Elsevier

Animal Behaviour

Volume 92, June 2014, Pages 33-43
Animal Behaviour

Discrimination of mates and intruders: visual and olfactory cues for a monogamous territorial coral reef butterflyfish

https://doi.org/10.1016/j.anbehav.2014.03.022Get rights and content

Highlights

  • Field experiments tested mate and intruder recognition by monogamous butterflyfish.

  • When visual and olfactory cues were intact, fish associated more with nonmates.

  • When olfactory cues were reversed, resident fish associated more with mates.

  • Fish failed to discriminate mates when vision and olfactory cues were not present.

  • Species recognition requires vision and mate recognition uses vision and olfaction.

Recognition of conspecifics is essential for territorial and monogamous animals in order to maintain pair bonds, mate-guard and defend territories. However, cues required for mate discrimination are essentially unknown in monogamous fishes, despite the importance of recognition behaviour that promotes this mating system. This field study tested the role of visual and olfactory cues in the discrimination of mates and unfamiliar conspecifics in the territorial, socially monogamous pebbled butterflyfish, Chaetodon multicinctus. A series of model bottle field experiments presented cues from a mate and an unfamiliar nonmate to a focal resident fish within its feeding territory. When both visual and olfactory cues were first matched, the resident spent more time and engaged in more agonistic displays near the bottled intruder. In contrast, when olfactory cues of bottled fish were first mismatched, the resident fish spent equivalent time at each bottle stimulus. When scent cues were then reversed to a matched odour condition (odour released next to bottled fish), the resident again spent more time with the nonmate. Resident fish spent equivalent time with the mate and nonmate in the absence of any associated odour stimuli. In addition, resident fish did not show a differential response when the mate's odour was associated with only one of two intruder fish. Thus both visual and olfactory cues are necessary for butterflyfish to discriminate their mate from intruders within feeding territories. These results indicate that mate recognition in animals with long-term pair bonds may require multimodal stimuli and future studies on mate recognition should address multiple sensory channels.

Section snippets

Experimental Pairs and Nonmate Fish

Mate recognition experiments were conducted by scuba divers on adult pebbled butterflyfish (standard length, SL, ≥72 mm) that occur in pairs on shallow reefs along the northwest shore of the island of Hawaii. Experimental fish pairs were confirmed by direct observations for 10–15 min of pair swimming/following behaviour, feeding and common defence of territorial borders (Tricas, 1989a, Tricas, 1989b). One member of the resident pair (the mate stimulus) was randomly selected, captured by hand net

Results

Resident fish were highly motivated to approach and interact with the visual stimulus produced by the model bottle fish in all experiments (see Supplementary Video). Once resident fish entered a square within the experimental arena, the percentage of time spent near at least one stimulus bottle was very high for at least the first phase of the experiment (between 23% and nearly 100%, median of all 32 experimental trials 81%). Fish were typically observed in close proximity to each of the

Discussion

The results of this study are consistent with the hypothesis that monogamous butterflyfish discriminate between their mate and a nonmate by both visual and olfactory cues. Our results further indicate that multiple stimuli may be necessary for butterflyfish to discriminate between mates and potential competitors that attempt to forage within their feeding territories. When visual and olfactory stimuli were both present, resident fish spent more time with the unfamiliar fish and engaged in

Acknowledgments

This work was partially funded by a University of Hawai'i Ecology, Evolution, and Conservation Biology Research Grant to K.S.B., a NOAA-Hawai'i Undersea Research Laboratory grant NA050AR4301108 to T.C.T. and an NSF grant IBN 0137883 to T.C.T. We thank T. Erin Cox and Nick Whitney for field assistance and Katherine Howard for logistical support. Brian W. Bowen and Kathleen S. Cole provided valuable comments on the study design and manuscript. This is contribution number 1583 from Hawaii

References (106)

  • U.E. Siebeck et al.

    A species of reef fish that uses ultraviolet patterns for covert face recognition

    Current Biology

    (2010)
  • R.S. Sousa-Lima et al.

    Signature information and individual recognition in the isolation calls of Amazonian manatees, Trichechus inunguis (Mammalia: Sirenia)

    Animal Behaviour

    (2002)
  • N. Stacey et al.

    Reproductive pheromones

  • M. Sutton

    Patterns of spacing in a coral reef fish in two habitats on the Great Barrier Reef

    Animal Behaviour

    (1985)
  • R.E. Thresher

    Field experiments on species recognition by the threespot damselfish, Eupomacentrus planifrons, (Pisces: Pomacentridae)

    Animal Behaviour

    (1976)
  • E.A. Tibbetts et al.

    Individual recognition: it is good to be different

    Trends in Ecology and Evolution

    (2007)
  • T.C. Tricas

    Determinants of feeding territory size in the corallivorous butterflyfish, Chaetodon multicinctus

    Animal Behaviour

    (1989)
  • D.A. Van Dyk et al.

    Familiar–unfamiliar discrimination based on visual cues in the Jacky dragon, Amphibolurus muricatus

    Animal Behaviour

    (2007)
  • J.R. Waas et al.

