Behavioral Ecology Advance Access published online on June 27, 2007
Behavioral Ecology, doi:10.1093/beheco/arm048
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Mechanisms and fitness effects of interspecific information use between migrant and resident birds
a Department of Ecology and Evolution, Animal Ecology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 d, SE-75236 Uppsala, Sweden b Department of Biology, University of Oulu, PO Box 3000, FI-90014 Oulu, Finland
Address correspondence to J.T. Forsman, who is now at the Department of Biology, University of Oulu, PO Box 3000, FI-90014 Oulu, Finland. E-mail: jukka.forsman{at}oulu.fi. R.L. Thomson is now at the Section of Ecology, Department of Biology, University of Turku, FI-20014 Turku, Finland. J.-T. Seppänen is now at the Department of Biological and Environmental Sciences, University of Jyväskylä, PO Box 35, FI-40014, Finland.
Received 7 December 2006; revised 6 March 2007; accepted 15 May 2007.
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ABSTRACT |
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Interactions with potential competitors are an important component of habitat quality. Due to the costs of coexistence with competitors, a breeding habitat selection strategy that avoids competitors is expected to be favored. However, many migratory birds appear to gain benefits from an attraction to the presence of resident birds, even though residents are assumed to be competitively dominant. Thus far the mechanisms of this habitat selection process, heterospecific attraction, are unknown, and the consequences for resident birds of migrant attraction remain untested. Through heterospecific attraction, migrants may gain benefits if the density or territory location of residents positively reflects habitat quality, and/or they gain benefits through increased frequency of social interactions with residents in foraging or predator detection. In this experiment, we examined the reciprocal effects of spatial proximity on fitness-related traits in migrant pied flycatcher (Ficedula hypoleuca) and resident great tit (Parus major) by experimentally forcing them to breed either alone or in close proximity to each other. Surprisingly, great tits bore all the costs of coexistence while flycatchers were unaffected, even gaining slight benefits. In concert with an earlier study, these results suggest that flycatchers use tits as information about good-quality nest-site locations while benefits from social interactions with tits are possible but less important. We suggest that utilizing interspecific social information may be a common phenomenon between species sharing similar resource needs. Our results imply that the effects of interspecific information use can be asymmetric and may therefore have implications for the patterns and consequences of species coexistence.
Key words: cavity nesting birds, habitat selection, interspecific competition, nest-site selection, resident and migrant birds, social information, species interactions.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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One of the most important factors affecting the fitness of organisms is the choice of environment for reproduction. Choices are complicated by variation in habitat quality with respect to various biotic and abiotic conditions, such as food resource levels, abiotic conditions at the microhabitat level, and the risk of predation that affects the reproductive success of individuals (Robinson et al. 1995
; Sinervo and DeNardo 1996; Forsman, Mönkkönen, Helle, and Inkeröinen 1998; Martin 2001; Thomson, Forsman, Mönkkönen, et al. 2006; Thomson, Forsman, Sardà-Palomera, and Mönkkönen 2006). Potential competitors are another important component of habitat quality. Coexistence with competitors usually results in fitness costs that can be due to direct interactions such as resource competition (e.g., Brown and Davidson 1977; Gustafsson 1987; Wedin and Tilman 1993; Martin PR and Martin TE 2001a) or indirect interactions mediated by shared predators or parasites (apparent competition, Holt 1977; e.g., Martin 1993; Holt and Lawton 1994; Martin PR and Martin TE 2001a). Consequently, avoidance of potential competitors is expected to be the best strategy in breeding habitat selection (see Martin PR and Martin TE 2001a, 2001b).
Sometimes, however, animals are paradoxically attracted to the presence of potential competitors. Studies conducted in northern forest bird communities show that later arriving passerine migrant birds use the presence or density of earlier established resident tit species as a cue for habitat quality and are attracted to them (for a review, see Mönkkönen and Forsman 2002). This habitat selection process was coined heterospecific attraction by Mönkkönen et al. (1990). Residents are present year round, initiate breeding before the arrival of most migrants, and have ample time to assess the quality of habitats. Therefore, their presence or relative density in the landscape can be assumed to reflect habitat quality through direct (habitat selection) or indirect (habitat-dependent mortality in winter) processes. Quick habitat selection is important for migrants because their breeding success rapidly declines with delayed onset of breeding (Klomp 1970). Experiments to date show that augmented resident titmice densities yield increased species number and density of migrant birds (Mönkkönen et al. 1990, 1997; Forsman, Mönkkönen, Helle, and Inkeröinen 1998; Thomson et al. 2003; see also Elmberg et al. 1997). In addition, pied flycatchers (Ficedula hypoleuca), potential competitors with resident tits (Parus spp.) (Haartman von 1957; Slagsvold 1975; see also Gustafsson 1987), prefer tit proximity in breeding site selection and gain fitness benefits in terms of a higher number and condition of nestlings (Forsman et al. 2002).
