Metazooplankton communities in the Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia): Spatiotemporal variations and trophic relationships

doi:10.1016/j.marpolbul.2012.01.025

Marine Pollution Bulletin

Volume 65, Issues 10–12, 2012, Pages 538-548

https://doi.org/10.1016/j.marpolbul.2012.01.025 Get rights and content

Abstract

Metazooplankton abundance, biomass (<80 μm, 200–500 μm and >500 μm) and community structure in the Ahe atoll were studied together with their relationships with environmental factors (temperature, salinity, wind) and trophic factors (phytoplankton, bacteria, heterotrophic nanoflagellates (HNF) and ciliates) during three periods in 2008–2009. Meroplankton, mainly bivalve and gastropod larvae, was dominant. Holoplankton was dominated by copepods, the main species being Oithona spp., Paracalanus parvus, Clausocalanus spp., Corycaeus spp., Acartia fossae and Undinula vulgaris. The results suggest a clear wind influence on the structure and horizontal distribution of the zooplankton communities. The metazooplankton appeared to be controlled mainly by food resources, suggesting a bottom-up control. The low nanophytoplankton biomass in contrast to the high abundance of picophytoplankton, HNF and nano-particle grazers (mainly Oithona spp., Paracalanus and bivalve larvae) highlighted the importance of the microbial loop in the food web.

Introduction

Metazooplankton plays a major role in the functioning and productivity of aquatic ecosystems through its impact on nutrient dynamics and its key position in food webs. Most mesozooplanktonic organisms exert a strong grazing impact on the phytoplankon and on the microzooplankton (Pont, 1995, Calbet, 2008). They are also a food source for organisms of the upper trophic levels such as planktivorous fish and carnivorous invertebrates (Pinel-Alloul, 1995). In coral reef and atoll lagoon environments, they are important contributors to the benthic and pelagic food webs (Bozec et al., 2004, Alldredge and King, 2009). Zooplankton organisms can also be used as biological indicators for pollution, water quality and eutrophication (Attayde and Bozelli, 1998, Webber et al., 2005). Their generation times may be short enough to respond quickly to acute stress but long enough to integrate the effects of chronic problems. These attributes can be useful to design a community ecosystem health indicator (Cairns et al., 1993). However, very few studies have dealt with zooplankton in atoll lagoons (Gerber, 1981) and only a few have concerned the Tuamotu Archipelago (Michel et al., 1971, Ricard et al., 1979, Le Borgne et al., 1989, Carleton and Doherty, 1998).

Coral reef and atoll lagoons are productive ecosystems, compared to surrounding ocean (Hatcher, 1997). They have been frequently exploited for aquaculture, as in the Tuamotu Archipelago (French Polynesia) where pearl oyster farming is a major driver of the local economy (Andrefouët et al., 2012). The planktonic pearl-oyster larvae mainly feed on nanophytoplankton with high ingestion rates (Doroudi et al., 2003). The adults, cultivated in sub-surface pelagic nets, are also important passive consumers of nanoparticles (Yukuhira et al., 1998, Fournier et al., 2012). Farmed pearl-oyster populations can be considered as components of the pelagic ecosystem in pearl farming lagoons. In these ecosystems, they share (and may compete for) food resources with several pelagic components (including zooplankton) and may serve as food for other ones. Studying the different communities of the pelagic ecosystem and evaluating their stocks and their inter-relationships are required to define the optimal conditions for the recruitment and development of oysters. This information is also necessary to determine the load capacity for cultivation (Niquil et al., 1998).

A multidisciplinary research program was funded by the European Development Fund (EDF) in 2007 to describe, among other goals, the ecological environment of the pearl-oyster Pinctada margaritifera (Linnaeus, 1758) and its relationship with the pelagic trophic network.

Our study is part of this multidisciplinary study on the trophic environment of P. margaritifera. It aimed at analyzing within a farmed lagoon the spatiotemporal variations of metazooplankton standing stock and community composition according to the main environmental and trophic parameters.

