The behavioural ecology of provisioning in birds

Ydenberg, R. 2000. The behavioural ecology of provisioning in birds. Ostrich 71 (1): 361.

In this talk I outline the idea of provisioning, stressing the difference between feeding and delivery. Foraging studies have just begun to recognise this distinction, and to explore some of its implications for behaviour. I outline a basic model of provisioning, based on central place foraging, in which the forager must spend some extra time on each excursion to gather enough energy to cover the excursion's energetic costs. I describe studies of provisioning pertinent to this framework, and go on to consider risk-sensitive provisioning, the role of predation danger in provisioning, and the question of how hard provisioners should work.     

The origin and early evolution of birds

Birds evolved from and are phylogenetically recognized as members of the theropod dinosaurs; their first known member is the Late Jurassic Archaeopteryx, now represented by seven skeletons and a feather, and their closest known non-avian relatives are the dromaeosaurid theropods such as Deinonychus. Bird flight is widely thought to have evolved from the trees down, but Archaeopteryx and its outgroups show no obvious arboreal or tree-climbing characters, and its wing planform and wing loading do not resemble those of gliders. The ancestors of birds were bipedal, terrestrial, agile, cursorial and carnivorous or omnivorous. Apart from a perching foot and some skeletal fusions, a great many characters that are usually considered ‘avian’ (e.g. the furcula, the elongated forearm, the laterally flexing wrist and apparently feathers) evolved in non-avian theropods for reasons unrelated to birds or to flight. Soon after Archaeopteryx, avian features such as the pygostyle, fusion of the carpometacarpus, and elongated curved pedal claws with a reversed, fully descended and opposable hallux, indicate improved flying ability and arboreal habits. In the further evolution of birds, characters related to the flight apparatus phylogenetically preceded those related to the rest of the skeleton and skull. Mesozoic birds are more diverse and numerous than thought previously and the most diverse known group of Cretaceous birds, the Enantiornithes, was not even recognized until 1981. The vast majority of Mesozoic bird groups have no Tertiary records: Enantiornithes, Hesperornithiformes, Ichthyornithiformes and several other lineages disappeared by the end of the Cretaceous. By that time, a few Linnean ‘Orders’ of extant birds had appeared, but none of these taxa belongs to extant ‘families’, and it is not until the Paleocene or (in most cases) the Eocene that the majority of extant bird ‘Orders’ are known in the fossil record. There is no evidence for a major or mass extinction of birds at the end of the Cretaceous, nor for a sudden ‘bottleneck’ in diversity that fostered the early Tertiary origination of living bird ‘Orders’.     

The ecology of mangrove forest birds in Peninsular Malaysia

The density, distribution and feeding ecology of birds of mangrove forests in Selangor on the west coast of Peninsular Malaysia were investigated between February and May 1989. Excluding aerial hunters and wading birds, 47 species were recorded from four mangrove forest sites in Selangor, though undoubtedly some rarer species were missed due to the brevity of the study. The estimated density of birds, using fixed-width transects, ranged from 15 to 26 birds per ha. One quarter of all birds counted belonged to just one species, the Ashy Tailorbird Orthotomus ruficeps. Excluding ground feeders (three species), four foraging guilds were recognized among 17 of the commonest bird species: obligate foliage-foraging insectivores (seven species), bark-foraging insectivores (four), facultative nectar-ivores (five) and aerial hawkers (one). Species within the first and third guilds apparently were partitioned by foraging technique and heights, while those of the second guild (woodpeckers) differed mainly in their selection of plant species. The horizontal distribution of several species corresponded to the zonation of mangroves. Avifaunal differences between sites reflected differences in forest floristics. The greatest number of species occurred at the dry landward edge site, which supported seven bird species not encountered elsewhere in Selangor. This habitat has almost completely disappeared from much of the peninsula owing to land reclamation. Four of the six resident mangrove-specialized bird species in Selangor were regularly recorded at two or more sites, another (Greater Gol-denback Woodpecker Chrysocolaptes lucidus) occurred at only one site and the last (Ruddy Kingfisher Halcyon coromanda) was never recorded. Two species of sunbirds probably play an important role in the pollination of several species of mangroves. The colonization of anthropogenic habitats by many mangrove-dwelling bird species is attributed partly to their generalized foraging niches, which may have evolved in response to regular fluctuations in food availability and the dynamic physiography of mangrove communities.     

