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Tri-trophic interactions with avian predators: the effect of host plant species and herbivore-induced plant volatiles on recruiting avian predators

<div> Herbivore-induced plant volatiles (HIPVs) are important signaling compounds released by plants upon wounding. These compounds have been shown to mediate tri-trophic interactions in recruiting insect predators and parasitoids. Recent work has begun to show that avian species, which were once thought to have a very limited sense of smell, can cue in on these HIPVs to find insect prey. Here, we test the ability for two general HIPVs, methyl jasmonate and methyl salicylate, to recruit avian predators. We test the recruitment efficacies of these HIPVs across 4 different host plant species (black walnut, red maple, cattail, and wheat) and use clay caterpillars to quantify predation by insectivorous birds. We found no significant differences in predation between treatment groups across any of our host plants. However, there was a nearly-significant effect of methyl salicylate in black-walnut trees. Interestingly, our results did show a significant effect of host plant species on predation levels. The two tree species, particularly black walnut, had higher levels of predation than the herbaceous species. We discuss the implications of these results and suggest a number of ideas and suggestions for future studies investigating the role of HIPVs in attracting insectivorous birds. </div>

Data from: Host sex modulates the energetics of pathogen proliferation and its dependence on environmental resources

Sex differences in immunity are predicted to underlie much of the frequently observed sex differences in the prevalence or severity of infection. We propose the additional hypothesis that differences in the ability of males and females to acquire and use resources will also affect how readily a pathogen can convert host energy into transmission stages, thereby contributing to sex differences in infection dynamics. To test this we manipulated the resource environment of male and female Daphnia magna by altering the availability of food and then exposed hosts to a bacterial pathogen. We measured the production of transmission spores and virulence via the reduction in life span, together with feeding rates and changes in mass-independent metabolic rate, as a measure of the intake and expenditure of energy during infection. When raised in the presence of high resource levels, females more readily allowed for resources in the environment to be translated to pathogen exploitation, as represented by increased spore production, greater virulence, and higher energy use. In contrast, the traits of infected males were robust to changes in resource availability. High food availability thus exaggerated the degree of sexual dimorphism observed between the sexes. It also modified the relationship between host energy use, virulence, and pathogen spore production for each sex. These results suggest that a host's resource environment can affect how a male or female is exploited by a pathogen and may thus be an additional factor driving sex-specific patterns of disease susceptibility or severity.

Fluctuating starvation conditions modify host-symbiont relationship between a leaf beetle and its newly identified gregarine species

Gregarines are ubiquitous endosymbionts in invertebrates, including terrestrial insects. However, the biodiversity of gregarines is probably vastly underestimated and the knowledge about their role in shaping fitness-related traits of their host in dependence of fluctuating environmental conditions is limited. Using morphological and molecular analyses, we identified a new gregarine species, Gregarina cochlearium sp. n., in the mustard leaf beetle, Phaedon cochleariae. Applying a full-factorial design, we investigated the effects of a gregarine infection in combination with fluctuating starvation conditions during the larval stage on the development time and fitness-related traits of adult beetles. Under benign environmental conditions, the relationship between gregarines and the host seemed neutral, as host development, body mass, reproduction and survival were not altered by a gregarine infection. However, when additionally exposed to starvation, the combination of gregarine infection and this stress resulted in the lowest reproduction and survival of the host, which points to a parasitic relationship. Furthermore, when the host experienced starvation, the development time was prolonged and the adult females were lighter compared to non-starved individuals, independent of the presence of gregarines. Counting of gregarines in the guts of larvae revealed a lower gregarine load with increasing host body mass under stable food conditions, which indicates a regulation of the gregarine burden in dependence of the host condition. Contrary, in starved individuals the number of gregarines was the highest, hence the already weakened host suffered additionally from a higher gregarine burden. This interactive effect between gregarine infection and fluctuating starvation conditions led to an overall reduced fitness of P. cochleariae. Our study emphasises the need to study endosymbionts as important components of the natural environment and to investigate the role of host-symbiont relationships under fluctuating environmental conditions in an evolutionary and ecological context.

opencc-by-4.0Mar 2022View details →

Virus isolation data improve host predictions for New World rodent orthohantaviruses

