Chec List Checklist of Amphibians in a Rice Paddy Area In

Checklist of amphibians in a rice paddy area in the pecies S

1* 1 1

ists Leonardo Felipe Bairos Moreira and Leonardo Maltchik L Uruguayan savanna, southern Brazil , Débora Schuck Knauth

1 Universidade do Vale do Rio [email protected] Sinos – UNISINOS, Laboratório de Ecologia e Conservação de Ecossistemas Aquáticos, Av. Unisinos, 950, CEP 93022–000, São Leopoldo, RS, Brazil. * Corresponding author. E-mail: Abstract: With the objective of contributing to conservation strategies for areas outside conservation areas, we present

an inventory of the amphibians occurring in rice fields with different types of management (conventional and organic), in Sentinela do Sul, state of Rio Grande do Sul, Brazil, a grassland area in the Uruguayan savanna ecoregion. Between August 2010 and April 2011, we collected tadpoles in rice fields and natural ponds. We recorded 14 species of six families, and only anuraneight of speciesthese species composition. occurred Since in rice few fields. areas Speciesof Uruguayan composition savanna differed lie within between conservation organic units,and conventional it is paramount fields. to developHabitat conservationfeatures (time measures of flooding, that presence help maintain of fish, biodiversity presence of in vegetation) agroecosystems. may act synergistically with agrochemical effects on

DOI: 10.15560/10.5.1014

Introduction Grande do Sul are concentrated in this region in southern Small wetlands have become one of the main priorities Rio Grande do Sul (Maltchik et al. 2003). of conservation agendas because they support high The objective of this study was to contribute to the development of conservation strategies for areas not et al. protected by conservation units. We surveyed amphibians 2002).aquatic Habitat diversity loss and associated are in decline with agriculturalthroughout expansionthe world, isdue probably to expansion the principal of the human cause ofpopulation natural wetland (Amezaga declines (conventional and organic) in the Uruguayan savanna ecoregion,in rice fields and we with also differentsampled natural management ponds near regimes the have been considered important wetland substitutes, and agricultural matrix to determine which species are actually (Czech and Parsons 2002). Managed by man, rice fields using the agricultural areas. We studied tadpoles instead foraging and reproduction (Duré et al. of adults to determine species presence, since some many organisms use et these al. 2010). cultivated Nevertheless, fields as the areas use for of characteristics make these individuals good models for 2008; Machado and Maltchikon management 2010; Piatti practices, such as use of agrochemicals orrice organic fields as cultivation, substitutes irrigationfor natural water wetlands origin, may and depend off- thanfield adults)inventories (Andrade and aquatic et al. 2007). monitoring studies (general et al. 2010). abundance and longer permanence in the aquatic habitats Materials and Methods inseason South use America, of crop areaand the(Donald state 2004; of Rio Kato Grande do Sul The study took place in Sentinela do Sul (Figure 1), in Currently, Brazil is an important area for rice production the central-west portion of the coastal plain of Rio Grande agroecosystemsaccounts for 67.5% is important of rice productionbecause conservation in Brazil (IBGEunits 2012). Information about the biota associated with these climatedo Sul (30°42′00″ of this region to 30°45′09″ is subtropical, S; 51°37′52″ moderately to 51°41′58″ humid, Most of the currently documented amphibian species andW), theover temperature one complete varies rice between field cycle 11°C (2010-2011). in the winter Theand cover only 3.4% of total area of the state (SCP 2011). 26°C in the summer, with an average annual temperature (Segalla et al. 2012). These new species descriptions, which inhave Brazil occurred have at been regular discovered rates, are over a strong the last indication forty years that mm/year (Maluf 2000). of 18.5°C. Annual precipitation varies from 1500 to 1700 inventories directly assess the diversity of an area over to management type (organic and conventional). athe short Brazilian amount amphibian of time. fauna This isdata poorly could known. be critically Species The rice fields were divided into two types according important to conservation policies created for natural and managed areas (Silveira et al. 2010). Amphibian richness organophosphorusAgrochemicals are notand applied carbamate to organic insecticides, fields, while and in glyphosate-basedthe conventionally herbicides managed application fields, inorganic is concentrated fertilizers, in higher,in Rio Grande especially do Sul in represents the Uruguayan approximately savanna 10%ecoregion, of the inspecies the southern registered portion in Brazil, of and the this state richness (Borges-Martins could be even et the early rice growing period. The flood regime is rotated al. 2007). Most of the wetlands and rice paddies of Rio lastin organic approximately fields to 2eliminate weeks, based arthropod on water pests availability and weeds in and keep the soil fertile. Cycles of flooding and dry downs

1014 Moreira et al. | Amphibians in rice fields, southern Brazil

Figure 1.

