L. cf. ocellatus, and Physalaemus evangelistai. lins, they probably would not have retained In the source puddle (Puddle 4), we found water long enough for colonization to occur, as calling males of Scinax duartei, S. squalirostris, evidenced in the first year. We also conducted a Leptodactylus furnarius, L. jolyi, Physalaemus stepwise, multiple linear regression to test cuvieri, and tadpoles of S. duartei, Lepto- whether the independent variables puddle volu- dactylus jolyi, Odontophrynus americanus, and me, permanency, pH, and distance from the , Physalaemus evangelistai. We also heard males colonizer source related to number of tadpole ~ .6f Hyla albopunctata and H. cipoensis calling predator richness, and another to test whether from the nearby stream. During the additional these same independent variables related to sampling period while we conducted the expe- tadpole predator abundance. riment and continued sampling Puddle 4, we Because we found few natural puddles at also found tadpoles of Phrynohyas venulosa and the study site, and many additional variables an egg mass of Physalaemus cuvieri in the (e.g., vegetatiol? cover, puddle morphometry; source puddle. This and some experimental Bunnell and Zampella, 1999; Marsh and puddles located nearby apparently were Borrell, 2001) may influence anuran connected to the stream during heavy rains colonization in these puddles, there were because a small fish (Trychomycterus brasilien- insufficient data to determine statistical1y the sis Reinhardt, Trichomycteridae) appeared in one of the 2-m artificial puddles 5 m from main factors determining anuran colonization . of the puddles. Puddle4.

Phyllomedusa- 1 (1), January 2002 Whv dl} breedinR frl}RS cl}linize some puddles mlJre than l}ther!

Table 2 Number of anuran species (tadpoles/calling males) found in artificial puddles at the Serra do Cip6 (MG) and in Puddle 4 (see Table I), from October 1999 to February 2001. Two artificial pools with 0.5 m diameter remained lined with a plastic tarPaulin during the second sampling period, keeping water for 6 months (*).

Distance Number Number Artificial from Number of Number of Total Number of months of Number puddles Volume the of species with pH species of of {m3) natural (by size) water per predator predators of species (m) puddle vear types calling larvae males (m)

1.56 6.89 4 14 4 ii

The tadpoles found in the artificial puddles from adults having bred at the puddles, rather occurred in large numbers and all the taxa, than the larvae having been washed in from the except Leptodactylus syphax, typically are stream by floods. Leptodactylus syphax tadpoles found as larvae in standing water. Therefore, we usually occupy permanent or temporary streams; assumed that the tadpoles we observed resulted however, their occurrence in three different ..

Phyllomedusa Jonuorv 2002 Eterovick and Fernande.v

Tahle 3 Number of anuran species that colonized artificial pools of different sizes and located at different distances from a potential colonizer source (the natural Puddle 4).

Distance from Anuran Number of Total number Puddle4 Species Dredator types of Dredators (m) total

s 3 4 4 4 24

10 1 1 4 5 6 32

20 1 3 2 4 5 22

40 1 O O 1 4 6

80 O O 2 2 3 6

160 O O O O O O

Total 1 4 ~ 7 7 90

puddles. along with their absence in the puddles 2) after the variables distance from source, pH, located among those occupied. suggest that they and predator abundance are eliminated through probably came directly from their nests rather the stepwise procedure. Puddle volume (P = than having been carried from the nearby stream 0.094) and permanency (P = 0.129) also were by floods. included in the model. The number of species of In the artificial puddles. we found calling tadpoles in the puddles are positively correlated males and tadpoles of Leptodactylus jolyi. to number of types of potential tadpole Odontophrynus americanus. and Physalaemus predators and puddle permanency (R = 0.877; P cuvieri. There were calling males of Scinax = 0.020 and P = 0.037, respectively; Figures 2 duartei and tadpoles of Leptodactylus labyrin- and 3). Puddle volume also was included in the thicus and L. syphax. model (P = 0.140) and the remaining variables The puddles with plastic liners retained were eliminated through the stepwise procedure. water for the entire rainy season. but no anurans The numbe:r of calling males are positively colonized them. Abundant growths of algae and related to abundances of potential tadpole fungi fouled the water. and this condition may predators (R = 0.640; P = 0.010; Figure 4). be unsuitable for the development of anuran , Potential tadpole predator richness increases '" eggs and tadpoles. We found dead egg clutches with puddle permanency (R = 0.700; P = 0.006; attacked by fungi at Serra do Cip6 in temporary Figure 5), after elimination of the variables stream backwaters that kept some standing water puddle volume and isolation. Potential tadpole during the dry season. The water in all natural predator abundance increases with puddle puddles having anuran eggs and tadpoles always permanency and volume (R = 0.806; P = 0.009 was clear. The pH of the artificial puddles varied and P = 0.041, respectively; Figure 5), with only from 6.89 to 7.ll.among puddles (Table 2). isolation having been eliminated from the The number of anuran species (including analvsis. . both tadpoles and calling males) that colonized the artificial experimental puddles are positively Discussion correlated to the number of types of potential tadpole predators (R = 0.977; P = 0.014; Figure Because natural, temporary puddles are

Phy11omedusa Januarv 2002 Why do breedingfrog.f colinize .fOme puddles more than others ?

