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.
In fall, Myzus persicae (Sulzer) (Homoptera: Aphididae) may exhibit population resurgence in winter oilseed rape in France. This resurgence may arise from pyrethroid treatments against Coleoptera (Psylliodes chrysocephala L.) that either kill parasitoids present during treatment or prevent recolonization by off-crop parasitoids. We studied the impact of Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae) on populations of M. persicae when parasitoids were introduced on deltamethrin-treated plants at increasing intervals after treatment. Parasitoids were introduced 1, 2, 7, or 14 d posttreatment on individually caged plants infested with established populations of M. persicae. Aphids were counted 7, 14 and 21 d after parasitoid introduction. First, we observed that both the pesticide and the parasitoid reduced aphid population growth and that their effects were additive. Second, there was no mortality of parasitoids exposed to treated leaves in a device with a refuge area, and only 20% of mortality without the refuge area. Furthermore, deltamethrin residues had no effect on the reproduction of D. rapae females. Compared with the known toxicity of deltamethrin to D. rapae on glass, this low mortality may have been due to both the high liposolubility of deltamethrin (leading to a rapid diffusion of residues in the oilseed rape leaf cuticle) and to the existence of a refuge area. This work suggests that D. rapae could limit populations of M. persicae in the fall, even after pyrethroid treatment, because the presence of deltamethrin residues had little impact on the parasitoid.
In field observations and laboratory experiments, we found that virgin females of the solitary parasitoid Aphelinus asychis did not emit a volatile sex pheromone to attract males, contrary to what has been reported in many other parasitoid species. Instead, we found that virgin females deposited a sex pheromone on the substrate to which males responded by intensively searching on and near the marked area. Males did not respond to leaves exposed to mated females or to other males. In patches of 64 wheat leaves, males were dispersed from a central release point, and more males were subsequently observed on leaves exposed to virgin females than on unexposed leaves. The pheromone faded to inactivity in less than 24 h. To examine whether the trail pheromone would be sufficient for mate finding by males in the field, we modeled random movement of males among plant stems where the trail pheromone was the only cue males used to find females. The probability that females encountered at least one male in their lifetime increased with male density and time after female emergence. Given the range of densities of A. asychis in barley and wheat fields near Montpellier, France, the model generated an encounter probability sufficient to explain the survival of established populations. The model also suggested that difficulty in finding mates at low density might be a problem for invading populations.
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.
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.
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, matefinding, 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.
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