Study area and habitats sampled: (A) map showing the location of study area (black square) in the central-west coastal plains of Rio Grande do Sul, Brazil; (B) natural pond; (C) conventional rice field; (D): organic rice field. landscape around crop edges (Figure 1), which have 2010), early growing (January 2011), and late growing relativelythe region. more Organic native crops vegetation also support than conventional a heterogeneous crops. (Aprilcycle: off-season2011). The (August off-season 2010), period soil preparation occurred when (October the The rice plantations in the study site were divided into various 1 ha plots that are interconnected by drainage irrigation canals and scattered ephemeral plots. During land is fallow, and the fields retained water only in the range of practices, such as plowing to incorporate stubble Watercanals leveland secondary in the drainage roads. canalsThe canals is controlled (2–5 m wideby weirs and anddry aerate field conditions, the soil, harrowing soil preparation and leveling includes to break a wide and that0.5–1.5 supply m deep) the arerice filled plots with (~10 water cm fromwater nearby per 130 streams. days) puddle clods of soil and incorporate organic matters into during the cultivation cycle. We sampled four study plots (1 ha) in each of the two by rice emergence (seedlings < 10 cm tall) and a shallow cultivation methods within a 10 km radius. We avoided watersoil thoroughly. level, while The the early rice growing was > 100period cm is tall characterized and water using plots near other types of vegetation because we were depth was increased to protect plants during the late growing period. specifically interested in the species that use rice fields. typicallyIt was not bordered possible by to a selectstrip of fields vegetation. surrounded We sampled by similar four collectedOn each by samplingkicking up occasion, the substrate tadpoles and werethen sweeping collected naturalhabitat inponds the organicto determine fields whichbecause species fields use in theagricultural area are abovewith a thedip disturbednet (0.4 × area.0.3 m; Three 0.5 mm).random The sweeps samples of were 2 m areas. The mean water depth is approximately 40 cm in the water volume of the ponds is greatly reduced. The each were performed in each rice study plot (rice field vegetationsampled natural around ponds; the ponds however, is composed during dryof a summers,mosaic of or pond). Collected tadpoles were anesthetized with semideciduous forest and steppe (Cordeiro and Hasenack thebenzocaine herpetological and fixed collection in 10% formalinof the Museu (collecting de Ciências permit – SISBIO # 24082-2). Voucher specimens are housed in

2009).Sampling The studyoccurred plots four were times at during least the 600 rice m cultivation from one e Tecnologia da Pontifícia Universidade Católica do Rio another to minimize spatial autocorrelation. Grande do Sul (MCP12570-12579), Brazil. We performed an ANOVA using permutation analysis1015 Moreira et al. | Amphibians in rice fields, southern Brazil to test for differences in tadpole richness and abundance in more than one ecoregion, such as Atlantic coast restingas, Cerrado, and Uruguayan savanna (Maneyro and Carreira et al. 2013). Despite the low sampling effort, between natural ponds and rice fields. ANOVA permutation amphibian richness in our study is comparable with other analyses were performed with the package lmPerm rice2012; paddies Haddad in South America (Table 2). Such results could Results(Wheler 2010) in R.15.1 (R Development Core Team 2012). be attributed to the idea that only generalist species are We found eleven anuran species of the following et al. et al. 2010). Amphibians that depend on able to remain in areas converted to rice fields (Doody Leptodactylusfamilies: Bufonidae fuscus group (1), Hylidae were assigned (4), Leptodactylidae to the same be 2006;exposed Piatti to high levels of agrochemicals, which could (5),taxon. and Anuran Odontophrynidae richness and (1) abundance (Table 1). differed Tadpoles between of the ponds within or surrounded by agriculturalet fieldsal. may = directly or indirectly affect biota (Peltzer 2008; natural ponds and rice fields (Figure 2; richness F2,45 2,45 4.146,type. Hylid p = 0.03; tadpoles abundance were F associated = 271.08, pwith = 0.05). organic We found rice seven species in the rice fields, four in each management pondsfields, andhad eightLeptodactylidae species, although species tadpole that make abundance foam nests was were found in conventional rice fields (Table 1). Natural adults of six species, divided into two orders (Anura and Gymnophiona),higher in these areaswere thancaught cultivated during tadpole areas. In samplings addition, (Figure 3). Three species were found in conventional rice Elachistocleis bicolor, Hypsiboas pulchellus, and Pseudopaludicola falcipes) and three species in natural pondsfields ( Chthonerpeton indistinctum, Leptodactylus latrans, and Rhinella dorbignyi). This raised the total number of amphibians registered to 14 species of six families. Tadpoles were registered in all samplings of natural season and in the early growing period of rice cultivation. Weponds. caught In organictadpoles crops, only during we caught the early tadpoles growing in the period off- distribution, we caught most of species in the spring/ summerin conventional samplings. rice Nevertheless, fields. With respectHypsiboas to pulchellus temporal and Physalaemus henselii were collected only in the winter.

