Examining the Management of Rare Insects Through the Lens of Biotic

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

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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 et al. 2012, Butler et al. 2013, Hall et al. 2015), U.S. states and three Canadian Provinces (Anderson 1982) but is identifying new county/regional records (Backlund et al. 2008, now restricted to only six states. Due to the rapid range contraction Jurzenski et al. 2011) and delineating conservation priority areas for this species, American burying beetles were listed as federally (Jurzenski et al. 2014), along with identifying abiotic factors that endangered in 1989 pursuant to the U.S. Endangered Species constrain American burying beetle populations (Schnell et al. 2008) Act (USFWS 1989, Raithel 1991). Self-sustaining populations of have occupied the attention of researchers. Only one small note in a the American burying beetle occur in Oklahoma, Arkansas, and comparatively low-impact journal has focused on a biotic interaction in American burying beetle s (Jurzenski and Hoback 2011); in this case, an isolated observation of a single predation event. Recent work with closely related Nicrophorus congeners hints that American burying beetles have likely evolved a complex suite of biotic interactions that may influence populations as critically as any of the aforementioned abiotic drivers (Engel et al. 2015, Duarte et al. 2017, Nehring et al. 2017, Wang and Rozen 2018, Woelber et al. 2018). Preliminary findings from two such ongoing studies are highlighted below, along with data related to the indirect effects of grazing on American burying beetle habitat utilization.

Niche Competition Species composition coupled to local environmental factors can influence the magnitude and direction of interspecies interactions in complex ways, including dictating the temporal and spatial structure of niche breadth (Pianka 1974, 1981; Sale 1974). In most cases, the predicted maximal niche overlap between putatively competing species should vary inversely with the Fig. 1. A male–female pair of American burying beetles (Nicrophorus intensity of competition, and thus given their similar use of americanus) beginning the process of carcass preparation and burial. vertebrate carcasses for reproduction, intra- and interspecies Copyedited by: OUP

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competition is the presumptive dynamic at play structuring niche Through a series of field abundance surveys over 12 yr at a study breadth in American burying beetles. This struggle to secure niche site in Osage County, OK (Tallgrass Prairie Preserve—36°50′N, space in the context of competition with other necrophilous insect 96°25′W), and through laboratory experiments with automated 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 species is thought to have implications for American burying animal locomotion monitors that track daily movement patterns, beetle population viability (Lomolino et al. 1995, Scott 1998), American burying beetle spatial and temporal niche interactions and is likely influenced by local landscape structure (Conley et al. were examined and described (Keller et al. unpublished data; 2015). While a portion of the presumptive niche breadth of the Figs. 2 and 3). Findings here reveal that American burying beetle American burying beetle is thought to be associated in part with spatial niche exhibits interannual variability related to both local carcass size (Trumbo 1990, Smith and Heese 1995), temporal Nicrophorine competitor density and landscape-level disturbance and spatial niche is presumed to exhibit adaptive plasticity and is patterns. Space use overlap between the American burying beetle coupled more closely to interspecies competitive composition. In population and that of four common congeners rarely exceeds 30% turn, dynamic interspecies competition is often parameterized by of the endangered species core range. Significant spatial segregation spatial factors related to habitat preference, density, and dispersal occurred between American burying beetles and two species patterns (Loreau 1989, Valeix et al. 2007, Castro‐ Arellano (N. marginatus and N. tomentosus; Fig. 2). The temporal niche of et al. 2010). In both grassland and forested ecosystems and their American burying beetles was similar to the forest-dwelling species ecotones, American burying beetle temporal and spatial niche N. orbicollis but did not strictly segregate from any of the tested could potentially overlap with several Nicrophorine congeners sympatric congeners. Interestingly, the American burying beetle including Nicrophorus orbicollis, N. tomentosus, N. pustulatus, has been described as nocturnal (Scott 1998), but experimental N. carolinus, N. sayi, and N. marginatus; the extent of spatial data revealed the species was most active for the first few hours and temporal niche interactions between these species has been after dawn (Fig. 3). These findings support a complex model of poorly understood. interspecies interactions in which space, time and carcass resource

