Temporal survey of a Carrion beetle (Coleoptera: silphidae) community in Indiana.
Keywords: Silphidae, carrion, forensic entomology, Nicrophorus tomentosus
After death, a vertebrate carcass assumes the role of a quality, yet highly ephemeral, nutrient resource that is utilized by insects and other organisms (Benbow et al. 2015). Though blow flies (Diptera: Calliphoridae) represent the most heavily scrutinized carrion-breeders by ecologists and forensic scientists (Amendt et al. 2004), beetles can also play a critical role in the decomposition process (Dekeirsschieter et al. 2013b). In particular, carrion beetles (Coleoptera: Silphidae) utilize carcasses to carry out their life cycles and represent novel models for behavioral ecology (Ratcliffe 1996).
Silphids are widespread in North America, with recorded observations in Arkansas (Holloway & Schnell 1997), Colorado (Smith et al. 2000), Indiana (Shubeck et al. 1977; Perez et al. 2014), Iowa (Coyle & Larsen 1998), Louisiana (Watson & Carlton 2005), Michigan (Werner & Raffa 2003), Missouri (Shubeck & Schleppnik 1984), Nebraska (Ratcliffe 1996), New Jersey (Shubeck 1983), Texas (Mullins et al. 2013), and Virginia (Beirne 2013). Two subfamilies (Nicrophorinae and Silphinae) comprise this family (Anderson & Peck 1985), and can be differentiated by both morphology (i.e., body shape) and resource utilization. Nicrophorine beetles ("Burying Beetles") not only directly consume the carcass (necrophagy), but also bury it for their offspring, thereby preventing intruders from "stealing" the carcass (Trurnbo 1990). In particular, nicrophorines (e.g., Nicrophorus investigator Zetterstedt) preferentially bury small (16-48 g) vertebrate carcasses (Smith & Heese 1995; Smith & Merrick 2001), thereby providing a protected, consistent resource on which to rear offspring. Larvae of this species are altricial, requiring one or both parents (biparental brood care) to feed them for the extent of their immature life stages. Meanwhile, silphine beetles (e.g., Necrophila americana Linnaeus) consume larger carcasses for feeding and will prey on other scavengers (necrophily), but do not bury carcasses or exhibit any parental care.
Members of the subfamily Nicrophorinae have been the focus of intense ecological research in the last century, as they exhibit a suite of remarkable reproductive behaviors, including communal breeding in response to competition with flies (Scott 1994), carcass modification (Pukowski 1933), and biparental care (Scott 1998). Nicrophorines also possess specialized chemosensory adaptations to efficiently locate a carcass (Dekeirsschieter et al. 2013a) and emit volatiles to kill microorganisms on the carcass (Haberer et al. 2014). In addition, nicrophorines exhibit complex ecological and evolutionary associations with phoretic mites in which the beetle acts as a vehicle to transport up to hundreds of mites to ephemeral resources, including carcasses. The mites, in turn, may consume eggs or larvae of competitors (Springett 1968; Wilson 1983; Schwarz & Muller 1992).
The population dynamics of common silphids have been previously investigated in other regions, including Nicrophorus americanus Olivier in Arkansas (Holloway & Schnell 1997), Indiana (Shubeck et al. 1977), and particularly populations of N. investigator in Colorado (Smith & Heese 1995; Smith et al. 2000; Smith & Merrick 2001). Silphid population sizes tend to be significantly correlated with small mammal biomass (Holloway & Schnell 1997; Smith & Merrick 2001). The purpose of this study was to re-assess a community of silphids that had been surveyed many years prior at Purdue University (West Lafayette, IN) (Shubeck et al. 1977). Results of this study are compared to what was previously found at the Purdue site, as well as results from a nearby site seeded with 53 pig (Sus scrofa Linnaeus) carcasses in Rensselaer, IN (Perez et al. 2014).
MATERIALS AND METHODS
Silphids were sampled from the FERC (Forensic Entomology Research Center) at Purdue University from June to December 2014. Beetles were collected passively via pitfall traps consisting of a plastic 6-quart (5.7 L) storage box filled with approximately 5 cm of pet-friendly RV & marine antifreeze (Super Tech[R]) and baited with approximately 500 g aged chicken liver and blood in a 710 mL plastic food storage container. This apparatus was buried flush with the surface of the ground and covered with chicken wire to exclude scavengers, and covered with an aluminum roof approximately two inches above ground to protect the trap from rain. Three pitfall traps were placed at approximately 15 m intervals and were checked every week in June and July 2014, and every two to three weeks thereafter for a total of 13 collections.
