A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees

Honeybees, Apis mellifera, show age-related division of labor in which young adults perform maintenance ("housekeeping") tasks inside the colony before switching to outside foraging at approximately 23 days old. Disease resistance is an important feature of honeybee biology, but little is known about the interaction of pathogens and age-related division of labor. We tested a hypothesis that older forager bees and younger "house" bees differ in susceptibility to infection. We coupled an infection bioassay with a functional analysis of gene expression in individual bees using a whole genome microarray. Forager bees treated with the entomopathogenic fungus Metarhizium anisopliae s.l. survived for significantly longer than house bees. This was concomitant with substantial differences in gene expression including genes associated with immune function. In house bees, infection was associated with differential expression of 35 candidate immune genes contrasted with differential expression of only two candidate immune genes in forager bees. For control bees (i.e. not treated with M. anisopliae) the development from the house to the forager stage was associated with differential expression of 49 candidate immune genes, including up-regulation of the antimicrobial peptide gene abaecin, plus major components of the Toll pathway, serine proteases, and serpins. We infer that reduced pathogen susceptibility in forager bees was associated with age-related activation of specific immune system pathways. Our findings contrast with the view that the immunocompetence in social insects declines with the onset of foraging as a result of a trade-off in the allocation of resources for foraging. The up-regulation of immune-related genes in young adult bees in response to M. anisopliae infection was an indicator of disease susceptibility; this also challenges previous research in social insects, in which an elevated immune status has been used as a marker of increased disease resistance and fitness without considering the effects of age-related development

Behavioral conservatism is linked to complexity of behavior in chimpanzees (<i>Pan troglodytes</i>):implications for cognition and cumulative culture

Cumulative culture is rare, if not altogether absent in nonhuman species. At the foundation of cumulative learning is the ability to modify, relinquish, or build upon previous behaviors flexibly to make them more productive or efficient. Within the primate literature, a failure to optimize solutions in this way is often proposed to derive from low-fidelity copying of witnessed behaviors, suboptimal social learning heuristics, or a lack of relevant sociocognitive adaptations. However, humans can also be markedly inflexible in their behaviors, perseverating with, or becoming fixated on, outdated or inappropriate responses. Humans show differential patterns of flexibility as a function of cognitive load, exhibiting difficulties with inhibiting suboptimal behaviors when there are high demands on working memory. We present a series of studies on captive chimpanzees that indicate that behavioral conservatism in apes may be underlain by similar constraints: Chimpanzees showed relatively little conservatism when behavioral optimization involved the inhibition of a well-established but simple solution, or the addition of a simple modification to a well-established but complex solution. In contrast, when behavioral optimization involved the inhibition of a well-established but complex solution, chimpanzees showed evidence of conservatism. We propose that conservatism is linked to behavioral complexity, potentially mediated by cognitive resource availability, and may be an important factor in the evolution of cumulative culture.</p

Foraging strategies of an aerial-hawking insectivore, the common noctule bat Nyctalus noctula

