Preference and performance of generalist and specialist herbivores on chemically defended host plants

1. Both the physiological efficiency (PE) hypothesis and the preference–performance (PP) hypothesis address the complex interactions between herbivores and host plants, albeit from different perspectives. The PE hypothesis contends that specialists are better physiologically adapted to their host plants than generalists. The PP hypothesis predicts that larvae perform best on the host plant preferred by ovipositing females. 2. This study tests components of both hypotheses using the specialist checkerspot, Euphydryas anicia, the generalist salt marsh caterpillar, Estigmene acrea, and host plants in the genus Penstemon, which are defended by iridoid glycosides. 3. In laboratory experiments, the generalist preferred and performed significantly better on the less well defended host plant species. This is consistent with results from a common garden experiment where the less well defended Penstemon species received more damage from the local community of generalists. Larvae of the specialist checkerspot preferred the more chemically defended species in the laboratory, but performed equally well on both hosts. However, field experiments demonstrated that adult checkerspot females preferred to oviposit on the less well defended host plant. 4. Components of the physiological efficiency hypothesis were supported in this system, as the specialist outperformed the generalist on the more iridoid glycoside‐rich host plant species. There was no support for the PP hypothesis, however, as there was no clear relationship between female preference in the field and offspring performance in the laboratory.     

Hosts as habitats: faunal similarity of phytophagous insects between host plants

1. Published lists on the phytophages recorded on 86 cabbage plant species (Brassicaceae) and 30 thistle species (Cynaroideae) were used to investigate patterns in the faunal similarity of phytophages. This was done by calculating the Jaccard index and a standardised index of similarity between pairs of host species using presence/absence data. 2. The faunal similarity measured as Jaccard indices indicated that pairs of cabbage hosts share on average 36% of phytophagous species whereas pairs of thistle hosts share only 10%. 3. The faunal similarity between two host species increased with the taxonomic affinity of hosts. This increase was more pronounced in thistles than in cabbage plants. 4. Irrespective of the taxonomic affinity of hosts, in the cabbage plants the faunal similarity of endophages was lower than in ectophages. In contrast, in the thistles faunal similarity differed only between endophages and ectophages for hosts of the same genera. 5. Differences in the patterns of faunal similarity between the two host taxa may be due to idiosyncratic characteristics of the plant taxa, e.g. the unique chemical properties of the cabbage plants and the resource‐rich flower heads of thistles.     

Field studies of the relationship between herbivore damage and tannin concentration in bracken (Pteridium aquilinum Kuhn)

Summary The acceptance of secondary plant metabolites as herbivore deterrents rests primarily on their deleterious effects on herbivores. Efforts to demonstrate differential fitness in natural plant populations with varying concentrations of tannin have failed, since coevolved plant predators may physiologically or behaviorally circumvent the defense, which results in apparently equal amounts of damage to defended and undefended individuals. In this study, two approaches were used to overcome this difficulty. 1) Theoretically, more energy should be allocated to the defense of parts which contribute more heavily to the plant's fitness. Bracken fern clones produce fronds throughout the growing season. Fronds which are produced early should be more heavily defended than late-emerging fronds which will return less photosynthate per unit cost of production. The results of this study do not support this prediction; it appears that the production of tannin is more closely linked to environmental factors such as water stress than to date of frond emergence. Fronds which emerged in August contained as much tannin as fronds which emerged in May. 2) By recording the temporal occurrence of herbivore damage in bracken ferns, it was found that in fronds which escaped attack until after reaching maturity there was a significant negative correlation between tannin concentration in the frond and the amount of damage experienced. This result supports the generally accepted assumption that herbivory has been a selective force in the evolution of tannin as a defensive substance.     

When should a trophically transmitted parasite exploit host compensatory responses?

