Ana L. Llandres

The effect of colour variation in predators on the behaviour of pollinators: Australian crab spiders and native bees

1. Australian crab spiders exploit the plant–pollinator mutualism by reflecting UV light that attracts pollinators to the flowers where they sit. However, spider UV reflection seems to vary broadly within and between individuals and species, and we are still lacking any comparative studies of prey and/or predator behaviour towards spider colour variation.

Spider Movement, UV Reflectance and Size, but Not Spider Crypsis, Affect the Response of Honeybees to Australian Crab Spiders

According to the crypsis hypothesis, the ability of female crab spiders to change body colour and match the colour of flowers has been selected because flower visitors are less likely to detect spiders that match the colour of the flowers used as hunting platform. However, recent findings suggest that spider crypsis plays a minor role in predator detection and some studies even showed that pollinators can become attracted to flowers harbouring Australian crab spider when the UV contrast between spider and flower increases. Here we studied the response of Apis mellifera honeybees to the presence of white or yellow Thomisus spectabilis Australian crab spiders sitting on Bidens alba inflorescences and also the response of honeybees to crab spiders that we made easily detectable painting blue their forelimbs or abdomen. To account for the visual systems of crab spiders prey, we measured the reflectance properties of the spiders and inflorescences used for the experiments. We found that honeybees did not respond to the degree of matching between spiders and inflorescences (either chromatic or achromatic contrast): they responded similarly to white and yellow spiders, to control and painted spiders. However spider UV reflection, spider size and spider movement determined honeybee behaviour: the probability that honeybees landed on spider-harbouring inflorescences was greatest when the spiders were large and had high UV reflectance or when spiders were small and reflected little UV, and honeybees were more likely to reject inflorescences if spiders moved as the bee approached the inflorescence. Our study suggests that only the large, but not the small Australian crab spiders deceive their preys by reflecting UV light, and highlights the importance of other cues that elicited an anti-predator response in honeybees.

A dynamic energy budget for the whole life-cycle of holometabolous insects

Alterations of the amount and quality of food consumed during ontogeny can affect different life-history traits, such as growth rate, developmental time, survival, adult size, and fitness. Understanding the dynamics of such metabolic and energetic pathways and investments is particularly challenging in the case of holometabolous insects due to their strikingly different life stages. We show how whole life-cycle energy and mass budgets can be achieved for holometabolic insects through dynamic energy budget (DEB) theory, permitting the fate of acquired and stored nutrients to be followed over a complete life-cycle. We applied the DEB theory to model the whole life-cycle energetics of an endoparasitic wasp, Venturia canescens (Hymenoptera: Ichneumonidae). Data on embryo, larval, and pupal dry mass, imago longevity, and fecundity were used for assessing the goodness of fit of the model. Our model predicted the growth curves of the larval and pupal stages, the number of eggs laid by the imago through time, and lifespan events, such as the different developmental times of the parasitoid. The model enabled us to distinguish and follow the energy invested in eggs through income and capital reserves. The mechanisms leading to the double costs of being small (a shorter life under starving conditions and fewer eggs) were identified by running the model for varying amounts of food eaten early in life, according to host sizes. The final larval instar harvests around 60 times the energy of a recently hatched larva. Around 90% of this energy is then used during pupation to build the structure of the imago and to pay maintenance. Imagoes, therefore, emerge with only a small percentage of the energy stored by the last instar larvae. Our study shows that, despite being small, this percentage of energy stored during the parasitoid development has a great impact on adult fitness, the loss of which cannot be compensated for by a rich adult environment. Our model is generic and has applications for a wide range of applied and theoretical questions about insect energetics, from population dynamics in multitrophic systems to responses to climate change and life-history strategies.

Resource competition triggers the co-evolution of long tongues and deep corolla tubes.

