Nest webs: A community-wide approach to the management and conservation of cavity-nesting forest birds

Forest Ecology and Management 115 (1999) 243±257

Nest webs: A community-wide approach to the management and conservation of cavity-nesting forest birds Kathy Martina,*, John M. Eadieb b

a Department of Forest Sciences, University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada, V6T 1Z4 Department of Wildlife, Fish and Conservation Biology, University of California, 1053 Academic Surge, Davis, CA 95616, USA

Abstract We propose that cavity-nesting bird communities are structured in nest webs analogous to food webs, where interspeci®c and intraspeci®c interactions are centered around nest site availability. Our sites of mixed deciduous coniferous forest in northcentral BC, Canada, support a rich diversity of eight species of primary cavity nesters (PCNs) (woodpeckers), four species of weak cavity nesters (nuthatch, chickadees) and 20 secondary cavity-nesting species (ducks, passerines and birds of prey). Richness varied across forest-types with some plots being `hotspots' and others being depauperate. Across a range of foresttypes, we measured species richness and abundance of birds and squirrels using point count census techniques, playbacks of taped calls of woodpeckers and owls, and by searching for active nests. We also measured resource use (trees able to support cavities, or existing cavities) in relation to availability (tree species, abundance and habitat characteristics such as edge-type and degree of fragmentation). In both 1995 and 1996, we found signi®cant positive correlations between the abundance of primary and secondary cavity-nesting birds, and negative correlations between both of these groups and weak cavity excavators. None of the three cavity-nesting groups was positively correlated with open-nesting (non-cavity) forest birds, rejecting our null hypothesis of common habitat quality. In contrast, the abundance of secondary cavity-nesting species was signi®cantly negatively correlated with non-cavity species, possibly because these species compete for resources other than nest sites, such as invertebrate prey. Using these data, we construct a nest web for the cavity-nesting community in northcentral British Columbia. This approach demonstrated strong and weak links among species in the web and identi®ed key species whose presence may be critical to the integrity of the community. We plan to test how nest web structure shifts in response to different forest-cutting regimes, and whether changes in species richness and abundance can be ameliorated with selective harvesting. # 1999 Elsevier Science B.V. All rights reserved. Keywords: Nest webs; Cavity-nesting birds; Community structure; Forestry operations; Bird±habitat interactions; Guild structure

1. Introduction Cavity-nesting birds comprise a major component of many forest bird communities. Primary cavitynesting species (e.g. woodpeckers) excavate cavities *Corresponding author. Tel.: +1-604-822-9695; fax: +1-604822-5410; e-mail: [email protected]

used by a large number of avian and mammalian species. Weak cavity excavators (e.g. chickadees, nuthatches) use cavities produced by primary cavity excavators, but also create cavities of their own. Secondary cavity nesters (SCNs, e.g. tree swallows, bluebirds, ducks) rely primarily on the cavities created by the ®rst two guilds or on a limited number of natural holes. Accordingly, cavity-nesting bird com-

0378-1127/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0378-1127(98)00403-4

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K. Martin, J.M. Eadie / Forest Ecology and Management 115 (1999) 243±257

munities exist within a clear hierarchy or guild structure with potentially strong interdependences among members of this community. Some species depend partly (weak cavity excavators) or entirely (SCNs) on other species (primary cavity nesters, PCNs) to produce a critical resource (cavities). Moreover, these ecological dependencies may vary with habitat features such as forest-type or tree health, and with the stage of forest succession. Cavity-nesting bird communities seem well suited to community analysis, but surprisingly, they have not been well studied from this perspective. Numerous reports exist on differences among species in resource use and resource overlap (tree preference, cavity size and orientation, snag availability and use; Van Balen et al., 1982; Angelstam, 1990; Dobkin et al., 1995; Sedgwick, 1997), but many of these studies have been descriptive. Few researchers have directly examined the links among species or the mechanisms that structure these communities; fewer still have considered the community of cavity nesters as an integrated whole (i.e. all guilds rather than just woodpeckers or just SCNs, but see Raphael and White, 1984). Community-wide studies designed to investigate the functional relationships among the members of these communities are needed to provide informed decision making by managers charged with the conservation of forest natural resources. Concern for cavity-nesting birds is increasing among forest managers because these species are highly dependent on old trees or dead wood for nesting, roosting and feeding, and many species are likely to be sensitive to the removal of these trees. The density and diversity of woodpeckers in forest stands could have a strong in¯uence on the richness and abundance of other species requiring nest cavities to breed or roost (i.e. SCNs). Hence, forest management practices could have a signi®cant impact on the overall diversity of forest bird and mammal communities. Many woodpeckers and other cavity nesters are associated with disturbance events (®res, insect outbreaks) and can co-exist with some frequency of openings in the forest canopy. However, in northern Scandinavia, where the majority of the deciduous forests have been removed, several woodpecker species have been locally extirpated or endangered (Angelstam and Mikusinski, 1994). The status of SCN species in these regions has received less attention, as have the rela-

