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Mechanisms of breeding aggregations in fishes

Abstract
The question of why many animals breed in crowded colonies has vexed ecologists for decades. Colonies are aggregations of breeding sites used only to raise offspring. The most venerable hypothesis, arising in the 1930�s, is that colonial animals benefit from high density breeding by finding safety from predators in dense groups. Although this idea has been examined throughout the history of the field, surprisingly, there have been no studies that have experimentally manipulated the formation of colonies. One reason for this gap is that the predominant study animals � birds � are not conducive to such experiments. We side-stepped this constraint by setting up fish colonies in our institute�s giant 16,000 liter ring-shaped aquarium. We introduced 16 males and 16 females of our study species, Neolamprologus caudopunctatus, into the tank and allowed them to pair up, build nests and lay eggs. Over a 2-year period, we observed the formation of 14 colonies, with alternative colonies having predators or no predators present in the tank. We found that breeders aggregated their nests at significantly higher densities when predators were present, making this the first study to experimentally demonstrate that predation can drive colony formation.
We combined such aquarium experiments with field research in which our team studied N. caudopunctatus in their native Lake Tanganyika in southern Africa. By mapping the nests and obtaining DNA samples from families in a colony of 126 nests, we obtained substantial new knowledge about the behavior of this colonial species. After performing DNA analyses in our institute�s genetics lab to determine the relatedness of individual fish to each other, we discovered that there were no extra-pair fertilizations. This means, that in contrast to most socially monogamous bird species, �adulterous� matings apparently do not occur wherein the female of the pair produces offspring that were fathered by an outside male. Instead, our DNA analyses revealed the common occurrence of apparent adoption. We found that most broods were a mixture of natal fry that were produced by both parents and foreign fry that were unrelated to both �parents�. For the first time in a study of adoption, we were able to genetically match a number (12) of foreign fry to their actual parents, and in several cases, the distances between the birth and foster nests were so far (maximum >40 m) as to make it virtually inconceivable that tiny juveniles could have traversed them without being predated by numerous predators surrounding the colony. In human terms, it would be like a toddler crossing a busy city on its own without mishap. Further analyses led to evidence that these fry were carried in the mouths of their parents (which occurs in this species) and deposited into other nests, where adoptive parents apparently allowed the unrelated fry to mix with their own. Such unselfish behavior appears to be a Darwinian paradox (i.e. organisms are expected to maximize their own reproductive success, and would obtain zero evolutionary fitness by raising unrelated young). However, there is an adaptive explanation for adoption, namely that one�s own offspring are less likely to be predated in a larger group. Thus our adoption study adds to the evidence of our colony formation experiment that predation may be a driving force of coloniality, to which animals evolve multiple behavioral adaptations.
Statistik Austria, science classification
106047         Animal ecology
106051         Behavioural biology
305102         DNA analysis (Forensic medicine)
Keywords
Brutaggregationen
Buntbarsch
Kolonie
Partnerwahl
"public information"
Lemma
Breeding aggregations in fishes
Project leader
Wagner Richard
Duration
01.05.08-30.04.13
Type of Research
Basic research
Staff
Lemmel-Schädelin F., Contact person
Vetmed Research Units
Konrad Lorenz Institute of Ethology
Funded by
FWF - Fonds zur Förderung der wissenschaftlichen Forschung, Sensengasse 1, 1090 Wien, Austria

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14 Publications

Van Dongen, WFD; White, J; Brandl, HB; Leclaire, S; Hatch, SA; Danchin, E; Wagner, RH (2019): Experimental evidence of a sexually transmitted infection in a wild vertebrate, the black-legged kittiwake (Rissa tridactyla). Biol J Linn Soc. 2019; 127(2): 292-298.

Schaedelin, FC; van Dongen, WF; Wagner, RH (2015): Mate choice and genetic monogamy in a biparental, colonial fish. Behav Ecol. 2015; 26(3):782-788
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Leclaire, S; van Dongen, WF; Voccia, S; Merkling, T; Ducamp, C; Hatch, SA; Blanchard, P; Danchin, E; Wagner, RH (2014): Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird. Sci Rep. 2014; 4:6920
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van Dongen, WF; Wagner, RH; Moodley, Y; Schaedelin, FC (2014): Sex biases in kin shoaling and dispersal in a cichlid fish. Oecologia. 2014; 176(4):965-974

Demus, P (2010): Colony formation and mate choice in Neolamprologus caudopunctatus. Diplomarbeit, University of Vienna, pp. 52.

Fischer, S (2010): Breeding aggregation and anti-predator defense in a monogamous cichlid. Diplomarbeit, University of Vienna, pp. 38.

van Dongen, WF; White, J; Brandl, HB; Moodley, Y; Merkling, T; Leclaire, S; Blanchard, P; Danchin, E; Hatch, SA; Wagner, RH (2013): Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol. 2013; 13:11
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Schaedelin, FC; van Dongen, WF; Wagner, RH (2013): Non-random brood mixing suggests adoption in a colonial cichlid. Behav Ecol. 2013; 24(2):
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Schädelin, F; van Dongen, W; Wagner, RH (2012): Non-random brood mixing suggests adoption in a colonial cichlid. ISBE 2012; AUG 12-17, 2012; Lund, SWEDEN. 2012.

Wagner, RW; Schädelin, F (2012): Experimental evidence that predation drives colony formation in a fish. ISBE 2012 ; AUG 12-17, 2012; Lund, SWEDEN. 2012.

Martins, CIM; Schaedelin, FC; Mann, M; Blum, C; Mandl, I; Urban, D; Grill, J; Schößwender, J; Wagner, RH (2012): Exploring novelty: a component trait of behavioural syndromes in a colonial fish. Behaviour. 2012; 149(2):215-231

Schädelin, FC; Fischer, S; Wagner, RH (2012): Reduction in predator defense in the presence of neighbors in a colonial fish. PLoS One. 2012; 7(5):e35833
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Schädelin, FC; Fischer, S; Wagner, RH (2011): Neighbors reduce the cost of predation deterrence by public information in a colonial breeding cichlid, Neolamprologus caudopunctatus. 13th congress of the evolutionary society for evolutionary biology; August 20-25, 2011; Tübingen, GERMANY. 2011.

White, J; Mirleau, P; Danchin, E; Mulard, H; Hatch, SA; Heeb, P; Wagner, RH (2010): Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol Lett. 2010; 13(12):1515-1524
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