Skip to main content

Advertisement

SpringerLink
Log in

Confronting the ‘nocturnal problem’ in coral reefs: sleeping site selection and cocoon formation in parrotfishes

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Habitat utilization is a major component of animal behavior and ecology, yet nighttime habitat utilization by diurnal animals remains understudied for many taxa. Sheltered sleeping sites are considered particularly important for parrotfishes (Labridae: Scarini) inhabiting coral reefs, where predation risk is most prominent at night. Parrotfishes are also known to sleep in mucus cocoons, which allegedly function as a means of predator and/or ectoparasite avoidance. In this study, we present the first systematic characterization of nocturnal habitat utilization and cocoon formation in parrotfishes, in their natural environment. We performed a total of 153 surveys and sampled 225 individual parrotfishes (of 11 species) and characterized their sleeping sites. We found that several species utilized sleeping sites with distinct characteristics, such as exposed sites that provided little to no coverage or sleeping sites well above the reef floor. However, most species exhibited substantial overlap in site characteristics and exposure. We found that the utilization of sheltered sleeping sites did not correlate with body size or life stage, suggesting that sleeping-site selection in parrotfish is unlikely to be driven by competitive exclusion. We also found that while some species either never or rarely formed cocoons, many species exhibited facultative cocoon formation that was not clearly associated with exposure or habitat. While we expected cocoons to be more frequent in exposed sites to avoid predators, or on soft substrates to avoid ectoparasites, we found no effect of either predictor. As many species exhibited a wide range of sleeping sites and behaviors, nocturnal habitat utilization does not appear to be a major axis for niche differentiation in this guild.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data and materials availability

Data presented and analyzed in this work can be found in Appendix B.

References

  • Adam TC, Kelley M, Ruttenberg BI, Burkepile DE (2015) Resource partitioning along multiple niche axes drives functional diversity in parrotfishes on Caribbean coral reefs. Oecologia 179:1173–1185

    PubMed  Google Scholar 

  • Allgeier JE, Adam TC, Burkepile DE (2017) The importance of individual and species-level traits for trophic niches among herbivorous coral reef fishes. Proc Biol Sci 284:20170307

    PubMed  PubMed Central  Google Scholar 

  • Almany GR (2004) Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141:105–113

    PubMed  Google Scholar 

  • Anderson JR (1998) Sleep, sleeping sites, and sleep-related activities: awakening to their significance. Am J Primatol 46:63–75

    CAS  PubMed  Google Scholar 

  • Arbizu PM (2020) pairwiseAdonis: Pairwise multilevel comparison using adonis R package

  • Aswani S, Hamilton RJ (2004) Integrating indigenous ecological knowledge and customary sea tenure with marine and social science for conservation of bumphead parrotfish (Bolbometopon muricatum) in the Roviana Lagoon, Solomon Islands. Environ Conserv 31:69–83

    Google Scholar 

  • Bardach JE, Winn HE, Menzel DW (1959) The role of the senses in the feeding of the nocturnal reef predators Gymnothorax moringa and G. vicinus. Copeia 1959:133–139

    Google Scholar 

  • Bellwood D (1995) Direct estimate of bioerosion by two parrotfish species, Chlorurus gibbus and C. sordidus, on the Great Barrier Reef, Australia. Mar Biol 121:419–429

    Google Scholar 

  • Bellwood DR, Choat JH (1990) A functional-analysis of grazing in parrotfishes (family Scaridae)-the ecological implications. Environ Biol Fishes 28:189–214

    Google Scholar 

  • Bellwood DR, Schultz O (1988) A review of the fossil record of the parrotfishes (Labroidei: Scaridae) with a description of a new Calotomus species from the Middle Miocene (Badenian) of Austria. Annalen des Naturhistorischen Museums in Wien Serie A für Mineralogie und Petrographie, Geologie und Paläontologie, Anthropologie und Prähistorie :55–71

  • Beukers JS, Jones GP (1998) Habitat complexity modifies the impact of piscivores on a coral reef fish population. Oecologia 114:50–59

    PubMed  Google Scholar 

  • Binning SA, Roche DG, Layton C (2013) Ectoparasites increase swimming costs in a coral reef fish. Biol Lett 9:20120927

