EFFECTS OF HABITAT DISTURBANCE ON REPRODUCTION IN BLACK-CAPPED CHICKADEES (POECILE ATRICAPILLUS) IN NORTHERN BRITISH COLUMBIA

Fort, Kevin T

ABSTRACT. –

Avian species that persist in breeding in disturbed habitats are often thought to be less affected by disturbance than habitat specialists lost following disturbances, yet there is growing evidence that human-altered environments may negatively affect reproductive behavior and nest success of those generalists as well. We compared nest success of Black-capped Chickadees (Poecile atricapillus) in two adjacent habitats: a mature mixed-wood forest (undisturbed) and a forest regenerating after logging (disturbed). Despite similar breeding densities, proportion of nests that successfully fledged young was lower in the disturbed habitat than in the undisturbed habitat. Abandonment was the most common cause of nest failure. A within-habitat comparison of the social rank of birds revealed that low-ranking birds had lower nest success than high-ranking birds in the disturbed, but not in the undisturbed, habitat. Clutch size and brood size of nests that progressed to the point of hatch did not differ significantly between habitats. Average total number of fledglings produced per pair, though not significantly different, was suggestively lower in the disturbed habitat. Across habitats, nests situated in snags with lower amounts of internal decay were more successful. Successful nests were also located in sites with higher canopy height, low understory density below 1 m, and higher understory density between 2 and 3 m-all attributes generally associated with undisturbed, mature forests in the region. Our results provide evidence that disturbed habitats may represent poor-quality habitat for this forest generalist, and that habitat quality differentially affects individuals, depending on their dominance rank. Received 15 January 2003, accepted 12 May 2004.

RÉSUMÉ. -Les espèces aviennes qui persistent à se reproduire dans des habitats perturbés sont souvent considérées comme moins affectées que les espèces spécialistes en terme d’habitat. Néanmoins, il semble que les espèces généralistes puissent être également affectées dans leur comportement reproducteur et leur succès de nidification au sein d’un environnement perturbé par l’Homme. Nous avons comparé le succès de nidification de Mésanges à tête noire (Poecile atricapillus) dans deux habitats adjacents: une forêt mature mixte (non perturbée) et une forêt en régénération après coupe (perturbée). Malgré des densités de nidification semblables, la proportion de nids avec éclosion était plus faible dans les habitats perturbés que dans les habitats non perturbés. L’abandon du nid était la cause la plus courante pour expliquer les échecs de nidification. Une comparaison intra-habitat du rang social des oiseaux a révélé que les oiseaux de bas-rang avaient un succès de nidification plus faible que ceux de haut-rang dans les habitats perturbés. Ce n’était pas le cas dans les habitats non perturbés. Les tailles de ponte et de couvée des nids avec éclosion ne différaient pas de manière significative entre les habitats. Le nombre total moyen d’oisillons produit par couple, bien que non significativement différent, était plus faible dans les habitats perturbés. Au sein des différents habitats, les nids situés dans les chicots les moins décomposés étaient les plus productifs. Les nids avec éclosion étaient également situés dans les sites avec une plus grande hauteur de canopée, une plus faible densité de sous-couvert inférieure à 1 m et une plus grande densité de sous-couvert entre 2 et 3 m. Des caractéristiques qui sont généralement associées aux forêts matures et non perturbées de la région. Nos résultats apportent la preuve qvie les habitats perturbés peuvent représenter des habitats de faible qualité pour les espèces généralistes. Par ailleurs, les individus sont affectés de manière différentielle par la qualité de l’habitat selon leur rang de dominance.

EFFECTS OF HABITAT disturbance on reproductive success of forest songbirds are typically studied at the community level and determined by presence-absence census methods (Schmiegelow et al. 1997). Single-species studies tend to focus on habitat specialists (i.e. species with rigid habitat requirements), because they are most likely to respond negatively to habitat disturbance (Bayne and Hobson 2001). Conversely, habitat generalists (i.e. species with broad habitat requirements) are more likely to persist in habitats that are anthropogenically disturbed. Such habitats, however, may differ in availability of resources needed for successful reproduction; thus, disturbed areas may represent habitat of varying quality to birds (Zanette 2001, Chase 2002, Tarvin and Garvin 2002). Habitat quality can ultimately be measured in terms of reproductive output (Muller et al. 1997), but factors contributing to habitat quality are various and include degree of predation risk, availability of food resources, and access to suitable nest locations and microhabitats.

