Abstract
Pontellid copepods are archetypical representatives of the neuston—the highly specialized community living in the top 5–10 cm of the ocean surface. Their deep blue pigmentation and large eyes are unique adaptations to surface irradiation and carnivory, but poor prerequisites for survival in the transparent waters beneath the sea surface. Here, we report the discovery of three reef-associated representatives of this group—Labidocera bataviae A. Scott, 1909; L. pavo Giesbrecht, 1889; and Labidocera sp.—living residential in coral reefs. We (1) document the presence of Labidocera spp. for two separate coral reefs on two expeditions to Papua New Guinea, (2) describe their migration behavior and substrate preference, and (3) quantify the effects of benthic reef community composition on their abundance. All life stages of Labidocera spp. were 43 to 94 times more abundant at the reef sites compared to offshore sites. Although pontellids are generally considered non-migrators, Labidocera spp. showed discernible diel vertical migrations: living in reef substrates during the day, emerging into the water column at night (sometimes more than once), and returning to the substrate at dawn. Labidocera spp. showed a pronounced substrate preference for coral rubble, microalgae, and turf, over branching coral, massive boulder coral, and sand.
Similar content being viewed by others
References
Alldredge AL, King JM (1977) Distribution, abundance, and substrate preferences of demersal reef zooplankton at Lizard Island lagoon, Great Barrier Reef. Mar Biol 41:317–333. https://doi.org/10.1007/BF00389098
Alldredge AL, King JM (1985) The distance demersal zooplankton migrate above the benthos: implications for predation. Mar Biol 84:253–260. https://doi.org/10.1007/BF00392494
Alldredge AL, King JM (1980) Effects of moonlight on the vertical migration patterns of demersal zooplankton. J Exp Mar Bio Ecol 44:133–156. https://doi.org/10.1016/0022-0981(80)90150-1
Allen R, Foggo A, Fabricius K et al (2016) Tropical CO2 seeps reveal the impact of ocean acidification on coral reef invertebrate recruitment. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2016.12.031
Alvarez-Cadena JN, Suarez-Morales E, Gasca R (2014) Copepod assemblages from a reef-related environment in the Mexican Caribbean Sea. Crustaceana 71:411–433
Boxshall GA, Halsey SH (2004) An introduction to copepod diversity, volume 2. Ray Society, London
Brady GS (1883) Report on the Copepoda collected by H.M.S. challenger during the years 1873-1876. Rep Sci Results Voy Chall Zool 8:1–142
Carleton J, Hamner W (2007) The hyperbenthic plankton community: composition, distribution, and abundance in a coral reef lagoon. Mar Ecol Prog Ser 336:77–88. https://doi.org/10.3354/meps336077
Carleton JH (1993) Zooplankton and coral reefs: an overview. South Pacific Underw Med Soc 23:102–107
Carleton JH, McKinnon AD (2007) Resident mysids: secondary production, consumption, and trophic role in a coral reef lagoon. Mar Ecol Prog Ser 336:89–98. https://doi.org/10.3354/meps336089
Chew L-L, Chong VC, Ooi AL, Sasekumar A (2015) Vertical migration and positioning behavior of copepods in a mangrove estuary: interactions between tidal, diel light and lunar cycles. Estuar Coast Shelf Sci 152:142–152. https://doi.org/10.1016/j.ecss.2014.11.011
Clarke GL (1934) The diurnal migration of copepods in St. Georges harbor, Bermuda. Biol Bull 67:456–460
Cohen JH, Forward RB (2002) Spectral sensitivity of vertically migrating marine copepods. Biol Bull 203:307–314. https://doi.org/10.2307/1543573
Cohen Y, Cohen JY (2008) Statistics and data with R: an applied approach through examples. John Wiley & Sons Ltd., Chichester, West Sussex, UK
Conley WJ, Turner JT (1985) Omnivory by the coastal marine copepods Centropages hamatus and Labidocera aestiva. Mar Ecol Prog Ser 21:113–120. https://doi.org/10.3354/meps021113
Donelson J, Munday P, McCormick M et al (2010) Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243. https://doi.org/10.3354/meps08366
Emery AR (1968) Preliminary observations on coral reef plankton. Limnol Oceanogr 13:293–303. https://doi.org/10.4319/lo.1968.13.2.0293
