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Helpers increase food abundance in the territory of a cooperatively breeding fish

  • Hirokazu Tanaka
  • Joachim G. Frommen
  • Masanori Kohda
Original Article
Part of the following topical collections:
  1. From sensory perception to behavior

Abstract

In cooperatively breeding or eusocial animals, increasing resources such as food is a major task of brood care helpers or workers. While such food acquisition has been shown in several animal taxa, evidence is absent in fishes. Here, we provide the first evidence of increased food abundance caused by helpers in a cooperatively breeding fish. Helpers of the cichlid Neolamprologus obscurus excavate cavities by digging sand from under stones, which serve as shelter for the group members. We test whether these cavities additionally increase the abundance of benthic invertebrates in the territory. Stomach content analyses of wild-caught fish revealed that benthic invertebrates pose the main food resource of N. obscurus. Experimental assessments of daily benthic invertebrate immigration into artificial cavities demonstrate a significant increase in invertebrate prey abundance according to the size of the excavated stone area. Finally, by applying correlational and experimental approaches in the field, we show that helpers play a crucial role in the maintenance of the excavated cavities. In combination, these results demonstrate that helpers increase the abundance of benthic invertebrates inside the territory of breeders in N. obscurus. Our results provide the first evidence of increased food abundance through helpers in fishes. Such foraging system may resemble those described in other species living in highly social groups, and appears to be a ubiquitous mechanism underpinning the maintenance of complex societies in animals.

Significance statement

Evidence of elaborate food acquisition such as farming or trap building is only known from a limited number of animal taxa. The cichlid Neolamprologus obscurus is a highly social fish, where all group members create and maintain cavities under stones, which serve as shelters. These fish feed on benthic invertebrates, which hide inside such cavities during daytime. We show that the cavities of N. obscurus additionally increase the food abundance in their territory. Behavioral observation and experiment in the field revealed that group members increase the excavated cavities in their territory, and food abundance increases according to the size of excavated cavities. Our results provide the first evidence of food acquisition by group members in fishes.

Keywords

Cichlid Cooperative foraging Group living Neolamprologus obscurus Helper effect Helping behavior 

Notes

Acknowledgments

We thank all Hasli members, especially Jon Andreja Nuotclà for fruitful discussions. We also thank Tetsumi Takahashi, Masaya Morita, Kazutaka Ota, Michio Hori, and the staff of the Lake Tanganyika Research Unit, Mpulungu, Zambia, especially Harris Phiri, Danny Sinyinza, Taylor Banda, Ruben Shapola, and Henry Simpembwa for supporting our studies in the field. We appreciate Michio Hori for valuable advice on examining stomach contents of the cichlids, and Vera Schluessel and two anonymous reviewers for valuable comments on an earlier version of the manuscript. We are grateful to the organizers of the 12th Topical Meeting of the Ethological Society for encouraging us to submit this paper.

Funding

This work was financially supported by JSPS KAKENHI (25304017, 23570033 and 4501) to MK. During manuscript preparation, HT was funded by a SNF grant (31003A_166470) to JGF.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

The study was carried out in the field in agreement with and approved by the Zambian Department of Fisheries: Ministry of Agriculture and Cooperatives. Data collection were in accordance with the current laws of the Republic of Zambia and followed the ASAB/ABS (2012) guidelines for the treatment of animals in behavioural research and teaching.