Data and code for "Virus isolation data improve host predictions for New World rodent orthohantaviruses" in Journal of Animal Ecology

Data for: The paradoxical rarity of a parasitic fruit fly fungus attacking a broad range of hosts

Understanding the factors that determine the realized and potential distribution of a species requires knowledge of abiotic, physiological, limitations as well as ecological interactions. Entomopathogenic fungi of the order Laboulbeniales specialize on arthropod hosts and are typically thought to be highly specialized on a single host or closely related group of hosts. Because infections are solely transmitted through direct contact of the hosts, the host ecology to a large extent determines the distribution and occurrence of the fungus. We examined ~20,000 fruit flies (Diptera: Dacinae) collected in Malaysia, Sulawesi, Australia and the Solomon Islands between 2017–2019 for ectoparasitic fungal infections and found 197 infected flies across eight different Bactrocera species. Morphology and small subunit (18S) DNA sequences both support that the infections are from a single polyphagous fungal species. This presents the paradox of why S. dacinus is not more common when its hosts are widespread and ubiquitous. In addition, the hosts are all Bactrocera, a genus with ~480 species, but many sympatric Bactrocera were never infected. Host-selection does not appear to be phylogenetically correlated. Our results show that a single fungus species can be found on different host species in different continents. We discuss factors that might be involved in determining the host and distribution range of S. dacinus, such as host resistance, and discuss the potential for population control of agriculturally important hosts, such as the pestiferous Oriental fruit fly Bactrocera dorsalis and the Queensland fruit fly B. tryoni.

Raw data for the study titled "Fungal ectoparasites increase winter mortality of ladybird hosts despite limited effects on their immune system"

Winter represents a challenging period for insects inhabiting temperate regions. A plethora of studies have investigated how abiotic environmental conditions such as temperature affect insect overwintering success. However, only a few studies have focused on biotic factors and the mechanisms affecting the overwintering performance of insects. Here, we investigated the effects of the parasitic fungus Hesperomyces virescens on the overwintering performance and immune system functioning of the invasive ladybird Harmonia axyridis. Winter survival was significantly lower for infected than for uninfected beetles. Body mass loss during overwintering tend to be higher for infected individuals compared to uninfected ones and for larger beetles. In addition, parasitic infection reduced post-winter longevity without food in male but not female ladybirds. Total haemocyte and protein concentration as well as antimicrobial activity against Escherichia coli significantly decreased during ladybird overwintering. However, haemolymph parameters were only poorly affected by Hesperomyces infection, with the exception of antimicrobial activity against Escherichia coli that tended to be higher in infected ladybirds. Interestingly, none of the pre-winter haemolymph parameters were good predictors of ladybird winter survival. Overall, our results indicate that energy exhaustion unrelated to immune system challenge is the most probable explanation for increased overwintering mortality in infected beetles.

Lagged effects of herbivory impact host-choice but not nymphal survivorship in an ant-protected treehopper

Theoretical studies have shown that in protection mutualism, modification of top-down control by protectors may be destabilizing. Central to this prediction are the assumptions that 1) protection mutualism increases the abundance of protected partners, 2) this increased abundance generates a lagged effect on partner resources, and 3) spatial dynamics can be ignored. Although a number of studies have confirmed that protection mutualism can increase the abundance of protected herbivores, the evidence for a negative effect of protected herbivores on plant quality is mixed, and we are unaware of any studies that have explored the effect of protected herbivores on plant quality across growing seasons. Here, we use the protection mutualism between ants and the treehopper Publilia concava to evaluate the assumption that treehopper herbivory has a lagged effect on plant quality. We also evaluated whether ant-protection exacerbated the negative effect of treehoppers on their host plants. We used a two-way factorial design that manipulated ant and treehopper presence on goldenrod host plants in one year, and assessed oviposition and survivorship on those same plants in the subsequent year. Treehopper herbivory was associated with a decrease in the probability of oviposition and female treehoppers laid significantly fewer egg masses on plants that had been fed on the previous year, regardless of ant-tending. In contrast, a prior history of herbivory had no impact on future treehopper performance as measured by nymph survival. Ant tending increased treehopper abundance and exacerbated the risk of plant mortality but otherwise did not significantly modify the negative effect of treehopper herbivory on plant quality or future treehopper performance. Although the increase in treehopper abundance associated with ant-tending and the lagged oviposition response of treehoppers is consistent with the core assumptions of a model showing that mutualism can be destabilizing, the avoidance of previously occupied plants for oviposition is not. These results highlight the importance of future modeling studies that explore spatiotemporal dynamics in protection mutualism, and long-term field studies that track the effect of mutualism across years.