Fabricius KE, De’ath G, Noonan S, Uthicke S (2014) Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc R Soc B biol Sci 281:20132479. Doi: 20132479
Fabricius KE, Langdon C, Uthicke S et al (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169. https://doi.org/10.1038/nclimate1122
Fancett MS, Kemmerrer WJ (1985) Vertical migration of a demersal copepod Pseudodiaptomus as a means of predator avoidance. J Exp Mar Bio Ecol 88:31–43
Ferrier-Pagès C, Hoogenboom M, Houlbrèque F (2011) The role of plankton in coral trophodynamics. Springer Science
Fukuoka K, Shimoda T, Abe K (2015) Community structure and abundance of copepods in summer on a fringing coral reef off Ishigaki Island, Ryukyu Islands, Japan. Plankt Benthos Res 10:225–232. doi: https://doi.org/10.3800/pbr.10.225
Gemmell BJ, Jiang H, Strickler JR, Buskey EJ (2012) Plankton reach new heights in effort to avoid predators. Proc R Soc B Biol Sci 279:2786–2792. https://doi.org/10.1098/rspb.2012.0163
Genin A, Jaffe JS, Reef R et al (2005) Swimming against the flow: a mechanism of zooplankton aggregation. Science 308:860–862. https://doi.org/10.1126/science.1107834
Gibson VR, Grice GD (1977) The developmental stages of Labidocera aestiva wheeler, 1900 (Copepoda, Calanoida)
Hairston NC (1976) Photoprotection by carotenoid pigments in the copepod Diaptomus nevadensis. Proc Natl Acad Sci U S A 73:971–974. https://doi.org/10.1073/pnas.73.3.971
Hammer RM (1981) Day-night differences in the emergence of demersal zooplankton from a sand substrate in a kelp forest. Mar Biol 62:275–280. https://doi.org/10.1007/BF00397694
Hamner WM, Carleton JH (1979) Copepod swarms: attributes and role in coral reef ecosystems. Limnol Oceanogr 24:1–14
Hamner WM, Jones MS, Carleton JH et al (1988) Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Bull Mar Sci 42:459–479
Hansson L-A (2000) Induced pigmentation in zooplankton: a trade-off between threats from predation and ultraviolet radiation. Proc R Soc London B 267:2327–2331. https://doi.org/10.1098/rspb.2000.1287
Hansson L-A, Hylander S, Sommaruga R (2007) Escape from UV threats in zooplankton: a cocktail of behavior and protective pigmentation. Ecology 88:1932–1939. https://doi.org/10.1890/06-2038.1
Heidelberg KB, Sebens KP, Purcell JE (2004) Composition and sources of near reef zooplankton on a Jamaican forereef along with implications for coral feeding. Coral Reefs 23:263–276. https://doi.org/10.1007/s00338-004-0375-0
Herring PJ (1965) Blue pigment of surface-living oceanic copepod. Nature 4966:103–104
Hirabayashi T, Ohtsuka S (2014) A new species of Labidocera (Copepoda, Calanoida, Pontellidae) collected from Okinawa, southwestern Japan, with establishment of five indo-West Pacific species groups in the L. detruncata species complex. Zookeys 447:21–34. https://doi.org/10.3897/zookeys.447.8171
Hobson ES (1991) Trophic relationships of fishes specialized to feed on zooplankters above coral reefs. The ecology of fishes on coral reefs. Academic Press, San Diego 69–95
Hobson ES (1973) Diel feeding migrations in tropical reef fishes. Helgolander Wissenschaftliche Meeresuntersuchungen 24:361–370. https://doi.org/10.1007/BF01609526
Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17. https://doi.org/10.1111/j.1469-185X.2008.00058.x
Hsiao Y-H, Dahms H-U, Hwang J-S (2013) Ecology of swarming in the planktonic copepod Dioithona sp. (Crustacea: Copepoda). J Nat Hist 47:739–751. https://doi.org/10.1080/00222933.2012.724717
Hunt ME, Scherrer MP, Ferrari FD, Matz MV (2010) Very bright green fluorescent proteins from the pontellid copepod Pontella mimocerami. PLoS One 5:3–10. https://doi.org/10.1371/journal.pone.0011517
Ikeda T, Hing Fay E, Hutchinson S, Boto G (1982) Ammonia and inorganic phosphate excretion by zooplankton from inshore waters of the Great Barrier Reef, Queensland. I. Relationship between excretion rates and body size. Mar Freshw Res 33:55. https://doi.org/10.1071/MF9820055
Jacoby CA, Greenwood JG (1988) Spatial, temporal, and behavioral patterns in emergence of zooplankton in the lagoon of Heron Reef, Great Barrier Reef, Australia. Mar Biol 97:309–328. https://doi.org/10.1007/BF00397762
Jacoby C, Greenwood J (1989) Emergent zooplankton in Moreton Bay, Queensland, Australia: seasonal, lunar, and diel patterns in emergence and distribution with respect to substrata. Mar Ecol Prog Ser 51:131–154. https://doi.org/10.3354/meps051131