5

'" 4 In 4 & ., " õ "u a. " "O 3 o. In 3 .B ~ "õ .. '" 2 ~ 2 8 8 ., ~ "u .. 8. 'õ .. '" ~ "õ -O E Q; o ~ .O 8 .o z o E ~ z , , 1 3 5 7 4 5 6 rfchness Puddle permanency

Figure 2 Relation between the number of tadpoles (b) Fi~ure 3 Relation between the number of tadpole and anuran species (tadpoles plus caIling ~a- species and puddle permanency (number of les) (Â.) and tadpole predator types foundf in months with water per year) in 18 experimental 18 experimental artificial puddles at the Srtra artificial puddles at the Serra do Cipó, do Cipó, Southeastern Brazil. southl:astem Brazil.

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.u " o. "' ~ O o

~ .o E " z 4 9 14 '9 Tadpole pradator abundance

..II ., Fi2ure 4 Relatlon between the number of specles ; f FIgure, 5 Relation between puddle permanency (number i. ca11ing males and tadpole predator types fou d of months with water) and richress (Â) and in 18 experimental artificial puddles at the S - abundance (O) of potential tadpole predators ra do Cip6, Southeastern Brazil. !1 found in the 18 experimental artificial puddles at the Serra do Cipó, Southeastem, Brazil.

uncommon at the study site and are highl~ diversity in four Amazonian ponds. If such variable in physical and biological propertie$, correlations exist, a larger sample size of ponds we found no correlates of these properties with may be necessary to reveal them. anuran species richness. Wild (1996) failed tp In the natural puddles that we studied at the 111 detected correlations among physical featur~ Serra do Cip6, many species that were not (water temperature, dissolved oxygen, and pIt present in the first sampling year appeared in the and tadpole species richness, evenness, c! second sampling year (e.g., Leptodactylus

Phvllomedusa - I). Jonuorv 2002 Eterovick and Fernande.v

syphax and Odontophrynus americanus in habitat selection occurred. L. labyrinthicus may Puddle 1, L. syphax in Puddle 2, L. cf. ocellatus have come from even greater distances, because in Puddle 5, Scinax duartei in Puddle 6); these we did not find this large species (SVL = 15 cm) occurrences may indicate colonization events. It with a loud mating call within a 200-m radius is also possible that some years prove unsuitable experimental area. Thus, the most distant artifi- for reproduction by certain species owing to cial puddles may have not been colonized some combination of environmental features; because they did not retain water long enough such species may remain in the area without for colonization to occur; thus, puddle perma- reproducing. Estimates of the rates of dispersal nency, rather than isolation, is the most likely and colonization of new breeding sites by limiting factor. Túngara frogs (Physalaemus anurans in patchy environments are needed. pustulosus) disperse from breeding sites and Anuran dispersal to new reproductive sites is gradual1y find new sites at greater and greater difficult to estimate by standard mark-recapture distances (Marsh et al., 1999). At least 30% of studies, because it is extremely difficult to these frogs regularly disperse between ponds 50- census alI possible dispersal destinations (Porter 200 m apart, and the species is known to move and Dooley, 1993). This is especially of sites more than 200 m from one pond to another such as the montane fields of the Serra do Cipó, (Marsh et al., 1999). Túngara frogs also repro- where many ephemeral habitats are used by duce in temporary bodies of water and such anurans for reproduction in ways that vary dispersal abilities may be widespread among annual1y (I. Sazima, unpubl. data; PC~, pers. anurans that use ephemeral habitats. The lengths of the transects through which obs.). A molecular approach might produce useful estimations of migration rates among artificial puddles were positioned might not populations (Parker et al., 1998) and is currently have posed any difficulties to dispersing being applied to estimate migration rates of anurans, but water turbidity and the presence of Hyla saxicola among breeding sites at the Serra fungi and decomposing matter seemed to prevent anuran oviposition in the puddles that do Cipó (PCE, unpubl. data). Al1 the puddles studied are isolated, but remained lined by tarpaulins. High concen- many anuran species that use them for repro- trations of organic acids can cause embryonic duction also can use swamps and stream pools mortality in anurans (Freda et al., 1990), and that may serve as colonizing sources. Based on low pH can facilitate fungal infections (Gascon our experiment, it is clear that distances up to 80 and Planas, 1986). In the remaining artificial m are traversed with ease by some dispersing puddles. the smal1 range of pH (0.22) values anurans. Leptodactylus labyrinthicus and probably was not important. The amount of Physalaemus cuvieri occupied a puddle locate~ emergent herbaceous vegetation (Bunnel1 and 80m from the source, and this puddle was the \ Zampella, 1999) influences tadpole richness in only one at this distance that kept water for more natural puddles; however, alI artificial puddles than two consecutive sampling months. The had bare soil on the bottom were surrounded by other puddles located 80 m from the source may ..homogeneous herbaceous vegetation and lacked not have retained water for a sufficient length of submerged vegetation. These features of the arti- time for colonization to occur. Physalaemus ficial puddles may have prevented their coloni- cuvieri may have used "stepping stone" zation by Scinax duartei and S.. squalirostris dispersal to reach the colonized puddle, but in from Puddle 4, because these frogs prefer to call spite of cal1ing from some puddles closer to the on shrubby vegetation and their tadpoles use natural colonization source, the species repro- microhabitats with aquatic or submerged vege- .. duced only at the most distant puddle containing tation (Eterovick and Sazima, 2000; PCE. pers. water. This seems to indicate that some kind of obs.).