tionships of non-cavity nesting species to changes in the cavity-nesting community. An enhanced understanding of the interactions and interdependence among cavity-nesting species is crucial for the effective management of forest birds. In this paper, we suggest a new approach in the analysis of cavity-nesting bird communities that may provide a fresh perspective, allow predictive tests of community structure, and aid in the development of conservation and management programs for forestnesting bird communities. Speci®cally, we propose that cavity-nesting bird communities (CNBCs) exist within `nest webs,' directly analogous to food webs. By viewing CNBCs as nest webs, we employ a broader community perspective in studying connectance, linkage and interactions among members of these webs, and we can appeal to established theory to predict more precisely the structure and function of these communities. Such an approach serves two purposes: (1) it may provide a stronger predictive basis for anticipating the effects of forest management practices on the stability and resilience of forestnesting bird communities and (2) it provides a unique opportunity to test food web theory in a novel system. We outline a rationale for considering `nest webs' as analogues to food webs, and demonstrate the application of this concept in an on-going study of cavitynesting communities in BC, Canada. We then consider how such an approach might improve our ability to manage and conserve forest bird communities. 2. Cavity-nesting bird communities as nest webs Food webs are typically characterized by: (a) a central resource required or provided by all members (food or prey); (b) a hierarchy of consumers (producers, primary consumers, secondary consumers, etc.; i.e. trophic levels); and (c) links and connectance between and within species in these trophic levels. Based on the number and strength of the links among members in the web, a variety of predictions about community stability, diversity, and resilience has been derived (e.g. Pimm, 1980; Warren, 1990; Waltho and Kolasa, 1994; de Ruiter et al., 1995). Food web theory has played a central organizing theme in community ecology for well over three decades and continues to be a hotly debated area.

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Table 1 Comparison of the structure of food webs and nest webs of CNBCs

Resource Organization Linkage/connectance Resource exchange within and between levels

Food webs

Nest webs

Food (prey) Trophic levels (primary producers, primary consumers, secondary consumers, etc.) Usually complex; non-linear and not necessarily size-structured Energy flow and nutrient cycling

Nests (cavities) Nidic levels (PCN, WPCN, SCN)

Although not traditionally viewed as such, cavitynesting communities have all of the features of communities structured as food webs: (a) there is a central resource required that is produced by members of the community (i.e. cavities); (b) there is a hierarchy of consumers (PCN, weak primary excavators, SCNs; i.e. `nidic' levels); and (c) there are links and connectance within and among species in these levels. These links may be facilitatory or competitive, direct or indirect. The striking parallels between food webs and nest webs suggest that CNBCs might well have a structure comparable to that of a food web (Table 1). By viewing CNBCs as a nest web, we may gain new insight into the structure, function, and response to perturbation of these forest bird communities. A simpli®ed nest web can be envisioned as comprising several levels or guilds (Fig. 1). The forest tree community represents the fundamental `producer' level ± without trees there can be no cavities and

Fig. 1. Hypothetical structure of a nest web at the guild level. The guilds considered are primary cavity nesters (PCN), weak primary cavity nesters (WPCN), secondary cavity nesters (SCN) and noncavity nesting species (NONCAV).

Relatively simple and linear; likely size structured Nest flow or nest cycling

hence no cavity-nesting community. PCNs, however, are the key to the production of the resource (cavities) required by the remaining species in the community. In effect, PCNs are the manufacturers, converting the raw resources (trees or snags) into a commodity (cavities) required by all other consumers. Heard (1994) referred to such interactions as a `processing chain.' Weak cavity excavators (WPCNs) use the cavities created by the PCNs, but also make cavities for themselves and so would have links with both PCNs and trees. In most analyses of cavity-nesting birds, WPCNs are considered SCNs. However, because of their partial independence from the activities of PCNs, this lumping could obscure some of the important structure within these communities. Our studies at Riske Creek and Knife Creek (described below) clearly demonstrate the need to consider WPCNs, separately. The third guild, SCNs, depends almost entirely upon PCNs and WPCNs for cavities as we have observed little apparent use of natural cavities in our system; their connection to trees is therefore indirect and may be mediated entirely by the abundance and activities of primary and WPCNs. Noncavity nesting birds species (NONCAV) comprise the ®nal group of forest birds. Although rarely considered in cavity-nesting bird community studies, non-cavity species may compete with cavity nesters for invertebrate prey and so could have important effects on the dynamics of the cavity-nesting community (see Bock et al., 1992). Moreover, analysis of the abundance of non-cavity nesting birds is useful to control for possible inter-guild associations that might be due simply to habitat quality correlates rather than to ecological interdependence among the guilds. Given this basic structure, we can predict the relationships among the guilds in a typical nest web (Fig. 1). These are:

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1. SCNs will be strongly and positively correlated with PCNs (SCNs need PCN to create cavities); 2. WPCNs will either be positively correlated with PCNs, if WPCNs use cavities excavated by PCNs, or uncorrelated if WPCNs rely primarily on natural cavities or cavities they make themselves; 3. SCNs will be positively correlated (although perhaps weakly) with WPCNs assuming that SCNs use WPCN cavities or if both rely on PCNs for cavities; and 4. NONCAVs will not be correlated to any of the cavity nesters unless all birds respond to the same habitat variables. Alternatively, NONCAVs may be negatively correlated to cavity-nesting species if they compete for food or non-nesting resources (e.g. Bock et al., 1992). We test these predictions for forest-nesting bird communities in the central interior of British Columbia. Our analyses focus ®rst on guild level associations. We then explore the nest web structure and interactions among individual species. 3. Study area and methods We present data from two general study sites (Riske Creek and Knife Creek) in the Chilcotin Region (518 520 N, 1228 210 W) of north central BC, Canada. These forests are in the Fraser River Basin Ecosection and are characterized as the very dry warm Interior Douglas Fir (IDF) Biogeoclimatic Zone (Meidinger and Pojar, 1991). The Riske Creek site has a rich mixture of deciduous and coniferous forest embedded in a matrix of grasslands, shallow ponds and wetlands. The Knife Creek sites have predominantly dry coniferous forest with deciduous riparian zones around small streams. Deciduous species include trembling aspen (Populus tremuloides) and some balsam poplar and black cottonwood (Populus balsamifera ssp.). The predominant coniferous species are Douglas Fir (Pseudotsuga menziesii), lodgepole pine (Pinus contorta) and white spruce (Picea glauca) with lesser amounts of jackpine (P. banksiana) and hybrid spruce (P. glauca x engelmannii). All sites are mature forest not previously cut, although some sites have second growth due to ®re or other disturbance events.

We designed the study to examine the importance of different forest riparian zone-types on the structure and function of communities of cavity-nesting birds, and to evaluate the possible impacts of different forest-harvesting practices. In 1995, we chose 11 plots on the Riske Creek site that represented the range of forest-types and fragmentation, including three complexes of small stands (0.1±5 ha), forest fragments of varying size, and extensive stands of coniferous or deciduous forest bordered by grasslands, ponds and/or lakes. In the continuous and fragmented forest, we established plots starting at the edge and extending 500 m into the stand; six transect lines were established in a grid 500 m long and 100 m wide representing a 30 ha area. A grid design was not possible in the complexes, so we established a transect line according to the same rules as the plots. In 1996, ®ve new plots were added in Knife Creek and all 1995 plots were re-sampled. In 1996, the plot size was reduced to 20 ha (4 lines 500 m long each) for a total of 20 ha. Our major treatment variables are: forest stand composition (deciduous, coniferous, mixed), forest stand structure (density, diameter at breast height (dbh)), degree of fragmentation (continuous, fragmented, and small complexes) and edge characteristics (forest interior, forest edge including dry edge (forest/grassland) and wet edge (pond, stream, wetland). The Knife Creek sites are scheduled to be cut from 1998 to 2001 either as clear cut blocks or by selective harvesting (removal of varying proportions of pine and spruce). Point count stations for bird censusing were established at the intersection of the grid lines (30 points in 1995 and 20 points per plot in 1996). Point count stations were 100 m apart with the ®rst station 50 m in from the forest edge. In the complexes, point count stations were established 100 m apart; if the fragment had a radius less than 50 m, only the forest area was censused. From 0500 to 0930 hours, ®xed radius (50 m) point counts were completed at each station for 8 min in 1995 and 6 min in 1996. Since woodpeckers are not well censused using point counts, we used playbacks of woodpecker calls at each station in 1995. We played the call of each woodpecker species twice, each call followed by 30 s of listening time, starting with the smaller species and moving to the largest species. To avoid the potential problem of over-sampling, we reduced the woodpecker playbacks to every

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second station in 1996. We noted the species and number of birds within 50 m and recorded whether they were seen, calling, singing, drumming or recorded during the woodpecker playback period. In 1995, 206 point count stations were censused on 11 plots by two observers, and in 1996, 264 stations were censused by two observers (one the same as in 1995) on 16 plots. Each year, three rounds of counts were completed from late May to late June. Between rounds, observers were rotated across the plots and the starting points varied to reduce effects of potential observer and time bias. In the analysis of point count census data, we used the total number of individuals detected for each species. On the same plots, we searched for nests for all cavity-nesting species. We located nests by looking for cavities, observing breeding behaviour and listening for excavating woodpeckers or begging chicks. The location of active cavity nests was recorded and the distance and bearing to the nearest point count station. We found a total of 203 nests for 16 species (112 in 1995 and 91 in 1996). We recorded the type of tree used (Nˆ201 nests), and if possible, determined which species made the cavity (Nˆ177 nests) or whether the nest was in a natural hole (Nˆ17 nests). To determine habitat use relative to availability, we established 11.2 m radius vegetation plots at each point count station and at each active nest tree. The point count station marker or the cavity tree were at the centre of the vegetation plot. Trees larger than 14 cm dbh (from preliminary data, this was the minimal size of tree that contained a cavity) were identi®ed to species, dbh measured, decay stage recorded, the number and type of cavities present, and any signs of disease recorded. Vegetation plots done at the point count stations were considered as random plots to compare with vegetation plots at nest sites. For active nests off plots, we chose a control vegetation plot in a random direction and a random distance (25±75 m from the nest site) in a habitat capable of supporting a cavity (i.e. the plot must contain at least one tree 14 cm dbh. To measure the inter-annual dynamics of tree growth, health and survival, and cavity dynamics, all trees 14 cm in the vegetation plots, including random points, were tagged with an individual numbered metal disc. A total of 6250 trees were `tagged.'