Background It is normally thought that deep corolla tubes evolve when a plants successful reproduction is contingent on having a corolla tube longer than the tongue of the flowers pollinators, and that pollinators evolve ever-longer tongues because individuals with longer tongues can obtain more nectar from flowers. A recent model shows that, in the presence of pollinators with long and short tongues that experience resource competition, coexisting plant species can diverge in corolla-tube depth, because this increases the proportion of pollen grains that lands on co-specific flowers. Methodology/Principal Findings We have extended the model to study whether resource competition can trigger the co-evolution of tongue length and corolla-tube depth. Starting with two plant and two pollinator species, all of them having the same distribution of tongue length or corolla-tube depth, we show that variability in corolla-tube depth leads to divergence in tongue length, provided that increasing tongue length is not equally costly for both species. Once the two pollinator species differ in tongue length, divergence in corolla-tube depth between the two plant species ensues. Conclusions/Significance Co-evolution between tongue length and corolla-tube depth is a robust outcome of the model, obtained for a wide range of parameter values, but it requires that tongue elongation is substantially easier for one pollinator species than for the other, that pollinators follow a near-optimal foraging strategy, that pollinators experience competition for resources and that plants experience pollination limitation.

Possible role of weaver ants, Oecophylla smaragdina, in shaping plant-pollinator interactions in South-East Asia

Although theoretical models suggest that ambush predators could have a wide range of ecological and evolutionary effects on plantnpollinator interactions, these models require predators that are both abundant and mobile. Crab spiders, the main model system for studying the effects of ambush predators on plantnpollinator interactions, are neither of these. The weaver ant Oecophylla smaragdina is a keystone predator in South-East Asian forests. It uses the flowers of a wide range of native and introduced species as hunting platforms for incoming pollinators. Weaver ants affect the behaviour of flower visitors and the reproductive success of their host plants. Due to their ubiquity and mobility, O.nsmaragdina ants satisfy the assumptions of the theoretical models. They have the potential to affect the structure of pollination networks. Synthesis. Oecophylla smaragdina in South-East Asia, and possibly other predatory ant species in African and American tropical forests, may play a key role in shaping the ecological and evolutionary trajectories of plantnpollinator interactions.

Environmental and hormonal factors controlling reversible colour change in crab spiders

SUMMARY Habitat heterogeneity that occurs within an individuals lifetime may favour the evolution of reversible plasticity. Colour reversibility has many different functions in animals, such as thermoregulation, crypsis through background matching and social interactions. However, the mechanisms underlying reversible colour changes are yet to be thoroughly investigated. This study aims to determine the environmental and hormonal factors underlying morphological colour changes in Thomisus onustus crab spiders and the biochemical metabolites produced during these changes. We quantified the dynamics of colour changes over time: spiders were kept in yellow and white containers under natural light conditions and their colour was measured over 15 days using a spectrophotometer. We also characterised the chemical metabolites of spiders changing to a yellow colour using HPLC. Hormonal control of colour change was investigated by injecting 20-hydroxyecdysone (20E) into spiders. We found that background colouration was a major environmental factor responsible for colour change in crab spiders: individuals presented with white and yellow backgrounds changed to white and yellow colours, respectively. An ommochrome precursor, 3-OH-kynurenine, was the main pigment responsible for yellow colour. Spiders injected with 20E displayed a similar rate of change towards yellow colouration as spiders kept in yellow containers and exposed to natural sunlight. This study demonstrates novel hormonal manipulations that are capable of inducing reversible colour change.

Social but not solitary bees reject dangerous flowers where a conspecific has recently been attacked

Social bees are known to avoid inflorescences marked with dead conspecifics or their smell. The avoidance response could be triggered by alarm signals actively given by attacked bees or by substances passively released through injuries as a by-product of the attack. To discriminate between these two options we note that both social and solitary bees are expected to react to nonsignalling cues associated with predation risk, while only social bees are expected to give alarm signals. We simulated risky inflorescences by pinching a landing bee with forceps, and compared the rate at which bees visited these experimental inflorescences and unmanipulated control inflorescences. We conducted the experiment with four species of social bees, Apis mellifera, Apis dorsata, Apis florea and Bombus terrestris and with three species of solitary bees, Eucera sp., Panurgus sp. and Nomia strigata. We found that while the three species of solitary bees responded similarly to control and experimental inflorescences, all four species of social bees strongly rejected inflorescences where we simulated a predation attempt. The finding that only social species avoided landing on dangerous inflorescences strongly suggests that the release of the alarm cue has been selected for its signalling value in social bees.

