Selina Ward

ENCORE: The effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions

Coral reef degradation resulting from nutrient enrichment of coastal waters is of increasing global concern. Although effects of nutrients on coral reef organisms have been demonstrated in the laboratory, there is little direct evidence of nutrient effects on coral reef biota in situ. The ENCORE experiment investigated responses of coral reef organisms and processes to controlled additions of dissolved inorganic nitrogen (N) and/or phosphorus (P) on an offshore reef (One Tree Island) at the southern end of the Great Barrier Reef, Australia. A multi-disciplinary team assessed a variety of factors focusing on nutrient dynamics and biotic responses. A controlled and replicated experiment was conducted over two years using twelve small patch reefs ponded at low tide by a coral rim. Treatments included three control reefs (no nutrient addition) and three + N reefs (NH4Cl added), three + P reefs (KH2PO4 added), and three + N + P reefs. Nutrients were added as pulses at each low tide (ca twice per day) by remotely operated units. There were two phases of nutrient additions. During the initial, low-loading phase of the experiment nutrient pulses (mean dose = 11.5 microM NH4+; 2.3 microM PO4(-3)) rapidly declined, reaching near-background levels (mean = 0.9 microM NH4+; 0.5 microM PO4(-3)) within 2-3 h. A variety of biotic processes, assessed over a year during this initial nutrient loading phase, were not significantly affected, with the exception of coral reproduction, which was affected in all nutrient treatments. In Acropora longicyathus and A. aspera, fewer successfully developed embryos were formed, and in A. longicyathus fertilization rates and lipid levels decreased. In the second, high-loading, phase of ENCORE an increased nutrient dosage (mean dose = 36.2 microM NH4+; 5.1 microM PO4(-3)) declining to means of 11.3 microM NH4+ and 2.4 microM PO4(-3) at the end of low tide) was used for a further year, and a variety of significant biotic responses occurred. Encrusting algae incorporated virtually none of the added nutrients. Organisms containing endosymbiotic zooxanthellae (corals and giant clams) assimilated dissolved nutrients rapidly and were responsive to added nutrients. Coral mortality, not detected during the initial low-loading phase, became evident with increased nutrient dosage, particularly in Pocillopora damicornis. Nitrogen additions stunted coral growth, and phosphorus additions had a variable effect. Coral calcification rate and linear extension increased in the presence of added phosphorus but skeletal density was reduced, making corals more susceptible to breakage. Settlement of all coral larvae was reduced in nitrogen treatments, yet settlement of larvae from brooded species was enhanced in phosphorus treatments. Recruitment of stomatopods, benthic crustaceans living in coral rubble, was reduced in nitrogen and nitrogen plus phosphorus treatments. Grazing rates and reproductive effort of various fish species were not affected by the nutrient treatments. Microbial nitrogen transformations in sediments were responsive to nutrient loading with nitrogen fixation significantly increased in phosphorus treatments and denitrification increased in all treatments to which nitrogen had been added. Rates of bioerosion and grazing showed no significant effects of added nutrients. ENCORE has shown that reef organisms and processes investigated in situ were impacted by elevated nutrients. Impacts were dependent on dose level, whether nitrogen and/or phosphorus were elevated and were often species-specific. The impacts were generally sub-lethal and subtle and the treated reefs at the end of the experiment were visually similar to control reefs. Rapid nutrient uptake indicates that nutrient concentrations alone are not adequate to assess nutrient condition of reefs. Sensitive and quantifiable biological indicators need to be developed for coral reef ecosystems. The potential bioindicators identified in ENCORE should be tested in future research on coral reef/nutrient interactions. Synergistic and cumulative effects of elevated nutrients and other environmental parameters, comparative studies of intact vs. disturbed reefs, offshore vs. inshore reefs, or the ability of a nutrient-stressed reef to respond to natural disturbances require elucidation. An expanded understanding of coral reef responses to anthropogenic impacts is necessary, particularly regarding the subtle, sub-lethal effects detected in the ENCORE studies.

