High levels of habitat loss and fragmentation limit reproductive success by reducing home range size and provisioning rates of Northern saw-whet owls

Abstract

Studies of the effects of habitat fragmentation have been heavily biased toward population and community questions, with less attention on the effects of habitat loss and fragmentation on individual behaviour and reproduction. We studied the effects of habitat amount and configuration on the foraging behaviour, provisioning rates and physiological condition of breeding male northern saw-whet owls (Aegolius acadicus) nesting in the fragmented aspen parkland of central Alberta, Canada. We then examined the relationship between provisioning behaviour and both reproductive success, and juvenile physiological condition. Males nesting in areas with little forest cover and large inter-patch distances spent more time perching, maintained smaller home ranges, and provisioned their nests less frequently. However, home range size and provisioning rates levelled off in landscapes with moderate to high forest cover. Male owls breeding in areas with low forest cover, and those raising large broods, also exhibited higher levels of chronic stress, as measured by heterophil/lymphocyte (H/L) ratios. Predictably, males that provisioned the nest less often fledged fewer young, which, in turn, exhibited higher variation in physiological condition. These results suggest that low levels of habitat loss and fragmentation may be beneficial to saw-whet owls, potentially by increasing prey abundance. However, high levels of habitat loss and fragmentation appeared to reduce the foraging efficiency of male saw-whet owls, increase their levels of physiological stress, and reduce their reproductive success. Increasing habitat loss and fragmentation may ultimately decrease population sizes of saw whet owls in this area and other species that are similarly affected by changes to in habitat composition or configuration.

Introduction

Habitat fragmentation is often used to describe two different, but linked processes: a reduction in the amount of habitat (composition) and changes in the configuration of the remaining patches (Wiens, 1994). The relative influences of habitat composition and configuration have been difficult to separate (Andrèn, 1994, Fahrig, 1997, Villard et al., 1999, Bélisle et al., 2001), and attract ongoing attention (Schmiegelow and Mönkkönen, 2002, Fahrig, 2003, Cushman, 2006). Theoretical work suggests that habitat configuration is often important only below some threshold of habitat amount (With and Crist, 1995, Fahrig, 2003), but both attributes appear to be important to the persistence of diverse bird populations (Radford et al., 2005).

Beyond the distinction between habitat composition and configuration, the majority of studies that address the effects of habitat fragmentation have focused on community and population effects (see reviews by Fahrig, 2003, Cushman, 2006). Habitat fragmentation is frequently associated with reductions in species richness within communities (e.g., Schmiegelow and Mönkkönen, 2002, Fahrig, 2003, Stewart et al., 2004). Loss in species richness presumably results from the effects of habitat fragmentation on populations for which there may be reductions in genetic diversity (e.g. Gibbs and Stanton, 2001), population growth rates (Donovan and Flather, 2002), or population sizes (e.g. Rolstad, 1991, Bender et al., 1998, Donovan and Flather, 2002). Within populations, however, less is known about how habitat fragmentation affects reproductive success (reviewed by Stevens et al., 2003), and very little is known about how the behaviour of individuals influences population responses.

Recent work on birds has shown that habitat loss increases movement costs to individuals, (Bélisle et al., 2001, Ruiz et al., 2002) and decreases breeding success (Hinsley et al., 1999). Although these effects have received the most attention in the context of individuals whose home range is encompassed within a single patch (e.g. Matthysen and Curie, 1996, Brooker et al., 1999, Bélisle and Desrochers, 2002), the effects of habitat loss and fragmentation can also apply to individuals that maintain home ranges that encompass multiple patches. These individuals may actually be more vulnerable to fragmentation effects than individuals whose home ranges are contained within a single patch (Grubb and Doherty, 1999, Hinsley, 2000). For individuals maintaining multiple patch home ranges, smaller and more isolated patches of habitat may require that they consistently travel farther for resources. Indeed, use of multiples patches of habitat within a home range appears to convey substantial costs for several bird species (Redpath, 1995b, Hinsley et al., 1999). These costs may accrue from increased energy expenditure to detour around gaps in habitat (e.g. St. Clair et al., 1998, Bélisle and Desrochers, 2002), and higher predation risk (Lima and Dill, 1990, Nonacs, 2001, Redpath, 1995b, Siffczyk et al., 2003, Turcotte and Desrochers, 2003), both of which may lower foraging efficiency and increase physiological costs as a result of chronic stress (Ruiz et al., 2002, Turcotte and Desrochers, 2003). When impediments to movement are associated with critical life stages, such as provisioning young, habitat fragmentation is more likely to reduce the reproductive success of individuals and, potentially, population viability (Rolstad, 1991, Hinsley, 2000).