247

4. Results 4.1. Composition of the cavity-nesting community Our sites of mixed deciduous±coniferous forest in north-central BC, Canada, support a rich diversity of eight species of woodpeckers (PCNs), four species of weak cavity nesters, 20 secondary cavity-nesting ducks, passerines and birds of prey, and 11 species of cavity-using mammals (Appendix A). Overall, the cavity-nesting community in our study area comprised 43 species of birds and mammals, about half of the forest fauna. Another 44 species of noncavity-nesting bird species were observed on our study plots. The relative abundance of each of the four guilds (measured as the total number of individuals detected per point count station census) varied considerably among the study plots (Fig. 2). The patterns of abundance for each guild showed considerable heterogeneity among our forest sites (i.e. there are `hot spots' and `cold spots'). `Hot spots' varied for each guild. The few sites that were `hot spots' for SCNs also held high numbers of PCNs; however, sites that were good for PCNs and SCNs typically held fewer WPCNs and NONCAVs. Since all guilds did not respond in the same manner within sites, patterns of abundance may re¯ect guild-speci®c requirements and are not simply an indicator of overall habitat quality. Had some sites simply been good bird habitat and others poor, we would have anticipated similar responses for all guilds. 4.2. Analysis at the guild level We used simple and partial correlation analyses to examine the relationships among guilds (partial correlations are calculated for each pair of guilds while controlling for the abundance of the remaining two guilds). The trends observed among the cavity-nesting guilds are illustrated in Fig. 3 while the simple and partial correlation coef®cients among guilds are provided in Table 2. In both 1995 and 1996, there was a weak negative correlation of PCNs with WPCNs, a very strong positive correlation of PCNs and SCNs, and a negative correlation of SCNs and WPCNs (Table 2). NONCAVs tended to be negatively associated with SCNs (signi®cantly so in 1996) and

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Fig. 2. The relative abundance of each guild in each study plot: primary cavity nesters (PCN), weak primary cavity nesters (WPCN), secondary cavity nesters (SCN) and non-cavity nesters (NONCAV).

positively associated with WPCNs. The partial correlation analyses were generally consistent with the simple correlation analyses, indicating that the relationships observed were not confounded by complex interactions among the guilds. Analyses based on nest counts provided very similar results to those based on the point count census (Table 2). Fig. 4 summarizes the analyses at the guild level (pooling both years). This schematic of the nest web at

Fig. 3. Pairwise scattergrams of relative abundance for three guilds of cavity-nesting birds in British Columbia; primary cavity nesters (PCN), weak primary cavity nesters (WPCN), secondary cavity nesters (SCN).

the guild level illustrates the connections and interaction strengths among the web components. The observed patterns ®t several of our predicted relationships: (i) there is a strong and highly signi®cant association of SCNs with PCNs; (ii) there is a weak relationship of SCNs and PCNs with WPCNs (the negative trend was not anticipated); and (iii) there is either no relationship or a negative relationship of cavity nesters with NONCAV species. We conclude

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249

Table 2 Pearson correlations and partial correlation coefficients (in parentheses) among cavity-nesting guilds in north-central British Columbia study plots

I. Point counts 1995 (Nˆ11)

1996 (Nˆ16)

II. Nest counts 1995 (Nˆ11)

1996 (Nˆ16)

WPCN

SCN

NONCAV

WPCN

ÿ0.52 (ÿ0.37) ±

SCN

±

0.88*** (0.84)*** ÿ0.40 (0.13) ±

ALLCAV

±

±

ÿ0.42 (ÿ0.24) 0.21 (ÿ0.02) ÿ0.36 (0.04) ÿ0.35

PCN WPCN

ÿ0.22 (ÿ0.11) ±

SCN

±

0.61** (0.72)** ÿ0.30 (ÿ0.08) ±

ALLCAV

±

±

PCN

ÿ0.01 (0.01) ±

0.69* (0.69)* ÿ0.02 (ÿ0.02)

0.03 (ÿ0.49) ±

0.79*** (0.84)*** 0.39 (0.60)*

PCN

WPCN PCN WPCN

0.06 (0.53)* 0.20 (0.11) ÿ0.50* (ÿ0.66)* ÿ0.14 ± ± ± ±

Analyses based on point counts and nest counts are presented separately. * p<0.05, **p<0.01, ***p<0.001.

4.3. Analysis at the species level

Fig. 4. Structure of the nest web at the guild level. Simple correlation coefficients and partial correlation coefficients (in parentheses) are shown. Analyses were based on point counts in 1995 and 1996. Significance values: *p<0.05, **p<0.01, ***p<0.001.

that the primary links in these communities are between PCNs and SCNs, whereas WPCNs appear to vary independently and in opposite direction.

Examination of cavity-nesting communities as a nest web, analogous to a food web, ultimately requires that we quantify interactions among species rather than guilds. To do so, we examined correlations among species based on the abundance of nest sites of each species on our study plots. By analysing nest data, rather than point count data, we focus more directly on nesting dynamics. We considered only the common species for which we have suf®cient data; these include two PCNs (NOFL and RNSA), two WPCNs (RBNU and MOCH), and four SCNs (MOBL, EUST, TRES and TAHU). Fig. 5 illustrates the nest web at the species level, summarizing nest data for both 1995 and 1996. Signi®cant positive correlations were found between three SCNs (EUST, MOBL and TRES), and between these species and both PCNs (with the exception of

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Fig. 5. Structure of the nest web at the species level. Analyses were based on nest count census pooled for 1995 and 1996. Values indicate simple correlation coefficients among species. Dotted lines indicate negative correlations and solid lines positive correlations. Bold lines indicate significant correlations (R2>0.20, p<0.05). Codes for each species are provided in Appendix A.

