Do human activities affect the picoplankton structure of the Ahe atoll lagoon (Tuamotu Archipelago, French Polynesia)?

Abstract

The spatial variations of the picoplankton (photoautotrophic and heterotrophic microorganisms) in the Ahe atoll lagoon were studied in May and October 2008 to assess whether they were affected by human activities along the atoll. Spatial patterns were studied using 10 sampling stations chosen according to the location of the anthropogenic activities (pearl farming, harbor). Experiments were also carried out to determine whether bacterial growth, with or without predators, was limited by inorganic (N and P) substrates. The results showed that heterotrophic bacterioplankton abundance was superior to the photoautotrophic organisms, especially in May. Significant increases in bacterial abundance were observed in May after 24 h incubation with +P and +N (but not in October). All samples complied with the quality levels for fecal indicator bacteria (FIB) defined by the European Union and there was no evidence that human sewage had any impact on picoplankton over the whole atoll.

Introduction

Human activities have a major impact on marine ecosystems. The pressures exerted are diverse and result from a wide range of activities such as coastal engineering, sediment dredging, pollution, fishing, aquaculture, urban development, maritime transport, tourism, mining, oil extraction, transport and refining of oil, agricultural and industrial activities (Islam and Tanaka, 2004, Halpern et al., 2008). All these activities have an effect on the components of the marine food web, from microorganisms to top animal predators. A recent report analyzed the ecological impact of anthropogenic activities in the oceans worldwide, focusing on stressors that can be evaluated at global scale (Halpern et al., 2008). All the analyzed ocean ecosystems (coral reefs, mangroves, seagrass meadows, seamounts, rocky reefs, soft shallow areas, continental shelf areas, slope areas, pelagic waters and the deep sea) can be considered to be affected by anthropogenic activities, although to different degrees (Nogales et al., 2011).

In a context of eutrophication, the composition and structure of microbial communities are also basic indicators of ecosystem status, including phytoplankton bloom and the heterotrophic activity of aerobic and anaerobic bacteria (Paerl et al., 2002, Bouvy et al., 2010). Nutrient availability (bottom-up control), predation by protozoa (top-down control) and viral lysis are the most important factors regulating bacterial communities. Organic carbon has usually been considered to be the main factor limiting the growth of pelagic heterotrophic bacteria. However, studies on nutrient limitation of such communities have shown that mineral limitation of growth rate is widespread in various marine ecosystems (Torréton et al., 2000, Carlsson and Caron, 2001). Nutrient enrichment is a direct consequence of eutrophication, modifying the biological abundance and activity at each trophic level and, for example, increasing bacterial standing stocks and production (Ducklow and Shiah, 1993). Nutrient enrichment bioassays are the most direct method for assessing the nutrient status of phytoplankton and bacterioplankton communities and this method has been widely used (Torréton et al., 2000, Bouvy et al., 2004).

Although viral infection is now considered to be one of the major structuring processes in the dynamics of marine microbial communities (Fuhrman, 1999), grazing by heterotrophic nanoflagellates (HNF) has been identified as the main limiting factor affecting bacteria and has been shown to hinder bacterial production, thus regulating bacterial biomass in a large number of pelagic ecosystems (Solic and Krstulovic, 1994, Christaki et al., 1999, Ferrier-Pagès and Furla, 2001). Size-selective grazing coupled with resource availability has been shown to be a shaping force in both the taxonomic and phenotypic structures of bacterial communities (Jürgens and Matz, 2002). However, although factors controlling bacterial communities in temperate and tropical areas have been studied, little research has been undertaken to study these microorganisms in atolls (Gonzalez et al., 1998, Ferrier-Pagès and Furla, 2001).

In addition to their role in the organic matter mineralization and in the diet for heterotrophic nanoflagellates, micro-organisms are effective descriptors for evaluating and predicting the environmental impact of human activities. Continental waters are often polluted by pathogenic microorganisms from recreational marinas, sewage disposal sites, septic tanks, rainfall runoff from urban areas and many other sources (Lipp et al., 2001, Aslan-Yilmaz et al., 2004). Fecal indicator bacteria (FIB) including thermo tolerant coliforms (TTC) and fecal streptococci (FS) are used as surrogates for human and animal pathogens for assessing water quality. In epidemiological studies, FIB are documented as being associated with an increased risk of contracting gastrointestinal and respiratory illnesses after contact with waters with high concentrations (Haile et al., 1999). Their origin has always been presumed to be anthropogenic (e.g. sewage, agricultural and urban runoff). An important criterion for assessing the potential health risk for recreational waters is the FIB density. Although FIB do not necessarily induce illness, they are often associated with pathogenic bacteria, viruses and parasites in domestic sewage. Microbial water quality varies according to the magnitude of inputs and the flow and dispersion of organisms as a result of near-shore hydrodynamics such as tides and currents (Davies-Colley et al., 1994).

French Polynesia made up of several lagoons are of great importance to the economy of the region, where farming of pearl oyster, Pinctada margaritifera, is the major source of export earnings, especially from Ahe atoll (Thomas et al., 2010, Andréfouët et al., 2012. The main objective of this study was to estimate the impacts of human activities along the Ahe atoll by determining fecal indicator bacteria (FIB) and by describing the abundance of heterotrophic and autotrophic picoplankton in the lagoon. For this, spatial patterns (10 sampling stations) and temporal patterns (before and after the rainy season) were studied using 10 biological indicators. Bacterial responses to nutrient enrichment based on bioassay experiments at one station were also studied for the two periods.