Agroforestry systems as habitat for herpetofauna: is there supporting evidence?

Camila P.Palacios, Beln Agero & Javier A.Simonetti

Agroforestry Systems An International Journal incorporating Agroforestry Forum ISSN 0167-4366 Agroforest Syst DOI 10.1007/s10457-012-9571-z

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Agroforest Syst DOI 10.1007/s10457-012-9571-z

Agroforestry systems as habitat for herpetofauna: is there supporting evidence?

ero Camila P. Palacios Belen Agu Javier A. Simonetti

Received: 12 September 2011 / Accepted: 14 September 2012 Springer Science+Business Media Dordrecht 2012

Abstract The need to carry out biological conservation outside protected areas requires avoiding, minimizing or mitigating impacts brought about by habitat transformation upon the biota. Usually, forest plantations hold fewer species than the original forest. However, structurally complex plantations support more species and individuals than simpler ones. Here we test if this phenomenon occurs in amphibian and reptilian assemblages, analyzing information regarding their richness and abundance in forestry plantations from 14 countries and 72 case studies which compare species richness and abundance in plantations and forests. Among amphibians, species richness is lower in plantations than in forests while among reptiles there is no signicant difference. The abundance of reptiles increases in plantations. Three studies dealt with reptile assemblages in relation to structural complexity of plantation, which suggest that species richness and abundance is higher in complex plantations. Despite accounting for 50 % of the terrestrial vertebrates, herpetological studies account for 15 % of the research available regarding the impact of plantation upon vertebrates, information deciency that hampers decision-making on the conservation of herpetozoans outside protected areas.

Keywords Amphibians Meta-analysis Reptiles Plantations Structural complexity Understory

Introduction Human activities have transformed landscape structure and functioning across the terrestrial biosphere. Currently, lands allocated to urban developments and agricultural account for 39 % of the ice-free areas of the planet (Ellis et al. 2010). Anthropogenic landscape changes brought about the expansion of agriculture poses a signicant treat to biodiversity survival (Tilman 1999; Sala et al. 2000). Nearly, 70 % out of 10,707 threatened terrestrial animal species are endangered by landscape transformations associated to agricultural and forestry-related activities (IUCN 2010). Agricultural and forestry systems are expected to expand to satisfy growing demands of food and forestry products, becoming a dominant landscape component, increasing its pressure upon natural habitats and its biota (Tilman et al. 2002). The need to reduce their impact upon biological diversity is therefore a pressing need (Norris 2008). Increasing evidence suggests that the detrimental impact of forestry activities upon biodiversity could be reduced or mitigated pending on management (Hartley 2002). On a world-wide basis, species richness and abundance of birds and mammal is lower in forestry

C. P. Palacios B. Aguero J. A. Simonetti (&) Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile, PO Box 653, Santiago, Chile e-mail: jsimonet@uchile.cl

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plantations than native forests. However, structurally complex plantations support higher richness and abundance than structurally simpler ones, enabling their incorporation into biodiversity conservation (Najera and Simonetti 2010a; Ramrez and Simonetti 2011). If a general phenomenon, to increase structural complexity might be a cost-effective management option to reduce direct impacts upon biodiversity, enhancing the possibility that agricultural and forestry areas are managed in order to ensure the conservation of biological diversity, as expected in the Aichi Biodiversity Targets of the Convention on Biological Diversity (CBD Convention on Biological Diversity 2010). Richness and abundance of amphibians and reptiles are altered in human-modied landscapes, embracing a variety of habitat changes from selective logging, secondary forests to agricultural elds and open areas (Gardner et al. 2007; Sodhi et al. 2010). Habitat structural changes are a presumed leading cause of species decline, as herpetozoans add up to 48 % of terrestrial animal species which are threatened by agroforestry and forestry activities (Gardner et al. 2007; IUCN 2010). Here, we focus in the response of the herpetofauna to agroforestry and forestry plantations, assessing if there is supporting evidence that these plantations could support amphibians and reptile biodiversity as occurs with birds and mammals.