    Male sticklebacks can distinguish between familiar rivals on the basis of visual cues alone

    Animal Behaviour

    (1994)
  • K. Warburton et al.

    Species discrimination in guppies: learned responses to visual cues

    Animal Behaviour

    (1996)
  • A. Wilkinson et al.

    Pigeons can discriminate group mates from strangers using the concept of familiarity

    Animal Behaviour

    (2010)
  • J.M. Aldenhoven

    Different reproductive strategies in a sex-changing coral reef fish Centropyge bicolor (Pomacanthidae)

    Australian Journal of Marine and Freshwater Research

    (1986)
  • T. Aubin et al.

    Localisation of an acoustic signal in a noisy environment: the display call of the king penguin Aptenodytes patagonicus

    Journal of Experimental Biology

    (2002)
  • S. Balshine-Earn et al.

    Individual recognition in a cooperatively breeding cichlid: evidence from video playback experiments

    Behaviour

    (1998)
  • G.W. Barlow

    Patterns of monogamy among teleost fishes

    Archiv für Fischereiwissenschaft

    (1984)
  • M.A. Bee et al.

    Individual voice recognition in a territorial frog (Rana catesbeiana)

    Proceedings of the Royal Society B: Biological Sciences

    (2002)
  • J. Behrmann-Godel et al.

    Kin and population recognition in sympatric Lake Constance perch (Perca fluviatilis L.): can assortative shoaling drive population divergence?

    Behavioral Ecology and Sociobiology

    (2006)
  • K.S. Boyle et al.

    Pulse sound generation, anterior swim bladder buckling and associated muscle activity in the pyramid butterflyfish, Hemitaurichthys polylepis

    Journal of Experimental Biology

    (2010)
  • K.S. Boyle et al.

    Sound production in the longnose butterflyfishes (genus Forcipiger): cranial kinematics, muscle activity and honest signals

    Journal of Experimental Biology

    (2011)
  • G.E. Brown et al.

    Fathead minnows use chemical cues to discriminate natural shoalmates from unfamiliar conspecifics

    Journal of Chemical Ecology

    (1994)
  • J.A. Brown et al.

    Individual and species recognition in centrarchid fishes: evidence and hypotheses

    Behavioral Ecology and Sociobiology

    (1986)
  • M.G. Carr et al.

    Individual recognition in the juvenile brown bullhead (Ictalurus nebulosus)

    Copeia

    (1985)
  • I. Charrier et al.

    Individual vocal identity in mother and pup Australian sea lions (Neophoca cinerea)

    Journal of Mammalogy

    (2006)
  • K.S. Cole et al.

    Attraction of female fathead minnows, Pimephales promelas, to chemical stimuli from breeding males

    Journal of Chemical Ecology

    (1992)
  • J.D. Crawford et al.

    Bioacoustic behavior of African fishes (Mormyridae): potential cues for species and individual recognition in Pollimyrus

    Journal of the Acoustical Society of America

    (1997)
  • J.D. Crawford et al.

    Communication signals and sound production mechanisms of mormyrid electric fish

    Journal of Experimental Biology

    (1999)
  • D.P. Croft et al.

    Intra-sexual preferences for familiar fish in male guppies

    Journal of Fish Biology

    (2004)
  • J.W. Driscoll et al.

    Pair behavior and spacing in butterflyfishes (Chaetodontidae)

    Environmental Biology of Fishes

    (1988)
  • M. Edenbrow et al.

    Kin and familiarity influence association preferences and aggression in the mangrove killifish Kryptolebias marmoratus

    Journal of Fish Biology

    (2012)
  • P.R. Ehrlich

    The behaviour of chaetodontid fishes with special reference to Lorenz's “poster coloration” hypothesis

    Journal of Zoology (London)

    (1977)
  • P.R. Ehrlich et al.

    Social behavior of butterflyfishes and surgeonfishes on coral reefs: some mirror experiments

    Oecologia

    (1982)
  • N.J. Fabian et al.

    Humic acid interferes with species recognition in zebrafish (Danio rerio)

    Journal of Chemical Ecology

    (2007)
  • H.S. Fisher et al.

    Alteration of the chemical environment disrupts communication in a freshwater fish

    Proceedings of the Royal Society B: Biological Sciences

    (2005)
  • H.W. Fricke

    Individual partner recognition in fish: field studies on Amphiprion bicinctus

    Naturwissenschaften

    (1973)
  • H.W. Fricke

    Pair-swimming and mutual partner guarding in monogamous butterflyfish (Pisces, Chaetodontidae): a joint advertisement for territory

    Ethology

    (1986)
  • A. Gaisner

    Parental care and reproductive behavior of the clown goby, Microgobius gulosus, with observations on predator interactions

    Environmental Biology of Fishes

    (2005)
  • F. Gherardi et al.

    Binary individual recognition in hermit crabs

    Behavioral Ecology and Sociobiology

    (2004)
  • S.W. Griffiths

    Learned recognition of conspecifics by fishes

    Fish and Fisheries

    (2003)
  • S. Griffiths et al.

    Social recognition of conspecifics

  • S.J. Hankison et al.

    Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues

    Behavioral Ecology

    (2003)
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