Many insects are associated with heritable symbionts that mediate ecological interactions, including host protection against natural enemies. The cowpea aphid, Aphis craccivora, is a polyphagous pest that harbors Hamiltonella defensa, which defends against parasitic wasps. Despite this protective benefit, this symbiont occurs only at intermediate frequencies in field populations. To identify factors constraining H. defensa invasion in Ap. craccivora, we estimated symbiont transmission rates, performed fitness assays, and measured infection dynamics in population cages to evaluate effects of infection. Similar to results with the pea aphid, Acyrthosiphon pisum, we found no consistent costs to infection using component fitness assays, but we did identify clear costs to infection in population cages when no enemies were present. Maternal transmission rates of H. defensa in Ap. craccivora were high (ca. 99%) but not perfect. Transmission failures and infection costs likely limit the spread of protective H. defensa in Ap. craccivora. We also characterized several parameters of H. defensa infection potentially relevant to the protective phenotype. We confirmed the presence of H. defensa in aphid hemolymph, where it potentially interacts with endoparasites, and performed real-time quantitative PCR (qPCR) to estimate symbiont and phage abundance during aphid development. We also examined strain variation of H. defensa and its bacteriophage at multiple loci, and despite our lines being collected in different regions of North America, they were infected with a nearly identical strains of H. defensa and APSE4 phage. The limited strain diversity observed for these defensive elements may result in relatively static protection profile for this defensive symbiosis.
Insect parasitoids and herbivores must balance the risk of egg limitation and time limitation in order to maximize reproductive success. Egg and time limitation are mediated by oviposition and egg maturation rates as well as by starvation risk and other determinants of adult lifespan. Here, we assessed egg load and nutritional state in the soybean aphid parasitoid Binodoxys communis under field conditions to estimate its risk of becoming either egg- or time-limited. The majority of female B. communis showed no signs of egg limitation. Experimental field manipulations of B. communis females suggested that an average of 4-8 eggs were matured per hour over the course of a day. Regardless, egg loads remained constant over the course of the day at approximately 80 eggs, suggesting that egg maturation compensates for oviposition. This is the first case of such "egg load buffering" documented for a parasitoid in the field. Despite this buffering, egg loads dropped slightly with increasing host (aphid) density. This suggests that egg limitation could occur at very high host densities as experienced in outbreak years in some locations in the Midwestern USA. Biochemical analyses of sugar profiles showed that parasitoids fed upon sugar in the field at a remarkably high rate. Time limitation through starvation thus seems to be very low and aphid honeydew is most likely a source of dietary sugar for these parasitoids. This latter supposition is supported by the fact that body sugar levels increase with host (aphid) density. Together, these results suggest that fecundity of B. communis benefits from both dynamic egg maturation strategies and sugar-feeding.
Greenhouse gas emissions associated with pesticide applications against invasive species constitute an environmental cost of species invasions that has remained largely unrecognized. Here we calculate greenhouse gas emissions associated with the invasion of an agricultural pest from Asia to North America. The soybean aphid, Aphis glycines, was first discovered in North America in 2000, and has led to a substantial increase in insecticide use in soybeans. We estimate that the manufacture, transport, and application of insecticides against soybean aphid results in approximately 10.6 kg of carbon dioxide (CO2) equivalent greenhouse gasses being emitted per hectare of soybeans treated. Given the acreage sprayed, this has led to annual emissions of between 6 and 40 million kg of CO2 equivalent greenhouse gasses in the United States since the invasion of soybean aphid, depending on pest population size. Emissions would be higher were it not for the development of a threshold aphid density below which farmers are advised not to spray. Without a threshold, farmers tend to spray preemptively and the threshold allows farmers to take advantage of naturally occurring biological control of the soybean aphid, which can be substantial. We find that adoption of the soybean aphid economic threshold can lead to emission reductions of approximately 300 million kg of CO2 equivalent greenhouse gases per year in the United States. Previous studies have documented that biological control agents such as lady beetles are capable of suppressing aphid densities below this threshold in over half of the soybean acreage in the U.S. Given the acreages involved this suggests that biological control results in annual emission reductions of over 200 million kg of CO2 equivalents. These analyses show how interactions between invasive species and organisms that suppress them can interact to affect greenhouse gas emissions.
Aphids commonly harbor bacterial facultative symbionts that have a variety of effects upon their aphid hosts, including defense against hymenopteran parasitoids and fungal pathogens. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is infected with the symbiont Arsenophonus sp., which has an unknown role in its aphid host. Our research goals were to document the infection frequency and diversity of the symbiont in field-collected soybean aphids, and to determine whether Arsenophonus is defending soybean aphid against natural enemies. We performed diagnostic PCR and sequenced four Arsenophonus genes in soybean aphids from their native and introduced range to estimate infection frequency and genetic diversity, and found that Arsenophonus infection is highly prevalent and genetically uniform. To evaluate the defensive role of Arsenophonus, we cured two aphid genotypes of their natural Arsenophonus infection through ampicillin microinjection, resulting in infected and uninfected isolines within the same genetic background. These isolines were subjected to parasitoid assays using a recently introduced biological control agent, Binodoxys communis [Braconidae], a naturally recruited parasitoid, Aphelinus certus [Aphelinidae], and a commercially available biological control agent, Aphidius colemani [Braconidae]. We also assayed the effect of the common aphid fungal pathogen, Pandora neoaphidis (Remaudiere & Hennebert) Humber (Entomophthorales: Entomophthoraceae), on the same aphid isolines. We did not find differences in successful parasitism for any of the parasitoid species, nor did we find differences in P. neoaphidis infection between our treatments. Our conclusion is that Arsenophonus does not defend its soybean aphid host against these major parasitoid and fungal natural enemies.