    PubMed  PubMed Central  Google Scholar 

  • Bonaldo RM, Krajewski JP, Sazima C, Sazima I (2006) Foraging activity and resource use by three parrotfish species at Fernando de Noronha Archipelago, tropical West Atlantic. Mar Biol 149:423–433

    Google Scholar 

  • Bouchet P, Perrine D (1996) More gastropods feeding at night on parrotfishes. B Mar Sci 59:224–228

    Google Scholar 

  • Bowers MA, Smith HD (1979) Differential habitat utilization by sexes of the Deermouse, Permomyscus maniculatus. Ecology 60:869–875

    Google Scholar 

  • Bruggemann JH, Kuyper MWM, Breeman AM (1994) Comparative analysis of foraging and habitat use by the sympatric Caribbean parrotfish Scarus vetuta and Sparisoma viride (Scaridae). Mar Ecol Prog Ser 112:51–66

    Google Scholar 

  • Byrne JE (1970) Mucous envelope formation in two species of Hawaiian parrotfishes (Genus Scarus)

  • Cardwell JR, Liley NR (1991) Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride. Gen Comp Endocrinol 81:7–20

    CAS  PubMed  Google Scholar 

  • Casimir MJ (1971) Zur morphologie, histochemie, tagesperiodik und biologie der operculardrüse bei labriden und Scariden (Pisces). Mar Biol 8:126–146

    Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244

    Google Scholar 

  • Chapman CA (1989) Spider monkey sleeping sites: use and availability. Am J Primatol 18:53–60

    PubMed  Google Scholar 

  • Choat J, Randall E (1986) A review of the parrotfishes (Family Scaridae) of the great barrier reef of Australia with description of a new species. Rec Aust Mus 38:175–228

    Google Scholar 

  • Choat JH, Klanten OS, Van Herwerden L, Robertson DR, Clements KD (2012) Patterns and processes in the evolutionary history of parrotfishes (Family Labridae). Biol J Linn Soc 107:529–557

  • Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896

    CAS  PubMed  Google Scholar 

  • Covert I, Lee S-I (2021) Improving KernelSHAP: Practical Shapley value estimation using linear regression. In: International Conference on Artificial Intelligence and Statistics :3457–3465

  • Davis K, Carlson PM, Bradley D, Warner RR, Caselle JE (2017a) Predation risk influences feeding rates but competition structures space use for a common Pacific parrotfish. Oecologia 184:139–149

    PubMed  Google Scholar 

  • Davis K, Carlson PM, Lowe CG, Warner RR, Caselle JE (2017b) Parrotfish movement patterns vary with spatiotemporal scale. Mar Ecol Prog Ser 577:149–164

    Google Scholar 

  • De Girolamo M, Scaggiante M, Rasotto M (1999) Social organization and sexual pattern in the Mediterranean parrotfish Sparisoma cretense (Teleostei: Scaridae). Mar Biol 135:353–360

    Google Scholar 

  • Dubin RE, Baker JD (1982) Two types of cover-seeking behavior at sunset by the princess parrotfish, Scarus taeniopterus, at Barbados, West Indies. B Mar Sci 32:572–583

    Google Scholar 

  • Ellis WL, Bell SS (2004) Conditional use of mangrove habitats by fishes: depth as a cue to avoid predators. Estuaries 27:966–976

    Google Scholar 

  • Ellison G, Wolfenden A, Kahana L, Kisingo A, Jamieson J, Jones M, Bettridge CM (2019) Sleeping site selection in the nocturnal northern lesser galago (Galago senegalensis) supports antipredator and thermoregulatory hypotheses. Int J Primatol 40:276–296

    Google Scholar 

  • Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Biol Ecol 224:1–30

    Google Scholar 

  • Gaston KJ (2019) Nighttime ecology: the “nocturnal problem” revisited. Am Nat 193:481–502

    PubMed  Google Scholar 

  • Goatley CH, Bellwood DR (2016) Body size and mortality rates in coral reef fishes: a three-phase relationship. Proc Biol Sci 283:20161858

    PubMed  PubMed Central  Google Scholar 

  • Gomi K, Nakamura Y, Kanda M, Honda K, Nakaoka M, Honma C, Adachi M (2021) Diel vertical movements and feeding behaviour of blue humphead parrotfish Scarus ovifrons in a temperate reef of Japan. J Fish Biol 99:131–142

