From the host's point of view: Effects of variation in burying beetle brood care and brood size on the interaction with parasitic mites

Autoři: Petra Schedwill aff001;  Sophia Paschkewitz aff001;  Heide Teubner aff001;  Nadine Steinmetz aff001;  Volker Nehring aff001
Působiště autorů: Evolutionary Biology & Ecology, Institute of Biology I, University of Freiburg, Freiburg, Germany aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


The fitness and virulence of parasites is often determined by how many resources they can wrangle out of their hosts. Host defenses that help to keep resources from the parasites will then reduce virulence and parasite fitness. Here, we study whether host brood care and brood size regulation can protect host fitness and harm a parasite. We use the biparental brood-caring burying beetle Nicrophorus vespilloides and its phoretic Poecilochirus carabi mites as a model. Since paternal brood care does not seem to benefit the offspring in a clean laboratory setting, the male presence has been suggested to strengthen the defense against parasites. We manipulated male presence and found no effect on the fitness of the parasitic mites or the beetle offspring. We further manipulated beetle brood size and found larger broods to reduce parasite fitness. The specific pattern we observed suggests that beetle larvae are strong competitors and consume the carrion resource before all parasites develop. They thus starve the parasites. These results shed new light on the observation that the parasites appear to reduce host brood size early on–potentially to avert later competition their offspring might have to face.

Klíčová slova:

Beetles – Host-pathogen interactions – Larvae – Mites – Parasitic diseases – Parasitism – Predation – Pupae


1. Ebert D, Joachim Carius H, Little T, Decaestecker E. The evolution of virulence when parasites cause host castration and gigantism. Am Nat. 2004;164: S19–S32. doi: 10.1086/424606 15540139

2. Forbes MR. Parasitism and host reproductive effort. Nord Soc Oikos. 1993;67: 444–450.

3. Clutton-Brock TH. The evolution of parental care. Princton University Press. 1991.

4. Wilson EO. Parental Care. Sociobiology. 25th ed. Harvard University Press; 2000. pp. 336–352.

5. Davies NB, Krebs JR, West SA. An introduction to Behavioural Ecology. 4th ed. John Wiley & Sons. Oxford, U.K.; 2012.

6. Maynard-Smith J. Parental investment: A prospective analysis. Anim Behav. 1977;25: 1–9. doi: 10.1016/0003-3472(77)90062-8

7. Lyon BE, Montgomerie RD, Hamilton LD. Male parental care and monogamy in snow buntings. Behav Ecol Sociobiol. 1987;20: 377–382. doi: 10.1007/BF00300684

8. Bart J, Tornes A. Importance of monogamous male birds in determining reproductive success—Evidence for house wrens and a review of male-removal studies. Behav Ecol Sociobiol. 1989;24: 109–116. doi: 10.1007/BF00299642

9. Scott MP. Brood guarding and the evolution of male parental care in burying beetles. Behav Ecol Sociobiol. 1990;26: 31–39. doi: 10.1007/BF00174022

10. Blackman SW. The ecology of parental care in the burying beetle Nicrophorus vespilloides Herbst. PhD Thesis, University of Edinburgh. 1995.

11. Moreno J, Veiga JP, Cordero PJ, Minguez E. Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor. Behav Ecol Sociobiol. 1999;47: 47–53.

12. Parker DJ, Cunningham CB, Walling CA, Stamper CE, Head ML, Roy-Zokan EM, et al. Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle. Nat Commun. Nature Publishing Group; 2015;6. doi: 10.1038/ncomms9449 26416581

13. Scott MP. The ecology and behavior of burying beetles. Annu Rev Entomol. 1998;43: 595–618. doi: 10.1146/annurev.ento.43.1.595 15012399

14. Eggert A-K, Müller JK. Biparental care and social evolution in burying beetles: lessons from the larder. In: Choe JC, Crespi BJ, editors. The Evolution of Social Behavior in Insects and Arachnids. Cambridge: Cambridge University Press; 1997. pp. 216–236.

