Xavier Fauvergue

The biology of small, introduced populations, with special reference to biological control.

Populations are introduced into novel environments in different contexts, one being the biological control of pests. Despite intense efforts, less than half introduced biological control agents establish. Among the possible approaches to improve biological control, one is to better understand the processes that underpin introductions and contribute to ecological and evolutionary success. In this perspective, we first review the demographic and genetic processes at play in small populations, be they stochastic or deterministic. We discuss the theoretical outcomes of these different processes with respect to individual fitness, population growth rate, and establishment probability. Predicted outcomes differ subtly in some cases, but enough so that the evaluating results of introductions have the potential to reveal which processes play important roles in introduced populations. Second, we attempt to link the theory we have discussed with empirical data from biological control introductions. A main result is that there are few available data, but we nonetheless report on an increasing number of well‐designed, theory‐driven, experimental approaches. Combining demography and genetics from both theoretical and empirical perspectives highlights novel and exciting avenues for research on the biology of small, introduced populations, and great potential for improving both our understanding and practice of biological control.

Oviposition behaviour and patch-time allocation in two aphid parasitoids exposed to deltamethrin residues

Neurotoxic insecticides are widely used for crop protection. One consequence is that changes in behaviour can be expected in surviving beneficial insects because of an impairment of host perception and motor abilities. Under laboratory conditions, we studied the impact of deltamethrin, a pyrethroid, on the oviposition behaviour of two hymenopterous parasitoids of aphids, Aphidius matricariae (Haliday) and Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae). They both parasitize Myzus persicae (Sulzer) (Homoptera: Aphididae), which is the preferred host of A. matricariae, regardless of the host plant, whereas D. rapae is a major parasitoid of aphids on Cruciferae crops, including M. persicae. After exposure to deltamethrin, the different items of oviposition behaviour and the total time spent on the patch were recorded. The results showed that the patch time allocation by both parasitoid species was not significantly affected by deltamethrin treatment, when compared with the controls. Nor were the frequencies and sequences of behavioural items modified (e.g., frequency of sting). It therefore appeared that the patch use of A. matricariae and D. rapae on new colonies of M. persicae was not disturbed by deltamethrin at the three doses tested. The possibility that parasitoid strains are partially tolerant to deltamethrin is discussed.

Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality

Charnov’s marginal value theorem predicts that female parasitoids should exploit patches of their hosts until their instantaneous rate of fitness gain reaches a marginal value. The consequences of this are that: (1) better patches should be exploited for a longer time; (2) as travel time between patches increases, so does the patch residence time; and (3) all exploited patches should be reduced to the same level of profitability. Patch residence time was measured in an egg parasitoid Anaphes victus (Hymenoptera: Mymaridae) when patch quality and travel time, approximated here as an increased delay between emergence and patch exploitation, varied. As predicted, females stayed longer when patch quality and travel time increased. However, the marginal value of fitness gain when females left the patch increased with patch quality and decreased with travel time. A. victus females appear to base their patch quality estimate on the first patch encountered rather than on a fixed innate estimate, as was shown for another egg parasitoid Trichogramma brassicae. Such a strategy could be optimal when inter-generational variability in patch quality is high and within-generational variability is low.

French wasps in the New World: experimental biological control introductions reveal a demographic Allee effect

Many populations introduced into a novel environment fail to establish. One underlying process is the Allee effect, i.e., the difficulty of individuals to survive and reproduce when rare, and the consequently low or negative population growth. Although observations showing a positive relation between initial population size and establishment probability suggest that the Allee effect could be widespread in biological invasions, experimental tests are scarce. Here, we used a biological control program against Diuraphis noxia (Mordvilko) (Hemiptera: Aphididae) in the United States to manipulate initial population size of the introduced parasitoid Aphelinus asychis Walker (Hymenoptera: Aphelinidae) originating from France. For eight populations and three generations after introduction, we studied spatial distribution and spread, density, mate-finding, and population growth. Dispersal was lower in small populations during the first generation. Smaller initial population size nonetheless resulted in lower density during the three generations studied. The proportion of mated females and the population sex ratio were not affected by initial population size or population density. Net reproductive rate decreased with density within each generation, suggesting negative density-dependence. But for a given density, net reproductive rate was smaller in populations initiated with few individuals than in populations initiated with many individuals. Hence, our results demonstrate a demographic Allee effect. Mate-finding is excluded as an underlying mechanism, and other component Allee effects may have been overwhelmed by negative density-dependence in reproduction. Impact of generalist predators could provide one potential explanation for the relationship between initial population size and net reproductive rate. However, the continuing effect of initial population size on population growth suggests genetic processes may have been involved in the observed demographic Allee effect.

