Host-parasitoid Synchrony Research Articles

A Phenology Model for Simulating Oobius agrili (Hymenoptera: Encyrtidae) Seasonal Voltinism and Synchrony With Emerald Ash Borer Oviposition.

In North America, the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), continues to spread, and its egg parasitoid, Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae), is being released for emerald ash borer biocontrol well beyond their endemic climatic ranges in China. We developed a multiple cohort rate summation model to simulate O. agrili F0, F1, and F2 generations, and emerald ash borer oviposition for examining host-parasitoid synchrony across a north-south gradient from Duluth, MN (latitude 46.8369, longitude -92.1833) to Shreveport, LA (latitude 32.4469, longitude -93.8242). Temporal occurrences of critical day length for O. agrili diapause induction were integrated into the model. We used O. agrili and emerald ash borer trapping data from south central and northwestern Lower Michigan for model validation. Simulations demonstrated that 1) F0 adult emergence consistently occurred 2-5 d before emerald ash borer oviposition began; 2) F1 adult emergence was most synchronized with peak emerald ash borer oviposition compared with other generations; and 3) emerald ash borer oviposition was complete, or near so, when F2 adult emergence was predicted across the north-south gradient. Comparison of O. agrili trap captures with model simulations demonstrated that primarily two adult O. agrili generations (F0 and F1) emerged per year in Michigan and almost all F2 larvae entered diapause despite day lengths longer than critical day length in south central Michigan. Critical day length varied temporally across the north-south gradient during emergence of O. agrili generations. Determining day lengths perceived by O. agrili larvae in the field should improve model realism for examining spatiotemporal variation in O. agrili population dynamics.

How climate change affects the seasonal ecology of insect parasitoids

1. In the context of global change, modifications in winter conditions may disrupt the seasonal phenology patterns of organisms, modify the synchrony of closely interacting species and lead to unpredictable outcomes at different ecological scales.2. Parasites are present in almost every food web and their interactions with hosts greatly contribute to ecosystem functioning. Among upper trophic levels of terrestrial ecosystems, insect parasitoids are key components in terms of functioning and species richness. Parasitoids respond to climate change in similar ways to other insects, but their close relationship with their hosts and their particular life cycle – alternating between parasitic and free‐living forms – make them special cases.3. This article reviews of the mechanisms likely to undergo plastic or evolutionary adjustments when exposed to climate change that could modify insect seasonal strategies. Different scenarios are then proposed for the evolution of parasitoid insect seasonal ecology by exploring three anticipated outcomes of climate change: (i) decreased severity of winter cold; (ii) decreased winter duration; and (iii) increased extreme seasonal climatic events and environmental stochasticity.4. The capacities of insects to adapt to new environmental conditions, either through plasticity or genetic evolution, are highlighted. They may reduce diapause expression, adapt to changing cues to initiate or terminate diapause, increase voltinism, or develop overwintering bet‐hedging strategies, but parasitoids' responses will be highly constrained by those of their hosts.5. Changes in the seasonal ecology of parasitoids may have consequences on host–parasitoid synchrony and population cycles, food‐web functioning, and ecosystem services such as biological pest control.

Loss of coevolved basal and plastic responses to temperature may underlie trophic level host-parasitoid interactions under global change

Climate change has complex impacts on insect life history traits, biogeography, survival, population dynamics and host-parasitoid seasonal phenologies that affect their synchrony. This is more pronounced in tropical southern Africa, where global warming may be relatively high. While some work on Plutella xylostella (L.) temperature tolerance has been reported, none focussed on African field insect populations and implications of trophic level interaction on biological control. To determine how climate change may affect coevolved trophic level interactions in a host-parasitoid trophic system, we compared the basal thermal tolerance of wild F1 populations of the parasitoid Cotesia vestalis (Haliday) to two life stages of herbivorous host P. xylostella (L.), a global economic pest of brassicas. Our results showed significantly lower C. vestalis critical thermal limits (P < .001) compared to the host. Similarly, the parasitoid heat knockdown time and chill comma recovery time tolerance were significantly lower than that of the host (P < .001). Lethal temperature assays revealed significantly lower survival rates (P < .001) for C. vestalis at both upper and lower temperature scales. Observed differential basal temperature responses may offset coevolved host-parasitoid synchrony through differences in host-parasitoid phenologies. Hence, future biological control programmes should aim at ‘creating’ resilience and climate-fitness in natural enemies through enhancing evolutionary potential to buffer them from the changing climate. This is the first report detailing trophic level thermal tolerance of P. xylostella and larval parasitoid, C. vestalis, focussing on ecological service implications of the field-wild parasitoid populations on the herbivore host.

Contrasting effects of heat pulses on different trophic levels, an experiment with a herbivore-parasitoid model system.