Ocean acidification reduces coral recruitment by disrupting intimate larval‐algal settlement interactions

Ecology Letters (2012) 15: 338-346 ABSTRACT: Successful recruitment in shallow reef ecosystems often involves specific cues that connect planktonic invertebrate larvae with particular crustose coralline algae (CCA) during settlement. While ocean acidification (OA) can reduce larval settlement and the abundance of CCA, the impact of OA on the interactions between planktonic larvae and their preferred settlement substrate are unknown. Here, we demonstrate that CO2 concentrations (800 and 1300 μatm) predicted to occur by the end of this century significantly reduce coral (Acropora millepora) settlement and CCA cover by ≥ 45%. The CCA important for inducing coral settlement (Titanoderma spp., Hydrolithon spp.) were the most deleteriously affected by OA. Surprisingly, the only preferred settlement substrate (Titanoderma) in the experimental controls was avoided by coral larvae as pCO2 increased, and other substrata selected. Our results suggest OA may reduce coral population recovery by reducing coral settlement rates, disrupting larval settlement behaviour, and reducing the availability of the most desirable coralline algal species for successful coral recruitment.

Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event

Pulse-amplitude-modulation chlorophyll fluorometry was used to examine changes in dark-adapted F-v/F-m of endosymbiotic dinoflagellate microalgae within the tissues of the temperate coral Plesiastrea versipora exposed to elevated seawater temperature. The F-v/F-m was markedly reduced following exposure of corals to 28 degrees C for 48 h. When corals were returned to ambient (24 degrees C) conditions, F-v/F-m increased in an initial rapid and then secondary slower phase. Tissue discolouration (coral bleaching), caused by a significant decrease in the density of algae, was observed during the first 2-3 days of the recovery period. After 14 days, F-v/F-m was still significantly lower than in control corals. The recovery of F-v/F-m is discussed in terms of repair processes within the symbiotic algae, division of healthy algae and also the selective removal of photo-damaged dinoflagellates. Under field conditions, bleached corals sampled at Heron Island Reef during a bleaching event had significantly lower F-v/F-m than non-bleached colonies; four months after the bleaching event, there were no differences in F-v/F-m or algal density in corals marked as having bleached or having shown no signs of colour loss. The results of this laboratory and field study are consistent with the hypothesis that an impairment of photosynthesis occurs during heat-stress, and is the underlying cause of coral bleaching.

Evidence for broadcast spawning as well as brooding in the scleractinian coral Pocillopora damicornis

The reproductive activity of 88 colonies of Pocillopora damicornis at Rottnest Island, Western Australia, was examined over 12 mo (20 August 1988 to 20 August 1989). Larvae were found close to the three new moons of February, March and April, 1989, but in large numbers only during March; 67% of all corals produced larvae. There was no obvious connection between gametogenesis and the production of brooded larvae; however, those corals which did not produce, larvae also did not produce ova but did produce, sperm, and must be considered male colonies. All colonies which produced ova went on to produce planulae. Spermatogenesis occurred throughout the year, but oogenesis occurred between September 1988 and April 1989. Dramatic declines in the percentage of polyps containing eggs and sperm occurred in early February and early April 1989. On these dates the amount of lipid in the tissue of the corals decreased, which suggests that the decline in the percentage of polyps with sperm and eggs was not due to the gametes being resorbed by the polyps. Therefore, P. damicornis at Rottnest Island appears to be both a brooder and a broadcaster with asexual reproduction through brooded larvae and sexual reproduction through spawning of gametes. This accounts for earlier evidence in the literature that some input from sexual reproduction had been occurring in the populations of P. damicornis at Rottnest Island. There is no direct evidence for spawning, as broadcasting of gametes has not been observed, but the indirect evidence provides a strong argument for the existence of this dual reproduction.

Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus during the ENCORE experiment

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.

The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus)

A population of the scleractinian coral Pocillopora damicornis (Linnaeus) was examined at Rottnest Island, off the Western Australian coast. This is a temperate zone and an area under considerable tourist pressure. Experiments were conducted at Little Salmon Bay and Mary Cove to investigate the effect of mechanical damage on the growth, reproduction and storage of lipid to see whether patterns of energy allocation were affected. These parameters were measured simultaneously 14 times over 13 months. Damage had an adverse effect on the performance of the corals. Dislodged corals had increased mortality, decreased growth, decreased reproduction but no change in lipids. Fragmented corals had no significant change in mortality, lipids or growth rate but had increased reproduction. The overall allocation of energy to growth, reproduction and lipid storage of dislodged corals appeared to decrease whereas the overall output of the fragmented corals has increased.

Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus

Scleractinian corals may acquire Symbiodinium from their parents (vertically) or from the environment (horizontally). In the present study, adult colonies of the coral Acropora longicyathus from One Tree Island (OTI) on the southern Great Barrier Reef (Australia) acquired two distinct varieties of symbiotic dinoflagellates (Symbiodinium) from the environment. Adult colonies had either Symbiodinium from clade C (86.7%) or clade A (5.3%), or a mixture of both clades A and C (8.0% of all colonies). In contrast, all 10-day-old juveniles were associated with Symbiodinium from clade A, while 83-day-old colonies contained clades A, C and D even though they were growing at the same location. Symbiodinium from clade A were dominant in both 10- and 83-day-old juveniles (99 and 97% of all recruits, respectively), while clade D was also found in 31% of 83-day-old juveniles. Experimental manipulation also revealed that parental association (with clade A or C), or the location within the OTI reef, did not influence which clade of symbiont was acquired by juvenile corals. The differences between the genetic identity of populations of Symbiodinium resident in juveniles and adult A. longicyathus suggest that ontogenetic changes in the symbiosis may occur during the development of scleractinian corals. Whether or not these changes are due to host selective processes or differences in the physical environment associated with juvenile versus adult colonies remains to be determined.

Impact of elevated ammonium on reproduction in two Hawaiian scleractinian corals with different life history patterns

Elevated nutrients have the potential to disrupt reproduction in scleractinian corals, with consequent impacts on population dynamics. Reproduction in broadcast spawning (Montipora capitata) and brooding (Pocillopora damicornis) species was assessed following exposure to elevated ammonium in a microcosm experiment. Planulation in P. damicornis ceased following 4 months of ammonium exposure and did not recover until 3 months after termination of nutrient enrichment. Larval settlement and survivorship were not affected by ammonium enrichment. Few significant changes were found for reproductive parameters of M. capitata. There was a significant but small decrease in egg size (430 microm in control eggs to 408 microm in eggs from ammonium enrichment treatments), but no differences in total fecundity or fertilization success. This may be related to the presence of zooxanthellae in the eggs of M. capitata, in contrast to changes in reproduction previously reported in Acropora species, whose eggs do not contain zooxanthellae.

Grazing by a small fish affects the early stages of a post-settlement stony coral

Short-term experiments were used to isolate the detrimental effects of grazer disturbance on young corals, and determine the stage of development at which recruits are no longer susceptible to this disturbance. Artificial substrata containing an algal matrix and coral recruits of different life stages were exposed to grazing by epilithic algal matrix (EAM) feeding combtoothed blennies, Salarias fasciatus. Single polyp recruits were vulnerable to grazer disturbance, while multi-polyp recruits (ca. 6–8 polyps) survived with evidence of minor damage in the form of tissue and polyp loss. The result indicates that blennies, although small and possessing weak dentition, can negatively influence the survival of young coral recruits. The protruding structure of micro-nubbins, representing juvenile corals were not damaged, suggesting that coral achieving that size and form can escape such damage.

Linking Demographic Processes of Juvenile Corals to Benthic Recovery Trajectories in Two Common Reef Habitats

Tropical reefs are dynamic ecosystems that host diverse coral assemblages with different life-history strategies. Here, we quantified how juvenile (<50 mm) coral demographics influenced benthic coral structure in reef flat and reef slope habitats on the southern Great Barrier Reef, Australia. Permanent plots and settlement tiles were monitored every six months for three years in each habitat. These environments exhibited profound differences: the reef slope was characterised by 95% less macroalgal cover, and twice the amount of available settlement substrata and rates of coral settlement than the reef flat. Consequently, post-settlement coral survival in the reef slope was substantially higher than that of the reef flat, and resulted in a rapid increase in coral cover from 7 to 31% in 2.5 years. In contrast, coral cover on the reef flat remained low (~10%), whereas macroalgal cover increased from 23 to 45%. A positive stock-recruitment relationship was found in brooding corals in both habitats; however, brooding corals were not directly responsible for the observed changes in coral cover. Rather, the rapid increase on the reef slope resulted from high abundances of broadcast spawning Acropora recruits. Incorporating our results into transition matrix models demonstrated that most corals escape mortality once they exceed 50 mm, but for smaller corals mortality in brooders was double those of spawners (i.e. acroporids and massive corals). For corals on the reef flat, sensitivity analysis demonstrated that growth and mortality of larger juveniles (21–50 mm) highly influenced population dynamics; whereas the recruitment, growth and mortality of smaller corals (<20 mm) had the highest influence on reef slope population dynamics. Our results provide insight into the population dynamics and recovery trajectories in disparate reef habitats, and highlight the importance of acroporid recruitment in driving rapid increases in coral cover following large-scale perturbation in reef slope environments.