Parasites are known to manipulate the behavior of their hosts in ways that increase their probability of transmission. Theoretically, different evolutionary routes can lead to host manipulation, but much research has concentrated on the ‘manipulation hypothesis’ sensu stricto. Among the arsenal of host compensatory responses, however, some seem to be compatible with the parasite objectives. Another way for parasites to achieve transmission, therefore, would be to trigger specific host compensatory responses. In order to explore the conditions favoring this manipulative strategy, we developed a simulation model in which parasites may affect their hosts' behavior by using two nonmutually exclusive strategies: a manipulation sensu stricto strategy and a strategy based on the exploitation of host compensatory responses. Our model predicts that the exploitation of host compensatory responses can be evolutionary stable when the alteration improves the susceptibility to predation by final hosts without compromising host survival during parasite development. Inversely, when the behavioral modification resulting from a compensatory response conflicts with the host's interest we expect parasites to use both strategies. From this result, we conclude that the strategy based on the exploitation of host compensatory responses should be more common among nontrophically transmitted parasites. Furthermore, our findings indicate that the transmission rate of parasites in a definitive host is highest when each of the two strategies affects different traits, which supports the hypothesis that host manipulation is a multidimensional phenomenon in which each altered trait contributes independently to increase parasite transmission efficiency.     

A role for immunology in invasion biology

Invasive species are of increasing conservation and economic concern, yet mechanisms underlying invasions remain poorly understood. We propose that variation in immune defences might help explain why only some introduced populations become invasive. Introduced species escape many of their native diseases, but also face novel pathogens that can induce costly, and sometimes deadly, immune responses in na?ve hosts. Therefore, favouring less resource-demanding and dangerous defence mechanisms and allocating a greater proportion of resources to growth and reproduction should favour invasion. Specifically, we argue that successful invaders should reduce costly systemic inflammatory responses, which are associated with fever and metabolic and behavioural changes, and rely more heavily on less expensive antibody-mediated immunity. Here we provide supporting arguments for this hypothesis and generate predictions that are testable using tools from the growing field of ecological immunology.     

Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata

The Red Queen hypothesis predicts that sex should be more common in populations heavily infested with parasites, than in those without. This hypothesis was investigated in the aquatic snail Melanoides tuberculata, in which both sexual and parthenogenetic individuals exist in natural populations, and some populations are heavily infested by trematodes. The presence of fertile males and the higher genetic diversity of bisexual populations are indicative of sexual reproduction. We compared sites in 1990, 1999, and 2001, and we looked for a positive correlation between male and parasite frequencies. Male frequency was not correlated with the frequency of individuals infected by trematodes. This lack of correlation was reconfirmed in a retrospective power analysis. In a period of 9 years, male frequencies decreased but infection levels increased. These results do not support the Red Queen hypothesis. In samples with high male frequency the number of embryos was low, perhaps indicating that males may have a negative effect on embryo numbers. This effect of males on fitness could perhaps suggest that the cost of sex is fewer embryos. The reduction in embryo numbers may also represent a trade-off between mating and egg production costs.     

Does chemical defence increase niche space? A phylogenetic comparative analysis of the Musteloidea

Avoidance of predation can impose opportunity costs on prey species that use behavioural avoidance strategies to evade detection. An animal that spends much time hiding or remaining immobile, for example, may have less time for other important activities such as foraging or finding mates. Here we examine the idea that the evolution of chemical defence may act to release prey from these constraints, freeing defended prey to exploit their habitats more effectively, and increasing their niche space. We tested this hypothesis using comparative methods on a mammal group containing both chemically defended and non-defended species: Musteloidea. We found that defended species had a more omnivorous diet and were more likely to be active during both day and night than non-defended species. We also found that chemically defended species were less likely to be strictly diurnal or to show sexual size dimorphism, and had earlier maturing females and a shorter lifespan than non-defended species. Taken together, our results support the hypothesis that chemical defence increases the niche space available to a species. More generally, this also supports recent suggestions that strategies taken to avoid natural enemies can have important effects on diverse components of life history.     

Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid: a time-saving foraging strategy

1. In studies on optimal foraging strategies, long-range decisions in the pursuit of resource are rarely considered. This is also the case for sympatric parasitoids, which may be confronted with the decision to accept or reject host larvae that are already parasitized by a competing species. They can be expected to reject already parasitized hosts if it is likely that they will lose the resulting intrinsic competition. However, examples of such interspecific host discrimination are rare. 2. We propose that parasitoids that are not egg-limited should reject inferior hosts only if it saves them time, and that this will be achieved mainly when the parasitoids are able to detect competitors from a distance. We tested this hypothesis using the sympatric parasitoids Cotesia marginiventris (Cresson) and Campoletis sonorensis (Cameron). 3. C. sonorensis was found to be the superior intrinsic competitor but, upon contact with a host larva, both wasps readily accepted hosts that had already been parasitized by the other species. However, in an olfactometer experiment, C. marginiventris females were found to strongly avoid the odour of their superior competitor. 4. These results are in accordance with a time optimization scenario, whereby the inferior competitor accepts competition if it costs only an egg, but avoids competition if it may save time that can be allocated to the search for more profitable hosts. 5. Models on host discrimination strategies in parasitoids had not yet considered discrimination from a distance. Long-range foraging decisions can also be expected for other organisms that have to choose between resources of varying suitability and profitability.     

Specialist by preference,generalist by need: availability of quality hosts drives parasite choice in a natural multihost–parasite system

Encountering suitable hosts is key for parasite success. A general assumption for disease transmission is that the contact of a parasite with a potential host is driven by the density or relative frequency of hosts. That assumption ignores the potential role of differential host attractiveness for parasites that can drive the encounter of hosts. It has been posited that hosts may be chosen by parasites as a function of their suitability, but the existing literature addressing that hypothesis is still very scarce. In a natural system involving a parasitic Philornis botfly and its multiple bird hosts, there are profound differences in host quality. The Great Kiskadee tolerates and does not invest in resisting the infection, which makes it an optimal host. Alternative hosts are frequently used, but whilst some of them may be good options, others are bad alternatives. Here we examined the host selection processes that drive parasite dynamics in this system with 8 years of data from a longitudinal study under natural conditions. We found that the use of an alternative host was not driven by its density or relative frequency, but instead selection of these hosts was strongly dependent on availability of more suitable hosts. When optimal hosts are plentiful, the parasite tends to ignore alternative ones. As broods of optimal hosts become limited, good alternative hosts are targeted. The parasite chooses bad alternative hosts only when better alternatives are not sufficiently available. These results add evidence from a natural system that some parasites choose their hosts as a function of their profitability, and show that host selection by this parasite is plastic and context-dependent. Such findings could have important implications for the epidemiology of some parasitic and vector-borne infections which should be considered when modelling and managing those diseases. The facultative host selection observed here can be of high relevance for public health, animal husbandry, and biodiversity conservation, because reductions in the richness of hosts might cause humans, domestic animals, or endangered species to become increasingly targeted by parasites that can drive the encounter of hosts.     

Testing alternative hypotheses for variation in amphipod behaviour and life history in relation to parasitism.

We tested two hypotheses concerning changes in investment in current reproduction for parasitised hosts, using amphipods (Corophium volutator) which act as second intermediate hosts for trematodes (Gynaecoyla aduncta). One hypothesis requires that parasites exert control over their hosts (parasite manipulation), whereas the other predicts that hosts control decisions over investment (adaptive host response). Although these hypotheses are viewed as mutually exclusive, our various results support both hypotheses. For example, female amphipods infected by late-stage larvae were often found crawling at times when predation by sandpipers (Calidris pusilla), which are the final hosts for trematodes, was likely, while uninfected females typically remained in their burrows. Furthermore, old females that were newly-infected by trematodes often aborted and ate their young. Both of these responses seem inconsistent with female investment in current reproduction, but can be interpreted as adaptive parasite manipulation. In contrast, young non-ovigerous females that were newly-infected hastened the onset of their parturial moult and thus, time to becoming receptive. This response can be explained as a host adaptation to minimise the cost of parasites. We contend that differences between parasitised and unparasitised hosts in behaviour or investment can be explained as both parasite and host adaptations, expressed at different times in the host's life history. Such compromise will help explain the persistence of parasite-host associations in nature.     