Relationship between colouration and body condition in a crab spider that lures pollinators.

SUMMARY Sit-and-wait predators have evolved several traits that increase the probability of encountering prey, including lures that attract prey. Although most crab spiders (Thomisidae) are known by their ability to change colour in order to match the background, a few use a different strategy. They are UV-reflective, creating a colour contrast against UV-absorbing flowers that is attractive for pollinators. The nature of the relationship between colour contrast and foraging success is unknown, as is how spiders trade off the potential costs and benefits of strong colour contrast. Therefore, this study investigated the relationship between spider colouration, foraging success and background colouration in a crab spider species known to lure pollinators via UV reflectance (Thomisus spectabilis). Field data revealed that spider body condition – a proxy of past foraging success – is positively related to overall colour contrast. We experimentally tested the effect of satiation and background colour on spider colour change. Throughout the experiment, spiders changed their colour contrast regardless of their food intake, suggesting that colour contrast and the UV component contributing to overall contrast are not caused by spider condition. Although spiders responded to different backgrounds by subtly changing their body colour, this did not result in colour matching. We believe that the observed variation in colour contrast and hence conspicuousness in the field, coupled with the spiders’ reaction to our manipulation, could be the result of plasticity in response to prey.

Increasing metabolic rate despite declining body weight in an adult parasitoid wasp

Metabolic rate is a positive function of body weight, a rule valid for most organisms and the basis of several theories of metabolic ecology. For adult insects, however, the diversity of relationships between body mass and respiration remains unexplained. The aim of this study is to relate the respiratory metabolism of a parasitoid with body weight and foraging activity. We compared the metabolic rate of groups of starving and host-fed females of the parasitoid Eupelmus vuilleti recorded with respirometry for 7days, corresponding to the mean lifetime of starving females and over half of the lifetime of foraging females. The dynamics of carbohydrate, lipid and protein in the body of foraging females were quantified with biochemical techniques. Body mass and all body nutrients declined sharply from the first day onwards. By contrast, the CO2 produced and the O2 consumed increased steadily. Starving females showed the opposite trend, identifying foraging as the reason for the respiration increase of feeding females. Two complementary physiological processes explain the unexpected relationship between increasing metabolic rate and declining body weight. First, host hemolymph is a highly unbalanced food, and the excess nutrients (protein and carbohydrate) need to be voided, partially through excretion and partially through respiration. Second, a foraging young female produces eggs at an increasing rate during the first half of its lifetime, a process that also increases respiration. We posit that the time-varying metabolic rate contributions of the feeding and reproductive processes supplements the contribution of the structural mass and lead to the observed trend. We extend our explanations to other insect groups and discuss the potential for unification using Dynamic Energy Budget theory.

Indirect cues in selecting a hunting site in a sit-and-wait predator

Sit‐and‐wait predators use relatively simple rules for their decisions to choose and leave a patch, such as using the direct presence of prey to select a hunting site. However, the direct presence of prey can only be used when there is a highly visited patch in the proximity of the predator. Therefore, it is plausible that sit‐and‐wait predators also exploit indirect cues of prey presence and, consequently, use associative learning to select a hunting site. The present study tests for the role of associative learning in a sit‐and‐wait predator species for which the ecology is well understood: Misumena vatia Clerck crab spiders. An ecologically relevant scenario is used by selecting flower colour as the conditioned stimulus and prey presence as the unconditioned stimulus. The results provide no evidence that M. vatia crab spiders use the association between flower colour and food presence for selecting a hunting site. After a training phase of being exposed to a colourful artificial flower highly visited by bees, spiders select a hunting site independently of its colour during the testing phase. Investigations of similar scope and ecological relevance are required with other sit‐and‐wait predators to identify the conditions promoting the use of associative learning for foraging site selection when animals face an unpredictable food supply.