Fig. 2. Kernel density estimate of American burying beetle abundance at The Nature Conservancy’s Tallgrass Prairie Preserve in Osage County, OK. American burying beetle spatial distribution across the landscape exhibits interannual variability and is highly heterogeneous, with the core range of the species exhibiting low spatial overlap with five congeners with which it is thought to compete. For example, in 2017 the core range overlap withN. marginatus (cross-hatched) and N. tomentosus (stippled) is limited to a small portion of the American burying beetles' highest densities along the eastern-most edge of the study area, where all three species’ core ranges overlap. Copyedited by: OUP

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between American burying beetles and the other comparator species are known to produce antifungal peptides, and likely play a role in reducing microbial degradation of the carcass used in reproduction. 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 While these preliminary results are tantalizing and build upon the growing literature on Nicrophorine-microbial interactions, additional work is needed to understand whether differences in the microbiome of the American burying beetle relates to its recent decline, how regional differences in the species’ microbiome might impact the success of reintroduction efforts, or how experimental manipulation of microbiomes might represent a viable approach to increase reproductive success as part of the species recovery portfolio.

Large Herbivore Grazing and American Burying Beetle Habitat Preferences In parts of their remaining range, American burying beetles are found Fig. 3. Mean daily temporal pattern for American burying beetles measured using an automated locomotor activity monitor. Previously thought to be in some of their highest densities in grassland ecosystems. Particularly strictly nocturnal, N. americanus exhibits two peak activity periods: the first abundant in regions of tallgrass prairie in Oklahoma (Flint Hills) occurs over 4 h on either side of light onset (0600 hours), while the second and Nebraska (Sand Hills), traditional range management practices smaller activity peak occurs at light offset (2000 hours). This temporal pattern influence the landscape in these remaining tallgrass ecoregions. does not significantly segregate from any of the five sympatric Nicrophorine Cattle grazing and/or mowing are the primary economic and congeners tested. ecological drivers, with spring season prescribed burning in the Flint Hills ecoregion viewed as a complementary range management size and availability likely interact to produce the highly variable practice. Tallgrass prairies, existing at the far western boundary of population densities of American burying beetles found along the the eastern hardwood forests of North America, are thought to have fringe of their current contracted range. been historically maintained by grazing and fire (Axelrod 1985). While grazing is ubiquitous across most of the grassland range of Microbial Symbionts N. americanus, the use of fire to structure botanical communities is American burying beetle reproductive behavior, like that of other regionally variable and not universally accepted nor implemented. Nicrophorine species, has likely evolved under the complex Grazing by wild and domesticated large herbivores produces selective pressures produced by internal and external microbial well-studied but variable effects on prairies, but tends to thwart symbiont and competitor communities that vary over space and woody invasion, increase grassland habitat heterogeneity, and time (Rozen et al. 2008, Cotter and Kilner 2010, Hall et al. 2011, influence nutrient cycling (Collins et al. 1998), while also interacting Jacobs et al. 2016, Trumbo et al. 2016). Burying beetles produce with fire behavior through reductions in fuel load (Hobbs 1996). oral and anal secretions known to thwart the growth of certain soil Grazing can structure both above-ground botanical composition and carcass-borne microbes that would accelerate carcass decay (Hickman et al. 2004) and below-ground edaphic communities (Hall et al. 2011, Arce et al. 2012), but also pass beneficial gut (Johnson and Matchett 2001). Cattle and bison grazing differ in microbes along to their offspring during development (Wang and their ecological effects (Plumb and Dodd 1993, Damhoureyeh and Rozen 2017). Burying beetle immune function is intimately tied Hartnett 1997, Towne et al. 2005), stimulating slightly different to environmental cues (contact with, preparation of, and parental post-grazing responses in grassland botanical and invertebrate care behaviors involving carcass handling) that predict exposure communities. These grazer-induced ecological outcomes are thought to microbial challenges (Steiger et al. 2011, Arce et al. 2013); both to influence prairie faunal populations across trophic levels (Todd recognition and upregulation mechanisms likely evolved due to the 1996, Griebel et al. 1998, Knapp et al. 1999, Matlack et al. 2001, high fitness costs associated with rapid carcass degradation. While Jonas and Joern 2007), but no studies have explicitly focused on how more work is needed to disentangle the details, it appears likely grazing interactions in tallgrass prairies might influence populations that burying beetles recruit microbe symbionts to produce some of American burying beetles, which rely obligately on grassland bird of the antimicrobial agents for them (Vogel et al. 2017). While the and small mammal species for reproduction. Mowing of grasslands coevolution of Nicrophorine burying beetles with their microbial can also produce ecological responses similar to grazing but fewer symbiont communities is emerging as a model for studying animal studies have examined mowing effects on tallgrass prairie trophic hologenomes, virtually nothing is known regarding these important structure (Lemen and Clausen 1984, Collins et al. 1998). biotic interactions in the American burying beetle. In a field study that examined Nicrophorine burying beetle American burying beetles are known as habitat and forage- abundances, spatial distributions, and individual post-capture type generalists; evidence suggests that they can increase their movement patterns across a large tallgrass prairie study site where fitness through the utilization of larger carcasses that may be multiple grazing regimes and seasonal mowing occurred, we found untenable for their sympatric congeners (Kozol et al. 1988). This that grazing influenced overall abundances and flight behavior of type of resource partitioning was hypothesized to potentially drive American burying beetles (unpublished data). Trap rates were differences in microbiome structure in the endangered species. From significantly greater at ungrazed sites than at either bison-grazed or microbiome data collected by Olmstead et al. (unpublished data), cattle-grazed locations. Ungrazed sites also exhibited greater mean American burying beetles were found to have greater microbial grass heights than cattle-grazed, bison-grazed or mowed study diversity compared to three sympatric congeners, but lower overall sites, and post-capture beetle flight behavior differed between the microbial abundance. Some of the microbial constituents shared grazing regimes. American burying beetles collected, tagged and Copyedited by: OUP