FIGURE 7 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 7. Immature stages with some notable characters indicated with arrows, Nhambikuara mima compared to Splendeuptychia furina; Paryphthimoides brixius compared to Paryphthimoides terrestris: 1a, b) Paryphthimoides brixius ultimate instar in dorsal view and lateral view; 2a, b) Paryphthimoides terrestris ultimate instar in dorsal view and lateral view; 3a, b) Nhambikuara mima ultimate instar in dorsal view and lateral view; 4a, b) Splendeuptychia furina ultimate instar prior to pupation in dorsal view and lateral view. 1c, 2c) Paryphthimoides brixius ultimate instar head capsule and Paryphthimoides terrestris ultimate instar head capsule; 3c, 4c) Nhambikuara mima ultimate instar head capsule and Splendeuptychia furina ultimate instar head capsule; 1d–f, 2d, e) pupa of Paryphthimoides brixius and Paryphthimoides terrestris; 3d–f, 4d, e) pupa of Nhambikuara mima compared to Splendeuptychia furina. All images for Nhambikuara mima, Splendeuptychia furina, and Paryphthimoides brixius are reproduced from the present article; All images for Paryphthimoides terrestris from Corahua-Espinioza et al. (in press).

FIGURE 6 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 6. Host plants for Magneuptychia harpyia: Olyra latifolia L.: 1a) leaves; 1b) close-up view of the nodes; 1c) close-up view of inflorescence materials; 1d) host plant in situ. 1e) Taquara micrantha in situ 2a, b) adult of Magneuptychia harpyia in dorsal and ventral view (based on 2021-FLP-IMM-0352).

FIGURE 4 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 4. Host plant, two variations of Taquara micrantha. Taquara micrantha with pubescence on the abaxial surface as a host plant for Nhambikuara mima and Paryphthimoides brixius: 1a) leaves; 1b) close-up view of the node and abaxial part showing pubescence; 1c) inflorescence materials; 1d) host plant in situ. Taquara micrantha lacking pubescence for Splendeuptychia furina: 2a) leaves and inflorescence in situ; 2b) close-up view of nodes; 2c) close-up view of abaxial surface showing lack of pubescence; 2d) host plant in situ.

FIGURE 5 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 5. Illustrations of head capsules: a, b, c) first, second, and fifth (ultimate) instar of Nhambikuara mima, in frontal view; d) fifth (ultimate) instar of N. mima, lateral view indicating labeled chalazae; e–h) first, second, fourth and fifth instar of Splendeuptychia furina, in frontal view; i, j) third and fifth (ultimate) instar of Paryphthimoides brixius, in frontal view. Figure a, b are based on 2021-FLP-IMM-0538; c, d are based on 2021-FLP-IMM-0489; e, f, g are based on 2021-FLP-IMM-0554; h are based on 2021-FLP-IMM-0316; i, j are based on 2021-FLP-IMM-0395.

FIGURE 3 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 3. Life history of Paryphthimoides brixius: 1a, b) third instar in dorsal and lateral view; 2a, b) fourth instar in dorsal and lateral view; 3a, b) fifth (ultimate) instar in dorsal and lateral view; 4a, b, c) pupa in dorsal, lateral and ventral view; 5a, b) adult in dorsal and ventral view. All illustrations based on 2021-FLP-IMM-0395.

