To identify limiting and regulatory processes in breeding areas, the demography of two parulid warbler species, the Black-throated Blue Warbler Dendroica caerulescens and the American Redstart were examined in depth. Long-term abundance data (1969–2005) for these two species are available from a 10-ha study area (Holmes et al. 1986, Holmes & Sherry 2001, my unpubl. data) and for 1986–98 on three replicate sites in other parts of the White Mountains (Holmes & Sherry 2001). Starting in the early 1980s, we expanded the Hubbard Brook study area to 64 ha and then to 100 ha for demographic studies of the two focal species. In these larger areas, we caught and individually marked with coloured rings all adults, and resighted returning individuals in subsequent years. We also followed and determined the fates of all nesting attempts, weighed nestlings prior to fledging, and estimated food (insect) availability and nest predator populations (see Holmes et al. 1992, 1996, Nagy & Holmes 2004, 2005a, 2005b, Sillett et al. 2004, Sillett & Holmes 2005). This information provided demographic information and data on important environmental factors. Because our data are most complete for the Black-throated Blue Warbler, the following discussion will focus on limitation and regulation of its population in the breeding period. This focal species occurs relatively commonly through forests in the northeastern United States and eastern Canada, and can be considered representative of the many small, forest-dwelling migratory passerines in temperate eastern North America.
Tests for density dependence
We found evidence for strong density dependence in the Black-throated Blue Warbler population at Hubbard Brook during the breeding season. Over the 37 years for which we have data, this Warbler population fluctuated from year to year, but remained relatively stable (Sillett & Holmes 2005, my unpubl. data). A time series analysis of abundances on the long-term census plot (1969–2005) showed strong density dependence (P = 0.0002, P.J. Doran & R.T. Holmes unpubl. data, see also Rodenhouse et al. 2003). Furthermore, fecundity (the number of young fledged/territory/breeding season) was significantly negatively correlated with adult Warbler density (Fig. 2A, Sillett & Holmes 2005). Recruitment of 1-year-old males into the population in the subsequent breeding season was also negatively correlated with adult warbler density (Fig. 2B, Sillett & Holmes 2005). No relationship was found between Warbler density and nest predation rate (Sillett & Holmes 2005). Using demographic data from our field population to parameterize a population model, we demonstrated that the observed density-dependent fecundity was sufficient to regulate this Warbler population (Sillett & Holmes 2005). The local abundance of this population therefore seems to be regulated by density-dependent processes, most related to factors affecting fecundity. Finally, not only was recruitment negatively related to adult Warbler density in the previous season, but there was also a strong and statistically significant positive relationship between recruitment and mean annual fecundity of Black-throated Blue Warblers in the previous breeding season (r = 0.78, P = 0.005, Sillett et al. 2000). This latter finding illustrates the importance of fecundity in maintaining local populations, even for a species that spends more than 8 months of the year away from the breeding grounds.
Figure 2. Density-dependent relationships of Black-throated Blue Warblers at Hubbard Brook, New Hampshire USA: (A) annual fecundity (number of young fledged per territory per year) is negatively correlated with adult Warbler density in the same season (modified from Sillett & Holmes 2005), and (B) annual recruitment of yearling Warblers is inversely related to Warbler density in the preceding season (modified from Sillett & Holmes 2005). Numbers on the graph represent the years of study.
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Determinants of fecundity
Demographic data gathered between 1986 and 1999, show that three factors – food availability (as indicated by changes in the Southern Oscillation Index, SOI; see below), nest predation and adult Warbler density – explained 91% of the variance in the mean number of young fledged/territory/year and 80% of the variance in the mean annual mass of young at fledging (Sillett & Holmes 2005). These findings led us to investigate how food, climate, nest predation and adult density influence Black-throated Blue Warbler fecundity.
First, food availability, as indicated by the abundance of Lepidoptera larvae – a major food item for our study species during the breeding season – varied greatly from year to year. Since studies at Hubbard Brook began in 1969, one major caterpillar irruption occurred in the early 1970s (Holmes et al. 1986, 1991). Since 1973, larval numbers have fluctuated annually, but at relatively low or endemic levels (Holmes et al. 1986, Reynolds et al. 2007). Between 1986 and 1998, these annual mean caterpillar abundances (as measured by larval biomass/unit vegetation) were significantly correlated with a climate variable – the mean monthly values of SOI, a standardized measure of the El Niño Southern Oscillation (ENSO, Sillett et al. 2000). Caterpillars were less abundant in El Niño years and higher in La Niña years. Mean annual Black-throated Blue Warbler fecundity and mean body mass of nestlings just prior to fledging were also correlated with SOI (r = 0.59, P < 0.04 and r = 0.79, P < 0.002, respectively), but adult Warbler density and annual nest predation rates were not (Sillett et al. 2000). Furthermore, fluctuations in the abundances of the six most common long-distance migrant species at Hubbard Brook and in three other sites in central New Hampshire were positively and significantly correlated with annual fluctuations in lepidopteran larvae (Jones et al. 2003). Thus, changes in the abundances of these species populations were synchronized with that of their lepidopteran food supply, which were related to the ENSO global climate patterns. These findings together suggest that weather, mediated in part by ENSO, influences caterpillar abundance (and biomass), which in turn affects Warbler fecundity, nestling growth and condition. Food is therefore implicated as an important factor affecting bird populations breeding in these temperate forests.