Section snippets

Study site and sampling strategy

The Ahe atoll (14°29′S; 146°18′S) to the north west of the Tuamotu Archipelago in the Pacific Ocean is 23.5 km long and a maximum of 12.2 km wide (Fig. 1). The lagoon is 142 km² in area with maximum depth of 70 m in the central zone. The atoll rim which surrounds the lagoon is not completely closed: there is a passage (300 m long and about 20 m deep) to the northwest between the lagoon and the ocean, and several spillways mostly in the southern part of the rim. The climate is wet tropical with one

Environmental and trophic variables

Different meteorological conditions were observed during the 3 sampling periods (Fig. 2). Rainfall were high in February 2009 (70 mm month⁻¹) compared to May and October 2008 (52 and 23 mm month⁻¹, respectively). Wind speed was lower during the May 2008 survey (0–7.7 m s⁻¹ during the sampling period) than for the other surveys (6.1–11.5 m s⁻¹ and 3.0–11.5 m s⁻¹ in October 2008 and February 2009, respectively). Water temperature and salinity showed significant variations between sampling seasons (Fig. 3).

Hydrobiological context

The phytoplanktonic biomass, as inferred from Chl a, measured in the Ahe lagoon was comparable to that in other oligotrophic ecosystems and similar to that in other lagoons of the Tuamotu Archipelago (Rancher and Rougerie, 1995). The proportion of picoplankton was close to that recorded in other atoll lagoons and in agreement with additional measurements in Ahe made in 2009 and 2010 (Charpy, 1996, Charpy et al., 2012).

High spatio-temporal variations of chlorophyll, autotrophic (picoeukaryotes,

Conclusion

Our results showed the predominance of meroplankton and bivalve larvae in Ahe as compared to other coral reef and atoll lagoons. while the dominance of bivalve larvae suggests potentially major community change arising from aquaculture activities (pearl oyster farming), it is probably mainly due to the importance of wild populations. Our study also suggests that tide-flushing and wind driven circulation of the lagoon, as evidenced in the study by Dumas et al. (2012), plays an important role in

Acknowledgements

This study was funded by the 9th European Development Fund (EDF) (grant POF/001/002 N°1 to Serge Andréfouët and Loic Charpy, IRD). The authors express their gratitude to the EDF and Service de la Perliculture staff, especially Alain Lo-Yat, for their efficient help during sample collection on Ahe atoll. They also thank two anonymous reviewers for helpful criticisms and comments on the first version of the manuscript.

References (73)

S. Andréfouët et al.
Recent reseach for pearl oyster aquaculture management in French Polynesia
Marine Pollution Bulletin
(2012)
L. Carassou et al.
Spatial and temporal distribution of zooplankton related to the environmental conditions in the coral reef lagoon of New Caledonia, Southwest Pacific
Marine Pollution Bulletin
(2010)
L. Charpy et al.
Physical and chemical control of the phytoplankton of Ahe lagoon, French Polynesia
Marine Pollution Bulletin
(2012)
F. Dumas et al.
Tidal flushing and wind driven circulation of Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia) from in situ observations and numerical modelling”
Marine Pollution Bulletin
(2012)
J. Dutz et al.
Inhibition of copepod feeding by exudates and transparent exopolymer particles (TEP) derived from a Phaeocystis globosa dominated phytoplankton community
Harmful Algae
(2005)
J. Fournier et al.
Pearl oysters Pinctada margaritifera grazing on natural plankton in Ahe atoll lagoon (Tuamotu archipelago, French Polynesia)
Marine Pollution Bulletin
(2012)
R. Le Borgne et al.
Plankton biomass and production in an open atoll lagoon: Uvea, New Caledonia
Journal of Experimental Marine Biology and Ecology
(1997)
S. Lefebvre et al.
Spatial and temporal dynamics of size-structured photosynthetic parameters (PAM) and primary production (13C) of pico- and nano-phytoplankton in an atoll lagoon
Marine Pollution Bulletin
(2012)
V. Michotey et al.
Spatio-temporal diversity of free-living and particle-attached prokaryotes in the tropical lagoon of Ahe atoll (Tumotu Archipelago) and its surrounding oceanic waters
Marine Pollution Bulletin
(2012)
M. Pagano et al.
Vertical migrations and feeding rhythms of mesozooplanktonic organisms in the Rhone River plume area (North-West Mediterranean Sea)
Estuarine Coastal and Shelf Science
(1993)

