Saskya van Nouhuys

Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids

Studies in crop species show that the effect of plant allelochemicals is not necessarily restricted to herbivores, but can extend to (positive as well as negative) effects on performance at higher trophic levels, including the predators and parasitoids of herbivores. We examined how quantitative variation in allelochemicals (iridoid glycosides) in ribwort plantain, Plantago lanceolata, affects the development of a specialist and a generalist herbivore and their respective specialist and generalist endoparasitoids. Plants were grown from two selection lines that differed ca. 5-fold in the concentration of leaf iridoid glycosides. Development time of the specialist herbivore, Melitaea cinxia, and its solitary endoparasitoid, Hyposoter horticola, proceeded most rapidly when reared on the high iridoid line, whereas pupal mass in M. cinxia and adult mass in H. horticola were unaffected by plant line. Cotesia melitaearum, a gregarious endoparasitoid of M. cinxia, performed equally well on hosts feeding on the two lines of P. lanceolata. In contrast, the pupal mass of the generalist herbivore, Spodoptera exigua, and the emerging adult mass of its solitary endoparasitoid, C. marginiventris, were significantly lower when reared on the high line, whereas development time was unaffected. The results are discussed with regards to (1) differences between specialist and generalist herbivores and their natural enemies to quantitative variation in plant secondary chemistry, and (2) potentially differing selection pressures on plant defense.

EFFECT OF IRIDOID GLYCOSIDE CONTENT ON OVIPOSITION HOST PLANT CHOICE AND PARASITISM IN A SPECIALIST HERBIVORE

The Glanville fritillary butterfly Melitaea cinxia feeds upon two host plant species in Å land, Finland, Plantago lanceolataand Veronica spicata, both of which produce iridoid glycosides. Iridoids are known to deter feeding or decrease the growth rate of many generalist insect herbivores, but they often act as oviposition cues to specialist butterflies and are feeding stimulants to their larvae. In this study, two iridoid glycosides (aucubin and catalpol) were analyzed by micellar electrokinetic capillary chromatography. We measured the spatial and temporal variation of iridoid glycosides in natural populations of the host plants of M. cinxia. We also analyzed the aucubin and catalpol content in plants in relation to their use by ovipositing females, and in relation to the incidence of parasitism of M. cinxia larvae in natural populations. The mean concentrations of aucubin and catalpol were higher in P. lanceolata than in V. spicata, and catalpol concentrations were higher than aucubin concentrations in both host species. Plantago lanceolata individuals that were used for oviposition by M. cinxia had higher aucubin concentrations than random plants and neighboring plants. Additionally, oviposition and random plants had higher catalpol concentrations than neighboring plants, indicating that ovipositing females select for high iridoid glycoside plants or that oviposition induces iridoid glycoside production in P. lanceolata. Parasitism by the specialist parasitoid wasp Cotesia melitaearum occurred most frequently in larval groups that were feeding on plants with low concentrations of catalpol, irrespective of year, population, and host plant species. Therefore, parasitoids appear to avoid or perform poorly in host larvae with high catalpol content.

Spatial and temporal patterns of caterpillar performance and the suitability of two host plant species

Abstract. 1. The butterfly Melitaea cinxia uses two host plant species in the Åland Islands of south‐west Finland. Survey data show that host plant use is spatially variable and that the two species are not used (fed on by M. cinxia larvae) in proportion to their abundances. The pattern of host plant use by M. cinxia has been attributed in part to plant distribution and spatial variation of butterfly oviposition preference.

A parasitoid wasp uses landmarks while monitoring potential resources

Social insects and insects that provision nests are well known to have complex foraging behaviour involving repeated visits to learned locations. Other insects do not forage from a central location and are generally assumed to respond to resources by simple attraction without spatial memory. This simple response to resource cues is generally taken as giving rise to patterns of resource use that correspond directly to resource distribution. By contrast, the solitary parasitoid wasp Hyposoter horticola monitors the locations of multiple potential hosts (butterfly eggs) for up to several weeks, until the hosts become susceptible to parasitism. Essentially all hosts in the landscape are found, and one-third of them are parasitized, independent of host density. Here, we show that the wasps do not relocate hosts using odour markers previously left by themselves or other foragers, nor do they find the eggs anew repeatedly. Instead, the wasps relocate host eggs by learning the position of the eggs relative to visual landmarks. The anticipatory foraging behaviour presented here is a key to the wasps exceptionally stable population dynamics.