Jeong HG, Suh HL, Jeong SB et al (2009) Labidocera species (Copepoda: Pontellidae) in waters of the Tsushima warm current with notes on their genital structure and zoogeography. Zool Stud 48:508–523
Kangtia P, Dahms H, Song SJ, Myoung J (2014) On the occurrence of a new species of benthic copepod, Zaus wonchoelleei (Harpacticoida, Harpacticidae), in a macroalgal habitat from Tongyong, Korea. Proc Biol Soc Washingt 127:585–602
Kimmerer WJ, Burau JR, Bennett WA (1998) Tidally-oriented vertical migration and position maintenance of zooplankton in a temperate estuary. Limnol Oceanogr 43:1697–1709. https://doi.org/10.4319/lo.1998.43.7.1697
Kimmerer WJ, McKinnon AD (1987) Zooplankton in a marine bay II. Vertical migration to maintain horizontal distributions. Mar Ecol Prog Ser 41:53–60. https://doi.org/10.3354/meps041053
Kramer MJ, Bellwood DR, Bellwood O (2013) Emergent fauna from hard surfaces on the Great Barrier Reef, Australia. Mar Freshw Res 64:687–691. https://doi.org/10.1071/MF12284
Land M (1988) The functions of eye and body movements in Labidocera and other copepods. J Exp Biol 391:381–391
Lewis JB, Boers JJ (1991) Patchiness and composition of coral reef demersal zooplankton. J Plankton Res 13:1273–1289. https://doi.org/10.1093/plankt/13.6.1273
Logan D, Townsend KA, Townsend K, Tibbetts IR (2008) Meiofauna sediment relations in leeward slope turf algae of Heron Island reef. Hydrobiologia 610:269–276. https://doi.org/10.1007/s10750-008-9442-9
Madhupratap M, Achuthankutty CT, Nair SRS (1991) Estimates of high absolute densities and emergence rates of demersal zooplankton from the Agatti atoll, Laccadives. Limnol Oceanogr 36:585–588. https://doi.org/10.4319/lo.1991.36.3.0585
Matsuo Y, Marumo R (1982) Diurnal vertical migration of pontellid copepods in the Kuroshio. Bull Plankt Soc Jap 29:89–98
Mauchline J (1988) The biology of Calanoid copepods. Academic Press
McKinnon AD (1991) Community composition of reef associated copepods in the lagoon of Davies Reef, Great Barrier Reef, Australia. Bull. Plankt. Soc. Japan 467–478
McWilliam PS, Sale PF, Anderson DT (1981) Seasonal changes in resident zooplankton sampled by emergence traps in One Tree Lagoon, Great Barrier Reef. J Exp Mar Bio Ecol 52:185–203. https://doi.org/10.1016/0022-0981(81)90036-8
Mojib N, Amad M, Thimma M et al (2014) Carotenoid metabolic profiling and transcriptome-genome mining reveal functional equivalence among blue-pigmented copepods and appendicularia. Mol Ecol 23:2740–2756. https://doi.org/10.1111/mec.12781
Mulyadi (2002) The calanoid copepods family Pontellidae from Indonesian waters, with notes on its species-groups
Nakajima R, Yoshida T, Othman BHR, Toda T (2008) Diel variation in abundance, biomass and size composition of zooplankton community over a coral-reef in Redang Island, Malaysia. Plankt Benthos Res 3:216–226. https://doi.org/10.3800/pbr.3.216
Ohlhorst SL (1982) Diel migration patterns of demersal reef zooplankton. J Exp Mar Biol Ecol 60:1–15
Ohtsuka S, Fosshagen A, Soh HY (1996) Three new species of the demersal calanoid copepod Placocalanus (Ridgewayiidae) from Okinawa, southern Japan. Sarsia 81:247–263. https://doi.org/10.1080/00364827.1996.10413623
Pessoa VT, Melo PAMC, Melo Junior M, Neumann-Leitao S (2014) Population dynamics of Calanopia americana Dahl F., 1894 (Copepoda, Calanoida) in a reef environment in tropical Brazil. Trop Oceanogr 42:24–32
Porter JW (1974) Zooplankton feeding by the Caribbean reef-building coral Montastrea cavernosa. Proc Second Int Coral Reef Symp 1:111–125
Porter JW, Porter KG (1977) Quantitative sampling of demersal plankton migrating from different coral reef substrates. Limnol Oceanogr 22:553–556
Robichaux DM, Cohen AC, Reaka ML, Allen D (1981) Experiments with zooplankton on coral reefs, or will the real demersal plankton please come up? Mar Ecol 2:77–94. https://doi.org/10.1111/j.1439-0485.1981.tb00092.x
Saigusa M, Oishi K (2000) Emergence rhythms of subtidal small invertebrates in the subtropical sea: nocturnal patterns and variety in the synchrony with tidal and lunar cycles. Zool Sci 17:241–251. https://doi.org/10.2108/zsj.17.241
