Christian Rutz

New frontiers in biologging science

The term ‘biologging’ refers to the use of miniaturized animal-attached tags for logging and/or relaying of data about an animals movements, behaviour, physiology and/or environment. Biologging technology substantially extends our abilities to observe, and take measurements from, free-ranging, undisturbed subjects, providing much scope for advancing both basic and applied biological research. Here, we review highlights from the third international conference on biologging science, which was held in California, USA, from 1 to 5 September 2008. Over the last few years, considerable progress has been made with a range of recording technologies as well as with the management, visualization, integration and analysis of increasingly large and complex biologging datasets. Researchers use these techniques to study animal biology with an unprecedented level of detail and across the full range of ecological scales—from the split-second decision making of individuals to the long-term dynamics of populations, and even entire communities. We conclude our report by suggesting some directions for future research.

Development of tool use in New Caledonian crows: inherited action patterns and social influences

New Caledonian crows, Corvus moneduloides, are the most advanced avian tool makers and tool users. We previously reported that captive-bred isolated New Caledonian crows spontaneously use twig tools and cut tools out of Pandanus spp. tree leaves, an activity possibly under cultural influence in the wild. However, what aspects of these behaviours are inherited and how they interact with individual and social experience remained unknown. To examine the interaction between inherited traits, individual learning and social transmission, we observed the ontogeny of twig tool use in hand-reared juveniles. Successful food retrieval was preceded by stereotyped object manipulation action patterns that resembled components of the mature behaviour, demonstrating that tool-oriented behaviours in this species are an evolved specialization. However, there was also an effect of social learning: juveniles that had received demonstrations of twig tool use by their human foster parent showed higher levels of handling and insertion of twigs than did their naive counterparts; a choice experiment showed that they preferred to handle objects that they had seen being manipulated by their human foster parent. Our observations are consistent with the hypothesis that individual learning, cultural transmission and creative problem solving all contribute to the acquisition of the tool-oriented behaviours in the wild, but inherited species-typical action patterns have a greater role than has been recognized.

Identifying governance strategies that effectively support ecosystem services, resource sustainability, and biodiversity

Conservation scientists, national governments, and international conservation groups seek to devise, and implement, governance strategies that mitigate human impact on the environment. However, few studies to date have systematically investigated the performance of different systems of governance in achieving successful conservation outcomes. Here, we use a newly-developed analytic framework to conduct analyses of a suite of case studies, linking different governance strategies to standardized scores for delivering ecosystem services, achieving sustainable use of natural resources, and conserving biodiversity, at both local and international levels. Our results: (i) confirm the benefits of adaptive management; and (ii) reveal strong associations for the role of leadership. Our work provides a critical step toward implementing empirically justified governance strategies that are capable of improving the management of human-altered environments, with benefits for both biodiversity and people.

The establishment of an urban bird population

1. Despite the accelerating global spread of urbanized habitats and its associated implications for wildlife and humans, surprisingly little is known about the biology of urban ecosystems. 2. Using data from a 60-year study period, this paper provides a detailed description of how the northern goshawk Accipiter gentilis L.--generally considered a shy forest species--colonized the city of Hamburg, Germany. Six non-mutually exclusive hypotheses are investigated regarding the environmental factors that may have triggered this invasion. 3. The spatio-temporal analysis of 2556 goshawk chance observations (extracted from a total data set of 1 174 493 bird observations; 1946-2003) showed that hawks regularly visited the city centre decades before the first successful breeding attempts were recorded. Many observations were made in parts of the city where territories were established in later years, demonstrating that these early visitors had encountered, but not used, potential nest sites. 4. Pioneer settlement coincided with: (i) an increase in (legal) hunting pressure on goshawks in nearby rural areas; (ii) an increase in avian prey abundance in the city; and (iii) a succession of severe winters in the Greater Hamburg area. On the other hand, there was no evidence to suggest that the early stages of the invasion were due to: (i) decreasing food availability in rural areas; (ii) major habitat changes in the city; or (iii) rural intraguild dynamics forcing hawks into urban refugia. While breeding numbers of a potential rural source population were at a long-term low when the city was colonized, prior to first settlement there was a sharp increase of goshawk chance observations in the city and its rural periphery. 5. The urban population expanded rapidly, and pair numbers began to stabilize after about 10 years. Ringing data (219 ringed nestlings from 70 urban broods; 1996-2000) demonstrated that most urban recruits had fledged in the city, but also confirmed considerable gene flow between urban and rural habitats. Analysis of chance observations (as raw data or as detrended time series) suggested a tight coupling of population dynamics inside and outside the city. 6. City-colonizations such as the one described here provide a valuable opportunity to study some fundamental aspects of population ecology on a scale at which detailed monitoring is logistically feasible. Furthermore, a good understanding of urban ecology has become essential for efficient wildlife conservation in modern, human-altered environments.

