Bicknell’s Thrush (Catharus bicknelli) habitat occupancy in Québec’s Laurentian Highlands
 
Taux d'occupation de l'habitat par la Grive de Bicknell (Catharus bicknelli) sur le plateau Laurentien du Québec

• Abstract
• Introduction
• Methods
  • Study area
  • Point counts
  • Site occupancy
  • Niche space occupancy
• Results
• Discussion
• Acknowledgments
• Responses to this article
• Acknowledgments
• Literature Cited

INTRODUCTION

In North America, several migratory bird species inhabiting boreal and eastern forests are declining (Sauer et al. 2013). Habitat loss, impairment, and fragmentation on breeding or wintering grounds or at stopover sites may play a significant role in these declines. The endangered status of several species has been directly linked to forest management issues. Those species include Olive-sided Flycatcher (Contopus cooperi; Robertson and Hutto 2007), Rusty Blackbird (Euphagus carolinus; Powel et al. 2010), Cerulean Warbler (Setophaga cerulea; Buehler et al. 2008), Kirtland’s Warbler (Setophaga kirtlandii; Long 2009), and Barrow̻s Goldeneye (Bucephala islandica; Vaillancourt et al. 2009, Gouvernement du Québec 2013). Forest management impacts, proven or hypothesized, have triggered calls for action by the scientific, philanthropic, and environmental advocacy communities, as exemplified by the “Boreal Birds Need Half” campaign (Wells et al. 2014), which aims to prevent habitat limitation from becoming a pervasive issue affecting boreal birds. Accordingly, forestry operators on breeding grounds are being asked to adopt more sustainable and bird-friendly practices (Booth et al. 1993, Franklin et al. 2002, Cyr et al. 2009, Bélanger 2010, Marzluff et al. 2000, Drapeau et al. 2016).

An essential requirement for effective and efficient recovery planning for a species at risk is the identification of the key limiting factors through its annual cycle (Faaborg et al. 2010, Rushing et al. 2016). Habitat availability is one of the most frequently cited limiting factors for a wide range of taxa (Hoekstra et al. 2005, Maxwell et al. 2016). This may be especially true for migratory species that depend on different habitats, each potentially under different threats, at different times through their annual cycle. Habitat may be limiting for a species at risk because it is rare, of low quality, inaccessible, or for more subtle reasons as in the case of species with spatially aggregated social systems (Macedo and Bianchi 1997, Bourque and Desrochers 2006) or a highly biased sex-ratio (Donald 2007).

To determine whether habitat availability limits a population, a logical first step is to determine how much suitable habitat is available yet unoccupied (Nelson and Buech 1996, Rappole et al. 2003, Gibson et al. 2007, Engler et al. 2014). High vacancy rates, i.e., low occupancy, would generally negate the hypothesis that habitat availability is limiting, at least in the geographic area considered (Hoekstra et al. 2005, Nielsen et al. 2006). However, apparently unoccupied areas could also reflect inadequacies of the survey method, i.e., low detection probability of the focal species (Gu and Swihart 2004) or of the habitat sampling design, i.e., failure to include important habitat variables for the species under consideration.

Bicknell’s Thrush (Catharus bicknelli) has one of the most restricted breeding ranges of all North American forest-breeding migratory birds (COSEWIC 2009, McFarland et al. 2013, Townsend et al. 2015, Hill and Lloyd 2017). At the continental scale, the species ranks as one of the highest conservation priorities (Rich et al. 2004, Rosenberg et al. 2014), while it is legally considered as threatened in Canada (Government of Canada 2012) and vulnerable in Québec (Gouvernement du Québec 2009). Most of Bicknell’s Thrush breeding habitat in Canada occurs in southern Québec in the Appalachian Range and on the Laurentian Highlands north of the St. Lawrence River (COSEWIC 2009). In the latter region, breeding habitat occurs primarily at high elevation in dense balsam fir dominated stands within industrial forestland where clear-cuts and forest management practices aimed at reducing stem density (hereafter called precommercial thinning) may affect habitat quality (Higdon et al. 2006, Chisholm and Leonard 2008, COSEWIC 2009, Aubry et al. 2011, 2016). Habitat loss and impairment on breeding grounds have been suggested as the major threats to the species (COSEWIC 2009, Lloyd and McFarland 2017). Consequently, there have recently been pressures and efforts to limit the extent and intensity of precommercial thinning throughout the species’ breeding range (Chisholm and Leonard 2008, BSC 2009, Gouvernement du Québec 2014, Lambert et al. 2017). Such changes can be costly to the industry, directly and indirectly affecting regional economies and, if misguided, impinge the credibility of science conservation advisors.

To better guide Bicknell’s Thrush conservation efforts, we studied habitat occupancy in Québec’s Laurentian Highlands. Our primary objective was to test whether maximum breeding habitat occupancy approached saturation (100%). We also tested the hypothesis that precommercial thinning is associated with lower occupancy of Bicknell’s Thrush breeding habitat, as found in other regions (Aubry et al. 2011). The species needs dense stands as a concealment for its nest and to avoid potential predation. Therefore, we predict that thinned stands are less occupied than unthinned stands. To test those two hypotheses, we performed site occupancy modeling as per Mackenzie et al. (2002). However, Bicknell’s Thrushes have large home ranges on their breeding grounds and a spatially aggregated social system (Aubry et al. 2011, Townsend et al. 2015), likely due to their polygynandric mating system (Goetz et al. 2003, Townsend et al. 2015), which may undermine the assumption of closure of the occupancy state required by occupancy models (MacKenzie et al. 2003). Thus, we also assessed occupancy using a graphical approach that represents Bicknell’s Thrush niche space based on a two-dimensional reduced projection of topographic and vegetation variables.

