Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1789, 2014, Pages

  Fischer, Stefan ^a   Zöttl, Markus ^a,b   Groenewoud, Frank ^a,c   Taborsky, Barbara ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Cichlids; Conflict; Cooperation; Eviction; Helping; Territory defence

Indexed keywords

ADAPTATION; CICHLID; COGNITION; COOPERATIVE BREEDING; GROUP BEHAVIOR; GROUP SIZE; LAKE ECOSYSTEM;

AGGRESSION; ANIMAL; CICHLID; COOPERATION; FEMALE; MALE; PHYSIOLOGY; POPULATION DENSITY; PUNISHMENT; REPRODUCTION; SOCIAL BEHAVIOR; SOCIAL DOMINANCE;

AGGRESSION; ANIMALS; CICHLIDS; FEMALE; HELPING BEHAVIOR; MALE; PHYSIOLOGY; POPULATION DENSITY; PUNISHMENT; REPRODUCTION; SOCIAL BEHAVIOR; SOCIAL DOMINANCE;

EID: 84903719027     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0184     Document Type: Article

References (76)

1. Bergmüller R, Johnstone RA, Russell AF, Bshary R. 2007 Integrating cooperative breeding into theoretical concepts of cooperation. Behav. Process. 76, 61-72. (doi:10.1016/j.beproc.2007. 07.001)
2. Lehmann L, Keller L. 2006 The evolution of cooperation and altruism-a general framework and a classification of models. J. Evol. Biol. 19, 1365-1376. (doi:10.1111/j.1420-9101.2006. 01119.x)
3. Hamilton WD. 1964 The genetical evolution of social behaviour I. J. Theor. Biol. 7, 1-16. (doi:10. 1016/0022-5193(64)90038-4)
4. Hamilton WD. 1964 The genetical evolution of social behaviour II. J. Theor. Biol. 7, 17-52. (doi:10. 1016/0022-5193(64)90039-6)
5. Woolfenden GE. 1975 Florida scrub jay helpers at nest. Auk 92, 1-15. (doi:10.2307/4084414)
6. Kokko H, Johnstone RA, Clutton-Brock TH. 2001 The evolution of cooperative breeding through group augmentation. Proc. R. Soc. Lond. B 268, 187-196. (doi:10.1098/rspb.2000.1349)
7. Brown JL, Brown ER. 1984 Parental facilitation: parent-offspring relations in communally breeding birds. Behav. Ecol. Sociobiol. 14, 203-209. (doi:10. 1007/bf00299620)
8. Komdeur J. 1996 Influence of helping and breeding experience on reproductive performance in the Seychelles warbler: a translocation experiment. Behav. Ecol. 7, 326-333. (doi:10.1093/beheco/ 7.4.417)
9. Zahavi A. 1974 Communal nesting by Arabian babbler: a case of individual selection. Ibis 116, 84-87. (doi:10.1111/j.1474-919X.1974.tb00225.x)
10. Gaston AJ. 1978 The evolution of group territorial behavior and cooperative breeding. Am. Nat. 112, 1091-1100. (doi:10.1086/283348)
11. Kokko H, Johnstone RA, Wright J. 2002 The evolution of parental and alloparental effort in cooperatively breeding groups: when should helpers pay to stay? Behav. Ecol. 13, 291-300. (doi:10. 1093/beheco/13.3.291)
12. Hamilton IM, Taborsky M. 2005 Unrelated helpers will not fully compensate for costs imposed on breeders when they pay to stay. Proc. R. Soc. B 272, 445-454. (doi:10.1098/rspb.2004.2961)
13. Mulder RA, Langmore NE. 1993 Dominant males punish helpers for temporary defection in superb fairy-wrens. Anim. Behav. 45, 830-833. (doi:10. 1006/anbe.1993.1100)
14. Zöttl M, Fischer S, Taborsky M. 2013 Partial brood care compensation by female breeders in response to experimental manipulation of alloparental care. Anim. Behav. 85, 1471-1478. (doi:10.1016/j. anbehav.2013.03.045)
15. Bergmüller R, Taborsky M. 2005 Experimental manipulation of helping in a cooperative breeder: helpers 'pay to stay' by pre-emptive appeasement. Anim. Behav. 69, 19-28. (doi:10.1016/j.anbehav. 2004.05.009)
16. Mitchell JS. 2003 Social correlates of reproductive success in false clown anemonefish: subordinate group members do not pay-to-stay. Evol. Ecol. Res. 5, 89-104.