Genetic Divergence Among Host-Specific Cryptic Species in Cotesia melitaearum Aggregate (Hymenoptera: Braconidae), Parasitoids of Checkerspot Butterflies

Abstract We used mitochondrial DNA sequence data and 12 microsatellite loci to examine the genetic structure of Cotesia melitaearum (Wilkinson) (Hymenoptera: Braconidae), a parasitoid wasp reared from two common butterfly species, Melitaea cinxia (L.) (Lepidoptera: Nymphalidae) and Euphydryas aurinia (Rottemburg) (Lepidoptera: Nymphalidae), across many localities in Europe and Asia, as well as from four more narrowly distributed related European species. The haplotypes of wasps reared from M. cinxia and E. aurinia show a complex geographic pattern presumably reflecting long-term history, but the microsatellite data yield two host-associated groups, each including populations across Europe and suggesting that currently there is no gene flow between the parasitoid populations attacking these two widely distributed host species. The cryptic species attacking E. aurinia also parasitizes the closely related Euphydryas desfontainii (Godart), but the three remaining host species have yet another, or possibly several, previously unrecognized parasitoid species. We support the cryptic species status of two C. melitaearum aggregate forms parasitizing M. cinxia and Melitaea athalia (Rottemburg) in the Åland Islands in Finland and provide behavioral and ecological data in addition to the molecular data.

Higher predation risk for insect prey at low latitudes and elevations

Risky in the tropics It is well known that diversity increases toward the tropics. Whether this increase translates into differences in interaction rates among species, however, remains unclear. To simplify the problem, Roslin et al. tested for predation rates by using a single approach involving model caterpillars across six continents. Predator attack rates were higher toward the equator, but only for arthropod predators. Science, this issue p. 742 Like diversity, predation rates among insects increase toward the equator and at lower altitudes. Biotic interactions underlie ecosystem structure and function, but predicting interaction outcomes is difficult. We tested the hypothesis that biotic interaction strength increases toward the equator, using a global experiment with model caterpillars to measure predation risk. Across an 11,660-kilometer latitudinal gradient spanning six continents, we found increasing predation toward the equator, with a parallel pattern of increasing predation toward lower elevations. Patterns across both latitude and elevation were driven by arthropod predators, with no systematic trend in attack rates by birds or mammals. These matching gradients at global and regional scales suggest consistent drivers of biotic interaction strength, a finding that needs to be integrated into general theories of herbivory, community organization, and life-history evolution.

Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata.

The ability to cope with plant defense chemicals differs between specialist and generalist species. In this study, we examined the effects of the concentration of the two main iridoid glycosides (IGs) in Plantago lanceolata, aucubin and catalpol, on the performance of a specialist and two generalist herbivores and their respective endoparasitoids. Development of the specialist herbivore Melitaea cinxia was unaffected by the total leaf IG concentration in its host plant. By contrast, the generalist herbivores Spodoptera exigua and Chrysodeixis chalcites showed delayed larval and pupal development on plant genotypes with high leaf IG concentrations, respectively. This result is in line with the idea that specialist herbivores are better adapted to allelochemicals in host plants on which they are specialized. Melitaea cinxia experienced less post-diapause larval and pupal mortality on its local Finnish P. lanceolata than on Dutch genotypes. This could not be explained by differences in IG profiles, suggesting that M. cinxia has adapted in response to attributes of its local host plants other than to IG chemistry. Development of the specialist parasitoid Cotesia melitaearum was unaffected by IG variation in the diet of its host M. cinxia, a response that was concordant with that of its host. By contrast, the development time responses of the generalist parasitoids Hyposoter didymator and Cotesia marginiventris differed from those of their generalist hosts, S. exigua and C. chalcites. While their hosts developed slowly on high-IG genotypes, development time of H. didymator was unaffected. Cotesia marginiventris actually developed faster on hosts fed high-IG genotypes, although they then had short adult longevity. The faster development of C. marginiventris on hosts that ate high-IG genotypes is in line with the “immunocompromized host” hypothesis, emphasizing the potential negative effects of toxic allelochemicals on the host’s immune response.