METHODS

Study area

The 17,350-km² study area is located north of the St. Lawrence River, centered approximately 75 km north of Quebec City, Québec, at the southeast edge of the Laurentian Highlands. It is part of the balsam fir-white birch bioclimatic domain (Grondin et al. 1998; Fig. 1) lying between 47° and 48.35°N and 70° and 72.30°W. The elevation varies from 130 to 1100 m and the mean annual temperature is 0° C. Abundant precipitations (1.2–1.6 m/year) are associated with a long fire cycle (> 500 years; Boucher et al. 2014). The vegetation is dominated by balsam fir (Abies balsamea) and paper birch (Betula papyrifera); black spruce (Picea mariana) occurs increasingly toward the north of the study area, and deciduous trees are often abundant in regenerating clear-cuts and recently burned areas (Grondin et al. 1998). Disturbances are mostly from anthropic origin, with forestry activities having occurred at all elevations since 1900 but more intensively at low elevation (Boucher and Grondin 2012, Boucher et al. 2014).

We determined stand age, the proportion of deciduous, and the extent of precommercial thinning over the study area from forest inventory data (Gouvernement du Québec 2015). We converted the original forestry and topographic map layers to rasters with a 10-m resolution, with the Spatial Analyst extension of ArcGIS (ESRI 2010). We calculated stand ages based on documented years of clear-cutting and other stand-renewing events, i.e., fire and major spruce budworm outbreaks. In places where only age classes were known, we determined stand age as the midpoint of the age class for even-aged stands, or as the lowest age class for heterogeneous stands. We extracted elevation at point counts and its variation within 1000 m from the Canadian Digital Elevation Data 2000 (available from https://open.canada.ca/data/en/dataset?organization=nrcan-rncan). We considered a habitat as suitable when it was at elevations greater than 550 m, composed of balsam fir-dominated stands, and had not been thinned (Lambert et al. 2005, Chisholm and Leonard 2008, Aubry et al. 2011, 2016).

Point counts

We compiled data from 7830 fixed radius point counts conducted for different projects in the study area between 1995 and 2016 (Fig. 1). Those projects focused on all bird species (> 98% of sites randomly selected) and covered a broader range of altitudes, while surveys targeting Bicknell’s Thrush covered sites with elevation > 800 m. The projects were the second Québec Breeding Atlas, Forêt Montmorency bird monitoring program, regional environmental impact assessments, Mountain BirdWatch monitoring scheme, Huron-Wendat Bicknell’s Thrush monitoring project, and provincial and federal governments’ Bicknell’s Thrush surveys. We retained 4818 point counts for analysis based on three criteria: a duration of 15 to 30 min (mean = 18 min), conducted before 9:00 (n = 4700) or after 19:00 (n = 118), and between 22 May and 25 July. Those periods correspond to high Bicknell’s Thrush vocal activity (Ball 2000). Nine percent of the point counts used playbacks of Bicknell’s Thrush calls and songs. Retained point counts were distributed among 2500 stations separated by at least 150 m, often (54%) along forestry roads. We surveyed 31% of the point count stations more than once in a year (Appendix 1), and surveyed 38 and 114 stations on two and three different years, respectively. Forty observers, all with experience with Bicknell’s Thrush vocalizations, participated in the point counts. We recorded all Bicknell’s Thrushes within 75 or 100 m-radii, depending on the data source. We assumed that the radius difference was sufficiently small across surveys, and that the distance between point counts was sufficient across the study areas, to prevent major biases (Yip et al. 2017).

Site occupancy

We fit nine competing single-season site occupancy models (Mackenzie et al. 2006) to measure site occupancy by Bicknell’s Thrush, given imperfect detection during point counts. Models were fit by maximum likelihood with the unmarked package 0.11-0 in R Version 3.3.1 (Fiske et al. 2011, R Development Core Team 2016). The models considered various combinations of 11 site-related occupancy and four point count-related detection variables, identified from our experience with the species, the published literature, and the habitat data generally available. (Table 1; Aubry et al. 2011, 2016, Lambert et al. 2005, Townsend et al. 2015). We introduced the variable Year in the models to account for a possible population trend. Further annual variation could result from nest predation by red squirrel (Tamiasciurus hudsonicus; Townsend et al. 2015), which may affect recruitment and demographic parameters, and hence occupancy. However, we have no quantitative information on cone crops or squirrel population densities throughout the duration and spatial extent of the study. Elevation was selected because the species is known to be associated with montane habitat (Townsend et al. 2015, Aubry et al. 2016) and we used the standard deviation of elevation within 1 km of point count as an index of terrain ruggedness. Proportion of deciduous within 1000 m along with proportion of precommercial thinning were selected as proxies for recent forestry activities and habitat structure. Bicknell’s Thrushes often establish their home range in regenerating or young forest stands (Townsend et al. 2015) ≥= 1.5–2 m high (personal observation). To account for a possible nonlinear response to forest age (Ter Braak and Looman 1986), we included a quadratic stand age term in the models. We used the standard deviation of stand age as an index of habitat heterogeneity. Some variables were estimated at local and/or at the landscape scale (within 100 and 1000 m of point count center, respectively) to explore the sensitivity of the species at those two scales. In the full model we included distance of point count from nearest road in view of concerns of a possible edge effect expressed earlier (Hanowski and Niemi 1995, but see Hutto et al. 1995, Lituma and Buehler 2016). Moreover, Bicknell’s Thrush may respond to edges, as shown in a recent study where the species was not avoiding stand edges in an industrial forest (Aubry et al. 2011), or as in a ski trail study where a higher nest density was observed in forest edges where vegetation was dense (Rimmer et al. 2004). In another study, in the White Mountains (New Hampshire, USA), the presence of hiking trails did not affect Bicknell’s Thrush abundance and detection probabilities (Deluca and King 2014). Models (Table 2) were selected to estimate site occupancy according to predation by squirrels (model 6), to habitat structure along with elevation (model 3) and year (model 1), to elevation (model 4) and topography (model 5) and to spatial variation in habitat structure (model 7) and habitat composition (model 8).

We computed Goodness-of-Fit for the best occupancy model using a parametric bootstrap approach (MacKenzie and Bailey 2004) with 100 replicates. The best, single-season model fit the data well with no apparent over dispersion (function parboot of package unmarked, p = 0.21). To facilitate convergence and parameter estimation, all numerical variables were standardized before analysis. We evaluated the degree of support for each model using Akaike’s Information Criteria (AIC_c) and standardized Akaike weights. The models with ΔAIC_c ≤ 2 were considered as supported models (Table 2).

