Copyedited by: OUP Annals of the Entomological Society of America, XX(X), 2019, 1–11 doi: 10.1093/aesa/saz008 Special Collection Special Collection Downloaded from https://academic.oup.com/aesa/advance-article-abstract/doi/10.1093/aesa/saz008/5372394 by University of New Hampshire Library user on 01 April 2019 Examining the Management of Rare Insects Through the Lens of Biotic Interactions: A Comparative Case Study of Nicrophorus americanus (Coleoptera: Silphidae) and Gryllotalpa major (Orthoptera: Gryllotalpidae) Daniel R. Howard1, and Carrie L. Hall Department of Biological Sciences, University of New Hampshire, 38 Academic Way, Durham, NH 03824 and 1Corresponding author, e-mail: [email protected] Subject Editor: Elsa Youngsteadt Received 28 September 2018; Editorial decision 24 January 2019 Abstract Recovery plans for rare and endangered insects most commonly focus on identifying critical abiotic habitat requirements for focal species, and then using these criteria in developing species management portfolios. Biotic interaction data are rarely available, and when produced are seldom integrated into management plans due to their complexity of interpretation. Here we examine advances in our understanding of biotic factors that regulate behavior and life history in two rare insect species of conservation focus: the carrion-breeding American burying beetle, Nicrophorus americanus (Olivier) and the lek mating Gryllotalpa major (Saussure). Current recovery and conservation plans for both species are heavily weighted by abiotic habitat considerations, despite the likely regulation of populations by critical biotic interactions such as interspecies competition, symbioses, predation, and behavioral variation. Examples presented here support a more cohesive approach to constructing conservation management plans to prioritize the integration of ecological interaction data, and to incentivize related research leading to more effective species recovery outcomes. Key words: Nicrophorus americanus, American burying beetle, Gryllotalpa major, prairie mole cricket, insect conservation Insects play a critical role in ecosystem function, extending their carrion and dung-feeding insect assemblages are known to shift with influence across trophic levels from soils to canopy (Berryman 1986), the successional state of disturbed or regenerating grassland and but many species have exhibited recent perilous declines (Shortall forest patches as a functional response to changing mammal and et al. 2009, Brooks et al. 2012, Baxter-Gilbert et al. 2015, Hallmann bird community assemblages found therein (Dunn 2004). et al. 2017, Lister and Garcia 2018). Due to their important ecological While insect declines are often rightfully attributed to changes functions related to herbivory, pollination services, decomposition, in local and regional abiotic conditions (Bender et al. 1998, nutrient cycling, and soil aeration, insect communities are critical Flockhart et al. 2015, Rodrigues et al. 2016), less is known about in maintaining ecosystem resilience in the face of climate-related how perturbations of biotic relationships, including dependencies, disequilibria and increasing impacts from anthropogenic disturbance relate to population declines and community composition changes (Lavelle et al. 2006, Weisser and Siemann 2008, Rader et al. 2013). (Albrecht et al. 2007, Styrsky and Eubanks 2007, Merrill et al. 2008, Insect populations both regulate and respond to changes in ecosystem Rasmann et al. 2014), especially in insect species of conservation structure (Matson and Addy 1975), with many species occupying interest. Many insect species have evolved intricate symbioses that specific and sometimes ephemeral positions in successional gradients render them potentially susceptible to decline if their symbiont (Majer et al. 2007). The biodiversity and abundance of herbivorous populations suffer (Kikuchi et al. 2016); moreover, changes insects is tied closely to ecosystem successional state due to post- in the dynamics of these symbiont relationships can produce disturbance botanical forage availability (Heliövaara and Vaisanen community-wide spillover effects. For example, Sanders et al. 1984, Niemelä et al. 1996), and insects occupying higher trophic (2016) manipulated the bacterial gut symbionts in one of three levels are often highly sensitive to the secondary and tertiary biotic aphid species in an experimental community, which conferred some interactions that constrain or facilitate food source availability (Price resistance to its parasitoid and allowed the treatment aphid species et al. 1980, Holloway et al. 1992, Dodd et al. 2012). For example, to increase in density. This led to a change in the relative densities of © The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America. 