At each collection, antifreeze containing trapped insects was filtered through a 20 cm diameter 88 mesh strainer and stored in 95% ethanol. Traps were reset with aged chicken liver bait, and filled with clean antifreeze. Silphids were identified to species via morphological taxonomy (Anderson & Peck 1985; Mullins et al. 2013), counted, and stored at -20[degrees]C. Temperature data (average, maximum, and minimum ([degrees]C)), for each site was posteriorly collected from archived historical weather data (www.wunderground.com). Specimens are vouchered at the Purdue Entomology Research Collection.
Statistics were performed in R using standard packages (R Core Team 2015), as well as the vegan package for biodiversity statistics (abundance, species richness, Simpson's index of diversity, and Jaccard's similarity coefficient) (Oksanen et al. 2015).
A total of 1607 silphids were collected from June to December 2014 (Fig. 1). Seven silphid species were collected (Necrodes surinamensis (Fabricius), Necrophila americana (Linnaeus), Oiceoptoma novaboracense (Forster), Oiceoptoma inaequale (Fabricius), Nicrophorus marginatus (Fabricius), Nicrophorus orbicollis (Say), and Nicrophorus tomentosus (Weber).
The summer months of June-August exhibited the greatest abundance of silphids (N = 543), as well as the highest average species richness (R = 5.28). Simpson's Index of Diversity (1-D) was greatest for late June/early July (1-D = 0.751), and late August (1-D = 0.720) when temperatures averaged 22.2[degrees]C (9.4-30.6[degrees]C) and 24.4 degrees]C (15.6-31.7[degrees]C), respectively. These dates also clustered together using Jaccard's Index (clustering between sites based on shared species), whereas dates of low abundance and low diversity also clustered together (Fig. 2). Silphid abundances were as follows: Np. Americana (N = 551, June-October), followed by O. inaequale (N = 386, June-August), N. tomentosus, (N = 199, June-October), N. orbicollis (N = 171, August-December), N. marginatus. (N = 5, June, August-September), and Ne. surinamensis (N= 2, July, August).
Silphid species sampled in this study corresponded to those reported previously by Shubeck et al. (1977), except for the absence of Nicrophorus pustulatus (Herschel) in our survey. Shubeck et al. (1977) observed O. novaboracense as the most prominent species (N = 2033, April July), followed by O. inaequale (N = 756, April July), Np. americana (N = 572, April-July), N. orbicollis (N = 318, August-September), N. tomentosus (N = 201, June-July), Ne. surinamensis (N = 25, June-July), and N. pustulatus (N = 13, June-September). Though rank order differs slightly, both Shubeck et al. (1977) and the current study show that the subfamily Silphinae predominates this region in early to mid-summer, and is replaced temporally by the Nicrophorinae from mid-summer to fall. Silphid diversity in the current study also aligns with observations made from 53 pig carcasses at Rensselaer, IN (Perez et al. 2014), the only discrepancy was that O. inaequale, was observed in our study but not in theirs.
The American Carrion Beetle, Np. americana. was the most predominant species collected (N = 551), and was present from mid-June to early October. This ground-dwelling silphid, with its preferences for an open-field habitat (Shubeck 1983), arrives at carcasses in late spring to early summer (Anderson 1982), and may arrive early in decomposition (Tabor et al. 2004). Collections of Np. americana have been made with carrion-baited pitfall traps (Coyle & Larsen 1998; Shubeck 1983; Werner & Raffa 2003), carcasses (Tabor et al. 2004), and isopropanol-baited pitfall traps (Reut et al. 2010). Two Oiceoptoma species (O. inaequale and O. novaboracense) comprised the second and third most abundant silphid sampled, but were only present from June to August. This genus appears 2-3 days after carcass deposition and can remain on or near remains until advanced decay (Tabor et al. 2004). Patterns of Oiceoptoma spp. sampled here align with those seen for O. inaequale and O. novaboracense in New Jersey, as they are most active in the early part of the summer and decline in abundance thereafter (Shubeck 1983). Though N. tomentosus was not the most abundant silphid overall, it was the most prevalent species in its subfamily, appearing at 11 of the 13 collections. This species has been speculated to be the "most active" species in this genus, as it may exhibit a broad flight range when searching for a carcass (Shubeck 1983). According to these collection data, N. tomentosus emerges in mid-late June and reaches peak abundance in August and September, a pattern that aligns with Anderson (1982).