Niche space occupancy

We conducted a Principal Component Analysis (function prcomp in R) using the three vegetation and topography variables that were identified as significantly related to Bicknell’s Thrush occupancy in the best performing occupancy model (Table 3), along with mean stand age (within 100 m of point count) that also appeared to be associated with occupancy (Fig. 2). We used the first two principal components to represent Bicknell’s Thrush niche space, and calculated two-dimensional kernel densities of Bicknell’s Thrush occurrences (R package MASS, function kde2d; Venables and Ripley 2002). The proportions of occupied point count stations falling in each kernel density category provided estimates of Bicknell’s Thrush occupancy.

RESULTS

Bicknell’s Thrush were reported at 121 (2.5%) of the 4818 point counts, and at 115 (4.6%) of the 2500 point count stations (Fig.1). The best-performing occupancy model included Year (+), Elevation (+), Elevation interactions with stand age (linear and quadratic), as well as the percentage of deciduous forest (+) and precommercial thinning (-) at the landscape scale (Table 2, Table 3). Given that estimate for forest stand age was positive and the age x elevation interaction estimate negative (Table 3), we interpret the significant interaction as a lower effect of stand age on occupancy at higher elevations. The best performing occupancy model as well as the other models, identified three point count-related detection variables that were significantly associated with the probability of detecting Bicknell’s Thrush (Table 3): date (increasing from May to July), duration (+), and use of playback (+). Detection probabilities in the morning were 0.16 ± 0.04 without playback and rose significantly to 0.63 ± 0.15 with playbacks. Detection probabilities were higher, but not significantly so (Table 3), in the evening, both without or with playbacks (0.36 ± 0.24, 0.83 ± 0.15, respectively). Occupancy increased significantly between 1995 and 2016 in the study area (Table 3, Fig. 3). An analysis where all variables except Year were set to their mean value over the entire study area, thereby removing confounding factors revealed that the temporal trend was consistent through time. Bicknell’s Thrushes were seldom reported below 800 m elevation (n = 6/121), and site occupancy was greater than 0.7 at only a handful of stations (n = 10) at the highest elevations (Fig. 4).

To better understand the relationship between stand age and occupancy, we contrasted the kernel density distributions of stand age at stations where Bicknell’s Thrushes were observed and not observed (Fig. 2). The distributions were substantially different, revealing higher occupancy of the youngest (20–30 years old) and oldest (> 70 years old) stands, and lower occupancy of mid-age stands.

In the niche space occupancy analysis, the first two axes of the principal component analysis accounted for 71% of the total variance (PC1: 0.44; PC2 0.27; Table 4). High values for the first factor reflected low elevation, but high deciduous and precommercial thinning cover. High values for the second factor reflected high elevation and young stands, independent of deciduous dominance or precommercial thinning. Of the 2500 point count stations surveyed, 1969 fell within the two-dimensional niche space defined by kernel density > 0.05 (Fig. 5). Unoccupied sites were dispersed throughout the biplot (Fig. 5) while occupied sites were mostly concentrated on the two left quadrants. Bicknell’s Thrush was largely unreported at stations in the lower right quadrant of the biplot, corresponding to lower elevation, high thinning, and more deciduous stands (Table 4). Bicknell’s Thrush reporting rate was consistently low, reaching less than 8% at point count stations in the most suitable habitat (i.e., kernel density estimates > 0.10; Fig. 6).

DISCUSSION

Our study of Bicknell’s Thrush site occupancy in the Laurentian Highlands of Québec, using two contrasted approaches, revealed that a large extent of potential habitat was unoccupied. Similar conclusions were reached from studies of several other avian species at risk, such as the Golden-cheeked Warbler (Setophaga chrysoparia; Rappole et al. 2003), Kirtland’s Warbler (Nelson and Buech 1996), Lesser Kestrel (Falco naumanni; Serano and Tella 2003), and White-browed Treecreeper (Climacteris affinis; Radford and Bennett 2004).

There is an apparent discrepancy between the positive regression estimate of % deciduous in Table 3, and the low reporting rates in the right quadrants of Fig 5, corresponding to high % deciduous values. We attribute this apparent discrepancy to the fact that occupancy estimates accounted for other covariables such as elevation, which was not the case in the principal component analysis. The significant negative interaction between forest age and elevation effects in the best occupancy model indicates that the occupancy of young forests, where deciduous stems are prevalent, is not as pronounced at high elevations as it is at lower elevations. Furthermore, the amount of deciduous forest was estimated within 1000 m around point count. At that scale and in an environment where forestry activity is ubiquitous, young deciduous dominated stands are common in the early stages of regenerating balsam fir forest. In our study area, below 800 m elevation, deciduous stands represented 40% (± 24) of the area within 1000 m of point count, and 28% (± 10) over 800 m. Despite that Bicknell’s Thrush is known as a balsam fir specialist, notable presence in deciduous stands has also been documented in New Brunswick (Nixon et al. 2001), in young regenerating stands where fir has not surpassed deciduous in height yet.

Our site occupancy models likely overestimated occupancy rates because the large home ranges of Bicknell’s Thrush (≥ 10 ha; Aubry et al. 2011) likely resulted in violations of the closure assumption (MacKenzie et al. 2006, Rota et al. 2009). On the other hand, imperfect detection may have led us to underestimate occupancy rates in the niche space occupancy analysis. This is unlikely since in a companion study (Aubry and Mazerolle, unpublished data), we estimated detection probabilities at ≥ 0.74 and ≥ 0.88 using point count techniques similar to those used here, i.e., 3 x 5 min. survey periods without and with an additional playback period, respectively. Biased occupancy rate estimates can also result from uneven accessibility of habitat patches across a study area, e.g., less access to high elevation sites. This was not at play in our research because the study area was covered by forestry roads, with almost no site beyond 300 m from a road, i.e., beyond the audible range of Bicknell’s Thrush calls. It is thus unlikely that imperfect detection has introduced a bias of sufficient importance to alter our conclusion.