Saigusa M, Okochi T, Ikei S (2003) Nocturnal occurrence, and synchrony with tidal and lunar cycles, in the invertebrate assemblage of a subtropical estuary. Acta Oecol 24:191–204. https://doi.org/10.1016/S1146-609X(03)00034-1
Sale PF, McWilliam PS, Anderson DT (1978) Faunal relationships among the near-reef zooplankton at three locations on Heron Reef, Great Barrier Reef, and seasonal changes in this fauna. Mar Biol 49:133–145. https://doi.org/10.1007/BF00387113
Scott A (1909) The Copepoda of the Siboga expedition. Part 1. Free-swimming, littoral and semi-parasitic Copepoda. E.J. Brill, Leydon
Sherman K (1962) Pontellid copepod distribution in relation to surface water types in the central North Pacific. Limnol Oceanogr 8:214–227
Sherman K (1964) Pontellid copepod occurrence in the central South Pacific. Limnol Oceanogr 9:476–484
Silas EG, Pillai P (1973) The calanoid copepod family Pontellidae from the Indian Ocean. J Mar Biol Assoc India 15:771–858
Smith JN, De’ath G, Richter C et al (2016) Ocean acidification reduces demersal zooplankton that reside in tropical coral reefs. Nat Clim Chang 6:1124–1129. https://doi.org/10.1038/nclimate3122
Sorokin YI, Sorokin PY (2010) Plankton of the central Great Barrier Reef: abundance, production and trophodynamic roles. J Mar Biol Assoc United Kingdom 90:1173–1187. https://doi.org/10.1017/S0025315410000597
Tester PA, Cohen JH, Cervetto G (2004) Reverse vertical migration and hydrographic distribution of Anomalocera ornata (Copepoda: Pontellidae) in the US South Atlantic bight. Mar Ecol Prog Ser 268:195–203. https://doi.org/10.3354/meps268195
Turner JT, Collard SB (1980) Winter distribution of pontellid copepods in the neuston of the eastern Gulf of Mexico continental shelf. Bull Mar Sci 30:526–530
Ueda H, Kuwahara A, Tanaka N, Azeta M (1983) Underwater observations on copepod swarms in temperate and subtropical waters. Mar Ecol Prog Ser 11:165–171. https://doi.org/10.3354/meps011165
Ueda H, Kuwatani M, Suzuki KW (2010) Tidal vertical migration of two estuarine copepods: Naupliar migration and position-dependent migration. J Plankton Res 32:1557–1572. https://doi.org/10.1093/plankt/fbq078
van Duren LA, Videler JJ (1995) Swimming behavior of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Mar Ecol Prog Ser 126:153–161
Walters K, Bell SS (1994) Significance of copepod emergence of benthic, pelagic, and phytal linkages in a subtidal seagrass bed. Mar Ecol Prog Ser 108:237–250. https://doi.org/10.3354/meps108237
Yahel R, Yahel G, Berman T et al (2005) Diel pattern with abrupt crepuscular changes of zooplankton over a coral reef. Limnol Oceanogr 50:930–944. https://doi.org/10.4319/lo.2005.50.3.0930
Youngbluth MJ (1982) Sampling demersal zooplankton: a comparison of field collections using three different emergence traps. J Exp Mar Biol Ecol 61:111–124
Zagalsky PF, Herring PJ (1972) Studies on a carotenoprotein isolated from the copepod, Labidocera acutifrons, and its relationship to the decapod carotenoproteins and other polyene-binding proteins. Comp Biochem Physiol Part B Comp Biochem 41:397–415
Zaret TM, Suffern S (1976) Vertical migration in zooplankton as a predator avoidance mechanism. Limnol Oceanogr 6:804–813
Acknowledgements
Special thanks to Obedi Daniel, Robin (‘Lei’) Luke, Julia Strahl, Sam Noonan, Alfred Sauwa, and crew members from the M/V Chertan for field assistance. This project was funded in part by the Erasmus Mundus-funded MARES Joint Doctoral Programme on Marine Ecosystem Health & Conservation (FPA 2011-0016), the Great Barrier Reef Foundation’s ‘Resilient Coral Reefs Successfully Adapting to Climate Change’ Program in collaboration with the Australian Government, the BIOACID Phase II Programme of the German Science Ministry BMBF (Grant 03F0655B), and the Australian Institute of Marine Science.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by P. Martinez Arbizu
Rights and permissions
About this article
Cite this article
Smith, J., Richter, C., Fabricius, K. et al. Neustonic copepods (Labidocera spp.) discovered living residentially in coral reefs. Mar Biodiv 49, 345–355 (2019). https://doi.org/10.1007/s12526-017-0810-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-017-0810-4