Effect of egg production dynamics on the functional response of two parasitoids.

Functional response describes the number of hosts attacked by a parasitoid in relation to host densities and plays an important role by connecting behavioral-level processes with community-level processes. Most functional response studies were carried out using simple experimental designs where the insects were confined to a plain and small arena with different host densities during a fixed period of time. With these designs, other factors that might affect the functional response of parasitoids were not analyzed, such as fecundity, age, and experience. We proposed a series of latent-variables Markovian models that comprised an integrated approach of functional response and egg production models to estimate the realized lifetime reproductive success of parasitoids. As a case study, we used the parasitoids Anagyrus cachamai and A. lapachosus (Hymenoptera: Encyrtidae), two candidate agents for neoclassical biocontrol of the Puerto Rican cactus pest mealybug, Hypogeococcus sp. (Hemiptera: Pseudococcidae). The tested species were assessed according to their physiology and prior experience. We estimated the number of mature eggs after emergence, egg production on the first day, egg production rate, the proportion of eggs resorbed, egg resorption threshold, and egg storage capacity. Anagyrus cachamai and A. lapachosus both presented a type III functional response. However, the two parasitoids behaved differently; for A. cachamai, the number of parasitized hosts decreased with female age and depended on the number of mature eggs that were available for oviposition, whereas A. lapachosus host parasitism increased with female age and was modulated by its daily egg load and previous experience. The methodology presented may have large applicability in pest control, invasive species management, and conservation biology, as it has the potential to increase our understanding of the reproductive biology of a wide variety of species, ultimately leading to improved management strategies.

Pilot Testing of an Area-Wide Biological Control Strategy against the Coffee Berry Borer in Colombia Using African Parasitoids.

The coffee berry borer (CBB), Hypothenemus hampei (Ferrari, 1867) (Coleoptera: Curculionidae: Scolytinae), native to Africa, is a major global insect pest of coffee. It has invaded many coffee production areas around the world that do not have natural enemies. In this study, two African parasitoids, Prorops nasuta Waterston (Hymenoptera: Bethylidae) and Phymastichus coffea Waterston (Hymenoptera: Eulophidae), were mass-reared for field release against H. hampei in Chinchiná, Colombia. More than 1.5 million wasps of each species were released on a 61-hectare coffee farm in replicated plots, resulting in parasitism rates of up to 7.7% for P. nasuta and 56.3% for P. coffea. This led to a maximum reduction in H. hampei field populations of 81% from dispersal coffee plots (old coffee crops before plant stumping) and 64.3% in colonization coffee plots (new coffee crops with active growing and fruiting plants) within the farm. As a result of this area-wide strategy, the percentage of CBB-infested coffee berries in colonization coffee plots decreased from 51.1 to 77.5% compared to coffee plots without parasitoid releases. This approach offers a promising alternative to the use of chemical insecticides and could be integrated into current pest management programs to control H. hampei.

Genomic and ecological evidence shed light on the recent demographic history of two related invasive insects.

Hypogeococcus pungens is a species complex native to southern South America that is composed of at least five putative species, each one specialized in the use of different host plants. Two of these undescribed species were registered as invasive in Central and North America: Hyp-C is a cactophagous mealybug that became an important pest that threatens endemic cactus species in Puerto Rico, and Hyp-AP feeds on Amaranthaceae and Portulacaceae hosts, but does not produce severe damage to the host plants. We quantified genomic variation and investigated the demographic history of both invasive species by means of coalescent-based simulations using high throughput sequencing data. We also evaluated the incidence of host plant infestation produced by both species and used an ecological niche modeling approach to assess potential distribution under current and future climatic scenarios. Our genetic survey evinced the footprints of strong effective population size reduction and signals of genetic differentiation among populations within each species. Incidence of plant attacks varied between species and among populations within species, with some host plant species preferred over others. Ecological niche modeling suggested that under future climatic scenarios both species would expand their distribution ranges in Puerto Rico. These results provide valuable information for the design of efficient management and control strategies of the Puerto Rican cactus pest and shed light on the evolutionary pathways of biological invasions.

Influence of competition and intraguild predation between two candidate biocontrol parasitoids on their potential impact against Harrisia cactus mealybug, Hypogeococcus sp. (Hemiptera: Pseudococcidae).