17. Balshine-Earn S, Neat FC, Reid H, Taborsky M. 1998 Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav. Ecol. 9, 432-438. (doi:10.1093/beheco/9.5.432)
18. Taborsky M. 1985 Breeder-helper conflict in a cichlid fish with broodcare helpers: an experimental analysis. Behaviour 95, 45-75. (doi:10.1163/ 156853985x00046)
19. Bergmüller R, Heg D, Taborsky M. 2005 Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. Proc. R. Soc. B 272, 325-331. (doi:10. 1098/rspb.2004.2960)
20. Bruintjes R, Taborsky M. 2008 Helpers in a cooperative breeder pay a high price to stay: effects of demand, helper size and sex. Anim. Behav. 75, 1843-1850. (doi:10.1016/j.anbehav.2007.12.004)
21. Heg D, Taborsky M. 2010 Helper response to experimentally manipulated predation risk in the cooperatively breeding cichlid Neolamprologus pulcher. PLoS ONE 5, e10784. (doi:10.1371/journal. pone.0010784)
22. MacLeod KJ, Nielsen JF, Clutton-Brock TH. 2013 Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat. Anim. Behav. 86, 1059-1067. (doi:10.1016/j.anbehav.2013.09.012)
23. Taborsky M. 1984 Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim. Behav. 32, 1236-1252. (doi:10.1016/s0003-3472(84)80241-9)
24. Zöttl M, Heg D, Chervet N, Taborsky M. 2013 Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay. Nat. Commun. 4, 1341. (doi:10.1038/ncomms2344)
25. Stiver KA, Dierkes P, Taborsky M, Gibbs HL, Balshine S. 2005 Relatedness and helping in fish: examining the theoretical predictions. Proc. R. Soc. B 272, 1593-1599. (doi:10.1098/rspb.2005.3123)
26. Zöttl M, Frommen JG, Taborsky M. 2013 Group size adjustment to ecological demand in a cooperative breeder. Proc. R. Soc. B 280, 20122772. (doi:10. 1098/rspb.2012.2772)
27. Zöttl M, Chapuis L, Freiburghaus M, Taborsky M. 2013 Strategic reduction of help before dispersal in a cooperative breeder. Biol. Lett. 9, 20120878. (doi:10.1098/rsbl.2012.0878)
28. Koenig WD, Walters EL. 2011 Age-related provisioning behaviour in the cooperatively breeding acorn woodpecker: testing the skills and the pay-tostay hypotheses. Anim. Behav. 82, 437-444. (doi:10.1016/j.anbehav.2011.05.028)
29. Reeve HK. 1992 Queen activation of lazy workers in colonies of the eusocial naked mole-rat. Nature 358, 147-149. (doi:10.1038/358147a0)
30. Cant MA. 2011 The role of threats in animal cooperation. Proc. R. Soc. B 278, 170-178. (doi:10. 1098/rspb.2010.1241)
31. Raihani NJ, Thornton A, Bshary R. 2012 Punishment and cooperation in nature. Trends Ecol. Evol. 27, 288-295. (doi:10.1016/j.tree.2011.12.004)
32. Wong M, Balshine S. 2011 The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. Biol. Rev. 86, 511-530. (doi:10.1111/j.1469-185X.2010.00158.x)
33. Taborsky M, Limberger D. 1981 Helpers in fish. Behav. Ecol. Sociobiol. 8, 143-145. (doi:10.1007/ bf00300826)
34. Dierkes P, Heg D, Taborsky M, Skubic E, Achmann R. 2005 Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol. Lett. 8, 968-975. (doi:10. 1111/j.1461-0248.2005.00801.x)
35. Heg D, Brouwer L, Bachar Z, Taborsky M. 2005 Large group size yields group stability in the cooperatively breeding cichlid Neolamprologus pulcher. Behaviour 142, 1615-1641. (doi:10.1163/ 156853905774831891)
36. Balshine S, Leach B, Neat F, Reid H, Taborsky M, Werner N. 2001 Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav. Ecol. Sociobiol. 50, 134-140. (doi:10.1007/s002650100343)
37. Cant MA, Hodge SJ, Bell MBV, Gilchrist JS, Nichols HJ. 2010 Reproductive control via eviction (but not the threat of eviction) in banded mongooses. Proc. R. Soc. B 277, 2219-2226. (doi:10.1098/rspb. 2009.2097)