The ultimate mechanism of heterospecific attraction remains unknown. Migrants are suggested to benefit through hastened and more accurate breeding habitat selection if the density or territory location of tits indicate high-quality habitats or nest sites (Forsman et al. 2002; Mönkkönen and Forsman 2002). Proximity to tits might also yield enhanced predator detection or foraging efficiency via social interactions (Mönkkönen et al. 1996; Forsman, Mönkkönen, Helle, and Inkeröinen 1998; Forsman and Mönkkönen 2001; Krams and Krama 2002). Also unknown are the consequences to resident tits that stem from migrants using heterospecific attraction as a habitat selection strategy. Owing to resident tits' larger body size and prior occupation of resources, they have traditionally been regarded as dominant competitors over migrants (MacArthur 1972; Herrera 1978). The effect of heterospecific attraction to tits has, as a result, been assumed to be either neutral (commensal interaction) or positive (mutualistic interaction). Crucially, however, this assumption has not been explicitly experimentally examined.
Experimental evidence suggests that migratory collared flycatchers (Ficedula albicollis) suffer from competition with resident tits (Gustafsson 1987). However, these flycatchers may also have negative impacts on residents (Sasvári et al. 1987). Mutually positive interactions between organisms on the same trophic level exist in certain environmental conditions in plant and sessile animal assemblages (Bertness and Callaway 1994; Bruno et al. 2003), but examples among mobile vertebrates are much sparser (but see Dickman 1992, ungulates). In this study, we examine the reciprocal fitness-related consequences of heterospecific proximity in both the migrant and resident bird to reveal the nature of the interactions between them and to assess whether social interactions contribute to the fitness benefits of heterospecific attraction reported before (Forsman et al. 2002).
We experimentally forced pied flycatchers and great tits (Parus major) to breed either alone or in close proximity to each other at random locations and tested whether this results in mutualistic (both benefit), commensal (one benefits and other is unaffected), competitive (both suffer), or even parasitic (one benefits and other suffers) interactions. In addition, by comparing the results of this study with those of Forsman et al. (2002), we are able to distinguish between mechanisms behind the positive fitness consequences of heterospecific attraction to migrants. As residents in that study were free to choose their nest sites, the improved performance of attracted migrants can be explained by microhabitat quality, quicker onset of, and social benefits during breeding. Here, our experimental design removed the effects of nest-site location and quality on breeding success, which has rarely been done in the wild. Therefore, if flycatchers breeding in proximity to tits do not exhibit improved reproductive output compared with flycatchers breeding alone, the benefits found in Forsman et al. (2002) did not result from social benefits but mainly through microhabitat quality and quicker onset of breeding. If, however, improved reproductive output occurs here also, social benefits from breeding in association with tits also play a significant role.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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The experiment was conducted near Oulu in northern Finland (64°50'N, 24°30'E) during 3 breeding seasons (2003–2005). Experimental great tit and pied flycatcher boxes were situated on 8 separate study plots, 7–21 ha in size. Forest characteristics among study areas were largely homogeneous. Forests were dominated by young to middle-aged birch (Betula spp.) with scattered aspen (Populus tremula) and coniferous trees (Pinus sylvestris, Picea abies). Great tits (resident, average body mass 18 g) and pied flycatchers (tropical migrant, average body mass 13 g) share similar breeding and food resource requirements, especially during the nestling rearing period (see Minot 1981
; Gustafsson 1987; Lundberg and Alatalo 1992).
The experiment consisted of 3 treatments: 1) great tits and 2) pied flycatchers breeding alone (>120 m to the nearest con- or heterospecific neighbor) and 3) flycatchers and tits breeding as neighbors (nest boxes 20 m apart). These distances were believed to result in a spatial arrangement of nest boxes that is free from plot-scale effects of con- and heterospecific density that affect individual success and yet bring about potential positive or negative effects of the heterospecific proximity at the nest-site scale (see Forsman et al. 2002). All initiated tit nests within the study plots were assigned to treatments in spring. Instead of a fully randomized design, we randomly assigned a treatment to every second nest to avoid accumulation of any treatment in some plots due to chance. When the first nest box became occupied by a great tit (hair in the box), it was randomly assigned a treatment to either breed "alone" or "with neighbor." The next occupied box within the same area was then assigned to the other treatment; the following occupied box was again randomly assigned and so forth. To control for effects of nesting site quality, tit boxes were gradually (over 5 days) moved 
50 m in a random direction during egg laying. Despite our study sites appearing homogeneous from a human perspective, it is likely that small-scale spatial variation or microhabitat differences especially in microclimatic factors (Horvath 1964; Walsberg 1985) exist. From the bird's perspective, altering nest-site location by 50 m should effectively control for the habitat quality in the vicinity of nests. Naef-Daenzer (2000) found that great tits spent 90% of their time within a 25 m radius of the nest site. Pied flycatchers only defend the immediate vicinity around the nest hole (radius of ca., 10 m, Lundberg and Alatalo 1992) and, although they may occasionally make foraging trips up to 50–100 m from the nest (Haartman von 1956), mostly forage close to the nest (Forsman JT, Thomson RL, Seppänen J-T, personal observation).