Assessing effects of habitat disturbance on a population by using presence-absence methods alone can be misleading. Specifically, if a disturbed environment is low-quality habitat for a breeding population, reproductive output may be diminished, despite breeding densities similar to those of populations breeding in undisturbed habitats. This reduced reproductive output might result from reproductive decisions by animals breeding under suboptimal and stressful conditions. A number of studies have shown that birds breeding in poor-quality territories will compensate for decreased resources by adjusting clutch size downward (Dhondt et al. 1990, 1992; Slagsvold and Lifjeld 1990). However, birds experiencing extremely stressful conditions may opt to forgo breeding altogether if the perceived survivorship risk is too high, as compared with the potential fitness benefit of a successful nest. How birds respond to variation in environmental quality may be condition-dependent; low-quality individuals may be forced to settle in poorer-quality habitats or, if settlement is random, may suffer disproportionately to high-quality individuals in those habitats (Fretwell and Lucas 1970). Regardless, such mechanisms may ultimately have population-level consequences if large portions of the population are breeding in low-quality, disturbed habitats.

The Black-capped Chickadee (Poecile atricapillus), a resident cavity-nesting songbird, is known to breed in fragmented and otherwise disturbed habitats (Smith 1991). Although its breeding behavior in relatively undisturbed woodland habitats has been well studied (Otter et al. 1999), effects of breeding in disturbed habitats are not well understood. If disturbed areas are low-quality habitat for Black-capped Chickadees, we predict that reproductive success should be lower there, as compared with adjacent undisturbed areas. Reduced reproductive success may manifest as a decrease in clutch or brood size or, alternatively, an increase in the rate of nest abandonment. Given that dominance rank is known to influence reproductive success and reproductive decisions in this species (Smith 1991; Otter and Ratcliffe 1996; Otter et al. 1998, 1999), reproductive strategies based on social ranks may interact with habitat effects to influence overall reproductive success of populations. For instance, breeding in low-quality habitats may differentially affect high- and low-ranking birds if competitively superior high-ranking birds are able to secure better breeding territories. If breeding success is reduced in disturbed habitats, it may be attributable to resource limitation or, alternatively, increased predation rates in those areas. Structural features of the habitat are likely correlated with resource availability; thus, if breeding success is being lowered through that mechanism, we would expect to find associations between critical habitat-structure variables and a measure of breeding success. Furthermore, we should expect to find that structural features associated with nest success are less available in low-quality habitats.

METHODS

Study area. – The study was conducted immediately west of the University of Northern British Columbia, Prince George (53°55’N, 122°50’W; 850 m elevation), within the Sub-boreal Spruce biogeoclimatic zone. The study area comprised two adjacent habitat types: (1) an 85-ha block of mature forest and (2) two sites (total area 85 ha) that have been disturbed as a result of forest-management practices (Fig. 1). The undisturbed habitat is a continuous forested area composed of patches of various mature-forest types. Canopy species represented are trembling aspen (Populus tremuloides), paper birch (Betula papyrifera), black cottonwood (P. balsamifera ssp. trichocarpa), hybrid spruce (Picen glauca × Pi. engelmannii), lodgepole pine (Pinus contorta), Douglas-fir (Pseudotsuga menziesii), and subalpine fir (Abies lasiocarpa). Canopy height is 25-30 m. Understory stratum is dominated by green alder (Alnus crispa), willow (Salix sp.), prickly rose (Rosa aacularis), low-bush cranberry (Viburnum edule), and twinberry (Lonicera involucrata).

The primary disturbed site (~75 ha) was logged in 1962 and cleared to agricultural standards for horse and cow pasture. The site was designated a model working forest in 1985, and many areas were cleared and replanted with lodgepole pine and other conifers between 1986 and 1989. Other sites regenerated naturally, and still others were never harvested. Consequently, the disturbed habitat is characterized by a mosaic of young managed lodgepole pine stands, somewhat older aspen-birch-willow stands, and isolated patches of mature forest. Although species composition is similar to that of the undisturbed site, canopy height is lower (5-15 m), there are fewer large trees, and there is a much larger understory component. Where small patches of mature forest exist, they are similar in composition and structure to the undisturbed site. However, they exist as isolated patches of 1-4 ha in the surrounding landscape. None of the birds classified as settling in disturbed habitat were able to establish territories exclusively in those patches. In all cases, the majority of the territory of any bird classified as breeding in disturbed habitat consisted of various early-serai habitat types. The smaller disturbed site (~9 ha) is a stand of mature birch that has been subjected to selective harvesting practices, which left many trees standing. As a result, canopy height is similar to that found in the undisturbed site, but canopy cover is drastically reduced, and there is a more pronounced understory component.

