Small Mammals and a Railway in the Atlantic Forest of Southern Brazil

Edge effects without habitat fragmentation? Small mammals and a railway in the Atlantic Forest of southern Brazil

R ICARDO A. S. CERBONCINI,JAMES J. ROPER and F ERNANDO C. PASSOS

Abstract Edge effects have been studied extensively in frag- et al., ). Edges between different habitats were once con- mented landscapes, often with conflicting findings. Edge ef- sidered beneficial for biodiversity (Leopold, ;Lay,)but fects may also be important in other situations, such as as studies focused on anthropogenic edges (Chasko & Gates, linear clearings (e.g. along roads, power lines or train ; Harris, ) their detrimental effects became apparent. tracks). We tested for responses of small mammals to a nar- Edges are abrupt transitions between habitats or ecosystems row (c.  m) linear clearing created by a railway in the lar- (Yahner, ;Riesetal.,) and their effects include any gest area of Atlantic Forest in southern Brazil. Only two changes that occur as a result of that transition (Murcia, environmental variables, light intensity and train noise, ). Abrupt transitions in vegetation at edges are usually as- were greatest at the edge and decreased with distance from sociated with similarly abrupt changes in climate, with conse- the edge. Temperature differed (greater extremes and more quent impacts on plants and animals (Chasko & Gates, ; variable) only at the edge itself. The few small mammal spe- Sork, ; Palik & Murphy, ;Matlack,; Oliveira et al., cies that were only rarely captured at the edge resulted in an ) as a result of changing resource distribution (Mills et al., apparent edge-effect with respect to species richness. The ;Berg&Pärt,;Ries&Sisk,) and biotic interac- abundance of small mammals, however, was independent tions (Berg & Pärt, ; Fagan et al., ). of distance from the railway. There was no correlation be- Diversity often increases near edges (especially in forest tween resource availability at the tracks and abundance of fragments) as a consequence of invasion by organisms from small mammals. Edge effects were minimal, which suggests areas adjacent to the edge, both the forest interior and the that narrow railways (in contrast with roads) in unfragmen- newly created open area causing the edge (Yahner, ; ted landscapes probably do not have a significant impact Laurance, ; Gascon et al., ; Pardini, ). (if any) on wildlife, as found elsewhere and especially in Conditions near edges are often similar to those of disturbed tropical forests. The use of railways instead of roads is a habitats (Chen et al., ; Cadenasso et al., ) and may potential strategy to minimize the effects of traversing therefore favour invasion by species typical of disturbances important habitats for commercial reasons. (Laurance, ; Pardini, ). Unique resources may be available near edges (Mills et al., ; Berg & Pärt, ; Keywords Atlantic Forest, Brazil, Didelphimorphia, frag- Ries & Sisk, ), also favouring invasion by species that mentation, linear clearing, microclimate, right of way, prefer those resources. Rodentia Edge effects are well known in the context of habitat loss and fragmentation (Yahner, ; Murcia, ; Ries et al., ). However, linear clearings for rights of way (e.g. power lines, roads, railways) also produce edges, often in Introduction otherwise well-preserved landscapes (Laurance et al., dge effects threaten biodiversity in many landscapes ). Studies of the effects of roads and highways on wild- Efragmented as a result of human activities (Harper life have shown that these edges affect the diversity of under- storey birds (Laurance, ) and small mammals   RICARDO A. S. CERBONCINI* (Corresponding author), JAMES J. ROPER† and (Goosem, ; Ruiz-Capillas et al., ). However, most FERNANDO C. PASSOS* Programa de Pós-Graduação em Ecologia e studies have addressed these effects where edges are exten- Conservação, Setor de Ciências Biológicas, Universidade Federal do Paraná, sive and obvious. More subtle settings, such as smaller roads Campus Centro Politécnico, 81531-970 Curitiba, Paraná, Brazil E-mail [email protected] and rights of way, remain understudied and may have unex- *Also at: Laboratório de Biodiversidade, Conservação e Ecologia de Animais pected effects as a result of inputs of new resources that Silvestres, Departamento de Zoologia, Setor de Ciências Biológicas, may, in turn, increase diversity (Carthew et al., ). For ex- Universidade Federal do Paraná, Curitiba, Paraná, Brazil ample, agricultural products may fall from trains while in †Also at: Programa de Pós-graduação em Ecologia de Ecossistemas, Universidade de Vila Velha, Vila Velha, Espírito Santo, Brazil transit, introducing plants or providing food for animals. Received  July . Revision requested  August . Anthropogenic edges in tropical forests are of particular Accepted  November . First published online  February . concern because of the contrast between the more constant