Bicknell’s Thrush nesting habitat quality seems to be mostly driven by elevation and associated vegetation dynamics (e.g., wind throw, fir waves sensu Sprugel 1976) in both the northeastern United States (Lambert et al. 2005, Hale 2006) and in Québec (Aubry et al. 2016). In Vermont, in mostly protected areas, occupancy of high-elevation habitat approaches 100% (Frey et al. 2012). Extrapolating from Lambert et al.’s (2005) elevational habitat model, we should have recorded Bicknell’s Thrush as low as 550 to 600 m in our study area. A similar model adapted for Québec latitudes predicted occurrences at even slightly lower elevations (Rimmer, unpublished report). However, we recorded the species below 800 m (641–777 m) in only six occasions, corresponding to an estimated occupancy rate of < 8%. The discrepancy between model predictions and our observations may be due to habitat quality impairment at low elevation resulting from major fires and intensive logging through the 20th century (Boucher and Grondin 2012), the prevalence of precommercial thinning, and possibly nest predation by red squirrel. A similar effect was observed by Whitaker et al. (2015; D. Whitaker, personal communication), who noted that on Newfoundland the closely related Gray-cheeked Thrush (Catharus minimus) became confined to high elevation forests following the introduction of squirrels (Payne 1976), which are restricted to lower elevations.

Even at higher elevations, site occupancy by Bicknell’s Thrush was generally well below saturation (Fig. 4). The most parsimonious explanation for this is an insufficient number of birds due to limiting factors acting outside of the breeding grounds. However, alternative phenomena may lead to a lack of breeders in optimal habitat. First, as for lower elevation, territory abandonment may occur over a large scale because of nest predation by red squirrels (McFarland et al. 2008). Second, polygynandry in Bicknell’s Thrush may lead to clustering through conspecific attraction (Nocera and Forbes 2010) and, in turn, reduce the suitability of small habitat patches, as is the case with several other forest songbirds (Bourque and Desrochers 2006, Desrochers et al. 2010). Third, incomplete occupancy of suitable habitat at higher elevation may be a constraint of dispersal because of insufficient numbers of females. Considering the highly male-biased sex-ratio of the species, unoccupied habitat can remain unoccupied for a long time because of the lack of conspecifics to attract dispersers (Schlossberg and Ward 2004). Last, we cannot rule out that some habitat attributes may have been overlooked because of our selection of variables, which was based on what was available at the time of the study.

During the study period, in New Hampshire (1993–2003; Lambert et al. 2008), an annual decline (-7%) was reported while recent analyses from data across its United States range (2011–2016) produced a nonsignificant decline (Hill and Lloyd 2017). Bicknell’s Thrush numbers were declining in the Canadian Maritimes and southeastern Québec where the species became extirpated from several locations (Whittam 2015, Québec Breeding Bird Atlas 2018). Contrastingly, we documented a significant increase in occupancy in the spatiotemporal bounds of the current study. We can only speculate on the causes of this local increase, but it may result from a nonlinear functional response to the strong increase in early-successional dense balsam fir forest stands following a major spruce budworm outbreak that began in the early 1970s (Hardy et al. 1983) and lasted for over two decades in our study area (Gray et al. 2000).

Although large areas of apparently suitable Bicknell’s Thrush habitat appear to be unoccupied in the Laurentian Highlands of Québec, habitat conservation efforts and thrush-friendly forestry practices should not be abandoned. Habitat availability can rapidly become a concern if management of successional dynamics and forest structure pushes large areas of forest outside the suitable stand age and density for the species. This appears to be the case in northwestern New Brunswick where, if current forest management plans are maintained, Bicknell’s Thrush potential habitat will have entirely disappeared by 2027 (Higdon et al. 2006). Similarly, a proposal to vastly expand old-growth areas in support of the conservation of woodland caribou (Rangifer tarandus caribou) in the Laurentian Highlands of Québec (Équipe de rétablissement du caribou forestier du Québec 2013) may conflict with the maintenance of suitable habitat for Bicknell’s Thrush. Considering the ephemeral habitat suitability status, it is therefore prudent to preserve more habitat than what a target population may occupy at a specific time (Rompré et al. 2010, Frey et al. 2012). This rationale underlies the recent publication by the Government of Québec of guidelines aimed at reducing precommercial thinning in Bicknell’s Thrush occupied and potential habitat, as well as avoiding incidental destruction of nests, eggs, and young (Gouvernement du Québec 2014).

In the Laurentian Highlands of Québec, there appears to be a shortage of Bicknell’s Thrushes rather than its breeding habitat. But considering that the population seems to have increased over the period of the study, there are good conservation-based reasons to maintain more habitat at higher elevation (> 800 m) than is required to allow the population to grow to the recovery target as prescribed by the Species at Risk Act. Without discontinuing efforts to conserve breeding habitat, greater attention should be paid to other potential limiting factors. Current challenges for the species outside the breeding range are habitat loss and degradation due to anthropogenic and natural causes on its wintering grounds in the Greater Antilles (Hill and Lloyd 2017, Lloyd et al. 2017).

LITERATURE CITED

Aubry, Y., A. Desrochers, and G. Seutin. 2011. Response of Bicknell’s Thrush (Catharus bicknelli) to boreal silviculture and forest stand edges: a radio-tracking study. Canadian Journal of Zoology 89(6):474-482. http://dx.doi.org/10.1139/z11-011

Aubry, Y., A. Desrochers, and G. Seutin. 2016. Regional patterns of habitat use by a threatened forest bird, the Bicknell’sThrush, in Quebec. Canadian Journal of Zoology 94(4):301-309. http://dx.doi.org/10.1139/cjz-2015-0209

Ball, M. 2000. Vocal behaviour of Bicknell’s Thrush (Catharus bicknelli). Thesis. Dalhousie University, Halifax, Nova Scotia, Canada.

Bélanger, L. 2010. À l’aube d’une nouvelle foresterie pour le Québec - the dawn of “new forestry” in Quebec. Forestry Chronicle 86(2):155-156.