Methods Information of herpetozoans in agricultural and forestry plantations was gathered through a review of the ISI Web of Knowledge, EBSCO, Scielo and Scholar Google databases for articles published between 1986 and 2012 dealing with amphibians and reptiles diversity and abundance in forestry and agroforestry plantations, using the search terms amphibian* ? plantation*, reptile* ? plantation*, reptile* ? planted forest* and reptile* ? agroforestry*. Additionally, we searched for the same taxa adding specic type of plantations such as oil palm, pine, eucalyptus, and cacao. Relevant publications cited in the retrieved works were also included when they were not captured in the databases. Articles were collated into those who compared richness and/or abundance between forests and plantations and those who compared plantations with different structural complexity. Plantations

exhibiting a single species canopy cover or those with scarce or nil understory cover were regarded as simple. Plantations with multiple vegetation strata, multiple species canopy cover or dense undergrowth were regarded as structurally complex (Najera and Simonetti 2010a). Each comparison was considered an independent case; articles might comprise more than one comparison. From each case we extracted information regarding the type of plantation, species richness (assessed either as mean species numbers per sampling unit or the total number of species) and abundance (expressed either as the mean number of individuals across all species per sampling unit or the total number of individuals). Changes in richness and abundance were statistically tested through sign tests, comparing the frequency of cases where the number of species or individuals in a plantation increased or decreased compared to the native forest. Other test, like log response ratio tried to be used but incomplete data reporting in several publications precluded the analysis of the effect sizes. Similarly, changes in richness and abundance in complex plantations compared to simple ones were also tested through sign tests (Borenstein et al. 2009). Power of the sign test was determined after Zar (1996) as the binomial distribution of the observed proportions compared to a hypothesized proportion of 0.5 at a signicant level of a and the available sample size. Similarity in species composition between forests and plantations was estimated through the Jaccard coefcient (Krebs 1989). Conservation status of amphibians and reptiles included in comparisons was obtained from IUCN (2010).

Results Regarding forest-plantation comparisons, a total of 27 scientic publications fullled search criteria, providing 72 case studies, 37 dealing with amphibians and 35 for reptiles (Table 1, Appendix 1). Amphibians are mostly studied in cocoa, eucalyptus, pine and coffee plantations, accounting for 70 % the case studies, while reptiles are most commonly studied in cocoa, pine and coffee plantations, accounting for 63 % the total number of comparisons (Table 1). Studies were carried out in 14 countries, largely located in tropical environments of Latin America and the Caribbean.

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Agroforest Syst Table 1 Number of publications and case studies per plantation type used for analyses of herpetozoan richness and abundance in forest and plantations Plantation Publications Case studies Amphibians Allspice Brush box Cardamom Coffee Eucalyptus Cocoa Oil palm Pine Rubber Mixeda Othersb Total
a

Table 3 Abundance response of IUCN-listed amphibian species to habitat change into plantations Threat level Data Decient Least Concern Near Threatened Vulnerable Endangered and Critically Endangered Increases 4 63 2 5 0 Decreases 13 122 10 8 12 p 0.05 (0.001 0.04 0.58 (0.001

Reptiles 2 1 5 4 12 5 2 4 35

1 1 1 6 3 6 1 6 1 2 1 27

2 1 1 5 5 12 2 4 1 2 2 37

Table 4 Abundance response of IUCN-listed reptile species to habitat change into plantations Threat level Data Decient Least Concern
a

Increases NI 11
a

Decreases NI 8
a

0.65

No species in our study is listed in this IUCN category

One plantation is comprised by cocoa, coconut, cashew nut, rice paddies, the other by cocoa, banana and nuts Wood plantation

Table 2 Species richness and abundance as a response after forest conversion to agroforestry and forestry plantations Increases Species richness Amphibians Reptiles Abundance Amphibians Reptiles 14 21 13 5 1 0.003 6 15 25 13 \0.001 0.85 Decreases p