Individual site choice of flycatchers was also randomized. We placed 3–4 empty nest boxes, 40 m apart, at a distance of 70 m from great tit nests assigned to the "neighbor" treatment. By that time, most great tit nests were already relocated to their final random position, had completed clutches, and incubation had begun. As a result, forthcoming flycatcher neighbor treatments could not have affected initial tit offspring investment. After 2 of the flycatcher boxes became occupied, one was randomly assigned to the alone treatment and the other to the neighbor treatment, and the remaining unoccupied boxes were removed. The neighbor box was gradually moved to within 20 m of the tit nest, and the alone box was moved to 120 m from the tit nest. This protocol ensured that the locations of all experimental nest boxes were random and free from individual choice as far as it is possible in these species and that all pairs went through similar moving manipulation. Adult birds were not caught but, the experimental procedure should control for any effects of adult phenotypic variation on response variables. Experimental procedures were approved by the ethical committee of the University in question and by the North Ostrobothnia Regional Environment Centre.
We monitored the date of first egg, clutch size, start of incubation, hatching date, and the number and the condition (body mass, length of tarsus, and wing) of nestlings when the oldest chicks were 13 days of age. We used a digital balance (accuracy ± 0.1 g) for body mass measurements, callipers for tarsus (±0.02 mm), and ruler (±1 mm) for wing and tail measurements. In 2003, all the measurements were done by J.T.F. and in other years by R.L.T. Nestling condition measurements were averaged within a brood, and these fitness-related measures were used as the treatment response variables. In the analyses of nestling number, condition, and survival, we used only those broods that had at least one nestling at the age of 13 days. The effect of treatments on response variables (except survival probability) was analyzed separately for both species using generalized linear model analysis of variance (ANOVA). In every model, we included the treatment (alone or with neighbor) as a fixed factor and year and study plot as random factors to account for their effect on breeding success. The interaction between treatment and year was visually explored to detect potential qualitative differences in the treatment effects among years (Quinn and Keough 2002). If the treatment effect differed between years, data was split accordingly and analyzed separately. For the nestling condition measurements, we also included the date of the first egg and clutch size as covariates to control for parental quality (date of first egg) and possible effects of investment in offspring (clutch size). We used Akaike's information criteria (AIC) (Burnham and Anderson 2002) to reach the most parsimonious statistical model of the models including different combinations of the explanatory variables. We report AIC values only for those competing models that showed significant treatment effects. The number of nestlings, their body mass, and lengths of tarsus and wing were log10 transformed to achieve homogeneity of error variances in ANOVA. We used orthogonal (Helmert) contrasts, which take into account the effect of possible covariates on response variable, as a post hoc test to examine the effect of treatments. Survival of nestlings to the age of 13 days was analyzed using generalized linear mixed models (GLMM) using year as a random factor, with binomial errors, a logit link function, and with the appropriate denominator (McCullagh and Nelder 1989). In the GLMM, AIC values for the competing models were calculated as advised by Quinn and Keough (2002, p. 370–371). Analyses were done in SPSS 12.0. and in GenStat 8.0. softwares.
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RESULTS |
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Number of nests, timing, and clutch size
A total of 51 great tit nests were included in the analyses across the 3 study years (12 + 11 + 28), out of which 27 were breeding with a neighbor and 24 alone. For flycatchers, the 56 nests in 3 study years (16 + 12 + 28) were equally assigned to each treatment (28 nests each). Great tits tolerated the moving of their nest boxes less well than pied flycatchers. In general, great tits are more sensitive to disturbance prior to the nestling period than flycatchers. About 25% (n = 20) of the initial experimental tit broods failed to produce offspring. Failures were partly due to nest predation (8%) and aggressive takeovers by pied flycatchers (Slagsvold 1975
) but also probably due to the experimental procedure. Of the failed tit nests, excluding depredated nests, 45% and 55% were in the neighbor and alone treatments, respectively, suggesting that the treatment did not affect the probability of abandonment. The actual number of aggressive pied flycatcher takeovers of tit nests is difficult to estimate because flycatchers may swiftly occupy abandoned tit nests, which afterwards resembles a takeover. Nevertheless, pied flycatchers are able to takeover tit nests, usually before tits have started incubation (Forsman JT, Thomson RL, Seppänen J-T, personal observation). Adverse weather also caused tit brood failures, especially in 2004, when there was a long cold spell in May when many tits were feeding nestlings. Of the initial pied flycatcher nests, about 3% were depredated and 9% abandoned. There were no differences between treatments in the average onset of egg laying, clutch size, and hatching date (results not shown in detail) in either great tit or pied flycatcher broods. This suggests that, as planned, manipulations did not affect the initial investment in offspring, and any differences between treatments likely occurred after hatching. On average, great tits began egg laying on 13 May, laid 10 eggs, and hatched on 7 June. The average onset of egg laying in pied flycatchers took place on 26 May; they laid 6.5 eggs that hatched on 15 June.