Oryx, 2016, 50(3), 460–467 © 2015 Fauna & Flora International doi:10.1017/S0030605314001070 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.22, on 29 Sep 2021 at 19:51:57, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605314001070 Edge effects without fragmentation? 461

forest interior and the variable temperatures and greater ex- Each group comprised four transects, one of which was at tremes of the adjacent open areas, which may be agricultural, the edge ( m), with c.  m between each transect (thus urban or rights of way for road, rail or power lines (Matlack, the last was c. m from the edge). This sampling design ; Pohlman et al., ; Laurance et al., ). As natural was based on the fact that edge effects usually penetrate up areas become increasingly fragmented, understanding the ef- to  m in fragments of tropical forest (Kapos, ; fects of fragmentation and edges is important for conser- Matlack, ; Stevens & Husband, ; Laurance et al., vation. An estimated % of the Atlantic Forest is ,  m ; Oliveira et al., ). Sampling points were estab- from an edge (Ribeiro et al., ). In the future, these lished at  m intervals along the  m transects. Sampling kinds of edges may be pervasive, and understanding their im- ( days,  nights) was carried out monthly during pact on wildlife will be important for appropriate manage- February–July ; storms prevented sampling in March. ment of biodiversity coexisting with small-scale edges. One Sherman trap (H.B. Sherman Traps, Tallahasse, Here we measured the response of small mammals to a USA) was placed at each sampling point. We alternated railway in an otherwise well-preserved natural landscape. six small ( ×  ×  mm) and four large ( ×  ×  This setting is useful because it minimizes the effects of mm) traps on and above the ground (.– m) on each tran- overdispersion of animals from an anthropogenic matrix sect. Captured animals were handled without anaesthesia, (i.e. farms, rural and urban areas). We tested three hypoth- and marked with a numbered ear tag. All individuals were eses: the railway creates an environmental gradient in the measured (head-and-body length) and weighed. Voucher forest (i.e. an edge effect exists), this edge has consequences specimens collected (licenses Instituto Ambiental do for the small mammals inhabiting the forest, and the new Paraná n°/ and Instituto Chico Mendes de resources introduced by trains hauling agricultural produce Conservação da Biodiversidade n°-) are in the mam- (usually soy and other grains) favour small mammals near mal collection of the Department of Zoology, Federal the edge. By elucidating the impact of this edge within a University of Paraná. Field procedures followed guidelines well-preserved forest we hope to separate edge effects of the American Society of Mammalogists (Sikes et al., from the larger scale of the surrounding matrix. ). Information on the species of small mammals captured is in Cerboncini et al. ().

Study site

We studied edge effects in Marumbi State Park (Parque Estadual Pico do Marumbi). The Park is in the central portion oftheCoastalMountainRange(SerradoMar)inthestateof Microclimate and environmental conditions Paraná, southern Brazil, and lies within the largest remnant of We measured air temperature (°C), relative humidity Atlantic Forest (Ribeiro et al., ; Fig. ). The climate is (%, thermo-hygrometer, Instrutemp ITHT-), light inten- humid year-round and without a marked dry season (mean sity (lux, Instrutemp ITLD-) and ambient noise (dB, annual rainfall c. , mm and mean annual temperature Instrutemp ITDEC-)atfiverandomlychosenpoints c. °C; Vanhoni & Mendonça, ). The study area is at on all transects once during each sampling period. Noise – m altitude; vegetation is evergreen (Veloso et al., was measured on each transect when a train passed by, ), with emergent trees .  m tall and canopy at – which occurred at – hour intervals, day and night. The m. The most common plant families are Bromeliaceae, mean of each variable (except noise from trains) on each tran- Myrtaceae, Rubiaceae, Melastomataceae and Fabaceae sect during each sampling period was used in analyses. (Silva, ; Kaehler et al., ). The Paranaguá–Curitiba rail- An additional  m transect perpendicular to the railway way, established in , passes through the Atlantic Forest of was used to measure a temperature gradient. For a fine-scale the Serra do Mar and connects the state capital, Curitiba, with assessment of the microclimate, air temperature was mea- the port of Paranaguá ( km). It is used for commercial sured along this transect using  Thermochron data loggers transportation of several products, such as grains (mainly (Maxim Integrated, San Jose, USA). Data loggers were soy, wheat and corn), fuel and paper, and also for tourism. placed at  m intervals for the first  m from the edge, In the study area the right of way is c.  mwide. and subsequently at  m intervals to  m and then  m intervals to  m. All data loggers recorded temperature  Methods simultaneously every hour for hours during each sampling period. Based on natural temperature divisions, we ca- Capture of small mammals tegorized the sampling periods as warm (February and April), mild (May and July), and cold (June), to compare We established four groups of transects parallel to the rail- how temperature varied with distance from the edge, con- way, with groups separated by $  m along the railway. trolling for seasonality.

