Abstract
In spite of the paramount ecological and socioeconomic relevance of tropical reef ecosystems, the dynamics of their meroplankton abundance remain poorly characterized. The small-scale distribution and detailed analysis of individual biomass of mesozooplankton were studied in the coastal reefs of Tamandaré (Brazil). Mesozooplankton (> 300 μm) was collected during nocturnal ebb tides at new moon, using three different devices to sample at three different environments: a standard ring net that was towed at subsurface, the Channel Midwater Neuston Net that collected at midwater in channels between patch reefs and the Reef Edge Net that captured organisms that are washed by ebb currents from reef tops toward the reef edge. Samples were analyzed using a ZooScan to obtain abundances and biovolume of each taxonomic group. Specific biomass measurements were taken to obtain allometric equations used to calculate zooplankton biomass from biovolume. The mesozooplankton were significantly more abundant at subsurface and at the reef edge compared to channel environments. The high abundance of organisms at reef edges suggests a low predation pressure on zooplankton at near-bottom areas, since the reefs of Tamandaré present a low coverage of planktivorous corals, being dominated by macroalgae. These results show that rather than sinks these ecosystems may be considered important sources of zooplankton available for planktivorous species. Regarding zooplankton composition, we found large amounts of initial stages of meroplanktonic larvae and newly hatched fish eggs, which presented consistently greater abundances compared to holoplankton and emergent benthic taxa. Decapod larvae were the most abundant group of the meroplankton, but cirripedian nauplii, stomatopod larvae, fish larvae and fish eggs were also abundant. More than 50% of the total biomass was due to meroplankton taxa, mainly composed of decapod larvae. This study indicates that the contribution of meroplankton to mesozooplankton composition and biomass off tropical reefs may have been underestimated.
Similar content being viewed by others
References
Acosta CA, Mark J, Butler IV (1999) Adaptive strategies that reduce predation on Caribbean spiny lobster postlarvae during onshore transport. Limnol Oceanogr 44:494–501
Alldredge AL, King JM (1985) The distance demersal zooplankton migrate above the benthos: implications for predation. Mar Biol 84:253–260
Alldredge AL, King JM (2009) Near-surface enrichment of zooplankton over a shallow back reef: implications for coral reef food webs. Coral Reefs 28:895–908
Anger K (2001) The biology of decapod crustacean larvae. In: Balkema AA (ed) Crustacean Issues. Lisse, The Netherlands, pp 1–419
Aschenbrenner A, Ferreira BP, Rooker JR (2016) Spatial and temporal variability in the otolith chemistry of the Brazilian snapper Lutjanus alexandrei from estuarine and coastal environments. J Fish Biol 89:753–769
Barbosa CF, Prazeres MF, Ferreira BP, Seoane JCS (2009) Foraminiferal assemblage and reef check census in coral reef health monitoring of East Brazilian margin. Mar Micropaleontol 73:62–69
Bessa E, Sabino J (2012) Territorial hypothesis predicts the trade off between reproductive opportunities and parental care in three species of damselfishes (Pomacentridae: Actinopterygii). Lat Am J Aquat Res 40:134–141
Brandão MC, Garcia CAE, Freire AS (2015) Large-scale spatial variability of decapod and stomatopod larvae along the South Brazil Shelf. Cont Shelf Res 107:11–23
D’Agostini A, Gherardi DFM, Pezzi LP (2015) Connectivity of marine protected areas and its relation with total kinetic energy. PLoS One 10:e0139601
Echelman T, Fishelson L (1990) Surface zooplankton dynamics and community structure in the Gulf of Aqaba (Eilat), Red Sea. Mar Biol 107:179–190
Feitosa JLL, Ferreira BP (2015) Distribution and feeding patterns of juvenile parrotfish on algal-dominated coral reefs. Mar Ecol 36:462–474
Feitosa JLL, Concentino AM, Teixeira SF, Ferreira BP (2012) Food resource use by two territorial damselfish (Pomacentridae: Stegastes) on South-Western Atlantic algal-dominated reefs. J Sea Res 70:42–49
Forward JRB (1987) Larval release rhythms of decapod crustaceans: An Overview. Mar Pollut Bull 41:165–176