Number, survival, and body mass of nestlings
In the great tit, treatment effects on the number of nestlings and their average body mass differed in 2004 compared with 2003 and 2005 (see Figure 1 for the qualitatively different treatment effects). We therefore analyzed data from 2004 separately. In 2004, the treatment term remained in the final model for the number of tit nestlings at 13 days. Indeed, great tits breeding with flycatchers produced 3.5 nestlings less (52%) than tits breeding alone (F1,10 = 7.39, P = 0.022, R2 = 42.5%; AIC of the model –23.16 vs. –4.47 for the second best model including date of the first egg) (Figure 1a). However, treatment did not significantly affect nestling body mass in 2004 (Figure 1b). This is largely due to the low number of great tit chicks in nests breeding in association with flycatchers (less sibling competition). Furthermore, in 2004, the survival of tit nestlings from hatching to 13 days old in the neighbor treatment was considerably lower (40.4%) than in the alone treatment (80.5%) (treatment: effect [standard error {SE}] = –1.75 [0.58], Wald = 9.03, degrees of freedom [df] = 1, P = 0.003; AIC of the model –5.77 vs. –4.01 for the second best model including the onset of egg laying).
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In 2003 and 2005, treatment effects on great tit nestling number and mass were parallel. Tits breeding alone in 2003 produced 0.34 nestlings more that were 1.66 g heavier than those of tits breeding with flycatchers, whereas the corresponding numbers in 2005 were 0.21 chicks and 1.54 g, respectively. We therefore pooled the great tit data from years 2003 and 2005. Treatment did not affect great tit nestling number (F1,33 = 0.094, P = 0.762) (Figure 1c), but nestling body mass was 1.55 g lower (8.8%) when breeding with flycatchers than when breeding alone (the final model included only treatment; F1,34 = 4.66, P = 0.038, R2 = 12.0%; AIC of the model –81.91 vs. –80.02 for the second best model including clutch size) (Figure 1d). In 2003 and 2005, tit nestling survival from hatching to 13 days differed, but treatment effects were parallel, and the data was again pooled. In 2003, nestling survival in the neighbor and alone treatments was 66.2% and 68.5% and in 2005 87.3% and 93.7%, respectively. Treatment did not have a significant effect on the survival of tit nestlings (treatment: effect [SE] = –0.40 [0.50], Wald = 0.65, df = 1, P = 0.420).
In the pied flycatcher, treatment effects did not differ between years (see Figure 1). However, to compare the effects of treatments with those of the great tit, data on nestling number and their body mass from 2003 to 2005 were pooled and 2004 was analyzed separately. In contrast to the great tit, treatment had no significant effect on nestling number, body mass (Figure 1a–d), or survival (average survival across all years in the neighbor = 95.08% and alone = 95.73% treatments) of flycatcher nestlings.
Nestling wing length
Treatment also had qualitatively different between-year effects on nestling wing length, and these data were analyzed separately. In the great tit, 2003 differed from the other years; tit nestlings raised in the neighbor treatment had 12.4% shorter wings than those in the alone treatment (the final model included only treatment: F1,10 = 5.63, P = 0.039, R2 = 36.0%; Figure 2a) (AIC of the model –24.89 vs. –20.47 for the second best model including clutch size), whereas in 2004 and 2005, there was no treatment effect. In the pied flycatcher, 2005 was different from the other years; after accounting for the effect of onset of egg laying, flycatcher nestlings raised in the neighbor treatment had 1.8 mm (3.4%) longer wings than those in the alone treatment (model R2 = 36.8%; treatment: F1,23 = 5.53, P = 0.044; onset of egg laying: F1,23 = 7.44, P = 0.012; Figure 2a) (AIC of the model –84.65 vs. –81.56 for the second best model including clutch size). In 2003 and 2004, there was no difference in nestling wing lengths between treatments.