Y. Thomas et al.

Multi-scale distribution and dynamics of bivalve larvae in a deep atoll lagoon (Ahe, French Polynesia)

Marine Pollution Bulletin

(2012)

Y. Thomas et al.

Bivalve larvae transport and connectivity within the Ahe atoll lagoon (Tuamotu Archipelago), with application to pearl oyster aquaculture management

Marine Pollution Bulletin

(2012)

J.-P. Torréton et al.

Correspondence between the distribution of hydrodynamic time parameters and the distribution of biological and chemical variables in a semi-enclosed coral reef lagoon

Estuarine Coastal and Shelf Science

(2007)

M. Troussellier et al.

Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids

Microbial Ecology

(1999)

A.L. Alldredge et al.

Near-surface enrichment of zooplankton over a shallow back reef: implications for coral reef food webs

Coral Reefs

(2009)

J.N. Alvarez-Cadena et al.

Composition and abundance of zooplankton groups from a coral reef lagoon in Puerto Morelos, Quintana Roo, Mexico, during an annual cycle

Revista de Biologia Tropical

(2009)

M. Atkinson et al.

Circulation in Enewetak Atoll lagoon

Limnology and Oceanography

(1981)

J.L. Attayde et al.

Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis

Canadian Journal of Fisheries and Aquatic Sciences

(1998)

J. Blanchot et al.

Size composition of particulate organic matter in the lagoon of Tikehau Atoll (Tuamotu Archipelago)

Marine Biology

(1989)

D. Boltovskoy et al.

The effects of wind and diel vertical migrations on the distribution of freshwater zooplankton

Studies on Neotropical Fauna and Environment

(1984)

Y.M. Bozec et al.

Trophic model of lagoonal communities in a large open atoll (Uvea, Loyalty islands, New Caledonia)

Aquatic Living Resources

(2004)

J. Cairns et al.

A proposed framework for developing indicators of ecosystem health

Hydrobiologia

(1993)

A. Calbet

The trophic roles of microzooplankton in marine systems

ICES Journal of Marine Science

(2008)

A. Calbet et al.

Planktonic herbivorous food webs in the catalan Sea (NW Mediterranean): temporal variability and comparison of indices of phyto-zooplankton coupling based on state variables and rate processes

Journal of Plankton Research

(1996)

J.H. Carleton et al.

Tropical zooplankton in the highly-enclosed lagoon of Taiaro Atoll (Tuamotu Archipelago, French Polynesia)

Coral Reefs

(1998)

L. Charpy

Phytoplankton biomass and production in two Tuamotu atoll lagoons (French Polynesia)

Marine Ecology Progress Series

(1996)

L. Charpy et al.

Photosynthetic picoplankton in French Polynesian atoll lagoons: estimation of taxa contribution to biomass and production by flow cytometry

Marine Ecology Progress Series

(1998)

L. Charpy et al.

Particulate organic matter fluxes in a Tuamotu atoll lagoon

Marine Ecology Progress Series

(1991)

L.A. Chisholm et al.

Size-weight relationships and biomass of tropical off Kingston, Jamaica

Marine Biology

(1990)

Conway, D.V.P., White, R.G., Hugues-Dit-Ciles, J., Gallienne, C.P., Robins, D.B., 2003. Guide to the coastal and...

B.E. Cuker et al.