Supplementary material

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References

  1. Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Froslev T, Rosendahl S, Boomsma JJ (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci USA 99(23):14887–14892.  https://doi.org/10.1073/pnas.222313099 CrossRefPubMedGoogle Scholar
  2. ASAB/ABS (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309CrossRefGoogle Scholar
  3. Avilés L (1997) Causes and consequences of cooperation and permanent-sociality in spides. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 476–498.  https://doi.org/10.1017/CBO9780511721953.024 CrossRefGoogle Scholar
  4. Awata S, Kohda M, Shibata JY, Hori M, Heg D (2010) Group structure, nest size and reproductive success in the cooperatively breeding cichlid Julidochromis ornatus: a correlation study. Ethology 116:316–328CrossRefGoogle Scholar
  5. Baird RW, Dill LM (1996) Ecological and social determinants of group size in transient killer whales. Behav Ecol 7(4):408–416.  https://doi.org/10.1093/beheco/7.4.408 CrossRefGoogle Scholar
  6. Bar-Oz G, Zeder M, Hole F (2011) Role of mass-kill hunting strategies in the extirpation of Persian gazelle (Gazella subgutturosa) in the northern Levant. Proc Natl Acad Sci USA 108:7345–7350CrossRefPubMedGoogle Scholar
  7. Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375–39, http://CRAN.R-project.org/package1/4lme4
  8. Biedermann PHW, Klepzig KD, Taborsky M (2009) Fungus cultivation by ambrosia beeltes: behavior and laboratory breeding success in three Xyleborine species. Environ Entomol 38(4):1096–1105.  https://doi.org/10.1603/022.038.0417 CrossRefPubMedGoogle Scholar
  9. Bilde T, Lubin Y (2001) Kin recognition and cannibalism in a subsocial spider. J Evol Biol 14(6):959–966.  https://doi.org/10.1046/j.1420-9101.2001.00346.x CrossRefGoogle Scholar
  10. Bilde T, Coates KS, Birkhofer K, Bird T, Maklakov AA, Lubin Y, Aviles L (2007) Survival benefits select for group living in a social spider despite reproductive costs. J Evol Biol 20(6):2412–2426.  https://doi.org/10.1111/j.1420-9101.2007.01407.x CrossRefPubMedGoogle Scholar
  11. Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton.  https://doi.org/10.1515/9781400858569 CrossRefGoogle Scholar
  12. Buskirk RE (1981) Sociality in the Arachnida. In: Hermann HR (ed) Social insects. Academic Press, London, pp 281–367Google Scholar
  13. Caraco T, Wolf LL (1975) Ecological determinants of group sizes of foraging lions. Am Nat 109(967):343–352.  https://doi.org/10.1086/283001 CrossRefGoogle Scholar
  14. Chapela IH, Rehner SA, Schultz TR, Mueller UG (1994) Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266(5191):1691–1694.  https://doi.org/10.1126/science.266.5191.1691 CrossRefPubMedGoogle Scholar
  15. Choe JC, Crespi BJ (1997) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge.  https://doi.org/10.1017/CBO9780511721953 CrossRefGoogle Scholar
  16. Cockburn A (1998) Evolution of helping behaviour in cooperatively breeding birds. Annu Rev Ecol Syst 29(1):141–177.  https://doi.org/10.1146/annurev.ecolsys.29.1.141 CrossRefGoogle Scholar
  17. Covas R, Griesser M (2007) Life history and the evolution of family living in birds. Proc R Soc Lond B 274(1616):1349–1357.  https://doi.org/10.1098/rspb.2007.0117 CrossRefGoogle Scholar
  18. Creel S, Creel NM (1995) Communal hunting and pack size in African wild dogs, Lycaon pictus. Anim Behav 51:1325–1339CrossRefGoogle Scholar
  19. Creel S, Creel NM (2002) The African wild dog: behavior, ecology and conservation. Princeton University Press, PrincetonGoogle Scholar
  20. Creel S, Creel NM (2015) Opposing effects of group size on reproduction and survival in African wild dogs. Behav Ecol 26(5):1414–1422.  https://doi.org/10.1093/beheco/arv100 CrossRefGoogle Scholar
  21. Creel S, Macdonald D (1995) Sociality, group size, and reproductive supression among carnivores. Adv Study Behav 24:203–257.  https://doi.org/10.1016/S0065-3454(08)60395-2 CrossRefGoogle Scholar
  22. Evans TA (1998) Factors influencing the evolution of social behaviour in Australian crab spiders (Araneae: Thomisidae). Biol J Linn Soc 63(2):205–219.  https://doi.org/10.1111/j.1095-8312.1998.tb01514.x CrossRefGoogle Scholar
  23. Foelix RF (1996) Biology of spiders. Oxford University Press, OxfordGoogle Scholar
  24. Fryer G (2006) Evolution in ancient lakes: radiation of Tanganyikan atyid prawns and speciation of pelagic cichlid fishes in Lake Malawi. Hydrobiologia 568(S1):131–142.  https://doi.org/10.1007/s10750-006-0322-x CrossRefGoogle Scholar
