Richard Ubels

Experimental evidence for adaptive personalities in a wild passerine bird

Individuals of the same species differ consistently in risky actions. Such ‘animal personality’ variation is intriguing because behavioural flexibility is often assumed to be the norm. Recent theory predicts that between-individual differences in propensity to take risks should evolve if individuals differ in future fitness expectations: individuals with high long-term fitness expectations (i.e. that have much to lose) should behave consistently more cautious than individuals with lower expectations. Consequently, any manipulation of future fitness expectations should result in within-individual changes in risky behaviour in the direction predicted by this adaptive theory. We tested this prediction and confirmed experimentally that individuals indeed adjust their ‘exploration behaviour’, a proxy for risk-taking behaviour, to their future fitness expectations. We show for wild great tits (Parus major) that individuals with experimentally decreased survival probability become faster explorers (i.e. increase risk-taking behaviour) compared to individuals with increased survival probability. We also show, using quantitative genetics approaches, that non-genetic effects (i.e. permanent environment effects) underpin adaptive personality variation in this species. This study thereby confirms a key prediction of adaptive personality theory based on life-history trade-offs, and implies that selection may indeed favour the evolution of personalities in situations where individuals differ in future fitness expectations.

Density fluctuations represent a key process maintaining personality variation in a wild passerine bird

Heritable personality variation is subject to fluctuating selection in many animal taxa; a major unresolved question is why this is the case. A parsimonious explanation must involve a general ecological process: a likely candidate is the omnipresent spatiotemporal variation in conspecific density. We tested whether spatiotemporal variation in density within and among nest box plots of great tits (Parus major) predicted variation in selection acting on exploratory behaviour (n = 48 episodes of selection). We found viability selection favouring faster explorers under lower densities but slower explorers under higher densities. Temporal variation in local density represented the primary factor explaining personality-related variation in viability selection. Importantly, birds did not anticipate changes in selection by means of adaptive density-dependent plasticity. This study thereby provides an unprecedented example of the key importance of the interplay between fluctuating selection and lack of adaptive behavioural plasticity in maintaining animal personality variation in the wild.

Local sex ratio affects the cost of reproduction

1. Costs and benefits of reproduction are central to life-history theory, and the outcome of reproductive trade-offs may depend greatly on the ecological conditions in which they are estimated. In this study, we propose that costs and benefits of reproduction are modulated by social effects, and consequently that selection on reproductive rates depends on the social environment. 2. We tested this hypothesis in a great tit Parus major population. Over 3 years, we altered parental reproductive effort via brood size manipulations (small, intermediate, large) and manipulated the local social environment via changes in the local fledgling density (decreased, increased) and the local sex ratio (female-biased, control, male-biased). 3. We found that male-biased treatment consistently increased the subsequent local breeding densities over the 3-year study period. We also found that parents rearing small broods in these male-biased plots had increased survival rates compared with the other experimental groups. 4. We conclude that reproductive costs are the product of an interaction between parental phenotypic quality after reproduction and the social environment: raising a small brood had long-lasting effects on some phenotypic traits of the parents and that this increased their survival chances in male-biased environment where habitat quality may have deteriorated (via increased disease/predation risk or intraspecific competition). 5. Our results provide the first experimental evidence that local sex ratio can affect reproductive costs and thus optimal clutch size.

Exploring patterns of variation in clutch size-density reaction norms in a wild passerine bird

Negative density dependence of clutch size is a ubiquitous characteristic of avian populations and is partly due to within‐individual phenotypic plasticity. Yet, very little is known about the extent to which individuals differ in their degree of phenotypic plasticity, whether such variation has a genetic basis and whether level of plasticity can thus evolve in response to selection. Using 18 years of data of a Dutch great tit population (Parus major), we show that females reduced clutch size with increasing population density (slopes of the reaction norms), differed strongly in their average clutch size (elevations of the reaction norms) at the population‐mean density and that the latter variation was partly heritable. In contrast, we could not detect individual variation in phenotypic plasticity (‘I × E’). Level of plasticity is thus not likely to evolve in response to selection in this population. Observed clutch sizes deviated more from the estimated individual reaction norms in certain years and densities, implying that the within‐individual between‐year variance (so‐called residual variance) of clutch size was heterogeneous with respect to these factors. Given the observational nature of this study, experimental manipulation of density is now warranted to confirm the causality of the observed density effects. Our analyses demonstrate that failure to acknowledge this heterogeneity would have inflated the estimate of ‘I × E’ and led to misinterpretation of the data. This paper thereby emphasizes the fact that heterogeneity in residuals can provide biologically insightful information about the ecological processes underlying the data.