    CAS  PubMed  Google Scholar 

  • Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–871

    Google Scholar 

  • Gregor CA, Anderson TW (2016) Relative importance of habitat attributes to predation risk in a temperate reef fish. Environ Biol Fishes 99:539–556

    Google Scholar 

  • Grömping U (2009) Variable importance assessment in regression: linear regression versus random forest. Am Stat 63:308–319

    Google Scholar 

  • Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30

    Google Scholar 

  • Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673

    CAS  Google Scholar 

  • Grutter AS (2003) Feeding ecology of the fish ectoparasite Gnathia sp (Crustacea : Isopoda) from the Great Barrier Reef, and its implications for fish cleaning behaviour. Mar Ecol Prog Ser 259:295–302

    Google Scholar 

  • Grutter AS, Rumney JG, Sinclair-Taylor T, Waldie P, Franklin CE (2011) Fish mucous cocoons: the “mosquito nets” of the sea. Biol Lett 7:292–294

    PubMed  Google Scholar 

  • Gust N (2002) Scarid biomass on the northern Great Barrier Reef: the influence of exposure, depth and substrata. Environ Biol Fishes 64:353–366

    Google Scholar 

  • Haggerty JM, Brett MN, Francini RB, Dinsdale EA (2012) Night Surveys Along the Abrolhos Bank, Brazil, Generate First Observation of Mucous Cocoon Production in Scarus Trispinosus. B Mar Sci 88:883–884

    Google Scholar 

  • Hall J (1978) New bathymetric map of the Gulf of Eilat (Aqaba). Tenth Int Conf Sedimentol, Jerusalem 1978(1):285

    Google Scholar 

  • Hamilton WJ 3rd (1982) Baboon sleeping site preferences and relationships to primate grouping patterns. Am J Primatol 3:41–53

    PubMed  Google Scholar 

  • Hamilton RJ, Hughes A, Brown CJ, Leve T, Kama W (2019) Community-based management fails to halt declines of bumphead parrotfish and humphead wrasse in Roviana Lagoon, Solomon Islands. Coral Reefs 38:455–465

    Google Scholar 

  • Hartig F, Hartig MF (2017) Package ‘DHARMa’ Vienna, Austria: R Development Core Team R Package

  • Hawkins JP, Roberts CM (2004) Effects of fishing on sex-changing Caribbean parrotfishes. Biol Cons 115:213–226

    Google Scholar 

  • Helfman GS (1986) Fish behaviour by day, night and twilight. In: Pitcher TJ (ed) The behaviour of teleost fishes. Springer, Boston, pp 366–387

    Google Scholar 

  • Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101

    Google Scholar 

  • Hixon MA, Jones GP (2005) Competition, predation, and density-dependent mortality in demersal marine fishes. Ecology 86:2847–2859

    Google Scholar 

  • Hobson ES (1965) Diurnal-nocturnal activity of some inshore fishes in the Gulf of California. Copeia 1965:291–302

    Google Scholar 

  • Hobson ES (1972) Activity of Hawaiian reef fishes during the evening and morning transitions between daylight and darkness. Fish Bull 70:715–740

    Google Scholar 

  • Hobson ES (1975) Feeding patterns among tropical reef fishes. Am Sci 63:382–392

    Google Scholar 

  • Hoey AS, Bellwood DR (2007) Cross-shelf variation in the role of parrotfishes on the great barrier reef. Coral Reefs 27:37–47

    Google Scholar 

  • Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–273

    PubMed  Google Scholar 

  • Howard KG, Claisse JT, Clark TB, Boyle K, Parrish JD (2013) Home range and movement patterns of the Redlip Parrotfish (Scarus rubroviolaceus) in Hawaii. Mar Biol 160:1583–1595

    Google Scholar 

  • Hughes R, Hughes D, Smith I (2014) The ecosystem roles of parrotfishes on tropical reefs. Oceanogr Mar Biol 20141169:81–132

    Google Scholar 

  • Jones CM, Grutter AS (2006) Variation in emergence of parasitic and predatory isopods among habitats at Lizard Island, Great Barrier Reef. Mar Biol 150:919–927