Francini-Filho RB, Coni EOC, Ferreira CM, Alves AC, Rodrigues LS, Amado-Filho GM (2012) Group nest clearing behavior by the sergeant major Abudefduf saxatilis (Pisces: Pomacentridae). Mar Pollut Bull 88:195–196
Francini-Filho RB, Coni EO, Meirelles PM, Amado-Filho GM, Thompson FL, Pereira-Filho GH, Bastos AC, Abrantes DP, Ferreira CM, Gibran FZ, Guth AZ, Sumida PY, Oliveira NL, Kaufman L, Minte-Vera CV, Moura RL (2013) Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS One 8:e54260
Francini CLB, Castro CB, Pires DO (2002) First record of a reef coral spawning event in the western South Atlantic. Invertebr Repr Dev 42:17–19
Gilchrist SL (2003) Hermit crab population ecology on a shallow coral reef (Bailey’s Cay, Roatan, Honduras): octopus predation and hermit crab shell use. Mem Mus Vic 60:35–44
Giraldes BW, Coelho Filho PA, Smyth DM (2015) Decapod assemblages in subtidal and intertidal zones—Importance of scuba diving as a survey technique in tropical reefs, Brazil. Glob Ecol Conserv 3:163–175
Gorsky G, Ohman MD, Picheral M, Gasparini S, Stemmann L, Romagnan J-B, Cawood A, Pesant S, García-Comas C, Prejger F (2010) Digital zooplankton image analysis using the ZooScan integrated system. J Plankton Res 32:285–303
Grosjean P, Picheral M, Warembourg C, Gorsky G (2004) Enumeration, measurement, and identification of net zooplankton samples using the ZOOSCAN digital imaging system. ICES J Mar Sci 61:518–525
Hamner WM, Carleton JH (1979) Copepod swarms: attributes and role in coral reef ecosystems. Limnol Oceanogr 24:1–14
Hamner WM, Colin PL, Hamner PP (2007) Export–import dynamics of zooplankton on a coral reef in Palau. Mar Ecol Prog Ser 334:83–92
Hamner WM, Jones DL, Carleton JH, Hauri IR, Williams DM (1988) Zooplankton, planktivorous fish, and water currents on a windward reef face: Great Barrier Reef, Australia. Mar Pollut Bull 42:459–479
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
Heidelberg KB, O’Neil KL, Bythell JC, Sebens KP (2010) Vertical distribution and diel patterns of zooplankton abundance and biomass at Conch Reef, Florida Keys (USA). J Plankton Res 32:75–91
Hobson ES (1991) Trophic relationships of fishes specialized to feed on zooplankters above coral reefs. In: Sale PF (ed) The Ecology of Fishes on Coral Reefs. Academic Press, Massachusetts, pp 69–95
Holzman R, Genin A (2003) Zooplanktivory by a nocturnal coral-reef fish effects of light, flow, and prey density. Limnol Oceanogr 48:1367–1375
Holzman R, Reidenbach MA, Monismith SG, Koseff JR, Genin A (2005) Near-bottom depletion of zooplankton over a coral reef II: relationships with zooplankton swimming ability. Coral Reefs 24:87–94
Jeffs AG, Montgomery JC, Tindle CT (2005) How do spiny lobster post-larvae find the coast? New Zeal J Mar Fresh 39:605–617
Johnson WS, Allen DM, Fylling M (2012a) Amphipods, Isopods, Tanaidaceans, and Cumaceans. In: Johnson WS, Allen DM (eds) Zooplankton of the Atlantic and Gulf Coasts: A guide to their identification and ecology. The Johns Hopkins University Press, Baltimore, pp 198–217
Johnson WS, Allen DM, Fylling M (2012b) Mysids: Opossum Shrimps. In: Johnson WS, Allen DM (eds) Zooplankton of the Atlantic and Gulf Coasts: A guide to their identification and ecology. The Johns Hopkins University Press, Baltimore, pp 184–197
Jones KMM (2005) The effect of territorial damselfish (family Pomacentridae) on the space use and behaviour of the coral reef fish, Halichoeres bivittatus (Bloch, 1791) (family Labridae). J Exp Mar Bio Ecol 324:99–111
Kough AS, Paris CB (2015) The influence of spawning periodicity on population connectivity. Coral Reefs 34:753–757
Leão ZM, Dominguez JML (2000) Tropical coast of Brazil. Mar Pollut Bull 41:112–122
Leão ZM, Kikuchi RK (2005) A relic coral fauna threatened by global changes and human activities, Eastern Brazil. Mar Pollut Bull 51:599–611
Lucatelli D, Bezerra LEA, Santos PJP, Coelho PA (2012) Checklist of Stomatopoda (Malacostraca: Hoplocarida) deposited in the MOUFPE collection, with a new record from Brazil. Nauplius 20:257–293
Macdonald KS, Rios R, Duffy JE (2006) Biodiversity, host specificity, and dominance by eusocial species among sponge-dwelling alpheid shrimp on the Belize Barrier Reef. Divers Distrib 12:165–178