Intensive grazing by Barnacle geese depletes High Arctic seed bank

Studies in the Canadian Arctic show dramatic effects of increased goose grazing on vegetation structure and soil conditions, but little is known of the role of goose grazing in the European Arctic. We focused on how geese might affect plant recruitment via effects on seed production and soil seed bank in High Arctic Svalbard. Experimental grazing by captive Barnacle geese (Branta leucopsis (Bechstein, 1803)) decreased flower densities both at normal and at high graz- ing pressure. Geese showed a clear preference for reproductive rather than vegetative shoots. Soil samples collected inside and outside 7-year-old exclosures in an intensively goose-grazed area revealed significant effects on the germinable soil seed bank. The density of viable seeds in the top soil layer inside exclosures was six times higher than in grazed plots. Lower densities of viable seeds occurred in the basal than in the top layer but there was no difference in basal layer seed density between exclosed and grazed plots. This study shows that geese have strong effects on floral abundance and conse- quently on the seed bank. We argue that goose grazing in these systems influences the potential for recovery after a dis- turbance event and thus the long-term plant species diversity and dynamics.

The correlation between coloration and exploration behaviour varies across hierarchical levels in a wild passerine bird.

In vertebrates, darker individuals are often found to be more active and willing to take risks (representing characteristics of a ‘proactive’ coping style), whereas lighter individuals are instead more cautious and less active (representing characteristics of a ‘reactive’ coping style). It is thus generally expected that melanin‐based coloration and proactivity form a suite of positively integrated traits at the among‐individual level. Here, we use a multigenerational pedigree of free‐living great tits (Parus major) to partition variation in, and the correlation between, melanin‐based breast stripe (‘tie’) size and exploration behaviour (a proxy for coping style) into its among‐ and within‐individual components. We show that both traits harbour heritable variation. Against predictions, tie size and speed of exploration were negatively correlated at the among‐individual level due to the combined influences of permanent environmental and additive genetic effects. By contrast, the two traits were weakly positively correlated within individuals (i.e. individuals increasing in tie size after moult tended to become more explorative). The patterns of among‐individual covariance were not caused by correlational selection as we found additive and opposite selection pressures acting on the two traits. These findings imply that testing hypotheses regarding the existence of a ‘syndrome’ at the among‐individual level strictly requires variance partitioning to avoid inappropriate interpretations as the negative ‘unpartitioned’ phenotypic correlation between exploration and tie size resulted from counteracting effects of within‐ and among‐individual correlations. Identifying sources and levels of (co)variation in phenotypic traits is thus critical to our understanding of biological patterns and evolutionary processes.

Sex-specific effects of the local social environment on juvenile post-fledging dispersal in great tits

An individual’s decision to disperse from the natal habitat can affect its future fitness prospects. Especially in species with sex-biased dispersal, we expect the cost–benefit balance for dispersal to vary according to the social environment (e.g., local sex ratio and density). However, little is known about the social factors affecting dispersal decisions and about the temporal and spatial patterns of the dispersal process. In our study, we investigated experimentally the effects of the social environment on post-fledging dispersal of juvenile great tits by simultaneously manipulating the density and sex ratio of fledglings within forest plots. We expected young females in the post-fledging period mainly to compete for resources related to food and, as they are subordinate to males, we predicted higher female dispersal from male-biased plots. Juvenile males compete for vacant territories already in late summer and autumn; thus, we predicted increased male dispersal from high density and male-biased plots. We found that juvenile females had a higher probability to leave male-biased plots and had dispersed further from male-biased plots in the later post-fledging phase when juvenile males start to become territorial and more aggressive. Juvenile males were least likely to leave male-biased plots and had smallest dispersal distances from female-biased plots early after fledging. The results suggest that the social environment differentially affected the costs and benefits of philopatry for male and female juveniles. The local sex ratio of individuals is thus an important social trait to be considered for understanding sex-specific dispersal processes.

Density-dependent switches in diet: a likely mechanism for negative feedbacks on goose population increase?

Goose grazing on arctic tundra vegetation has shown both positive and negative effects on subsequent foraging conditions. To understand the potential of a density-dependent feedback on herbivore population size, the relation between grazing pressure and future foraging conditions is essential. We studied the effect of increasing grazing pressure of barnacle geese (Branta leucopsis) on Spitsbergen. During the establishment of a breeding colony in the period 1992–2004, the proportion of graminoids decreased in the diet of wild geese, while the percentage of mosses increased. Grazing trials with captive geese in an unexploited area showed a similar shift in diet composition. High-quality food plants were depleted within years and over years. Intake rate declined too and as consequence, metabolisable energy intake rate (MEIR) decreased rapidly with increasing grazing pressure. During three successive years of experimental grazing, MEIR decreased at all levels of grazing pressure and declined below minimal energetic requirements when grazing exceeded natural levels of grazing pressure. This suggests that foraging conditions rapidly decline with increasing grazing pressure in these low-productive habitats. The potential for density-dependent feedbacks on local population increase is discussed.