INVADING PARASITOIDS SUFFER NO ALLEE EFFECT: A MANIPULATIVE FIELD EXPERIMENT

One frequent explanation for the failure of biological invasions is the Allee effect: due to positive density dependence, initially small invading populations may fail to establish and spread. Populations released for biological control are similar to fortuitous invading populations and may therefore suffer from Allee effects. However, unlike fortuitous invasions, biological control allows the experimental manipulation of initial population size and, thus, offers a unique opportunity to test for the occurrence of Allee effects. We manipulated the initial size of 45 populations of a parasitoid wasp introduced for the biological control of a phytophagous insect and followed the population dynamics of both parasitoids and hosts during three years. Our results suggest an absence of Allee effects but clear negative density dependence instead: (1) the probability of establishment after three years was not affected by initial population size; (2) net reproductive rate was highest at low parasitoid density and high host density; (3) the sex ratio, reflecting the proportion of virgin females, did not increase at low density, suggesting that low densities did not impede mate-finding; (4) the depression of host populations did not depend upon the number of parasitoids introduced. This is, to our knowledge, the first experimental test of the Allee effect in an invading parasitoid. It leads us to propose that a number of behavioral and life-history features of many parasitoids could protect them from Allee effects.

Olfactory response of two aphid parasitoids, Lysiphlebus testaceipes and Aphidius colemani, to aphid-infested plants from a distance

The role of volatile stimuli in the host‐searching behaviour of the two parasitoid species Lysiphlebus testaceipes Cresson and Aphidius colemani Viereck (Hymenoptera: Braconidae) was studied in relation to the host Aphis gossypii Glover (Homoptera: Aphididae) on cucumber plants, Cucumis sativa L. (Cucurbitaceae). Experiments were carried out in the laboratory in a wind tunnel, exposing individual parasitoids to signals from three sources simultaneously: (1) a complex of cucumber plants, Cucumis sativa, and A. gossypii; (2) uninfested cucumber plants; and (3) dummy cardboard plants. The flight response of the female parasitoids was considered oriented when they landed on plants and non‐oriented when the females landed elsewhere (tunnel floor, sides, or top). Results showed that the proportion of oriented flights was significantly higher than non‐oriented flights. A comparison between the two wasp species suggested that A. colemani females may be better able to locate plants than L. testaceipes, as the proportion of females that made an oriented flight was higher in this species. For females of both wasp species which made an oriented flight, landing was more often observed on real plants (i.e., with no difference between infested and uninfested plants), than on dummy plants. A description of the flight behaviour of the two parasitoid species is presented. One difference between the species was that flight duration was higher in L. testaceipes than in A. colemani. This work shows that the two parasitoid species respond to stimuli from the host‐plants of A. gossypii in a similar way to parasitoids of aphid pests in other crops.

Response of the melon aphid, Aphis gossypii, to host-plant resistance: evidence for high adaptive potential despite low genetic variability

In agrosystems, pests are submitted to strong human‐imposed selective pressures to which they sometimes adapt rapidly, either through selection of genotypes resulting from mutation and/or recombination events, or through phenotypic plasticity. Understanding how insects respond to such selective pressures is of great importance for sustainable pest management strategies, such as the use of resistant plants. In this study, we investigated the genetic and phenotypic variability of anholocyclic Aphis gossypii Glover (Hemiptera: Aphididae) strains, in response to the resistance gene Vat that is present in melon crops. Forty‐nine aphid colonies were sampled on several melon crops in southern France, genotyped using 15 microsatellite loci, and tested in phenotypic experiments using Vat or non‐Vat melons. The level of genetic polymorphism between these colonies was low, as only seven multilocus genotypes were detected. In contrast, the phenotypic variability for life‐history and behavioral traits between colonies, including those sharing the same genotype, was unexpectedly high, with a continuum of response to the Vat gene from complete susceptibility to strong virulence. The low genetic polymorphism associated with a strong phenotypic variability highlights the high adaptive potential of A. gossypii and the major role of environmental cues in shaping phenotypic responses of this aphid to pest management strategies.

