Our study investigated the fungistatic effects of the anal secretions of Nicrophorus nepalensis Hope on mouse carcasses. The diversity of fungi on carcasses was investigated in five different experimental conditions that corresponded to stages of the burial process. The inhibition of fungal growth on carcasses that were treated by mature beetles before burial was lost when identically treated carcasses were washed with distilled water. Compared with control carcasses, carcasses that were prepared, buried, and subsequently guarded by mature breeding pairs of beetles exhibited the greatest inhibition of fungal growth. No significant difference in fungistasis was observed between the 3.5？g and the 18 to 22？g guarded carcasses. We used the growth of the predominant species of fungi on the control carcasses, Trichoderma sp., as a biological indicator to examine differences in the fungistatic efficiency of anal secretions between sexually mature and immature adults and between genders. The anal secretions of sexually mature beetles inhibited the growth of Trichoderma sp., whereas the secretions of immature beetles did not. The secretions of sexually mature females displayed significantly greater inhibition of the growth of Trichoderma sp. than those of sexually mature males, possibly reflecting a division of labor in burying beetle reproduction. 1. Introduction Burying beetles (Nicrophorus spp.) use small vertebrate carcasses as food for their larval broods by depositing their eggs around a buried carcass [1, 2]. Carcasses are nutritious yet rare resources [3, 4]. During the lifetime of a beetle, it may find only one carcass that is suitable for reproduction [5]. Competition for carcasses is intense [6–8], and burying beetles of the same or different species may fight to maintain occupancy of the carcass [1, 9–11]. Bacterial and fungal decomposers destroy carcasses, and scavenging animals have evolved behavioral and physiological counterstrategies to maintain food sources [12]. Before burying a carcass, the burying beetles remove the fur or feathers from the carcass, compact the carcass by rolling it repeatedly, and smear its surface with their anal secretions [1]. Carcasses used by beetles typically vary in size from 1 to 75？g [9, 10, 13] and are encountered in variable states of decay. Burying beetles exhibit adaptive strategies that enable them to manage the carrion resources in such diverse conditions, such as adjusting the number of eggs laid [13, 14] and practicing infanticide [15, 16], with the number of surviving larvae positively correlated with
References
[1]
E. Pukowski, “？kologische untersuchungen an Necrophorus F,” Zeitschrift für Morphologie und ？kologie der Tiere, vol. 27, no. 3, pp. 518–586, 1933.
[2]
S. B. Peck, “Nicrophorus (Silphidae) can use large carcasses for reproduction (Coleoptera),” The Coleopterists Bulletin, pp. 40–44, 1986.
[3]
E. O. Wilson, The Insect Societies, Belknap Press, Cambridge, UK, 1971.
[4]
I. Hanski and Y. Cambefort, Dung Beetle Ecology, Princeton University Press, Princeton, NJ, USA, 1991.
[5]
M. P. Scott and D. S. Gladstein, “Calculating males? An empirical and theoretical examination of the duration of paternal care in burying beetles,” Evolutionary Ecology, vol. 7, no. 4, pp. 362–378, 1993.
[6]
D. S. Wilson and J. Fudge, “Burying beetles: intraspecific interactions and reproductive success in the field,” Ecological Entomology, vol. 9, no. 2, pp. 195–203, 1984.
[7]
D. S. Wilson, W. G. Knollenberg, and J. Fudge, “Species packing and temperature dependent competition among burying beetles (Silphidae, Nicrophorus),” Ecological Entomology, vol. 9, no. 2, pp. 205–216, 1984.
[8]
S. T. Trumbo, “Interference competition among burying beetles (Silphidae, Nicrophorus),” Ecological Entomology, vol. 15, no. 3, pp. 347–355, 1990.
[9]
J. Bartlett and C. M. Ashworth, “Brood size and fitness in Nicrophorus vespilloides (Coleoptera: Silphidae),” Behavioral Ecology and Sociobiology, vol. 22, no. 6, pp. 429–434, 1988.
[10]
M. Otronen, “The effect of body size on the outcome of fights in burying beetles (Nicrophorus),” Annales Zoologici Fennici, vol. 25, no. 2, pp. 191–201, 1988.
[11]
J. K. Müller, A. K. Eggert, and E. Furlkr？ger, “Clutch size regulation in the burying beetle Necrophorus vespilloides Herbst (Coleoptera: Silphidae),” Journal of Insect Behavior, vol. 3, no. 2, pp. 265–270, 1990.
[12]
D. H. Janzen, “Why fruits rot, seeds mold, and meat spoils,” The American Naturalist, vol. 111, no. 980, pp. 691–713, 1977.
[13]
J. K. Müller, A. K. Eggert, and J. Dressel, “Intraspecific brood parasitism in the burying beetle, Necrophorus vespilloides (Coleoptera: Silphidae),” Animal Behaviour, vol. 40, no. 3, pp. 491–499, 1990.