1 All rights reserved. For permissions, please e-mail: [email protected]. Copyedited by: OUP 2 Annals of the Entomological Society of America, 2019, Vol. XX, No. XX the three aphid species, which in turn led to the ultimate extinction Nebraska, with disjunct reintroduced populations occurring in of the other aphids’ specialist parasitoids. As another example, the Kansas, Missouri, and Rhode Island; unsuccessful reintroductions larvae of many lycaenid butterflies are tended by mutualistic ants have occurred in Ohio. Members of the Nicrophorine genus of Downloaded from https://academic.oup.com/aesa/advance-article-abstract/doi/10.1093/aesa/saz008/5372394 by University of New Hampshire Library user on 01 April 2019 that putatively protect them from natural predators and in return Silphid burying beetles, American burying beetles and conspecifics receive honey-dew secretions that the larvae produce to incentivize are notable for a reproductive life history that includes locating and the symbiosis (Elmes et al. 1998, Saarinen et al. 2006). Declines in burying small vertebrate carcasses that are subsequently used as a native ant populations (Porter and Savignano 1990), in combination feeding resource for their carefully attended offspring (Pukowski with other abiotic factors, could then easily lead to a recovery 1933, Scott 1998). As such their reproductive behavior is thought tipping point for some of the more at-risk lycaenids (Trager et al. to facilitate soil nutrient cycling, but few studies have examined this 2009). Perhaps equally problematic is that when these types of empirically. Most burying beetles provide bi-parental care (Scott biotic interaction data are available for a species, their difficulty in 1998) and produce antimicrobial oral and anal secretions that interpretation or applicability often results in their exclusion from preserve the carcass resource from soil microbe degradation for the species recovery and management portfolios. week or so that offspring are actively feeding during development Here we examine evidence that biotic community interactions (Rozen at al 2008, Hall et al. 2011). While the causes of the decline influence insect behavior, ecology, and evolution in two species of of the species remain under investigation and debated, Sikes and conservation concern. With these data in mind, we aim to promote a Raithel (2002) identified several factors that may have led to the discussion centered on how our understanding of biotic interactions rapid decline of the species including 1) pesticide use, 2) artificial can inform stakeholders and have applied usefulness. We then offer lighting, 3) pathogens, 4) habitat alteration, 5) increased competition recommendations for incorporating such research into species for breeding resources, and 6) the decline of appropriately sized recovery and management plans. One species has been formally faunal assemblages that provide breeding carcasses for successful protected under the U.S. Endangered Species Act since the late recruitment. While the American burying beetle is considered 1980s, and is currently embroiled in politically inspired delisting a habitat generalist, evidence is building that some of its biotic efforts, while the other was proposed for listing as a threatened interactions may be more specialized. species in 1990 but did not receive formal protection at the federal Much of the research on the American burying beetle has level. Its conservation plight has drawn little attention. While the focused on conducting biological field surveys and understanding foci of research on these two exemplars have diverged dramatically what constitutes suitable habitat for the species. Anderson (1982) over the past three decades, it is increasingly evident that identifying hypothesized that the decline of the species might relate to the loss of important biotic interactions represents a critical dimension in their primary forest that once covered eastern North America. Creighton conservation. et al. (2009) found that clearcutting forestry practices likely caused local extirpation of American burying beetles at a research site in southeastern Oklahoma, while in Nebraska, American burying beetle Case Studies populations in grasslands declined across a region where an eastern American Burying Beetle (Nicrophorus americanus red cedar forest became established (Walker and Hoback 2007). Olivier) Efforts at American burying beetle habitat modeling (Crawford The American burying beetle (Fig. 1) is a federally endangered and Hoagland 2010), refining trapping and marking designs (Butler necrophilous insect species whose range once extended across 35 et al. 2012, Leasure