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Cooperative Breeding in the Lake Tanganyika Cichlid Julidochromis ornatus

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Abstract

Cooperative breeding has been described for several cichlids from the genus Julidochromis (Perciformes: Cichlidae) under laboratory conditions, but field evidence is scarce. Here we describe the breeding system of the cichlid Julidochromis ornatus (Boulenger) in Lake Tanganyika (Zambia). Groups defended a breeding shelter under a large flat stone. Smaller group members stayed and fed under or close to the stone, actively guarded by the larger group members. Six out of 28 groups were newly established by breeders, joined by subordinates from a large pool of independent fish (comprising 50–70% of the total population), and four groups were seen to dissolve during a total of 77 observation days. Breeding groups consisted of a large breeding male and female with zero to five smaller subordinates (average 2). Larger breeders and subordinates were found in larger groups. All group members participated in territory defence and -maintenance, but the breeders were only present at the shelter 48% of the time, in contrast to the subordinates which guarded the breeding shelter 94% of the time. Smaller group members showed submissive behaviours to larger group members. We conclude subordinates in J. ornatus are helpers, but we did not find evidence that helpers increased the group’s current reproductive success. Personal observations combined with a literature review revealed at least 19 species of Lake Tanganyika cichlids show evidence of cooperative breeding, entirely confined to the substrate breeding tribe of the Lamprologini (24% of 80 species in total): 2 Chalinochromis spp., 5 Julidochromis spp., 12 Neolamprologus spp. More effort should be put into detecting cooperative breeding in American and Asian substrate breeding cichlid species.

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Acknowledgments

We express our deepest gratitude to C. Kapasa, H. Phiri, R. Shapola, L. Makasa, D. Sinyinza and C. Lukwesa from the Zambia Ministry of Agriculture, Food & Fisheries for their continuous support of our project. We thank the Hasli crew, and the members of the Lake Tanganyika Diving Expedition 2003 for their assistance. We are grateful to R. Eggler, S. Maurer and P. Stettler for co-organising the expedition. We thank M. Aibara, N. Duftner, M. Kohda, S. Koblmüller, K. Ota, C. Sturmbauer, M. Taborsky, and particularly H. Büscher for their lively input in the project and discussions of cichlid phylogeny. We thank Marcel Häsler, Ralph Bergmüller and the anonymous reviewers for comments on earlier versions of the manuscript. The project was supported by the Swiss National Science Foundation (SNF grant 3100–064396 to Michael Taborsky). D.H. is supported by SNF grant 3100A0–108473.

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Authors and Affiliations

  1. Department of Behavioural Ecology, Zoological Institute, University of Bern, CH-3032 , Hinterkappelen, Switzerland

    Dik Heg & Zina Bachar

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  1. Dik Heg
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  2. Zina Bachar
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Correspondence to Dik Heg.

Appendix

Appendix

Evidence for cooperative breeding in Lake Tanganyika cichlids

Species

CB

GL

M

S

References and commentsa

Chalinochromis

    Ch. brichardi (Poll 1974)

Yes

Yes

Yes

R

M. Kohda (personal communication); Brichard (1999): offspring stay,

    Ch. popelini (Brichard 1989)

Yes

Yes

Yes

R

Brichard (1999): offspring stay

Julidochromis

    J. dickfeldi (Staeck 1975)

Yes

Yes

No?

R

Brichard (1999): offspring stay

    J. marlieri (Poll 1956)

Yes

Yes

Yes

R

Kalas (1976), Yamagishi (1988), Yamagishi and Kohda (1996), Sunobe (2000)

    J. ornatus (Boulenger 1898)

Yes

Yes

Yes

R

This study, Kalas (1976), Hattori (1993), Awata et’al. (2005)

    J. regani (Poll 1942)

Yes

Yes

Yes?

R

Kalas (1976) , Kuwamura (1997)

    J. transcriptus (Matthes 1958)

Yes

Yes

Yes?

R

Kuwamura (1997)

Neolamprologus b*†

    N. brevis (Boulenger 1899)

No

Yes

Yes

O

Sato and Gashagaza (1997); M. Aibara (2003 personal communication) individually marked fish suggest high turn-over rate of territorial males and satellite males, no stable groups (Wonzye Point, Zambia)

    N. brichardi c (Poll 1974)

Yes

Yes

Yes

R

See references in Introduction

    N. buescheri (Staeck 1983)

Yes?

Yes

Yes

R

Büscher (1992 d and personal communication). H.H. Büscher and D. Heg, aquarium observations: adult offspring stay in and close to breeding shelter and show submissive behaviours to adult breeders

    N. calliurus (Boulenger 1906)

No

No

Yes

O

Sato and Gashagaza (1997); M. Aibara (2003 personal communication): variant of brevis at sand-rock margins, shows ordinary polygyny (Wonzye Point, Zambia)

    N. crassus (Brichard 1989)

Yes?

