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Habitat loss, fragmentation and degradation are drivers of major declines in biodiversity and species extinctions. The actual causes of species population declines following habitat change are more difficult to discern and there is typically high covariation among the measures used to infer the causes of decline. The causes of decline may act directly on individual fitness and survival, or through disruption of population processes. We examined the relationships among configuration, extent and status of native vegetation and three commonly used indicators of individual body condition and chronic stress (haemoglobin level, haematocrit, residual body mass condition index) in 13 species of woodland-dependent birds in south-eastern Australia. We also examined two measures of changes to population processes (sex ratio and individual homozygosity) in ten species and alleic richness in five species. We found little support for relationships between site or landscape characteristics and individual or population response variables, notwithstanding that our simulations showed we had sufficient power to detect relatively small effects. We discuss possible causes of the absence of detectable habitat effects in this system and the implications for the usefulness of individual body condition and easily measured haematological indices as indicators of the response of avian populations to habitat change.
Habitat loss and fragmentation are well established as the most prevalent causes of anthropogenically induced bio diversity loss through local and global population decline and extinction (Fahrig 2003, World Resources Inst. 2005). However, the identification of the mechanisms of these negative effects has proven more difficult to establish. Species’ responses to loss and degradation of habitat differ greatly (Mönkkönen and Reunanen 1999, Bennett and Radford 2009) because a wide range of life-history traits can be affected by fragmentation (Banks et al. 2007). There is often covariation of many landscape and site attributes (e.g. habitat clearance, fragmentation of remnants and decrease in mean remnant size and remnant structure and condition) that may influence whether an area can support a population (Saunders et al. 1991, Yates and Hobbs 1997, Ewers and Didham 2005, Lindenmayer and Luck 2005, Radford et al. 2005). Despite this problem, biodiversity protection and restoration require the teasing apart of the processes underlying biodiversity declines that are the consequence habitat loss, fragmentation and degradation (Lindenmayer and Fischer 2007). There is a considerable tension in the literature between those emphasising the importance of extrinsic and stochastic factors in determining population decline following habitat loss (Caughley 1994), and those who argue for an important, though often difficult to detect, role for intrinsic factors (such as individual condition and genetics) in population declines (Arcese 2003). Species declines may result directly from loss of habitat or indirectly through changes in population processes due to habitat fragmentation. Vegetation structure is a common determinant of avian diversity and individual species’ habitat preferences (Rotenberry 1985, Mac Nally 1990). Human-induced changes to vegetation structure decrease habitat suitability for some species while increasing it for others (Lindenmayer et al. 2008). Reduction in the size and increase in edge ratio of patches in fragmented forests and woodlands can lead to decreased vegetation condition (Yates and Hobbs 1997), elevated predation and competition and reduced food availability for woodland-dependent birds (Andren 1992, Zanette et al. 2000, Huhta et al. 2004, Maron et al. 2011).
The effects of clearing on habitat quality stem from the selective clearing of more productive parts of the landscape for agriculture (Vesk and Mac Nally 2006). In the woodlands of south-eastern Australia, the majority of the remnants are in areas of low primary productivity, and have often been heavily grazed, with much of the ground layer and understorey degraded. The lower productivity of the remnants lead to reduced food resouces for insectivorous birds (Watson 2011). The avifaunas of dry woodland systems of southern Australia continue to decline, due primarily to habitat loss compounded by a range of other factors (Robinson and Traill 1996, Ford et al. 2001, Mac Nally et al. 2009, Ford 2011), although the mechanisms generating these declines remain unclear.
The physiological status of individual birds may offer an insight into processes that vary in response to extent, configuration and condition of remnant habitat. Haematological and morphological measures have been used for assessment of individual condition (Norte et al. 2009a). Whole blood haemoglobin levels (Hb) and haematocrit (the ratio of packed blood cells to total blood volume, HCT) have been used to assess condition and physiological response in relation to habitat and to individual behaviour, such as reproductive investment and exercise levels (Campbell 1995). These measures have also been related to the effects of environmental stressors including parasite load, food availability and environmental toxins (Acquarone et al. 2002, Dudaniec et al. 2006, Linkie et al. 2006). Residual body mass (RBM), a measure of mass that accounts for structural size, is frequently used as an index of ‘body condition’ in ecological studies (Schulte-Hostedde et al. 2005, Stevenson and Woods 2006). It reflects variation in stored fuel reserves, particularly lipids, (Seewagen 2008), which have been shown to influence individual inclusive fitness in some birds (Ardia 2005).