FIGURE 2 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 2. Life history of Splendeuptychia furina: 1a) egg with brown stripes and mandibles showing through translucence, 1b) head capsule showing through translucence two days prior to hatching; 2a, b) first instar in dorsal and lateral view; 3a, b) second instar in dorsal and lateral view; 4a, b) third instar in dorsal and lateral view; 5a, b) fourth instar in dorsal and lateral view; 6a, b) fifth (ultimate) instar in dorsal and lateral view; 7a, b) ultimate instar exhibiting purple colouration a day prior to pupation, dorsal and lateral view; 8a, b, c) pupa in dorsal, lateral and ventral view; 9a, b) adult in dorsal and ventral view. Figure 2b, 3b are based on 2021-FLP-IMM-0556; otherwise illustrations based on 2021-FLP-IMM-0554.

FIGURE 1 in Immature stages and new host plant records for four satyrine species feeding on herbaceous bamboos in southeastern Peru (Lepidoptera: Nymphalidae: Satyrinae: Satyrini)

FIGURE 1. Life history of Nhambikuara mima: 1a) egg, 1b) black patches present on egg two days prior to hatching; 2a, b) first instar in dorsal and lateral view; 3a, b) second instar in dorsal and lateral view; 4a, b) third instar in dorsal and lateral view; 5a, b) fourth instar in dorsal and lateral view; 6a, b) fifth (ultimate) instar in dorsal and lateral view; 7a, b, c) pupa in dorsal, lateral and ventral view; 8a, b) adult in dorsal and ventral view. Figure 1a based on 2021-FLP-IMM-0542; 1b, 2a, b, 3a, b are based on 2021-FLP-IMM-0538; otherwise illustrations based on 2021-FLP-IMM-0489.

Latitudinal influence on gametogenesis and host-parasite ecology in a marine bivalve model

Reproduction and parasites have significant impacts on marine animal populations globally. This study aimed to investigate the associative effects of host reproduction and a host-parasite interplay on a marine bivalve, along a geographic gradient of latitude. Cockles Cerastoderma edule were sampled from five European sites (54°N to 40°N), between April 2018 and October 2019. A histological survey provided data on trematode (metacercaria and sporocyst life stages), prevalence and cockle stage of gametogenesis to assess the influence of a latitudinal gradient on both interplays. Sex ratios at the northernmost sites were skewed towards females and spawning size was reduced at the lower latitudes. Trematode infection did not follow a latitudinal gradient. Localised site-related drivers, namely: seawater temperature varied spatially, having an impact on cockle-trematode interactions. Spawning was related to elevated temperatures at all sites. Prolonged spawning occurred at southern latitudes, where seawater temperatures were warmer. Trematode prevalence and the impact of trematodes on gametogenesis were found to be spatially variable, but not latitudinally. Therefore it is not possible to determine the likelihood of boom and bust events in cockles, based on the latitudinal location of a population. In terms of sublethal impacts, it appeared that energy was allocated to reproduction rather than somatic growth in southern populations, with less energy allocated to reproduction in the larger, northern cockles. The demonstrated spatial trend of energy allocation indicates the potential of a temporal trend of reduced cockle growth at northern sites, as a result of warming sea temperatures. This awareness of the spatially varying drivers of populations is crucial considering the potential for these drivers/inhibitors to be exacerbated in a changing marine environment.

Pollinator sharing, copollination, and speciation by host shifting among six closely related dioecious fig species

The obligate pollination mutualism between figs (Ficus, Moraceae) and pollinator wasps (Agaonidae, Hymenoptera) is a classic example of cospeciation. However, examples of phylogenetic incongruencies between figs and their pollinators suggest that pollinators may speciate by host shifting. To investigate the mechanism of speciation by host shifting, we examined the phylogenetic relationships and population genetic structures of six closely related fig species and their pollinators from southern China and Taiwan-Ryukyu islands using various molecular markers. The results revealed 1) an extraordinary case of pollinator sharing, in which five distinct fig species share a single pollinator species in southern China; 2) two types of copollination, namely, sympatric copollination by pollinator duplication or pollinator migration, and allopatric copollination by host migration and new pollinator acquisition; 3) fig species from southern China have colonized Taiwan repeatedly and one of these events has been followed by host shifting, host specificity reestablishment, and pollinator speciation, in order. Based on our results, we propose a model for pollinator speciation by host shifting in which reestablishment of host-specificity plays a central role in the speciation process. These findings provide important insights into understanding the mechanisms underlying pollinator speciation and host specificity in obligate pollination mutualism.