Overall, this study demonstrated that silphid beetle communities exhibit consistent interannual diversity and abundance patterns for this site. Additional molecular analyses of silphid communities and individual species in the Midwest would greatly improve upon this work and would shed light on the population genetic structure of carrion beetles. A community-based molecular approach to track changes in allele frequencies over time could give insight into why population dynamic patterns do not vary over time.
Amendt, J., R. Krettek & R. Zehner. 2004. Forensic entomology. Die Naturwissenschaften 91:51-65.
Anderson, R. & S. Peck. 1985. Coleoptera: Silphidae and Agyrtidae, The carrion beetles of Canada and Alaska. Edmonton, Alberta, Canada: University of Alberta. 121 pp.
Anderson, R.S. 1982. Resource partitioning in the carrion beetle (Coleoptera:Silphidae) fauna of southern Ontario: ecological and evolutionary considerations. Canadian Journal of Zoology 60:1314-1325.
Beirne, S. 2013. Distribution of carrion beetles (Coleoptera: Silphidae) in different geographic regions of Virginia. Master of Science Thesis, Virginia Polytechnic Institute and State University, Blackburg, Virginia. 63 pp.
Benbow, M.E., J.K. Tomberlin & A.M. Tarone. 2015. Carrion Ecology, Evolution, and Their Applications. CRC Press, Boca Raton, Florida. 577 pp.
Coyle, D. & K. Larsen. 1998. Carrion beetles (Coleoptera: Silphidae) of northeastern Iowa: a comparison of baits for sampling. Journal of the Iowa Academy of Science 105:161-164.
Dekeirsschieter, J., C. Frederickx, G. Lognay, Y. Brostaux, F.J. Verheggen & E. Haubruge. 2013a. Electrophysiological and behavioral responses of Thanatophilus sinuatus Fabricius (Coleoptera: Silphidae) to selected cadaveric volatile organic compounds. Journal of Forensic Sciences 58:917-923.
Dekeirsschieter, J., C. Frederickx, F.J. Verheggen, D. Drugmand & E. Haubruge. 2013b. Diversity of forensic rove beetles (Coleoptera: Staphylinidae) associated with decaying pig carcass in a forest biotope. Journal of Forensic Sciences 58:1032-1040.
Haberer, W., S. Steiger & J.K. Muller. 2014. Dynamic changes in volatile emissions of breeding burying beetles. Physiological Entomology 39:153-164.
Holloway, A.K. & G.D. Schnell. 1997. Relationship between numbers of the endangered American burying beetle Nicrophorus americanus Olivier (Coleoptera : Silphidae) and available food resources. Biological Conservation 81:145-152.
Mullins, P.L., E.G. Riley & J.D. Oswald. 2013. Identification, distribution, and adult phenology of the carrion beetles (Coleoptera: Silphidae) of Texas. Zootaxa 3666:221-251.
Oksanen, J., Blanchet, F., Kindt, R., Legendre, P., Minchin, P., O'Hara, R., Simpson, G., Solymos, P., Henry, M., Stevens, H., & Wagner, H. (2015). vegan: Community Ecology Package, R package (Version 2.3-1). At: http://CRAN.R-project.org/package=vegan.
Perez, A.E., N.H. Haskell & J.D. Wells. 2014. Evaluating the utility of hexapod species for calculating a confidence interval about a succession based postmortem interval estimate. Forensic Science International 241:91-95.
Pukowski, E. 1933. Okologische untersuchungen an Necrophorus f. Zeitschrift fur Morphologie und Okologie der Tiere 27:518-586.
R Core Team. 2015. R: A language and environment for statistical computing (Version 3.2.2). Vienna, Austria: R Foundation for Statistical Computing. At: http://www.R-project.org/.