Movement is a key signature of life. Yet, the integration of movement ecology and biodiversity concepts was only recently formalize. In this framework, an individual’s movement path and the underlying drivers are used to explain interactions between individuals and eventually species coexistence. Interactions influence the individual’s environment including species assemblage, and thereby feed back on the individual’s movement path. Foraging represents one of the most common movements of many animals, and thus has been of interest for ecologists ever since. Yet, classical foraging ecology predominantly focused on optimality models to explain the behaviour of single foragers, but rarely took into account the interactions between moving individuals. The overarching question of the three studies in this thesis thus was “How can different foraging strategies support coexistence?”. Being highly mobile and showing a large niche overlap with several other species, the insectivorous Common noctule bat Nyctalus noctula (Schreber, 1774) is an ideal model species to study intra- and interspecific interactions during foraging movements. I therefore investigated movement behaviour and space use of N. noctula during aerial foraging, and evaluated the potential role of different foraging strategies for the coexistence of competing bat species in the light of different competitor densities and prey distributions. In chapter one, I asked whether foraging N. noctula adjust their space use to abiotic factors (i.e. moonlight) which might be linked to prey distribution. I used GPS (global positioning system) loggers to investigate the habitat use of nine N. noctula during high and low moonlight intensities. During moonlit nights, N. noctula hunted preferentially over open fields, whereas they avoided open fields in dark nights. I suppose that foraging activity followed changes in insect activity triggered by the lunar cycle. The results suggest that N. noctula might be able to predict cyclic changes in prey distribution. The exploitation of prey aggregations in lit habitats might be an advantage towards competing bat species that are less light tolerant. In chapter two, I asked whether the use of social foraging by N. noctula depends on season, possibly as a response to changes in insect availability. I quantified N. noctula activity at foraging sites in early and late summer during acoustic playbacks of either hunting conspecifics or heterospecifics. N. noctula activity increased during heterospecific playbacks in early summer, but decreased in late summer. There was no clear reaction towards conspecific playbacks, irrespective of the season. The results suggest that external factors determine the strengths of intraspecific and interspecific competition, but that insectivorous bats mitigate different competitive pressures through flexibility in foraging strategy and fine scale space use. I argue that conspecific might impair each other by acoustic interference of echolocation calls and competition for flight space. However, niche segregation might make social foraging with heterospecifics beneficial, given that there is low competition for prey items. In chapter three, I asked whether the foraging strategy of N. noctula depends on the combination of conspecifics density and landscape features that might determine prey distribution. I used combined GPS-ultrasound loggers to record the nightly foraging movements and hunting activity of 27 N. noctula above farmland and forested landscape. Acoustic records also allowed quantification of nearby conspecifics. I deduced two movement states - area restricted movement and directed movement - from the GPS tracks. Above farmland, N. noctula switched to area restricted movements after encounters with conspecifics, and foraging activity was highest during those movements. Above forested landscape, encounters with conspecifics had little influence on the movement behaviour of N. noctula, and foraging activity occurred during directed and area restricted movements alike. N. noctula encountered more conspecifics above the forested landscape than above farmland. I argue that N. noctula was able to integrate prey distribution and competitive pressure when deciding whether or not to pursue a social foraging strategy. The use of a social foraging strategy might be a prerequisite for survival in agricultural landscapes where prey is patchily distributed and ephemeral. In contrast, solitary foraging might be the optimal strategy in forested landscapes that offer evenly distributed prey and support larger populations. In conclusion, the results showed that N. noctula integrated environmental factors that probably influenced prey distribution, adverse effects from intra- and interspecific competition, and public information about prey availability provided by hunting con- and heterospecifics. N. noctula used this compiled information to decide where to forage and whether to forage solitary or socially. The studies highlighted that N. noctula can adjust its foraging strategy context dependently. This flexibility was achieved through dynamic feedbacks between the movement paths and the perceived environment. These dynamic feedbacks may play a pivotal role in promoting the coexistence of competing species. In particular, the similarity of movement behaviours and resulting foraging strategies among conspecifics might stabilize species assemblages through intraspecific competition, while slight differences in the movement behaviour among heterospecifics might allow fine-scale niche segregation and thereby equalize the fitness of coexisting species. I propose that dynamic foraging behaviour might act stabilizing and equalizing not only in insectivorous bats but on assemblages of highly mobile predators in general

Processes underlying the fine-scale partitioning and niche diversification in a guild of coral reef damselfishes