FIG. 1 The study site, where the Paranaguá–Curitiba railway passes through Marumbi State Park, in the Atlantic Forest of southern Brazil. The rectangle on the inset shows the location of the main map in Paraná state. Data on distribution of Atlantic forest patches are from SOS Mata Atlântica & INPE ().

Resources and edges We tested for a correlation between small mammal abundance near the edge ( m) and number of grains collected, We estimated resource availability at the railway tracks by firstly using overall abundance of all species, and secondly collecting grains that had fallen from trains. We used focusing on granivorous species, following the dietary classi-   seven seed-collectors ( × cm) set in place on the first fication of Paglia et al. (). All statistical analyses were  day of each sampling period, at m intervals on both carried out with Rv... (R Development Core Team, sides of the track (three on one side, four on the other). ); vegan (Oksanen et al., ) was used for ANOSIM.  After days we counted the number of grains collected as For statistical significance we assumed a % error rate. our relative estimate of grain availability. We focused on comparing sampling periods rather than estimating grain abundance on the railway. Results     Edge and climate Air temperature (F, = . ,P= . ),     Data analysis relative humidity (F, = . ,P= . ) and environmental     noise intensity (F, = . ,P= . ) were independent of We tested for correlations between total number of captures,   distance from the edge. Light intensity (F, = . , abundance and number of species of small mammals, and    ,     r = . ,P . ) and train noise intensity (F, = . , distance from the edge. We also tested for relationships be-  r = .,P, .) decreased with increasing distance from tween distance from the edge and environmental variables, the edge (Fig. ). There was no temperature gradient using linear regression analysis. Species abundance estimates beginning at the edge during any season; only at the edge were categorized according to distance from the edge (for itself was temperature different from all other points. In the same sampling effort): ,  m, – m, – m, and general, higher maximum temperatures (but similar .  m. We calculated the Jaccard dissimilarity index be- minimum temperatures) and thus greater variability were tween all sampling transects and tested if species composition found at the edge (Fig. ). depended on these edge distance categories, using ANOSIM (analysis of similarity) with  permutations. To estimate body condition we used the residuals of a Small mammals We captured  small mammal species, linear regression of body weight against length (Schulte- four of which are granivorous (Table ). Total capture Hostedde et al., ). For species with .  individuals cap- (S = .,P=., transect median = .) and abundance tured on more than three transects within an interval of at (S = .,P=., transect median = ) were independent least  m from the edge we tested for a relationship between of distance from the edge, whereas the number of species condition, sex and distance from edge, using analysis of co- captured declined towards the forest interior (S = , −    ,  variance. To avoid pseudoreplication we included only the rs = . ,P= . , median for transects m from the first capture of any individual in the analysis. edge = , – m from the edge = , and .  m from the

FIG. 2 The relationship of distance from the Paranaguá–Curitiba railway to light intensity (unfilled circles) and train noise (filled circles) in the Atlantic Forest in southern Brazil (Fig. ). Axes are log scaled.

edge = ; Fig. ). The most common species were approximately equally abundant at various distances from the edge, whereas the most uncommon species were captured only near the edge (Fig. ). Species composition was similar at all distances from the edge (ANOSIM, R=.,P=.). Body condition of all animals was independent of sex, and therefore sex was not included in the analysis of body condition and distance from edge. Body condition was independent of distance from the edge in all species (P . .). FIG. 3 Variation in temperature with distance from the Paranaguá–Curitiba railway towards the interior of the Atlantic Forest in southern Brazil (Fig. ) during warm (February and Railway resources Soy (% of all grains), corn (%) and April), mild (May and July) and cold (June) seasons. wheat (%) that fell from passing trains were collected in our seed traps. The number of grains collected varied from  in February to  in May ( in April,  in June from the train tracks, yet there was only a marked variation and  in July). Grain was available near the tracks during in temperature at the edge itself. In the tropics and elsewhere  every period, and the number of grains collected seemed changes in microclimate can be detected up to m from   to represent true availability (few grains were seen on the the edge (Kapos, ; Matlack, ; Stevens & Husband,  tracks during February, whereas large numbers were seen ). However, microclimate responses to edges are stron- in May). The number of individuals of all mammal gest when small forest fragments are bordered by open areas  species captured at the edge was always independent of (Didham & Lawton, ). The magnitude of microclimatic the number of grains collected (all species: S = ., gradients as a result of edges usually depends on the size of  n=,P=.; granivorous species only: S = ., the clearing (Pohlman et al., ). Thus the absence of a n=,P=.). microclimate gradient may be attributable to the clearing along the Paranaguá–Curitiba railway being narrow and linear (Laurance et al., ) in a well-preserved, forested Discussion landscape. Edge effects on light intensity (Kapos, ; Matlack,    Microclimate and edge ; Young & Mitchell, ; Cadenasso et al., ) can influence plant survival, reproduction and seed germination Despite the clear and abrupt transition between the open (Boardman, ). This interaction often favours pioneer space and the forest, the edge had no apparent influence or invasive plants (Bazzaz, ; Kapos, ; Brothers & on microclimate. There was a marked gradient in both Spingarn, ) and can cause an increase in plant density light and noise, both of which diminished with distance (Willson & Crome, ; Camargo & Kapos, ) and