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released in ungrazed areas and recollected in cattle-grazed pastures The Oklahoma Natural Heritage Inventory’s (OHNI) database in exhibited greater daily flight distances (1267.31 m/d) than beetles February 1995 listed 74 sites in 17 counties. Based on data from initially collected in and subsequently recaptured in cattle-grazed the OHNI survey sheets, new surveys were conducted in 1994–1996 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 areas (406.66 m/d). This may in part be explained by the more in 14 of those counties, sponsored by the U.S. National Biological consolidated spatial pattern of cattle-grazed regions at the site but Service (Hill 1996). Visits were made to 36 of the sites during may also point to a link between habitat heterogeneity and foraging the known active calling period, and an additional 13 sites were behavior in American burying beetles. Moreover, these interactions evaluated outside that time. Of the 36 sites sampled, 23 (63.9%) between grassland botanical structure and American burying beetle no longer supported prairie mole crickets. However, 12 new sites abundance and space use are likely related to habitat utilization were found in 1995–1996, including new sites in Tulsa County and patterns of the small vertebrates used by Nicrophorus species for new county records for Logan and Pottawatomie counties. Most of reproduction and deserve a more in-depth experimental evaluation these sites identified during the surveys in the early 1990s have not of hypotheses generated by these data. been revisited however, and the data gathered in subsequent years has been from two primary grassland study sites in Craig and Osage Gryllotalpa major Saussure (Proposed Common Counties, Oklahoma (Hill 1999, Howard and Hill 2007, Hill et al. Name: Prairie Mole Cricket) 2009). The prairie mole cricket (Fig. 4) is a rare grassland insect found in Much of what we have learned during these studies at these prairie remnants in the southern plains of the United States. In the two sites has been related to the species reproductive biology and 1980s, the species was considered extinct, but opportunistic spot mating behavior. The adult mating period is brief and occurs in surveys that identified an extant population led to an Invertebrate spring from late March until early May most years (Figg and Calvert Species Notice of Review being issued by the U.S. Fish and Wildlife 1987). Males emerge onto mating aggregations (leks) in the spring Service (USFWS 1990). Subsequent surveys of historic ranges in (Hill 1999) and construct an acoustic burrow from which they call Oklahoma, Kansas, Missouri, and Arkansas in 1990–1991 (Figg to attract flying females (Walker and Figg 1990, Hill et al. 2006). and Calvert 1987, Busby 1991, USFWS 1991, Vaughn & Rudman The male’s loud acoustic call (Hill 2000) is produced at dusk, with 1991, Caire et al. 1993, Vaughn et al. 1993) using the male’s call as individual males calling for approximately 40 min each, and an entire a presence indicator located additional populations, but insufficient lek active for approximately 1 h after sunset. Calling behavior in an information was available on the species to support either listing aggregation is highly dependent upon local microclimate conditions or elimination from consideration (USFWS 1992). From 1987 to at a site (Hill 1999), with air and soil temperature interacting with 1991 the USFWS found 120 sites where prairie mole cricket males wind speed to influence a male’s decision to call and for how long were calling across 18 counties in Oklahoma (USFWS 1991). to invest in advertisement. Females are attracted to male calls, which are produced at a relatively low dominant frequency (2 KHz) and carry information on the sender’s size (Howard and Hill 2006) and position on the lek (Howard et al. 2011). Courtship occurs in the male burrow, but the details of where mating and oviposition takes place remains a mystery. Adults are thought to survive a single reproductive season, but details regarding development, diet, predator-prey dynamics, or invasive species interactions remain undescribed in the species. Prairie mole crickets are tallgrass prairie endemics, found historically in untilled grassland sites where range management often combines grazing with prescribed burning regimes. While small relict tracts of tallgrass prairie persist in the northern Midwest, substantial intact remnants exist only in portions of Oklahoma, Missouri, Arkansas, and Kansas, and it is in these remaining grassland tracts where the species persists. Small prairie mole cricket populations can easily go undetected, due to the species’ fossorial biology. Despite its well-known reliance on tallgrass prairie for ecological persistence, relatively little is known regarding biotic interactions with other grassland community constituents. Following are three examples of such interactions, and how these interactions might be considered when evaluating conservation implications.