HCT, Hb and RBM have been used to assess effects of environmental variation, including habitat fragmentation and habitat quality (and related food availability), on individual condition in wild passerines (Hõrak et al. 1998, Strong and Sherry 2000, Mazerolle and Hobson 2002) and small mammals (Johnstone et al. 2011). These three measures differ between sexes, and with reproductive status, age and season (Norte et al. 2009a), while RBM also varies with moult (Bojarinova et al. 1999). It is necessary to account for these covariates when investigating relationships between physiological condition and habitat. Where a relationship is found, further work is required to determine causality. The relationship may represent a direct effect of habitat on individual physiology, alternatively, individual condition may influence settlement choice (Porlier et al. 2009) or lead to competitive exclusion of individuals in poorer condition from favoured habitat (Latta and Faaborg 2002).
There has been much work assessing the impacts of changes in landscape composition and configuration on individual movement, gene flow and population genetics (Manel et al. 2003, Storfer et al. 2007). Less attention has been given to the influence of landscape characteristics on individual genetic diversity, despite the important role that this quantity plays in evolutionary processes (Porlier et al. 2009). Population processes such as mating systems may be affected by changes in landscape structure and habitat condition (Banks et al. 2007) that could be reflected in individual heterozygosity levels (García-Navas et al. 2009). Heterozygosity may be positively associated with offspring fitness, reproductive success, local survival and recruitment into the adult population (Coulson et al. 1998, 1999, Coltman et al. 1999, Amos et al. 2001, Hansson et al. 2001, Banks et al. 2010) though meta-analysis of such heterozy gosity-fitness correlations suggests that the effects are usually weak (Chapman et al. 2009). Such effects need not be restricted to sessile organisms; where mobile or dispersing individuals assess habitat quality before settling, fitter individuals (with higher individual heterozygosity) may choose and be able to defend higher quality territories (Seddon et al. 2004).
In addition to the individual-based responses to habitat alteration outlined above, disruption of natural patterns of mobility can lead to changes in population parameters, such as sex ratios or genetic diversity, with downstream consequences for individual and population fitness (Banks et al. 2007). For example, disrupted dispersal of the usual dispersing sex, females, in the brown treecreeper Climacteris picumnus in Australian woodlands, has been implicated in low female recruitment, isolated patches containing no females, and local patch extirpation (Cooper and Walters 2002, Cooper et al. 2002a, b). Also, reduction in dispersal and gene flow, recent bottlenecks and/or disruptions of mating systems may lead to decreased levels of population genetic diversity (Palstra and Ruzzante 2008). Thus associations of sex ratios and genetic diversity (measured by allelic richness; AR) with landscape conditions may provide evidence of important responses to landscape alteration.
The dry woodlands of south-eastern Australia have suffered considerable habitat clearance and degradation and there has been a corresponding and ongoing decline of the region's avifauna (Robinson and Traill 1996, Ford et al. 2001, Mac Nally et al. 2009). A pattern of disproportionately large decline in incidence in apparently suitable remnant habitat in many woodland-dependent birds compared to decline in landscape tree-cover has been documented (Radford et al. 2005, Radford and Bennett 2007). Species showing this pattern of disproportionate decline have been termed ‘decliner’, while those that show no relationship of incidence landscape tree-cover have been termed ‘tolerant’ (Bennett and Radford 2009, Amos et al. 2012).
In this study, we examine the relationships of landscape structure and habitat condition with physiological status, individual and population genetic diversity and local sex ratio to explore whether these might be mechanisms underpinning some of the decline of resident woodland birds of south-eastern Australia. Specifically, we explore the possibility that there are impacts of landscape and site attributes on individual physical condition and heterozy gosity, or on population genetic diversity and local sex ratios, that may be contributing to the observed pattern of decline through reduced individual and population condition and reproductive output, disruption of population processes, fitness and function (Hõrak et al. 1998, Kilgas et al. 2006).
We predicted that, if landscape and/or site condition are contributing to the decline of woodland-dependent birds in the study area, evidence of a relationship with RBM, HCT, or Hb should be found in the decliner species, and not in the tolerant species. Site condition is expected to affect sedentary species (those that stay in the same home range year round) more strongly than mobile ones, which may move locally or regionally between areas of varying condition. With regards to the effects of landscape and site on homozygosity-by-locus (HL), AR or sex ratio, evidence of differences related to landscape and site quality would support the hypothesis that population or social processes have been disrupted by change in habitat confi guration or quality (Banks et al. 2007). Relationships between site and landscape variables and the response variables may also be due to condition-dependent settlement patterns. Nevertheless the existence of differences in response variables relating to anthropogenic habitat change would be evidence of disruption of the birds’ interaction with their ecosystem.
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We found support of an effect of landscape or site condition on individual body condition, levels of AR, HL or sex-ratio skew in only two of 389 combinations of species, responses and predictors. The study therefore provides little evidence that these effects contribute to the observed decline in woodland birds in the box-ironbark region.