[14]
J. K. Müller, “Replacement of a lost clutch: a strategy for optimal resource utilization in Necrophorus vespilloides (Coleoptera: Silphidae),” Ethology, vol. 76, pp. 74–80, 1987.
[15]
J. Bartlett, “Filial cannibalism in burying beetles,” Behavioral Ecology and Sociobiology, vol. 21, no. 3, pp. 179–183, 1987.
[16]
J. K. Müller and A. K. Eggert, “Time-dependent shifts between infanticidal and parental behavior in female burying beetles a mechanism of indirect mother-offspring recognition,” Behavioral Ecology and Sociobiology, vol. 27, no. 1, pp. 11–16, 1990.
[17]
C. W. Beninger and S. B. Peck, “Temporal and spatial patterns of resource use among Nicrophorus carrion beetles (Coleoptera: Silphidae) in a Sphagnum bog and adjacent forest near Ottawa, Canada,” Canadian Entomologist, vol. 124, no. 1, pp. 79–86, 1992.
[18]
T. N. Sherratt, D. M. Wilkinson, and R. S. Bain, “Why fruits rot, seeds mold and meat spoils: a reappraisal,” Ecological Modelling, vol. 192, no. 3-4, pp. 618–626, 2006.
[19]
D. E. Rozen, D. J. P. Engelmoer, and P. T. Smiseth, “Antimicrobial strategies in burying beetles breeding on carrion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 46, pp. 17890–17895, 2008.
[20]
C. L. Hall, N. K. Wadsworth, D. R. Howard et al., “Inhibition of microorganisms on a carrion breeding resource: the antimicrobial peptide activity of burying beetle (Coleoptera: Silphidae) oral and anal secretions,” Environmental Entomology, vol. 40, no. 3, pp. 669–678, 2011.
[21]
W. W. Hoback, A. A. Bishop, J. Kroemer, J. Scalzitti, and J. J. Shaffer, “Differences among antimicrobial properties of carrion beetle secretions reflect phylogeny and ecology,” Journal of Chemical Ecology, vol. 30, no. 4, pp. 719–729, 2004.
[22]
R. L. Rana, W. Wyatt Hoback, N. A. A. Rahim, J. Bedick, and D. W. Stanley, “Pre-oral digestion: a phospholipase A2 associated with oral secretions in adult burying beetles, Nicrophorus marginatus,” Comparative Biochemistry and Physiology B, vol. 118, no. 2, pp. 375–380, 1997.
[23]
S. Suzuki, “Suppression of fungal development on carcasses by the burying beetle Nicrophorus quadripunctatus (Coleoptera: Silphidae),” Entomological Science, vol. 4, no. 4, pp. 403–405, 2001.
[24]
B. J. Jacques, S. Akahane, M. Abe, W. Middleton, W. W. Hoback, and J. J. Shaffer, “Temperature and food availability differentially affect the production of antimicrobial compounds in oral secretions produced by two species of burying beetle,” Journal of chemical ecology, vol. 35, no. 8, pp. 871–877, 2009.
[25]
S. C. Cotter and R. M. Kilner, “Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides,” Journal of Animal Ecology, vol. 79, no. 1, pp. 35–43, 2010.
[26]
W. Hwang and S. F. Shiao, “Use of carcass by burying beetles Nicrophorus nepalensis Hope (Coleoptera: Silphidae),” Formosan Entomologist, vol. 28, no. 2, pp. 87–100, 2008.
[27]
M. P. Scott, “The ecology and behavior of burying beetles,” Annual Review of Entomology, vol. 43, pp. 595–618, 1998.
[28]
A.-K. Eggert and J. K. Müller, “Joint breeding in female burying beetles,” Behavioral Ecology and Sociobiology, vol. 31, no. 4, pp. 237–242, 1992.
[29]
S. T. Trumbo, “Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus),” Ecological Entomology, vol. 17, no. 3, pp. 289–298, 1992.
[30]
M. P. Scott, “Competition with flies promotes communal breeding in the burying beetle, Nicrophorus tomentosus,” Behavioral Ecology and Sociobiology, vol. 34, no. 5, pp. 367–373, 1994.
[31]
M. P. Scott, W. J. Lee, and E. D. Van Der Reijden, “The frequency and fitness consequences of communal breeding in a natural population of burying beetles: a test of reproductive skew,” Ecological Entomology, vol. 32, no. 6, pp. 651–661, 2007.
[32]
M. P. Scott, “The benefit of paternal assistance in intra- and interspecific competition for the burying beetle, Nicrophorus defodiens,” Ethology Ecology and Evolution, vol. 6, no. 4, pp. 537–543, 1994.