Phy1lomedusa -1 (1 ), January 2002 ..

,

Whv do breedini froRs ,linize some puddles more than others ?

In experimental puddles, total number of which develop in one and one to two months, potential tadpole predators are positively related respectively (PCE, unpubl. data). Tadpoles are to the number of species of calling males. and subject to a trade-off between their abilities to potential tadpole predator richness is the most garner resources and avoid predation at the same useful parameter to explain the distribution of time (Skelly, 1996). Populations living in tadpoles and cal1ing males plus tadpoles. It temporary waters must be adapted to a seems that males do not avoid puddles that chemically and physically unstable medium, and represent a higher predation risk for their must be able to reproduce and develop in offspring, and may select puddles based on other compressed time frames in a fluctuating features. These features also may attract the environment (Bonner et al., 1997). Species aquatic invertebrates that prey upon tadpoles. having rapid developmental rates may be able to Skelly (1996) found average predator density use more ephemeral habitats and thereby avoid a and richness to increase with pond permanency. higher predation risk. as did we. Tadpoles. as well as their predators. In habitats with low predictability (e.g., have higher species richness in puddles that temporary bodies of water), community retain water for longer periods of time. structure probably is governed by stochastic The longer a puddle persists, the greater the processes (Bonner et al., 1997). Therefore, it is opportunity for anuran colonization. We did not erroneous to make generalizations about a observe a temporal distribution of colonization "typical" temporary pool ecosystem, becatlse however. because it occurred mostly in each ephemeral pool is a unique habitat. December. when most puddles were ful1. If Moreover, reproductive success of anuran females are more sensitive than males to choice populations in such habitats may vary greatly of reproductive sites. then the reproductive from year to year (Bonner et al., 1997). In spite success of males calling from more permanent of this unpredictability and stochasticity, a puddles would be greater than those cal1ing from relationship between puddle permanency and ephemeral sites. Alternatively, clutches tadpole species richness could be detected in deposited in puddles that are more permanent this study, and puddle permanency seems to be a may have been more successful, because key factor influencing the composition of anuran tadpoles in more ephemeral puddles die from communities in temporary habitats at the Serra desiccation. This hypothesis seems less probable do Cipó. because if tadpoles had been present in such temporary puddles, we would have recorded Acknowledgements them while the puddles retained the water. The positive correlation between the number of &.We thank I. S. Barros, M. Callisto, M. O. C. predator types and the number of species of Goulart, I. F. Gonçalves-Ir., and L. B. Nasci- tadpoles may be a consequence of longer puddle mento for help in field work, R. Altig, C. permanency. which is advantageous for both Gascon, C. F. B. Haddad, and W. R. Heyer for predators and prey. Indeed, both potential critical revision of the manuscript, alI the staff of tadpole predator richness and abundance the Parque Nacional da Serra do Cipó for their increases with puddle permanency. The only kindness and for providing us with lodging anUran species found in. a puddle that kept water during the field work; the Sansuy Indústria de for two months was Physalaemus cuvieri; Plásticos for providing the plastic tarpaulins for however. no egg clutches or tadpoles were the experiment with artificial puddles, the Insti- . found. The most temporary puddle in which we tuto Nacional do Meio Ambiente e dos Recursos found tadpoles included Leptodactylus Naturais Renováveis (Ibama) for the license to labyrinthicus and P. cuvieri. the tadpoles of conduct this work at the Parque Nacional da

Phyllomedusa -1 ( January 2002 Eterovick (lnd Fernande.1'

Serra do Cipó; the Programa de Demanda Social Marsh, D. M., E. H. Fegraus, and S. Harrison. 1999. Effects of breeding pond isolation on the spatial and (Capes), the Fundação de Desenvolvimento da temporal dynamics of pond use by the tungara frog, Pesquisa (Fundep), and the Post Graduation Physalaemas pustulosus. Journal of Ecology Program in Ecologia, Conservação e Manejo de 68: 804-814. Vida Silvestre for financial support. ~ Morin, P. J. 1983. Predation, competition, and the composition of larval anuran guilds. Ecological M(mographies 53: 119-138.

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Marsh, D. M. and B. J. Borrell. 2001. in press. Flexible Wild, E. R. 1996. Natural history and resource use of four oviposition strategies in túngara frogs and their Amazonian tadpole assemblages. Occasional Papers imDlications for tadDole sDatial distributions. Oikos 92. (}f the Museum of Natural Hi.ftory of the University of Kansas 176: 1-59.

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Phyllomedusa- 1 (1), January 2002