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.

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.

Revisiting the influence of learning in predator functional response, how it can lead to shapes different from type III.

Predator/parasitoid functional response is one of the main tools used to study predation behavior, and in assessing the potential of biological control candidates. It is generally accepted that predator learning in prey searching and manipulation can produce the appearance of a type III functional response. Holling proposed that in the presence of alternative prey, at some point the predator would shift the preferred prey, leading to the appearance of a sigmoid function that characterized that functional response. This is supported by the analogy between enzyme kinetics and functional response that Holling used as the basis for developing this theory. However, after several decades, sigmoidal functional responses appear in the absence of alternative prey in most of the biological taxa studied. Here, we propose modeling the effect of learning on the functional response by using the explicit incorporation of learning curves in the parameters of the Holling functional response, the attack rate (a), and the manipulation time (h). We then study how the variation in the parameters of the learning curves causes variations in the shape of the functional response curve. We found that the functional response product of learning can be either type I, II, or III, depending on what parameters act on the organism, and how much it can learn throughout the length of the study. Therefore, the presence of other types of curves should not be automatically associated with the absence of learning. These results are important from an ecological point of view because when type III functional response is associated with learning, it is generally accepted that it can operate as a stabilizing factor in population dynamics. Our results, to the contrary, suggest that depending on how it acts, it may even be destabilizing by generating the appearance of functional responses close to type I.

Spatial and host related genomic variation in partially sympatric cactophagous moth species.

Surveys of patterns of genetic variation in natural sympatric and allopatric populations of recently diverged species are necessary to understand the processes driving intra- and interspecific diversification. The South American moths Cactoblastis cactorum, Cactoblastis doddi and Cactoblastis bucyrus are specialized in the use of cacti as host plants. These species have partially different geographic ranges and differ in patterns of host plant use. However, there are areas that overlap, particularly, in northwestern Argentina, where they are sympatric. Using a combination of genome-wide SNPs and mitochondrial data we assessed intra and interspecific genetic variation and investigated the relative roles of geography and host plants on genetic divergence. We also searched for genetic footprints of hybridization between species. We identified three well delimited species and detected signs of hybridization in the area of sympatry. Our results supported a hypothetical scenario of allopatric speciation in the generalist C. cactorum and genetic interchange during secondary geographic contact with the pair of specialists C. bucyrus and C. doddi that probably speciated sympatrically. In both cases, adaptation to new host plants probably played an important role in speciation. The results also suggested the interplay of geography and host plant use as drivers of divergence and limiting gene flow at intra and interspecific levels.

Contributions to the knowledge of the Cicadellini sharpshooters (Hemiptera: Cicadellidae) associated with citrus orchards in Argentina.

Xylella fastidiosa Wells et al. is a xylem-borne bacterium that causes some of the most important plant diseases to woody plants such as citrus, olives, almonds and other cultures. This pathogen is mainly transmitted by sharpshooters, among which the tribe Cicadellini (Cicadellinae) includes the largest number of proven vectors. The correct identification of the vectors, along with biological and phenological information, are necessary to identify the key vectors involved in the spread of the bacterium and, consequently, establish control strategies and evaluate risks at a local or regional scale. However, lack of information on the Cicadellini from Argentina has delayed the implementation of control measures. Based on surveys conducted in the main citrus producing areas along with bibliographic data, this contribution provides the first list of Cicadellini species from Argentina that are potential vectors of X. fastidiosa; an identification key to these sharpshooters is provided. Twelve species were recorded from northeastern citrus groves, while from northwestern orchards, with previous information totally absent, 10 species were recorded. Eight species are shared by all producing regions, and five of them are proven vectors of X. fastidiosa (Bucephalogonia xanthophis (Berg), Dilobopterus costalimai Young, Macugonalia cavifrons (Stål), M. leucomelas (Walker), Sonesimia grossa (Signoret)). This contribution provides 22 new insect-plant relationships, information on their natural enemies, the geographic distribution of all species is broadened and the female genitalia of three proven vectors are described for the first time.

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.

Species complex diversification by host plant use in an herbivorous insect: The source of Puerto Rican cactus mealybug pest and implications for biological control.