No experimental evidence for local competition in the nestling phase as a driving force for density‐dependent avian clutch size

1. In birds, local competition for food between pairs during the nestling phase may affect nestling growth and survival. A decrease in clutch size with an increase in breeding density could be an adaptive response to this competition. To investigate whether breeding density causally affected the clutch size of great tits (Parus major), we manipulated breeding density in three out of eight study plots by increasing nest-box densities. We expected clutch size in these plots to be reduced compared to that in control plots. 2. We analysed both the effects of variation in annual mean density (between-year comparisons) and experimental density (within-year comparison between plots) on clutch size variation, the occurrence of second broods and nestling growth. We examined within-female variation in clutch size to determine whether individual responses explain the variation over years. 3. Over the 11 years, population breeding density increased (from 0.33 to 0.50 pairs ha(-1)) while clutch size and the occurrence of second broods decreased (respectively from 10.0 to 8.5 eggs and from 0.39 to 0.05), consistent with a negative density-dependent effect for the whole population. Nestling growth showed a declining but nonsignificant trend over years. 4. The decline in population clutch size over years was primarily explained by changes occurring within individuals rather than selective disappearance of individuals laying large clutches. 5. Within years, breeding density differed significantly between manipulated plots (0.16 pairs ha(-1) vs. 0.77 pairs ha(-1)) but clutch size, occurrence of second broods and nestling growth were not affected by the experimental treatment, resulting in a discrepancy between the effects of experimental and annual variation in density on reproduction. 6. We discuss two hypotheses that could explain this discrepancy: (i) the decline in breeding performance over time was not due to density, but resulted from other, unknown factors. (ii) Density did cause the decline in breeding performance, but this was not due to local competition in the nestling phase. Instead, we suggest that competition acting in a different phase (e.g. before egg laying or after fledgling) was responsible for the density effect on clutch size among years.

Delayed Age at First Breeding and Experimental Removals Show Large Non-Breeding Surplus in Pied Flycatchers

Avian breeding populations have been shown to be regulated by territorial behaviour, often creating a surplus of non-breeding individuals. However, most evidence is of a male non-breeder surplus, whereas for a surplus to actually buffer a population both non-breeding males and females should be present. Here, we provide descriptive and experimental evidence for the existence of a population buffer consisting of mostly male and potentially also female Pied Flycatchers using nest box areas. First we show that local recruits often do not breed in their first year, with 23% of all recruiting males observed breeding in their first year, and 51% of females. When accounting for mortality in the years prior to observed first breeding, we estimate that only 9% of all first-year males breed locally, and 29% of first-year females. Similar percentages of first-year flycatchers skipping breeding have been observed in other study populations. We show that in the year of new establishment of our nest box plots, most known-aged flycatchers were first-year birds (77%), whereas after establishment, recruiting immigrants from the same source population were mostly older (28% first-year birds). An experimental removal of paired flycatchers from one study plot in two years (19 and 58 individuals removed) resulted in complete replacement by males and females. Male but not female replacements were younger than removed individuals. These results imply that a non-breeding surplus is present in Pied Flycatcher populations. The average later age at first-breeding in males compared to females, suggests that this non-breeding surplus is strongly male-biased. Skipping breeding in the first year(s) is not just caused by shortage of suitable nesting sites, as we observed on average 12% of males defending a nest box without pairing up with a female. Using stable isotopes ratios, we show that non-breeding first-year individuals do not stay at their African wintering grounds. Competition for nest sites is one cause for refraining from breeding, as shown by our experiments, but cannot be the sole cause, as many nest boxes remain unused in a season, and up to 20% of territorial males defend a nest box without pairing up with a female. We hypothesize that many young flycatchers arrive too late for breeding and are therefore not seen in their first year. Indeed first-year Pied Flycatchers that do breed/defend a nest box arrive on average later at the breeding grounds, and we argue that the non-observed group arrives even later. The causes of their later arrival could be the need for learning, lower quality wintering sites resulting in later departure, and/or a trade-off between low breeding success and the costs of early arrival. These could be general factors in long-distance migrants, and this pleads for a better understanding of how migration develops during ontogeny.