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Nestling tarsus length
In the great tit, nestling tarsus length was pooled across study years. There was a strong effect of year on tarsus length (F2,42 = 65.26, P < 0.0001), but treatment effects were parallel among years. After accounting for year effect, treatments had no effect on tarsus length of great tit nestlings (F1,42 = 1.85, P = 0.181; Figure 2b). In the pied flycatcher, treatment did not affect the tarsus lengths of nestlings in 2003. However, in 2004 and 2005, treatment effects were qualitatively different. In these years, flycatcher nestlings raised in proximity to tits had 0.33 mm (more than 4 times the standard error of the mean; 0.076 mm) longer tarsus than those breeding alone (F1,33 = 9.36, P = 0.004, R2 = 22.1%; Figure 2b) (AIC of the model –141.73 vs. –139.18 for the second best model including clutch size).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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In recent years, there has been increasing interest in understanding how animals gather information from other individuals and use it in decision making (termed social information, for reviews, see Valone and Templeton 2002
; Danchin et al. 2004). Most studies exploring social information use are constrained to a within-species context (but see Coolen et al. 2003; Parejo et al. 2005). Our results reported here, in concert with earlier studies (Mönkkönen et al. 1990, 1997; Forsman, Mönkkönen, Helle, and Inkeröinen 1998; Forsman et al. 2002; Thomson et al. 2003), emphasize that the presence of an individual conveys information about the quality of the site to individuals of other species with some ecological overlap. Such interspecific information use has earlier went largely unnoticed but is probably common in nature (for review, see Seppänen et al. 2007) and also seems to be adaptive (Forsman et al. 2002).
Consequences for flycatchers
In an earlier experiment, we showed that pied flycatchers preferred the presence and close proximity of tits in breeding habitat selection and gained fitness benefits (more and heavier nestlings with longer wings) as a result (Forsman et al. 2002). In the present study, flycatchers breeding together with titmice had nestlings somewhat larger (longer tarsus) than flycatchers breeding alone. However, the positive effects of living with tits occurred in only some years and were not as strong as observed in Forsman et al. (2002). For example, in Forsman et al. (2002), the average body mass of flycatcher nestlings breeding with tits was 0.46 g (3.2%) heavier than in flycatchers breeding alone, whereas in the present study, flycatcher chicks in the neighbor treatment were 0.20 g (1.4%) lighter than those reared in the alone treatment (difference not statistically significant). Also, the positive effect on the wing length of nestlings was only observed in one year. In this study, the positive effect of tit proximity on the wing length compared with breeding alone was about the same as in the earlier study (1.8 mm [3.5%] and 1.2 mm [2.3%], respectively). Positive effects on nestling tarsus length were somewhat stronger in this study than in the earlier (0.33 mm [1.9%] and 0.07 mm [0.3%, not statistically significant], respectively).
Importantly, unlike in Forsman et al. (2002), this study manipulated great tit and pied flycatcher nest-site selection to a random location 50 m away, which should control for the habitat quality in the vicinity of the nest for both species (Haartman von 1956; Naef-Daenzer 2000). This suggests that the increased flycatcher reproductive success in Forsman et al. (2002) mainly resulted from the quicker decision making and enhanced likelihood of finding high-quality microhabitats through heterospecific attraction, although social factors may also have some contribution (see below). Resident birds have time to assess the quality of sites and settle at the best sites. It is therefore very likely that a site occupied by a tit is of a higher quality than a randomly chosen site. By settling in close proximity to a tit nest, flycatchers are assured of a good breeding site while simultaneously saving much of the time a direct assessment would require. Timonen et al. (1994) showed that chaffinches (Fringilla coelebs) tended to be more abundant on willow tit (Parus montanus) territories compared with random locations suggesting that attraction to the vicinity of resident tit nests may be widespread among migratory birds.
Social interactions with tits may also be of importance because in some years flycatchers gained benefits from breeding in proximity to tits. Flycatchers may gain benefits through mechanisms similar to those operating in conspecific (Morse 1970) or in heterospecific (Sasvári 1992; Dolby and Grubb 1998) aggregations, that is, enhanced foraging success and/or predator protection. Many other migrants aggregate with resident birds during the breeding period, and both foraging benefits (Mönkkönen et al. 1996) and predator protection (Forsman, Mönkkönen, Inkeröinen, and Reunanen 1998; Forsman and Mönkkönen 2001) have been suggested. Occurrence of social interactions may have been hindered by our experimental design that kept population densities of tits and flycatchers relatively low. Benefits of social interactions may become more apparent at moderate population densities when some minimum group size for foraging, for example, can be reached. The ultimate mechanism of heterospecific attraction may thus be both acquisition of good-quality breeding sites and benefits via social interactions with heterospecifics.
