Effects of the herbicide diuron on the early life history stages of coral

Abstract

The effects of the herbicide diuron on the early life history stages of broadcast spawning and brooding corals were examined in laboratory experiments. Fertilisation of Acropora millepora and Montipora aequituberculata oocytes were not inhibited at diuron concentrations of up to 1000 μg l⁻¹. Metamorphosis of symbiont-free A. millepora larvae was only significantly inhibited at 300 μg l⁻¹ diuron. Pocillopora damicornis larvae, which contain symbiotic dinoflagellates, were able to undergo metamorphosis after 24 h exposure to diuron at 1000 μg l⁻¹. Two-week old P. damicornis recruits on the other hand were as susceptible to diuron as adult colonies, with expulsion of symbiotic dinoflagellates (bleaching) evident at 10 μg l⁻¹ diuron after 96 h exposure. Reversible metamorphosis was observed at high diuron concentrations, with fully bleached polyps escaping from their skeletons. Pulse amplitude modulation (PAM) chlorophyll fluorescence techniques demonstrated a reduction in photosynthetic efficiency ($\mathrm{\Delta }F/F_{\mathrm{m}}^{\prime }$) in illuminated P. damicornis recruits after a 2 h exposure to 1 μg l⁻¹ diuron. The dark-adapted quantum yields (F_v/F_m) also declined, indicating chronic photoinhibition and damage to photosystem II.

Introduction

Herbicides are used widely on sugarcane plantations in catchments adjacent to the Great Barrier Reef (GBR) (Hamilton and Haydon, 1996). Little is known of the relative concentrations of herbicides in near shore waters of the GBR; however, of all the herbicides used in GBR catchments, diuron has been detected in the highest concentrations (up to 10 μg kg⁻¹) in marine sediments (Haynes et al., 2000a). In one rainfall event, 470 kg of the herbicide diuron was estimated lost from the Pioneer catchment adjacent to the GBR (Simpson, 2002, White et al., 2002). The relatively high solubility of diuron, combined with high application rates in GBR catchments have lead to concerns that diuron may be one of the most harmful agrochemical pollutants to GBR organisms and ecosystems (Haynes and Michalek-Wagner, 2000, Williams, 2001).

Diuron, along with other herbicides such as tebuthiuron, Irgarol 1051, simazine and ametryn, targets the photoreduction site of photosystem II in the chloroplasts of plants and algae, where it competes with plastoquinone for the Q_B binding site (Lavergne, 1982, Sandmann and Boelger, 1986, Jones et al., 2003). This results in restriction of electron transfer from Q_A to Q_B, leading to a reduction of photosynthetic efficiency (yield), which can be detected in situ using a pulse amplitude modulation (PAM) fluorometer (see Materials and Methods). Laboratory experiments have shown that both seagrasses and adult corals can be affected by diuron at very low concentrations. Photosynthetic efficiency is reduced in several species of seagrass at diuron concentrations as low as 0.1 μg l⁻¹ (Ralph, 2000, Haynes et al., 2000b). Most corals rely on symbiotic dinoflagellates (Symbiodinium spp.) to provide additional energy required for colony maintenance, growth and reproduction (Rinkevich, 1989, Rowan, 1998). Some coral larvae also contain these symbionts, from which they obtain metabolites (Richmond, 1987). Diuron can inhibit the photosynthetic efficiency of dinoflagellates isolated from corals at 0.25 μg l⁻¹ (Jones et al., 2003, Owen et al., 2003) and dinoflagellates within the coral tissue (in hospite) at 0.3 μg l⁻¹ (Jones and Kerswell, 2003). Two other herbicides, Irgarol 1051 and ametryn, affect photosynthesis in hospite at even lower concentrations (Jones and Kerswell, 2003). Reduction of photosynthesis in symbionts by herbicides is thought to reduce the fitness of adult corals, and high concentrations of diuron have also been shown to cause expulsion of symbionts from the host (bleaching) (Jones and Kerswell, 2003, Jones et al., 2003).

Scleractinian corals have two distinct strategies for reproduction: broadcast spawning of gametes and brooding of larvae (see review by Harrison and Wallace, 1990). The broadcast spawning corals release gametes into the water column synchronously, usually after a full moon in October to December on the GBR. The gametes are fertilized externally and planula larvae develop over several days in the water column, becoming competent to settle and undergo metamorphosis within a week. Brooded larvae develop within the parent colonies and can result from self-fertilisation or intake of spermatocytes. Larvae of brooding corals are usually released in lunar cycles that may peak at certain times in the year, and are often competent to settle immediately following release. Oocytes from some broadcast spawning species and larvae from some brooding species contain parentally derived symbiotic algae, whereas recruits from other species obtain symbionts from the seawater a few days to weeks after settlement and metamorphosis.

Early life history stages of corals (such as oocytes, sperm, larvae and new recruits), as well as critical transitions in life history (including fertilisation and metamorphosis), may be more or less susceptible to toxicants such as diuron than the adult colonies. These early stages may be affected by herbicides in a variety of ways, including: reduction in photosynthetic efficiency of symbionts leading to impaired cellular function in the host and/or algal symbiont; build-up of reactive oxygen radicals under high light leading to cellular damage of symbiont and host; or direct interference with cellular function of the host such as endocrine disruption. We compare the effects of the herbicide diuron in laboratory experiments on: fertilisation rates of broadcasted coral oocytes with and without symbionts, rates of metamorphosis of coral larvae, and the photosynthetic efficiency, extent of bleaching and rates of survival of coral recruits and adult colonies.