Intraguild predation (IGP) occurs when one predator species attacks another predator species with which it competes for a shared prey species. Despite the apparent omnipresence of intraguild interactions in natural and managed ecosystems, very few studies have quantified rates of IGP in various taxa under field conditions. We used molecular analyses of gut contents to assess the nature and incidence of IGP among four species of coccinellid predators in soybean fields. Over half of the 368 predator individuals collected in soybean contained the DNA of other coccinellid species indicating that IGP was very common at our field site. Furthermore, 13.2% of the sampled individuals contained two and even three other coccinellid species in their gut. The interaction was reciprocal, as each of the four coccinellid species has the capacity to feed on the others. To our knowledge, this study represents the most convincing field evidence of a high prevalence of IGP among predatory arthropods. The finding has important implications for conservation biology and biological control.
The soybean aphid, Aphis glycines Matsumura, has become the single most important arthropod pest of soybeans in North America. Native to Asia, this invasive species was first discovered in North America in July 2000 and has rapidly spread throughout the northcentral United States, much of southeastern Canada, and the northeastern United States. In response, important elements of the ecology of the soybean aphid in North America have been elucidated, with economic thresholds, sampling plans, and chemical control recommendations widely adopted. Aphid-resistant soybean varieties were available to growers in 2010. The preexisting community of aphid natural enemies has been highly effective in suppressing aphid populations in many situations, and classical biological control efforts have focused on the addition of parasitoids of Asian origin. The keys to sustainable management of this pest include understanding linkages between the soybean aphid and other introduced and native species in a landscape context along with continued development of aphid-resistant varieties.
A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (mummies) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.
In the north central United States, populations of the exotic soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are highly variable across space, complicating effective aphid management. In this study we examined relationships of plant nutrients, landscape structure, and natural enemies with soybean aphid abundance across Iowa, Michigan, Minnesota, and Wisconsin, representing the range of conditions where soybean aphid outbreaks have occurred since its introduction. We sampled soybean aphid and its natural enemies, quantified vegetation land cover and measured soybean nutrients (potassium [K] and nitrogen [N]) in 26 soybean sites in 2005 and 2006. Multiple regression models found that aphid abundance was negatively associated with leaf K content in 2005, whereas it was negatively associated with habitat diversity (Simpsons index) and positively associated with leaf N content in 2006. These variables accounted for 25 and 27% of aphid variability in 2005 and 2006, respectively, suggesting that other sources of variability are also important. In addition, K content of soybean plants decreased with increasing prevalence of corn-soybean cropland in 2005, suggesting that landscapes that have a high intensification of agriculture (as indexed by increasing corn and soybean) are more likely to have higher aphid numbers. Soybean aphid natural enemies, 26 species of predators and parasitoids, was positively related to aphid abundance; however, enemy-to-aphid abundance ratios were inversely related to aphid density, suggesting that soybean aphids are able to escape control by resident natural enemies. Overall, soybean aphid abundance was most associated with soybean leaf chemistry and landscape heterogeneity. Agronomic options that can ameliorate K deficiency and maintaining heterogeneity in the landscape may reduce aphid risk.
The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is native to eastern Asia and was accidentally introduced into North America in 2000. Within a few years, it was found throughout the U.S. and Canadian soybean-growing regions. The spread of A. glycines in North America is partly ascribed to its great flight capacity. We conducted direct measurements of flight performance of winged A. glycines adults and correlated this to their subsequent longevity and fecundity to determine whether there are trade-offs between flight and fecundity. We also estimated fecundity and development time of the offspring of females that had flown varying distances to examine potential maternal effects linked to flight. The experiment was conducted using a specifically designed aphid flight mill system in which winged aphids were tethered by their abdomens and flight duration, distance and speed were quantified. Fecundity, longevity and reproductive periods of 12-h-old A. glycines alates that had engaged in > 0.5 km long flights were significantly lower than those of < 0.5-km individuals. The offspring of alates with flight experiences of > 1.5 km also had lower fecundity than those produced by individuals that had engaged in flights < 1.5 km. Our results are therefore consistent both with direct trade-offs between flight and fecundity and a trade-off between flight and fecundity via maternal effects.