Study species. – The Black-capped Chickadee (hereafter “chickadee”) is a small (~11 g) resident songbird. Chickadees are territorial during the breeding season (mid-April to early July locally), but forage and travel in small flocks consisting of two to five mated pairs during most of the nonbreeding season. During most of the year, chickadees consume a mixed diet of seeds, berries, and invertebrates, but they switch to a completely insectivorous diet during the breeding season (Smith 1991).

Weak cavity excavators, chickadees nest in hardwood snags, dead limbs, or knot-holes of live trees. Thus, they are dependent on significant densities of trees or snags with advanced decay and have evolved primarily in mature forests of North America. However, the species is known to breed in fragmented and otherwise disturbed habitats (Smith 1991), and preliminary investigations revealed that population densities in disturbed and undisturbed portions of our study site were roughly equivalent.

Nest sites are chosen in late April, at which time both pair members excavate the nest cavity. Egg-laying in our study site commenced during the first or second week of May. One egg is laid daily until the clutch is complete (average clutch size is six eggs in the study area). Incubation begins on the day prior to laying of the last egg and lasts for a period of 12-13 days (Smith 1991). Only the female incubates the eggs, though the male will devote considerable effort to feeding the female at the nest during incubation.

Once the eggs hatch, both sexes deliver food to the nestlings, though the female will also spend much of her time in the nest cavity, especially when fledglings are young and unable to thermoregulate effectively. Fledging typically takes place 16 days after hatch, though disturbance at the nest after day 13 will likely trigger an early fledge. In our study area, most nests fledged in mid- to late June, though a few nests did not fledge until early July.

Postfledge dispersal takes place in late summer through early fall. Newly independent birds disperse in random directions from the natal area, visually settling a few kilometers from the nest site as low-ranking members of winter flocks (Smith 1991). This is the primary dispersal phase of the species, and although recapture of nestlings after dispersal is low, our banding records show that nestling dispersal is not habitat specific: nestlings born in undisturbed habitats have been found in the disturbed site, and vice versa (K. Fort and K. Otter unpubl. data). Following that initial settlement, movement between sites is extremely uncommon in this sedentary species.

Chickadees maintain a rigid social hierarchy in winter flocks, which can be used as a measure of male resource-holding potential (Ficken et al. 1990). Because the species is resident year-round, dominance rankings of color-banded birds can be determined in the nonbreeding season by observing aggressive interactions at winter feeders (Ficken et al. 1990).

Winter banding and dominance assessment.-We captured adult chickadees at established feeding stations using box (Potter) traps mounted on platform feeders and banded them during December through February of both years. The banding protocol consisted of applying one numbered aluminum band (under Canadian Wildlife Services license) and three color plastic bands. Each bird was given a unique color combination, which allowed us to identify individuals from a distance. At time of banding, body measurements were taken (length of rectrices, flattened wing chord, and mass). Sex of the bird can be determined with 90% accuracy at time of banding, using a combination of those three measures (Desrochers 1990); we confirmed those sex determinations by observing behavior during the breeding season. We determined age of birds by examining the shape of rectrices (Meigs et al. 1983). Birds were classified as either second-year (SY; i.e. entering their second calendar year and therefore approaching their first breeding season) or after-second-year (ASY; i.e. entering their third or later calendar year and second or later breeding season).