Avoid,attack or do both? Behavioral and physiological adaptations in natural enemies faced with novel hosts

Background

Confronted with well-defended, novel hosts, should an enemy invest in avoidance of these hosts (behavioral adaptation), neutralization of the defensive innovation (physiological adaptation) or both? Although simultaneous investment in both adaptations may first appear to be redundant, several empirical studies have suggested a reinforcement of physiological resistance to host defenses with additional avoidance behaviors. To explain this paradox, we develop a mathematical model describing the joint evolution of behavioral and physiological adaptations on the part of natural enemies to their host defenses. Our specific goals are (i) to derive the conditions that may favor the simultaneous investment in avoidance and physiological resistance and (ii) to study the factors that govern the relative investment in each adaptation mode.

Results

Our results show that (i) a simultaneous investment may be optimal if the fitness costs of the adaptive traits are accelerating and the probability of encountering defended hosts is low. When (i) holds, we find that (ii) the more that defended hosts are rare and/or spatially aggregated, the more behavioral adaptation is favored.

Conclusion

Despite their interference, physiological resistance to host defensive innovations and avoidance of these same defenses are two strategies in which it may be optimal for an enemy to invest in simultaneously. The relative allocation to each strategy greatly depends on host spatial structure. We discuss the implications of our findings for the management of invasive plant species and the management of pest resistance to new crop protectants or varieties.

     

State-dependent risk-taking by predators in systems with defended prey

Even defended prey items may contain nutrients that can sustain predators in times of energetic need. Conversely, a well-fed predator might be expected to avoid attacking prey items that have a chance of being defended, particularly if there is an abundance of familiar palatable prey to support it. To further understand the implications of optimal state-dependent foraging behaviour by predators in systems that contain defended prey, I developed a stochastic dynamic programming model. This state-dependent approach formally accounts for the trade-off between avoiding starvation and minimising harm from attacking defended prey. It predicts that the mean attack probability of predators on defended models and their undefended mimics should decline in a sigmoidal fashion with increasing availability of alternative undefended prey, and that the foraging decisions of predators should in general be relatively insensitive to the probability that a potentially defended prey item is indeed defended. Some implications of these predictions are that conspicuous warning signals are more likely to evolve in systems that contain an abundance of alternative undefended prey, and that imperfect mimicry will provide almost complete protection to the mimic when predators are readily supported by alternative food sources. Somewhat surprisingly, increasing the density of nutritious undefended mimics while keeping the densities of all other prey types constant tended to decrease the attack rates of predators on encounter with mimics and their defended models. This increase in dietary conservatism arose because in these cases there would be more prey available to sustain the predator if it ever found itself critically low in energy.     

Performance of secondary parasitoids on chemically defended and undefended hosts

Defensive chemicals produced by plants can travel up the food chain by being sequestered by herbivores, and then in turn being sequestered by their parasitoids. Insect species with wide host ranges are predicted to perform poorly in the face of specific chemical defence. However, a species at a high trophic level is expected to have a wide host range. This creates a conflict for hyperparasitoids, many of which depend on specialized hosts. We studied the performance of two hyperparasitoids, Lysibia nana and Gelis agilis, both of which have wide host ranges, on two host species, one chemically defended and the other not. We predicted that both hyperparasitoids would perform better using the undefended host Cotesia glomerata than the defended host C. melitaearum, which sequesters terpenoid allelochemicals (iridoid glycosides). Furthermore, we expected that the progeny of G. agilis collected from an area where hosts defended by iridoid glycosides are absent (the Netherlands) would perform poorly using C. melitaearum in comparison with G. agilis collected from an area where C. melitaearum is a common host (Åland, Finland). In a series of laboratory experiments we found that, contrary to prediction, both hyperparasitoids performed well on both hosts, reaching a larger size on C. glomerata, but having a higher conversion efficiency and developing more quickly on the chemically defended C. melitaearum. Lysibia nana metabolized the plant derived iridoid glycosides, which are chemicals that it does not normally encounter. Gelis agilis retained some of the iridoid glycosides. But whereas Finnish G. agilis retained both aucubin and catalpol, Dutch G. agilis mainly retained aucubin, illustrating that though generalists, local populations still cope differently with toxic allelochemicals.     

On sex, mate selection and the red queen.

