Jeffrey A. Harvey

Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists

Plants function in a complex multitrophic environment. Most multitrophic studies, however, have almost exclusively focused on aboveground interactions, generally neglecting the fact that above- and belowground organisms interact. The spatial and temporal dynamics of above- and belowground herbivores, plant pathogens, and their antagonists, can differ in space and time. This affects the temporal interaction strengths and impacts of above- and belowground higher trophic level organisms on plants. Combining both above- and belowground compartments in studies of multitrophic interactions throughout the life cycle of plants will improve our understanding of ecology and evolution in the real world.

The Life Cycle

This chapter is concerned with approaches and techniques used in studying those aspects of parasitoid and predator life cycles that have an important bearing on the major topics covered by other chapters in this book. To illustrate what we mean, consider the female reproductive system of parasitoids which we discuss in some detail (section 2.3). As pointed out by Donaldson and Walter (1988), at least some knowledge of its function/in particular of ovarian dynamics, is crucial to a proper understanding of foraging behaviour in parasitoids. The physiological status of the ovaries may determine: (a) the duration of any preoviposition period following eclosion; (b) the rate of oviposition, (c) the frequency and duration of non-ovipositional activities, e.g. host-feeding; and (d) the insect’s response to external stimuli, e.g. odours, hosts (Collins and Dixon, 1986) (subsection 1.5.1). Note that egg load (defined in subsection 1.2.2) is now being incorporated into foraging models, as it is becoming increasingly clear that certain foraging decisions depend importantly upon the insect’s reproductive state (Jervis and Kidd, 1986; Mangel, 1989a; Chan and Godfray, 1993). It also follows from the above that a female parasitoid’s searching efficiency depends upon the functioning of its reproductive system (subsection 5.3.7), and this may in turn influence parasitoid and host population processes.

Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity

Parasitoid wasps have long been considered as model organisms for examining optimal resource allocation to different fitness functions, such as body size and development time. Unlike insect predators, which may need to consume many prey items to attain maturity, parasitoids generally rely on a limited amount of resources that are obtained from a single source (the host). This review discusses a range of ecophysiological constraints that affect host quality and concomitantly the evolution of development strategies in parasitoids. Two macroevolutionary differences in host usage strategies (idiobiosis, koinobiosis) are initially described. Over many years, particular attention has been paid in examining a range of quantitative host attributes such as size, age, or stage, as these affect idiobiont and koinobiont parasitoid development. Parasitoids and their hosts, however, constitute only a small part of an ecological community. Consequently, host quality may be affected by a broad range of factors that may operate over variable spatial and temporal scales. Intimate factors include aggressive competition with other parasitoids and pathogens for access to host resources, whereas less intimate factors include the effects of toxic plant compounds (allelochemicals) on parasitoid performance as mediated through primary and/or secondary hosts. It is suggested that future experiments should increase the levels of trophic complexity as these influence the evolution of life history and development strategies in parasitoids. This includes integration of a suite of direct and indirect mechanisms, including biological processes occurring in different ecological realms, such as above‐ground and below‐ground interactions.

FLEXIBLE LARVAL GROWTH ALLOWS USE OF A RANGE OF HOST SIZES BY A PARASITOID WASP

Recent optimality models of host-parasitoid associations have assumed that host quality varies with host size or age at parasitism. This is based on the fact that larger hosts provide more resources, making size a reliable indicator of the amount of resources available for parasitoid development. Few studies have examined this in parasitoids that allow their hosts to continue development after parasitism (koinobiont parasitoids). In this study we compared growth trajectories of the koinobiont ichneumonid endoparasitoid Venturia canescens developing in four larval instars of one of its hosts, the moth Plodia interpunctella. Hosts were reared with excess food and parasitized as late second, third, fourth, and fifth instars. Hosts were dissected at intervals after parasitism, and host and parasitoid dry mass determined. The survivorship, development time, and size of eclosing adult wasps were also monitored. Hosts parasitized by Venturia continued to grow and become prepupae, although their maximum masses were progressively smaller the earlier that the hosts were parasitized: second-instar (L2) hosts grew to 70% of control (unpar- asitized) size, while L4 and L5 hosts reached control size. The maximum larval dry mass, as well as eclosing adult size, varied with host instar at parasitism. Venturia larvae spent prolonged periods as first instars when developing from L2 hosts and grew most rapidly during early stages in L5 larvae. The data show that for Venturia, host quality is not a direct function of host size at parasitism. Furthermore, the pattern of development shown by Venturia differs markedly from that shown by aphidiid koinobiont parasitoids.

Successful range-expanding plants experience less above-ground and below-ground enemy impact

Many species are currently moving to higher latitudes and altitudes. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.

Interactions between aboveground and belowground induced responses against phytophages