Discussion of speciesIn our study, richness the totalobserved number in theof species region found(Loebmann in the rice fields and neighboringet al. ponds representset about al. 2011). 60% Figure 2. Mean values of tadpole richness and abundance in natural 2005; Borges-Martins 2007; Quintela By analyzing geographical distribution, all species are ponds and rice fields, throought the rice cultivation cycle (2010–2011), in a rice paddy area in Sentinela do Sul, RS, Brazil. TABLEcommon 1 in open areas of southern Brazil and can be found ORGANIC CONVENTIONAL NATURAL FAMILY . List of tadpoleSPECIES species sampled from a rice paddy area in Sentinela do Sul, Rio Grande do Sul, Brazil, with total abundance by habitatTOTAL type. RICE FIELDS RICE FIELDS PONDS Bufonidae Rhinella dorbignyi 3 3

Hylidae Dendropsophus minutus (Duméril & Bibron, 1841) Hypsiboas pulchellus (Peters, 1872) 11 208 318 Pseudis minuta (Duméril & Bibron, 1841) Scinax squalirostris Günther,1858 2 194 196 Leptodactylidae Leptodactylus gr. fuscus (A. Lutz, 1925) 30 32 62 Physalaemus biligonigerus(Schneider, 1799) 1 1 Physalaemus gracilis (Cope, 1861 “1860”) Physalaemus henselii (Boulenger, 1883) 2335 3523 Pseudopaludicola falcipes (Peters, 1872) 6 4 Odontophrynus americanus (Hensel, 1867) 81 181 OdontophrynidaeTotal (Duméril & Bibron, 1841) 22 40 145 207

1016 Moreira et al. | Amphibians in rice fields, southern Brazil

Attademo et al. number of tadpoles of species that deposit eggs in foam affects the structure of habitat in which amphibians forage nests inside subterranean constructed chambers (mode 2011).et Agricultural al. intensificationet al. 2010). also Leptodactylus fuscus e.g. mode 1 species group were grouped in a single taxon. Because andsensu reproduce (Peltzer 2006; Piatti 30).the Intadpoles this study, of individualsthe L. fuscus of genusgroup have very similar someMore protection generalized against reproductive desiccation modes (e.g., modes [ 11 and morphology, external traits are not helpful for species 30) are Haddad more favored and Prado in open (2005)] areas oror environments modes that confer with et al. 2007). Four species belonging environments are more likely to dry up and are, therefore, todiagnostic the fuscus purposes group are (Langone known forand the De study Sá 2005; area Prado (L. fuscus, and occupiedseasonal availability by species with of water, rapid such development as rice fields. and Temporary those that L.D’Heursel gracilis, 2006;L. latinasus, De Sá and L. mystacinus build foam nests, which allows the larvae to survive until et al. 2007). A more detailed examination of internal oral anatomy and chondrocranium would be; Borges-Martinsinstructive and the next rain/flood (Zina 2006). Indeed, we found a higher