38. Clutton-Brock TH, Brotherton PN, Smith R, McIlrath GM, Kansky R, Gaynor D, O'Riain MJ, Skinner JD. 1998 Infanticide and expulsion of females in a cooperative mammal. Proc. R. Soc. Lond. B 265, 2291-2295. (doi:10.1098/rspb.1998.0573)
39. Mulder RA. 1995 Natal and breeding dispersal in a cooperative, extra-group-mating bird. J. Avian Biol. 26, 234-240. (doi:10.2307/3677324)
40. Johnstone RA, Cant MA. 1999 Reproductive skew and the threat of eviction: a new perspective. Proc. R. Soc. Lond. B 266, 275-279. (doi:10.1098/ rspb.1999.0633)
41. Bruintjes R, Bonfils D, Heg D, Taborsky M. 2011 Paternity of subordinates raises cooperative effort in cichlids. PLoS ONE 6, e25673. (doi:10.1371/journal. pone.0025673)
42. Heg D, Hamilton IM. 2008 Tug-of-war over reproduction in a cooperatively breeding cichlid. Behav. Ecol. Sociobiol. 62, 1249-1257. (doi:10. 1007/s00265-008-0553-0)
43. Heg D, Jutzeler E, Bonfils D, Mitchell JS. 2008 Group composition affects male reproductive partitioning in a cooperatively breeding cichlid. Mol. Ecol. 17, 4359-4370. (doi:10.1111/j.1365-294X.2008. 03920.x)
44. Heg D, Bergmüller R, Bonfils D, Otti O, Bachar Z, Burri R, Heckel G, Taborsky M. 2006 Cichlids do not adjust reproductive skew to the availability of independent breeding options. Behav. Ecol. 17, 419-429. (doi:10.1093/beheco/arj056)
45. Dierkes P, Taborsky M, Kohler U. 1999 Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behav. Ecol. 10, 510-515. (doi:10. 1093/beheco/10.5.510)
46. Doerr ED, Doerr VAJ. 2007 Positive effects of helpers on reproductive success in the brown treecreeper and the general importance of future benefits. J. Anim. Ecol. 76, 966-976. (doi:10.1111/j.1365-2656.2007.01280.x)
47. Clutton-Brock TH, Hodge SJ, Flower TP. 2008 Group size and the suppression of subordinate reproduction in Kalahari meerkats. Anim. Behav. 76, 689-700. (doi:10.1016/j.anbehav.2008.03.015)
48. Field J, Cant MA. 2009 Social stability and helping in small animal societies. Phil. Trans. R. Soc. B 364, 3181-3189. (doi:10.1098/rstb.2009.0110)
49. Duftner N, Sefc KM, Koblmüller S, Salzburger W, Taborsky M, Sturmbauer C. 2007 Parallel evolution of facial stripe patterns in the Neolamprologus brichardi/pulcher species complex endemic to Lake Tanganyika. Mol. Phylogenet. Evol. 45, 706-715. (doi:10.1016/j.ympev.2007.08.001)
50. Limberger D. 1983 Pairs and harems in a cichlid fish, Lamprologus brichardi. J. Comp. Ethol. 62, 115-144.
51. Heg D, Bachar Z, Brouwer L, Taborsky M. 2004 Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. Proc. R. Soc. Lond. B 271, 2367-2374. (doi:10. 1098/rspb.2004.2855)
52. Bruintjes R, Taborsky M. 2011 Size-dependent task specialization in a cooperative cichlid in response to experimental variation of demand. Anim. Behav. 81, 387-394. (doi:10.1016/j.anbehav.2010.10.004)
53. Bruintjes R, Hekman R, Taborsky M. 2010 Experimental global food reduction raises resource acquisition costs of brood care helpers and reduces their helping effort. Funct. Ecol. 24, 1054-1063. (doi:10.1111/j.1365-2435.2010.01715.x)
54. Taborsky M. 1982 Brutpflegehelfer beim Cichliden Lamprologus brichardi, Poll (1974): Eine Kosten/ Nutzen Analyse. Dissertation, University of Vienna, Austria.
55. Hamilton IM, Heg D, Bender N. 2005 Size differences within a dominance hierarchy influence conflict and help in a cooperatively breeding cichlid. Behaviour 142, 1591-1613. (doi:10.1163/ 156853905774831846)
