Elsevier

Animal Behaviour

Volume 169, November 2020, Pages 119-128
Animal Behaviour

Body-generated hydrodynamic flows influence male–male contests and female mate choice in a freshwater fish

https://doi.org/10.1016/j.anbehav.2020.09.005Get rights and content

Highlights

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    The role of mechanosensory signals in fish communication is not well understood.

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    Males without access to mechanosensory information won fewer contests.

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    Females without access to mechanosensory signals showed reduced mate discrimination.

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    Mechanosensory signals play an important role in social decision making in fish.

The lateral line system of fishes is composed of neuromast mechanoreceptors that detect movement through vibration and changes in pressure gradients in the water. Although mechanosensory information has been shown to be important in the contexts of predator escape and foraging, little is known about the role of the lateral line system during intraspecific interactions, such as reproduction. However, many species of fish demonstrate complex courtship and aggressive repertoires that involve movement of the body and fins, resulting in local displacement of the surrounding water. This displacement has the potential to function as a signal that contains information about the sender. In this study, we conducted two behavioural experiments using fathead minnows, Pimephales promelas, to test the hypothesis that the outcomes of male–male contests and male–female courtship interactions are influenced by hydrodynamic flows generated during conspecific interactions. In the first experiment, we pitted control males against those with an ablated lateral line system and assessed both overall aggression and the likelihood of territory acquisition. In the second experiment, we conducted dual-choice female mate choice experiments to determine whether control females and those without access to mechanosensory information (ablated females) differed in patterns of discrimination and the use of courtship as a criterion of choice. In experiment 1, control males won a significantly greater proportion of territorial contests than expected by chance and were more likely to use noncontact threat displays during aggressive interactions compared with ablated males. In experiment 2, females with access to the mechanosensory information channel showed enhanced mate discrimination compared to ablated females. These data are among the first to show that mechanosensory signals are an important criterion of territorial and reproductive success in fishes and are likely important contributors to multimodal communication in this group.

Section snippets

Experimental Animals, Housing and Maintenance

Sexually mature fathead minnows (>6 months old) were obtained from a laboratory culture facility (Aquatic Bio Systems, Inc.; Fort Collins, CO, U.S.A.) and housed in separate-sex groups in 37-litre tanks until use in experimental trials. The fish were maintained at 21–25 °C under a 14:10 h light:dark photoperiod and fed an ad libitum diet of live brine shrimp (Artemia franciscana) twice daily.

Fathead minnows are small, North American freshwater fish with a geographical range that extends over much

Experiment 1: the Role of the Mechanosensory Lateral Line System in Male–Male Territorial Contests

As expected, no male in any group performed aggressive behaviours during pretrial observations. However, males aggressively competed for the territory after the divider was pulled and the subjects had an opportunity to interact (mean frequency of all behaviours ± SD: pretrial: 0 ± 0; trial 1: 34.7 ± 47.3; t250 = -8.2, P = < 0.001). Territorial contests occurred in 100% of trials and were typically resolved within 6 h (N = 63 total trials ; N = 21 per trial scenario); the male that was under the nest site

Discussion

A robust understanding of how animals detect and respond to the individual components of a multimodal signal is the first step to understanding how receivers integrate different signal components. In this study, manipulation of the ability of receivers to detect and respond to mechanosensory stimuli had significant effects on the behaviour of males and females during reproductive interactions. In territorial contests that paired males with and without access to sensory information from the

Acknowledgments

We thank Kamal Islam and Mark Pyron for insightful discussions during the study and the dedicated undergraduate students (Autum Auxier, Katie Esarey, Hannah Mullinax and Lauren Reed) who assisted with this project. We also thank Julie Butler and Jackie Webb for guidance on pharmacological ablation and staining procedures. Finally, we are grateful to two anonymous referees for their thoughtful comments and suggestions for improvement on the manuscript. Funding for this project was provided by a

References (99)

  • N. Kemper

    Veterinary antibiotics in the aquatic and terrestrial environment

    Ecological Indicators

    (2008)
  • R. Knapp et al.

    Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus)

    Hormones and Behavior

    (1999)
  • E. Lloyd et al.

    Evolutionary shifts towards lateral line dependent prey capture behavior in the blind Mexican cavefish

    Developmental Biology

    (2018)
  • F.C. Neat et al.

    Proximate costs of fighting in male cichlid fish: The role of injuries and energy metabolism

    Animal Behaviour

    (1998)
  • S. Östlund et al.

    Female fifteen-spined sticklebacks prefer better fathers

    Animal Behaviour

    (1998)
  • K.N. Owens et al.

    Response of mechanosensory hair cells of the zebrafish lateral line to aminoglycosides reveals distinct cell death pathways

    Hearing Research

    (2009)
  • S. Partan et al.

    Female pigeons, Columba livia, respond to multisensory audio/video playbacks of male courtship behaviour

    Animal Behaviour

    (2005)
  • A.R. Reddon et al.

