Robust predictive performance of indicator species despite different co-occurrence patterns of birds in natural and managed boreal forests
Introduction
The success of decision-making in biodiversity conservation and natural resource management relies upon a detailed understanding of spatial and temporal patterns of biodiversity (Heywood and Watson, 1995, Van Jaarsveld et al., 1998). However, thorough biodiversity assessments can be extremely expensive and time-consuming (Knight et al., 2006, Pressey et al., 2000), and conservation biologists frequently use biodiversity surrogates such as indicator species to assess biodiversity without detailed species inventories (Leal et al., 2010, Pearson, 1994, Thomson et al., 2007). Indicator species, which are small sets of species whose presence or absence are correlated with the biodiversity of a larger group of species (Fleishman et al., 2005), have been successfully used to predict biodiversity of numerous taxa, including plants, invertebrates, and vertebrates, and across a variety of ecosystems (Azeria et al., 2009, Lindenmayer and Likens, 2011). One of the most important applications of indicator species is to assess the impacts of anthropogenic disturbance, such as forest harvesting, on biodiversity (Drever et al., 2008, Lindenmayer et al., 2000).
The selection of indicator species often relies on knowledge of species co-occurrence patterns (Azeria et al., 2009), which may be altered by anthropogenic disturbance. Habitats under anthropogenic disturbance tend to harbor different species communities compared to corresponding habitats in their natural state, even many years following disturbance events (Edwards et al., 2014, Kneitel and Chase, 2004, Zhao et al., 2013). Anthropogenic disturbance can also disrupt patterns of interspecific associations (Azeria et al., 2011, Sarà et al., 2006). As a result, the performance of indicator species identified under natural conditions can be poor in ecosystems under anthropogenic disturbance due to alterations in environmental filtering, interspecific interactions, and, ultimately, species co-occurrence (Lindenmayer and Likens, 2011). This is a critical issue because the reliability of indicator species may be lowest where there is the greatest need for accurate assessments of anthropogenic impacts on biodiversity, thus imposing a unique challenge to the applications of indicator species. Surprisingly, few studies have investigated how the performance of indicator species in predicting biodiversity changes with anthropogenic disturbance (Lawton et al., 1998, Schulze et al., 2004).
Boreal forests are regularly harvested under sustainable forest management strategies, such as ecosystem-based management, with the goal of maintaining a balance between economic interests and biodiversity conservation. Despite the fact that ecosystem-based management aims to develop forestry practices that best emulate natural disturbance regimes such as wildfire (Bergeron et al., 2002), the practice of clearcutting is still widely used. Clearcutting strongly modifies the structure of boreal forest ecosystems by converting old-growth stands to young, even-aged stands (Cyr et al., 2009, Imbeau et al., 2001) and removing most standing trees and snags, which are key structural elements in post-fire conditions (Hutto, 2006). Consequently, managed forests often harbor contrasting species communities to natural forests, even many years following harvest (Azeria et al., 2011, Zhao et al., 2013). The potential for contrasting species co-occurrence patterns in managed and natural boreal forests means that indicator species could be ineffective for assessing the long term impacts of forestry on biodiversity.
Our overarching goal was to examine the effect of variation in bird species co-occurrence on the predictive performance of indicator species in natural and managed boreal forests. Indicator species may provide a practical and efficient measure for evaluating avian diversity in boreal forests, where poor visibility in dense forests and the cryptic nature of many species can make full inventories of diverse avian communities difficult to achieve (Drapeau et al., 2000, Zhao et al., 2013). We studied boreal bird communities in natural forests (originating from natural disturbances such as wildfire, disease and blow-downs) dominated by old-growth stands, and managed forests (originating from clearcutting for the timber industry) dominated by early successional stands. Our objectives were to (1) compare species co-occurrence patterns in natural and clearcut stands, (2) select indicator species based on co-occurrence patterns to predict species richness, and (3) evaluate the predictive performance of indicator species under both natural and clearcutting disturbance regimes using the same training data set and an independent testing data set.
Section snippets
Study area
The study was conducted in the boreal forest of the Côte-Nord region of Québec, Canada (49°-52°N, 65°-70°W) (Zhao et al., 2013). The climate in the region is humid, with a mean annual temperature of −2.5 to 0.0 °C and total annual precipitation of 1000–1400 mm, with 35% of this falling as snow (Grondin et al., 1996). Due to its high precipitation the area has a long fire cycle (average length >270 years), resulting in landscapes dominated by uneven-aged, old-growth stands (Bouchard et al., 2008).
Species co-occurrence classification
We recorded 70 bird species across the 185 sites in the training data set, of which 56 occurred in more than 1% of sites. Of these 56 species, 25 (44.6%) were mature forest species, 10 (17.9%) were young forest species, 10 (17.9%) were shrubland species and 11 (19.6%) were generalists (Table S1). Hierarchical clustering analysis based on sites in both stand types identified a set of five empirical groups (Fig. S1a). We recorded 47 bird species in more than 2% of the sites in natural stands, of
Discussion
Our study demonstrates that examining species co-occurrence patterns in natural and managed forests can produce important insights into the performance of biodiversity surrogates. First, we reveal that species co-occurrence patterns are not always consistent with species’ known primary habitat associations, and are different in natural and clearcut stands, suggesting that species have responded to novel environmental conditions created by forest harvesting differently. Second, due to the
Acknowledgments
We thank our industrial partners for providing access to forest management areas. We are grateful to all field assistants for their efforts in data collection. Two anonymous reviewers provided valuable comments. This project was funded by the Natural Sciences and Engineering Research Council of Canada-Laval University Industrial Research Chair in Silviculture and Wildlife.
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Qing Zhao and Tom H.E. Mason have equal contributions.