To test whether food was actually a limiting factor, we performed both food reduction and food augmentation experiments. Using a combination of observations across years and experimental reductions of caterpillar populations by aerial spraying with a larvacide, Bacillus thuriengensis (Bt), Rodenhouse and Holmes (1992) showed that in seasons with more abundant larvae when compared with years when food was scarce, both the number of young Black-throated Blue Warblers fledged per clutch and the number of clutches per season increased, while the frequency of nestling starvation decreased. No change occurred in clutch size across years or food treatments. Similarly, in experiments involving food supplementation rather than food reduction, females given more food fledged significantly more young per season compared with those that were not. In these experiments, the change in annual fecundity was not due to an increase in clutch size or the number of young fledged per nesting attempt, but to an increase in the frequency of multiple brooding by the females (Nagy & Holmes 2005b). Thus, food clearly limits reproductive output in this species, and this limitation probably occurs to at least some extent in most breeding seasons (Nagy & Holmes 2005b).
A second major factor shown to affect annual fecundity significantly was nest predation. Nest predation is a major source of mortality for Warbler eggs and young at Hubbard Brook (Holmes et al. 1992, my unpubl. data), as it is for many passerine species (Ricklefs 1969, Newton 1993). Annual predation rates on Black-throated Blue Warbler nests range from as low as 17% to a high of 42% (my unpubl. data). There is a large suite of nest predator species at Hubbard Brook, both bird and mammal (Reitsma et al. 1990, Sloan et al. 1998, my unpubl. data). Two sciurids – Red Squirrels (Tamiasciurus hudsonicus) and Eastern Chipmunks (Tamias striatus) – are the most important, but mice (e.g. Peromyscus spp.), raptors (Accipiter striatus), mustelids (Martes pennanti) and corvids (e.g. Cyanocitta cristatus) are also involved. Nest predation by snakes has not been documented at Hubbard Brook, nor has brood parasitism by Brown-headed Cowbirds (Molothrus ater). The latter species, however, does occur in human-disturbed habitats in valley areas a few kilometres away.
Both experimental studies (Reitsma 1992, Sillett et al. 2004) and analyses of field data (Sillett & Holmes 2005) indicate that the nest predation rate at Hubbard Brook is not related to nest density nor to adult Warbler density, i.e. it is not density dependent. The abundances of the sciurids, the major nest predators, are most strongly affected by seed crops of the dominant tree species, especially American Beech, which occur irregularly at 2–4-year intervals (my unpubl. data). Thus, year-to-year differences in predation rate on Black-throated Blue Warbler nests vary closely with the masting cycle of the tree species in this forest, and even though nest predation is an important source of mortality (i.e. an important limiting factor), it is not a major regulatory force.
The third major influence on annual fecundity was adult Warbler density, i.e. intraspecific density. The inverse relationship between adult density and the number of young fledged per female per season (Fig. 2A, see Rodenhouse et al. 2003, Sillett & Holmes 2005) is a classic example of density dependence. It, in combination with the effect of climate/food and nest predation, acts to limit and regulate the local abundance of this population during the breeding season (Sillett & Holmes 2005). Density of adult Black-throated Blue Warblers in this forest is further related to density of vegetation in the shrub layer, especially of Hobblebush, a major nesting and foraging substrate (Steele 1992, 1993, Doran & Holmes 2005). Finally, in our studies at Hubbard Brook, no evidence has been found for calcium as a limiting nutrient (Taliaferro et al. 2001), as has been reported for some passerines in Europe (e.g. Graveland & Drent 1997).
Mechanism(s) of density dependence
To explore the mechanisms underlying the density-dependent fecundity in this population, we tested two hypotheses: (1) crowding and (2) site dependence. A crowding mechanism would involve some interaction among close neighbours in a population that might interfere with breeding activity, leading to lower reproductive output. To investigate this mechanism experimentally, we reduced local density by removing conspecifics from around focal Black-throated Blue Warbler territories and then compared the behaviour and reproductive success of these focal birds with those on control territories (Sillett et al. 2004). The results indicated that young fledged per territory, territory size and the proportion of time males spent foraging were all significantly greater for birds on territories with fewer neighbours. The effect of neighbour removal was most pronounced in an El Niño year when conditions for breeding were least favourable. Thus, crowding can mediate interactions among territory holders that result in lower fecundity. Crowding therefore accounts for at least a part for the observed density dependence. In this case, crowding involved a change in male behaviour and use of space that may have its strongest impact when environmental conditions are relatively poor (Sillett et al. 2004).
Another mechanism that could generate the density-dependent negative feedback shown in Figure 2 involves what Rodenhouse et al. (1997) termed site-dependent regulation. This mechanism extends the ideas of Pulliam (1988), Pulliam and Danielson (1991) and Dhondt et al. (1992), and involves the pre-emptive use of sites that differ in suitability for survival or reproduction (McPeek et al. 2001). The basic premises are (1) that sites (territories) differ in quality, (2) that individuals occupy the best site available and are seldom replaced (pre-emptive occupancy), and (3) that site suitability determines reproductive success or survival. Tests of this mechanism conducted at Hubbard Brook (Rodenhouse et al. 2003, 2006) reveal that sites occupied by individual territorial birds differ strongly in quality, even in seemingly homogeneous habitat, that sites occupied every year are on average better than those occupied only periodically, and that the best sites (most food, fewest predators, highest vegetation density) yield the greatest annual fecundity. Similarly, Doran and Holmes (2005) reported that Black-throated Blue Warblers showed temporal and spatial variability in their choice of territory sites, but selectively chose territory sites with higher shrub density, greater food levels and lower predator levels, all of which influenced individual reproductive output.
Thus, heterogeneity among sites (territories) coupled with density-dependent territorial behaviour of male Black-throated Blue Warblers contributes to the annual variability in fecundity at the population level. Our findings indicate that both mechanisms – crowding and site dependence – are involved simultaneously in population regulation. Crowding operates in high-quality, high-density habitats at the scale of individuals and their neighbours, while site dependence occurs on a larger (i.e. landscape) spatial scale (Rodenhouse et al. 2003, 2006, Sillett et al. 2004).