After banding the birds, we assessed dominance ranks by monitoring aggressive interactions between birds at winter feeding stations. A bird was considered dominant to another if it “won” the majority of dyadic interactions. Three behaviors were used to assess dominance. If (1) a focal bird supplanted or chased away its opponent, (2) the focal bird gave a display that elicited a submissive posture in an opponent, or (3) the opponent waited for the bird to leave before approaching a feeder (Picken et al. 1990, Otter et al. 1998), the focal bird was considered dominant to its opponent. We determined flock membership by observing patterns of feeder use and by tracking foraging activities throughout the flock’s range. We collected those data vising a voice-activated recorder (Optimus CTR-116, Tandy, Fort Worth, Texas) at a distance ≥10 m from the station to minimize the risk of influencing feeding behavior. A linear dominance matrix was determined for each flock; birds were classified as low-, mid-, or high-ranking, depending on their position within the flock. Because the female chickadee’s rank is correlated with the rank of her social mate (Smith 1991, Otter et al. 1999), we concentrated on determining relative rank of males within flocks. In flocks consisting of three pairs, the male submissive to the alpha male but dominant over the low-ranking male was considered mid-ranking. No flocks consisting of more than three mated pairs were observed in the study area over the course of the two-year study period. In flocks consisting of two mated pairs (the most common flock size in our study area), the dominant male was assigned the high rank, and the other male was considered low-ranking. This relative ranking system is likely a more biologically accurate measure than absolute ranks, because highranking birds from one flock tend to dominate lowranking individuals from other flocks. We occasionally had the opportunity to record interactions between birds that ultimately settled in different treatments. In those instances, high-ranking birds in disturbed habitat were consistently dominant to low-ranking birds in undisturbed habitat (Fort and Otter 2004).

In early spring (prior to flock breakup) of the first year, we created a 50 χ 50 m grid system in the undisturbed habitat and marked grid points with flagging tape. All grid points were recorded using a Geoexplorer III (Trimble, Sunnyvale, California) handheld global positioning system (GPS) unit. Thus, location of bird observations and territory boundaries in relation to aerial photos of the study site could be determined later with a high degree of accuracy. We also marked locations of specific landmarks in either habitat; the geographical information system (GIS) images could thus be superimposed onto satellite images of the area to give a high degree of accuracy in marking animal movements. It was unnecessary to establish a grid system in the disturbed habitat, because existing trails and other landmarks were sufficient for determining locations of territory boundaries and nest sites with accuracy comparable to that in the grid-marked undisturbed site.

Breeding season. -After the breakup of flocks in early spring, the authors and two field assistants conducted surveys of the study area daily from 0800 to 1600 hours to determine settling patterns, territorial boundaries, and nest locations. Territorial boundaries were determined by recording locations of territorial disputes between neighboring males, male singing posts, and the geographical extent of foraging bouts by mated pairs. During that period, mated pairs will excavate nest cavities; we recorded and monitored those sites to determine when pairs initiated incubation. All nest sites were marked with flagging tape at a random distance (≥5 m away) and direction (indicated on the marker flag to facilitate relocation of the nest) from the actual cavity tree to minimize the risk of attracting potential nest predators. We also maintained a distance of >5 m from the nest during all monitoring activities.

Once a nest site had been determined, it was monitored every 3-4 days for changes in status (i.e. excavation, nest lining, egg laying, incubation, hatch, fledge). Change in nesting status can often be determined (within a range of accuracy of 1-2 days) by noting certain characteristic behaviors. During the nest-lining phase, females will bring nesting materials, such as animal hair or dried plant parts, to the cavity. The egg-laying phase is accompanied (a few days prior to onset) by use of the “broken dee” call by the female (D. Mennill pers. comm.). Once incubation begins, the female spends the majority of her time within the cavity, and the male feeds the female at the nest entrance. After the eggs have hatched, both male and female feed the young, though the female still spends much of her time brooding within the cavity. However, when the male arrives with food, the female will often leave the cavity to allow the male to enter, feed the young, and remove any fecal sacs.

On or around day 7 post-hatch, we visited all accessible nests to band nestlings. We were able to gain access to most nests by using a 10-rn extension ladder or a tree-climbing belt, or with the help of a professional tree-climber. At the nest cavity, we used a small saw to cut a square portal in the side of the tree several centimeters above the level of the nest cup. Whenever possible, chicks were removed in two stages to minimize risk of nest abandonment (no nests were abandoned as a result of our activities). We enumerated nestlings and examined the nest cup for unhatched eggs. Once the nestlings were returned to the nest, the portal was re-inserted and secured with tape. (We monitored inaccessible nests from the ground to determine whether a successful fledge took place.)