    Google Scholar 

  • Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251–8253

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KA, Ratcliffe N, Votier SC, Newton J, Forcada J, Dickens J, Stowasser G, Staniland IJ (2020) Intra-specific Niche Partitioning in Antarctic Fur Seals. Arctocephalus Gazella Sci Rep 10:3238

    CAS  PubMed  Google Scholar 

  • Kane CN, Brooks AJ, Holbrook SJ, Schmitt RJ (2008) The role of microhabitat preference and social organization in determining the spatial distribution of a coral reef fish. Environ Biol Fishes 84:1–10

    Google Scholar 

  • Kerry JT, Bellwood DR (2011) The effect of coral morphology on shelter selection by coral reef fishes. Coral Reefs 31:415–424

    Google Scholar 

  • Lazarus M, Belmaker J (2021) A review of seascape complexity indices and their performance in coral and rocky reefs. Methods Ecol Evol 12:681–695

    Google Scholar 

  • Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:8–13

    CAS  PubMed  Google Scholar 

  • Lele SR, Keim JL, Solymos P (2019) ResourceSelection: Resource Selection (Probability) Functions for Use-Availability Data R Package

  • Lellys NT, de Moura RL, Bonaldo RM, Francini-Filho RB, Gibran FZ (2019) Parrotfish functional morphology and bioerosion on SW Atlantic reefs. Mar Ecol Prog Ser 629:149–163

    Google Scholar 

  • Liaw A, Wiener M (2002) Classification and regression by randomForest R news R Package

  • Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723–736

    Google Scholar 

  • Lindholm J, Knight A, Kaufman L, Miller S (2006) Site fidelity and movement of the parrotfishes Scarus coeruleus and Scarus taeniopterus at Conch Reef (northern Florida Keys). Caribb J Sci 42:138–144

    Google Scholar 

  • Lugendo BR, Pronker A, Cornelissen I, de Groene A, Nagelkerken I, Dorenbosch M, van der Velde G, Mgaya YD (2005) Habitat utilisation by juveniles of commercially important fish species in a marine embayment in Zanzibar, Tanzania. Aquat Living Resour 18:149–158

    Google Scholar 

  • Lundberg SM, Lee SI (2017) A unified approach to interpreting model predictions. Adv Neur Inf Process Syst 30

  • Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K, Studer M (2013) Package ‘cluster’ R Package

  • Manderson JP, Pessutti J, Hilbert JG, Juanes F (2004) Shallow water predation risk for a juvenile flatfish (winter flounder; Pseudopleuronectes americanus, Walbaum) in a northwest Atlantic estuary. J Exp Mar Biol Ecol 304:137–157

    Google Scholar 

  • Manning JC, McCoy SJ, Benhamou S (2022) Spatial interactions between parrotfishes and implications for species coexistence. bioRxiv

  • Manning JC, McCoy SJ (2023) Territoriality drives patterns of fixed space use in Caribbean parrotfishes. Ecol Evol 13:e9833

    PubMed  PubMed Central  Google Scholar 

  • Mayer M (2023a) shapviz: SHAP Visualizations R Package

  • Mayer M (2023b) kernelshap: Kernel SHAP R Package

  • McAfee ST, Morgan SG (1996) Resource use by five sympatric parrotfishes in the San Blas Archipelago, Panama. Mar Biol 125:427–437

    Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models. Chapman and Hall, London

    Google Scholar 

  • Meyer C (2006) Acoustic monitoring of long-term movement patterns, habitat use and site fidelity of coral reef fishes implications for marine protected area design: final report for NOAA Coral Grant NA05NMF4631041

  • Mohanty NP, Wagener C, Herrel A, Thaker M (2022) The ecology of sleep in non-avian reptiles. Biol Rev Camb Philos Soc 97:505–526

    PubMed  Google Scholar 

  • Morris DW (2003) How can we apply theories of habitat selection to wildlife conservation and management? Wildl Res 30:303–319

    Google Scholar 

  • Mugridge RER, Stallybrass HG (1983) A Mortality of Eels, Anguilla-Anguilla L Attributed to Gnathiidae. J Fish Dis 6:81–82

    Google Scholar 

  • Mumby PJ, Wabnitz CCC (2002) Spatial patterns of aggression, territory size, and harem size in five sympatric Caribbean parrotfish species. Environ Biol Fishes 63:265–279