EUST-RNSA). All other correlations were weak and insigni®cant. As with the guild level analysis, negative correlations were observed between some of the WPCNs (e.g. RBNU) and PCNs and SCNs. The central message from this analysis is that the same relationships observed at the guild level are found at the species level. The strong links in the web clearly appear to be those between the PCNs and SCNs. Interactions with the WPCNs, in contrast, are typically weak and often negative. 4.4. Resource availability and use: Nest flow The above analyses construct the nest web on the basis of species associations or correlations. It is possible, however, to adopt a more functional approach by examining `nest ¯ow'; that is, determining which species make most of the cavities (and in what trees) and which species then use these cavities. The species of trees that are most important to cavitynesting birds are shown in Fig. 6(a). Lodgepole pine (Pl) was the most abundant species on our study area, followed by trembling aspen (At), Douglas Fir (Fd), hybrid spruce (Sx), white spruce (Sw) and jackpine (Pj). However, almost all of the active cavity nests were found in aspen, with only a small number in lodgepole pine and Douglas Fir. Aspen was selected

Fig. 6. (a) Tree species available (shaded) and used (filled) for nesting on 16 study sites in north-central British Columbia in 1995 and 1996 (Nˆ201 nests). Tree species codes: lodgepole pine (Pl), trembling aspen (At), Douglas Fir (Fd), hybrid spruce (Sx), white spruce (Sw) and jackpine (Pj). (b) Frequency of nest cavities created by species of primary and weak primary cavity excavating birds; Bird species codes provided in Appendix A, Nat ± natural hole, ? ± species creating the cavity not determined; (Nˆ201 nests).

disproportionately to its availability by all species of cavity-nesting birds, and appears to be the key species for nesting. The relative contributions of each of the cavity excavators are shown in Fig. 6(b). Two species, namely red-naped sapsucker (RNSA) and northern ¯icker (NOFL) created about 74% of all cavities used and 90% of the 79 nests used by SCN where we could determine the creator of the cavity. Very few nests were found in cavities created by the other primary cavity-excavating species, such as pileated wood-

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Table 3 Correlation coefficients of the abundance of each guild (based on point counts) with habitat characteristics in each study plot

1995 (Nˆ11 plots) % Fragmented % Wet % Edge % Deciduous 1996 (Nˆ11 plots) % Fragmented % Wet % Edge % Deciduous *

Fig. 7. Nest flow in the nest web as measured by the proportion of trees or cavities used by cavity-nesting species in north-central British Columbia in 1995 and 1996. Lines connect species that use resources provided by the species below. The sample size for the SCN level is 79 nests, the WPCN level is 34 nests, the PCN level is 82 nests and the tree level is 195 nests. See text for details.

pecker (PIWO), hairy woodpecker (HAWO), downy woodpecker (DOWO), or three-toed woodpecker (TTWO). Likewise, few cavities were produced by the weak cavity excavators (red-breasted nuthatch (RBNU), mountain chickadee (MOCH) and blackcapped chickadee (BCCH)), although nuthatches created relatively more cavities than several of the primary cavity species (Fig. 6(b)). About 7.5% of nests were located in natural cavities (NAT). Given our study design and logistics, our data currently underestimate the importance of natural holes for SCNs. In Fig. 7, we summarize these relationships by determining the proportion of trees or cavities used or created by each species in the nest web. From this analysis, the linkage and interdependence among species becomes clear. Aspen is the key tree species used by virtually all primary cavity species. Northern ¯icker and RNSA are the two critical primary cavity excavators, although the importance of each species varied among SCNs (e.g. TAHU and TRES nests were found more often in cavities created by RNSA, and MOBL, EUST and BUFF depended more on NOFL cavities). Although some of the less common cavity excavators (PIWO, HAWO) do not make a large number of cavities, they were essential in creating cavities required by certain species (e.g. NSOW).

p<0.05,

**

p<0.01,

PCN

WPCN

SCN

NONCAV

0.66* ÿ0.20 0.68* 0.51

ÿ0.55 0.15 ÿ0.52 0.40

0.70* ÿ0.22 0.77** 0.63*

ÿ0.03 0.57 ÿ0.09 ÿ0.42

0.67* ÿ0.03 0.68* 0.44

ÿ0.49 0.55 ÿ0.37 ÿ0.55

0.69* ÿ0.35 0.79** 0.64*

0.05 0.51 ÿ0.06 ÿ0.34

***

p<0.001.