Bird Studies Canada (BSC). 2009. Conserving the Bicknell’s Thrush: stewardship and management practices for high elevation forest. BSC, Atlantic Region, Sackville, New Brunswick, Canada. [online] URL: http://www.bsc-eoc.org/library/ACHELPforestflyer-en.pdf

Booth, D. L., D. W. K.Boulter, D. J. Neave, A. A. Rotherham, and D. A. Welsh. 1993. Natural forest landscape management: a strategy for Canada. Forestry Chronicle 69(2):141-145. http://dx.doi.org/10.5558/tfc69141-2

Boucher, Y., and P. Grondin. 2012. Impact of logging and natural stand-replacing disturbances on high-elevation boreal landscape dynamics (1950–2005) in eastern Canada. Forest Ecology and Management 263:229-239. http://dx.doi.org/10.1016/j.foreco.2011.09.012

Boucher, Y., P. Grondin, and I. Auger. 2014. Land use history (1840–2005) and physiography as determinants of southern boreal forests. Landscape Ecology 29:437-450. http://dx.doi.org/10.1007/s10980-013-9974-x

Bourque, J., and A. Desrochers. 2006. Spatial aggregation of forest songbird territories and possible implications for area sensitivity. Avian Conservation and Ecology - Écologie et conservation des oiseaux 1(2):3. http://dx.doi.org/10.5751/ACE-00043-010203

Buehler, D. A., J. J. Giocomo, J. Jones, P. B. Hamel, C. M. Rogers, T. A. Beachy, D. W. Varble, C. P. Nicholson, K. L. Roth, J. Barg, R. J. Robertson, J. R. Robb, and K. Islam. 2008. Cerulean Warbler reproduction, survival, and models of population decline. Journal of Wildlife Management 72(3):646-653. http://dx.doi.org/10.2193/2006-339

Chisholm, S. E., and M. L. Leonard. 2008. Effect of forest management on a rare habitat specialist, the Bicknell’s Thrush (Catharus bicknelli). Canadian Journal of Zoology 86(3):217-223. http://dx.doi.org/10.1139/Z07-131

Committee on the Status of Endangered Wildlife in Canada (COSEWIC). 2009. COSEWIC assessment and status report on the Bicknell’s Thrush Catharus bicknelli in Canada. COSEWIC, Ottawa, Ontario, Canada. [online] URL: http://www.sararegistry.gc.ca/virtual_sara/files/cosewic/sr_Bicknell%27s%20Thrush_0810_e.pdf

Cyr, D., S. Gauthier, Y. Bergeron, and C. Carcaillet. 2009. Forest management is driving the eastern North American boreal forest outside its natural range of variability. Frontier in Ecology and Environment 7(10):519-524. http://dx.doi.org/10.1890/080088

Deluca, W. V., and D. I. King. 2014. Influence of hiking trails on montane birds. Journal of Wildlife Management 78(3):494-502. http://dx.doi.org/10.1002/jwmg.675

Desrochers, A., C. Renaud, W. M. Hochachka, and M. Cadman. 2010. Area-sensitivity by forest songbirds: theoretical and practical implications of scale-dependency. Ecography 33(5):921-931. http://dx.doi.org/10.1111/j.1600-0587.2009.06061.x

Donald, P. F. 2007. Adult sex ratios in wild bird populations. Ibis 149:671-692. http://dx.doi.org/10.1111/j.1474-919X.2007.00724.x

Drapeau, P., M.-A. Villard, A. Leduc, and S. J. Hannon. 2016. Natural disturbance regimes as templates for the response of bird species assemblages to contemporary forest management. Diversity and Distributions 22:385-399. http://dx.doi.org/10.1111/ddi.12407

Engler, J. O., D. Rödder, D. Stiels, and M. I. Förschler. 2014. Suitable, reachable but not colonised: seasonal niche duality in an endemic mountainous songbird. Journal of Ornithology 155:657-669. http://dx.doi.org/10.1007/s10336-014-1049-5

Équipe de rétablissement du caribou forestier du Québec. 2013. Lignes directrices pour l’aménagement de l’habitat du caribou forestier (Rangifer tarandus caribou). Équipe de rétablissement du caribou forestier, Québec, Canada. [online] URL: http://www.bape.gouv.qc.ca/sections/mandats/uranium-enjeux/documents/NAT13.1.pdf

ESRI. 2010. ArcGIS® 10. Environmental Systems Research Institute, Inc., Redlands, California, USA.

Faaborg, J., R. T. Holmes, A. D. Anders, K. L. Bildstein, K. M. Dugger, S. A. Gauthreaux Jr, P. Heglund, K. A. Hobson, A. E. Jahn, D. H. Johnson, S. C. Latta, D. J. Levey, P. P. Marra, C. L. Merkord, E. Nol, S. I. Rothstein, T. W. Sherry, T. S. Sillett, F. R. Thompson III, and N. Warnock. 2010. Conserving migratory land birds in the New World: Do we know enough? Ecological Applications 20(2):398-418. http://dx.doi.org/10.1890/09-0397.1

Fiske, I., R. B. Chandler, and A. Royle. 2011. Unmarked: models for data from unmarked animals. R package version 0.11-0. [online] URL: http://CRAN.R-project.org/package=unmarked.

Franklin, J. F., T. A. Spies, R. Van Pelt, A. B. Carey, D. A. Thornburgh, D. R. Berg, D. B. Lindenmayer, M. E. Harmon, W. S. Keeton, D. C. Shaw, K. Bible, and J. Chen. 2002. Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. Forest Ecology and Management 155:399-423. http://dx.doi.org/10.1016/S0378-1127(01)00575-8

Frey, S. J. K., A. M. Strong, and K. P. McFarland. 2012. The relative contribution of local habitat and landscape context to metapopulation processes: a dynamic occupancy modeling approach. Ecography 35(7):581-589. http://dx.doi.org/10.1111/j.1600-0587.2011.06936.x

Gibson, L., B. Barrett, and A. Burbridge. 2007. Dealing with uncertain absences in habitat modelling: a case study of a rare ground-dwelling parrot. Diversity and Distributions 13:704-713. http://dx.doi.org/10.1111/j.1472-4642.2007.00365.x

Goetz, J. E., K. P. McFarland, and C. C. Rimmer. 2003. Multiple paternity and multiple male feeders in Bicknell’s Thrush (Catharus bicknelli). Auk 120(4):1044-1053. http://dx.doi.org/10.1642/0004-8038(2003)120[1044:MPAMMF]2.0.CO;2

Gouvernement du Québec. 2009. Décret 1006-2009, 16 septembre 2009. Loi sur les espèces fauniques menacées ou vulnérables (L.R.Q., c. E-12.01). Gazette officielle du Québec, 30 septembre 2009, vol. 141 no 39. Québec, Canada.