[33]
J. K. Müller, A. K. Eggert, and S. K. Sakaluk, “Carcass maintenance and biparental brood care in burying beetles: are males redundant?” Ecological Entomology, vol. 23, no. 2, pp. 195–200, 1998.
[34]
G. S. Halffter, C. Huerta, and A. Huerta, “Nidification des Nicrophorus (Col. Silphidae),” Bulletin de la Société Entomologique de France, vol. 88, pp. 648–666, 1983.
[35]
J. Bartlett, “Male mating success and paternal care in Nicrophorus vespilloides (Coleoptera: Silphidae),” Behavioral Ecology and Sociobiology, vol. 23, no. 5, pp. 297–303, 1988.
[36]
S. T. Trumbo, “Reproductive benefits and the duration of paternal care in a biparental burying beetle, Necrophorus orbicollis,” Behaviour, vol. 117, no. 1-2, pp. 82–105, 1991.
[37]
I. C. Robertson, “Nest intrusions, infanticide, and parental care in the burying beetle, Nicrophorus orbicollis (Coleoptera: Silphidae),” Journal of Zoology, vol. 231, no. 4, pp. 583–593, 1993.
[38]
S. T. Trumbo, “Interspecific competition, brood parasitism, and the evolution of biparental cooperation in burying beetles,” Oikos, vol. 69, no. 2, pp. 241–249, 1994.
[39]
I. A. Fetherston, M. P. Scott, and J. F. A. Traniello, “Behavioural compensation for mate loss in the burying beetle Nicrophorus orbicollis,” Animal Behaviour, vol. 47, no. 4, pp. 777–785, 1994.
[40]
D. O. Carter, D. Yellowlees, and M. Tibbett, “Cadaver decomposition in terrestrial ecosystems,” Naturwissenschaften, vol. 94, no. 1, pp. 12–24, 2007.
[41]
L. J. Milne and M. J. Milne, “The social behavior of the burying beetles,” Scientific American, vol. 235, pp. 84–89, 1976.
[42]
D. H. Larone, Medically Important Fungi: A Guide to Identification, ASM Press, Washington, DC, USA, 4th edition, 2002.
[43]
C. M. S. Kumar, K. Jeyaram, and H. B. Singh, “First record of the entomopathogenic fungus Entomophaga aulicae on the Bihar hairy caterpillar Spilarctia obliqua in Manipur, India,” Phytoparasitica, vol. 39, no. 1, pp. 67–71, 2011.
[44]
C. Nielsen and A. E. Hajek, “Diurnal pattern of death and sporulation in Entomophaga maimaiga-infected Lymantria dispar,” Entomologia Experimentalis et Applicata, vol. 118, no. 3, pp. 237–243, 2006.
[45]
X. L. Wang and Y. J. Yao, “Host insect species of ophiocordyceps sinensis: a review,” ZooKeys, vol. 127, pp. 43–59, 2011.
[46]
A. Hagn, K. Pritsch, M. Schloter, and J. C. Munch, “Fungal diversity in agricultural soil under different farming management systems, with special reference to biocontrol strains of Trichoderma spp.,” Biology and Fertility of Soils, vol. 38, no. 4, pp. 236–244, 2003.
[47]
D. J. Roiger, S. N. Jeffers, and R. W. Caldwell, “Occurrence of Trichoderma species in apple orchard and woodland soils,” Soil Biology and Biochemistry, vol. 23, no. 4, pp. 353–359, 1991.
[48]
T. Degenkolb, R. A. Düring, and A. Vilcinskas, “Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions,” Journal of Chemical Ecology, vol. 37, no. 7, pp. 724–735, 2011.
[49]
S. T. Trumbo, “Defending young biparentally: female risk-taking with and without a male in the burying beetle, Nicrophorus pustulatus,” Behavioral Ecology and Sociobiology, vol. 61, no. 11, pp. 1717–1723, 2007.
[50]
I. A. Fetherston, M. P. Scott, and J. F. A. Traniello, “Parental care in burying beetles: the organization of male and female brood-care behavior,” Ethology, vol. 95, no. 3, pp. 179–190, 1990.
[51]
E. V. Jenkins, C. Morris, and S. Blackman, “Delayed benefits of paternal care in the burying beetle Nicrophorus vespilloides,” Animal Behaviour, vol. 60, no. 4, pp. 443–451, 2000.
[52]
P. T. Smiseth and A. J. Moore, “Behavioral dynamics between caring males and females in a beetle with facultative biparental care,” Behavioral Ecology, vol. 15, no. 4, pp. 621–628, 2004.
[53]
P. T. Smiseth, C. Dawson, E. Varley, and A. J. Moore, “How do caring parents respond to mate loss? Differential response by males and females,” Animal Behaviour, vol. 69, no. 3, pp. 551–559, 2005.