WPCNs relied more on natural cavities or excavated their own in aspen. 4.5. Habitat correlates To determine how forest habitat affects the structure of the nest web and its components, we examined correlations between the abundance of each guild and several habitat variables (Table 3). There were signi®cant positive correlations between the abundance of PCNs and the percentage of the plot that was fragmented and the percentage of edge (Table 3). The abundance of SCNs was likewise correlated with these variables and also with the percentage of deciduous trees. In contrast, there were no signi®cant correlations with any habitat variable for either WPCNs or NONCAVs. In fact, many of the correlations for these two guilds were in the opposite direction to those for PCNs and SCNs. 5. Discussion 5.1. Community structure on the study site The Chilcotin region of north-central British Columbia represents an area of high vertebrate species richness. The assemblage of cavity-nesting birds and mammals is among the richest reported in the province and in North America generally. Our sites contain eight species of woodpeckers living sympatrically out of a total of 12 species resident in the province

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(Campbell et al., 1990). Short and Horne (1990) report that four to ®ve sympatric species are typical of nontropical regions of North America and Eurasia, but up to eight species may occur where trees are diverse. However, the tree community in our region is relatively simple compared to other local biogeoclimatic regions. The total number of species (32) of cavitynesting birds on our sites is also exceptionally rich compared to other sites in North America and Europe. Most studies do not survey or consider the entire cavity-nesting community, thus, direct comparisons of species richness or abundance and nest web structure of our site with others is problematic. Li and Martin (1991) report 14 species of cavity-nesting birds in mixed deciduous and coniferous forest in Arizona (six excavators and nine non-excavators (SCNs and WPCNs combined)). Dobkin et al. (1995) indicated that cavity-nesting birds comprise almost 50% of all breeding birds in riparian sites in the Great Basin of Oregon but mention only 10 species of cavity nesters. In our census data, 25 of the 76 species of breeding birds on our sites were cavity-nesting birds. Compiling comparative data about the complexities of the nest web is also dif®cult. In Europe, Johnsson et al. (1993) indicate that 12 species of vertebrates use the holes of the black woodpecker (Dryocopus martius) in Sweden. Across Norway, seven species of woodpeckers produce holes that are used by 21 species of SCN birds and mammals, but not all species live sympatrically (Aanderaa et al., 1996). 5.2. The structure of the nest web Analyses at both guild and species levels, using independent data sets (point count census and nest

counts) and conducted over 2 years indicate consistent relationships among the species in the cavity-nesting community. The positive association between PCNs and SCNs was highly repeatable and statistically signi®cant in all analyses. This is in accord with our predictions based on the premise that SCNs require cavities created by PCNs (Table 4). While this relationship may seem intuitive, surprisingly few studies have demonstrated this link empirically, usually because most studies focus only on one of these guilds. PCNs and SCNs were also the only guilds that exhibited strong associations with any of the habitat variables (Table 3). Thus, the nest web on our study area appears to be structured strongly around the interactions among these species (Figs. 4 and 5). In contrast, WPCNs were less predictable, only weakly associated with measured habitat variables and negatively correlated with both PCNs and SCNs. This result was unanticipated and contradicts our expectation that WPCNs would be positively correlated with PCNs and SCNs (Table 4). The different response of WPCNs reveals substructuring among the cavity-nesting guilds and highlights the need to consider WPCNs separately from SCNs. Unlike most studies of cavity-nesting birds, we also considered relationships with NONCAV species. As predicted (Table 4), we found few signi®cant relationships of NONCAVs with cavity-nesting species, indicating that patterns of abundance on our study plots were not simply an artifact of variation in habitat quality. For example, positive associations among species could be explained if some plots were simply poor habitat while others were of excellent quality, resulting in sites depapurate or rich in species, respectively. Monitoring the abundance of NONCAV species

Table 4 Summary of predicted and observed relationships between guilds of cavity-nesting birds Predicted relationship

Observed relationship

Conclude

PCN±SCN PCN±WPCN

‡‡ 0 or ‡

‡‡ ±

SCN±WPCN

0 or ‡

±

CAV±NONCAV

0 or ÿ

0 or ÿ

Strong dependence of SCN on PCN Surprising; suggests no facilitation; perhaps competition or different habitat preferences Also surprising; no facilitation; competition or different habitat preferences Patterns found for other guilds are not confounded by selection of plots, habitat effects, etc. (serves as control); negative correlation with SCNs may be due to competition or different habitat preferences

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allowed us to test, and reject, this possibility. One surprising result was the signi®cant negative correlation between NONCAV species and SCNs (Table 2; Fig. 4). This may simply re¯ect different habitat preferences, although the abundance of PCNs did not covary with NONCAVs in the same manner, as might be expected. Alternatively, the negative correlation among these guilds may be due to the competition for invertebrate prey (Bock et al., 1992). Many of the SCNs rely on insects and invertebrates for food, as do several of the NONCAV species. Bock et al. (1992) reported that experimental increases of cavity-nesting birds (via addition of nest boxes) resulted in a signi®cant reduction of NONCAV birds on a study site in Arizona. Admittedly, many of our analyses are correlative and the links demonstrated (e.g. Fig. 5) are not necessarily functional or causative. However, the consistent patterns illustrated in both years, using either point count census or nest counts, suggest that the structure of the nest web re¯ects real biological patterns. Moreover, an analysis of nest use by each of the cavitynesting species (Fig. 7) demonstrates directly the functional relationships between PCNs and certain tree species, and between SCNs and certain PCNs. The results reported here are preliminary and serve to illustrate our technique. We need to resolve the problems of sampling diverse taxa occurring at different spatial scales. Our web structure will become more complex (Figs. 5 and 7) as we devote more time to nest searching, and locate nests for a greater number of species. For example, there are abundant numbers of American Kestrels breeding on our sites, but we located our ®rst nests in 1997. The forest owls, bats and ducks are not adequately sampled at present, but we initiated work on these groups in 1997. Here, we present data only for the breeding season, but there are winter dimensions to the nest web. In late summer, we observed signi®cant sequential use of our nesting cavities. In fall and winter, there is proportionately stronger representation by WPCNs and cavity-nesting mammals. Despite at least eight tree species on our plots, over 95% of the nests we located were in aspen trees and this result held for all species. The strong and nonrandom use of aspen in relation to its availability is a common result for woodpecker studies in British Columbia (Harestad and Keisker, 1989; Steeger et al.,