Diel vertical migration of zooplankton in contrasting habitats of the Chesapeake Bay

Estuaries

(2002)

S. Dolédec et al.

Co-inertia analysis: an alternative method for studying species-environment relationships

Freshwater Biology

(1994)

M.S. Doroudi et al.

Variation in clearance and ingestion rates by larvae of the black-lip pearl oyster (Pinctada margaritifera, L.) feeding on various microalgae

Aquaculture Nutrition

(2003)

R.P. Gerber

Species composition and abundance of lagoon zooplankton at Eniwetak atoll, Marshall Isalnds

Atoll research Bulletin

(1981)

R.P. Gerber et al.

Ingestion of detritus by the lagoon pelagic community at Eniwetok Atoll

Limnology and Oceanography

(1974)

K. Gundersen et al.

Elemental C, N and P cell content of individual bacteria collected at the Bermuda Atlantic Time-series Study (BATS) site

Limnology and Oceanography

(2002)

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Metazooplankton communities in the Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia): Spatiotemporal variations and trophic relationships

Abstract

Introduction

Section snippets

Study site and sampling strategy

Environmental and trophic variables

Hydrobiological context

Conclusion

Acknowledgements

Marine Pollution Bulletin

Marine Pollution Bulletin

Marine Pollution Bulletin

Marine Pollution Bulletin

Harmful Algae

Marine Pollution Bulletin

Journal of Experimental Marine Biology and Ecology

Marine Pollution Bulletin

Marine Pollution Bulletin

Estuarine Coastal and Shelf Science

Marine Pollution Bulletin

Marine Pollution Bulletin

Estuarine Coastal and Shelf Science

Microbial Ecology

Near-surface enrichment of zooplankton over a shallow back reef: implications for coral reef food webs

Coral Reefs

Composition and abundance of zooplankton groups from a coral reef lagoon in Puerto Morelos, Quintana Roo, Mexico, during an annual cycle

Revista de Biologia Tropical

Circulation in Enewetak Atoll lagoon

Limnology and Oceanography

Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis

Canadian Journal of Fisheries and Aquatic Sciences

Size composition of particulate organic matter in the lagoon of Tikehau Atoll (Tuamotu Archipelago)

Marine Biology

The effects of wind and diel vertical migrations on the distribution of freshwater zooplankton

Studies on Neotropical Fauna and Environment

Trophic model of lagoonal communities in a large open atoll (Uvea, Loyalty islands, New Caledonia)

Aquatic Living Resources

A proposed framework for developing indicators of ecosystem health

Hydrobiologia

The trophic roles of microzooplankton in marine systems

ICES Journal of Marine Science

Planktonic herbivorous food webs in the catalan Sea (NW Mediterranean): temporal variability and comparison of indices of phyto-zooplankton coupling based on state variables and rate processes

Journal of Plankton Research

Tropical zooplankton in the highly-enclosed lagoon of Taiaro Atoll (Tuamotu Archipelago, French Polynesia)

Coral Reefs

Phytoplankton biomass and production in two Tuamotu atoll lagoons (French Polynesia)

Marine Ecology Progress Series

Photosynthetic picoplankton in French Polynesian atoll lagoons: estimation of taxa contribution to biomass and production by flow cytometry

Marine Ecology Progress Series

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Marine Ecology Progress Series

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Marine Biology

Diel vertical migration of zooplankton in contrasting habitats of the Chesapeake Bay

Estuaries

Co-inertia analysis: an alternative method for studying species-environment relationships

Freshwater Biology

Variation in clearance and ingestion rates by larvae of the black-lip pearl oyster (Pinctada margaritifera, L.) feeding on various microalgae

Aquaculture Nutrition

Species composition and abundance of lagoon zooplankton at Eniwetak atoll, Marshall Isalnds

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Ingestion of detritus by the lagoon pelagic community at Eniwetok Atoll

Limnology and Oceanography

Elemental C, N and P cell content of individual bacteria collected at the Bermuda Atlantic Time-series Study (BATS) site

Limnology and Oceanography