Gouvernement du Québec. 2013. Mesure de protection du garrot d’Islande à l’égard des activités d’aménagement forestier. Ministère des Forêts, de la Faune et des Parcs et Sous-comité faune de l'entente administrative, Québec, Canada. [online] URL: http://mffp.gouv.qc.ca/publications/forets/amenagement/Mesure-protection-garrot-Islande.pdf

Gouvernement du Québec. 2014. Protection measure for the Bicknell’s Thrush in relation to forest management activities. Sous-comité faune de l'Entente administrative, Québec, Canada. [online] URL: http://mffp.gouv.qc.ca/english/publications/forest/Protection-measure-Bicknell-Thrush.pdf

Gouvernement du Québec. 2015. Normes de stratification écoforestière. Quatrième inventaire écoforestier du Québec méridional. Ministère de la Faune, des Forêts et des Parcs, Québec, Québec, Canada. [online] URL: https://www.mffp.gouv.qc.ca/forets/inventaire/pdf/norme-stratification.pdf

Government of Canada. 2012. Canada Gazette, part II, SOR/2012-133, June 20, 2012. Species at Risk Act, vol.146, no. 14. Government of Canada, Ottawa, Ontario, Canada. [online] URL: http://www.sararegistry.gc.ca/virtual_sara/files/orders/g2-14614i_e.pdf

Gray, D. R., J. Régnière, and B. Boulet. 2000. Analysis and use of historical patterns of spruce budworm defoliation to forecast outbreak patterns in Quebec. Forest Ecology and Management 127:217-231. http://dx.doi.org/10.1016/S0378-1127(99)00134-6

Grondin, P., J. Blouin, P. Racine, H. D'Avignon, and S. Tremblay. 1998. Rapport de classification écologique du sous-domaine bioclimatique de la sapinière à bouleau blanc de l'est. Forêt Québec, Direction des inventaires forestiers, Ministère des ressources naturelles du Québec (révision 2000), Québec, Canada.

Gu, W., and R. K. Swihart. 2004. Absent or undetected? Effects of non-detection of species occurrence on wildlife-habitat models. Biological Conservation 116:195-203. http://dx.doi.org/10.1016/S0006-3207(03)00190-3

Hale, S. R. 2006. Using satellite imagery to model distribution and abundance of Bicknell’s Thrush (Catharus bicknelli) in New Hampshire White Mountains. Auk 123(4):1038-1051. http://dx.doi.org/10.1642/0004-8038(2006)123[1038:USITMD]2.0.CO;2

Hanowski, J. M., and G. J. Niemi. 1995. A comparison of on-and off-road bird counts: do you need to go off road to count birds accurately? Journal of Field Ornithology 66(4):469-483.

Hardy, Y. J., A. Lafond, and L. Hamel. 1983. The epidemiology of the current spruce budworm outbreak in Quebec. Forest Science 29(4):715-725.

Higdon, J. W., D. A. MacLean, J. M. Hagan, and M. Reed. 2006. Risk of extirpation for vertebrate species on an industrial forest in New Brunswick, Canada: 1945, 2002, and 2027. Canadian Journal of Forest Research 36:467-481. http://dx.doi.org/10.1139/x05-260

Hill, J. M., and J. D. Lloyd. 2017. A fine-scale U.S. population estimate of a montane spruce-fir bird species of conservation concern. Ecosphere 8(8):e01921. http://dx.doi.org/10.1002/ecs2.1921

Hoekstra, J. M., T. M. Boucher, T. H. Ricketts, and C. Roberts. 2005. Confronting a biome crisis: global disparities of habitat loss and protection. Ecology Letters 8:23-29. http://dx.doi.org/10.1111/j.1461-0248.2004.00686.x

Hutto, R. L., S. J. Hejl, J. F. Kelley, and S. M. Pletschet. 1995. A comparison of bird detection rates derived from on-road versus off-road point counts in northern Montana. Pages 103-110 in C. J. Ralph, J. R. Sauer, and S. Droege, editors. Monitoring bird populations by point counts. General Technical Report PSW-GTR-149. U.S. Forest Service, Pacific Southwest Research Station, Albany, California, USA.

Lambert, J. D., D. I. King, J. P. Buonaccorsi, and L. S. Prout. 2008. Decline of a New Hampshire Bicknell’s Thrush population, 1993-2003. Northeastern Naturalist 15(4):607-618. http://dx.doi.org/10.1656/1092-6194-15.4.607

Lambert, J. D., K. P. McFarland, and C. C. Rimmer. 2017. Guidelines for managing Bicknell’s thrush habitat in the United States. High Branch Conservation Services, Hartland, Vermont, USA. [online] URL: http://highbranchconservation.com/wp-content/uploads/2017/02/Guidelines-for-Managing-Bicknells-Thrush-Habitat-in-the-United-States-2017.pdf

Lambert, J. D., K. P. McFarland, C. C. Rimmer, S. D. Faccio, and J. L. Atwood. 2005. A practical model of Bicknell’s Thrush distribution in the northeastern United States. Wilson Bulletin 117:1-11. http://dx.doi.org/10.1676/04-013

Lituma, C. M., and D. A. Buehler. 2016. Minimal bias in surveys of grassland birds from roadsides. Condor 118:715-727. http://dx.doi.org/10.1650/CONDOR-16-73.1

Lloyd, J. D., and K. P. McFarland, editors. 2017. A conservation action plan for Bicknell’s Thrush (Catharus bicknelli). International Bicknell’s Thrush Conservation Group. https://doi.org/10.6084/m9.figshare.4962608