Under predicted global climate change, species will be gradually exposed to warmer temperatures, and to a more variable climate including more intense and more frequent heatwaves. Increased climatic variability is expected to have different effects on species and ecosystems than gradual warming. A key challenge to predict the impact of climate change is to understand how temperature changes will affect species interactions. Herbivorous insects and their natural enemies belong to some of the largest groups of terrestrial animals, and thus they have a great impact on the functioning of ecosystems and on the services these ecosystems provide. Here we studied the life history traits of the plant-feeding insect Plutella xylostella and its specialist endoparasitoid Diadegma semiclausum, when exposed to a daily heat pulse of 5 or 10°C temperature increase during their entire immature phase. Growth and developmental responses differed with the amplitude of the heat pulse and they were different between host and parasitoid, indicating different thermal sensitivity of the two trophic levels. With a +5°C heat pulse, the adult parasitoids were larger which may result in a higher fitness, whereas a +10°C heat pulse retarded parasitoid development. These results show that the parasitoid is more sensitive than its host to brief intervals of temperature change, and this results in either positive or negative effects on life history traits, depending on the amplitude of the heat pulse. These findings suggest that more extreme fluctuations may disrupt host-parasitoid synchrony, whereas moderate fluctuations may improve parasitoid fitness.

Comparative emergence phenology of the orange wheat blossom midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae) and its parasitoids (Hymenoptera: Pteromalidae and Platygastridae) under controlled conditions

The orange wheat blossom midge, Sitodiplosis mosellana (Géhin) (Diptera: Cecidomyiidae), is a wheat (Triticum aestivum L.) pest that can cause significant yield losses. Several hymenopterous parasitoids are known to attack S. mosellana. For the effective biological control of this pest by its parasitoids, the host-parasitoid synchrony is particularly important. The synchronization between the emergence of S. mosellana and its parasitoids was studied under controlled conditions with soils sampled from two locations. For both sites, three parasitoid species were identified: Macroglenes penetrans (Kirby) (Hymenoptera: Pteromalidae), Euxestonotus error (Fitch) (Hymenoptera: Platygastridae) and Platygaster tuberosula (Kieffer) (Hymenoptera: Platygastridae). The hypothesis that parasitoid emergence is triggered by the same rainfall that induces host emergence was tested by simulating three rainfall events, a week apart. The parasitoid M. penetrans emerged later than S. mosellana with a mean of 57 ± 7 DD (degree-days above 7 °C) for insects collected from Juprelle and 68 ± 10 DD for those from Veurne (i.e., 4–5 days after its host). M. penetrans was therefore closely synchronized with its host through the same inductive rainfall, but this was not the case for E. error or P. tuberosula. Depending on when the rainfall that triggered the emergence of S. mosellana occurred, E. error and P. tuberosula emerged either before or after their host. M. penetrans is a more effective biocontrol agent of S. mosellana compared to P. tuberosula and E. error. Greater knowledge about parasitoid emergence could lead to the better positioning of insecticide treatments against wheat midge that protect and conserve the parasitoid populations.

Predicting the Impact of Temperature Change on the Future Distribution of Maize Stem Borers and Their Natural Enemies along East African Mountain Gradients Using Phenology Models.

Lepidopteran stem borers are among the most important pests of maize in East Africa. The objective of the present study was to predict the impact of temperature change on the distribution and abundance of the crambid Chilo partellus, the noctuid Busseola fusca, and their larval parasitoids Cotesia flavipes and Cotesia sesamiae at local scale along Kilimanjaro and Taita Hills gradients in Tanzania and Kenya, respectively. Temperature-dependent phenology models of pests and parasitoids were used in a geographic information system for mapping. The three risk indices namely establishment, generation, and activity indices were computed using current temperature data record from local weather stations and future (i.e., 2055) climatic condition based on downscaled climate change data from the AFRICLIM database. The calculations were carried out using index interpolator, a sub-module of the Insect Life Cycle Modeling (ILCYM) software. Thin plate algorithm was used for interpolation of the indices. Our study confirmed that temperature was a key factor explaining the distribution of stem borers and their natural enemies but other climatic factors and factors related to the top-down regulation of pests by parasitoids (host-parasitoid synchrony) also played a role. Results based on temperature only indicated a worsening of stem borer impact on maize production along the two East African mountain gradients studied. This was attributed to three main changes occurring simultaneously: (1) range expansion of the lowland species C. partellus in areas above 1200 m.a.s.l.; (2) increase of the number of pest generations across all altitudes, thus by 2055 damage by both pests will increase in the most productive maize zones of both transects; (3) disruption of the geographical distribution of pests and their larval parasitoids will cause an improvement of biological control at altitude below 1200 m.a.s.l. and a deterioration above 1200 m.a.s.l. The predicted increase in pest activity will significantly increase maize yield losses in all agro-ecological zones across both transects but to a much greater extent in lower areas.