Relative brain size and ecology in birds

We test the hypothesis that the relative sizes of the different parts of the brain (brain stem, optic lobes, cerebellum and cerebral hemispheres), measured after body size effects have been removed, are associated with differences in behaviour and ecology across bird species.
The results demonstrate that behavioural and ecological correlates of relative brain size are not independent of each other. When the effects of variation in other categories are accounted for, the strongest single effect is due to relatively large brain sizes being associated with altricial development. It is unlikely that this effect is due to the confounding influence of taxonomic associations.
Overall, the results do not provide support for the idea that differences in measures of environmental complexity select for differences in relative brain size.     

Cooperative breeding in birds: the role of ecology

Theory predicts that cooperative breeding should only occurin species in which certain individuals are constrained frombreeding independently by some peculiarity of the species' ecology.Here, we use comparative methods to examine the role of variationin ecology in explaining differences between taxa in the frequencyof cooperative breeding. We address three questions. First,does the frequency of cooperative breeding vary at just one phylogeneticlevel, or across several levels? Second, are differences inthe frequency of cooperative breeding among closely-relatedspecies correlated with ecology? Last, are ecological differencesbetween ancient lineages important in predisposing certain lineagesto cooperative breeding? We find that variation in the frequencyof cooperative breeding occurs across all phylogenetic levels,with 40% among families and 60% within families. Also, variationin the frequency of cooperative breeding between closely related speciesis associated with ecological differences. However, differencesin the frequency of cooperative breeding among more ancientlineages are not correlated with differences in ecology. Together,our results suggest that cooperative breeding is not due toany single factor, but is a two step-process: life-history predispositionand ecological facilitation. Low annual mortality predisposescertain lineages to cooperative breeding. Subsequently, changesin ecology facilitate the evolution of cooperative breedingwithin these predisposed lineages. The key ecological changesappear to be sedentariness and living in a relatively invariableand warm climate. Thus, although ecological variation is notthe most important factor in predisposing lineages to cooperativebreeding, it is important in determining exactly which speciesor populations in a predisposed lineage will adopt cooperativebreeding.     

Physical constraints on the foraging ecology of a predatory snail

We studied the effects of aerial exposure and high summer temperatures on the southern oyster drill ( Stramonita haemastoma ), feeding on the American oyster, Crassostrea virginica . In the laboratory, oyster drill feeding rates and growth were highest at 25 and 30°C, some mortality occurred at 35°C, all snails died at 40 and 45°C, and the 28-day LC 50 was 35.7°C. In a second experiment where both water temperature (25 vs . 33°C) and aerial exposure were varied, only simulated tidal exposure lowered oyster drill feeding and growth rates. In field cage experiments, oyster drills had reduced feeding rates and growth at intertidal sites, but snail growth rates increased in late summer with warmer water temperature. We therefore conclude that aerial exposure, not high temperature, is the major factor limiting oyster drill feeding and growth in intertidal oyster reefs. Field experiments with partial cages also suggested that ambient predation rates were much higher at a subtidal than at a nearby intertidal site. Because southern oyster drills have depressed feeding, growth, and possibly lower fitness in intertidal oyster reefs during the summer, this reduced predation risk may provide a refuge for intertidal oysters.     

Differences in predatory pressure on terrestrial snails by birds and mammals

The evolution of shell polymorphism in terrestrial snails is a classic textbook example of the effect of natural selection in which avian and mammalian predation represents an important selective force on gene frequency. However, many questions about predation remain unclear, especially in the case of mammals. We collected 2000 specimens from eight terrestrial gastropod species to investigate the predation pressure exerted by birds and mice on snails. We found evidence of avian and mammalian predation in 26.5% and 36.8% of the shells. Both birds and mammals were selective with respect to snail species, size and morphs. Birds preferred the brown-lipped banded snail Cepaea nemoralis (L.) and mice preferred the burgundy snail Helix pomatia L. Mice avoided pink mid-banded C. nemoralis and preferred brown mid-banded morphs, which were neglected by birds. In contrast to mice, birds chose larger individuals. Significant differences in their predatory pressure can influence the evolution and maintenance of shell size and polymorphism of shell colouration in snails.     