A major goal of ecology is to explain the mechanisms that drive species distributions and ecological partitioning along gradients in the natural environment. The distributions and coexistence of ecologically similar animals may depend on the degree of niche diversification and competitive interactions within and among species. The extent of ecological partitioning in guilds of coral reef fishes was hotly debated in the 1980s, and despite 4 decades of research, the issue remains unresolved. In particular, the link between niche partitioning and agonistic interactions together have received little attention. In the thesis I investigated finescale species distributions, resource use (e.g., habitat and food), and competition in a guild of 7 territorial damselfish species in Kimbe Bay, Papua New Guinea. Common generalisations about the ecological function of territorial damselfish and associated interactions with important roving herbivorous fishes were also investigated. Using ecological surveys, laboratory-based analytical methods, observational studies, and manipulative field experiments, this thesis addresses novel questions about the ecology and functional role of territorial damselfish and the resulting community effects. Competition over resources is recognised to play a primary role in the structure of coral reef fish communities. The distribution of ecologically similar species may depend on the degree to which traditional niche mechanisms operate alongside competitive dynamics. In Chapter 2 these effects were examined by investigating fine-scale species distributions, microhabitat use, and aggression among territorial damselfishes. I documented patterns of habitat partitioning across the 3 reef zones – reef flat, reef crest, and reef slope – with distinct patterns of distribution within these zones at extremely fine scales (1 − 2 m). Distinct differences between neighbouring species in the microhabitat use selected were also observed. Furthermore, aggression elicited by neighbouring species was significantly higher for all species, compared with non-adjacent species. This chapter revealed a fine level of spatial partitioning among reef zones and microhabitats in this guild of damselfish, which was likely maintained by agonistic interactions among neighbouring species. While Chapter 2 found that neighbouring damselfish constrain their microhabitat use to facilitate the co-habitation of reef zones, microhabitat selectivity alone was insufficient to explain the distinct zonation and limited distributional overlap. I hypothesised that in this highly partitioned ecological community, where there are intense agonistic interactions for resources, ecologically neighbouring territorial damselfish may also partition food resources. Other studies had previously quantified diet contributions for the study species, but no isotopic analysis had been conducted for territorial damselfish to date to specifically target pelagic-based food sources. In Chapter 3 I quantified the trophic niches of the territorial damselfish guild through the use of stable isotopes (δ¹³C and δ¹⁵N). Adjacent species on the reef flat, reef crest, and reef slope exhibited high to intermediate trophic niche partitioning when examining pelagic versus reef-based dietary sources, with two species previously described as benthic herbivores actually exhibiting pelagic feeding. Findings of Chapter 3 indicate that diet choice reinforces the patterns of spatial partitioning and coexistence among ecologically similar species. In addition, evidence of planktivorous pelagic feeding adds to the growing view that interspecific differences among similar species are lost when categorizing species into broad functional classifications. In Chapter 4 the direct and indirect effects of interference competition on resource partitioning were measured. The previous chapters found that microhabitat selectivity and dietary diversification facilitated the co-habitation of reef zones among the territorial damselfish guild. Additionally, evidence suggested that interspecific aggression helped maintain the distributional boundaries between neighbouring species. However, an experimental removal of a dominant competitor was necessary to understand if interference competition is present and if subordinate distributional shifts would occur. I employed an observational experiment and a large-scale removal experiment (220 m²) to examine the intensity of agonistic interactions among species and the extent to which the most abundant species influenced the distribution and abundance of neighbouring and non-neighbouring species in the guild. The findings indicated that the distinct distribution patterns among the reef crest species were linked to levels of interspecific agonistic behaviour. The competitive release following the removal of a superior competitor resulted in comprehensive direct and indirect effects, with the subordinate neighbour shifting into the newly available space, followed by successive shifts in species responding to the change in the distributions of their immediate neighbours. Through a novel multi-species large-scale experiment, Chapter 4 provides the conclusive evidence that distributions and the coexistence of the territorial damselfish guild are a result of niche diversification and competitive interactions within and among species. Chapter 5 broadens the thesis by investigating the common perception that all territorial damselfish negatively influence overall reef function and roving herbivorous fishes. Similar to Chapter 2 where generalisations about the guild's diet were questioned, here I challenged the paradigm that intermediate-sized territorial damselfishes have a negative influence on surgeonfish, parrotfish, and rabbitfish abundance and foraging behaviour. To test this, I conducted experimental removals (220 m²) of the most abundant territorial damselfish to examine its impact on roving herbivores and the benthic community structure. The overall relative abundance (MaxN) of roving herbivores was not influenced by the removal. No changes in foraging patterns were observed for parrotfish, the family that received the highest rate of agonistic interactions, and rabbitfish. Instead, the removal resulted in a significant decrease in surgeonfish feeding, suggesting the territorial damselfish species altered foraging patterns indirectly through territorial maintenance and not aggression. The results indicate that all territorial damselfishes do not have a negative impact on all roving herbivores and instead may enhance surgeonfish foraging indirectly through the removal of sediment. The generalisation that territorial damselfish reduce foraging rates of roving herbivores may not be applicable in all systems or for all species. In summary, this thesis investigated the mechanisms that drive species distributions and ecological partitioning along gradients in the natural environment as a precursor to the long-term ecological changes on coral reefs. It first established fine-scale partitioning in a guild of competing fishes on a high-diversity coral reef. Second, the research showed that microhabitat selectivity and dietary diversification facilitates the co-habitation of reef zones, and that interspecific aggression maintains the distributional boundaries between neighbouring species. In order to demonstrate how competitive interactions and resource partitioning influence species coexistence in a complex ecosystem a large-scale field experiment was conducted. The results demonstrate that when exploring coexistence in reef fish communities, the more traditional niche mechanisms operate alongside direct and indirect competitive dynamics, and within highly diverse systems these ecological processes are magnified. Moreover, the thesis highlights the importance of challenging common generalisations and paradigms. By examining the functional role of territorial damselfishes this research provides evidence of novel dietary diversification and demonstrates the complexity of territorial damselfish and roving herbivore interactions

