Onset of zooplanktivory and optimal water flow rates for prey capture in newly settled polyps of ten Caribbean coral species
Tóm tắt
Zooplanktivory is an important source of nutrients in corals, providing up to 35% of daily metabolic energy requirements in some species. However, little is known about coral zooplanktivory shortly after larval settlement and metamorphosis. In most species it is unclear if, when and under which conditions newly settled polyps are able to capture and ingest prey. This remains a critical knowledge gap, as zooplanktivory could allow coral settlers to replenish energy reserves shortly after metamorphosis, possibly improving settler condition during one of their most vulnerable life stages. Here, we documented the onset of prey (Artemia salina nauplii) capture in ten Caribbean coral species and assessed optimal water flow rates (WFR) for prey capture in five of these species. All species initiated zooplanktivory within six days following metamorphosis, with the exception of Acropora palmata which was never observed capturing nauplii during our 20-day study. Optimal WFR for prey capture varied among species, with Favia fragum displaying maximum prey capture rates in zero flow and Diploria labyrinthiformis most effectively capturing nauplii under WFR of 5–20 cm s−1. Under each species’ optimum WFR, prey capture abilities varied considerably, with F. fragum capturing up to one nauplius every two minutes compared to one nauplius every nine minutes in Colpophyllia natans. Using these findings, we make species-specific recommendations to optimize coral husbandry and larval-based restoration practices for these ten coral species.
Tài liệu tham khảo
Aihara Y, Maruyama S, Baird AH, Iguchi A, Takahashi S, Minagawa J (2019) Green fluorescence from cnidarian hosts attracts symbiotic algae. Proc Natl Acad Sci U S A 116:2118–2123
Bak RPM (1975) Ecological aspects of the distribution of reef corals inthe Netherlands Antilles. Bijdr Tot Dierkd 45:181–190
Carrillo-Baltodano A, Morales-Ramirez A (2016) Changes in abundance and composition of a Caribbean coral reef zooplankton community after 25 years. Rev Biol Trop 64(3):1029–1040
Chamberland VF, Vermeij MJA, Brittsan M, Carl M, Schick M, Snowden S, Schrier A, Petersen D (2015) Restoration of critically endangered elkhorn coral (Acropora palmata) populations using larvae reared from wild-caught gametes. Glob Ecol Conserv 4:526–537
Chamberland VF, Latijnhouwers KRW, Huisman J, Hartmann AC, Vermeij MJA (2017) Costs and benefits of maternally inherited algal symbionts in coral larvae. Proc R Soc London B Biol Sci 284:20170852
Conlan JA, Humphrey CA, Severati A, Parrish CC, Francis DS (2019) Elucidating an optimal diet for captive Acropora corals. Aquaculture 513:734420
Cumbo VR, Fan TY, Edmunds PJ (2012) Scleractinian corals capture zooplankton within days of settlement and metamorphosis. Coral Reefs 31:1155
Dai C-F, Lin M-C (1993) The effects of flow on feeding of three gorgonians from southern Taiwan. J Exp Mar Biol Ecol 173:57–69
Edmunds PJ, Cumbo VR, Fan TY (2013) Metabolic costs of larval settlement and metamorphosis in the coral Seriatopora caliendrum under ambient and elevated pCO2. J Exp Mar Biol Ecol 443:33–38
Fabricius KE, Genin A, Benayahu Y (1995) Flow-dependent herbivory and growth in zooxanthellae-free soft corals. Limnol Oceanogr 40:1290–1301
Forsman ZH, Kimokeo BK, Bird CE, Hunter CL, Toonen RJ (2012) Coral farming: effects of light water motion and artificial foods. J Mar Biolog Assoc UK 92(4):721–729
Goreau TF, Goreau NI, Yonge CM (1971) Reef corals: autotrophs or heterotrophs? Biol Bull 141:247–260
Graham EM, Baird H, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Hata T, Madin JS, Cumbo VR, Denny M, Figueiredo J, Harii S, Thomas CJ, Baird AH (2017) Coral larvae are poor swimmers and require fine-scale reef structure to settle. Sci Rep 7:1–9
Higgins JE, Ford MD, Costello JH (2008) Transitions in morphology, nematocyst distribution, fluid motions, and prey capture during development of the scyphomedusa Cyanea capillata. Biol Bull 214:29–41
Hirose M, Kinzie RA III, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280
Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17
Huettel M, Wild C, Gonelli S (2006) Mucus trap in coral reefs: formation and temporal evolution of particle aggregates caused by coral mucus. Mar Ecol Prog Ser 307:69–84
IBM Corp. (2016) IBM SPSS Statistics for Windows, Version 24.0.