Using the methodology just described, we determined clutch size (number hatched + number unhatched eggs is a valid measure, because chickadees are not known to remove unhatched eggs or dead nestlings; Otter et al. 1999), brood size, and proportion hatched (number hatched/clutch size). We defined a successful nest as one that was still active at day 14 post-hatch; although fledging does not normally take place until day 15 or 16, any disturbance in the vicinity of the nest on or beyond day 14 will trigger fledging. We classified failed nests according to cause of failure (abandonment, nest predation, weather event) whenever possible. Nest predation events could be determined easily, because local nest predators -red squirrels (Tainiasciitnis hudsonictis), pine martens (Mustela martes), and, in one instance, a young black bear (Ursus nniericaiius) – leave signs of forced entry in and around the cavity entrance. Abandoned nests were further classified according to nesting phase (pre-incubation, incubation, or nestling) during which abandonment occurred.

Vegetation sampling protocol. – Nest-site habitat characteristics were assessed using, at each established nest site, a 0.04-ha (11.3-m-radius) circular plot centered on the cavity tree. Vegetation sampling took place within two weeks after fledging. Given that the vegetation is fully developed well before time of fledging, our vegetation plots should accurately reflect habitat conditions at the nest during the nestling phase. We recorded species of the cavity tree, its height (using a clinometer) and diameter at breast height (DBH), nest height, and cavity type (top or side entrance, knot-hole, or branch). We also recorded species and DBH (in six size classes) of each live tree in the plot. Height, species, and DBH of a representative canopy tree were also recorded. We measured canopy cover using a convex densiometer at the edge of the plot in the four cardinal directions. For all snags within the plot, we recorded species, DBH size class, height, and decay class. We assessed the understory component by estimating overall percentage of cover (in seven cover classes) of all shrub species (including young trees) at four vertical height classes (0-1, 1-2, 2-3, and 3-4 m).

Statistical analyses. -We used G-tests to determine if nest success (whether a pair successfully fledge at least one nestling in a season) differed between disturbed and undisturbed nests, between high- and low-ranking birds, and between years, and to assess whether birds responded differentially by rank within each habitat type. When cell frequencies were too low, we used Fisher’s exact tests. Because rank is known to influence reproductive output (Otter et al. 1999), we included rank as an additional factor in analyses of nest data. Two-factor ANOVA was used where assumptions were met. Poisson multiple regressions were used for count variables. Year was included as a factor in Poisson and ANOVA models. If annual variation was detected in ANOVA analyses, we standardized the data by determining the average value of the variable for each year and then expressed the data as a deviation from the yearly average (Otter et al. 1999). Because incubation date was not distributed normally and is known to be highly correlated with rank (Smith 1991), a nonparametric comparison of high-ranking birds only was used to control for that factor.

We employed backward-stepwise multiple-logistic regression to determine which, if any, variables were predictive of nest success, in terms of cavity-tree and nest-plot characteristics, irrespective of overall habitat type. Such analysis allows differentiation of success based on microhabitat, within larger landscape categories. Data were collected from 69 nest plots in 2000 and 2001. The following cavity-tree variables were entered into the cavity-tree model: height, DBH, nest height, decay class at cavity, and number of cavities. Decay class was assessed using the wood classification system outlined in the Field Manual for Describing Terrestrial Ecosystems (British Columbia Ministry of Environment, Lands and Parks and British Columbia Ministry of Forests 1998). The nest-plot vegetation variables entered into the model were canopy height (distance from ground to top of canopy layer), canopy cover, understory cover (in four 1-m vertical classes), basal area of all trees, snag density, and density of large hardwoods.

A Kolmogorov-Smirnov test was used to determine whether distribution of snags in each decay class differed between disturbed and undisturbed sites. Also, we used a f-test to determine if the ratio of nest height to canopy height differed significantly between disturbed and undisturbed habitats. All statistical analyses were performed using SYSTAT 9.0 (SPSS, Chicago, Illinois).