Maida M, Ferreira BP (1997) Coral reefs of Brazil: an overview. Proc 8th Int Coral Reef Symp 1:263–274
Marcolin CR, Schultes S, Jackson GA, Lopes RM (2013) Plankton and seston size spectra estimated by the LOPC and ZooScan in the Abrolhos Bank ecosystem (SE Atlantic). Cont Shelf Res 70:74–87
Mayal EM, Neumann-Leitão S, Feitosa FAN, Schwamborn R, Silva TA, Silva-Cunha MGG (2009) Hydrology, plankton, and corals of the Maracajaú Reefs (Northeastern Brazil) - an ecosystem under severe thermal stress. Braz Arch Biol Technol 52:665–678
McCammon A, Sikkel PC, Nemeth D (2010) Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment. Coral Reefs 29:419–426
McKeon CS, Moore JM (2014) Species and size diversity in protective services offered by coral guard-crabs. PeerJ 2:1–15
Melo PAMC, Silva TA, Neumann-Leitão S, Schwamborn R, Gusmão LMO, Porto Neto F (2010) Demersal zooplankton communities from tropical habitats in the southwestern Atlantic. Mar Biol Res 6:530–541
Morgan SG, Christy JH (1995) Adaptive significance of the timing of larval release by Crabs. Am Nat 145:457–479
Motoda S (1959) Devices of simple plankton apparatus. Mem Fac Fish Kagoshima Univ 7:73–94
Motro R, Ayalon I, Genin A (2005) Near-bottom depletion of zooplankton over coral reefs: III: vertical gradient of predation pressure. Coral Reefs 24:95–98
Nakajima R, Yoshida T, Othman BHR, Toda T (2008) Diel variation of zooplankton in the tropical coral-reef water of Tioman Island, Malaysia. Aquat Ecol 43:965–975
Nakajima R, Yoshida T, Othman BHR, Toda T (2014) Biomass and estimated production rates of metazoan zooplankton community in a tropical coral reef of Malaysia. Mar Ecol 35:112–131
Nanami A, Sato T, Ohta I, Akita Y, Suzuki N (2013) Preliminary observations of spawning behavior of white-streaked grouper (Epinephelus ongus) in an Okinawan coral reef. Ichthyol Res 60:380–385
Nolan CJ, Danilowicz BS (2008) Advantages of using crest nets to sample presettlement larvae of reef fishes in the Caribbean Sea. Fish Bull 106:213–221
Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320
Omori K, Yanagisawa Y, Hori N (1994) Life history of the caridean shrimp Periclimenes ornatus bruce associated with a sea anemone in southwest Japan. J Crustacean Biol 14:132–145
Pagano M, Rodier M, Guillaumot C, Thomas Y, Henry K, Andréfouët S (2017) Ocean-lagoon water and plankton exchanges in a semi-closed pearl farming atoll lagoon (Ahe, Tuamotu archipelago, French Polynesia). Estuar Coast Shelf Sci 191:60–73
Picheral M, Colin S, Irisson J-O (2017). EcoTaxa, a tool for the taxonomic classification of images. http://ecotaxa.obs-vlfr.fr
Platt T, Denman K (1977) Organization in pelagic ecosystem. Helgoland Wiss Meer 30:575–581
Samoilys MA (1997) Periodicity of spawning aggregations of coral trout Plectropomus leopardus (Pisces: Serranidae) on the northern Great Barrier Reef. Mar Ecol Prog Ser 160:149–159
Santos GS, Brito-Lolaia M, Schwamborn R (2017) Two new methods for sampling zooplankton and larval assemblages in tropical reef ecosystems. J Exp Mar Bio Ecol 491:27–37
Santos GS, Burgos DC, Lira SM, Schwamborn R (2015) The Impact of Trampling on Reef Macrobenthos in Northeastern Brazil: How Effective are Current Conservation Strategies? Environ Manage 56:847–858
Sebens KP, DeRiemer K (1977) Diel cycles of expansion and contraction in coral reef anthozoans. Mar Biol 43:247–256
Sebens KP, Grace SP, Helmuth B, Maney EJ, Miles JS (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa and Porites porites, in a field enclosure. Mar Biol 131:347–360
Sheppard CR, Davy SK, Pilling GM (2009) The biology of coral reefs. Oxford University Press, Oxford
Silva-Falcão EC, Severi W, De Araújo ME (2012) Spatial–temporal variation of Achirus larvae (Actinopterygii: Achiridae) in mangrove, beach and reef habitats in north-eastern Brazil. J Mar Biol Assoc U K 93:381–388
Unesco (1966) Determination of photosynthetic pigments in sea-water. Monographs on Oceanographic Methodology, Paris, p 69
Williams DM, Wolanski E, Andrews JC (1984) Transport mechanisms and the potential movement of planktonic larvae in the central region of the Great Barrier Reef. Coral Reefs 3:229–236