Figure 3. Rhinella dorbignyi Hypsiboas pulchellus Leptodactylus latrans, (D) Pseudopaludicola falcipes Adult amphibiansElachistocleis found in a ricebicolor paddy area in SentinelaChthonerpeton do Sul, RS, indistinctum Brazil, throught. the rice cultivation cycle (2010–2011), during tadpole samplings. Family Bufonidae: (A) . Hylidae: (B) . Leptodactylidae: (C) . Microhylidae: (E) . Caeciliidae: (F) Table 2 RICHNESS ECOREGION. Number of amphibianLOCALITY species found by habitat type in five rice paddy areas in three different ecoregions of SouthREFERENCE America.*: not informed. RICE FIELD CHANNELS NEIGHBOR PONDS Southern Cone Corrientes, Argentina 10 10 7 (Duré et al. Mesopotamian savanna Uruguayan savanna 12 * 10 (Machado and 2008) Maltchik 2010) * et al. 2010) Mostardas, Brazil Uruguayan savanna * 10 * (Maltchik et al. 2011) Pantanal Miranda, Brazil 8 9 (Piatti Uruguayan savanna * 10 This work Mostardas, Brazil Sentinela do Sul, Brazil 9 1017 Moreira et al. | Amphibians in rice fields, southern Brazil help to identify these species. act synergistically with agrochemical effects on anuran The low tadpole abundance in our results were of the Uruguayan savanna ecoregion in the state of Rio habitats for many species that originally use natural Grandespecies do composition. Sul, few areas In of spite this ofecoregion the extensive are protected coverage by wetlandsunexpected (Machado since rice and fields Maltchik can be 2010). potential Although surrogate the conservation units. We hope that this work may stimulate presence of tadpoles might be a good indicator that rice others to present data on agricultural areas and encourage crops are effectively used for breeding activity, this must discussion of conservation practices outside conservation be heeded cautiously. Tadpoles might have originally areas.

Author’s Contribution Statement: LFBM carried out the design of study and performed the data collection, and drafting of the manuscript. foroccurred explosive in other breeding flooded species areas and(Rhinella then ended dorbignyi up in andthe Odontophrynusrice fields via irrigation americanus water.), becauseThis scenario a large seems number be true of manuscript. LM helped in several aspects along this work, as well as acting tadpoles would have been expected after a breeding event. DSK participated in the tadpole identification and drafting of the