TABLE 1 The  small mammal species captured along the railway at Marumbi State Park, Paraná, Brazil (Fig. ), with number of captures, and type of diet.

Taxon No. of captures Diet* Didelphimorphia Big-eared opossum Didelphis aurita 7 Frugivorous/Omnivorous South-eastern four-eyed opossum Philander frenatus 18 Insectivorous/Omnivorous Tate’s woolly mouse opossum Marmosa paraguayana 54 Insectivorous/Omnivorous Brazilian gracile opossum Gracilinanus microtarsus 1 Insectivorous/Omnivorous Rodentia Cricetidae Lesser Wilfred’s mouse Juliomys pictipes 28 Frugivorous/Seed predator Montane grass mouse Akodon montensis 11 Insectivorous/Omnivorous Hocicudo Oxymycterus sp. 3 Insectivorous/Omnivorous Russet rice rat Euryoryzomys russatus 179 Frugivorous/Granivorous South American water rat Nectomys squamipes 3 Frugivorous/Omnivorous Rat-headed rice rat Sooretamys angouya 24 Frugivorous/Granivorous Black-footed pygmy rice rat Oligoryzomys nigripes 11 Frugivorous/Granivorous Echimyidae Ihering’s spiny rat Trinomys iheringi 1 Frugivorous/Granivorous

*Diet classification following Paglia et al. ()

pass every few hours and, although noise may be intensely loud (up to  dB) near the railway, infrequent passage probably minimizes any effects on small mammals. It is also possible that small mammals derive a benefit from the noise because it may perturb potential predators. If so, this effect was not at a scale that was detectable in this study. Thus, the effect of noise from trains is apparently in- significant at current rates of train traffic in the Park.

Small mammals did not respond to the edge

We found no clear influence of edge effects on the group of mammals studied, which were typical of well-preserved FIG. 4 The variation in number of species of small mammals Atlantic Forest (Cerboncini et al., ). Capture probability captured with distance from the Paranaguá–Curitiba railway in of the most common mammal in the study, the russet rice  the Atlantic Forest in southern Brazil (Fig. ). The higher rat Euryoryzomys russatus, was independent of all edge number of species near the edge is partly attributable to the characteristics. A few uncommon species were captured capture of one or few individuals of some species (Fig. ). only near the edge (Fig. ) but are not thought to be associated with edges or disturbances. Spiny rats Trinomys diversity (Harper et al., ). Here, however, if such edge spp. are typical in well-conserved coastal Atlantic Forest conditions existed their influence on small mammals (Vieira et al., ), and Ihering’s spiny rat Trinomys iher- (through their influence on vegetation) was not measurable. ingi was found in the Park at the limits of its distribution Anthropogenic noise can be detrimental to wildlife for a (Cerboncini et al., ). Similarly, the South American variety of reasons, such as increased stress causing abnormal water rat Nectomys squamipes is often found in forest feeding and reproductive behaviours and other conse- patches with riparian areas, regardless of the size or quality quences that can influence fitness (Marler & Sherman, of the fragment (Pires et al., ; Viveiros de Castro & ; Andersen et al., ; Awbrey & Bowles, ). We Fernandez, ). The Brazilian gracile mouse opossum suggest that noise along the railway track is sporadic and Gracilinanus microtarsus is a habitat generalist, as long as relatively rare compared to other edge situations, and prob- forest is available (Pardini et al., ), and therefore the ably causes little disturbance. The impact of noise near roads fact that this species was captured only near the edge does depends on noise intensity and the rate and duration of traf- not suggest an edge effect (i.e. changes in community near fic, and thus there is a greater impact on wildlife near larger edges), given the small number of captures. Anthropogenic, roads (Kaseloo, ). In Marumbi State Park trains usually permanent linear clearings such as train rights of way may

to rodents near edges is necessary to compare the impacts of various types of edges.