Intraspecific Interactions: Male Relatedness in Calling Aggregations The traditional view of lek mating systems emphasizes inter-male competition leading to strong sexual selection and the prevalence of a stark mating skew (Bradbury 1981, Beehler and Foster 1988, Höglund and Alatalo 1995). In prairie mole cricket mating Fig. 4. The prairie mole cricket (Gryllotalpa major) is a rare tallgrass prairie endemic insect species with a current range limited to portions of Oklahoma, aggregations, the prevailing thought was that males constructed Missouri, Arkansas, and Kansas. Males call from specialized acoustic burrows acoustic burrows across the lek in a favorable position to attract a in the spring, forming aggregations that attract flying females during the mate, and that unrelated rival males positioned nearby (within 2–4 short nightly calling period at dusk. Photo by Ryan West. m) represented direct inter-male competition for responding females. Copyedited by: OUP

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However, more recent work by Keane et al. (2016) surprisingly Hedwig 2006). Experimental work to describe the precise tuning confirmed that these small clusters of males within the lek exhibit curves of the subgenual organ will likely provide additional insights high levels of genetic relatedness. These sibling or near-sibling males into predator-prey dynamics in the system. 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 may benefit from this spatial arrangement through active cooperation Neurophysiological studies on the auditory system suggest that that ostensibly produces more attractive acoustic ‘hotspots’ on the calling prairie mole cricket males position their burrows across lek, leading to either direct benefits via female preference for these the lek at distances such that they can detect the acoustic signal of loud and acoustically complex signaling clusters or indirect genetic other calling males (Howard et al. 2008). This likely has an adaptive benefits when a neighboring related male is successful in attracting benefit with respect to how females search for and ultimately select a mate (Keane et al. 2018). Females collected at active lek sites were a mate. But prairie mole cricket hearing exhibits a bimodal tuning less related to each other or to the lek males than were the advertising curve (Fig. 5A), with the primary sensitivity associated with the males to each other, suggesting that females are the dispersing natural frequency range of the male call, and a second sensitivity sex. This genetic relatedness dynamic was somewhat dependent peak in the ultrasonic range (~25 KHz). While males sequestered upon the size of the calling aggregation, but holds implications and calling in the confines of a calling burrow likely encounter low for conservation when considering species reintroductions where risk of bat predation, females fly at dusk during peak periods of understanding how mating behavior influences the genetic diversity insectivorous bat foraging. While no study has yet confirmed bat and population structure of founder populations might dictate long- predation in these large flying orthopterans, the form of the prairie term metapopulation success. mole cricket sensory system hints at a predation-avoidance function. Several species of aerial-hawking bats have been documented at sites Interactions With Predators: Indirect Evidence From where prairie mole crickets are reproductively active in the spring, Sensory Adaptations but additional experimental work is needed to directly test for this While no study has directly evaluated predator-prey interactions potentially important biotic interaction, and to assess how bat in prairie mole crickets, attributes of the species’ sensory system predation might influence female mate-locating behavior and local point toward several potentially important biotic interactions. population dynamics. Field behavioral studies of calling prairie mole cricket males confirm that they use substrate-borne vibrations produced by the Grassland Botanical Structure and Mating Behavior airborne call of a neighboring male for making fine-scale spacing When prairie mole cricket males begin calling in the spring, the and calling decisions (Hill and Shadley 1997, 2001). While males location of their burrows at a site does not appear to relate to fine- generally ignore airborne external sound while calling, they are scale differences in soil type (Hill et al. 2009), but the grassland exceptionally sensitive to any seismic (soil-borne) disturbance and botanical structure does appear to matter (Fig. 5B), influencing both immediately stop calling if exposed to vibration. Living most of where leks emerge on the prairie and how males space themselves and their lives subsurface, prairie mole crickets likely interface with construct their burrows. Prairie mole cricket mating aggregations are potential surface and subterranean predators via the substrate-borne found preferentially on recently burned sites (Howard and Hill 2007) vibrations that they produce; thus, the organs in the legs that respond with lower botanical biomass than adjoining unburned sites. While to this form of vibration (subgenual organs) in a primary predator other explanations for why these insects might prefer burned sites detection context are likely coopted into use for assessing nearby have not been investigated (favorable temperatures, lower predation/ males while the auditory system is inhibited. This occurs as a result competition), this site preference dynamic related to botanical of an auditory system corollary discharge, and in effect renders them structure may have evolved in parallel with acoustic adaptation, in temporarily insensitive to airborne sound during calling (Poulet and which both signal transmission and receiver detection and localization