in the coordination. All Weauthors are readthankful and approved to all privatethe final ownersmanuscript. that tools for better determining breeding sites. We were not Acknowledgments: Information about amplectant pairs and eggs are useful the exception of two Pseudopaludicola falcipes amplectant Mouraauthorized and twothe anonymoususe of their refereesrice fields for for improvements our research. on We the also manuscript. thank D. unable to confirm breeding activity in rice quadrats, with Araujo for field and laboratory assistance. We are grateful to E. Toriani- Hoplias sp. We thank Sistema de Autorização e Informação em Biodiversidade andpairs Oligosarchus and some floating foam nests. Moreover, we observed (SISBIO) for the collecting permit. This research was supported by funds fish species that generally prey upon tadpoles ( from UNISINOS (02.00.023/00-0), Fundação de Amparo a Pesquisa no Rio Grande do Sul—FAPERGS (11/1149-7), and Conselho Nacional de sp.) inside rice quadrats and irrigation addition to the predation effect on tadpoles and adults, the LiteratureDesenvolvimento cited Científico e Tecnológico-CNPq (52370695.2). channels of fields under both cultivation methods. In amphibians (Werner et al. et al. Acta presence of fish influences breeding site selection by many Amezaga,Oecologica J.M., L. Santamaría and A.J. Green. 2002. Biotic wetland connectivity: supporting a new approach for wetland policy. additive or synergistic effects 2007; Bothof pesticide 2009). use These and 23: 213–222. fish species were also found in natural ponds. However, Andrade, G.V., P.C. Eterovick, D.C. Rossa-Feres and L. Schiesari. 2007. (org.).Estudos Herpetologia sobre girinos no Brasil no Brasil: II Histórico, conhecimento atual e demonstrated in amphibians (Mann et al. deperspectivas; Herpetologia. pp. 127–145, in L.B. Nascimento and M.E. Oliveira habitat homogenization on tadpole predation have been . Belo Horizonte: Sociedade Brasileira (residents or not) could explain species absence 2009). during Thus, C. Junges and A. Basso. 2011. B-esterase activities and blood cell Attademo,morphology A.M., M.in Cabagna-Zenklusen, the frog R.C. Lajmanovich , P.M. Peltzer, thefish late predation growing associated period. with low tadpole abundance Leptodactylus chaquensis (Argentina). Ecotoxicology (Amphibia: both off-season and growing periods, may be associated Leptodactylidae) on rice agroecosystems from Santa Fe Province Presence of hylid tadpoles in organic rice fields, in 20:274–282 (doi: 10.1007/s10646-010- with the presence of a strip of vegetation close to the rice 0579-8). plots. Although the goal of our study was not to compare Borges-Martins,Moura (ed.). M.,Biodiversidade: P. Colombo, Regiões C. Zank, da F.G. Lagoa Becker do andCasamento M.T.Q. Melo.e dos cultivation methods, studies indicate that the effect of Butiazais2007. Anfíbios; de Tapes, pp. Planície 276–291, Costeira in F.G. do Becker, Rio Grande R.A. Ramosdo Sul and L.A. Ministério do Meio Ambiente. organic farming might be biased by the study of species . Brasília: in different or multiple guilds (Fuller et al. and temporal descriptors for neotropical tadpole communities in et al. Both, C., M. Solé, T.G.Hydrobiologia Santos and S.Z. Cechin. 2009. The role of spatial 2005; Hole southern Brazil. 624: 125–138 (doi: 10.1007/s10750- and drainage 2005; Moreira canals, andand Maltchikthere were 2014). ephemeral During poolsthe off- in tadpole008-9685-5). richness and guild composition in ponds in subtropical season, the organic fields retained water in the irrigation Both,grasslands? C., S.Z. Cechin,Austral A.S.Ecology Melo, S.M. Hartz. 2011. What controls which were drained and sometimes used for cattle 36: 530–536 (doi: 10.1111/j.1442- the rice plots. This was not true for conventional fields 9993.2010.02183.x). predicts tadpole guild composition in grasslands (Santos Cordeiro, J.L.P. and H. Hasenack.Campos 2009. sulinos: Cobertura conservação vegetal e uso atual sustentável do Rio grazing. It has been suggested that degree of permanence daGrande biodiversidade. do Sul; pp. 285–299, in V.D. Pillar, S.C. Müller, Z.M.S. Castilhos et al. et al. and A.V.A. Jacques (ed.). a review. Waterbirds Brasília: Ministério do Meio Ambiente. 2007; Bothi.e. 2011). In this case, presence of hylid Czech, H.A. and K.C. Parsons. 2002. Agricultural wetlands and waterbirds: tadpoles in organic fields might simply be related to earlier Leptodactylus notoaktites 25: 56–65.. South American Journal of Herpetology not exclude other effects of organic management, such as De Sá, R.O., J.A. Langone and M.V. Segalla. 2007. The tadpole of flood dates ( , longer flood period). However, this does Conservation and maintenance of a heterogeneous landscape around Biology2(1): 69–75. no or little use of chemical pesticides/inorganic fertilizers Donald, P.F. 2004. Biodiversity impacts of some agricultural. crop edges, of contributing to abundance in nearby areas. Vertebrate 18(1): biodiversity 17–37. on Australian rice farms Doody, J.S., W. Osborne, D. Bourne, B. Rennie and R.A. Sims. 2006. in anuran surveys and species inventories that focus on . Kingston ACT: Rural Tadpole identification difficulty is a major obstacle Industries Research and Development Corporation. Interciencia larval forms (Rossa-Feres and Nomura 2006), even though Duré, M.I., A.I. Kehr, E.F. Schaefer and F. Marangoni. 2008. Diversity of tadpoles are easier to encounter and collect than adults. amphibians in rice fields from northeastern Argentina. Joys,33(7): F. 523–527.Mathews, R.C. Stuart, M.C. 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15: 3499–3513 (doi: 10.1007/s10531- August 2014 004-2940-9). Received: October 2013 Peltzer,eutrophication P.M., R.C. Lajmanovich, on survival J.C.and Sánchez-Hernandez health status of , Scinax M.C. Cabagna, nasicus Accepted: Camila C. Both A.M Attademo and A. Basso. 2008. Effects of agricultural pond Published online: October 2014 Editorial responsibility:

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