The widespread occurrence of sexual reproduction despite the two-fold disadvantage of producing males, is still an unsolved mystery in evolutionary biology. One explanatory theory, called the "Red Queen" hypothesis, states that sex is an adaptation to escape from parasites. A more recent hypothesis, the mate selection hypothesis, assumes that non-random mating, possible only with sex, accelerates the evolution of beneficial traits. This paper tests these two hypotheses, using an agent-based or "micro-analytic" evolutionary algorithm where host-parasite interaction is simulated adhering to biological reality. While previous simpler models testing the "Red Queen" hypothesis considered mainly haploid hosts, stable population density, random mating and simplified expression of fitness, our more realistic model allows diploidy, mate selection, live history constraints and variable population densities. Results suggest that the Red Queen hypothesis is not valid for more realistic evolutionary scenarios and that each of the two hypotheses tested seem to explain partially but not exhaustively the adaptive value of sex. Based on the results we suggest that sexual populations in nature should avoid both, maximizing outbreeding or maximizing inbreeding and should acquire mate selection strategies which favour optimal ranges of genetic mixing in accordance with environmental challenges.     

Influences of host feeding-niche and foodplant type on generalist and specialist parasitoids

Abstract. 1. We classified the parasitoids of 185 British herbivorous insect species as being koinobionts (which should tend to be specialists) or idiobionts (potential generalists) to examine the influences of host feeding-niche and foodplant type on the numbers of parasitoid species attacking individual host species.
2. The majority of parasitoid species of exophytic hosts are koinobionts, whereas endophytic hosts support mainly idiobionts.
3. Parasitoid assemblage size increases with host foodplant size and complexity; for endophytic hosts this is due to an increase in idiobionts on hosts on large plants, but for exophytic hosts it is the number of koinobionts that increases with foodplant size.
4. Comparison of these patterns with those predicted under a competition hypothesis suggests that parasitoid communities associated with endophytic hosts may be commonly limited by interspecific competition, whereas those of exophytic hosts probably are not.     

Long‐term coevolution between avian brood parasites and their hosts

Coevolutionary theory predicts that the most common long‐term outcome of the relationships between brood parasites and their hosts should be coevolutionary cycles based on a dynamic change selecting the currently least‐defended host species, given that when well‐defended hosts are abandoned, hosts will be selected to decrease their defences as these are usually assumed to be costly. This is assumed to be the case also in brood parasite‐host systems. Here I examine the frequency of the three potential long‐term outcomes of brood parasite–host coevolution (coevolutionary cycles, lack of rejection, and successful resistance) in 182 host species. The results of simple exploratory comparisons show that coevolutionary cycles are very scarce while the lack of rejection and successful resistance, which are considered evolutionary enigmas, are much more frequent. I discuss these results considering (i) the importance of different host defences at all stages of the breeding cycle, (ii) the role of phenotypic plasticity in long‐term coevolution, and (iii) the evolutionary history of host selection. I suggest that in purely antagonistic coevolutionary interactions, such as those involving brood parasites and their hosts, that although cycles will exist during an intermediate phase of the interactions, the arms race will end with the extinction of the host or with the host acquiring successful resistance. As evolutionary time passes, this resistance will force brood parasites to use previously less suitable host species. Furthermore, I present a model that represents the long‐term trajectories and outcomes of coevolutionary interactions between brood parasites and their hosts with respect to the evolution of egg‐rejection defence. This model suggests that as an increasing number of species acquire successful resistance, other unparasitized host species become more profitable and their parasitism rate and the costs imposed by brood parasitism at the population level will increase, selecting for the evolution of host defences. This means that although acceptance is adaptive when the parasitism rate and the costs of parasitism are very low, this cannot be considered to represent an evolutionary equilibrium, as conventional theory has done to date, because it is not stable.     