The term idiobiont refers to those parasitoid species that permanently paralyse their hosts during parasitism, causing the cessation of host growth and development. This is in contrast to koinobiont parasitoids, which allow their hosts to continue developing after being parasitized. While no koinobiont species induce permanent paralysis in their hosts, a minority of koinobionts induce a temporary paralysis that does not interfere with overall host growth and development. We characterized transient paralysis induction in two koinobiont aphid parasitoids in the genus Binodoxys (Hymenoptera: Aphidiinae). Both Binodoxys species induced transient paralysis in Aphis glycines, with paralysis time ranging between 4.5 and 8 min (depending upon parasitoid species and host instar). In a separate experiment, B. communis was capable of inducing transient paralysis in nine aphid species. We addressed two hypotheses potentially explaining the adaptive value of temporary host paralysis in experiments using A. nerii, which is readily accepted but engages in strong defensive behaviour. The first hypothesis is that paralysis increases oviposition success by interfering with host defences and the second is that it aids in the avoidance of self-superparasitism. Paralysed aphids were more likely to be rejected by B. communis than were aphids that had never been stung or that had recovered from paralysis. This result supports the avoidance-of-self-superparasitism hypothesis and is inconsistent with the hypothesis that transient paralysis increases oviposition success of B. communis.
The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.
Natural enemies may go through genetic bottlenecks during the process of biological control introductions. Such bottlenecks are expected to be particularly detrimental in parasitoid Hymenoptera that exhibit complementary sex determination (CSD). CSD is associated with a severe form of inbreeding depression because homozygosity at one or multiple sex loci leads to the production of diploid males that are typically unviable or sterile. We observed that diploid males occur at a relatively high rate (8-13% of diploid adults) in a field population of Cotesia rubecula in Minnesota, USA, where this parasitoid was introduced for biological control of the cabbage white Pieris rapae. However, our laboratory crosses suggest two-locus CSD in a native Dutch population of C. rubecula and moderately high diploid males survival (approximately 70%), a scenario expected to produce low proportions of diploid males. We also show that courtship behavior of diploid males is similar to that of haploid males, but females mated to diploid males produce only very few daughters that are triploid. We use our laboratory data to estimate sex allele diversity in the field population of C. rubecula and discuss the possibility of a sex determination meltdown from two-locus CSD to effective single-locus CSD during or after introduction.
The host range of insect parasitoids and herbivores is influenced by both preference-related traits which mediate host choice behaviour, and performance-related traits which mediate the physiological suitability of the consumer-resource interaction. In a previous study, we characterised the influence of preference- and performance-related traits on the host range of the aphid parasitoid Binodoxys communis (Hymenoptera: Braconidae) and herein we build upon those data sets by mapping a series of these traits onto the phylogeny of the (aphid) host species. We found a strong effect of host phylogeny on overall parasitoid reproduction on the 20 host species tested, but no effect of the phylogeny of host plants of the aphids. We found an effect of aphid phylogeny on host acceptance and sting rates (related to preference) from behavioural observations and for pupal survivorship (related to performance), showing that both classes of traits show phylogenetic conservatism with respect to host species.
An important assumption in insect parasitoid life-history theory is that, within parasitoid complexes (species assemblages associated with particular hosts), members attacking young host stages are more fecund than members targeting older ones. This hypothesis reflects the general trajectory of host survivorship curves: as a host cohort ages, availability to female parasitoids declines, as can the risk that the host - and the parasitoid offspring it carries - succumbs to extrinsic mortality. However, the analyses that provided empirical support for the hypothesis did not control for phylogeny. Using the original datasets, we use phylogenetically corrected analyses to test whether the results of the seminal study are upheld. Although we show those findings to be robust, the decline in fecundity could be a sampling artefact. We conclude that it would be unwise to assume the paradigm to be generally representative of natural parasitoid complexes.
Facultative bacterial endosymbionts can play an important role in the evolutionary trajectory of their hosts. Aphids (Hemiptera: Aphididae) are infected with a wide variety of facultative endosymbionts that can confer ecologically relevant traits, which in turn may drive microevolutionary processes in a dynamic selective environment. However, relatively little is known about how symbiont diversity is structured in most aphid species. Here, we investigate facultative symbiont species richness and prevalence among worldwide populations of the cowpea aphid, Aphis craccivora Koch. We surveyed 44 populations of A. craccivora, and detected 11 strains of facultative symbiotic bacteria, representing six genera. There were two significant associations between facultative symbiont and aphid food plant: the symbiont Arsenophonus was found at high prevalence in A. craccivora populations collected from Robinia sp. (locust), whereas the symbiont Hamiltonella was almost exclusively found in A. craccivora populations from Medicago sativa (alfalfa). Aphids collected from these two food plants also had divergent mitochondrial haplotypes, potentially indicating the formation of specialized aphid lineages associated with food plant (host-associated differentiation). The role of facultative symbionts in this process remains to be determined. Overall, observed facultative symbiont prevalence in A. craccivora was lower than that of some other well-studied aphids (e.g., Aphis fabae and Acyrthosiphon pisum), possibly as a consequence of A. craccivoras almost purely parthenogenetic life history. Finally, most (70 %) of the surveyed populations were polymorphic for facultative symbiont infection, indicating that even when symbiont prevalence is relatively low, symbiont-associated phenotypic variation may allow population-level evolutionary responses to local selection.
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