Impact of latitude on synchrony of a scale (Fiorinia externa) (Hemiptera: Diaspididae) and its parasitoid (Encarsia citrina) (Hymenoptera: Aphelinidae) in the Eastern United States

Elongate hemlock scale (EHS) (Fiorinia externa Ferris) is an invasive species from Japan that attacks eastern hemlock (Tsuga canadensis L. Carrière) and Carolina hemlock (Tsuga caroliniana Engelmann) in the United States. Scale density is much higher in the United States compared to Japan despite the presence in both regions of the parasitoid Encarsia citrina Crawford, the species assumed to be responsible for low scale densities in Japan. EHS and E. citrina have two distinct, synchronous generations in southern Japan (Kyoto), but only one and a half generations of EHS occur in the northeastern United States (Connecticut), and these are asynchronous with E. citrina flight. It has been hypothesized that good host-parasitoid synchrony explains low scale densities in Japan. If so, then it would follow that in the southern United States, where there are two full generations of the scale, there should be a seasonal pattern of host-parasitoid synchrony similar to that found in Kyoto. To test this hypothesis, sites in Connecticut, Pennsylvania, and North Carolina were sampled weekly in 2006 and 2007. We confirmed the presence of two full generations of EHS in North Carolina; however, phenology of the vulnerable scale stage (second instar) was still asynchronous with E. citrina flight and parasitism rates were lower than in either Pennsylvania or Connecticut. The primary reason for asynchrony appears to be the occurrence of overlapping life stages and generations of EHS, which is not seen in Japan. This overlap of scale generations appears to result from long life span of first generation adult females. Longer life span may be due to host quality. Our findings emphasize the importance of research to determine differences in the population dynamics of pest species in both the native and invaded range for biological control efforts. We identify regions in Japan with high climatic match to each of our study areas, which suggest locations for future natural enemy exploration.

Influence of experimental warming and shading on host–parasitoid synchrony

AbstractAs the climate warms, many species are showing altered phenology patterns, potentially disrupting synchrony between interacting species. Recent studies have documented disrupted synchrony in plant–herbivore and predator–prey interactions. However, studies investigating climate‐related asynchrony in host–parasitoid interactions and exploring the relative responses of interacting hosts and parasitoids to climate change are lacking. This is an important gap in knowledge given the ubiquity of insect parasitoids and their importance in influencing the abundance and dynamics of their hosts. In the threatened marsh fritillary butterflyEuphydryas aurinia(Lepidoptera: Nymphalidae) and its specialized parasitoid,Cotesia bignellii(Hymenoptera: Braconidae) phenological synchrony (and consequently population fluctuations) are thought to be weather‐dependent. To assess the likely influence of climate and microenvironment change on synchrony betweenE. auriniaandC. bignellii, we experimentally manipulated the exposure of sensitive‐stage host larvae and parasitoid pupae to temperature (ambient or elevated) and shading (shaded or unshaded) regimes. We also analysed a 20‐year population dynamic dataset from the United Kingdom forE. auriniato investigate whether population variations could be explained by interannual variations in the thermal and sunshine environment. Development times were affected significantly by the experimental temperature and shading treatments forE. auriniabut not forC. bignellii. However, the contrasting responses were insufficient to significantly affect host availability for parasitoids. In the field, thermal and sunshine conditions did not influence population fluctuations, and population variations across a large (UK‐wide) scale were uncorrelated. Changes to the thermal and sunshine environment of the magnitude investigated in our experiment and within the range experienced by wildE. auriniapopulations over the last 20‐years thus seem unlikely to cause breakdown in host–parasitoid synchrony. We suggest that experiments investigating the mechanistic responses of interacting species to environmental change are needed to support the analysis and interpretation of observational data on species' phenology.

Parasitoid–host metapopulation dynamics: the causes and consequences of phenological asynchrony

SummaryThe strength of interaction between the specialist parasitoidCotesia melitaearumand the host butterflyMelitaea cinxiais influenced by the coincidence of the adult stage of the parasitoid with the larval stage of the host.We show that there is great variation in this developmental synchrony among local populations and among years, ranging from complete synchrony to complete asynchrony.The causal mechanism is early spring temperature, which affects parasitoid development differently than the development of the host.At cool air temperatures the dark‐coloured and mobile host larvae benefit from basking in the sun, while the white and immobile parasitoid cocoons develop slowly in shaded microclimates, becoming adults after hosts have pupated and are no longer available for parasitism. At warm temperatures many adult wasps emerge in time to parasitize host larvae.We show that the host–parasitoid synchrony influences subsequent parasitoid population size and the rate of colonization of previously uninhabited host populations, contributing to parasitoid metapopulation dynamics.We detected no direct effect of the phenological synchrony on local host population size, but the synchrony is likely to be important for overall host metapopulation dynamics via variation in the rate of colonization by the parasitoid.