  25. Griesser M, Drobniak SM, Nakagawa S, Botero CA (2017) Family living sets the stage for cooperative breeding and ecological resilience in birds. PLoS Biol 15(6):e2000483.  https://doi.org/10.1371/journal.pbio.2000483 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Groenewoud F, Frommen JG, Josi D, Tanaka H, Jungwirth A, Taborsky M (2016) Predation risk drives social complexity in cooperative breeders. Proc Natl Acad Sci USA 113(15):4104–4109.  https://doi.org/10.1073/pnas.1524178113 CrossRefPubMedGoogle Scholar
  27. Hata H, Kato M (2006) A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biol Lett 2(4):593–596.  https://doi.org/10.1098/rsbl.2006.0528 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Heg D, Bachar Z (2006) Cooperative breeding in the Lake Tanganyika cichlid Julidochromis ornatus. Environ Biol Fish 76(2-4):265–281.  https://doi.org/10.1007/s10641-006-9032-5 CrossRefGoogle Scholar
  29. Heg D, Bachar Z, Taborsky M (2005) Cooperative breeding and group structure in the Lake Tanganyika cichlid Neolamprologus savoryi. Ethology 111:1017–1043CrossRefGoogle Scholar
  30. Hori M (1987) Mutualism and commensalism in the fish community of Lake Tanganyika. In: Kawano S, Connell JH, Hidaka T (eds) Evolution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, pp 219–239Google Scholar
  31. Hynes HBN (1950) The food of fresh-water sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius), with a review of methods used in studies of the food of fishes. J Anim Ecol 19(1):36–58.  https://doi.org/10.2307/1570 CrossRefGoogle Scholar
  32. Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge.  https://doi.org/10.1017/CBO9780511606816 CrossRefGoogle Scholar
  33. Koenig WD, Dickinson JL (2016) Cooperative breeding in vertebrates. Cambridge University Press, Cambridge.  https://doi.org/10.1017/CBO9781107338357 CrossRefGoogle Scholar
  34. Koenig WD, Walters EL, Haydock J (2016) Acorn woodpeckers: helping at the nest, polygynandry, and dependence on a variable acorn crop. In: Koenig WD, Dickinson JL (eds) Cooperative breedign in vertebrates. Cambridge University Press, pp 217–236Google Scholar
  35. Kohda M, Shibata JY, Awata S, Gomagano D, Takeyama T, Hori M, Heg D (2008) Niche differentiation depends on body size in a cichlid fish: a model system of a community structured according to size regularities. J Anim Ecol 77(5):859–868.  https://doi.org/10.1111/j.1365-2656.2008.01414.x CrossRefPubMedGoogle Scholar
  36. Konings AD (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El PasoGoogle Scholar
  37. Kraft B (1979) Organisation et évolution des societiés d’araignées. Aust J Psychol 1:23–51Google Scholar
  38. Kullmann EJ (1972) Evolution of social behavior in spiders (Aranea; Eresidae and Theridiidae). Am Zool 12(3):419–426.  https://doi.org/10.1093/icb/12.3.419 CrossRefGoogle Scholar
  39. Kuznetsova A, Brockhoff PB, Christensen RHB (2014) lmerTest: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0–6, http://cran.r-project.org/package=lmerTest
  40. Lubin Y, Bilde T (2007) The evolution of sociality in spiders. Adv Study Behav 37:83–145.  https://doi.org/10.1016/S0065-3454(07)37003-4 CrossRefGoogle Scholar
  41. Mann J, Patterson EM (2013) Tool use by aquatic animals. Philos Trans R Soc B 368(1630):20120424.  https://doi.org/10.1098/rstb.2012.0424 CrossRefGoogle Scholar
  42. Matsumoto K, Kohda M (2007) Male foraging avoidance in female feeding territories in a harem polygynous cichlid in Lake Tanganyika. J Ethol 25(1):21–27.  https://doi.org/10.1007/s10164-006-0200-z CrossRefGoogle Scholar
  43. O’Riain MJ, Faulkes CG (2008) African mole-rats: eusociality, relatedness and ecological constraints. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer Verlag, Berlin, pp 207–223.  https://doi.org/10.1007/978-3-540-75957-7_10 CrossRefGoogle Scholar
  44. Ochi H (1993) Maintenance of separate territories for mating and feeding by males of a maternal mouthbrooding cichlid, Gnathochromis pfefferi, in Lake Tanganyika. Jpn J Ichthyol 40:173–182Google Scholar
  45. Ochi H, Awata S, Hata H, Kohda M (2017) A Tanganyikan cichlid Neolamprologus mustax selectively exploits territories of another cichlid Variabilichromis moorii due to its inter-individual variation in aggression. Hydrobiologia 791(1):103–114.  https://doi.org/10.1007/s10750-016-2822-7 CrossRefGoogle Scholar
  46. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org Google Scholar
  47. Rasband WS (2014) Image J. U. S. National Institutes of Health, Bethesda http://imagej.nih.gov/ij/ Google Scholar