Parasitoids use herbivore-induced information to adapt patch exploitation behaviour

Abstract.  1. Optimal foraging models ultimately predict that female parasitoids should exploit rich host patches for longer than poorer ones. At the proximate level, mechanistic models and experimental studies show that parasitoids use both chemicals produced by their hosts and direct encounters with their hosts to estimate patch quality. Although it has been extensively studied in the context of host location, the use of herbivore‐induced plant response by insect parasitoids has never been considered in the context of patch time allocation.

A review of mate‐finding Allee effects in insects: from individual behavior to population management

Like other animals and plants, insects may find it difficult to survive and reproduce in small populations, to the extent that their long‐term persistence may be jeopardized. The Allee effect is a theoretical framework that formalizes this decrease in survival or reproduction in small populations, and the resulting decrease in population growth and persistence. Mating failure in low‐density populations is likely to generate an Allee effect and, therefore, has a major effect on the functioning of small populations. Here, I review mate‐finding Allee effects in insect species, and their consequences for individual mating success, population dynamics, and population management. I focus, in particular, on the comparison of theoretical expectations with observational data. Several studies have reported some degree of mating failure at low density. However, almost none of the datasets available allow comparison with the predictions of classical mate‐searching models. A few studies at the population level have reported the co‐occurrence of mating failure at low density and a demographic Allee effect, but no study has yet clearly demonstrated a causal relationship between mating failure and lower rates of population growth. Thus, although the theoretical development of management tactics based on Allee effects is considered promising, the current lack of evidence supporting this strategy limits its potential relevance. I call here for a more rigorous approach to the study of mate‐finding Allee effects and propose new approaches for this purpose.

Parasitoid mating structures when hosts are patchily distributed : field and laboratory experiments with Leptopilina boulardi and L. heterotoma

Populations spatially structured at the time of mating may experience local mate competition (LMC) and inbreeding, two factors known to select, in haplodiploid organisms, for a female biased sex ratio. Populations of the two Drosophila parasitoids Leptopilina boulardi and L. heterotoma could have such a structure because although males and females develop from different hosts, many hosts are clumped within fruits decaying on the ground. However, contrary to theoretical expectations. we found field sex ratios to be only slightly female biased (L. heterotoma) or even male biased (L. boulardi). This raised the question of whether populations of these two species experience any level of LMC and inbreeding. To address this question. we studied male and female spatio-temporal patterns of emergence, dispersal, and male attraction to females. We found that within days, emergence was synchronized, with males starting to emerge slightly before females. However, when emergence was analyzed day-by-day for individuals laid during the same oviposition bout, males and females emerged on different days. A similar analysis for fruits collected in the field showed that about 20% of males and 20% of females emerged in the absence of any potential mate Furthermore, males dispersed from their natal sites soon after emergence, at a rate similar to that of conspecific females. With laboratory and field experiments, we found that dispersing males were attracted to virgin females via in-flight orientation mediated by a volatile sex pheromone. These data suggest that the mating structures of L. boulardi and L. heterotoma differ from that assumed by classic LMC models. Because males disperse and search for females from other patches, local mate competition and inbreeding will be reduced to an extent depending on male mating success after dispersal. Inbreeding could also be reduced because synchronous emergence of males and females mainly results from asynchronous oviposition bouts, so that on-patch matings should concern unrelated individuals, Such a mating structure explains the absence of a strong sex ratio bias toward females in these two species. More generally, through a review of the published literature on sex pheromones, we suggest that mating structures with a non-negligible fraction of off-patch matings could be widespread among parasitoids.