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Journal of Experimental Marine Biology and Ecology 246 2000 179–221
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Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus
during the ENCORE experiment
Selina Ward , Peter Harrison
Centre for Coastal Management , Southern Cross University, Lismore NSW, Australia
Received 24 April 1999; received in revised form 3 September 1999; accepted 7 December 1999
Abstract
Colonies of two scleractinian reef coral species, Acropora longicyathus and Acropora aspera were transplanted into patch reefs at One Tree Reef, Great Barrier Reef, Australia as part of the
ENCORE experiment. These corals and colonies of A . aspera which were naturally present in the
patch reefs were exposed to four treatments over two years: controls with normal seawater, elevated levels of nitrogen only, phosphorus only, or nitrogen plus phosphorus. These corals were
sampled and used to determine whether gametogenic cycles and fecundity were affected by nutrient enrichment. Acropora longicyathus had a single annual gametogenic cycle. Corals
exposed to elevated nitrogen produced significantly smaller and fewer eggs and contained less testes material than those which were not exposed to nitrogen. Exposure to elevated phosphorus
only resulted in corals producing more but smaller eggs, and more testes material. Egg numbers of colonies from other treatments decreased as the gametogenic cycles continued, but those of the
phosphorus colonies showed almost no reduction in egg numbers between the early and late stages of the gametogenic cycles. These results have important management implications for coral reefs
as they demonstrate that small increases in concentrations of nitrogen and phosphorus can have severe effects on reproductive activity in these species of scleractinian corals.
2000 Elsevier
Science B.V. All rights reserved.
Keywords : Coral; Reproduction; Nutrients; ENCORE; Fecundity
1. Introduction
Coral reefs typically flourish in nutrient poor tropical seas Darwin, 1842; Odum and
Corresponding author. Present address: Centre for Marine Studies, The University of Queensland, Australia. E-mail address
: selinawardbigpond.com S. Ward 0022-0981 00 – see front matter
2000 Elsevier Science B.V. All rights reserved.
P I I : S 0 0 2 2 - 0 9 8 1 9 9 0 0 1 8 2 - 3
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. Ward, P. Harrison J. Exp. Mar. Biol. Ecol. 246 2000 179 –221
Odum, 1955, although they also occur in a wide range of nutrient concentrations Kinsey, 1979; Kinsey and Davies, 1979; Smith et al. 1981. Nutrient levels in waters
around coral reefs range from 0 to 4 mM nitrogen and 0.05–0.6 mM phosphorus Kinsey, 1988; D’Elia and Wiebe, 1990, however nutrient concentrations on coral reefs
are usually an order of magnitude lower than those of shallow water temperate ecosystems.
Eutrophication causes significant problems for coral reefs, and can result in degra- dation of reef ecosystems e.g. Banner, 1974; Smith et al., 1981; Pastorok and Bilyard,
1985; Tomascik and Sander, 1985; Bell, 1992a,b. Nutrient enrichment can lead to enhanced growth of phytoplankton and attached algae Pastorok and Bilyard, 1985;
Schaffelke and Klumpp, 1998, changes in the composition of algal, coral and other benthic communities Banner, 1974; Walker and Ormond, 1982; Naim, 1993, and a
deterioration in water quality Brodie, 1992. Elevated levels of nutrients can reduce the rate of growth and calcification of corals, and reef calcification Kinsey and Davies,
1979; Walker and Ormond, 1982; Dubinsky and Jokiel, 1994 but Atkinson et al. 1995 found no reduction in growth rates of corals exposed to high nutrient levels in aquaria.
Field studies along a gradient of eutrophication and other pollution in Barbados, West Indies, showed that planula production by the brooding reef coral Porites porites was
reduced in polluted areas Tomascik and Sander, 1987, and the abundance and diversity of coral recruits decreased with increasing eutrophication Tomascik, 1991; Hunte and
Wittenberg, 1992.
