Phenology of brown marmorated stink bug described using female reproductive development

Authors: NIELSON, ANNE - Rutgers University; FLEISCHER, SHELBY - Pennsylvania State University; HAMILTON, GEORGE - Rutgers University; Hancock, Torri; KRAWCZYK, GREGORZ - Pennsylvania State University; Lee, Jana; OGBURN, EMILY - The Ohio State University; POTE, JOHN - Rutgers University; RAUDENBUSH, AMY - The Ohio State University; RUCKER, ANN - Rutgers University; SAUNDERS, MICHAEL - Pennsylvania State University; SKILLMAN, VICTORIA - Oregon State University; SULLIVAN, JEANNE - Wesleyan University; TIMER, JODY - Pennsylvania State University; WALGENBACH, JAMES - The Ohio State University; WIMAN, NIK - Oregon State University; Leskey, Tracy

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2017
Publication Date: 7/21/2017
Citation: Nielson, A., Fleischer, S., Hamilton, G., Hancock, T., Krawczyk, G., Lee, J.C., Ogburn, E., Pote, J., Raudenbush, A., Rucker, A., Saunders, M., Skillman, V., Sullivan, J., Timer, J., Walgenbach, J., Wiman, N., Leskey, T.C. 2017. Phenology of brown marmorated stink bug described using female reproductive development. Ecology and Evolution. 7(17):6680-6690. https://doi.org/10.1002/ece3.3125.

Interpretive Summary: The seasonal cycles of insects are often estimated by a development model that monitors the egg to adult stages based on time and temperature. We expand a temperature-based model by defining the reproductive period of brown marmorated stink bug (BMSB), an economically important invasive. A five stage ranking system based on ovary development was developed and a significant relationship between ovary rank and body weight was found. Whether a female had mated or not was related to its spermatheca width; the spermatheca is a structure in the female that stores sperm after mating. This ovary ranking method was examined among BMSB over the year across geographic locations. Female stink bugs were collected from Allentown, PA, Biglerville, PA, Bridgeton, NJ, Kearneysville, WV, Asheville, NC and the Willamette Valley, OR from 2006-2008 (Allentown, PA only) and 2012-2014. Results confirm that BMSB no longer carry eggs in the ovary in temperate locations in the fall and that a delay in egg development occurs after females emerge in the spring from their overwintering shelter. Continuous reproduction was observed at all sites. About 12.9 h of daylight in the spring was estimated as needed for BMSB to start reproducing once 10% of females carry eggs. With this 12.9 h daylight estimate, we found differences between locations as to when the parental overwintering generation changes from being non-reproductive to reproductive. This suggests that signals for BMSB to end their inactive period and their rate of egg formation may be influenced by environmental factors and thus differ across its invaded range in the United States.

Technical Abstract: Identification of insect seasonality is frequently estimated through temperature-based degree-day models. We expand on the use of a temperature-based process defining timing of life stages through the incorporation of female reproductive physiology for the invasive pentatomid species Halyomorpha halys. A five stage ranking system based on ovary development was developed and a significant relationship between rank and body mass was found. The mated status of females also corresponded to spermatheca width. This ranking method was applied to describe aspects of H. halys’ seasonality, overwintering biology, and phenology across geographic locations. Female H. halys were collected from Allentown, PA, Biglerville, PA, Bridgeton, NJ, Kearneysville, WV, Asheville, NC and the Willamette Valley, OR from 2006-2008 (Allentown, PA only) and 2012-2014. Results confirm that H. halys enters into reproductive diapause in temperate locations in the fall and that a delay occurs in developmental maturity after diapause termination in the spring. Continuous reproduction was observed at all sites, with a higher number of pre-vitellogenic females at most sites beginning around 600 DD14.17, which matches the DD requirements for F1 female eclosion. A biofix of 12.9h photoperiod to define initiation of reproduction was estimated using the DD accumulation at which 10% of females were vitellogenic in the spring. Applying this biofix, we demonstrated significant differences between locations for the rate at which the parental (overwintering) generation transitions into reproductive status, suggesting that diapause termination cues or the rate of vitellogenesis may be influenced by environmental factors and thus differ across its invaded range in the United States.