Habitat-Quality Effects on Metapopulation Dynamics in Greater White-Toothed Shrews, Crocidura Russula

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Habitat-Quality Effects on Metapopulation Dynamics in Greater White-Toothed Shrews, Crocidura Russula Ecology, 89(10), 2008, pp. 2777–2785 Ó 2008 by the Ecological Society of America HABITAT-QUALITY EFFECTS ON METAPOPULATION DYNAMICS IN GREATER WHITE-TOOTHED SHREWS, CROCIDURA RUSSULA 1 J. JAQUIE´RY, J. GUE´LAT,T.BROQUET,L.BERSET-BRA¨NDLI,E.PELLEGRINI,R.MORESI,A.H.HIRZEL, AND N. PERRIN Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland Abstract. The effects of patch size and isolation on metapopulation dynamics have received wide empirical support and theoretical formalization. By contrast, the effects of patch quality seem largely underinvestigated, partly due to technical difficulties in properly assessing quality. Here we combine habitat-quality modeling with four years of demographic monitoring in a metapopulation of greater white-toothed shrews (Crocidura russula)to investigate the role of patch quality on metapopulation processes. Together, local patch quality and connectivity significantly enhanced local population sizes and occupancy rates (R2 ¼ 14% and 19%, respectively). Accounting for the quality of patches connected to the focal one and acting as potential sources improved slightly the model explanatory power for local population sizes, pointing to significant source–sink dynamics. Local habitat quality, in interaction with connectivity, also increased colonization rate (R2 ¼ 28%), suggesting the ability of immigrants to target high-quality patches. Overall, patterns were best explained when assuming a mean dispersal distance of 800 m, a realistic value for the species under study. Our results thus provide evidence that patch quality, in interaction with connectivity, may affect major demographic processes. Key words: colonization; connectivity; Crocidura russula; ecological-niche factor analysis (ENFA); extinction; greater white-toothed shrew; habitat suitability; metapopulation dynamics; occupancy; Valle´ede Joux, Switzerland. INTRODUCTION given landscape depends on the ‘‘capacity’’ of the The concept of metapopulation refers to a set of local metapopulation, a function of the sizes and positions demes (or patches) connected by some level of migration of its patches. The size of a patch (considered as a and undergoing disequilibrium dynamics characterized surrogate for local carrying capacity) affects its extinc- by local extinctions and recolonizations (Hanski and tion rate and contribution to the migrant pool, while its Gaggiotti 2004). One of the earliest attempts to isolation matters by affecting connectivity (i.e., contri- formalize these dynamics was Levins’s (1969) patch- bution to recolonization). occupancy island model. Assuming that all local demes Patch quality has rarely been explicitly considered in are equivalent in terms of extinction probability and this context and might be seen as the main missing connectivity, this model predicts expected occupancy parameter in current metapopulation modeling (e.g., rate as a function of extinction and colonization rates. Thomas et al. 2001). Habitat quality is indeed bound to These first inroads prompted research on different affect all processes determining metapopulation dynam- fronts. On the empirical side, subsequent investigations ics. On the one hand, high-quality patches may benefit have shown that Levins’s simplifying assumptions of from lower extinction rates (by enhancing individual homogeneous rates are often not tenable. Local demes survival or fecundity) or higher colonization rates (by differ in extinction rate and connectivity, which affects attracting immigrants or facilitating settlement). On the metapopulation dynamics (e.g., Verboom et al. 1991, other hand, they may send more migrants (owing to Kindvall and Ahlen 1992, Hanski and Thomas 1994, higher productivity), and thereby contribute more than Eber and Brandl 1996). On the theoretical side, attempts others to recolonization processes. Patch quality might were made to integrate these heterogeneities into thus also provide an excellent surrogate for local metapopulation modeling (e.g., Hanski 1994, Hastings carrying capacity. Although some studies have con- and Harrison 1994). Hanski and Ovaskainen (2000, firmed a role for habitat quality in occupancy, coloni- 2003, see also Ovaskainen and Hanski 2001, 2004) zation, or extinction patterns (e.g., Thomas et al. 2001, contributed significantly to the theory of stochastic Fleishman et al. 2002, Franken and Hik 2004), these patch occupancy models by allowing patches to differ in topics remain largely underinvestigated, presumably due size and connectivity. The condition for viability in a to practical difficulties in assessing habitat quality. Recent developments in habitat-quality modeling are now tracing new