Ratcliffe, B.C. 1996. The carrion beetles (Coleoptera: Silphidae) of Nebraska. Bulletin of the University of Nebraska State Museum 13:1-100.
Reut, M., B. Cowell & M.A. Pszczolkowski. 2010. Traps baited with isopropanol attract the American Carrion Beetle, Necrophila americana (L.) (Coleoptera: Silphidae). Coleopterists Bulletin 64:230-234.
Schwarz, H.H. & J.K. Muller. 1992. The dispersal behaviour of the phoretic mite Poecilochirus carabi (Mesostigmata, Parasitidae): adaptation to the breeding biology of its carrier Necrophorus vespilloides (Coleoptera, Silphidae). Oecologia 89:487-493.
Scott, M.P. 1994. Competition with flies promotes communal breeding in the burying beetle, Nicrophorus tomentosus. Behavioral Ecological Sociobiology 34:367-373.
Scott, M.P. 1998. The ecology and behavior of burying beetles. Annual Review of Entomology 43: 595-618.
Shubeck, P.P. 1983. Habitat preferences of carrion beetles in the Great Swamp National Wildlife Refuge, New Jersey (Coleoptera: Silphidae, Dermestidae, Nitidulidae, Histeridae, Scarabaeidae). Journal of the New York Entomological Society 91:333-341.
Shubeck, P.P., N.M. Downie, R.L. Wenzel & S.B. Peck. 1977. Species composition of carrion beetles in a mixed-oak forest. William L. Hutcheson Memorial Forest Bulletin 4:12-17.
Shubeck, P.P. & A.A. Schleppnik. 1984. Silphids attracted to carrion near St. Louis, Missouri (Coleoptera: Silphidae). Journal of the Kansas Entomolical Society 57:360-362.
Smith, R.J. & B. Heese. 1995. Carcass selection in a high altitude population of the burying beetle, Nicrophorus investigator (Silphidae). The Southwestern Naturalist 40:50-55.
Smith, R.J., A. Hines, S. Richmond, M. Merrick, A. Drew & R. Fargo. 2000. Altitudinal variation in body size and population density of Nicrophorus investigator (Coleoptera: Silphidae). Environmental Entomology 29:290-298.
Smith, R.J. & M.J. Merrick. 2001. Resource availability and population dynamics of Nicrophorus investigator, an obligate carrion breeder. Ecological Entomology 26:173-180.
Springett, B.P. 1968. Aspects of the relationship between burying beetles, Necrophorus spp. and the mite, Poecilochirus necrophori Vitz. Journal of Animal Ecology 37:417-424.
Tabor, K.L., C.C. Brewster & R.D. Fell. 2004. Analysis of the successional patterns of insects on carrion in southwest Virginia. Journal of Medical Entomology 41:785-795.
Trumbo, S.T. 1990. Interference competition among burying beetles (Silphidae: Nicrophorus). Ecological Entomology 15:347-355.
Watson, E.J. & C.E. Carlton. 2005. Insect succession and decomposition of wildlife carcasses during fall and winter in Louisiana. Journal of Medical Entomology 42:193-203.
Werner, S.M. & K.F. Raffa. 2003. Seasonal activity of adult, ground-occurring beetles (Coleoptera) in forests of northeastern Wisconsin and the Upper Peninsula of Michigan. Amercian Midland Naturalist 149:121-133.
Wilson, D.S. 1983. The effect of population structure on the evolution of mutualism: a field test involving burying beetles and their phoretic mites. American Naturalist 121:851-870.
Manuscript received 30 December 2015, revised 29 March 2016.
Charity G. Owings (1) and Christine J. Picard: Department of Biology, Indiana University Purdue University, Indianapolis, IN 46202 USA
(1) Corresponding author: Charity G. Owings, 317-274-6520, email@example.com.
Please note: Some tables or figures were omitted from this article.
|Printer friendly Cite/link Email Feedback|
|Author:||Owings, Charity G.; Picard, Christine J.|
|Publication:||Proceedings of the Indiana Academy of Science|
|Date:||Jun 27, 2016|
|Previous Article:||The vascular flora and plant communities of Holthouse Woods Nature Preserve in Wayne County, Indiana.|
|Next Article:||130th Annual Academy Meeting: Presidential Plenary Address by Arden L. Bement Jr. "Connective Pathways in Science".|