Fig. 5. The auditory sensitivity threshold of Gryllotalpa major (A) is tightly tuned to the frequency of the male call song (2.0 KHz; shaded vertical ellipse)) and includes a second sensitivity peak in the ultrasound around 25 KHz, which is likely a mechanism for eavesdropping on foraging bats. The shaded horizontal ellipse represents local bat biosonar frequency range. Male spacing across a mating aggregation was influenced by the botanical structure across the lek (B). Above-ground botanical biomass was significantly correlated with three spatial parameters of the calling aggregation: furthest neighbor distance (circular points and solid fit line in graph), inter-burrow distance (square points and broken fit line in graph), and nearest neighbor distance (triangular points and dotted fit line in graph). Copyedited by: OUP

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are optimized in less acoustically complex environments. Grazing political pressure to relax protections for American burying beetles. and mowing may likewise produce the same lek location preference Moreover, concern over climate-related impacts to the species has effects, but these rangeland disturbances remain unstudied. Even resulted in recently proposed federal efforts to shift conservation 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 in recently burned prairies, grassland botanical composition is efforts away from the core population found in Oklahoma to the generally heterogeneous, and prairie mole cricket males respond to northern portion of the existing American burying beetle range in this structural variation in making their acoustic burrow spacing Nebraska and Kansas, leading to conflict between the USFWS and decisions. At sites with greater mean botanical biomass and grass portions of the scientific community due to the perceived lack of height, males space themselves further apart from each other than scientific support for this policy (https://www.washingtonpost. at sites where the grass and forb abundance and density have been com/energy-environment/2018/09/03/shocked-disappointed-pair- reduced by fire and/or grazing (Fig. 5B; Howard and Hill 2007). researchers-say-they-felt-pressed-by-federal-wildlife-officials-bury- While the function of this interaction with plant structure needs risk-endangered-beetle/?utm_term=.d37fde1e3973). Conversely, experimental attention, this response may allow prairie mole cricket prairie mole crickets have received scant conservation attention females, which have to navigate the complex structural environment since the original petition for protection was tabled by the USFWS. of the tallgrass prairie substrate after landing near a calling male, Recently, however, state natural resource departments have to localize males more efficiently. Moreover, males modify their taken steps to prioritize the collection of relevant data to support acoustic burrows in response to the local botanical structure by conservation efforts for the species. For example, the Oklahoma increasing the dip angle of the burrow at sites where the grass height Department of Wildlife Conservation recently elevated the prairie is greater (Howard and Hill 2009). This likely directs the sound field mole cricket to a tier 1 species in the state, which for the first time upward in a fashion that increases detectability for airborne females makes the species an eligible target for state-level research funding. during phonotaxis, and represents another subtle biotic interaction While most published studies and current research on American between calling male prairie mole crickets and the botanical micro- burying beetle biology have emphasized abiotic influences on life environment in which they advertise for mates. history and behavior, new discoveries related to biotic interactions hold promise for contributions to species recovery. Understanding how American burying beetle niche breadth responds to variable Concluding Remarks interspecific competition is likely critical in predicting local These examples highlight important biotic interactions that occur persistence in the face of disturbance and climate change in between botanical communities and the non-herbivorous insects established populations, but also for assessing the probability of found there; additional work is required to disentangle the precise success in reintroductions. For example, recent American burying nature