Age-dependent diet choice in an avian top predator

Age-dependent breeding performance is arguably one of the best-documented phenomena in ornithology. The existence of age-related trends has major implications for life-history theory, but the proximate reasons for these patterns remain poorly understood. It has been proposed that poor breeding performance of young individuals might reflect lack of foraging skills. We investigated this possibility in a medium-sized, powerful raptor—the northern goshawk Accipiter gentilis. Male goshawks are responsible for providing their females and their offspring with food. We hypothesized that young males may generally show poor breeding performance or even delay breeding, because they lack the experience to hunt efficiently—especially, their principal avian prey, the feral pigeon Columba livia. Our study exploited a rare ‘natural experiment’, the expansion phase of an urban population, where intraspecific interference was negligible and many young males bred successfully. This enabled us to examine the improvement of foraging skills in a larger sample of young individuals, and in more controlled conditions than usually possible. Using data from individually identified male breeders, we show that, consistent with our hypothesis, the proportion of pigeons in the diet increased significantly with male age, for at least the first three years of life. Other studies have shown a parallel increase in productivity, and a positive effect of a pigeon-rich diet on brood size and nestling condition, stressing the potential fitness relevance of this prey species for goshawks. Our results suggest a causal link between patterns of age-dependence in foraging ecology and reproductive performance. Furthermore, our study is, to our knowledge, the first demonstration that prey choice of breeders, which might reflect individual hunting skills, is age-dependent in a raptor.

Food-limitation in a generalist predator

Investigating food-limitation in generalist predators is difficult, because they can switch to alternative prey, when one of their staple prey becomes scarce. Apart from data on the dynamics of the predator population, a robust study requires: (i) a documentation of the predators entire prey base; and (ii) an experimental or natural situation, where profitable dietary shifts are impossible, because several preferred prey species decline simultaneously. Here, we provide a detailed description of how food-supply has limited a generalist avian top predator, the northern goshawk Accipiter gentilis. In our study area, populations of several principal goshawk prey species crashed simultaneously during 1975–2000, whereas other extrinsic factors remained essentially unchanged. The breeding and non-breeding segments of the local goshawk population declined markedly, associated with a significant increase in nest failures. Brood size of successful pairs remained unaffected by changes in prey availability. Breeding recruitment ceased at a time when potential replacement birds (‘floaters’) were still present, providing a rare empirical demonstration of an ‘acceptance threshold’ in raptor territory choice. To investigate how goshawk diet changed in response to varying food-supplies, we make novel use of an analytical tool from biodiversity research—‘abundance–biomass–comparison curves’ (ABC curves). With increasing levels of food-stress, the dominance of principal prey species in the diet decreased, and the number of small-bodied prey species increased, as did intra-guild predation. Our finding that breeder and non-breeder segments declined in concert is unexpected. Our results carry the management implication that, in food-limited raptor populations, externally induced breeder mortality can rapidly depress population size, as losses are no longer buffered when floaters reject breeding opportunities.

Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows.

Humans are expert tool users, who manipulate objects with dextrous hands and precise visual control. Surprisingly, morphological predispositions, or adaptations, for tool use have rarely been examined in non-human animals. New Caledonian crows Corvus moneduloides use their bills to craft complex tools from sticks, leaves and other materials, before inserting them into deadwood or vegetation to extract prey. Here we show that tool use in these birds is facilitated by an unusual visual-field topography and bill shape. Their visual field has substantially greater binocular overlap than that of any other bird species investigated to date, including six non-tool-using corvids. Furthermore, their unusually straight bill enables a stable grip on tools, and raises the tool tip into their visual fields binocular sector. These features enable a degree of tool control that would be impossible in other corvids, despite their comparable cognitive abilities. To our knowledge, this is the first evidence for tool-use-related morphological features outside the hominin lineage.

