ORIGINAL ARTICLE Thomas Puttker �� Yvonne Meyer-Lucht Simone Sommer Effects of fragmentation on parasite burden (nematodes) of generalist and specialist small mammal species in secondary forest fragments of the coastal Atlantic Forest, Brazil Received: 22 September 2006/ Accepted: 7 February 2007/ Published online: 17 March 2007 �� The Ecological Society of Japan 2007 Abstract Parasites are considered to play an important role in the regulation of wild animal populations. We investigated parasite burden of gastrointestinal nema- todes and body condition in specialist and generalist small mammal species in secondary forest fragments in the highly endangered coastal Atlantic Forest. We hypothesized that body condition decreases with increasing parasite load and that parasite burden in- creases with increasing fragmentation in specialist spe- cies but not in generalist species as a consequence of differing responses to fragmentation effects. Investigated species were Akodon montensis, Oligoryzomys nigripes, and Delomys sublineatus (rodents) and the marsupials Marmosops incanus and Gracilinanus microtarsus. Prev- alence of parasites was high in all species except for the arboreal G. microtarsus, presumably because of de- creased infection probability. No correlation was found between body condition and parasite load in any of the species. Contrary to our expectations, body condition of the specialists D. sublineatus and M. incanus increased in both species with increasing fragmentation. In D. sub- lineatus, parasite burden increased and body condition decreased in fragments with relatively high density probably due to increased contact rates and facilitation of infection with nematodes. In all generalist species, low or no correlation between parasite burden and frag- mentation was detected, suggesting little effect of frag- mentation on population health. Keywords Fragmentation �� Gastrointestinal nematodes �� Coastal Atlantic Forest �� Rodents �� Marsupials Introduction Parasites play an important role in natural communities, and various studies have indicated that they are able to control host populations in size and demography simi- larly to the impact of predators or limitation of re- sources (Anderson and May 1979 Gregory 1991 Murray et al. 1997 Poulin 1999 Hugot et al. 2001 Nunn et al. 2003). For example, studies have indicated that parasitism may lead to reduced reproduction (Murray et al. 1997 Murray et al. 1998), altered host morphology (Kristan 2002), altered mating behavior (Ehman and Scott 2002 Kavaliers et al. 2005), altered physiology (Kristan and Hammond 2000, 2001), and increased predation risk (Murray et al. 1997 Haukisalmi and Henttonen 2000). For these reasons, the nutritional status of the host is an important factor regarding the impact of parasitism. Malnourished host individuals with degraded condition and immunological competence are less able to defend against parasite infections (May and Anderson 1979 Poulin 1996 Koski and Scott 2001). Additionally par- asites may pose substantial energetic demands on the host and may further reduce host condition (Yuill 1987 Coop and Holmes 1996 Delahay et al. 1998 Gillespie and Chapman 2006). In addition to interactions with parasite infections and food supply, the conditional status of an animal might also be influenced by intra- specific and interspecific competition (Guyer 1988 Lin and Batzli 2001 D��az and Alonso 2003), which is a function of the density of host populations. High den- sities facilitate stress induced by competition (May and Anderson 1979) and increase interspecific contact rates, which in turn improve transmission circumstances for directly transmitted parasites. T. Puttker �� Y. Meyer-Lucht �� S. Sommer Animal Ecology and Conservation, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany Present address: T. Puttker �� Y. Meyer-Lucht �� S. Sommer (&) Leibniz Institute for Zoo- and Wildlife Research (IZW), Alfred-Kowalke-Str. 17, 10315 Berlin, Germany E-mail: sommer@izw-berlin.de Tel.: +49-30-5168315 Fax: +49-30-5126104 Ecol Res (2008) 23: 207���215 DOI 10.1007/s11284-007-0366-z

Few studies have been conducted on the effects of anthropogenic habitat disturbance on parasite burden within host species populations (Gillespie et al. 2005). Tests of theoretical expectations are di���cult due to many confounding parameters. Fragmentation and the associated change in habitat quality (e.g., increased edge effects) may have an influence on the conditional status of species (D��az et al. 1999), advantaging parasite infections by a depressed immune system. Isolation of host populations by increasing fragmentation of suitable habitat makes colonization di���cult for vector-driven pathogens or parasites. On the other hand, infections can have a severe impact on the isolated host population (e.g., Macdonald 1996 Allan et al. 2003). The coastal Atlantic Forest (Mata Atlantica) in Brazil is one of the most diverse and most threatened biomes in the world (Myers et al. 2000). Due to severe human impact over