Jacobson LM, Edmunds PJ (2010) Long-term changes in the concentration of zooplankton and particulate material over a fringing reef in St. John, US Virgin Islands. Bull Mar Sci 86(3):763–772
Koehl AR, Strother JA, Reidenbach MA, Koseff JR, Hadfield MG (2007) Individual-based model of larval transport to coral reefs in turbulent, wave-driven flow: behavioral responsdes to dissolved settlement inducer. Mar Ecol Prog Ser 335:1–18
Latijnhouwers KRW, Ter Horst L, Schneider J, Van Duijnhoven J, Miller M, Vermeij MJAV, Chamberland, VF (2022) Feeding of coral settlers in large in situ mesocosms greatly increases their long term survival. Abstract Book, 15th International Coral Reef Symposium, p 980
Leal MC, Ferrier-Pagès C, Petersen D, Osinga R (2014) Coral aquaculture: applying scientific knowledge to ex situ production. Rev Aquac 8:136–153
Leichter JJ, Shellenbarger G, Genovese SJ, Wing SR (1998) Breaking internal waves on a Florida (USA) coral reef: A plankton pump at work? Mar Ecol Prog Ser 166:83–97
Lewis JB (1974) The importance of light and food upon the early growth of the reef coral Favia fragum (esper). J Exp Mar Biol Ecol 15:299–304
Lewis JB, Price WS (1975) Feeding mechanisms and feeding strategies of Atlantic reef corals. J Zool 176:527–544
Marhaver KL, Vermeij MJA, Medina MM (2015) Reproductive natural history and successful juvenile propagation of the threatened Caribbean Pillar Coral Dendrogyra cylindrus. BMC Ecol 15:9
McClounan S, Seymour J (2012) Venom and cnidome ontogeny of the cubomedusae Chironex fleckeri. Toxicon 60:1335–1341
Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. In: Dubinsky Z (ed) Ecosystems of the World, Coral Reefs, vol 25. Elsevier Science Publishing Company, Inc, Amsterdam, The Netherlands, pp 75–87
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460
NOAA Coral Reef Watch (2018) Daily global 5-km satellite virtual station time series data for Curaçao and Aruba, Jan. 01-Dec. 31, 2018. College Park, Maryland, USA. http://coralreefwatch.noaa.gov/satellite/vs/caribbean.php
NOAA Coral Reef Watch (2020) Daily global 5-km satellite virtual station time series data for Curaçao and Aruba, Jan. 01-Dec. 31, 2020. College Park, Maryland, USA. http://coralreefwatch.noaa.gov/satellite/vs/caribbean.php
Osinga R, Schutter M, Griffioen B, Wijffels RH, Verreth JAJ, Shafir S, Henard S, Taruffi M, Gili C, Lavorano S (2011) The biology and economics of coral growth. Mar Biotechnol 13:658–671
Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 300:79–89
Palardy JE, Grottoli AG, Matthews KA (2006) Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific. J Exp Mar Biol Ecol 331:99–107
Petersen D, Wietheger A, Laterveer M (2008) Influence of different food sources on the initial development of sexual recruits of reefbuilding corals in aquaculture. Aquaculture 277:174–178
Porter JW (1976) Autotrophy, heterotrophy, and resource partitioning in Caribbean reef-building corals. Am Nat 110:731–742
Randall CJ, Negri AP, Quigley KM, Foster T, Ricardo GF, Webster NS, Bay LK, Harrison PL, Babcock RC, Heyward AJ (2020) Sexual production of corals for reef restoration in the Anthropocene. Mar Ecol Prog Ser 635:203–232