When two or more parasitoid species, particularly candidates for biocontrol, share the same target in the same temporal window, a complex of behaviors can occur among them. We studied the type of interactions (competition and intraguild predation) that existed between the nymphal parasitoids Anagyrus cachamai and A. lapachosus (Hymenoptera: Encyrtidae), two candidate neoclassical biocontrol agents against the Puerto Rican cactus pest mealybug, Hypogeococcus sp. (Hemiptera: Pseudococcidae). The surrogate native congener host in Argentina, the cactus mealybug Hypogeococcus sp., was studied to predict which species should be released; in the case that both should be released, in which order, and their potential impact on host suppression. In the laboratory we conducted experiments where different densities of the host mealybug were exposed to naive females of A. cachamai and A. lapachosus sequentially in both directions. Experiments were analyzed by combining a series of competitive behavioral and functional response models. A fully Bayesian approach was used to select the best explaining models and calculate their parameters. Intraguild predation existed between A. cachamai, the species that had the greatest ability to exploit the resource, and A. lapachosus, the strongest species in the interference competition. The role that intraguild predation played in suppression of Hypogeococcus sp. indicated that a multiple release strategy for the two biocontrol agents would produce better control than a single release; as for the release order, A. lapachosus should be released first.

Untangling the Hypogeococcus pungens species complex (Hemiptera: Pseudococcidae) for Argentina, Australia, and Puerto Rico based on host plant associations and genetic evidence.

Hypogeococcus pungens, a mealybug native of southern South America, is devastating native cacti in Puerto Rico and threatening cactus diversity in the Caribbean, and potentially in Central and North America. The taxonomic status of H. pungens is controversial since it has been reported feeding not only on Cactaceae but also on other plant families throughout its distribution range. However, in Australia, where the species had been exported from Argentina to control weedy American cacti, it was never found on host plants other than Cactaceae. These conflicting pieces of evidence not only cast doubt on the species identity that invaded Puerto Rico, but also have a negative impact on the search for natural enemies to be used in biological control programs against this pest. Here we present reproductive incompatibility and phylogenetic evidences that give support to the hypothesis that H. pungens is a species complex in which divergence appears to be driven by the host plants. The nuclear EF1α and 18S and the mitochondrial COI genes were used as markers to evaluate the phylogenetic relationships among H. pungens populations collected in Argentina, Australia and Puerto Rico feeding on Cactaceae and/or Amaranthaceae. Additionally, we conducted reciprocal crosses between mealybugs from both hosts. Species delimitation analysis revealed two well-supported putative species within H. pungens, one including mealybugs feeding on Amaranthaceae (H. pungens sensu stricto), and a new undescribed species using Cactaceae as hosts. Additionally, we found asymmetric reproductive incompatibility between these putative species suggesting recent reproductive isolation. The Bayesian species delimitation also suggested that the Australian mealybug population may derive from another undescribed species. Overall, the patterns of genetic differentiation may be interpreted as the result of recent speciation events prompted by host plant shifts. Finally, the finding of a single haplotype in the Puerto Rico population suggests only one invasive event. We still need to identify the geographical origin of the pest in order to enable the use of biological control to reduce the threat to cacti diversity in the Caribbean.

Invasive plant species in the West Indies: geographical, ecological, and floristic insights.

The level of invasion (number or proportion of invasive species) in a given area depends on features of the invaded community, propagule pressure, and climate. In this study, we assess the invasive flora of nine islands in the West Indies to identify invasion patterns and evaluate whether invasive species diversity is related to geographical, ecological, and socioeconomic factors. We compiled a database of invasive plant species including information on their taxonomy, origin, pathways of introduction, habitats, and life history. This database was used to evaluate the similarity of invasive floras between islands and to identify invasion patterns at regional (West Indies) and local (island) scales. We found a total of 516 alien plant species that are invasive on at least one of the nine islands studied, with between 24 to 306 invasive species per island. The invasive flora on these islands includes a wide range of taxonomic groups, life forms, and habitats. We detected low similarity in invasive species diversity between islands, with most invasive species (>60%) occurring on a single island and 6% occurring on at least five islands. To assess the importance of different models in predicting patterns of invasive species diversity among islands, we used generalized linear models. Our analyses revealed that invasive species diversity was well predicted by a combination of island area and economic development (gross domestic product per capita and kilometers of paved roadways). Our results provide strong evidence for the roles of geographical, ecological, and socioeconomic factors in determining the distribution and spread of invasive species on these islands. Anthropogenic disturbance and economic development seem to be the major drivers facilitating the spread and predominance of invasive species over native species.