the last few centuries most of the primary coastal Atlantic Forest has been destroyed. Only 8% of its original extent remains, and the remaining forest is highly fragmented (Terborgh 1992 Galindo-Leal and de Gusmao Camara 2003 Tabarelli et al. 2005). The Mata Atlantica harbors a large number of endemic species (Ayres et al. 2005). Among the 92 species of small mammals known to inhabit the Mata Atlantica, 43 are restricted to only this biome (Fonseca et al. 1996). Small mammals in particular play a key role in forest ecosystems in terms of seed dispersal (Forget 1991 Sanchez-Cordero and Mart��nez-Gallardo 1998 Brewer and Reimanek 1999 Vieira and Izar 1999 Vieira et al. 2003 Pimentel and Tabarelli 2004) and the dis- persal of mycorrhizal fungi (Janos and Sahley 1995). Furthermore, they affect the forest���s regeneration by predation on seedlings (Forget 1993 Pizo 1997 Forget et al. 2000 Vieira et al. 2003). This study forms a part of a larger project investi- gating the small mammal community (Pardini et al. 2005 Umetsu and Pardini 2007). Umetsu and Pardini (2007) found that the rodents Akodon montensis (Tho- mas 1902), Oligoryzomys nigripes (Olfers 1818), and Delomys sublineatus (Thomas 1903) as well as the mar- supials Marmosops incanus (Lund 1840) and Gracilin- anus microtarsus (Wagner 1842) differed in their response to habitat fragmentation. D. sublineatus and M. incanus were specialized according to the use of habitat compared to the other species and were captured only in native vegetation. Furthermore, the density of D. sublineatus decreased with increasing fragmentation effects and both D. sublineatus and M. incanus were captured mostly in locations providing mature forest vegetation structure (T. Puttker et al. 2006, unpublished data). On the other hand, A. montensis, O. nigripes, and G. microtarsus were habitat generalists. They were captured in native forests but also in anthropogenically altered habitats such as eucalyptus plantations (Umetsu and Pardini 2007). Density of A. montensis and O. nigr- ipes did not correlate with fragmentation effects (T. Puttker et al. 2006, unpublished data), and abun- dance of G. microtarsus did not differ between large connected and small isolated forest fragments (Pardini et al. 2005). Based on these results, we addressed in the present study whether fragmentation has a different impact on parasite load as well as body condition of these gener- alist and specialist small mammal species in secondary forest fragments. We focused on gastrointestinal nema- todes, one of the most important and prevalent groups of parasites (Hugot et al. 2001), which are a major cause of disease and death in humans, domestic animals, and wildlife (Stear et al. 1997). Since laboratory studies have shown that malnutrition of rodents leads to increased parasite survival (Bolin et al. 1977 Gbakima 1993 Koski and Scott 2001 and references therein), we ex- pected to find a similar pattern between nutrition, esti- mated via body condition, and parasite burden in the field and hypothesized that body condition of species decreases with increasing parasite load. Thereby, the consequences of fragmentation might differ between generalist and specialist species. Specialist species that suffer from fragmentation effects might be faced with suboptimal circumstances, including resource availabil- ity (D��az et al. 1999) as well as increased environmental stress in smaller fragments (Marchand et al. 2003). The investigated fragments of the coastal Atlantic Forest differed in size, degree of isolation, relation of forest edge to area, and proportion of human altered area in the vicinity to the fragment. Therefore, we hypothesized that body condition decreases and parasite load con- currently increases with increasing fragmentation effects in the specialist species D. sublineatus and M. incanus. On the other hand, we assumed that condition and parasite load of generalists A. montensis, O. nigripes, and G. microtarsus are not or only marginally influenced by fragmentation. Furthermore, because higher host den- sities improve transmission circumstances for parasites (Haukisalmi et al. 1996 Bush et al. 2001), we examined the relation between parasite load and density of the different species as well as correlation between condition and density. Methods Investigated species Akodon montensis is a terrestrial, insectivore���omnivore rodent with a body mass of 19���57 g. Oligoryzomys nigripes lives on the ground as well as in trees and weighs about 9���40 g. It feeds on fruits and seeds. The biggest investigated rodent was the terrestrial D. sublineatus at 20���75 g [all information about locomotion habits, weights and feeding habits from Fonseca et al. (1996) and Emmons and Feer (1997)]. Feeding habits of D. sublineatus are so far unknown. All three species are nocturnal and belong to the family Muridae, subfamily Sigmodontinae (Musser and Carleton 1993). D. sub- lineatus is endemic to the Atlantic Forest (Fonseca et al. 1996 Bonvicino et al. 2002), whereas A. montensis and 208