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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
ASAB/ABS (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309
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
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 116:316–328
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
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 108:7345–7350
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
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
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
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
Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton. https://doi.org/10.1515/9781400858569
Buskirk RE (1981) Sociality in the Arachnida. In: Hermann HR (ed) Social insects. Academic Press, London, pp 281–367
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
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
Choe JC, Crespi BJ (1997) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511721953
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
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
Creel S, Creel NM (1995) Communal hunting and pack size in African wild dogs, Lycaon pictus. Anim Behav 51:1325–1339
Creel S, Creel NM (2002) The African wild dog: behavior, ecology and conservation. Princeton University Press, Princeton
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
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
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
Foelix RF (1996) Biology of spiders. Oxford University Press, Oxford
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
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
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
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
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
Heg D, Bachar Z, Taborsky M (2005) Cooperative breeding and group structure in the Lake Tanganyika cichlid Neolamprologus savoryi. Ethology 111:1017–1043
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 219–239
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
Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511606816
Koenig WD, Dickinson JL (2016) Cooperative breeding in vertebrates. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9781107338357
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 217–236
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
Konings AD (1998) Tanganyika cichlids in their natural habitat. Cichlid Press, El Paso
Kraft B (1979) Organisation et évolution des societiés d’araignées. Aust J Psychol 1:23–51
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
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
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
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
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
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
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 40:173–182
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
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org
Rasband WS (2014) Image J. U. S. National Institutes of Health, Bethesda http://imagej.nih.gov/ij/
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
Sanz CM, Call J, Boesch C (2013) Tool use in animals. Cambridge Univesity Press, Cambridge. https://doi.org/10.1017/CBO9780511894800
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 19:197–218
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
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
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
Stiner MC, Barkai R, Gopher A (2009) Cooperative hunting and meat sharing 400-200 kya at Qesem Cave, Israel. Proc Natl Acad Sci USA 106:13207–13212
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
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
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
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 69:169–181
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
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
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
West SA, Pen I, Griffin AS (2002) Cooperation and competition between relatives. Science 296:72–75
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
Yanagisawa Y (1987) Social organization of a polygynous cichlid Lamprologus furcifer in Lake Tanganyika. Jpn J Ichthyol 34:82–90
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Additional information
Communicated by V. Schluessel
This article is a contribution to the Topical Collection From Sensory Perception to Behavior—Guest Editors: Theo C. M. Bakker, Horst Bleckmann, Joachim Mogdans, Vera Schlüssel
Electronic supplementary material
ESM 1
(DOCX 3913 kb)
Rights and permissions
About this article
Cite this article
Tanaka, H., Frommen, J.G. & Kohda, M. Helpers increase food abundance in the territory of a cooperatively breeding fish. Behav Ecol Sociobiol 72, 51 (2018). https://doi.org/10.1007/s00265-018-2450-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-018-2450-5