15. Pukowski E. Oekologische Untersuchungen an Necrophorus F. Zeitschrift fuer Morphol und Oekologie der Tiere. 1933;27: 518–586. German. doi: 10.1007/BF00403155

16. Otronen M. The effect of body size on the outcome of fights in burying beetles (Nicrophorus). Ann Zool Fennici. 1988;25: 191–201.

17. Müller JK, Eggert AK, Dressel J. Intraspecific brood parasitism in the burying beetle, Necrophorus vespilloides (Coleoptera: Silphidae). Anim Behav. 1990;40: 491–499. doi: 10.1016/S0003-3472(05)80529-9

18. Bartlett J. Filial cannibalism in burying beetles. Behav Ecol Sociobiol. 1987;21: 179–183. doi: 10.1007/BF00303208

19. Bartlett J, Ashworth CM. Brood size and fitness in Nicrophorus vespilloides (Coleoptera: Silphidae). Behav Ecol Sociobiol. 1988;22: 429–434.

20. Müller Josef K., Eggert AK., Furlkröger E. Clutch size regulation in the burying beetle Necrophorus vespilloides Herbst (Coleoptera: Silphidae). J Insect Behav. 1990;3: 265–270.

21. Smiseth PT, Lennox L, Moore AJ. Interaction between parental care and sibling competition: Parents enhance offspring growth and exacerbate sibling competition. Evolution (N Y). 2007;61: 2331–2339. doi: 10.1111/j.1558-5646.2007.00192.x 17711464

22. Eggert A-K, Reinking M, Müller JK. Parental care improves offspring survival and growth in burying beetles. Anim Behav. 1998;55: 97–107. doi: 10.1006/anbe.1997.0588 9480676

23. Bartlett J. Male mating success and paternal care in Nicrophorus vespilloides (Coleoptera: Silphidae). Behav Ecol Sociobiol. 1988;23: 297–303.

24. Müller JK, Eggert AK, Sakaluk SK. Carcass maintenance and biparental brood care in burying beetles: Are males redundant? Ecol Entomol. 1998;23: 195–200. doi: 10.1046/j.1365-2311.1998.00119.x

25. Keppner EM, Ayasse M, Steiger S. Manipulation of parental nutritional condition reveals competition among family members. J Evol Biol. 2018;31: 822–832. doi: 10.1111/jeb.13266 29573021

26. Pilakouta N, Richardson J, Smiseth PT. State-dependent cooperation in burying beetles: Parents adjust their contribution towards care based on both their own and their partner’s size. J Evol Biol. 2015;28: 1965–1974. doi: 10.1111/jeb.12712 26245748

27. Pilakouta N, Hanlon EJH, Smiseth PT. Biparental care is more than the sum of its parts: Experimental evidence for synergistic effects on offspring fitness. Proc R Soc B Biol Sci. 2018;285: 1–7. doi: 10.1098/rspb.2018.0875 30068674

28. Pilakouta N, Richardson J, Smiseth PT. If you eat, I eat: Resolution of sexual conflict over consumption from a shared resource. Anim Behav. Elsevier Ltd; 2016;111: 175–180. doi: 10.1016/j.anbehav.2015.10.016

29. Boncoraglio G, Kilner RM. Female burying beetles benefit from male desertion: Sexual conflict and counter-adaptation over parental investment. PLoS One. 2012;7. doi: 10.1371/journal.pone.0031713 22355390

30. De Gasperin O De, Kilner RM. Interspecific Interactions and the Scope for Parent-Offspring Conflict: High Mite Density Temporarily Changes the Trade-Off between Offspring Size and Number in the Burying Beetle, Nicrophorus vespilloides. 2016; 1–18. doi: 10.1371/journal.pone.0150969 26985819

31. Trivers RL. Parent-offspring conflict. Am Zool. 1974;14: 249–264.

32. Ward RJS, Cotter SC, Kilner RM. Current brood size and residual reproductive value predict offspring desertion in the burying beetle Nicrophorus vespilloides. Behav Ecol. 2009;20: 1274–1281. doi: 10.1093/beheco/arp132

33. Springett BP. Aspects of the Relationship Between Burying Beetles, Necrophorus Spp. and the Mite, Poecilochirus necrophori Vitz. Br Ecol Soc. 1968;37: 417–424.