RESULTS

Overall reproductive success between habitats.We collected nest-success data for 68 breeding pairs over the two-year study period. Number of nests failing did not differ significantly between years (15 of 37 failed in 2000, and 9 of 31 failed in 2001; G-test, P = 0.14), so we combined both years for analysis of breeding success across habitats. Birds breeding in disturbed habitat had significantly lower nest success than those in undisturbed habitat (16 of 32 nesting attempts failed in disturbed habitat, whereas only 8 of 36 attempts failed in undisturbed habitat; G-test, P = 0.02). In the 52 breeding pairs for which dominance rank was known, high-ranking birds had significantly higher nest success than low-ranking birds (G-test, P = 0.02). For clarity, this analysis also excluded the small number of mid-ranked birds. To look for a possible interaction between, habitat and rank, we compared ratio of successful to failed nests in each habitat separately by rank (Fig. 2). Rank influences patterns of nest success to a much greater extent in disturbed habitat (G-test, P = 0.05) than in undisturbed habitat (Fisher exact test, P = 0.26), in that the majority of successful nests in disturbed habitat belonged to highranking birds.

Breeding densities were not appreciably different between habitats or years. There were 0.25 pairs ha^sup -1^ breeding in the disturbed habitat averaged over two years, compared with 0.33 pairs ha^sup -1^ in the undisturbed habitat. Nest failure resulting from predation was a relatively rare event (

Comparisons of nesting chronology and reproductive output between habitats.- High-ranking birds nesting in disturbed habitat started incubating earlier than those in undisturbed habitat (MannWhitney U-test, U = 10.5, P = 0.01, n = 11 undisturbed vs. 7 disturbed nests). However, hatch date, incubation period, and fledge date did not differ between habitats or ranks (Table 1).

Clutch size and brood size of nests that progressed to the point of hatch did not differ between habitats (β = 0.13 and 0.18, P = 0.51 and 0.53), and ranks (β = -0.01 and -0.11, P = 0.97 and 0.68). However, both clutches and broods tended to be larger in the second year of the study (β = -0.34 and -0.51, P = 0.05 and 0.06). Nests that failed before incubation (n = 14) were excluded from that analysis, as were nests that failed because males abandoned them (n = 2) and a single nest where behavioral and genetic evidence implicated egg dumping (K. Otter, B. Murray, K. Fort, and C. Holschuh unpubl. data).

To compare productivity between disturbed and undisturbed areas, we calculated the average number of fledglings per pair over two years in both habitats. Because the data did not conform to a Poisson distribution, we analyzed fledgling productivity nonparametrically. We did not consider pairs for which the number of fledglings was not known (i.e. inaccessible nests) in this analysis, but we did include all nests where pairs initiated a clutch and abandoned either before or after hatch. In undisturbed habitat, 3.33 ± 0.49 fledglings were produced per pair, whereas only 2.30 ± 0.56 fledglings per pair were produced in the disturbed site over the same period. Those estimates did not, however, differ statistically (Mann-Whitney Li-test, U = 323, P = 0.17, n = 30 undisturbed and 27 disturbed). Although it was not significant, low-ranking birds appeared to produce fewer fledglings than high-ranking birds in both habitats (U = 303.5, P = 0.098, n = 25 low-ranking and 19 high-ranking pairs), and the disparity in productivity estimates between ranks was greater in disturbed habitat. Lowranking birds produced 1.96 fewer birds per pair than high-ranking birds in the disturbed habitat, but only 1.11 fewer birds per pair in the undisturbed habitat.

Nest success and habitat.-The cavity-tree multiple-logistic-regression model was significant (χ^sup 2^ = 8.45, df = 1, P

Distribution of decay class among snogs. – Cavity decay was negatively associated with nest success, and pairs breeding in disturbed habitats experienced nest failure more often than birds in undisturbed habitat (Fig. 2). Therefore, we hypothesized that snags in the lower decay classes would be relatively less abundant in disturbed habitats than in undisturbed habitats. We used snag information collected from 69 nest plots to calculate average snag-decayclass distributions for nest sites in disturbed and undisturbed habitats (Fig. 3). We excluded snags

Ratio of canopy height to nest height. – Canopy height was positively associated with nest success (Table 3), and was significantly lower at disturbed (x = 17.9 ± 1.55, n = 30) than undisturbed (x = 23.6 ± 1.19) (t-test, t = -2.936, P = 0.005) nest sites. However, nest height was not predictive of nest success, nor did it differ significantly between habitats (Mann-Whitney U-test, U = 466.0, P = 0.15, n = 39 in undisturbed and 30 in disturbed). If nest sites in disturbed habitats are relatively closer to the height of the canopy, they may be more exposed, possibly resulting in suboptimal cavity microclimates. The difference in meters between the height of the cavity and the surrounding canopy height was greater around nests in undisturbed than disturbed habitat (Mann-Whitney Li-test, U = 423.0, P = 0.05, n = 39 in undisturbed and 30 in disturbed), which suggests that nests in disturbed habitats may be more exposed.