Yes

Yes

R

H.H. Büscher (personal communication). H.H. Büscher and D. Heg, aquarium observations: adult offspring stay in and close to breeding shelter and show submissive behaviours to adult breeders

    N. falcicula (Brichard 1989)

Yes

Yes

Yes

R

M. Taborsky (personal communication): mixed colonies with N. pulcher (Tanzania); Brichard (1999): lives in pairs or very small groups, usually close to N. brichardi (Burundi)

    N. gracilis(Brichard 1989)

Yes

Yes

Yes

R

Woodland (2002), H.H. Büscher (personal communication)

    N. helianthus (Büscher 1997)

Yes

Yes

Yes

R

H.H. Büscher (personal communication)

    N. marunguensis (Büscher 1989)

Yes

Yes

Yes

R

H.H. Büscher (personal communication)

    N. multifasciatus (Boulenger (1906)

Yes

Yes

Yes

F

Rossiter (1993), Kohler (1998), Schradin and Lamprecht (2000, 2002)

    N. niger (Poll 1956)

Yes

Yes

Yes

R

Konings (1998): young of previous broods are tolerated in shelter (aquarium observations only); Brichard (1999): co-dominant with N. savoryi in main habitat

    N. nigriventris (Büscher 1992b)

No?

Yes

Yes

R

Büscher (1992b and personal communication): more field studies needed, offspring stay

    N. obscurus (Poll 1978)

No?

Yes

No

R

Brichard (1999): offspring stay, but juveniles are expelled from natal territory and defend communal shelter

    N. olivaceous(Brichard 1989)

Yes

Yes

Yes

R

H.H. Büscher (personal communication)

    N. pulcher c (Trewavas & Poll 1952)

Yes

Yes

Yes

R

See references in Introduction

    N. savoryi(Poll 1949)

Yes

Yes

Yes

R

Kondo (1986), Heg et’al. (2005)

    N. similis (Büscher 1992a)

Yes

Yes

Yes

F

Barlow (2000): dwarf snail-cichlid, cooperative breeder like N. multifasciatus; H.H. Büscher (1992a and personal communication)

    N. splendens (Brichard 1989)

Yes

Yes

Yes

R

H.H. Büscher (personal communication)

Telmatochromis *

    T. dhonti

No?

Yes

Yes

F

Sato and Gashagaza (1997): polygyny, probably no cooperative breeding

    T. temporalis

No

Yes

Yes

F

Katoh et’al. (2005): occasional polyandry with satellite males

    T. vittatus

No

Yes

Yes

F

Ota and Kohda (2006): various breeding systems, including satellite and sneaker males, no evidence for long-term stable group formation, offspring retention or helpers

  1. Only Lamprologine species were identified as potential cooperative breeders. Cooperative breeding was suspected in all species listed based on the main sources, which also excluded the species were extensive work has shown no evidence of cooperative breeding. Underlined are the species from the ‘brichardi’-complex (‘helianthus & olivaceous-clades’ from Salzburger et’al. 2002). Definition of terms: CB ‘Cooperative breeding’: positive evidence that subordinates assist breeders raising a brood (e.g. territory defence, shelter maintenance and/or direct brood care), may include subordinates engaging in reproduction (e.g. Kohler 1998; Dierkes et’al. 1999; Awata et’al. 2005). GL ‘Group living’: lives in closely packed groups or colonies, indicative of cooperative breeding, but where group living might also be due to the presence of satellite males, polygyny, polyandry and/or polygynandry. M ‘Multi-male or multi-female groups’: lives in polygynous, polyandrous and/or polygynandrous groups, i.e. more than two breeders are (probably) engaged in reproduction. S ‘Spawning inside snail’: ‘O’ = obligate, ‘F’ = facultative, ‘R’ = rare or absent
  2. aMain sources: Büscher (1989–1998), Staeck and Linke (1981), Taborsky and Limberger (1981), Taborsky (1994), Brichard (1997, 1999), Kawanabe et’al. (1997), Kuwamura (1997), Sato and Gashagaza (1997), Konings (1998). Comments: ‘offspring stay’ = offspring of successive broods stay in the natal territory
  3. bInsufficient information is available on (in brackets name giver(s)): N. finalimus (Nichols & La Monte 1931), N. stappersi (Pellegrin 1927), N. longicaudatus (Nakaya & Gashagaza 1995), and T. brachygnathus (Hanssens & Snoeks 2003)
  4. cProbably sub-species or sister-species, see Grantner and Taborsky (1998)
  5. *Note that the genus Neolamprologus and Lamprologus are under continuing revision and some species have been formerly grouped under the latter name. Lamprologus meleagris vs. L. stappersi are treated as separate species by www.fishbase.org, but are more likely synonyms. The same applies to Telmatochromis burgeoni vs. T. temporalis
  6. †Grouped under non-cooperative breeders, but more information needed on (in brackets name giver(s)): N. longior (Staeck 1980) and N. wauthioni (Poll 1949).

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Heg, D., Bachar, Z. Cooperative Breeding in the Lake Tanganyika Cichlid Julidochromis ornatus . Environ Biol Fish 76, 265–281 (2006). https://doi.org/10.1007/s10641-006-9032-5

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