Effect of host lizard anemia on host choice and feeding rate of larval western black-legged ticks (Ixodes pacificus)

Although ticks are known to exhibit preferences among host species, there is little evidence that ticks select hosts within a species based on physiological condition. It may be beneficial for ticks to choose hosts that are easier to feed upon if the ticks can perceive indicative chemical or other signals from the host. For example, if ticks can detect host hematocrit they may choose hosts with high hematocrit, facilitating a faster blood meal. It may similarly be adaptive for ticks to avoid anemic hosts because it may be difficult for them to obtain an adequate meal and feeding duration may be extended. We tested the hypothesis that larval western black-legged ticks (Ixodes pacificus) detect host hematocrit using external cues and choose healthy over anemic hosts, allowing them to feed more quickly. We presented groups of larval ticks with pairs of healthy and anemic male western fence lizards (Sceloporus occidentalis), allowed them to select a host, and measured the feeding duration of the ticks. We found that the ticks did not exhibit a statistically significant preference for healthy over anemic lizards, but that the ticks fed to repletion significantly faster on healthy hosts than on anemic hosts. Larval ticks may not be able to detect external cues indicating the health of the host, at least not in terms of their hematocrit. The extended feeding duration likely reflects the extra time needed for the ticks to concentrate the blood meal of their anemic hosts.     

Modeling the consequence of increased host tolerance toward avian brood parasitism

Avian brood parasites greatly reduce the reproductive success of their hosts. Empirical studies have demonstrated that some hosts have evolved defenses against parasitism like an ability to recognize and reject parasitic eggs that are dissimilar to their own eggs. Detailed mechanisms of how hosts recognize parasitism still remain unknown, but recent studies have shown that the host’s recognition, in many cases, is based on discordance of the eggs in a clutch, and that hosts are more error-prone when the nest is multiply parasitized, i.e., hosts tend to accept more multiple parasitism than single parasitism. In an area in Hungary, the great reed warbler Acrocephalus arundinaceus, one of the main hosts of the common cuckoo Cuculus canorus, is heavily parasitized and the parasitism rate has been kept at quite a high level for decades. Previous mathematical models suggest that such a high parasitism rate can be maintained because the focal host population behaves as a sink where few hosts can reproduce but immigration from outside replenishes the loss of host reproduction in the sink population. Here, we explore the consequences of the increased host tolerance towards multiple parasitism which has been overlooked in the previous studies using a simple model. Our model analysis shows that the increased host tolerance can dramatically contribute to both the parasite abundance and the parasitism rate being kept at a high level. We suggest that such a host behavior, combined with host immigration, can be an important factor responsible for the observed severe parasitism.     

Parental defence in Long-eared Owls Asio otus: effects of breeding stage, parent sex and human persecution

The responses of male and female Long-eared Owls to a human approaching the nest were examined. Each nest was only tested once. Nest defence increased significantly throughout the breeding season because older chicks were defended more strongly than younger chicks and eggs. No correlations were however found between defence intensity and laying date, clutch- or brood-size. These results generally do not support either the renesting-potential hypothesis or the positive reinforcement hypothesis but are in accordance with both the age-investment hypothesis and the vulnerability hypothesis. Females defended nestlings more often and more vigorously than did males. Given division of labour between sexes and the related reversed sexual dimorphism in size, female Long-eared Owls may be more willing to engage in nest defence simply because they are always nearer eggs and chicks during all breeding stages and are larger/heavier than males; consequently they may allocate more time and energy to this activity. Finally, owls experiencing higher levels of human persecution took smaller risks when defending nests than owls breeding in an undisturbed area.     

Host physiological phenotype explains pathogen reservoir potential

Control of emerging infectious diseases often hinges on identifying a pathogen reservoir, the source of disease transmission. The potential to function as a pathogen reservoir can be influenced by host lifespan, geographic provenance and phylogeny. Yet, no study has identified factors that causally determine the reservoir potential of diverse host species. We propose the host physiological phenotype hypothesis, which predicts that hosts with short‐lived, poorly defended, nutrient rich and high metabolism tissue have greater values for three epidemiological parameters that determine reservoir potential: host susceptibility to infection, competence to infect vectors and ability to support vector populations. We experimentally tested these predictions using a generalist vectored virus and six wild grass species. Host physiological phenotype explained why hosts differed in all three epidemiological parameters while host lifespan, provenance and phylogeny could not explain host competence. Thus, a single, general axis describing variation in host physiological phenotype may explain reservoir potential.