Herpetofauna in plantations have been studied largely in Brasil, Mexico, Nicaragua, Costa Rica and Grenada (52 % of publications and 59 % of cases). Amphibians and reptiles responded differently to the transformation of forests into plantations. Species richness of amphibians was signicantly lower in plantations than in forests, holding fewer species in 68 % of the cases (Table 2). While the number of reptiles species in plantations was higher in 43 % of cases, difference was not signicant, although this might be due to low statistical power (Power = 0.57; Table 2). Total abundance of amphibians does not signicantly increase in plantations (Power = 0.70; Table 2). The abundance of reptiles increases

signicantly in plantations, plantations supporting more individuals in 81 % of cases (Table 2). In forest-plantation comparisons, species richness of reptiles and amphibians did not change in seven and ve cases, respectively. Despite holding the same number of species, assemblages in plantations comprise a partially different group of species than the original suite of species in the forest. In fact, similarity in species composition between cases in which species richness does not change compared to those in which it does, does not signicantly differ neither among amphibians nor reptiles (Jaccard coefcient 0.59 0.08 vs. 0.39 0.03; U = 29.5, p = 0.08 for amphibians, and 0.60 0.11 vs. 0.39 0.05; U = 42.5, p = 0.08 for reptiles). That is, plantations are holding compositionally modied species assemblages. The presence of threatened amphibian species also decreases in plantations compared to forests (Table 3). Species listed in all categories but Vulnerable exhibited lower abundance in plantations than in forests. Sample size for Vulnerable species is low enough to have statistical power (Power C 0.27), hence the lack of difference ought to be cautiously considered. Further, Critically Endangered and Endangered species were lumped due to low sample size of the rst ones (n = 2; Table 3). Only Least Concern reptile species are covered in the studies reviewed, whose numbers do not signicantly vary across plantations and forests (Power = 0.36, Table 4).

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Three publications compared assemblages of herpetozoans in plantations with different structural complexity, all dealing with reptiles, and just one provides tabulated data. In this single study, carried out in coffee plantations, species richness is 1.7 times higher in complex ones. Similarly, overall abundance is 1.8 times higher in complex plantations than in structurally simple ones, where eight out of 12 species increase its abundance or is present only in complex ones (see Macip-Ros and Munoz-Alonso 2008a).

Discussion Habitat loss is the most signicant environmental driver threatening biodiversity (Sala et al. 2000). Conversion of forests into agro-forestry plantations reduces vertebrate species richness, including herpetozoans (Donald 2004; Gardner et al. 2007). On a world-wide basis (14 countries) and a wide array of commodities (ten mono-specic plantations and two mixed ones), in most cases, plantations harbor a depauperated suite of species. Particularly, threatened species are indeed scarce in plantations. These facts suggest that species thriving in plantations are a modied subset of species, usually of low conservation concern, possibly generalist ones, as occurs in birds as well (e.g. Faria et al. 2007a; Macip-Ros and Munoz-Alonso 2008a for reptiles, Harvey and Gon zalez-Villalobos 2007 for birds). However, as occurs in mammals and birds, despite plantations support an impoverished subset of species, they are no biological desert, as several species thrive in these human-dominated habitats (Hartley 2002). In some cases, richness and abundance might even be higher than the original forest (Najera and Simonetti 2010a; Ramrez and Simonetti 2011). Unraveling the variables that impinge upon vertebrate assemblages in plantations can help to manage them for species conservation in plantations. In fact, at the assemblage level reptile abundance might even be higher in plantations, suggesting that for some species at least, plantationsparticularly their edgesmight be expanding thermally suitable habitat increasing overall abundance (e.g. Gardner et al. 2007; Rubio and Simonetti 2011). Amphibian richness and abundance though might be reduced in silvicultural edges unless structural elements such as understory cover are retained or enhanced in plantations borders