Lloyd, J. D., J. Scarl, J. C. Martínez-Sánchez, C. Rimmer, L. Prout, and S. Mathison. 2017. Bicknell’s Thrush mitigation across borders: a strategy for full life-cycle conservation. Vermont Center for Ecostudies, White River Junction, Vermont, USA. https://doi.org/10.6084/m9.figshare.4775680.v1

Long, J. N. 2009. Emulating natural disturbance regimes as a basis for forest management: a North American view. Forest Ecology and Management 257:1868-1873. http://dx.doi.org/10.1016/j.foreco.2008.12.019

Macedo, R. H., and C. A. Bianchi. 1997. Communal breeding in tropical Guira Cuckoos Guira guira sociality in the absence of a saturated habitat. Journal of Avian Biology 28:207-215. http://dx.doi.org/10.2307/3676971

MacKenzie, D. I., and L. L. Bailey. 2004. Assessing the fit of site-occupancy models. Journal of Agricultural, Biological, and Environmental Statistics 9:300-318. http://dx.doi.org/10.1198/108571104X3361

MacKenzie, D. I., J. D. Nichols, J. E. Hines, M. G. Knutson, and A. B. Franklin. 2003. Estimating site occupancy, colonization, and local extinction when a species is detected imperfectly. Ecology 84:2200-2207. http://dx.doi.org/10.1890/02-3090

MacKenzie, D. I., J. D. Nichols, G. B. Lachman, S. Droege, J. A. Royle, and C. A. Langtimm. 2002. Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248-2255. http://dx.doi.org/10.1890/0012-9658(2002)083[2248:ESORWD]2.0.CO;2

MacKenzie, D. I., J. D. Nichols, J. A. Royle, K. H. Pollock, L. L. Baile, and J. E. Hines. 2006. Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Academic Press, New York, New York, USA.

Marzluff, J. M., M. G. Raphael, and R. Sallabanks. 2000. Understanding the effects of forest management on avian species. Wildlife Society Bulletin 28(4):1132-1143.

Maxwell. S. L., R. A. Fuller, T. M. Brooks, and J. E. M. Watson. 2016. Biodiversity: the ravages of guns, nets and bulldozers. Nature 536:143-145. http://dx.doi.org/10.1038/536143a

McFarland, K. P., C. C. Rimmer, S. J. K. Frey, S. D. Faccio, and B. B. Collins. 2008. Demography, ecology and conservation of Bicknell’s Thrush in Vermont, with a special focus on the Northeast Highlands. Technical Report 08-03, Vermont Center for Ecostudies, Norwich, Vermont, USA. [online] URL: https://www.researchgate.net/publication/228412299_Demography_ecology_and_conservation_of_Bicknell%27s_Thrush_in_Vermont_with_a_special_focus_on_the_Northeastern_Highlands

McFarland, K. P., C. C. Rimmer, J. E. Goetz, Y. Aubry, J. M. Wunderle Jr, A. Sutton, J. M. Townsend, A. Llanes Sosa, and A. Kirkconnell. 2013. A winter distribution model for Bicknell’s Thrush (Catharus bicknelli), a conservation tool for a threatened migratory songbird. PLoS ONE 8(1):e53986. http://dx.doi.org/10.1371/journal.pone.0053986

Nelson, M. D., and R. R. Buech. 1996. Test of 3 models of Kirtland’s Warbler habitat suitability. Wildlife Society Bulletin 24(1):89-97.

Nielsen, S. E., G. B. Stenhouse, and M. S. Boyce. 2006. A habitat-based framework for grizzly bear conservation in Alberta. Biological Conservation 130:217-229. http://dx.doi.org/10.1016/j.biocon.2005.12.016

Nixon, E. A., S. B. Holmes, and A. W. Diamond. 2001. Bicknell’s Thrushes (Catharus bicknelli) in New Brunswick clear cuts: their habitat associations and co-occurrence with Swainson’s Thrushes (Catharus ustulatus). Wilson Bulletin 13(1):33-40. http://dx.doi.org/10.1676/0043-5643(2001)113[0033:BTCBIN]2.0.CO;2

Nocera, J. J., and G. J. Forbes. 2010. Incorporating social information to improve the precision of models of habitat use. Condor 112(2):235-244. http://dx.doi.org/10.1525/cond.2010.090237

Payne, N. 1976. Red squirrel introduction to Newfoundland. Canadian Field Naturalist 90:60-64.

Powell, L. L., T. P. Hodgman, and W. E. Glanz. 2010. Home ranges of Rusty Blackbirds breeding in wetlands: how much would buffers from timber harvest protect habitat? Condor 112(4):834-840. http://dx.doi.org/10.1525/cond.2010.100151

Québec Breeding Bird Atlas. 2018. Bicknell’s Thrush map. Regroupement QuébecOiseaux, Environment Canada’s Canadian Wildlife Service, and Bird Studies Canada. Québec, Québec, Canada. [online] URL: http://www.atlas-oiseaux.qc.ca/donneesqc/cartes.jsp?lang=en

R Development Core Team. 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Radford, J. Q., and A. F. Bennett. 2004. Thresholds in landscape parameters: occurrence of the White-browed Treecreeper Climacteris affinis in Victoria, Australia. Biological Conservation 117:375-391. http://dx.doi.org/10.1016/j.biocon.2003.08.002

Rappole, J. H., D. I. King, and J. Diez. 2003. Winter- vs. breeding-habitat limitation for an endangered avian migrant. Ecological Applications 13:735-742. http://dx.doi.org/10.1890/1051-0761(2003)013[0735:WVBLFA]2.0.CO;2

Rich, T. D., C. J. Beardmore, H. Berlanga, P. J. Blancher, M. S. W. Bradstreet, G. S. Butcher, D. W. Demarest, E. H. Dunn, W. C. Hunter, E. E. Iñigo-Elias, J. A. Kennedy, A. M. Martell, A. O. Panjabi, D. N. Pashley, K. V. Rosenberg, C. M. Rustay, J. S. Wendt, and T. C. Will. 2004. Partners in Flight North American Landbird Conservation Plan. Cornell Lab of Ornithology, Ithaca, New York, USA.