34. Wilson DS, Knollenberg WG. Adaptive indirect effects: the fitness of burying beetles with and without their phoretic mites. Evol Ecol. 1987;1: 139–159. doi: 10.1007/BF02067397

35. Sun S, Kilner RM. Mutualistic interactions with phoretic mites Poecilochirus carabi expand the realised thermal niche of the burying beetle Nicrophorus vespilloides. bioRxiv. 2019; 590125.

36. De Gasperin O, Kilner RM. Interspecific interactions change the outcome of sexual conflict over prehatching parental investment in the burying beetle Nicrophorus vespilloides. Ecol Evol. 2015;5: 5552–5560. doi: 10.1002/ece3.1795 27069605

37. Beninger C. Egg predation by Poecilochirus carabi (Mesostigmata, Parasitidae) and its effect on reproduction of Nicrophorus vespilloides (Coleoptera, Silphidae). Environ Entomol. 1993;22: 766–769. doi: 10.1093/ee/22.4.766

38. Blackman SW, Evans GO. Observations on a mite (Poecilochirus davydovae) predatory on the eggs of burying beetles (Nicrophorus vespilloides) with a review of its taxonomic status. J Zool. 1994;234: 217–227.

39. De Gasperin O, Duarte A, Kilner RM. Interspecific interactions explain variation in the duration of paternal care in the burying beetle. Anim Behav. Elsevier Ltd; 2015;109: 199–207. doi: 10.1016/j.anbehav.2015.08.014 26778845

40. De Gasperin O, Kilner RM. Friend or foe: inter-specific interactions and conflicts of interest within the family. Ecol Entomol. 2015;40: 787–795. doi: 10.1111/een.12259 26681822

41. Nehring V, Müller JK, Steinmetz N. Phoretic Poecilochirus mites specialize on their burying beetle hosts. Ecol Evol. 2017;00: 1–9. doi: 10.1002/ece3.3591 29299254

42. Nehring V, Teubner H, König S. Dose-independent virulence in phoretic mites that parasitize burying beetles. Int J Parasitol. 2019;49: 759–767. doi: 10.1016/j.ijpara.2019.05.011 31401062

43. Pike VL, Lythgoe KA, King KC. On the diverse and opposing effects of nutrition on pathogen virulence. Proc B. 2019;286: 1–8.

44. Hall SR, Simonis JL, Nisbet RM, Tessier AJ, Cáceres CE. Resource ecology of virulence in a planktonic host-parasite system: An explanation using dynamic energy budgets. Am Nat. 2009;174: 149–162. doi: 10.1086/600086 19527119

45. Korn W. Zur Vergesellschaftung der Gamasidenarten Poecilochirus carabi G. u. R. Canestrini 1882 (= P. necrophori Vitzthum 1930), P. austroasiaticus Vitzthum 1930 und P. subterraneus Müller 1859 mit Aaskäfern aus der Familie der Silphidae. Spixiana. 1983. pp. 251–279.

46. Schwarz HH, Starrach M, Koulianos S. Host specificity and permanence of associations between mesostigmatic mites (Acari: Anactinotrichida) and burying beetles (Coleoptera: Silphidae: Nicrophorus). J Nat Hist. 1998;32: 159–172.

47. Fox J, Weisberg S. An {R} Companion to Applied Regression [Internet]. 3rd ed. Thousand Oaks CA: Sage; 2019. Available:

48. Scott MP. Male parental care and reproductive success in the burying beetle, Nicrophorus orbicollis. J Insect Behav. 1989;2: 133–137. doi: 10.1007/BF01053623

49. Schwarz HH, Müller JK. The dispersal behavior of the phoretic mite Poecilochirus carabi (Mesostigmata, Parasitidae): adaptation to the breeding biology of its carrier Necrophorus vespilloides (Coleoptera, Silphidae). Oecologia. 1992;89: 487–493. doi: 10.1007/BF00317154 28311878

50. Schwarz HH, Koulianos S. When to leave the brood chamber? Routes of dispersal in mites associated with burying beetles. Exp Appl Acarol. 1998;22: 621–631. doi: 10.1023/A:1006054604520

Článek vyšel v časopise


2020 Číslo 1
Nejčtenější tento týden