of these relationships and the direct or indirect mechanisms beetle reintroduction efforts in Missouri have met with success, that underlie the measured responses. Flight patterns, habitat while a multi-year effort in Ohio has failed to establish a sustainable occupancy and spatial behavior of both prairie mole crickets and population (Ferrari 2014). While abiotic factors may play a part American burying beetles are intimately intertwined with plant in the divergent patterns of recruitment in these two conservation community structure and disturbance. Understanding the functional efforts, the magnitude and direction of local Nicrophorine and importance of these plant-insect interactions and how they change vertebrate competition for carcasses likely structured the outcome over space and time can inform how managers promote species of these reintroduction efforts. Similarly, recent discoveries in recovery across landscape scales. Recent findings demonstrating microbial ecology provide increasing support for the notion that the the importance of the microbiome in facilitating or constraining ubiquitous parental care behavior for which Nicrophorine burying reproductive success in Nicrophorine burying beetles like the beetles are known are likely, in part if not entirely, mediated by American burying beetle point to the importance of advancing our microbial symbionts. Given the apparent difference in the American understanding of these same types of symbioses in other rare insect burying beetle microbial community with those maintained by their species. Given its edaphic biology, soil microbial communities likely closest relatives, studies addressing whether the species decline is play an important selective role in driving many of the fossorial related to or in fact the result of the perturbation of these microbial adaptations of prairie mole crickets and yet this dimension of the relationships represents a research frontier deserving of study. species’ ecology remains largely unexplored. Similarly, understanding Moreover, since 2012 the USFWS has incentivized the establishment American burying beetle sensory ecology and fine-scale genetic of conservation tracts designated for American burying beetle structure of beetle populations might directly or indirectly reveal recovery (American burying beetle conservation banks). The biotic interactions that could aid in the species’ recovery. Likewise, purpose of these conservation banks is to provide a mitigation soil arthropod niche and competition dynamics remain a virtually solution for industry stakeholders that sponsor activities impacting unstudied frontier; understanding where prairie mole crickets fit into lands with established American burying beetle populations. The these trophic structures could prove important in managing for this management portfolio for these conservation banks includes cryptic soil-dwelling species. an array of tools to establish and maintain habitat suitable for Both American burying beetles and prairie mole crickets likely American burying beetle populations to thrive, supporting regional represent species whose conservation fate remain tenuous and population resiliency. Considering the widespread use of grazing in uncertain; their stories continue to unfold as conservation policy the core range of the American burying beetle and its consideration attempts to integrate new science and respond to stakeholder for use on conservation banks, understanding how grazing regimes interests. While new populations of American burying beetles have can differentially influence American burying beetle populations is been reported since the original listing under the U.S. Endangered critical. Additional research is needed to identify the intersection of Species Act, the documented range of the species has not expanded sustainable American burying beetle conservation management and appreciably, and human impacts related to extractive activities have best practices with respect to cattle stocking levels. increased in magnitude across the region in Oklahoma where the Comparatively, most research attention on the biology of the core population is found. The regulatory costs of compliance with prairie mole cricket has focused on biotic influences on the species’ the ESA has resulted in a fossil fuel industry initiative to apply life history and behavior. In the absence of funding allocated Copyedited by: OUP

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specifically for the species’ conservation, these large edaphic insects underlaying monarch butterfly (Danaus plexippus Linnaeus) and have emerged as a model system for studying lek mating behavior, other native pollinator declines could energize cross-disciplinary female choice and acoustic communication. As the species has research partnerships while producing critical new scientific insights 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 reemerged as a conservation target, however, several of these studies that could improve current intervention efforts. Other insect focused on biotic interactions hold promise to aid in its recovery. species of conservation interest for which recovery plans remain Understanding genetic relatedness dynamics within and across in development albeit hampered by a dearth of basic biological leks can inform how animals are selected for relocation initiatives. data, such as Papaipema eryngii Bird (the Eryngium root borer or Given that these large mating aggregations consist mostly of highly rattlesnake-master borer moth) and the rusty patched bumblebee related males, with low relatedness between visiting females, efforts (Bombus affinis Cresson) would also benefit from innovative to select founders for a reintroduction should prioritize collecting studies that unravel the biotic interactions that likely structure their males from multiple leks. Sensory system adaptations in this species behavior, ecology and populations. While biotic interaction data are not only suggest cryptic patterns of predator-prey dynamics, but intrinsically fascinating to the scientific community, making them also generate hypotheses regarding how anthropogenic factors accessible, meaningful, and relevant in an applied context can increase might influence mating behavior and reproduction. Given the high the impact of basic entomological research, and ensure its resonance sensitivity of prairie mole crickets to substrate-borne vibration, it is across a broader audience of stakeholders. For instance, in the case of likely that human-related sources of vibrational noise will interfere Cicindela albissima Rumpp (the Coral pink sand dunes tiger beetle), with both male acoustic behavior and female phonotaxis. Moreover, understanding the species’ sensory ecology might reveal how these while the species auditory system is adapted to detect bat predators, rare, endemic beetles detect and interact with ecologically relevant this auditory sensitivity may also carry a cost; ultrasonic noise may predators and prey, but could also reveal how they respond to the evoke a startle response that would also inhibit mating behavior. substrate-borne vibrations produced by off-road vehicles that are Anthropogenic noise effects on insects of conservation interest, thought to represent a primary threat to the isolated habitats where especially noise in the ultrasonic range and via substrate-borne their populations are found (Knisley 2011). Widening the net to transmission, deserves additional study. As in American burying engage a broader community of stakeholders can also synergize and beetle and livestock grazing effects, the interaction of prairie mole diversify the scope of biotic interaction questions considered relevant, crickets with botanical structure can have applied consequences. resulting in increased research innovation, and ultimately a deeper Prairie mole cricket males prefer to establish mating aggregations understanding of the ‘little things that run the world’ (Wilson 1987). during the spring mating season in areas where fire and/or grazing have produced more open landscapes. It is not known whether this same prairie botanical structure optimizes female oviposition Acknowledgments requirements or larval development. Implementing local range We thank Kevin Stubbs and Anita Barstow of the U.S. Fish and Wildlife management strategies such as patch-burn grazing (Fuhlendorf and Service, Tulsa EFSO; Robert Hamilton and Jay Pruett of The Nature Engle 2001), which emphasizes grassland heterogeneity, may offer Conservancy of Oklahoma; Jann Hayman, Osage Nation Department of the greatest conservation payback in this species. Natural Resources; and Mark Brian, Advance Ecology, Ltd. for their technical Recent technological advancements in several fields hold and logistical support of our work with the American burying beetle and the promise to aid investigators in studying rare and often cryptic biotic prairie mole cricket in Oklahoma over the past 15 yr. Additionally, data in interactions. The -omic revolution, with tools used to study the preparation for publication by our graduate students (E. Joels, M. Keller, and genome, proteome or metabolome, have proven useful in revealing M. Olmestead) has greatly supported this review. Financial support has been provided by grants from the U.S. National Science Foundation, U.S. Fish and important insect–plant and insect-microbial relationships (Barah Wildlife Service, Oklahoma Department of Wildlife Conservation, The Nature and Bones 2015). The refinement of unmanned aerial vehicle (UAV) Conservancy, Oklahoma Chapter, and the New Hampshire Agricultural technologies, which can easily be fitted with lightweight but high- Experiment Station. resolution sensors that can collect data at spatial and temporal scales relevant to insect biology represents an exciting research front (Näsi References Cited et al. 2015), especially when considering the potential of using small micromechanical UAV insects (Chechetka et al. 2017) in studies Albrecht, M., P. Duelli, B. Schmid, and C. B. Müller. 2007. Interaction addressing interspecies interactions. 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