Abstract Since their discovery about thirty years ago, induced plant responses have mainly been studied in interactions of plants with aboveground (AG) pathogens, herbivores and their natural enemies. Many induced responses, however, are known to be systemic and thus it is likely that responses induced by AG phytophages affect belowground (BG) phytophages feeding on the same plant, and vice versa . The awareness that interactions between AG and BG phytophages may be an important aspect in the evolution of induced responses came only recently and little research has been done to date. In this review we first summarise ecological studies that show how AG phytophages may affect BG phytophages, and vice versa . Then we focus on mechanisms governing interactions between AG and BG induced responses, such as cross-talk between signals. We chose the genus Nicotiana and the family Brassicaceae as two examples of plant groups that have been well studied for their induced responses both AG and BG – but not in concert – and explore how interactions between AG and BG induced compounds may link multitrophic interactions associated with these plants. We propose that future research on AG and BG interactions should focus on: 1). Identification of compounds and signalling pathways involved in AG and BG induced responses and analysis of their interaction mechanisms, 2). Evaluation of how induced responses affect interactions between BG and AG phytophages and their natural enemies, 3). Evaluation of the effects of AG and BG phytophages -in combination with their natural enemies- on plant fitness to identify keystone interactions that are driving the natural selection for induced responses in plants. Seit ihrer Entdeckung vor ca. dreisig Jahren werden induzierte pflanzliche Antworten der Pflanzen zumeist mit solchen Pathogenen, Herbivoren und deren naturlichen Feinden untersucht, die an oberirdischen Pflanzenteilen zu finden sind. Viele induzierte Antworten der Pflanzen konnen aber systemisch sein. Daher ist es wahrscheinlich, dass pflanzliche Antworten, die durch oberirdische Organismen induziert werden, auch solche Phytophagen beeinflussen, die unterirdisch an der Pflanze fressen, und umgekehrt. Das Bewustsein darum, dass Interaktionen zwischen ober- und unterirdischen Phytophagen ein wichtiger Aspekt in der Evolution von induzierten pflanzlichen Abwehrreaktionen sein konnen, kam erst in neuerer Zeit auf. Deshalb gibt es bisher wenig Forschung auf diesem Gebiet. In diesem Uberblick werden zunachst die Studien zusammengefasst, die den Einfluss oberirdischer Phytophager auf die unterirdischen Phytophagen zeigen und umgekehrt. Weiterhin wird auf die Mechanismen fokussiert, die Interaktionen zwischen ober- und unterirdisch fressenden Phytophagen steuern, wie z.B. Wechselwirkungen zwischen Signalen. Die Gattung Nicotiana und die Familie Brassicaceae werden als Modellpflanzen ausgewahlt, an denen die induzierte Abwehr gegen entweder oberirdische oder unterirdische Phytophage – aber nicht gegen beide gleichzeitig – bereits gut untersucht wurde. Es wird analysiert, wie Interaktionen zwischen ober- und unterirdisch induzierten Verbindungen mit multitrophischen Interaktionen dieser Pflanzen in Zusammenhang stehen. Es werden Vorschlage unterbreitet, worauf zukunftige Forschung an ober- und unterirdisch induzierten Interaktionen fokussieren sollte: (1) Identifizierung der Verbindungen und der Signalwege, die bei ober- und unterirdischer Induktion von Bedeutung sind und Analyse der Interaktionsmechanismen, (2) Untersuchung der Frage, wie induzierte Reaktionen der Pflanze sich auf Interaktionen zwischen ober- und unterirdischen Phytophagen und deren naturlichen Feinden auswirken, (3) Analyse der Auswirkungen der Effekte von ober- und unterirdisch fressenden Phytophagen unter Berucksichtigung auch ihrer naturlichen Feinde auf die pflanzliche Fitness, um solche Schlusselinteraktionen zu identifizieren, die entscheidend sind fur die Selektion der induzierten pflanzlichen Reaktion auf Angriffe durch Phytophage.

GENETIC VARIATION IN DEFENSE CHEMISTRY IN WILD CABBAGES AFFECTS HERBIVORES AND THEIR ENDOPARASITOIDS

Populations of wild Brassica oleracea L. grow naturally along the Atlantic coastlines of the United Kingdom and France. Over a very small spatial scale (i.e., <15 km) these populations differ in the expression of the defensive compounds, glucosinolates (GS). Thus far, very few studies have examined interactions between genetically distinct populations of a wild plant species and associated consumers in a multitrophic framework. Here, we compared the development of a specialist (Pieris rapae) and a generalist (Mamestra brassicae) insect herbivore and their endoparasitoids (Cotesia rubecula and Microplitis mediator, respectively) on three wild populations and one cultivar of B. oleracea under controlled greenhouse conditions. Herbivore performance was differentially affected by the plant population on which they were reared. Plant population influenced only development time and pupal mass in P. rapae, whereas plant population also had a dramatic effect on survival of M. brassicae. Prolonged development time in P. rapae corresponded with high levels of the indole GS, neoglucobrassicin, whereas reduced survival in M. brassicae coincided with high levels of the aliphatic GS, gluconapin and sinigrin. The difference between the two species can be explained by the fact that the specialist P. rapae is adapted to feed on plants containing GS and has evolved an effective detoxification system against aliphatic GS. The different B. oleracea populations also affected development of the endoparasitoids. Differences in food-plant quality for the hosts were reflected in adult size in C. rubecula and survival in M. mediator, and further showed that parasitoid performance is also affected by herbivore diet.

Plant invaders and their novel natural enemies: who is naïve?

Introduced exotic species encounter a wide range of non-coevolved enemies and competitors in their new range. Evolutionary novelty is a key aspect of these interactions, but who benefits from novelty: the exotic species or their new antagonists? Paradoxically, the novelty argument has been used to explain both the release from and the suppression by natural enemies. We argue that this paradox can be solved by considering underlying interaction mechanisms. Using plant defenses as a model, we argue that mismatches between plant and enemy interaction traits can enhance plant invasiveness in the case of toxin-based defenses, whereas invasiveness is counteracted by mismatches in recognition-based defenses and selective foraging of generalist herbivores on plants with rare toxins. We propose that a mechanistic understanding of ecological mismatches can help to explain and predict when evolutionary novelty will enhance or suppress exotic plant invasiveness. This knowledge may also enhance our understanding of plant abundance following range expansion, or during species replacements along successional stages.

Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations.

Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species : implications for host quality and parasitoid fitness

1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae.