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Mucus provisioning behavior in teleost fishes: a novel model system for the evolution of secretory provisioning in vertebrates

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Abstract

Across teleost fishes, a wide range of parental care strategies have been observed. However, despite this large variation in parental care behaviors, postnatal nutritional provisioning has rarely been documented in fishes. In other taxa, anecdotal evidence suggests that nutritional provisioning of offspring via mucus secretion by parents may occur, although this phenomenon has received little attention from evolutionary biologists, especially in fishes. To address this knowledge gap, we investigate the intra- and interspecific differences, functions, and the costs and benefits of provisioning behaviors that have potentially evolved independently in different teleost clades. Furthermore, we review and discuss within an ecological and evolutionary context, the anecdotal reports and limited available empirical evidence that shows support for mucus provisioning in teleost fishes.

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References

  • Balshine S (2012) Patterns of parental care in vertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 62–80

    Google Scholar 

  • Bernardi G, Crane NL, Longo GC, Quiros AL (2017) The ecology of Altrichthys azurelineatus and A. curatus, two damselfishes that lack a pelagic larval phase. Environ Biol Fish 100: 111–120

    Google Scholar 

  • Brust DG (1993) Maternal brood care by Dendrobates pumilio: a frog that feeds its young. J Herpetol 27:96–98

    Google Scholar 

  • Buckley J, Maunder RJ, Foey A, Pearce H, Val AL, Sloman KA (2010) Biparental mucus feeding: a unique example of parental care in an Amazonian cichlid. J Exp Biol 213:3787–3795

    CAS  PubMed  Google Scholar 

  • Burchard JE (1965) Family structure in the dwarf cichlid Apistogramma trifasciatum Eigenmann and Kennedy*. Zeitschrift für Tierpsychologie 22:150–162

    PubMed  Google Scholar 

  • Cacho MSRF, Yamamoto ME, Chellappa S (2007) Mating system of the Amazonian cichlid angel fish, Pterophyllum scalare. Braz JBiol 67:161–165

    CAS  PubMed  Google Scholar 

  • Chong, K, Ying TS, Foo J, Jin LT, Chong A (2005) Characterization of proteins in epidermal mucus of discus fish (Symphysodon spp.) during parental phase. Aquaculture 249:469–476

    CAS  Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Crampton WG (2008) Ecology and life history of an Amazon floodplain cichlid: the discus fish Symphysodon (Perciformes: Cichlidae). Neotrop Ichthyol 6:599–612

    Google Scholar 

  • Dall SR, Boyd IL (2004) Evolution of mammals: lactation helps mothers to cope with unreliable food supplies. Proc R Soc Lond B 271:2049–2057

    Google Scholar 

  • Dijkstra C, Bult A, Bijlsma S, Daan S, Meijer T, Zijlstra M (1990) Brood size manipulations in the kestrel (Falco tinnunculus): Effects on offspring and parental survival. J Anim Ecol 59:269–285

    Google Scholar 

  • Drummond H, (2001) A revaluation of the role of food in broodmate aggression. Anim Behav 61: 517–526

    Google Scholar 

  • Enjapoori AK, Grant TR, Nicol SC, Lefèvre CM, Nicholas KR, Sharp JA (2014) Monotreme lactation protein is highly expressed in monotreme milk and provides antimicrobial protection. Genome Biol Evol 6:2754–2773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farias IP, Leão A, Almeida YS, Verba JT, Crossa M, Honczaryk A, Hrbek T (2015) Evidence of polygamy in the socially monogamous Amazonian fish Arapaima gigas (Schinz, 1822) (Osteoglossiformes, Arapaimidae). Neotrop Ichthyol 13:195–204

    Google Scholar 

  • Fujiwara K, Okada K (2007) Development of the embryo, larva and early juvenile of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae). Developmental staging system. Dev Growth Differ 49:301–324

    Google Scholar 

  • Gross MR, Sargent RC (1985) The evolution of male and female parental care in fishes. Am Zool 25:807–822

    Google Scholar 

  • Hamilton WD (1963) The evolution of altruistic behavior. Am Nat 97:354–356

    Google Scholar 

  • Hildemann WH (1959) A cichlid fish, Symphysodon discus, with unique nurture habits. Am Nat 93:27–34

    Google Scholar 

  • Hori M (1993) Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260:216–219

    CAS  PubMed  Google Scholar 

  • Iq KC, Shu-Chien AC (2011) Proteomics of buccal cavity mucus in female tilapia fish (Oreochromis spp.): a comparison between parental and non-parental fish. PLoS One 6:e18555

  • Jordan LA, Herbert-Read JE, Ward AJ (2013) Rising costs of care make spiny chromis discerning parents. Behav Ecol Sociobiol 67:449–455

    Google Scholar 

  • Kavanagh K (1998) Notes on the frequency and function of glancing behavior in juvenile Acanthochromis (Pomacentridae). Copeia: 493–496

  • Keenleyside MH (1981) Parental care patterns of fishes. Am Nat 117:1019–1022

    Google Scholar 

  • Kishida M, Specker JL (2000) Paternal mouthbrooding in the black-chinned tilapia, Sarotherodon melanotheron (Pisces: cichlidae): changes in gonadal steroids and potential for vitellogenin transfer to larvae. Horm Behav 37:40–48

    CAS  PubMed  Google Scholar 

  • Kupfer A, Müller H, Antoniazzi MM, Jared C, Greven H, Nussbaum RA, Wilkinson M (2006) Parental investment by skin feeding in a caecilian amphibian. Nature 440:926–929

    CAS  PubMed  Google Scholar 

  • Lee HJ, Heim V, Meyer A (2016) Genetic evidence for prevalence of alloparental care in a socially monogamous biparental cichlid fish, Perissodus microlepis, from Lake Tanganyika supports the “selfish shepherd effect” hypothesis. Ecol Evol 6:2843–2853

    PubMed  PubMed Central  Google Scholar 

  • Lewis RW (1970) Fish cutaneous mucus: a new source of skin surface lipid. Lipids 5:947–949.

    CAS  Google Scholar 

  • López-Fernández H, Winemiller KO, Honeycutt RL (2010) Multilocus phylogeny and rapid radiations in neotropical cichlid fishes (Perciformes: Cichlidae: Cichlinae). Mol Phylogenetics Evol 55:1070–1086

    Google Scholar 

  • May RC (1974) Larval mortality in marine fishes and the critical period concept. In: Blaxter JHS (eds) The early life history of fish. Springer, Heidelberg, pp 3–19

    Google Scholar 

  • McKaye KR (1986) Trophic eggs and parental foraging for young by the catfish Bagrus meridionalis of Lake Malawi, Africa. Oecologia 69:367–369

    PubMed  Google Scholar 

  • Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  • Noakes DL (1979) Parent-touching behavior by young fishes: incidence, function and causation. Environ Biol Fish 4:389–400

    Google Scholar 

  • Ochi H, Yanagisawa Y, Omori K (1995) Intraspecific brood-mixing of the cichlid fish Perissodus microlepis in Lake Tanganyika. Environ Biol Fishes 43:201–206

    Google Scholar 

  • Ota K, Kohda M (2014) Maternal food provisioning in a substrate-brooding African cichlid. PloS One 9:e99094

    PubMed  PubMed Central  Google Scholar 

  • Perrone M, Zaret TM (1979) Parental care patterns of fishes. Am Nat 113:351–361

    Google Scholar 

  • Pires TH, Campos DF, Röpke CP, Sodré J, Amadio S, Zuanon J (2015) Ecology and life-history of Mesonauta festivus: biological traits of a broad ranged and abundant Neotropical cichlid. Environ Biol Fishes 98:789–799

    Google Scholar 

  • Robertson DR (1973) Field observations on the reproductive behaviour of a pomacentrid fish, Acanthochromis polyacanthus. Z Tierpsychol 32:319–324

    CAS  PubMed  Google Scholar 

  • Rodrigues RR, Zuanon J, Del-Claro K, Carvalho LN (2012) Reproductive behavior of the Amazonian dwarf cichlid Apistogramma hippolytae Kullander, 1982: offsetting costs and benefits. Acta Ethol 15:47–53

    Google Scholar 

  • Royle NJ, Smiseth PT, Kölliker M (2012) The evolution of parental care. Oxford University Press, Oxford

    Google Scholar 

  • Satoh S, Awata S, Tanaka H, Jordan LA, Kakuda U, Hori M, Kohda M (2019) Bi-parental mucus provisioning in the scale-eating cichlid Perissodus microlepis (Cichlidae). Biol J Linn Soc 128:926–935

    Google Scholar 

  • Satoh S, Tanoue H, Mohri M (2018) Costs and benefits of biparental mucus provisioning in discus fish (Symphysodon aequifasciatus). Ichthyol Res 65:510–514

    Google Scholar 

  • Satoh S, Tanoue H, Ruitton S, Mohri M, Komatsu T (2017) Morphological and behavioral ontogeny in larval and early juvenile discus fish Symphysodon aequifasciatus. Ichthyol Res 64:37–44

    Google Scholar 

  • Schütz M, Barlow GW (1997) Young of the Midas cichlid get biologically active nonnutrients by eating mucus from the surface of their parents. Fish Physiol Biochem 16:11–18

    Google Scholar 

  • Shephard KL (1994) Functions for fish mucus. Rev Fish Biol Fisher 4:401–429

    Google Scholar 

  • Smiseth PT, Kölliker M, Royle NJ (2012) What is parental care? In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 1–17

    Google Scholar 

  • Sparks JS (2004) Molecular phylogeny and biogeography of the Malagasy and South Asian cichlids (Teleostei: Perciformes: Cichlidae). Mol Phylogenetics Evol 30:599–614

    CAS  Google Scholar 

  • Stephens WZ, Burns AR, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJM (2016) The composition of the zebrafish intestinal microbial community varies across development. ISME J 10:644–654

    PubMed  Google Scholar 

  • Sylvain FÉ, Derome N (2017) Vertically and horizontally transmitted microbial symbionts shape the gut microbiota ontogenesis of a skin-mucus feeding discus fish progeny. Sci Rep UK 7:5263

    Google Scholar 

  • Takeuchi Y, Hori M, Oda Y (2012) Lateralized kinematics of predation behavior in a Lake Tanganyika scale-eating cichlid fish. PLoS One 7:e29272

    CAS  PubMed  PubMed Central  Google Scholar 

  • Torati LS, Migaud H, Doherty MK, Siwy J, Mullen W, Mesquita PE, Albalat A (2017) Comparative proteome and peptidome analysis of the cephalic fluid secreted by Arapaima gigas (Teleostei: Osteoglossidae) during and outside parental care. PloS One 12:e0186692

    PubMed  PubMed Central  Google Scholar 

  • Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine Press, Chicago, pp 139–179

    Google Scholar 

  • Trivers R (1974) Parent–offspring conflict. Am Zool 14:249–264

    Google Scholar 

  • Vandeputte-Poma J (1980) Feeding, growth and metabolism of the pigeon, Columba livia domestica: duration and role of crop milk feeding. J Comp Physiol B 135:97–99

    Google Scholar 

  • Walters JR (1984) The evolution of parental behavior and clutch size in shorebirds. In: Burger J, Olla BL (eds) Shorebirds: breeding behavior and populations. Plenum Press, New York, pp 243–287

    Google Scholar 

  • Welsh JK, May JT (1979) Anti-infective properties of breast milk. J Prediat 94:1–9

    CAS  Google Scholar 

  • Wen B, Zhou JQ, Geo JZ, Chen HR, Shen YQ, Chen ZZ (2020) Sex-dependent changes in the skin mucus metabolome of discus fish (Symphysodon haraldi) during biparental care. J Proteom 221:103784

    CAS  Google Scholar 

  • Wessler E, Werner I (1957) On the chemical composition of some mucous substances of fish. Acta Chem Scand 11:1240–1247

    CAS  Google Scholar 

  • Wiersma EJ, Collins C, Fazel S, Shulman MJ (1998) Structural and functional analysis of J chain-deficient IgM. J Immunol 160:5979–5989

    CAS  PubMed  Google Scholar 

  • Wisenden BD, Keenleyside MHA (1994) The dilution effect and differential predation following brood adoption in free-ranging convict cichlids (Cichlasoma nigrofasciatum). Ethology 96:203–212

    Google Scholar 

  • Wisenden BD, Lanfranconi TL, Keenleyside MH (1995) Fin digging and leaf lifting by the convict cichlids, Cichlasoma nigrofasciatum: example of parental food provisioning. Anim Behav 49:623–631

    Google Scholar 

  • Wourms JP, Grove BD, Lombardi J. (1988) The maternal‐embryonic relationship in viviparous fishes. In: Randall DJ. (eds) Fish physiology. Academic Press, Cambridge, pp 1–134

    Google Scholar 

  • Yanagisawa T, Ochi H, Rossiter A (1996) Intra-buccal feeding of young in an undescribed Tanganyikan cichlid Microdontochromis sp. Environ Biol Fishes 47:191–201

    Google Scholar 

  • Zworykin DD, Budaev SV (2000) Parental brood provisioning as a component of parental care in neotropical cichlid fishes (Perciformes: Cichlidae). J Ichthyol 40:271–280

    Google Scholar 

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Acknowledgments

Prof. Masanori Kohda, Assoc. Prof. Satoshi Awata, and the members of the Maneno Tanganyika Research team and the Animal Sociology Laboratory of Osaka City University provided helpful comments and discussion. Mr. Yusuke Fuke helped with the phylogenetic analysis. Editage (https://www.editage.com) provided English language editing. Dr. L. Alex Jordan and Mr. Shunichi Asamura provided photographs for the manuscript. This paper was improved by the comments and suggestions made by the anonymous reviewers and Editor Dr. Mari Kawaguchi. This study was supported financially by KAKENHI (nos. H17J11490, N19K23765 and N19KK0189 to S.S.) and a JSPS fellowship (to W.S.). The authors declare no conflict of interest.

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Satoh, S., Sowersby, W. Mucus provisioning behavior in teleost fishes: a novel model system for the evolution of secretory provisioning in vertebrates. Ichthyol Res 68, 1–10 (2021). https://doi.org/10.1007/s10228-020-00785-z

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