  48. Rutz C, Klump BC, Komarczyk L, Leighton R, Kramer J, Wischnewski S, Sugasawa S, Morrissey MB, James R, St Clair JJH, Switzer RA, Masuda BM (2016) Discovery of species-wide tool use in the Hawaiian crow. Nature 537(7620):403–407.  https://doi.org/10.1038/nature19103 CrossRefPubMedGoogle Scholar
  49. Sanz CM, Call J, Boesch C (2013) Tool use in animals. Cambridge Univesity Press, Cambridge.  https://doi.org/10.1017/CBO9780511894800 CrossRefGoogle Scholar
  50. Scharf I, Ovadia O (2005) Factors influencing site abandonment and site selection in a sit-and-wait predator: a review of pit-building antlion larvae. J Insect Behav 19:197–218CrossRefGoogle Scholar
  51. Schneider JM, Bilde T (2008) Benefits of cooperation with genetic kin in a subsocial spider. Proc Natl Acad Sci USA 105(31):10843–10846.  https://doi.org/10.1073/pnas.0804126105 CrossRefPubMedGoogle Scholar
  52. Silliman BR, Newell SY (2003) Fungal farming in a snail. Proc Natl Acad Sci USA 100(26):15643–15648.  https://doi.org/10.1073/pnas.2535227100 CrossRefPubMedGoogle Scholar
  53. Sorato E, Griffith SC, Russell AF (2016) The price of associating with breeders in the cooperatively breeding chestnut-crowned babbler: foraging constraints, survival and sociality. J Anim Ecol 85(5):1340–1351.  https://doi.org/10.1111/1365-2656.12539 CrossRefPubMedGoogle Scholar
  54. Stiner MC, Barkai R, Gopher A (2009) Cooperative hunting and meat sharing 400-200 kya at Qesem Cave, Israel. Proc Natl Acad Sci USA 106:13207–13212CrossRefPubMedGoogle Scholar
  55. Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32(4):1236–1252.  https://doi.org/10.1016/S0003-3472(84)80241-9 CrossRefGoogle Scholar
  56. Taborsky M (2016) Cichlid fishes: a model for the integrative study of social behavior. In: Koenig WD, Dickinson JL (eds) Cooperative breeding in vertebrates. Cambridge University Press, Cambridge, pp 272–293.  https://doi.org/10.1017/CBO9781107338357.017 CrossRefGoogle Scholar
  57. Taborsky M, Grantner A (1998) Behavioural time-energy budgets of cooperatively breeding Neolamprologus pulcher (Pisces: Cichlidae). Anim Behav 56(6):1375–1382.  https://doi.org/10.1006/anbe.1998.0918 CrossRefPubMedGoogle Scholar
  58. Tanaka H, Heg D, Takeshima H, Takeyama T, Awata S, Nishida M, Kohda M (2015) Group composition, relatedness, and dispersal in the cooperatively breeding cichlid Neolamprologus obscurus. Behav Ecol Sociobiol 69:169–181CrossRefGoogle Scholar
  59. Tanaka H, Frommen JG, Takahashi T, Kohda M (2016) Predation risk promotes delayed dispersal in the cooperatively breeding cichlid Neolamprologus obscurus. Anim Behav 117:51–58.  https://doi.org/10.1016/j.anbehav.2016.04.019 CrossRefGoogle Scholar
  60. Tanaka H, Frommen JG, Engqvist L, Kohda M (2018) Task-dependent workload adjustment of female breeders in a cooperatively breeding fish. Behav Ecol 29(1):221–229.  https://doi.org/10.1093/beheco/arx149 CrossRefGoogle Scholar
  61. Tizo-Pedroso E, Del-Claro K (2007) Cooperation in the neotropical pseudoscorpion, Paratemnoides nidificator (Balzan, 1888): feeding and dispersal behavior. Insect Soc 54(2):124–131.  https://doi.org/10.1007/s00040-007-0931-z CrossRefGoogle Scholar
  62. West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75CrossRefPubMedGoogle Scholar
  63. Whitehouse ME, Lubin Y (2005) The functions of societies and the evolution of group living: spider societies as a test case. Biol Rev 80(03):347–361.  https://doi.org/10.1017/S1464793104006694 CrossRefGoogle Scholar
  64. Yanagisawa Y (1987) Social organization of a polygynous cichlid Lamprologus furcifer in Lake Tanganyika. Jpn J Ichthyol 34:82–90Google Scholar
  65. Yip EC, Rayor LS (2014) Maternal care and subsocial behaviour in spiders. Biol Rev 89(2):427–449.  https://doi.org/10.1111/brv.12060 CrossRefPubMedGoogle Scholar
  66. Yip EC, Powers KS, Avilés L (2008) Cooperative capture of large prey solves scaling challenge faced by spider societies. Proc Natl Acad Sci USA 105(33):11818–11822.  https://doi.org/10.1073/pnas.0710603105 CrossRefPubMedGoogle Scholar
  67. Yuma M (1994) Food habitats and foraging behaviour of benthivorous cichlid fishes in Lake Tanganyika. Environ Biol Fish 39(2):173–182.  https://doi.org/10.1007/BF00004935 CrossRefGoogle Scholar
  68. Yuma M, Narita T, Hori M, Kondo T (1998) Food resources of shrimp-eating cichlid fishes in Lake Tanganyika. Environ Biol Fish 52(1/3):371–378.  https://doi.org/10.1023/A:1007370204240 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Behavioural Ecology, Institute of Ecology and EvolutionUniversity of BernHinterkappelenSwitzerland
  2. 2.Laboratory of Animal Sociology, Department of Biology and Geosciences, Graduate School of ScienceOsaka City UniversityOsakaJapan

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