Tool use by wild New Caledonian crows Corvus moneduloides at natural foraging sites.

New Caledonian crows Corvus moneduloides use tools made from sticks or leaf stems to ‘fish’ woodboring beetle larvae from their burrows in decaying wood. Previous research on this behaviour has been confined to baited sites, leaving its ecological context and significance virtually unexplored. To obtain detailed observations of natural, undisturbed tool use, we deployed motion-triggered video cameras at seven larva-fishing sites. From 1797 camera hours of surveillance over 111 days, we recorded 317 site visits by at least 14 individual crows. Tool use was observed during 150 site visits. Our video footage revealed notable variation in foraging success among identifiable crows. Two nutritionally independent, immature crows spent considerable time using tools, but were much less successful than local adults, highlighting the potential role of individual and social learning in the acquisition of tool-use proficiency. During systematic surveys of larva-fishing sites, we collected 193 tools that crows had left inserted in larva burrows. Comparing these tools with the holes in which they were found, and with raw materials available around logs, provides evidence for tool selectivity by New Caledonian crows under natural conditions. Taken together, these two complementary lines of investigation provide, to our knowledge, the first quantitative description of larva fishing by wild crows in its full ecological context.

Assessing the breeding season diet of goshawks Accipiter gentilis: biases of plucking analysis quantified by means of continuous radio-monitoring

Plucking analysis is a standard method for assessing the breeding season diet of goshawks Accipiter gentilis .R esults may be biased, however, due to differences in the detectability of remains of certain prey species and to selective prey transportation by hawks. This study investigated prey choice of three goshawk breeding pairs in the city of Hamburg, Germany, during 1997–99. Predation data obtained by continuous radio-monitoring of the adult males were used to quantify biases of simultaneous plucking analyses, which were conducted in the nesting territories of the corresponding breeding pairs. A comparison of estimated average food requirements with actual biomass intake observed in two of the monitored goshawks (with sufficient sample sizes) indicated that it was possible to record virtually all kills that occurred during tracking sessions. Therefore, radio-tracking data could be used to evaluate the accuracy of plucking analysis. Comparisons showed that the proportions of small birds and of feral pigeons Columba livia f. domestica were underestimated by the scanning method by 10% and 13%, respectively. The latter finding was unexpected as pigeons have large, conspicuously coloured feathers that are easy to detect. However, as goshawks plucked large prey more thoroughly at the capture site than smaller prey, a comparatively small number of their feathers were present in the nesting areas. This source of bias in plucking analysis has passed unnoticed in previous studies. It may have important implications for the interpretation of results of future projects that aim to estimate predation rates in goshawks and other bird-eating raptor species.

New Caledonian crows attend to multiple functional properties of complex tools

The ability to attend to the functional properties of foraging tools should affect energy-intake rates, fitness components and ultimately the evolutionary dynamics of tool-related behaviour. New Caledonian crows Corvus moneduloides use three distinct tool types for extractive foraging: non-hooked stick tools, hooked stick tools and tools cut from the barbed edges of Pandanus spp. leaves. The latter two types exhibit clear functional polarity, because of (respectively) a single terminal, crow-manufactured hook and natural barbs running along one edge of the leaf strip; in each case, the ‘hooks’ can only aid prey capture if the tool is oriented correctly by the crow during deployment. A previous experimental study of New Caledonian crows found that subjects paid little attention to the barbs of supplied (wide) pandanus tools, resulting in non-functional tool orientation during foraging. This result is puzzling, given the presumed fitness benefits of consistently orienting tools functionally in the wild. We investigated whether the lack of discrimination with respect to (wide) pandanus tool orientation also applies to hooked stick tools. We experimentally provided subjects with naturalistic replica tools in a range of orientations and found that all subjects used these tools correctly, regardless of how they had been presented. In a companion experiment, we explored the extent to which normally co-occurring tool features (terminal hook, curvature of the tool shaft and stripped bark at the hooked end) inform tool-orientation decisions, by forcing birds to deploy ‘unnatural’ tools, which exhibited these traits at opposite ends. Our subjects attended to at least two of the three tool features, although, as expected, the location of the hook was of paramount importance. We discuss these results in the context of earlier research and propose avenues for future work.