Microbial vectoring capacity by internal- and external-infesting stored product insects after varying dispersal periods between novel food patches: An underestimated risk

Authors: PONCE, MARCO - Kansas State University; MAILLE, JACQUELINE - Kansas State University; JAMES, AVERY - Kansas State University; BRUCE, ALEXANDER - University Of Tennessee; KIM, TANIA - Kansas State University; Scully, Erin; Morrison, William - Rob

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/19/2024
Publication Date: 6/25/2024
Citation: Ponce, M.A., Maille, J.M., James, A., Bruce, A., Kim, T.N., Scully, E.D., Morrison Iii, W.R. 2024. Microbial vectoring capacity by internal- and external-infesting stored product insects after varying dispersal periods between novel food patches: An underestimated risk. Ecology and Evolution. 14(6). Article e11368. https://doi.org/10.1002/ece3.11368.
DOI: https://doi.org/10.1002/ece3.11368

Interpretive Summary: As stored product insects move among postharvest commodities at different locations, they have the potential to pick up and transport microbes. Several of these microbes are pathogenic to human and animals and have the potential to produce mycotoxins, thus, increasing the risk that insect infestations pose. The aim of this study was to determine how insect dispersal time between food patches impacts microbial colonization at new food patches. Using laboratory populations of rice weevil and cigarette beetle, both economically important stored product pest species, increasing dispersal time resulted in multiple-fold reductions in microbial growth in new food patches for cigarette beetle, but not for rice weevil. However, the number of unique microbial species identified in the new food patches decreased with increasing dispersal time for rice weevil, but not for cigarette beetle. Furthermore, when rice weevils were exposed to grain with a high inoculation level of Aspergillus flavus, a fungus commonly found in grain which can produce aflatoxin, increased dispersal time led to reduced microbial growth. Rice weevil had 2.3 fold more microbial growth and 1.4 fold greater species richness in new food patches compared to cigarette beetle. Rice weevils collected from the field resulted in increased microbial growth and increased microbial community diversity compared to those from laboratory populations, which included fungi from 13 genera. A total of 23% and 16% of these fungi were classified as Aspergillus and Penicillium, respectively, several strains of which can have negative consequences on human and animal health. Our data suggest that there is a persistent risk of microbial contamination by both species, which has important food safety implications at food facilities.

Technical Abstract: Understanding the ability of internal- and external-infesting stored product insects to vector microbes is important for estimating the relative risk that insects pose to postharvest commodities as they move between habitat patches and in the landscape. Thus, the aim of the current study was to evaluate and compare the microbial growth in novel food patches at different dispersal periods by different populations of Sitophilus oryzae (e.g., internal-infesting) and Lasioderma serricorne (e.g., external-infesting). Adults of both species collected from laboratory colonies or field-captured populations were either placed immediately in a novel food patch, or given a dispersal period of 24 or 72 h in a sterilized environment before entering a surrogate food patch. Vectored microbes in new food patches were imaged after 3 or 5 d of foraging, and microbial growth was processed using ImageJ, while fungal species were identified through sequencing the ITS4/5 ribosomal subunit. We found increasing dispersal time resulted in multiple-fold reductions in microbial growth surrogate food patches by L. serricorne, but not S. oryzae. This was likely attributable to higher mobility by S. oryzae than L. serricorne. A total of 20 morphospecies were identified from 13 genera among the 59 sequences, with a total of 23% and 16% classified as Aspergillus and Penicillium spp. Our data suggest that there is a persistent risk of microbial contamination by both species, which has important food safety implications at food facilities.Understanding the ability of internal- and external-infesting stored product insects to vector microbes is important for estimating the relative risk that insects pose to postharvest commodities as they move between habitat patches and in the landscape. Thus, the aim of the current study was to evaluate and compare the microbial growth in novel food patches at different dispersal periods by different populations of Sitophilus oryzae (e.g., internal-infesting) and Lasioderma serricorne (e.g., external-infesting). Adults of both species collected from laboratory colonies or field-captured populations were either placed immediately in a novel food patch, or given a dispersal period of 24 or 72 h in a sterilized environment before entering a surrogate food patch. Vectored microbes in new food patches were imaged after 3 or 5 d of foraging, and microbial growth was processed using ImageJ, while fungal species were identified through sequencing the ITS4/5 ribosomal subunit. We found increasing dispersal time resulted in multiple-fold reductions in microbial growth surrogate food patches by L. serricorne, but not S. oryzae. This was likely attributable to higher mobility by S. oryzae than L. serricorne. A total of 20 morphospecies were identified from 13 genera among the 59 sequences, with a total of 23% and 16% classified as Aspergillus and Penicillium spp. Our data suggest that there is a persistent risk of microbial contamination by both species, which has important food safety implications at food facilities.