    Google Scholar 

  • Nanami A (2021) Spatial distribution of parrotfishes and groupers in an Okinawan coral reef: size-related associations in relation to habitat characteristics. PeerJ 9:e12134

    PubMed  PubMed Central  Google Scholar 

  • Nanami A, Nishihira M, Suzuki T, Yokochi H (2005) Species-specific habitat distribution of coral reef fish assemblages in relation to habitat characteristics in an Okinawan coral reef. Environ Biol Fishes 72:55–65

    Google Scholar 

  • Nicholson GM, Clements KD (2023) Micro-photoautotroph predation as a driver for trophic niche specialization in 12 syntopic Indo-Pacific parrotfish species. Biol J Linn Soc :blad005

  • Nicholson GM, Clements KD (2021) Ecomorphological divergence and trophic resource partitioning in 15 syntopic Indo-Pacific parrotfishes (Labridae: Scarini). Biol J Linn Soc 132:590–611

    Google Scholar 

  • Nicholson GM, Clements KD (2022) Scarus spinus, crustose coralline algae and cyanobacteria: an example of dietary specialization in the parrotfishes. Coral Reefs 41:1465–1479

    Google Scholar 

  • Nugraha WA, Newman SP, Mill AC, Polunin NV (2017) Caribbean parrotfish density and size inside and outside marine protected area. Aquac Aquar Conserv Legis 10:1257–1265

    Google Scholar 

  • Ogden JC, Buckman NS (1973) Movements, foraging groups, and diurnal migratons of the striped parrotfish Scarus croicensis Bloch (Scaridae). Ecology 54:589–596

    Google Scholar 

  • Öhman MC, Munday PL, Jones GP, Caley MJ (1998) Settlement strategies and distribution patterns of coral-reef fishes. J Exp Mar Biol Ecol 225:219–238

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Package ‘vegan’ Community ecology package, version R Package

  • Ortiz DM, Tissot BN (2008) Ontogenetic patterns of habitat use by reef-fish in a Marine Protected Area network: a multi-scaled remote sensing and in situ approach. Mar Ecol Prog Ser 365:217–232

    Google Scholar 

  • Paula JR, Sun D, Pissarra V, Narvaez P, Rosa R, Grutter AS, Sikkel PC (2021) The role of corals on the abundance of a fish ectoparasite in the Great Barrier Reef. Coral Reefs 40:535–542

    Google Scholar 

  • Pereira PHC, Araujo JC, Lima GV, Cortes LGF, Gomes E, Magris RA (2022) Effectiveness of management zones for recovering parrotfish species within the largest coastal marine protected area in Brazil. Sci Rep 12:12232

    CAS  PubMed  PubMed Central  Google Scholar 

  • Phoonjampa R, Koenig A, Borries C, Gale GA, Savini T (2010) Selection of sleeping trees in pileated gibbons (Hylobates pileatus). Am J Primatol 72:617–625

    PubMed  Google Scholar 

  • Pickholtz R, Kiflawi M, Crossin GT, Pickholtz EY, Zamsky R, Kahan I, Gavriel T, Belmaker J (2022) Highly repetitive space-use dynamics in parrotfishes. Coral Reefs 41:1059–1073

    Google Scholar 

  • Questel S-LA, Russ GR (2018) No-take marine reserve effects on parrotfish and parrotfish-benthos interactions Biology of parrotfishes. CRC Press, Boca Raton, pp 329–354

    Google Scholar 

  • R Development Core Team (2022) R: A language and environment for statistical computing

  • Radespiel U, Ehresmann P, Zimmermann E (2003) Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. Am J Primatol 59:139–151

    PubMed  Google Scholar 

  • Rattenborg NC, de la Iglesia HO, Kempenaers B, Lesku JA, Meerlo P, Scriba MF (2017) Sleep research goes wild: new methods and approaches to investigate the ecology, evolution and functions of sleep. Philos Trans R Soc Lond B Biol Sci 372:20160251

    PubMed  PubMed Central  Google Scholar 

  • Reinboth R (1968) Protogynie bei papageifischen (Scaridae). Zeitschrift Für Naturforschung B 23:852–855