Cryptic taxa have often been observed in the form of host-associated species that diverged as the result of adaptation to alternate host plants. Untangling cryptic diversity in species complexes that encompass invasive species is a mandatory task for pest management. Moreover, investigating the evolutionary history of a species complex may help to understand the drivers of their diversification. The mealybug Hypogeococcus pungens was believed to be a polyphagous species from South America and has been reported as a pest devastating native cacti in Puerto Rico, also threatening cactus diversity in the Caribbean and North America. There is neither certainty about the identity of the pest nor the source population from South America. Recent studies pointed to substantial genetic differentiation among local populations, suggesting that H. pungens is a species complex. In this study, we used a combination of genome-wide SNPs and mtDNA variation to investigate species diversity within H. pungens sensu lato to establish host plant ranges of each one of the putative members of the complex, to evaluate whether the pattern of host plant association drove diversification in the species complex, and to determine the source population of the Puerto Rican cactus pest. Our results suggested that H. pungens comprises at least five different species, each one strongly associated with specific host plants. We also established that the Puerto Rican cactus pest derives from southeastern Brazilian mealybugs. This is an important achievement because it will help to design reliable strategies for biological control using natural enemies of the pest from its native range.

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.

A new Anagyrus (Hymenoptera: Encyrtidae) from Argentina, parasitoid of Hypogeococcus sp. (Hemiptera: Pseudococcidae) on Harrisia pomanensis (Cactaceae).

A new species of Anagyrus Howard (Hymenoptera: Encyrtidae), A. lapachosus sp. n., is described from Salta Province of Argentina as a parasitoid of Hypogeococcus sp. (Hemiptera: Pseudococcidae) on Harrisia pomanensis cactus (Cactaceae). It is a candidate "new association" biological control agent for quarantine evaluation and possible following introduction to Puerto Rico (USA) against another Hypogeococcus sp., commonly called the Harrisia cactus mealybug and often misidentified as H. pungens Granara de Willink (according to our unpublished data the latter attacks only Amaranthaceae), which devastates or threatens the native cacti there and also in some other Caribbean islands (Triapitsyn, Aguirre et al. 2014; Carrera-Martínez et al. 2015).

Two new species of Anagyrus (Hymenoptera: Encyrtidae) from Argentina, parasitoids of Hypogeococcus spp. (Hemiptera: Pseudococcidae), with taxonomic notes on some congeneric taxa.

Two new species of Anagyrus Howard (Hymenoptera: Encyrtidae) are described from Argentina, A. cachamai Triapitsyn, Logarzo & Aguirre sp. n. (Catamarca, Córdoba, Salta and Tucumán Provinces) and A. quilmes Triapitsyn, Logarzo & Aguirre sp. n. (Catamarca, Salta and Tucumán). Both new species are parasitoids of Hypogeococcus spp. (Hemiptera: Pseudococcidae). Anagyrus cachamai is a parasitoid of H. pungens Granara de Willink on Alternanthera paronychioides, A. pungens and Gomphrena sp. (Amaranthaceae), and also of a Hypogeococcus sp. on Cleistocactus baumannii and Hypogeococcus sp. on C. smaragdiflorus (Cactaceae). Anagyrus quilmes is a parasitoid of H. pungens on A. paronychioides, A. pungens and Gomphrena sp. Other biological traits of the new species are also reported. These parasitoids may be of importance as potential candidate biological control agents against a Hypogeococcus sp., commonly called the Harrisia cactus mealybug and identified as H. pungens, but possibly not belonging to that species. This mealybug threatens the native cacti in some Caribbean islands and Florida, USA, and is devastating the native columnar cacti in Puerto Rico. Illustrations and taxonomic notes on the type specimens of some other, little known described species of Anagyrus from Argentina and Chile are provided, and a key to females of the 14 species of Anagyrus known from Argentina is given. Anagyrus nigriceps (De Santis) syn. n. is synonymized under A. bellator (De Santis). Lectotypes are designated for Paranusia bifasciata Brèthes, Philoponectroma pectinatum Brèthes, and Protanagyrus aciculatus Blanchard. 

Native ecotypic variation and the role of host identity in the spread of an invasive herbivore, Cactoblastis cactorum.