253

1996) and elsewhere for cavity nesters generally (Li and Martin, 1991; Dobkin et al., 1995). However, the situation is reversed for foraging. For three studies of woodpeckers in British Columbia, totalling 945 observations of foraging, over 75% of the trees used were conifers (®r, pine, and larch; Steeger et al., 1996). Clearly, management for cavity-nesting birds requires a full consideration of their life history requisites rather than a survey of the trees used for nesting. The effects of fragmentation of landscapes for wildlife species have been an issue in both Europe and North America, with an emphasis on identifying whether adverse effects of fragmentation occur (Opdam, 1991; Schmiegelow et al., 1997). Negative edge effects are often highlighted as the factor responsible for the apparent declines of neotropical songbirds in the highly fragmented forests of the eastern United States (reviews by Askins et al., 1990; Robinson and Wilcove, 1994). There has been particular concern with respect to forestry activities (Angelstam and Mikusinski, 1994). In most forested landscapes in central and western North America, however, negative edge effects have not been strongly evident, especially in landscapes with a matrix of young and old forest (Walters, in press.). In our study, we demonstrated a positive edge effect on abundance of both PCNs and SCNs and a negative effect of edge for WPCNs (Table 4). This relationship may be driven by our 11 plots on the Riske Creek site which represent a largely natural fragmented landscape matrix of grassland, pond and forest. Equally interesting is the negative effect of edge for WPCNs, especially for the BCCH a species characterized generally as being more common near woodland edge (Smith, 1993). The association of chickadees with forest interior in this study may constitute indirect support for the hypothesis that WPCNs are inferior competitors with other cavity-nesting guilds (PCNs, SCNs) for the rich riparian habitats associated with forest edge. 5.3. Nest webs and managed forests Most woodpecker species use trees to perform their daily activities of nesting and foraging and communication, and are assumed to be sensitive to extensive forest harvesting (Winkler et al., 1995). In northern Europe, managed forests with little structural or compositional diversity have replaced the once vast boreal

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forest. Large scale declines and local extirpation of woodpecker populations in these managed forests have been observed (Angelstam, 1990; Angelstam and Mikusinski, 1994). Less information is available for the status of the associated SCNs. For most species of woodpeckers in western North America, restricted ranges appear to be most strongly associated with degree of endangerment, but there is strong concern about the impact of forestry activities. Extensive clearcutting of mature forest is likely to result in a simpler assemblage of cavity nesters. In a montane spruce forest site in eastern British Columbia, the cavity nester assemblage comprised two species of PCN and four species of SCN in a matrix of clearcut patches interspersed with old forest (Holt and Martin, 1997). All species had low abundance. In that study, data were lacking on the pre-harvest condition. The recent Forest Practices Code in British Columbia has established guidelines for harvesting that aim to retain existing ecological assemblages of forest wildlife. With our experimental cut plots, we hope to separate what cavity nesters prefer to use in unharvested forests (presented above) from what trees they can and will use for both nesting and foraging in managed forests. On all sites, the riparian habitats immediately around streams containing mostly deciduous trees will be retained. The results presented here suggest a suf®cient supply of trees for nesting would be retained for PCNs and SCNs in these riparian strips. However, in a clear cutting scenario, WPCNs are likely not to fare well due to the limited nest sites in interior forest and PCNs would lack conifers for foraging. Other studies demonstrated a strong use of ®r for foraging, but only limited use of spruce and pine. Hence, with selective harvesting where all the aspen and Douglas Fir will be retained together with some pine and spruce, most needs of all cavity-nesting guilds may be met. We will examine the harvesting levels at which cavity-nesting birds suffer direct ecological costs, and whether the costs are borne by one or a few species. If we observe costs to key species, we predict the impact will show an ecological cascade through the community. 6. Conclusion: The value of a nest web perspective Our central thesis is that cavity-nesting bird communities exist in a structure directly analogous to food

webs, with a clear hierarchy of producers and consumers. We contend that there are several advantages of such a perspective. First, a nest web analysis reveals the kinds of interactions (links) that might exist among all the species in the community. Too often, attention is focused only on single or several species in these communities (e.g. woodpeckers, or certain secondary nesters), with the result that key relationships with other species in the community are ignored, misunderstood or mismanaged. Applying a nest web perspective allows a broader community focus that is feasible to test. Secondly, nest web analysis explicitly outlines the direct and indirect links and interactions that must be detailed before one can predict how the community would respond to perturbations or change. By metaphor, imagine that the species in Fig. 5 are connected by ecological `rubber bands,' the strength of which is dictated by the value of the correlation coef®cient. What happens when one band is stretched or cut? Answering such a question in the real world is a complex undertaking and adopting a nest web perspective offers one method to begin such a task. We recognize that many of the analyses in the present study are correlative, and do not imply functional links. However, this is a useful ®rst step and we might view these correlations simply as hypotheses that could be tested by future studies using experimental approaches and detailed demographic data. Alternatively, more sophisticated statistical approaches such as path analysis might be employed to partition the strong and weak, and direct and indirect pathways. In either case, a nest web perspective forces one to outline explicitly all of the species that comprise the web and to hypothesize the links that might exist between them. Thirdly, analysis of the community as a nest web may help to identify keystone species or keystone interactions. For example, our analyses showed that trembling aspen was a critical species in providing nesting trees to cavity-nesting birds. Likewise, RNSA and NOFL were keystone cavity excavators upon which most (but not all) of the SCN species relied. Given the strengths of these interactions, we can better anticipate the response of the community to forest management practices that might impact these key species. Finally, an important value of the nest web approach is that we can appeal to existing ecological theory on