inroads into this area. Habitat-quality Manuscript received 1 November 2007; accepted 31 January 2008. Corresponding Editor: F. S. Dobson. modeling is emerging as a discipline of its own, building 1 E-mail: [email protected] on a set of spatially explicit tools (geographic informa- 2777 2778 J. JAQUIE´RY ET AL. Ecology, Vol. 89, No. 10 tion systems) and associated statistics to identify tored in summer (August to September) in 106 sites, of environmental variables affecting a species’ distribution which 62 were studied in 2003 and 84 in each of the years and assess local habitat suitability (reviewed in Guisan 2004, 2005, and 2006 (Fig. 1). Sampling sites consisted and Zimmermann 2000). Up to now, applications to of 20 3 20 m areas within private gardens. These were metapopulation studies have been mostly restricted to always adjacent to human habitations and usually the delineation of local patches (e.g., Akc¸akaya et al. comprised some lawn, a vegetable garden, a compost 1995, Akc¸akaya and Atwood 1997, Akc¸akaya 2000a, b). heap, a garden dwarf, wood piles, stone walls, and Efforts were made by Moilanen and Hanski (1998) to hedges. Forty-two of these sites were sampled over all formally integrate habitat modeling into a metapopula- four years, 40 sites over three consecutive years, two tion dynamics framework, but the predictive power of sites over two consecutive years, and 22 sites only once. these models was not improved beyond the effects of Individuals were livetrapped using 20 Longworth small- patch area and isolation. mammal traps (B. N. Bolton, Inc, Vernon, British In the present paper, we combine spatially explicit Columbia, Canada) per garden, baited with Tenebrio modeling with a four-year demographic study to molitor larvae. After a pre-baiting period of two to four investigate the role of habitat quality on metapopulation days, each site was visited four times during two dynamics in a small mammal, the greater white-toothed consecutive days. The traps were opened daily around shrew (Crocidura russula). The species and study area (at 06:30 hours, checked at 10:00 and at 13:30 hours, and the altitudinal margin of its distribution) were chosen on then closed for the night. All caught individuals were several grounds. First, owing to strong dependence on individually marked by toe clipping and immediately human habitations, local populations are discrete, released. highly structured, and easily identified. Second, owing Local population size was estimated for each site as to harsh climatic conditions, local populations are small the mean number of individuals captured per year. A and prone to local extinctions induced by demographic site occupancy rate was defined as the proportion of or environmental stochasticity. Third, this species years in which at least one individual was captured. A displays high dispersal ability and short life span, which site’s colonization rate was estimated as the number of should combine with these features to induce high annual transitions from an empty to an occupied state, population turnover rates. Finally, its high trappability divided by the total number of transitions from an should facilitate mark and recapture studies. As empty state. Extinction rate was similarly estimated as metapopulation dynamics are poorly documented in the number of transitions from an occupied to an empty mammals, this study system had the potential to state, divided by the total number of transitions from an contribute significantly to the field. occupied state. METHODS Habitat quality and connectivity Field sampling Habitat quality (or suitability) was estimated using Crocidura russula is a small insectivorous mammal the ecological-niche factor analysis (ENFA; Biomapper widespread in southwestern Europe. The life cycle is 3.2; Hirzel et al. 2002, 2004) with the median algorithm mostly annual (Jeanmaire-Besanc¸on 1988) and the (Hirzel and Arlettaz 2003) at a 25-m cell resolution. This mating system mostly monogamous (Cantoni and Vogel multivariate analysis extracts a series of independent 1989, Bouteiller and Perrin 2000). Breeding pairs defend factors (linear combinations of environmental variables) territories where they may rear several litters from that maximize the marginality and specialization of a March to September (Jeanmaire-Besanc¸on 1988). In the focal species, relative to the reference area. Marginality northern part of the species range (including the study measures how much environmental conditions in area), individuals are preferentially anthropophilic presence sites depart from average, and specialization below 600 m and strictly so at higher altitudes (Genoud measures the narrowness of their distributions, relative 1985), relying on thermally favorable sites (farms, to that of reference sites. ENFA requires only presence stables, and compost heaps) to meet the
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