Environmental niche models (ENMs) have gained enormous popularity as tools to investigate potential changes in species distributions resulting from climate change and species introductions. Despite recognition that species interactions can influence the dynamics of invasion spread, most implementations of ENMs focus on abiotic factors as the sole predictors of potential range limits. Implicit in this approach is the assumption that biotic interactions are relatively unimportant, either because of scaling issues, or because fundamental and realized niches are equivalent in a species' native range. When species are introduced into exotic landscapes, changes in biotic interactions relative to the native range can lead to occupation of different regions of niche space and apparent shifts in physiological tolerances. We use an escaped biological control organism, Cactoblastis cactorum (Berg.), to assess the role of the environmental envelope as compared with patterns of host-herbivore associations based on collections made in the native range. Because all nonnative populations are derived from a single C. cactorum ecotype, we hypothesize that biotic interactions associated with this ecotype are driving the species' invasion dynamics. Environmental niche models constructed from known native populations perform poorly in predicting nonnative distributions of this species, except where there is an overlap in niche space. In contrast, genetic isolation in the native range is concordant with the observed pattern of host use, and strong host association has been noted in nonnative landscapes. Our results support the hypothesis that the apparent shift in niche space from the native to the exotic ranges results from a shift in biotic interactions, and demonstrate the importance of considering biotic interactions in assessing the risk of future spread for species whose native range is highly constrained by biotic interactions.

Proconiini sharpshooters of Argentina, with notes on its distribution, host plants, and natural enemies.

The American tribe Proconiini (Hemiptera: Cicadellidae: Cicadellinae) is one of the largest groups of xylem-feeding insects and includes the majority of the known vectors of xylem-born phytopathogenic organisms. The significance of the pathogens that this group transmits gives them an important role as pests, mostly for citrus fruit, grapes, and almonds. Knowledge of these Hemiptera in Argentina is insufficient and fragmentary. Thus one of the aims of this paper is to summarize the available information of the Proconiini sharpshooters in Argentina. In addition, 14 species are mentioned for the first time in the country, and new distributional data are given for 18 species. Thirty-four new associations between sharpshooters and host plants are recorded. New records of egg parasitoids are given for Dechacona missionum, Molomea consolida, M. lineiceps, and Tapajosa similis.

Geographic host use variability and host range evolutionary dynamics in the phytophagous insect Apagomerella versicolor (Cerambycidae).

The high diversity of phytophagous insects has been explained by the tendency of the group towards specialization; however, generalism may be advantageous in some environments. The cerambycid Apagomerella versicolor exhibits intraspecific geographical variation in host use. In northern Argentina it is highly specialized on the herb Pluchea sagittalis (Asteraceae), while in central and southern areas it uses seven Asteraceae species. To study host species geographical variation from ecological and evolutionary perspectives, we investigated field host availability and use across a wide latitudinal range, and performed laboratory studies on insect oviposition preference and larval performance and mitochondrial DNA (mtDNA) variation in a phylogeographical framework. Geographic variation in host use was unrelated to host availability but was highly associated with laboratory oviposition preference, larval performance, and mtDNA variation. Genetic studies revealed three geographic races of A. versicolor with gene flow restriction and recent geographic expansion. Trophic generalism and oligophagy within A. versicolor seem to have evolved as adaptations to seasonal and spatial unavailability of the preferred host P. sagittalis in cooler areas of the species' geographic range. No single genotype is successful in all environments; specialization may be advantageous in environments with uniform temporal and spatial host availability, while being a trophic generalist may provide an adaptive advantage in host-constrained environments.

Occurrence of the Tamarix Leafhopper, Opsius stactogalus Fieber (Hemiptera: Cicadellidae), in Argentina.

The paleartic tamarix leafhopper, Opsius stactogalus Fieber (Hemiptera: Cicadellidae), can reduce the growth of tamarisk due to the aggregate feeding imposed by their populations. The species was mentioned for Argentina in Metcalf's catalogue (1967) without locality or region reference, and the contributions on Cicadellidae published by many authors after Metcalf omitted this distributional data. Populations of O. stactogalus on Tamarix sp. were found in 12 sites between 28 degrees 48' to 39 degrees 17' S and 64 degrees 06' to 70 degrees 04' W, located in both the Neotropical and Andean biogeographic regions.