Long-term community dynamics of aphidophagous coccinellids in response

1. Long-term community dynamics of aphidophagous coccinellids in response to repeated invasion in a diverse agricultural landscape Christie Bahlai*,  Manuel Colunga-Garcia,  Stuart Gage, and Douglas Landis Kellogg Biological Station, Department of Entomology, Michigan State University *contact: Center for Integrated Plant Systems Laboratory, Room 204, 578 Wilson Rd., East Lansing, MI, USA 48824 cbahlai@msu.edu Background Fig. 5. Captures of three key coccinellid species by habitat changed relative to each other. Harmonia axyridis is an exotic species that reached very high densities in 2001-2006, coinciding with the establishment of soybean aphid, an invasive crop pest. During this time, habitat use patterns of Coccinella trifasciata and Adalia bipunctata changed (arrows): these species moved out of cultivated habitat and were only recovered in unmanaged forest sites. Aphidophagous ladybeetles (Coleoptera: Coccinellidae) are important providers of herbivore suppression in aqgroecosystems.1 In the last 30 years, the invasion of exotic coccinellid species coupled with observed declines in native species has led to renewed interest in the community dynamics and ecosystem function of this guild (Fig 1).2 Several hypotheses have been proposed to describe the mechanism of invasion coupled with native species declines (i.e. vacant niche exploitation, competitive displacement and habitat compression, intraguild predation),3,4and the relationship of this decline to biodiversity and herbivore suppression. We examined the response of coccinellid communities at the Kellogg Biological Station Long-Term Ecological Research (KBS-LTER) site to invasion. Since 1985, the resident coccinellid community has been invaded by four species (Fig. 2) and is increasingly dominated by non-native species (Fig. 3). Fig. 3. Exotic species increasingly dominate captures of coccinellids at KBS. Only one native coccinellid species continues to appear in great numbers at KBS: Coleomegilla maculata reaches relatively high numbers in years when maize is planted at the site. This species is omnivorous and is known to feed on maize pollen. Fig. 1. Aggregation of Harmonia axyridis, an exotic species. This species has become very abundant in central North America since 1999. Photo by Morgan Jackson, http://www.biodiversityinfocus.com/ Fig. 7. Average herbivore suppression potential of coccinellids captured on traps in three habitats remained roughly constant over the course of the study, but became more variable during 2001-2006, coinciding with extremely high numbers of Harmonia axyridis. Gaussian smoothing lines are used to visualize trends. Fig. 6. Average Shannon index of captured coccinellids, per plot, per week, in three habitats increased over time, but was decreased in 2001-2006, coinciding with extremely high numbers of Harmonia axyridis. Gaussian smoothing lines are used to visualize trends. 2012 1989 Fig. 4. Coccinellid captures vary dramatically from year to year. Several species appear to have characteristic boom-bust population cycles; others respond numerically to sporadic pest outbreaks. Fig. 2. Multiple ladybeetle invasions in southern Michigan. Four exotic species have invaded the coccinellid community at KBS. In 1985 Coccinella septempunctata became established, followed by Harmonia axyridis in 1993, Hippodamia variegata in 1997, and Propylea quatuordecimpunctata in 2007 Discussion • We found that competitive exclusion from agricultural habitats by invading species is likely playing a major role in the decline of several formerly-dominant native species. Several native species (Adalia bipunctata and Coccinella trifasciata) persist at low numbers in semi-natural forest habitats embedded in agricultural landscapes but are no longer observed in cultivated habitat (Fig 5). This finding provides support to Evans’3 habitat compression hypothesis, a consequence of competitive exclusion in which native coccinellid species ‘retreat’ to ancestral habitats when resources in these habitats become depleted by exotic species that have co-evolved with cultivated habitats. • We found that the herbivore suppression potential of the ladybeetle community remained roughly constant since the initiation of the study (Fig. 5), and Shannon diversity of the community increased slightly (Fig 6). These results suggest that, despite invasions, the coccinellid community is still capable of providing the same level of pest suppression ecosystem service. However, declines in biodiversity are likely to occur if semi-natural habitats within the agricultural matrix are lost. • Future work will explore niche interactions for species within the community and examine population cycling of individual species in the context of resource availability • References • 1. Gordon, R. D. 1985. The Coccinellidae (Coleoptera) of America North of Mexico. Journal of the New York Entomological Society 93: i-912. • 2. Harmon, J. P., et al. 2007. The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation 11: 85-94. • 3. Evans, E.W. 2004. Habitat displacement of North American ladybirds by an introduced species. Ecology 85: 637-647. • 4. Snyder, W.E., Coccinellids in diverse communities: Which niche fits? Biological Control, 2009. 51: 323-335 • 5. Bahlai, C.A., R.M. Weiss, and R.H. Hallett. 2013. A mechanistic model for a tritrophic interaction involving soybean aphid, its host plants, and multiple natural enemies. Ecological Modelling 254: 54-70 Approach Each growing season since 1989, coccinellid populations have been monitored weekly in a variety of habitats at the KBS-LTER in southwestern Michigan (Fig. 4). Coccinellid captures on yellow sticky traps were recorded in annual crops of maize, soybean, wheat (in three year rotation), perennial crops of alfalfa, poplar, and early successional vegetation and in unmanaged forest plots including coniferous, deciduous and successional forest. Previous work has suggested that communities of natural enemies vary along a management intensity gradient, so we grouped plots into three habitat types by management/disturbance intensity: annual crops, perennial crops, and forests (Fig. 5). We examined these data in the context of several hypotheses regarding invasions and mechanisms of native species decline in coccinellids,3,4and evaluated the diversity and herbivore suppression potential of the community from the time the study was initiated to present. We examined the time-series captures of each coccinellid species by habitat type to identify changes in habitat use (Fig. 6). Shannon diversity was computed for each plot by year (Fig. 7). Herbivore suppression potential was computed using estimates of voracity for a given species to weight their abundance , and then summed across all species (Fig 8).5 Fig. 4. Coccinellid communities vary significantly between habitats (ANOSIM, Global R =0.295, p=0.001). Non-metric multidimensional scaling of coccinellid captures by habitat type with distances in figure represent Bray –Curtis similarity of fourth root transformed coccinellid captures. The Kellogg Biological Station Long-Term Ecological Research site is funded by the National Science Foundation