    Rules of engagement for resource contests in a social fish

    Animal Behaviour

    (2011)
  • A.K. Schnell et al.

    Giant Australian cuttlefish use mutual assessment to resolve male–male contests

    Animal Behaviour

    (2015)
  • M.A.B. Schwalbe et al.

    Sensory basics for detection of benthic prey in two Lake Malawi cichlids

    Zoology

    (2014)
  • R.C. Taylor et al.

    Faux frogs: Multimodal signalling and the value of robotics in animal behaviour

    Animal Behaviour

    (2008)
  • W.J. van Trump et al.

    Gentamicin is oxotoxic to all hair cells in the fish lateral line system

    Hearing Research

    (2010)
  • B.B.M. Wong

    Superior fighters make mediocre fathers in the pacific blue-eyed fish

    Animal Behaviour

    (2004)
  • M.B. Anderson

    Sexual selection: Monographs in behavior and ecology

    (1994)
  • I. Braasch et al.

    Evolution of pigment synthesis pathways by gene and genome duplication in fish

    BMC Evolutionary Biology

    (2007)
  • J.M. Butler et al.

    The mechanosensory lateral line is used to assess opponents and mediate aggressive behaviors during territorial interactions in an African cichlid fish

    Journal of Experimental Biology

    (2015)
  • J.M. Butler et al.

    The mechanosensory lateral line system mediates activation of socially-relevant brain regions during territorial interactions

    Frontiers in Behavioral Neuroscience

    (2016)
  • J.M. Butler et al.

    Mechanosensory signaling as a potential mode of communication during social interactions in fishes

    Journal of Experimental Biology

    (2016)
  • D. Campagner et al.

    Prediction of choice from competing mechanosensory and choice-memory cues during active tactile decision making

    Journal of Neuroscience

    (2019)
  • U. Candolin

    The use of multiple cues in mate choice

    Biological Reviews

    (2003)
  • A.G. Carton et al.

    A comparison of lateral line morphology of blue cod and torrentfish: Two sandperchers of the family Pinguipedidae

    Environmental Biology of Fishes

    (2004)
  • T.S. Clement et al.

    Female affiliative preference depends on reproductive state in the African cichlid fish, Astatotilapia burtoni

    Behavioral Ecology

    (2005)
  • S. Coombs et al.

    The lateral line system

    (2014)
  • S. Coombs et al.

    The orientating response of Lake Michigan mottled sculpin is mediated by canal neuromasts

    Journal of Experimental Biology

    (2001)
  • S. Dijkgraaf

    The functioning and significance of the lateral-line organs

    Biological Reviews

    (1962)
  • B. Ding et al.

    Quantitative genetic analyses of male color pattern and female mate choice in a pair of cichlid fishes of Lake Malawi, East Africa

    PLoS One

    (2014)
  • J.N. Divino et al.

    Importance of nest and paternal characteristics for hatching success in fathead minnow

    Copeia

    (2008)
  • J. Engelmann et al.

    Lateral line reception in still and running water

    Journal of Comparative Physiology

    (2002)
  • E.K. Fischer et al.

    Genetically and environmentally mediated divergence in lateral line morphology in the Trinidadian guppy (Poecilia reticulata)

    Journal of Experimental Biology

    (2013)
  • M.B. Girard et al.

    Female preference for multi-modal courtship: Multiple signals are important for male mating success in peacock spiders

    Proceedings of the Royal Society B

    (2015)
  • P.A. Green et al.

    Mutual assessment during ritualized fighting in mantis shrimp (Stomatopoda)

    Proceedings of the Royal Society B

    (2018)
  • W. Halfwerk et al.

    Toward testing for multimodal perception of mating signals

    Frontiers in Ecology and Evolution

    (2019)
  • M.L. Head et al.

    Sexual display and mate choice in an energetically costly environment

    PLoS One

    (2010)
  • E.A. Hebets

    Seismic signal dominance in the multimodal courtship display of the wolf spider Schizocosa stridulans Stratton 1991

    Behavioral Ecology

    (2008)
  • E.A. Hebets et al.

    Complex signal function: Developing a framework of testable hypotheses

    Behavioral Ecology and Sociobiology

    (2005)
  • J.P. Higham et al.

    An introduction to multimodal communication

    Behavioral Ecology and Sociobiology

    (2013)
  • C.D. Hoefler et al.

    Evolutionarily costly courtship displays in a wolf spider: A test of viability indicator theory

    Behavioral Ecology

    (2008)
  • S.P. Hudman et al.

    Intra- and intersexual selection on male body size are complimentary in the fathead minnow (Pimephales promelas)

    Behaviour

    (2007)
  • R.A. Johnstone

    Multiple displays in animal communication: ‘Backup signals’ and ‘multiple messages’

    Philosophical Transactions of the Royal Society B

    (1996)

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