    CAS  Google Scholar 

  • Robertson DR, Sheldon JM (1979) Competitive Interactions and the Availability of Sleeping Sites for a Diurnal Coral-Reef Fish. J Exp Mar Biol Ecol 40:285–298

    Google Scholar 

  • Robertson DR, Warner RR (1978) Sexual patterns in the labroid fishes of the Western Caribbean, II, the parrotfishes (Scaridae). Smithson Contrib Zool. https://doi.org/10.5479/si.00810282.255

    Article  Google Scholar 

  • Rogers A, Blanchard JL, Mumby PJ (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Curr Biol 24:1000–1005

    CAS  PubMed  Google Scholar 

  • Roos NC, Pennino MG, Carvalho AR, Longo GO (2019) Drivers of abundance and biomass of Brazilian parrotfishes. Mar Ecol Prog Ser 623:117–130

    Google Scholar 

  • Roos NC, Longo GO, Pennino MG, Francini-Filho RB, Carvalho AR (2020) Protecting nursery areas without fisheries management is not enough to conserve the most endangered parrotfish of the Atlantic Ocean. Sci Rep 10:1–10

    Google Scholar 

  • Rypel AL, Layman CA, Arrington DA (2007) Water depth modifies relative predation risk for a motile fish taxon in Bahamian tidal creeks. Estuar Coast 30:518–525

    Google Scholar 

  • Sachs BD (1988) The development of grooming and its expression in adult animals. Ann N Y Acad Sci 525:1–17

    CAS  PubMed  Google Scholar 

  • Santos TRN, Sikkel PC (2017) Habitat associations of fish-parasitic gnathiid isopods in a shallow reef system in the central Philippines. Mar Biodivers 49:83–96

    Google Scholar 

  • Sazima I, Ferreira CEL (2006) A cocoon-producing parrotfish in the Southwestern Atlantic. Coral Reefs 25:212–212

    Google Scholar 

  • Shimose T, Katahira H, Kanaiwa M (2020) Interspecific variation of prevalence by Scaphanocephalus (Platyhelminthes: Trematoda: Heterophyidae) metacercariae in parrotfishes (Labridae: Scarini) from an Okinawan coral reef. Int J Parasitol Parasites Wildl 12:99–104

    PubMed  PubMed Central  Google Scholar 

  • Shulman MJ (1985) Coral reef fish assemblages: intra-and interspecific competition for shelter sites. Environ Biol Fishes 13:81–92

    Google Scholar 

  • Singhal S, Johnson MA, Ladner JT (2007) The behavioral ecology of sleep: Natural sleeping site choice in three Anolis lizard species. Behaviour 144:1033–1052

    Google Scholar 

  • Smit NJ, Bruce NL, Hadfield KA (2019) Parasitic Crustacea: State of knowledge and future trends. Springer, Cham

    Google Scholar 

  • Strandburg-Peshkin A, Clutton-Brock T, Manser MB, Smiseth P (2019) Burrow usage patterns and decision-making in meerkat groups. Behav Ecol 31:292–302

    Google Scholar 

  • Taylor BM, Lindfield SJ, Choat JH (2015) Hierarchical and scale-dependent effects of fishing pressure and environment on the structure and size distribution of parrotfish communities. Ecography 38:520–530

    Google Scholar 

  • Tesch F-W, Bartsch P (2003) The eel. Wiley Online Library, Wiley

    Google Scholar 

  • Thieurmel B, Elmarhraoui A, Thieurmel MB (2019) Package ‘suncalc’ R Package

  • van Toor ML, Jaberg C, Safi K (2011) Integrating sex-specific habitat use for conservation using habitat suitability models. Anim Conserv 14:512–520

    Google Scholar 

  • Videler H, Geertjes GJ, Videler JJ (2005) Biochemical characteristics and antibiotic properties of the mucous envelope of the queen parrotfish. J Fish Biol 54:1124–1127

    Google Scholar 

  • Wakefield ED, Cleasby IR, Bearhop S, Bodey TW, Davies RD, Miller PI, Newton J, Votier SC, Hamer KC (2015) Long-term individual foraging site fidelity—why some gannets don’t change their spots. Ecology 96:3058–3074

    PubMed  Google Scholar 

  • Waldner RE, Robertson DR (1980) Patterns of habitat partitioning by eight species of territorial Caribbean damselfishes (Pisces: Pomacentridae). B Mar Sci 30:171–186