Railway resources

Increased availability of resources may be one of the main reasons for increased diversity near edges (McCollin, , Ries & Sisk, ; Ries et al., ). Food is often super- abundant as a result of grain falling from trains but abundance of this resource had no measurable impact on small mammals. Although the number of small mammal species captured was greater near the edge, this is probably not a typical edge effect but a consequence of minor changes in the forest near the edge.

Rights of way and wildlife conservation

In Brazil roads are used more often than railways for commercial transportation. However, railways appear to have less impact on wildlife than do roads and highways. The construction of roads is usually followed by uncontrolled immigration and logging, hunting, agriculture and land speculation, which are the main causes of the destruction of tropical forests (Young, ; Laurance et al., ; Fearnside, ). Increasing the use of railways for transport could be a useful conservation strategy, especially where it is necessary to transport agricultural or industrial products through important habitats. Environmental edge effects in this landscape were minimal, with no measurable consequences for small mammals, except for infrequent encounters with some species only at the edge. It is important to note that the Paranaguá– Curitiba railway is .  years old and some species may

FIG. 5 Variation in abundance of small mammal species with have had sufficient time to adapt to the different environ- distance from the Paranaguá–Curitiba railway in the Atlantic mental conditions created by the right of way. Whether forest in southern Brazil (Fig. ). newly constructed railways produce more intense edge effects remains to be investigated.

be unsuitable, and even dangerous, for wildlife but appear to Acknowledgements have little effect in the nearby forest. The lack of correlation between the body condition of We thank the following for their invaluable help in the field: small mammals and distance from the edge also suggest lit- Talita V. Braga, Marcelo B. G. Rubio, Itiberê P. Bernardi, tle or no edge effect. Body condition is important for sur- Jennifer de S. B. Pereira, Viviane Mottin, Bruna C. R. de vival and reproduction (Millar & Hickling, ; Virgl & Jesus, Luiz H. Varzinczak, Felipe L. S. Shibuya, Fernanda Messier, ; Zuercher et al., ; Schulte-Hostedde F. C. de Lima and Jaqueline P. Duarte. Our research was per- et al., ), and in female mammals is often associated mitted by Instituto Ambiental do Paraná and the Park with reproductive success (Atkinson & Ramsay, ; Manager Lothário H. Stoltz Jr, who also provided transpor- Dobson & Michener, ; Wauters & Dhondt, ). The tation and accommodation at the study site. Instituto Chico absence of an effect suggests there is no stress associated Mendes de Conservação da Natureza provided permits to with the edge or associated noises. In contrast, a study in capture and collect small mammals. Marcelo Passamani the Caribbean found the body condition of female rodents and Maurício O. Moura provided valuable suggestions for declined near roads (Fuentes-Montemayor et al., ). this article. A scholarship was granted to RASC by the Further study to determine which factors are detrimental Coordenação de Aperfeiçoamento de Pessoal de Nível

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Biographical sketches SCHULTE-HOSTEDDE, A.I., ZINNER, B., MILLAR, J.S. & HICKLING, G.J. () Restitution of mass–size residuals: validating body condition RICARDO CERBONCINI is interested in ecology, conservation and indices. Ecology, , –. evolution of biodiversity. His research focuses on the ecology of ro- SIKES, R.S., GANNON, W.L. & THE ANIMAL CARE AND USE dents and marsupials in human-altered landscapes, and on the evol- COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS ution of behavioural traits, especially breeding systems and parental () Guidelines of the American Society of Mammalogists for care of birds. JAMES ROPER is interested in a broad variety of ecological the use of wild mammals in research. Journal of Mammalogy, , and evolutionary questions, especially those related to population dy- –. namics. Most of his research includes analysis of reproductive success SILVA, F.C. () Composição florística e estrutura fitossociológica and survival of terrestrial vertebrates. FERNANDO PASSOS works in da floresta tropical ombrófila da encosta Atlântica no wildlife biology and conservation. His research includes small and município de Morretes (Paraná). Boletim de Pesquisa Florestal, large mammals, and he has developed most of his studies based on /, –. the bats and primates of the Atlantic Forest.