(de Maynadier and Hunter 1998). Interestingly, this habitat component foster the presence of mammals and birds in plantations (Najera and Simonetti 2010a, b; Ramrez and Simonetti 2011). If herpetozoans were responding also to this structural feature as well, a common management recommendation could have been advanced for all terrestrial vertebrates. Harnessing agro-forestry and forestry plantations for biodiversity conservation is an increasing need (Norris 2008). Protected areas, albeit necessary, might not sufce to conserve herpetozoans as several species are not represented in parks or reserves, among other factors (e.g. Young et al. 2004). Paradoxically then, a suite of species survive in human-dominated landscapes such as plantations, a habitat type that threatens them. Unfortunately, information regarding the potential role of structural complexity in mitigating the impact of habitat transformation upon herpetozoans is virtually non-existing. Just three studies focusing in reptiles suggest increased habitat heterogeneity might reduce biodiversity decline in forestry plantations (Macip-Ros and Munoz-Alonso 2008; Wanger et al. 2009, 2010) but no one deals with amphibians, paucity that prevents informing managerial practices for these taxa. Despite terrestrial herpetozoans comprise half the living vertebrate species, they are clearly understudied compared with mammals and birds regarding their response to habitat change into forestry plantations. Up to day, 146 articles refer to changes in terrestrial vertebrates in agro-forestry plantations (this survey and data from Najera and Simonetti 2010a; Ramrez and Simonetti 2011). Only 19 % of these (27 out of 146) of publications refers to amphibians and reptiles, compared with the remaining 81 % addressing the response of mammals and birds (see Najera and Simonetti 2010a; Ramrez and Simonetti 2011). Bias against herpetozoans is frequent not only in conservation but even in taxonomic and systematic studies, where studies focusing on threatened species and description rate of new species lags behind taxonomic work devoted to birds and mammals (Simonetti 2001; Brito 2008). Manipulative experimental approaches are urgently required for properly test the causal relationship between habitat characteristics and the attributes of assemblages in plantations (Wanger et al. 2009; Najera and Simonetti 2010b). Currently, the few studies comparing the response of herpetozoans to structural complexity on plantations analyze changes

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in species diversity and abundance along altitudinal gradients (Macip-Ros and Munoz-Alonso 2008; Wanger et al. 2010), precluding the assessment of changes in habitat itself but also the potential inuence of synergistic factors such as microclimate, increased UVB exposure and concomitant increased susceptibility to diseases (Gardner 2001). That is, despite growing information suggesting that forestry plantations could contribute to biological conservation (Hartley 2002), information deciency regarding amphibians and reptiles hampers decision-making for their conservation outside protected areas.
Acknowledgments This wok has been supported by Fondecyt 1095046 and Programa Domeyko-Biodiversidad (Iniciativa Transversal 3), Universidad de Chile.

Appendix 1 Publications used in the analysis Amo L, Lopez P, Martn J (2007) Natural oak forest vs. ancient pine plantations: lizard microhabitat use may explain the effects of ancient reforestations on distribution and conservation of Iberian lizards. Biodivers Conserv 16:34093422. Camurugi F, Lima TM, Merces EA and Junca FA (2010) Anurans of the Reserva Ecologica da Michelin, Municipality of Igrapiuna, State of Bahia, Brazil. Biota Neotrop. 10(2): http://www.biotaneotropica.org.br/ v10n2/en/abstract?inventory?bn02810022010. Faria D, Paciencia MLB, Dixo M, Laps RR, Baumgarten J (2007) Ferns, frogs, lizards, birds and bats in forest fragments and shade cacao plantations in two contrasting landscapes in the Atlantic forest, Brazil. Biodivers Conserv 16:23352357. Gardner T A, Ribeiro-Junior MA, Barlow J, Avi1aPerez TCS, Hoogmoed MS, Peres CA (2007) The value of primary, secondary, and plantation forests for a neotropical herpetofauna. Conserv Biol 21:775787. Germano JM, Sander JM, Henderson RW, Powell R (2003) Herpetofaunal communities in Grenada: a comparison of altered sites, with an annotated checklist of Grenadian amphibians and reptiles. Caribb J Sci 39:6876. Gillespie G, Howard S, Lockie D, Scroggie M, Boeadi (2005) Herpetofaunal richness and community structure of offshore islands of Sulawesi, Indonesia. Biotropica 37:279290.