    Google Scholar 

  • Welsh JQ, Bellwood DR (2011) Spatial ecology of the steephead parrotfish (Chlorurus microrhinos): an evaluation using acoustic telemetry. Coral Reefs 31:55–65

    Google Scholar 

  • Williams DM (1991) Patterns and process in the distribution of coral reef fishes. In: Sale PF (ed) The ecology of fishes on coral reefs. Elsevier, Amsterdam, pp 437–474

    Google Scholar 

  • Winn H (1955) Formation of a mucous envelope at night by parrot fishes. Zoologica 40:145–149

    Google Scholar 

  • Winn HE, Bardach JE (1957) Behavior, Sexual Dichromatism, and Species of Parrot Fishes. Science 125:885–886

    CAS  PubMed  Google Scholar 

  • Winn HE, Bardach JE (1959) Differential food selection by moray eels and a possible role of the mucous envelope of parrot fishes in reduction of predation. Ecology 40:296–298

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Viviana Farstey for assisting in identification of Gnathiids from photographs and videos, Inbal Kahan for assistance with validating data entry and proofing, Daphna Shapiro-Goldberg for proofreading and language editing, and to the personnel of the IUI diving center for their logistic support.

Funding

This work was partially supported by a Grant from the Tel Aviv University Center for AI and Data Science (TAD) to JB, Y. Yovel and Y. Ram.

Author information

Authors and Affiliations

  1. School of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel

    Renanel Pickholtz, Yehezkel Buba, Shahar Chaikin, Tal Gavriel, Mai Lazarus, Shahar Malamud, Sagi Marom, Karin Olsson, Tal Perevolotsky, Shira Salingrè, Noy Shapira & Jonathan Belmaker

  2. Department of Life-Sciences, Ben-Gurion University of the Negev, POB 653, 84105, Beer-Sheva, Israel

    Moshe Kiflawi

  3. Institute of Earth Sciences, Hebrew University of Jerusalem, Jerusalem, Israel

    Gil Lapid

  4. The Interuniversity Institute for Marine Sciences of Eilat, 88103, Eilat, Israel

    Renanel Pickholtz, Moshe Kiflawi, Gil Lapid, Nir Marom, Sagi Marom, Tal Perevolotsky & Hava Wandel

  5. Steinhardt Museum of Natural History, Tel Aviv University, Tel Aviv, Israel

    Shahar Malamud, Shevy Bat-Sheva Rothman & Jonathan Belmaker

  6. The School of Marine Sciences, Ruppin Academic Center, 40297, Michmoret, Israel

    Maayan Nieger-Rachmilevitz & Bar Sternbach

  7. Marine-Monitoring, Lysekil, Sweden

    Karin Olsson

Authors
  1. Renanel Pickholtz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Moshe Kiflawi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yehezkel Buba
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shahar Chaikin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tal Gavriel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gil Lapid
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mai Lazarus
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shahar Malamud
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Nir Marom
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sagi Marom
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maayan Nieger-Rachmilevitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Karin Olsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tal Perevolotsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Shevy Bat-Sheva Rothman
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Shira Salingrè
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Noy Shapira
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Bar Sternbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Hava Wandel
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Jonathan Belmaker
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study was conceived by RP. Study design was performed by RP, MK, and JB. Fieldwork was performed by RP, YB, SC, TG, GL, ML, SM, NM, SM, MNR, KO, TP, SR, SS, NS, BS, HW, and JB. Analyses were performed by RP and supported by JB. The first draft of the manuscript was written by RP, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Renanel Pickholtz.

Ethics declarations

Conflicts of interest

We declare we have no conflicts of interest nor competing interests.

Ethical approval

Visual surveys using SCUBA did not entail handling or contact with animals and thus did not require additional permits (i.e., from a committee for ethical care and use of animals in experiments, nor the Israeli Nature and Parks Authority).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pickholtz, R., Kiflawi, M., Buba, Y. et al. Confronting the ‘nocturnal problem’ in coral reefs: sleeping site selection and cocoon formation in parrotfishes. Coral Reefs 42, 811–825 (2023). https://doi.org/10.1007/s00338-023-02389-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-023-02389-1

Keywords

Search

Navigation