Variations in cone photoreceptor abundance and the visual ecology of birds

The relative abundance and topographical distribution of retinal cone photoreceptors was measured in 19 bird species to identify possible correlations between photoreceptor complement and visual ecology. In contrast to previous studies, all five types of cone photoreceptor were distinguished, using bright field and epifluorescent light microscopy, in four retinal quadrants. Land birds tended to show either posterior dorsal to anterior ventral or anterior dorsal to posterior ventral gradients in cone photoreceptor distribution, fundus coloration and oil droplet pigmentation across the retina. Marine birds tended to show dorsal to ventral gradients instead. Statistical analyses showed that the proportions of the different cone types varied significantly across the retinae of all species investigated. Cluster analysis was performed on the data to identify groups or clusters of species on the basis of their oil droplet complement. Using the absolute percentages of each oil droplet type in each quadrant for the analysis produced clusters that tended to reflect phylogenetic relatedness between species rather than similarities in their visual ecology. Repeating the analysis after subtracting the mean percentage of a given oil droplet type across the whole retina (the 'eye mean') from the percentage of that oil droplet type in each quadrant, i.e. to give a measure of the variation about the mean, resulted in clusters that reflected diet, feeding behaviour and habitat to a greater extent than phylogeny.     

Hormones in the city: endocrine ecology of urban birds

Urbanization dramatically changes the landscape, presenting organisms with novel challenges and often leading to reduced species diversity. Urban ecologists have documented numerous biotic and abiotic consequences of urbanization, such as altered climate, species interactions, and community composition, but we lack an understanding of the mechanisms underlying organisms' responses to urbanization. Here, I review findings from the nascent field of study of the endocrine ecology of urban birds. Thus far, no clear or consistent patterns have been revealed, but we do have evidence that urban habitat can shape endocrine traits, and that those traits might contribute to adaptation to the urban environment. I suggest strong approaches for future work addressing exciting questions about the role of endocrine traits in mediating responses to urbanization within species across the globe.     

A theoretical basis for the study of predatory syrphid fly ecology

Predacious syrphid fly species, also known as flower flies or hover flies, are cosmopolitan diptera that play two important ecological roles: predator and pollinator. In decades past, syrphid flies were studied by agricultural researchers due to their larvae’s ability to function as a biological control agent. In recent years, the global decline in both honey bees and various important wild bee species has led ecological researchers to investigate the role of syrphid fly pollination in both natural systems and agriculture. While these two roles have often been considered separately, they are rarely considered together in single studies. Syrphid fly population fluctuations in natural and agricultural systems are understudied, prompting calls for further study into the fundamental drivers of population dynamics of syrphid communities. In order to develop a deeper understanding of the fundamental dynamics of syrphid ecology, the present study offers a community model where both syrphid predation and pollination are incorporated into a single dynamic model. Using populations of predacious syrphid flies, herbivorous insects, and a shared resource flowering plant, the model is used to investigate community dynamics and persistence across different levels of plant reproductive dependence on syrphid pollination. Results indicate distinct levels of community viability across different pollination relationships as well as a tendency toward chaotic dynamics inherent to the trophic interactions of the community.     

Behaviour and ecology of birds in tropical rain forest canopies

The canopy of rain forests exhibits several distinct features that determine avian adaptations. Light intensity and colour, wind, and temperature are the most important components of the physical environment. Tree architecture poses many challenges for the evolution of avian morphological features, and resource availability varies greatly. The canopy is easily accessible for birds that are equipped to travel over considerable distances. Given these conditions, high behavioural flexibility, and adaptations in behaviour and morphology related to a nomadic life-style, should prevail among canopy birds. The easy access for certain groups of birds also has consequences for the historical processes that shape canopy bird communities. Birds may contribute greatly to forest dynamics and composition, mainly due to their role as seed dispersers. We elaborate on these points with behavioural, morphological, and ecological data collected at our Neotropical study site in southern Venezuela (Surumoni Canopy Crane Project). We discuss how behaviour and morphological features reflect the ecological demands in the canopy. We contrast the specific behavioural and ecological characteristics of canopy birds with those of species found in the other tiers of the rain forest. It is pointed out that much of our knowledge is biased towards the Neotropics, and that better knowledge of the larger canopy species is needed for conservation.     

The predatory Chironomidae of an iron-rich stream: feeding ecology and food web structure

Abstract. 1. Three species of Tanypodinae (Chironomidae) were found in an acid and iron-rich stream in southern England. Maximum abundance was achieved in summer and they were sparse at other times. Individuals were aggregated on the stream bed and were overrepresented in accumulations of leaf litter.
2. The diets of all three species consisted of a mixture of prey (prominently detritivorous chironomid larvae) and detritus. More detritus and fewer prey were taken in winter than in summer.
3. When comparing large tanypod species with small and, intraspecifically, late instars with early, the proportion of guts containing prey increased with increasing body size.
4. Stonefly larvae were more prominent in the diet of Zavrelimyia barbatipes (Kieffer) in summer than in winter but for the other two species the reverse was true. A bigger proportion of Trissopelopia longimana (Staeger) guts contained prey in early summer than in August whereas more Macropelopia goetghebueri (Kieffer) guts contained prey in August. This was apparently a consequence of seasonal differences in the distribution of body size among the populations of these two species.
5. The stream contains two further common predators, Plectrocnemia conspersa (Curtis) and Sialis fuliginosa Pict. These are important predators of tanypod larvae but might also compete with them since they severely deplete populations of prey taken in common.
6. Analysis of the food-web in Broadstone Stream reveals remarkably high values of connectance (C and C_max) and of species richness times connectance (SC_max). Such characteristics are theoretically associated with fragile and dynamically unstable food webs, and may be found in 'constant' environments. There is also an apparently unusual prevalence of omnivory in the community.     