Yahel R, Yahel G (2005) Diel pattern with abrupt crepuscular changes of zooplankton over a coral reef. Limnol Oceanogr 50:930–944
Yahel R, Yahel G, Genin A (2005) Near-bottom depletion of zooplankton over coral reefs: I: diurnal dynamics and size distribution. Coral Reefs 24:75–85
Yoda M, Aoki M (2002) Comparative study of benthic and pelagic populations of Bodotria similis (Cumacea) from Izu Peninsula, Southern Japan. J Crustacean Biol 22:543–552
Zar JH (1996) Biostatistical Analysis. Prentice-Hall, Eryelwood Cliffs
Acknowledgements
The authors thank Mauro Maida, Beatrice Padovani Ferreira, the Tamandaré Municipality and the CEPENE/ICMBio research center for logistical support, and the Brazilian National Council for the Improvement of Higher Education (CAPES) for the Ph.D. scholarship granted to the first author. We thank Laisa Madureira for chlorophyll a readings, Jana Santana for identifying fish larvae and Dr. Marcus Silva for processing the S4 current data. Thanks to Amanda Elineau for helping us in the use of the EcoTaxa Platform. The authors would like to thank the PIQv-platform of EMBRC-France, a national Research Infrastructure supported by ANR, under the reference ANR-10-INSB-02. Many thanks to Marc Picheral (LOV, France) and Sylvain Fèvre (Hydroptic, France) for assistance with the ZooScan equipment and the ZooProcess software. The authors thank the Brazilian ministry for the environment (MMA) for SISBIO Permits Nos. 38428 and 34067. We thank all people involved in the fieldwork and laboratory analyses, especially CEPENE’s boat drivers, Andrea Pinto, Morgana Brito, Sigrid Neumann Leitão and all students and colleagues at the Zooplankton Laboratory at UFPE’s Oceanography Department for their enthusiastic support. Thanks to the National Council for the Scientific and Technological Development (CNPq—Grant No. 471038/2012-1) and INCT AmbTropic (CNPq/CAPES/FAPESB) for funding the fieldwork. The last author received a research productivity grant from CNPq. The authors thank the editor and two anonymous reviewers for their helpful corrections, suggestions and comments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors contributed equally to the elaboration of this manuscript and declared that there is no conflict of interest.
Additional information
Topic Editor Michael Lee Berumen
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
338_2019_1860_MOESM2_ESM.tif
Supplementary material 2 - Relative abundance (%) of zooplankton major groups sampled close to Pirambú and Ilha da Barra patch reefs at reef edge, channels and subsurface environments around the reefs of Tamandaré (northeastern Brazil). Data provided by each sampling day. The others contains: Hydrozoa, Siphonophorae, Gastropoda, Polychaeta, Cirripedia (nauplii), Belzebub faxoni (decapod shrimp), Euphausiacea and Ostracoda. (TIFF 3969 kb)
338_2019_1860_MOESM3_ESM.tif
Supplementary material 3 - Relative biomass (%) of zooplankton major groups sampled close to Pirambú and Ilha da Barra patch reefs at reef edge, channels and subsurface environments around the reefs of Tamandaré (northeastern Brazil). Data provided by each sampling day. The others contains: Hydrozoa, Siphonophorae, Gastropoda, Polychaeta, Cirripedia (nauplii), Belzebub faxoni (decapod shrimp), Euphausiacea and Ostracoda. (TIFF 4443 kb)
338_2019_1860_MOESM4_ESM.tif
Supplementary material 4 – Abundance (ind m−3) of the total zooplankton sampled close to Pirambú and Ilha da Barra patch reefs at reef edge, channels and subsurface environments around the reefs of Tamandaré (northeastern Brazil). Data provided by each sampling day. (TIFF 2314 kb)
338_2019_1860_MOESM5_ESM.tif
Supplementary material 5 - Biomass (µg C m−3) of the main zooplankton groups sampled at reef edge, channels and subsurface environments around the reefs of Tamandaré (northeastern Brazil). Gelatinous contains: Hydrozoa and Siphonophorae. (TIFF 2669 kb)
Rights and permissions
About this article
Cite this article
Santos, G.S., Stemmann, L., Lombard, F. et al. Are tropical coastal reefs sinks or sources of mesozooplankton? A case study in a Brazilian marine protected area. Coral Reefs 38, 1107–1120 (2019). https://doi.org/10.1007/s00338-019-01860-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-019-01860-2