Ritson-Williams R, Arnold SN, Paul VJ (2016) Patterns of larval settlement preferences and post-settlement survival for seven Caribbean corals. Mar Ecol Prog Ser 548:127–138
Schutter M, Kranenbarg S, Wijffels RH, Verreth J, Osinga R (2011) Modification of light utilization for skeletal growth by water flow in the scleractinian coral Galaxea fascicularis. Mar Biol 158:769–777
Sebens KP, Johnson AS (1991) Effects of water movement on prey capture and distribution of reef corals. Hydrobiologia 216–217:247–248
Sebens KP, Vandersall KS, Savina LA, Graham KR (1996a) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–331
Sebens KP, Grace SP, Helmuth B, Maney EJ, Miles JS (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernoss and Porites porites in a field enclosure. Mar Biol 131:347–360
Sebens KP (1997) Adaptive responses to water flow: morphology, energetics and distribution of reef corals. In: Proceedings 8th international coral reef symposium, pp 1053–1058
Sorek M, Diaz-Almeyda EM, Medina M, Levy O (2014) Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar Genomics 14:47–57
Suzuki G, Yamashita H, Kai S, Hayashibara T, Suzuki K, Iehisa Y, Okada W, Ando W, Komori T (2013) Early uptake of specific symbionts enhances the post-settlement survival of Acropora corals. Mar Ecol Prog Ser 494:149–158
Szmant-Froelich A, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum: lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892
Toh TC, Peh JWK, Chou LM (2013a) Early onset of zooplanktivory in equatorial reef coral recruits. Mar Biodivers 43:177–178
Toh TC, Peh JWK, Chou LM (2013b) Heterotrophy in recruits of the scleractinian coral Pocillopora damicornis. Mar Freshw Behav Physiol 46:313–320
Toh TC, Ng CSL, Peh JWK, Ben TK, Chou LM (2014) Augmenting the post-transplantation growth and survivorship of juvenile scleractinian corals via nutritional enhancement. PLoS ONE 9:e98529
Tomascik T, Sander F (1987) Effects of eutrophication on reef-building corals - III. Reproduction of the reef-building coral Porites porites. Mar Biol 94:77–94
Vermeij MJA, Sandin SA (2008) Density-dependent settlement and mortality structure the earliest life phases of a coral population. Ecology 89:1994–2004
Vermeij MJA, Fogarty ND, Miller MW (2006) Pelagic conditions affect larval behavior, survival, and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119–128
Vermeij MJ, Chamberland VF, Marhaver KL (2021) Coral Spawning Predictions for the Southern Caribbean 2007–2021. CARMABI, Curacao. https://www.researchstationcarmabi.org/predictions-for-coral-spawning-events-in-the-southern-caribbean-for-2022/
Wijgerde T, Diantari R, Lewaru MW, Verreth JAJ, Osinga R (2011) Extracoelenteric zooplankton feeding is a key mechanism of nutrient acquisition for the scleractinian coral Galaxea fascicularis. J Exp Biol 214:3351–3357
Wijgerde T, Spijkers P, Karruppannan E, Verreth JAJ, Osinga R (2012) Water flow affects zooplankton feeding by the scleractinian coral Galaxea fascicularis on a polyp and colony level. J Mar Biol 2012:1–7
Yahel R, Yahel G, Berman T, Jaffe JS, Genin A (2005) Diel pattern with abrupt crepuscular changes of zooplankton over a coral reef. Limnol Oceanogr 50(3):930–944