56. Reddon AR, O'Connor CM, Marsh-Rollo SE, Balshine S. 2012 Effects of isotocin on social responses in a cooperatively breeding fish. Anim. Behav. 84, 753-760. (doi:10.1016/j.anbehav.2012.07.021)
57. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White JS. 2009 Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127-135. (doi:10.1016/j.tree.2008.10.008)
58. Engqvist L. 2005 The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 70, 967-971. (doi:10.1016/j.anbehav.2005. 01.016)
59. R Core Development Team. 2013 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
60. Bates D, Maechler M, Bolker B. 2013 lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-2. See http://cran.r-project.org/ web/packages/Ime4/index.html.
61. McDonald PG, Kazem AJN, Wright J. 2009 Cooperative provisioning dynamics: fathers and unrelated helpers show similar responses to manipulations of begging. Anim. Behav. 77, 369-376. (doi:10.1016/j.anbehav.2008.10.009)
62. Bell MBV. 2007 Cooperative begging in banded mongoose pups. Curr. Biol. 17, 717-721. (doi:10. 1016/j.cub.2007.03.015)
63. Wright J, Dingemanse NJ. 1999 Parents and helpers compensate for experimental changes in the provisioning effort of others in the Arabian babbler. Anim. Behav. 58, 345-350. (doi:10.1006/anbe. 1999.1152)
64. Cant MA, Field J. 2005 Helping effort in a dominance hierarchy. Behav. Ecol. 16, 708-715. (doi:10.1093/beheco/ari051)
65. Heinsohn R, Legge S. 1999 The cost of helping. Trends Ecol. Evol. 14, 53-57. (doi:10.1016/s0169-5347(98)01545-6)
66. Hert E. 1985 Individual recognition of helpers by the breeders in the cichlid fish Lamprologus brichardi (Poll, 1974). J. Comp. Ethol. 68, 313-325.
67. Balshine-Earn S, Lotem A. 1998 Individual recognition in a cooperatively breeding cichlid: evidence from video playback experiments. Behaviour 135, 369-386. (doi:10.1163/ 156853998793066221)
68. Carpenter JP. 2007 Punishing free-riders: how group size affects mutual monitoring and the provision of public goods. Game. Econ. Behav. 60, 31-51. (doi:10.1016/j.geb.2006.08.011)
69. Boyd R, Richerson PJ. 1988 The evolution of reciprocity in sizable groups. J. Theor. Biol. 132, 337-356. (doi:10.1016/S0022-5193(88)80219-4)
70. Santema P, Clutton-Brock TH. 2012 Dominant female meerkats do not use aggression to elevate work rates of helpers in response to increased brood demand. Anim. Behav. 83, 827-832. (doi:10.1016/ j.anbehav.2011.12.032)
71. Riehl C. 2013 Evolutionary routes to non-kin cooperative breeding in birds. Proc. R. Soc. B 280, 20132245. (doi:10.1098/rspb.2013.2245)
72. Baglione V, Canestrari D, Chiarati E, Vera R, Marcos JM. 2010 Lazy group members are substitute helpers in carrion crows. Proc. R. Soc. B 277, 3275-3282. (doi:10.1098/rspb.2010.0745)
73. Clutton-Brock TH, Brotherton PN, O'Riain MJ, Griffin AS, Gaynor D, Sharpe L, Kansky R, Manser MB, McIlrath GM. 2000 Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta. Proc. R. Soc. Lond. B 267, 301-305. (doi:10.1098/rspb.2000.1000)
74. Wright J, McDonald PG, te Marvelde L, Kazem AJ, Bishop CM. 2010 Helping effort increases with relatedness in bell miners, but 'unrelated' helpers of both sexes still provide substantial care. Proc. R. Soc. B 277, 437-445. (doi:10.1098/rspb. 2009.1360)
75. Clutton-Brock TH. 2009 Cooperation between nonkin in animal societies. Nature 462, 51-57. (doi:10. 1038/nature08366)
76. Fischer S, Zöttl M, Groenewoud F, Taborsky B. 2014 Group-size dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay. Dryad Digital Repository (doi:10.5061/ dryad.s3720)