DISCUSSION

Nest success.-Overall, birds nesting in disturbed habitats experienced lower nest success than those breeding in undisturbed habitats. High-ranking birds were generally more successful than low-ranking birds, irrespective of habitat. However, low-ranking birds appear to experience much lower overall reproductive success in disturbed habitat than in undisturbed habitat. In contrast, reproductive success of higher-ranking birds appears less sensitive to habitat disturbance. The majority of nest failure is attributable to nest abandonment, not predation, on our study site. Additionally, most nest failures occurred early in the breeding season (i.e. before onset of incubation).

The difference in rates of nest success between habitats may be best explained by the relative availability of suitable breeding habitat. Given that chickadee density did not differ markedly between disturbed and undisturbed habitats, good-quality nest sites and breeding territories may have been more limited in the disturbed than in the undisturbed habitat. Within the disturbed site, that may have created increased competition among males for access to those patches containing desired resources. Dominance rank in male chickadees is known to be a good measure of resource-holding potential (Smith 1991). Also, other studies have shown that female chickadees seek opportunities to pair with high-ranking males (Otter and Ratcliffe 1996) and that those females gain reproductive benefits from such pairings (Otter et al. 1999). In disturbed sites, competitively superior highranking males may be better able to incorporate remnant mature-forest patches into their territories, which might provide favored nest sites for their mates, excluding lower-ranking birds from those resources. Undisturbed habitat is not likely to be as variable in relative habitat quality, so one would expect the disparity in quality between territories of high- and low-ranking pairs to be reduced. Thus, intraspecific competition for reproductive resources biased in favor of highranking birds could explain the high incidence of nest-attempt abandonment in disturbed habitat as compared with undisturbed habitat.

In other studies, poor territory quality has been associated with such nest-data variables as low clutch size and clutch productivity (Dhondt et al. 1990, 1992) and delayed onset of laying (von Bromssen and Jansson 1980). However, we found no differences between habitats with respect to any nest-data variables, with the exception of estimated start of incubation, which was earlier in the disturbed habitat. Thus, pairs in disturbed habitat that established nests did not appear to be suffering from decreased resource availability in comparison to birds in undisturbed habitat, which suggests that those (predominantly high-ranking) birds were able to obtain territories and nest sites comparable to those in undisturbed habitat. However, the high rate of nest abandonment by low-ranking birds in the disturbed site suggests that there is a greater disparity between good- and poor-quality territories in disturbed habitat. Low-ranking birds forced into suboptimal territories in the disturbed site may be confronted with a breeding territory so resource-poor that attempting a clutch becomes prohibitively costly. Thus, lower-ranking birds may elect to forgo breeding attempts altogether, rather than (1) lower their clutch size to accommodate decreases in resource availability or (2) lower their own future survival prospects by attempting to breed in suboptimal conditions.

Lack of evidence for settlement bias by habitat.One explanation for decreased breeding success of birds nesting in disturbed habitats is that poor-quality individuals are forced to settle in those suboptimal areas. If there is a despotic settlement pattern (Fretwell and Lucas 1970), we might expect individuals within disturbed sites to be lower in social rank, thus explaining the increased rate of nest abandonment. However, there is no difference in the age distribution of settling pairs in either habitat (Fort and Otter 2004), nor were there any indications that birds in either habitat were inherently lower in social rank across habitats. At winter feeders bordering the two sites, we had occasion to witness interactions between birds that eventually settled in one of the two habitats for breeding; birds that were high-ranking in disturbed sites dominated low-ranking birds that settled in undisturbed sites (Fort and Otter 2004). Moreover, there was no consistent pattern of dominance among like-ranked individuals; birds classified as highranking in undisturbed habitat did not consistently prevail over high-ranking birds from disturbed habitat, and the same was true of low-ranking dyads. Thus, there is little evidence to suggest a settlement bias between habitats. That is consistent with current knowledge of chickadee ecology -dispersal occurs in the fall following hatch and appears to be random in directionality (Smith 1991). Judging from the few banding recoveries we have made, the two study areas seem to reciprocally exchange nestlings; nestlings born in disturbed habitat have later been recovered in undisturbed habitat, and vice versa, in equal numbers. Although we are continuing to pursue research measuring relative condition of settling individuals, the patterns of nest abandonment seen here appear to result from habitat effects on individuals that occur post-settlement, rather than reflecting settlement biases among sites.