Salmonid species diversity predicts salmon consumption by terrestrial wildlife

1. Resource waves—spatial variation in resource phenology that extends feeding opportunities for mobile consumers—can affect the behaviour and productivity of recipient populations. Interspecific diversity among Pacific salmon species (Oncorhynchus spp.) creates staggered spawning events across space and time, thereby prolonging availability to terrestrial wildlife. 2. We sought to understand how such variation might influence consumption by terrestrial predators compared with resource abundance and intra- and interspecific competition. 3. Using stable isotope analysis, we investigated how the proportion of salmon in the annual diet of male black bears (Ursus americanus; n = 405) varies with species diversity and density of spawning salmon biomass, while also accounting for competition with sympatric black and grizzly bears (U. arctos horribilis), in coastal British Columbia, Canada. 4. We found that the proportion of salmon in the annual diet of black bears was ≈40% higher in the absence of grizzly bears, but detected little effect of relative black bear density and salmon biomass density. Rather, salmon diversity had the largest positive effect on consumption. On average, increasing diversity from one salmon species to ~four (with equal biomass contributions) approximately triples the proportion of salmon in diet. 5. Given the importance of salmon to bear life histories, this work provides early empirical support for how resource waves may increase the productivity of consumers at population and landscape scales. Accordingly, terrestrial wildlife management might consider maintaining not only salmon abundance but also diversit

Publisher correction:Resource landscapes explain contrasting patterns of aggregation and site fidelity by red knots at two wintering sites

[This corrects the article DOI: 10.1186/s40462-018-0142-4.].</p

Investigating the physical and ecological drivers of change in a coastal ecosystem: from individual to population scale impacts.

Coastal ecosystems are undergoing unprecedented rates of environmental change. Many of these changes are anthropogenically-driven and linked to long-term, climate-related phenomena. This thesis focusses on ecological change in soft sediment intertidal habitats. One of the largest harbours in Europe, Poole Harbour, is used as a case study. It contains a variety of important habitats including intertidal mudflat and non-tidal saline lagoon. The two main themes of the thesis are 1) assessing the physical and ecological factors that determine benthic invertebrate abundance, distribution and community structure, which is examined at the scale of the whole harbour, and at the scale of individual habitats: an intertidal mudflat and a saline lagoon; and 2) predicting the response of an overwintering shorebird population, the pied avocet (Recurvirostra avosetta), to future environmental changes, such as sea-level rise and habitat loss. This is achieved by development of an individual-based model (IBM) and consideration of the species’ unique foraging behaviour. This study contributes to the understanding of the factors structuring soft sediment benthic communities, including the use of data from fine-scale hydrodynamic models. It offers a unique comparison of the spatial and temporal variables driving community structure of a saline lagoon and an intertidal mudflat. It also provides insight into the foraging ecology of the pied avocet at a level of detail that has not previously been considered, including a comparison of foraging behaviour in a tidal and non-tidal habitat, the importance of social foraging, and the novel application of an IBM to this species

Behavioral Flexibility, Curiosity, and Cooperative Breeding: Dealing with Complex Concepts and Paradigms

In comparative cognition, and in empirical pursuits more generally, having clear definitions and a mutual understanding of terms and concepts is essential to producing accurate results. However, as philosophers of science Taylor & Vickers (2017) argue, many concepts today have become “fragmented” and different definitions are used in different fields on the basis of their theoretical usefulness. In an attempt not only to better understand the concept of behavioral flexibility – an organism’s ability to adaptively modify behavior in response to new or changing circumstances and contingencies – but also to highlight the importance of having a coherent conceptual framework for studying any phenomena, this thesis will explore the concept of behavioral flexibility in relation to two other concepts: curiosity and cooperative breeding. I review and critically analyze the concept of behavioral flexibility in order to disambiguate the relevant cognitive processes, their behavioral manifestations, and the tasks that are used to test them. After additionally reviewing cooperative breeding and the study species, I present my novel study of curiosity and inhibition (a component of behavioral flexibility) in the cooperatively breeding common marmoset (Callithrix jacchus). Here, I find that group size and the interaction between breeding status, age, and curiosity score has a significant effect on inhibition score. These results provide insights in to the connections and relationships between these phenomena while also emphasizing the importance of having coherent conceptual frameworks for gaining an accurate understanding of reality, particularly in the field of comparative cognition