Gillespie GR, Ahmad E, Elahan B, Evans A, Ancrenaz M, Goossens B, Scroggie MP (2012) Conservation of amphibians in Borneo: relative value of secondary tropical forest and non-forest habitats. Biol Conserv 152:136144. Heinen J T (1992) Comparisons of the leaf-litter herpetofauna in abandoned cacao plantations and primary rain forest in Costa Rica: some implications for faunal restoration. Biotropica 24:431439. Kanowski JJ, Reis TM, Catterall CP, Piper SD (2006) Factors affecting the use of reforested sites by reptiles in cleared rainforest landscapes in tropical and subtropical Australia. Restor Ecol 14:6776. King DI, Hernandez-Mayorga MD, Trubey R, Raudales R, Rappole JH (2007) An evaluation of the contribution of cultivated allspice (Pimenta dioca) to vertebrate biodiversity conservation in Nicaragua. Biodivers Conserv 16:12991320. Krishna SN, Krishna SB, Vijayalaxmi KK (2005) Variation in anuran abundance along the streams western Ghats, India. Herpetolog J 15:167172. Lieberman S (1986) Ecology of the leaf-litter herpetofauna of a neotropical rain forest: La Selva, Costa Rica. Acta Zool Mexicana 15:172. Macip-Ros R, Munoz-Alonso A (2008) Diversidad de lagartijas en cafetales y bosque primario en el Soconusco Chiapaneco. Rev Mex Biodivers 79: 185195. Mitchell JC, Rinehart SC, Pagels JF, Buhlmann KA, Pague CA (1997) Factors inuencing amphibian and small mammal assemblages in central Appalachian forests. For Ecol Manage 96:6576. Mott B, Alford RA, Schwarzkopf L (2010) Tropical reptiles in pine forests: assemblage responses to plantations and plantation management by burning. For Ecol Manage 259:916925. Parris KM, Lindenmayer DB (2004) Evidence that creation of a Pinus radiata plantation in south-eastern Australia has reduced habitat for frogs. Acta Oecol 25:93101. Pineda E, Halffter G (2004) Species diversity and habitat fragmentation: frogs in a tropical montane landscape in Mexico. Biol Conserv 117:499508. Pineda E, Moreno C, Escobar F, Halffter G (2005) Frogs, bat and dung beetle diversity in the cloud forest and coffe agroecosystems of Veracruz, Mexico. Conserv Biol 19:400410. Ribeiro-Junior MA, Gardner TA, Avi1a-Perez TCS (2008) Evaluating the effectiveness of herpetofaunal

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sampling techniques across a gradient of habitat change in a tropical forest landscape. J Herpetol 42:733749. Ryan T. J., T. Philippi, Y. A. Leiden, M. E. Dorcas, T. B. Wigley, J. W. Gibbons (2002) Monitoring herpetofauna in a managed forest landscape: effects of habitat types and census techniques. For Ecol Manage 167:8390. Santos-Barrera G, Pacheco J, Mendoza-Quijano F, Bolanos F, Chaves G, Daily GC, Ehrlich PR, Ceballos G (2008) Diversity, natural history and conservation of amphibians and reptiles from the San Vito Region, southwestern Costa Rica. Rev Biol Trop 56:755778. Santos-Barrera G, Urbina-Cardona JN (2011) The role of the matrix-edge dynamics of amphibian conservation in tropical montane fragmented landscapes. Rev Mex Biodivers 82:679687. Sung Y, Karraker NE, Hau BCH (2012) Terrestrial herpetofaunal assemblages in secondary forests and exotic lophostemon confertus plantations in south China. For Ecol Manage 270:7177. Vallan D (2002) Effects of anthropogenic environmental changes on amphibian diversity in the rain forest of eastern Madagascar. J Trop Ecol 18:725742. Vonesh JR (2001) Patterns of richness and abundance in a tropical african leaf-litter herpetofauna. Biotropica 33:502510. Wanger TC, Iskandar DT, Motzke I, Brook BW, Sodhi NS, Clough Y, Tscharntke T (2010) Effects of land-use change on community composition of tropical amphibians and reptiles in Sulawesi, Indonesia. Conserv Biol 24:795802. Whiteld SM, Bell KE, Philippi T, Sasa M, Bolanos F, Chaves G, Savage JM, Donnelly MA (2007) Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proc Natl Acad Sci USA 104:83528356.

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