Rimmer, C. C., K. P. McFarland, and R. B. Renfrew. 2004. Evaluating the use of Vermont ski areas by Bicknell’s Thrush: applications for Whiteface Mountain. Vermont Institute of Natural Science, Woodstock, Vermont, USA. [online] URL: https://www.researchgate.net/profile/Christopher_Rimmer/publication/254424226_Evaluating_the_Use_of_Vermont_Ski_Areas_by_Bicknell’s_Thrush_Applications_for_Whiteface_Mountain/links/54bd01600cf218da939004fc.pdf

Robertson, B. A., and R. L. Hutto. 2007. Is selectively harvested forest an ecological trap for Olive-sided Flycatchers? Condor 109:109-121. http://dx.doi.org/10.1650/0010-5422(2007)109[109:ISHFAE]2.0.CO;2

Rompré, G., Y. Boucher, L. Bélanger, S. Côté, and W. D. Robinson. 2010. Conservation de la biodiversité dans les paysages forestiers aménagés: utilisation des seuils critiques d’habitat. Forestry Chronicle 86(5):572-579. http://dx.doi.org/10.5558/tfc86572-5

Rosenberg, K. V., D. Pashley, B. Andres, P. J. Blancher, G. S. Butcher, W. C. Hunter, G. Mehlman, A. O. Panjabi, M. Parr, G. Wallace, and D. Wiedenfeld. 2014. The state of the birds 2014 watch list. North American Bird Conservation Initiative, U.S. Committee, Washington, D.C., USA. [online] URL: http://www.stateofthebirds.org/2014/extinctions/watchlist.pdf

Rota, C.T., R. J. Fletcher Jr, R. M. Dorazio, and M. G. Betts. 2009. Occupancy estimation and the closure assumption. Journal of Applied Ecology 46:1173-1181. http://dx.doi.org/10.1111/j.1365-2664.2009.01734.x

Rushing, C. S., T. B. Ryder, and P. P. Marra. 2016. Quantifying drivers of population dynamics for a migratory bird throughout the annual cycle. Proceedings of the Royal Society B: Biological Sciences 283(1823). http://dx.doi.org/10.1098/rspb.2015.2846

Sauer, J. R., W. A. Link, J. E. Fallon, K. L. Pardieck, and D. J. Ziolkowski Jr. 2013. The North American breeding bird survey 1966-2011: summary analysis and species accounts. North American Fauna 79:1-32. http://dx.doi.org/10.3996/nafa.79.0001

Schlossberg, S. R., and M. P. Ward. 2004. Using conspecific attraction to conserve endangered birds. Endangered Species Update 21:132-138.

Serano, D., and J. E. Tella. 2003. Dispersal within a spatially structured population of Lesser Kestrels: the role of spatial isolation and conspecific attraction. Journal of Animal Ecology 72:400-410. http://dx.doi.org/10.1046/j.1365-2656.2003.00707.x

Sprugel, D. G. 1976. Dynamic structure of wave-generated Abies balsamea forests in the northeastern United States. Journal of Ecology 64(3):889-911. http://dx.doi.org/10.2307/2258815

Ter Braak, C. J. F., and C. W. N. Looman. 1986. Weighted averaging, logistic regression and the Gaussian response model. Vegetatio 65:3-11. http://dx.doi.org/10.1007/BF00032121

Townsend, J. M., K. P. McFarland, C. C. Rimmer, W. G. Ellison, and J. E. Goetz. 2015. Bicknell’s Thrush (Catharus bicknelli). In P. G. Rodewald, editor. The birds of North America. Cornell Lab of Ornithology, Ithaca, New York, USA.

Vaillancourt, M., P. Drapeau, M. Robert, and S. Gauthier. 2009. Origin and availability of large cavities for Barrow’s Goldeneye (Bucephala islandica), a species at risk inhabiting the eastern Canadian boreal forest. Avian Conservation and Ecology - Écologie et conservation des oiseaux 4(1):6. [online] URL: http://www.ace-eco.org/vol4/iss1/art6/

Venables, W. N., and B. D. Ripley. 2002. Modern applied statistics with S. Fourth Edition. Springer, New York, New York, USA. http://dx.doi.org/10.1007/978-0-387-21706-2

Wells, J., D. Childs, F. Reid, K. Smith, M. Darveau, and V. Courtois. 2014. Boreal birds need half: maintaining North America’s bird nursery and why it matters. Boreal Songbird Initiative, Seattle, Washington, USA, Ducks Unlimited Inc., Memphis, Tennessee, USA, and Ducks Unlimited Canada, Stonewall, Manitoba, Canada.

Whitaker, D. M., P. D. Taylor, and I. G. Warkentin. 2015. Gray-cheeked Thrush (Catharus minimus minimus) distribution and habitat use in a montane forest landscape of western Newfoundland, Canada. Avian Conservation and Ecology 10(2):4. [online] URL: http://www.ace-eco.org/vol10/iss2/art4/

Whittam, B. 2015. Bicknell’s Thrush. Pages 390-391 in R. L. M. Stewart, K. A. Bredin, A. R. Couturier, A. G. Horn, D. Lepage, S. Makepeace, P. D. Taylor, M.-A. Villard, and R. M. Whittam, editors. Second atlas of breeding birds of the Maritime Provinces. Bird Studies Canada, Environment Canada, Natural History Society of Prince Edward Island, Nature New Brunswick, New Brunswick Department of Natural Resources, Nova Scotia Bird Society, Nova Scotia Department of Natural Resources, and Prince Edward Island Department of Agriculture and Forestry, Canada. [online] URL: http://www.mba-aom.ca/pdfs/atlas_en_390-419.pdf

Yip, D. A., L. Leston, E. M. Bayne, P. Sólymos, and A. Grover. 2017. Experimentally derived detection distances from audio recordings and human observers enable integrated analysis of point count data. Avian Conservation and Ecology 12(1):11. [online] URL: http://www.ace-eco.org/vol12/iss1/art11/ http://dx.doi.org/10.5751/ACE-00997-120111