How the seed coat affects the mother’s oviposition preference and larval performance in the bean beetle (Acanthoscelides obtectus, Coleoptera: Chrysomelidae, Bruchinae) in leguminous species

Abstract

Background The host specificity and host range of the dry bean beetle, Acanthoscelides obtectus (Coleoptera: Chrysomelidae, Bruchinae), a seed predator of beans, is poorly known. In addition, the female oviposition preference and larval performance relationship is complicated by the respective importance of seed coat and cotyledon, because, paradoxically, females lay eggs on the basis of stimuli of the seed coat alone, without directly being able to assess the quality of the cotyledon’s suitability for larval development. Conversely, the thickness of seed coat may prevent first instar larvae from entering the seeds, even if cotyledons are suitable for development. Methods The seeds of 62 leguminous species and 75 cultivars and accessions occurring in Hungary were evaluated for preference-performance relations. The preference of female bean beetles for seeds was measured in no-choice egg-laying tests. The ability of first instar larvae to overcome the seed coat as a physical barrier was tested with intact seed coat, while pre-drilled seed coats allowed the larvae to assess the suitability of cotyledon for development. The number of emerging adults was recorded. The thickness of seed coats and the weight of seeds were measured. Nonparametric tests and logistic regression were used for the statistical analyses of data and effect sizes were also calculated. Results Seeds of 18 leguminous species (35% of them Lathyrus) supported larval development to adults if the seed coat was pre-drilled; however, only nine leguminous species supported development to adults if the seed coat was intact. Seed coat thickness beyond a critical threshold of 0.1 mm strongly influenced survival of first instar larvae. There was no overall positive correlation between oviposition preference and larval performance, except for 16 so-called acceptable non-hosts (Kendall’s τ = 0.3088). A. obtectus females also showed an ovipositional hierarchy of legume species even in no-choice tests. Conclusions The results suggest that whereas the use of some acceptable non-host species by the A. obtectus is possible in seed stores, the same is unlikely under outdoor conditions, where the recognition of a diverse set of seed pod-related compounds would be necessary to induce egg-laying.

A semiochemical view of the ecology of the seed beetle Acanthoscelides obtectus Say (Coleoptera: Chrysomelidae, Bruchinae)

“…Oviposition occurs when acceptability of a substrate exceeds the individual motivational threshold determined by genetic and physiological status, and the different acceptability levels create a rank order. Variation in egg‐laying is also modulated by factors such as egg load (Szentesi, 2021 ) and is modified by learning (Á. Szentesi, unpublished).…”

“…This situation only occurs in granaries, where several legume species may be stored together, whereas the choices the larvae face in the field are restricted to differences in seed size and quality within a pod of a single host species. The seed testa of the primary host, P. vulgaris , presents an effective physical barrier, with more than a quarter of L1 larvae dying outside the beans; however, if the seed coat has pre‐drilled artificial entry holes, larval mortality is significantly lower (Szentesi, 2021 ). This is in part due to seed coat thickness (host and acceptable non‐host seeds have thinner testa; Szentesi, 2021 ), toughness (water content; Thiéry, 1984 ), but also chemical composition.…”

“…The seed testa of the primary host, P. vulgaris , presents an effective physical barrier, with more than a quarter of L1 larvae dying outside the beans; however, if the seed coat has pre‐drilled artificial entry holes, larval mortality is significantly lower (Szentesi, 2021 ). This is in part due to seed coat thickness (host and acceptable non‐host seeds have thinner testa; Szentesi, 2021 ), toughness (water content; Thiéry, 1984 ), but also chemical composition. Bean seed surface chemistry stimulates larval drilling into the seed by providing host recognition cues (Thiéry et al, 1994 ), but the seed coat material itself is spat out by chewing larvae because of the presence of toxic substances.…”

“…Szentesi (2021) postulates that the seed coat does not completely inhibit the detection of chemical cues from the seed cotyledon, thereby enabling egg-laying A. obtectus females to assess substrate suitability for larval survival by integrating oviposition-stimulating positive and larval development-impeding negative chemical stimuli. Such infochemicals might include volatile organic compounds(Khelfane-Goucem et al, 2014).…”

Assessment of Sex-Specific Toxicity and Physiological Responses to Thymol in a Common Bean Pest Acanthoscelides obtectus Say

“…Beside the primary host common bean Phaseolus vulgaris L. it can also feed on other crops belonging to 11 different genera ( Johnson, 1981 ; Labeyrie, 1990 ). In a study of Szentesi (2021) 18 legume species are shown to be acceptable, and nine of them support complete development to adults even if seed coat was intact. A. obtectus originates from South America but widened its areal of distribution to Europe, North America, Australia and Africa due to human-mediated migrations and tolerance to broad range of environmental conditions ( Alvarez et al, 2005 ).…”