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255

Appendix A. Cavity-nesting species present at the study sites in north-central British Columbia Code

Common name

Scientific name

Primary cavity nesters Woodpeckers NOFL RNSA PIWO DOWO HAWO TTWO BBWO RBSA

Northern flicker Red-naped sapsucker Pileated woodpecker Downy woodpecker Hairy woodpecker Three-toed woodpecker Black-backed woodpecker Red-breasted sapsucker

Colaptes auritus Sphyrapicus nuchalis Dryocopus pileatus Picoides pubescens Picoides villosus Picoides tridactylus Picoides arcticus Sphyrapicus ruber

Weak cavity excavators RBNU MOCH BCCH BOCH

Red-breasted nuthatch Mountain chickadee Black-capped chickadee Boreal chickadee

Sitta canadensis Parus gambeli Parus atricapillus Parus borealis

Secondary cavity nesters Insectivorous birds MOBL EUST TRES VGSW BRCR HOWR VASW

Mountain bluebird European starling Tree swallow Violet-green swallow Brown creeper House wren Vaux's swift

Sialia currucoides Sturnus vulgaris Tachycineta thalassina Tachycineta bicolor Certhia americana Troglodytes aedon Chaetura vauxi

Ducks COGO BAGO BUFF COME HOME

Common goldeneye Barrow's goldeneye Bufflehead Common merganser Hooded merganser

Bucephala clangula Bucephala islandica Bucephala albeola Mergus merganser Lophodytes cucullatus

Birds of prey AMKE NSOW GHOW NPOW BAOW BOOW FLOW NHOW

American kestrel Northern Saw-whet owl Great horned owl Northern pygmy owl Barred owl Boreal owl Flammulated owl Northern hawk owl

Falco sparverius Aegolius acadicus Bubo virginianus Glaucidium gnoma Strix varia Aegolius funereus Otus flammeolus Surnia ulula

Mammals TAHU GLSA MYEV MYLU MYVO MYUV LACI LANO EPFU PLTO ANPA

Red squirrel Northern flying squirrel Western long-eared myotis Little brown myotis Long-legged myotis Yuma myotis Hoary bat Silver-haired bat Big Brown bat Townsend's big-eared bat Pallid bat

Tamiasciurus hudsonicus Glaucomys sabrinus Myotis evotis Myotis lucifugus Myotis volans Myotis yumanensis Lasiurus cinereus Lasionycteris noctivagans Eptesicus fuscus Plecotus townsendii Antrozous pallidus

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food webs to predict the structure, stability and resilience of these communities (e.g. Pimm, 1980; Warren, 1990; Waltho and Kolasa, 1994; de Ruiter et al., 1995). Although debate continues on the properties of food webs and their relationship to ecosystem function, analysis of nest webs offers both an opportunity to test the food web theory in a new and perhaps more tractable system, and grounds the study of cavitynesting bird communities ®rmly within the foundations of ecological theory. Acknowledgements We acknowledge the able assistance of ®eld workers, S. Taylor (project manager), L. Elliott, and E. Voller. This project was supported by Natural Resources and Engineering Research Council of Canada research grants to K. Martin (University of British Columbia) and to J. Eadie (Univ. of Toronto), research grants from the Canadian Wildlife Service (K. Martin) and the Dennis Raveling Waterfowl Endowment and Agricultural Experiment Station (University of California, Davis) to J. Eadie. We also gratefully acknowledge Forest Renewal British Columbia research support from grants shared with F. Cooke (Simon Fraser University), and S.M. Glenn (University of British Columbia) and invaluable logistical assistance was provided by Dave Conly and Shawn Meisner, Lignum Limited (Williams Lake, British Columbia). Dan Gilmour (Canfor Forest Products Ltd., Alberta), D.J. Huggard and two anonymous reviewers did thoughtful and thorough reviews. Some of the ideas that motivated this research arose from discussions with J. Elmberg and P. Lundberg. References Aanderaa, R., Rolstad, J., Sognen, S.M., 1996. Biological Diversity in Forests, Norges Skogeierforbund og A/S Landbruksforlaget, p. 112. Angelstam, P., 1990. Factors determining the composition and persistence of local woodpecker assemblages in taiga forest in Sweden ± A case for landscape ecological studies. In: Carlson, A., Aulen, G. (Eds.), Conservation and Management of Woodpecker Populations, Swedish University of Agricultural Sciences, Department of Wildlife Ecology, Report 17, Uppsala, Sweden.

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