A number of anthropogenic activities increase nutrient loadings in marine environ- ments, including runoff from agricultural and urban areas Bell, 1992b; Brodie, 1992
and deforestation in catchments Webb, 1984; Kuhlmann, 1988; Brodie, 1992; Byron and Brodie, 1992. One of the most important anthropogenic sources of nitrogen and
phosphorus to marine environments is sewage, and this can be a major problem for coral reefs e.g. Doty, 1969; Banner, 1974; Kinsey, 1979; Marszalek, 1981; Smith et al., 1981;
Walker and Ormond, 1982; Pastorok and Bilyard, 1985; Grigg, 1995. Phosphorus is found in both human waste and phosphorus based detergents, and in Australia 10 000
tonnes of phosphorus and 100 000 tonnes of nitrogen are produced in sewerage effluent annually Brodie, 1992.
The ENCORE Elevated Nutrients on Coral Reefs Experiment experiment was conducted in order to better understand the effects of elevated levels of nitrogen and
phosphorus on coral reefs. ENCORE was a large scale manipulative reef fertilization experiment designed to quantify the fate of nitrogen and phosphorus within a coral reef
and to assess their relative impact on a variety of coral reef organisms Steven and Larkum, 1993; Larkum and Steven, 1994. An important difference between the
ENCORE experiment and previous work on nutrients is that ENCORE concentrated on examining effects of nitrogen and phosphorus in isolation, rather than in conjunction
with other confounding factors such as sediment, heavy metals and other toxins that are often associated with nutrient enrichment in eutrophic areas. Thus, differences between
treatments in ENCORE can be directly attributed to the effects of the nutrients.
Scleractinian corals have a similar pattern of gametogenesis to that of other cnidarians Giese and Pearse, 1974, and either broadcast spawn gametes for external fertilization
and development or brood larvae within polyps, and may be hermaphroditic or
S . Ward, P. Harrison J. Exp. Mar. Biol. Ecol. 246 2000 179 –221
181
gonochoric Fadlallah, 1983; Harrison and Wallace, 1990. In hermaphroditic coral species, eggs and spermaries may develop on the same mesenteries as in the faviids and
mussids, on different mesenteries within the same polyp most pocilloporids and acroporids, in different polyps within the same colony, or rarely, at different times
within the same colony Fadlallah, 1983; Harrison and Wallace, 1990. Acroporids are hermaphroditic with eggs and spermaries on different mesenteries within the same
polyp.
Measures of fecundity such as the number of eggs or the number of planulae per polyp can provide a useful index of reproductive effort and, as such, are a useful
indicator of the health of a coral Kojis and Quinn, 1984; Harrison and Wallace, 1990. Consequently, changes in these measures can be an indication of sublethal stress in
corals. However, fecundity alone can underestimate the reproductive effort of the coral and is better combined with other reproductive measures such as the size of the eggs and
the volume of testes material Harrison and Wallace, 1990. It is important to understand the gametogenic cycle of the species so that sampling can occur at the most appropriate
times.
The aims of these experiments were to examine the potential effects of elevated levels of nutrients on gametogenesis and fecundity in two reef coral species, Acropora
longicyathus and Acropora aspera, transplanted into the experimental microatolls. Secondly, fecundity in colonies of Acropora aspera occurring naturally in the mi-
croatolls was quantified to determine whether these were affected by the nutrient treatments. These species were chosen as they have relatively large polyps that can be
dissected by hand so that the eggs and testes may be measured without the use of histological sections Oliver, 1979; Wallace, 1985. When measuring reproductive output
it is preferable to use polyp dissections rather than histology, as tissue shrinkage occurs during histological processes, and gametes or larvae may not occur in some sections,
hence reproductive output may be underestimated in histological sections Harrison and Wallace, 1990. A
. longicyathus is also very suitable for transplantation because as the colonies grow, the basal areas die off, so that individual sections of one or more
branches usually attach directly onto the substratum so sections of the colonies can be removed without damaging the remainder of the colony. The bottlebrush growth form
also allows easy fragmentation.
2. Methods