opencc-zeroMay 2022View details →

Interacting host modifier systems control Wolbachia-induced cytoplasmic incompatibility in a haplodiploid mite

Reproductive parasites such as Wolbachia spread within host populations by inducing cytoplasmic incompatibility (CI). CI occurs when parasite-modified sperm fertilizes uninfected eggs and is typified by great variation in strength across biological systems. In haplodiploid hosts, CI has different phenotypic outcomes depending on whether the fertilized eggs die or develop into males. Genetic conflict theories predict the evolution of host modulation of CI, which in turn influences the stability of reproductive parasitism. Yet, despite the ubiquity of CI-inducing parasites in nature, there is scarce evidence for intraspecific host modulation of CI strength and phenotype. Here, we tested for intraspecific host modulation of Wolbachia-induced CI in haplodiploid Tetranychus urticae mites. Using a single CI-inducing Wolbachia variant and mitochondrion, a nuclear panel was created that consisted of infected and cured near-isogenic lines. We performed a highly replicated age-synchronized full diallel cross comprised of incompatible and compatible control crosses. We uncovered host modifier systems that cause striking variation in CI strength when carried by infected T. urticae males. We observed a continuum of CI phenotypes in our crosses and identified strong intraspecific female modulation of CI phenotype. Crosses established a recessive genetic basis for the maternal effect and were consistent with polygenic Mendelian inheritance. Both male and female modulation interacted with the genotype of the mating partner. Our findings identify spermatogenesis as an important target of selection for host modulation of CI strength and underscore the importance of maternal genetic effects for the CI phenotype. Our findings reveal that intraspecific host modulation of CI is underpinned by complex genetic architectures and confirm that the evolution of reproductive parasitism is contingent on host genetics.

opencc-zeroMay 2022View details →

Data from: Host developmental stage effects on parasite resistance and tolerance

Hosts can defend themselves against parasites by either preventing or limiting infections (resistance), or limiting parasite-induced damage (tolerance). However, it remains underexplored how these defense types vary over host development with shifting patterns of resource allocation priorities. Here, we studied the role of developmental stage on resistance and tolerance in Atlantic salmon (Salmo salar). This anadromous fish has distinct life stages related to living in fresh and sea water. We experimentally exposed one-year old salmon, either at the freshwater stage or at the stage transitioning to the marine phase, to the trematode Diplostomum pseudospathaceum. Using 56 pedigreed families and multivariate animal models, we show that developmental transition is associated with reduced resistance, but does not affect tolerance. Furthermore, by comparing tolerance slopes (host fitness against parasite load) based on additive genetic effects among infected and unexposed control relatives, we observed that the slopes can be largely independent of the infection, that is they may not reflect tolerance. Together, our results suggest that the relative importance of different defense types may vary with host development and emphasize the importance of including control treatments for more confident interpretations of tolerance estimates.

opencc-by-4.0May 2022View details →

The host-feeding choice of early-instar Mythimna separata larvae can be regulated by female-released sex pheromone

Insect sex pheromones are important chemical signals in sexual communication, they are traditionally thought to be inactive to larvae. However, it was found that some lepidopteran larvae can be significantly attracted by sex pheromones of the same species in a food context. Here we reported that the host-feeding choice of early-instar Mythimna separata larvae can be effectively regulated by the sex pheromone component (Z)-11-hexadecenal (Z11-16: Ald). Further exploration revealed that two olfactory proteins, M. separata general odorant binding protein 2 (MsGOBP2) and olfactory receptor 3 (MsOR3), were molecular basis of the host-feeding choice regulation mediated by Z11-16: Ald. Silencing either MsGOBP2 or MsOR3 led to a sharply reduced preference for Z11-16: Ald-spiked hosts. It is possible that the Z11-16: Ald-based preference of the M. separata larvae for host is governed by the interplay between MsGOBP2 and MsOR3. In the present research, the interactions between MsGOBP2 and Z11-16: Ald were also discussed using molecular dynamics-based approaches. Our research explored insight into the Z11-16: Ald-mediated host-feeding choice regulation of M. separata larvae, all the results would aid in developing olfaction-based methods for controlling pests in larval stage.