Factors associated with nest success.-Rates of predation did not differ between disturbed and undisturbed habitats. Because mechanisms associated with reduced resource-availability are therefore likely responsible for observed patterns of breeding success in our study, we chose to investigate that hypothesis through analyses linking nest-site habitat characteristics and nest success, irrespective of habitat type. We found that successful nest sites in disturbed habitat were often structurally similar to nest sites in undisturbed habitat; successful birds tended to find remnant patches of mature forest in which to situate their nests. Similarly, unsuccessful nests in the undisturbed site were situated in locations similar to typical habitat conditions in the disturbed site.

Birds nesting in cavity trees with lower stages of internal decay were more successful. That may be attributable to increased protection from predation afforded by such nesting substrate (Hooge et al. 1999). However, we consider that an inadequate explanation of patterns of nest success in our data, because predation rates within our study site were generally low. Successful nests were surrounded by a higher canopy, and unsuccessful cavities were closer to the level of the canopy than successful nests. Hooge et al. (1999) found that greater cavity-tree integrity was correlated both with more-stable microclimates and with higher rates of nest success. Nest microclimate is also known to influence incubation demands on parents (Hoi et al. 1994). Because canopy height is generally lower in disturbed areas, smaller crown areas could result in lower abundance of caterpillar species, the breeding chickadees’ primary food source. Indirect evidence of that effect is emerging, in that pairs in disturbed habitats appear to have lowered nestling feeding rates (van Oort 2004), and we are currently using frass-fall traps to directly assess lepidopteran abundance.

Body condition is likely the primary proximate mechanism driving both pre-incubation and post-incubation abandonment decisions (Ruiz et al. 2002). Females breeding in suboptimal habitat may be in poor condition because of lower food-intake levels. If the nest site is also suboptimal in terms of providing a stable microclimate and is more exposed to weather conditions, female body condition will decrease further as a result of increased thermoregulatory costs. Those factors may act in concert to reduce body condition to such an extent that females may elect to forgo a breeding attempt altogether. Differences in microclimate of the nest and condition of breeding pairs are currently being investigated. Preliminary results suggest that males in disturbed habitats are undergoing greater physiological stress during the breeding season (van Oort 2004).

Songbirds breeding in disturbed habitat may be experiencing reproductive losses despite their continued presence in such habitats at densities comparable to those found in adjacent undisturbed woodlands. The primary cause of nest failure was breeding-attempt abandonment by low-ranking birds, whereas nest success of high-ranking birds was unaffected by habitat type. Low food-resource levels, combined with increased thermoregulatory costs associated with poor nest microclimate, may lower body condition to such an extent that breeding becomes too energetically costly for low-ranking birds unable to secure high-quality breeding habitat in disturbed sites.

ACKNOWLEDGMENTS

We thank C. Holschuh, Z. McDonnell, K. Litwinow, B. Burkholder, J. Campbell, M. Marcullo, K. Lawrence, S. Taylor, D. Thomspson, M. Bidwell, H. Swystun, and D. Leman for field assistance. Access to land was provided by the City of Prince George and the University of Northern British Columbia (UNBC). Funding for the study was provided by a Natural Sciences and Engineering Research Council (NSERC) postgraduate scholarship and a Canfor Scholarship to K.F., an NSERC research grant and Canada Foundation for Innovation (CFI)/BC Knowledge Development grant to K.O., by UNBC, and by the Northern Land Use Institute.

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Associate Editor: S. G. Sealy

KEVIN T. FORT1 AND KEN A. OTTER2

Ecosystems Science and Management Program, University of Northern British Columbia, 3333 University Way, Prince George, British Columbia V2N 4Z9, Canada

1 Present address: Pacific Wildlife Research Centre, Canadian Wildlife Service, 5421 Robertson Road, RR 1, Delta, British Columbia V4K 3N2, Canada.

2 Address correspondence to this author. E-mail: otterk@unbc.ca

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