Consequences for tits
The results of this study suggest that, surprisingly, resident great tits seem to be the suffering party in the interaction resulting from the process of heterospecific attraction. Depending on the year, great tits breeding with pied flycatchers produced fewer nestlings of poorer condition than solitary breeding tits. Even though the splitting of data due to among-year variation resulted in moderate sample sizes for some analyses, in general, flycatchers negatively affected the condition traits of tit nestlings, potentially decreasing their survival probability after fledging and future reproductive potential (Lindström 1999). Although all breeding pairs were treated equally (see methods), this result must be interpreted with care. Great tits are sensitive to disturbance prior to hatching, and moving boxes to random locations may have caused stress, which, coupled with presence of flycatcher in the neighbor treatment, may have unduly exacerbated differences between procedural effects of treatments. Sasvári et al. (1987), however, found correlative evidence of asymmetric interactions between tits and flycatchers; collared flycatchers negatively affected the breeding success of great tits, whereas the impact of tits on flycatchers was less clear. This suggests that our observed treatment effects in great tits are probably real and not confounded by the experimental procedure. In contrast, flycatchers breeding in proximity to tits were not affected negatively in any year and in some years benefited especially in terms of longer tarsus of nestlings, which is positively associated with survival and future breeding habitat quality (Lindén et al. 1992; Lindström 1999).
The nature of interactions between tits and flycatchers
How should we then categorize the interaction between flycatchers and great tits? The consequences of interspecific competition can be asymmetric but usually result in costs for all involved parties (e.g., Martin PR and Martin TE 2001a). Using long-term breeding data, Sasvári et al. (1987) found that hatching success and the number of fledglings in the great tit were negatively correlated with the density of collared flycatchers, a close relative of the pied flycatcher, whereas effects of tits on flycatchers were less clear and apparent only at highest tit densities. This supports the results of our experiments that suggest at low densities, great tits seem to suffer (this study) and flycatchers benefit from the vicinity of tits (Forsman et al. 2002; this study). Also in line with Sasvári et al. (1987), Gustafsson (1987) showed experimentally that the reproductive success of collared flycatchers was reduced at experimentally augmented tit densities compared with lower (close to natural) tit densities, probably due to competition over food. Tits also occasionally kill adult collared and pied flycatchers if they meet in the nest box (Merilä and Wiggins 1995; Forsman JT, Thomson RL, Seppänen J-T, personal observation). On the other hand, flycatchers often harass tits especially at the time of arrival in spring and may take over their nest cavities (Slagsvold 1975; Sasvári et al. 1987; Forsman JT, Thomson RL, Seppänen J-T, personal observation). The interactions between flycatchers and tits are therefore complex and do not seem to entail costs for both species in all conditions (see also Mönkkönen et al. 2004).
This and other studies (Gustafsson 1987; Sasvári et al. 1987) suggest that the net result of interactions may depend on the population density of species and the scale of measurements. Because flycatchers lag 10–14 days behind tits in breeding, the tits' peak in food consumption overlaps with late incubation and early hatching period of flycatchers, which is when their need for food increases. The exploitative competition by tits on flycatchers seems to outweigh the benefits only at moderate tit densities upwards (Gustafsson 1987; Sasvári et al. 1987), so that the net effect for flycatchers at low tit density and close proximity remains positive (Forsman et al. 2002; this study). Flycatchers in turn seem to affect tits via interference competition so that the proximity of a single flycatcher neighbor is influential even at low population densities (this study). Thus, the interactions between flycatchers and tits may vary depending on the local conditions. At low tit densities or at the nest-site scale, interactions resemble exploitation where pied flycatchers use tits in breeding site selection and gain benefits while tits seem to suffer. At higher tit densities and at the population level, interaction resembles more interspecific competition in which all parties suffer. Collared flycatchers indeed seem to take the effects of population densities of tits into account in breeding habitat selection because habitats with intermediate tit densities are preferred over high densities (Forsman JT, Hjernquist MB, Taipale J, Gustafsson L, unpublished data). There is also some evidence from other birds that later arriving species use the presence of the earlier established species in their breeding site selection (Slagsvold 1980; Groom 1992; see also Martin PR and Martin TE 2001b), the net result of which may be positive for the later arriving birds but can conceivably be negative for the earlier established bird via direct or apparent competition (see Martin PR and Martin TE 2001a,b).
To conclude, the results of this study highlight the importance of information transfer between individuals of different species regarding shared resources. Such a mechanism can clearly influence the patterns and consequences of species coexistence and should perhaps be incorporated in models attempting to explain it.
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Funding |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFundingREFERENCES |
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Academy of Finland (project no. 202388 to J.T.F.), European Commission (Marie Curie Intra-European Fellowship, project MEIF-CT-2003-500554 to J.T.F.), and Ella and Georg Ehrnrooth foundation and Oulun Yliopiston tukisäätiö (R.L.T.).
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ACKNOWLEDGEMENTS |
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We thank L. Gustafsson, M. Mönkkönen, and 2 anonymous reviewers for comments on the earlier drafts of this paper.