The evolution of communal roosting in birds: origin and secondary losses

Three main benefits are thought to underlie communal roostingin birds: areduction in thermoregulation demands, a decreasein predation risk, and anincrease in foraging efficiency. Iinvestigated interspecific variation incommunal roosting tendenciesacross categories of several ecological factorsto examine therelevance of each functional hypothesis in the evolutionarytransitionto communal roosting and the secondary reversal to solitaryroostinghabits. The study phylogenetic tree included 30 families and437species. Evolutionary transitions to communal roosting occurredmore often onbranches with flocking species and with largerspecies but were not associatedwith diet, territoriality, geographicalarea, or time of day. The associationwith flocking activitiessuggests that increased foraging efficiency, a factorthoughtto operate through the formation of flocks, may have been akey factorin the origin of avian communal roosting. However,several transitions tocommunal roosting occurred on brancheswith nonflocking species, indicatingthat foraging efficiencymay not be the only factor involved in the evolutionof communalroosting. Secondary losses of communal roosting habits occurredonseveral branches, with a concomitant loss of flocking behaviorand a tendencyto exhibit territorial behavior and nocturnalforaging. Secondary lossessuggest that communal roosting iscostly to perform and maintain and may belost when an asocialselection regime operates. The large number of exceptionstothe above patterns may force a reevaluation of current functionalhypothesesabout communal roosting in birds.     

On the origin of brood parasitism in altricial birds

The probability that obligate interspecific brood parasitism(OP), among altricial birds evolved directly from the normalbreeding (no parasitism, NP) mode or indirectly through intraspecificnest parasitism (INP) was examined by using maximum-likelihoodand parsimony approaches. We examined the probability of ancestralstates at 24 key nodes in order to test our hypotheses. Thestate of the most basal node in a tree of 565 genera of altricialbirds is equivocal; however, the state probability of NP atthis node is about 5.5-fold more likely than the state of obligateparasite. A similar trend was observed for basal nodes of mostfamilies examined. The INP state was supported only in the Hirundinidae.The high incidence of INP among martins and swallows explainsthis finding. Contrary to our predictions, even in other groupswhere there is a high incidence of INP and OP, such as in thetribe Icteri and the Old World finches, the probability of NPbeing ancestral was very high. We conclude that in all casesbut one (Hirundinidae) obligate, and probably facultative, broodparasitism evolved directly from normal breeding mode ratherthan indirectly through some other form of parasitism.     

Torpor in birds: taxonomy, energetics, and ecology

Recent reports on patterns and occurrence of torpor and other natural hypothermic states in birds have prompted a revision of many longstanding opinions. For instance, a larger assortment of birds covering a wider range of body mass than previously recognized uses energy-conserving mechanisms in the face of abundant food supplies. Thus, although acute energetic stress triggers the occurrence of hypometabolic states in many birds, energy deficits can no longer be regarded as the sole stimulus for avian torpor. Additionally, the phenology of this phenomenon (phases, duration, depth) shows more interspecific variation than previously appreciated, and traditional concepts of the phases of torpor are not always adequate. Hence, inclusive definitions of torpor based on physiological and/or behavioral criteria have become more difficult to formulate. However, average nighttime body temperature, which is highly consistent throughout the class Aves (38.54 degrees +/- 0.96 degrees C, n = 202), provides a convenient reference for detecting natural hypothermic states. Of the putative ecological factors associated with avian torpor, food specialization seems a prime candidate as an ultimate factor in the occurrence of this state in birds. With few exceptions, all of these animals capable of torpor are either frugivorous, nectarivorous, or insectivorous, suggesting a correlation between thermoregulatory pattern and predictability of food supply. To date, no clear answer exists as to whether the variety of thermoregulatory patterns evident in birds involves discrete mechanisms or merely steps in a physiological continuum. However, I suggest that the occurrence of differences in torpor patterns among closely related species (e.g., within families) favors the latter interpretation.