Our simulations showed that the models used were capable of detecting moderate effects, R2 > 0.2 with relatively small samples (n = 60) and very small effects with R2 as small as ca 0.05 with large (n > 250) samples. For a few species and response variables, sample sizes were too small to detect any but the largest effect (i.e. Hb and HCT in weebill, and to a lesser extent in buff-rumped thornbill and dusky woodswallow). However for the majority of tests, sample sizes were sufficient to detect an effect if it were present, either for aggregate samples (204 tests where n > 140), or in many cases also for individual sexes (Table 2).
While Hb, HCT and RBM have been identified as useful measurements for estimation of individual condition in relation to environmental factors (Campbell 1995, Norte et al. 2009a, b), they are subject to variation due to age, sex, moult status and between season, year and time of day; breeding status and parasite loads also affect these measures (Hõrak et al. 1998, Ots et al. 1998, Fair et al. 2007, Norte et al. 2009a, 2010). Where used independently as indices of individual condition, these measures may lead to erroneous conclusions. HCT in particular has been challenged as an independent indicator of condition as it is affected by state of hydration (Dawson and Bortolotti 1997, Fair et al. 2007). Relationships of all three indices with individual condition are not monotonic, and similar values may be caused by positive or negative influences (Fair et al. 2007).
Nevertheless, a main aim of this study was to identify any evidence of an effect of our chosen site or landscape condition measures, which are widely used to describe landscape and habitat change, on Hb, HCT, RBM, HL or sex ratio. We incorporated age, sex, moult status, season, and year into our models as random or fixed effects. We also modelled the two factors explaining the greatest variance, sex and age, separately. Despite the capacity of our analyses to detect small effects, we were unable to detect effects in the comparisons of interest (vegetation and individual condition) in this study.
The studies showing an effect of fragmentation on individual condition mostly examined breeding individuals or their nestlings. Studies restricted to nestlings, or specifically to birds of known breeding status (Suorsa et al. 2003a, Norte et al. 2009b, 2010) allow the removal of the effects of age or reproductive status from analysis. They offer more sensitive probes of response to vegetation variables. Such studies are likely to be limited to single species readily sampled at the nest, or intensive studies of marked populations. Our study attempted a more general, multi-species approach, sampling many sites without repeated sampling of individuals. We could estimate age only from plumage, and could not be sure of the breeding status of birds, unless they had a marked brood patch, and therefore we had limited ability to account for age and breeding status per se.
The region in which the study was undertaken was under extreme climatic stress at the time of the study, having suffered one of the most extreme droughts worldwide from 1997 to 2010 (Leblanc et al. 2009). While earlier studies recorded declines in avifauna related to area of remnant treecover in the landscape (Radford et al. 2005, Radford and Bennett 2007), the more recent reports found that decline in numbers was occurring across the region regardless of amount of remnant tree-cover (Mac Nally et al. 2009). These declines were found across all foraging guilds, including the nectarivores and insectivores of our study. The declines were probably due to reduced food resources (Mac Nally et al. 2009). This may have led to a uniform degree of stress across the entire region, so that effects of landscape configuration or in-site vegetation would be difficult to ascribe. Turcotte and Desrochers (2008) argued that the lack of effect of habitat fragmentation on body condition may be due to differential mortality, predation, or attempted emigration of individuals in poorer condition from fragments. Such a mechanism may explain the lack of effect in our system, although Turcotte and Desrochers’ (2008) birds were subject to regular seasonal stresses rather than the longer-term set of stresses caused by drought in our study system, albeit also causing reduced food abundance, and potentially reduced breeding (Mac Nally et al. 2009). There is a paradox here, if all except the best-conditioned birds are absent from localities (or indeed a whole region due to intrinsic attributes of the individuals), then it may not be possible to detect the effect in the birds themselves, because the poorer conditioned individuals are absent. The result may be fewer birds remaining, that is, the decline in occurrence observed (Radford and Bennett 2007, Mac Nally et al. 2009) with the proximate cause of the decline no longer apparent since the poorer condition birds are absent.
A second factor that may have reduced our ability to detect an effect was the small range of habitat condition in sites that were of sufficient quality to contain woodland-dependent birds. Habitat scores (Parkes et al. 2003) for sample sites had relatively little variation (12–52 out of a possible 75). Most sites had a similar level of degradation; there were no sites in very good condition, and only a few in exceptionally poor condition. Broad modelling of vegetation condition across the state of Victoria showed that the majority of our sites were at the upper end of the available range of condition (Dept of Sustainability and Environment 2008). Our sampling sites, of necessity, were located where sufficient birds were present to make sampling practical; most sites in very poor condition had few woodland-dependent birds present.
Our results indicate that the commonly used measures of avian condition considered here are not useful for discerning the effects of landscape and vegetation change for woodland-dependent birds. Moreover, there is little evidence that stress per se, at least as indicated by these condition measures, is responsible for the decline or otherwise of the woodland birds. There were good grounds for expecting differences, especially between decliner and tolerant species and between sedentary and mobile species, given the rich background of data from prior work. We had substantial capacity to discern effects of stress were these important.