The northern saw-whet owl (Aegolius acadicus) provides an excellent opportunity for examining how habitat fragmentation affects the movements, foraging efficiency and reproductive success of a species whose home range typically encompasses multiple habitat patches. These owls are considered to be forest specialists (Cannings, 1993) and thus, may generally be more vulnerable to the effects of habitat fragmentation (Harris and Reid, 2002). Although saw-whet owls can hunt from forest edges, habitat loss and fragmentation may reduce perch availability, alter prey availability (Bayne and Hobson, 1998, Silva et al., 2005) and increase predation by open-area species such as the great horned owl (Bubo virginianus; Cannings, 1993). Because males are the sole provisioners to the nest for the bulk of incubation and brooding (Cannings, 1993), northern saw-whet owls present a relatively simple system for studying foraging and provisioning behaviour and their effects on reproductive success with varying degrees of forest fragmentation.

Optimal foraging theory (sensuStephens and Krebs, 1986) offers several unexplored predictions about how owls foraging in multiple patches might behave in a fragmented landscape. In particular, the Marginal Value Theorem suggests that individuals that travel farther between successive patches will spend longer periods of time foraging within a given patch (sensuCharnov, 1976). As increasing habitat loss and fragmentation isolates resources into patches (Bruun and Smith, 2003), individuals may simultaneously be obliged to forage farther from their nests (Frey-Roos et al., 1995, Bruun and Smith, 2003), and maintain larger home ranges (Redpath, 1995b), resulting in fewer provisioning trips to the nest (Frey-Roos et al., 1995, Bruun and Smith, 2003). Conversely, landscapes may contain so little habitat that the distance between patches may exceed a species’ gap-crossing tolerance (e.g., Desrochers and Hannon, 1997, Harris and Reid, 2002). In these cases, territorial movements may be constrained to reduce the sizes of home ranges, putting a greater strain on available resources. Either effect should ultimately reduce the rate at which individuals can provision their young (Frey-Roos et al., 1995, Tella et al., 1998, Hinsley, 2000, Bruun and Smith, 2003) with consequential effects on their own or their offspring’s growth and condition (Tarlow et al., 2001). Travelling through fragmented areas may also result in increased stress to the provisioning parent as a result of increased predation risk (Lima and Dill, 1990) and higher movement costs (Hinsley, 2000), which may be expressed physiologically (Bélisle et al., 2001, Ruiz et al., 2002) as a decrease in body mass relative to size (Perez-Tris et al., 2004) or in an immunological response (Ruiz et al., 2002).

The objective of this study was to examine how variation in habitat composition and configuration affect foraging decisions, provisioning behaviour and physiological condition of male northern saw-whet owls. We also examined how male provisioning behaviour relates to individual reproductive success and juvenile condition prior to fledging. Based on these objectives, and combined with the theory described above, we generated five specific predictions. (1) As the distance between foraging perches and patches increases, the time an individual spends at a perch or in each patch will also increase. (2) Male home range sizes and foraging radii will vary quadratically, increasing as lower forest cover and increasing distance between patches spreads out resources, but then decreasing when the distance between patches exceeds the gap-crossing tolerance of individuals. (3) A reduction in forest cover and an increase in the distance between remaining patches will be reflected in lower provisioning rates. (4) Males that provision the nest less frequently will fledge fewer young and produce fledglings in poorer physiological condition. (5) Males breeding in areas with low forest cover and greater distances between remaining patches will also exhibit poorer physiological condition.