Reprint of “Conservation biological control and enemy diversity on a landscape scale” [Biol. Control 43 (2007) 294–309]

Abstract Conservation biological control in agroecosystems requires a landscape management perspective, because most arthropod species experience their habitat at spatial scales beyond the plot level, and there is spillover of natural enemies across the crop–noncrop interface. The species pool in the surrounding landscape and the distance of crop from natural habitat are important for the conservation of enemy diversity and, in particular, the conservation of poorly-dispersing and specialized enemies. Hence, structurally complex landscapes with high habitat connectivity may enhance the probability of pest regulation. In contrast, generalist and highly vagile enemies may even profit from the high primary productivity of crops at a landscape scale and their abundance may partly compensate for losses in enemy diversity. Conservation biological control also needs a multitrophic perspective. For example, entomopathogenic fungi, plant pathogens and endophytes as well as below- and above-ground microorganisms are known to influence pest-enemy interactions in ways that vary across spatiotemporal scales. Enemy distribution in agricultural landscapes is determined by beta diversity among patches. The diversity needed for conservation biological control may occur where patch heterogeneity at larger spatial scales is high. However, enemy communities in managed systems are more similar across space and time than those in natural systems, emphasizing the importance of natural habitat for a spillover of diverse enemies. According to the insurance hypothesis, species richness can buffer against spatiotemporal disturbances, thereby insuring functioning in changing environments. Seemingly redundant enemy species may become important under global change. Complex landscapes characterized by highly connected crop–noncrop mosaics may be best for long-term conservation biological control and sustainable crop production, but experimental evidence for detailed recommendations to design the composition and configuration of agricultural landscapes that maintain a diversity of generalist and specialist natural enemies is still needed.

Patch Time Allocation by a Parasitoid: The Influence of Con-specifics, Host Abundance and Distance to the Patch

Patch residence time is at the core of models of decision making by foragers living in patchy environments. We studied patch residence time (PRT) of Ibalia leucospoides, a parasitoid of the woodwasp Sirex noctilio, as assigned to 4 treatments (recent feeding and/or oviposition experience) foraging in an array of host-infested pine logs. We tested the effects of distance from release point, host abundance, and the number of con-specifics at the time of arrival, on patch (pine log) residence time. PRT depended on a combination of patch quality (number of hosts in a log) and distance from the release point. Neither the presence of con-specifics on the patch, prior exposure to hosts, nor feeding prior to the experiment affected the time spent on a patch. We conclude that PRT in I. leucospoides meets Marginal Value Theorem predictions qualitatively, overruling the effects recent oviposition experience, access to food and contact with conspecifics. These findings are in line with the reported pro-ovigeny in I. leucospoides as well as the strong spatial aggregation of hosts in the field.

Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly

Variation of host quality affects population dynamics of parasitoids, even at the landscape scale. What causes host quality to vary and the subsequent mechanisms by which parasitoid population dynamics are affected can be complex. Here, we examine the indirect interaction of a plant pathogen with a parasitoid wasp. Under laboratory conditions, parasitoids from hosts fed fungus-infected plants weighed less than those from hosts fed uninfected plants,. indicating that the fungus causes the hosts to be of poor quality. However, parasitoids reared from hosts fed fungal-infected diet also tended to be female, a characteristic associated with high host quality. The pathogen, herbivore and parasitoid persist regionally as metapopulations in a shared landscape in Åland, Finland. In an analysis of the metapopulation dynamics of the parasitoid over 6 years, the probability of colonization of a host population increased by more than twofold in patches occupied by the plant pathogen. While we cannot determine that the relationship is causal, a compelling explanation is that the plant pathogen facilitates the establishment by the parasitoid by increasing the fraction of female offspring. This is a novel mechanism of spatial multi-trophic level interactions.