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REFERENCES |
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Bertness MD, Callaway R. Positive interactions in communities. Trends Ecol Evol (1994) 9:191–193.[CrossRef]
Brown JH, Davidson DW. Competition between seed-eating rodents and ants in desert ecosystems. Science (1977) 196:880–882.
Bruno JF, Stachowicz JJ, Bertness MD. Inclusion of facilitation into ecological theory. Trends Ecol Evol (2003) 8:119–125.
Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. (2002) 2nd ed. New York: Springer-Verlag.
Coolen I, van Bergen Y, Day RL, Laland KN. Species difference in adaptive use of public information in sticklebacks. Proc R Soc Lond B Biol Sci (2003) 270:2413–2419.[Medline]
Danchin E, Giraldeau L-A, Valone TJ, Wagner RH. Public information: from nosy neighbours to cultural evolution. Science (2004) 305:487–491.
Dickman CR. Commensal and mutualistic interactions among terrestrial vertebrates. Trends Ecol Evol (1992) 7:194–197.[CrossRef]
Dolby AS, Jr Grubb TC. Benefits to satellite members in mixed species foraging groups: an experimental analysis. Anim Behav (1998) 56:501–509.[CrossRef][Web of Science][Medline]
Elmberg J, Pöysä H, Sjöberg K, Nummi P. Interspecific interactions and co-existence in dabbling ducks: observations and an experiment. Oecologia (1997) 111:129–136.[CrossRef][Web of Science]
Forsman JT, Mönkkönen M. Responses by breeding birds to heterospecific song and mobbing call playbacks under varying predation risk. Anim Behav (2001) 62:1067–1073.[CrossRef][Web of Science]
Forsman JT, Mönkkönen M, Helle P, Inkeröinen J. Heterospecific attraction and food resources in migrants' breeding patch selection in northern boreal forest. Oecologia (1998) 115:278–286.[CrossRef][Web of Science]
Forsman JT, Mönkkönen M, Inkeröinen J, Reunanen P. Aggregate dispersion of birds after encountering a predator: experimental evidence. J Avian Biol (1998) 29:44–48.[CrossRef]
Forsman JT, Seppänen J-T, Mönkkönen M. Positive fitness consequences of interspecific interaction with a potential competitor. Proc R Soc Lond B Biol Sci (2002) 269:1619–1623.[Medline]
Groom MJ. Sand-colored nighthawks parasitize the anti-predator behavior of three nesting bird species. Ecology (1992) 73:785–793.[CrossRef][Web of Science]
Gustafsson L. Interspecific competition lowers fitness in collared flycatchers Ficedula albicollis: an experimental demonstration. Ecology (1987) 68:291–296.[CrossRef][Web of Science]
Haartman von L. Territory in the pied flycatcher, Muscicapa hypoleuca. Ibis (1956) 98:460–475.[CrossRef]
Haartman von L. Adaptation in hole-nesting in birds. Evolution (1957) 11:339–347.[CrossRef][Web of Science]
Herrera CM. On the breeding distribution patterns of European migrant birds: MacArthur's theme re-examined. Auk (1978) 95:496–509.[Web of Science]
Holt RD. Predation, apparent competition and the structure of prey communities. Theor Popul Biol (1977) 12:197–229.[CrossRef][Web of Science][Medline]
Holt RD, Lawton JH. The ecological consequences of shared natural enemies. Annu Rev Ecol Syst (1994) 25:495–520.[CrossRef][Web of Science]
Horvath O. Seasonal differences in Rufous Hummingbird nets height and their relation to nest climate. Ecology (1964) 45:235–241.[CrossRef][Web of Science]
Klomp H. The determination of clutch size in birds. Ardea (1970) 58:1–124.[Web of Science]
Krams I, Krama T. Interspecific reciprocity explains mobbing behaviour of the breeding chaffinches, Fringilla coelebs. Proc R Soc Lond B Biol Sci (2002) 269:2345–2350.[Medline]
Lindén M, Gustafsson L, Pärt T. Selection on fledgling mass in the collared flycatcher and the great tit. Ecology (1992) 73:336–343.[CrossRef][Web of Science]
Lindström J. Early development and fitness in birds and mammals. Trends Ecol Evol (1999) 14:343–347.[CrossRef][Medline]
Lundberg A, Alatalo RV. The pied flycatcher. (1992) London: T & AD Poyser.
MacArthur RM. Geographical ecology. (1972) New York: Harper & Row.
Martin PR, Martin TE. Ecological and fitness consequences of species coexistence: a removal experiment with wood warblers. Ecology (2001a) 82:189–206.[CrossRef][Web of Science]
Martin PR, Martin TE. Behavioral interactions between coexisting species: song playback experiment with wood warblers. Ecology (2001b) 82:207–218.[CrossRef][Web of Science]
Martin TE. Nest predation and nest sites: new perspectives on old patterns. Bioscience (1993) 43:523–532.[CrossRef][Web of Science]
Martin TE. Abiotic vs. biotic influences on habitat selection of coexisting species: climate change impacts? Ecology (2001) 82:175–188.[CrossRef][Web of Science]
McCullagh P, Nelder JA. Generalized linear models. (1989) 2nd ed. London: Chapman & Hall.
Merilä J, Wiggins DA. Interspecific competition for nest holes causes adult mortality in the collared flycatcher. Condor (1995) 97:445–450.
Minot EO. Effects of interspecific competition for food in breeding blue and great tits. J Anim Ecol (1981) 59:375–385.
Mönkkönen M, Forsman JT. Heterospecific attraction among forest birds: a review. Ornithol Sci (2002) 1:41–51.[CrossRef]
Mönkkönen M, Forsman JT, Helle P. Mixed-species foraging aggregations and heterospecific attraction in boreal bird communities. Oikos (1996) 77:127–136.[CrossRef][Web of Science]
Mönkkönen M, Forsman JT, Thomson RL. Qualitative geographical variation in interspecific interactions. Ecography (2004) 27:112–118.
Mönkkönen M, Helle P, Niemi GJ, Montgomery K. Heterospecific attraction affects community structure and migrant abundances in northern breeding bird communities. Can J Zool (1997) 75:2077–2083.[CrossRef]
Mönkkönen M, Helle P, Soppela K. Numerical and behavioural responses of migrant passerines to experimental manipulation of resident tits (Parus spp.): heterospecific attraction in northern breeding bird communities? Oecologia (1990) 85:218–225.[CrossRef][Web of Science]
Morse DH. Ecological aspects of some mixed-species foraging flocks of birds. Ecol Monogr (1970) 40:119–165.[CrossRef][Web of Science]
Naef-Daenzer B. Patch time allocation and patch sampling by foraging great and blue tits. Anim Behav (2000) 59:989–999.[CrossRef][Web of Science][Medline]
Parejo D, Danchin E, Aviles J. The heterospecific habitat copying hypothesis: can competitors indicate habitat quality? Behav Ecol (2005) 16:96–105.
Quinn GP, Keough MJ. Experimental design and data analysis for biologists. (2002) Cambridge (UK): Cambridge University Press.
Robinson SK, Thompson FR 3rd, Donovan TM, Whitehead DR, Faaborg J. Regional forest fragmentation and the nesting success of migratory birds. Science (1995) 267:1987–1990.
Sasvári L. Great tits benefit from feeding in mixed-species flocks: a field experiment. Anim Behav (1992) 43:289–296.[CrossRef][Web of Science]
Sasvári L, Török J, Tóth L. Density dependence between three competitive bird species. Oecologia (1987) 72:127–130.[CrossRef][Web of Science]
Seppänen J-T, Forsman JT, Mönkkönen M, Thomson RL, Forthcoming. Social information use is a process across space, time and ecology, reaching heterospecifics. Ecology (2007) 88:622–1633.
Sinervo B, DeNardo D. Costs of reproduction in the wild: path analyses of natural selection and experimental tests of causation. Evolution (1996) 50:1299–1313.[CrossRef][Web of Science]
Slagsvold T. Competition between the great tit Parus major and the pied flycatcher Ficedula hypoleuca in the breeding season. Ornis Scand (1975) 6:179–190.[CrossRef]
Slagsvold T. Habitat selection in birds: on the presence of other species with species regard to Turdus pilaris. J Anim Ecol (1980) 49:523–536.[CrossRef]
Thomson RL, Forsman JT, Mönkkönen M. Positive interactions between migrant and resident birds: testing the heterospecific attraction hypothesis. Oecologia (2003) 134:431–438.[Web of Science][Medline]
Thomson RL, Forsman JT, Mönkkönen M, Hukkanen M, Koivula K, Rytkönen S, Orell M. Predation risk effects on fitness related measures in a resident bird. Oikos (2006) 113:325–333.[CrossRef][Web of Science]
Thomson RL, Forsman JT, Sardà-Palomera F, Mönkkönen M. Fear factor: prey habitat selection in a predation risk landscape. Ecography (2006) 29:507–514.
Timonen S, Mönkkönen M, Orell M. Does competition with residents affect the distribution of migrant territories? Ornis Fenn (1994) 71:55–60.
Valone TJ, Templeton JJ. Public information for the assessment of quality: a widespread social phenomenon. Philos Trans R Soc Lond B Biol Sci (2002) 357:1549–1557.
Walsberg GE. Physiological consequences of micro-habitat selection. In: Habitat selection in birds—Cody L, ed. (1985) Orlando (FL): Academic Press. 389–413.
Wedin D, Tilman D. Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecol Monogr (1993) 63:199–229.[CrossRef][Web of Science]
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