Algal growth and species composition under experimental control of herbivory,phosphorus and coral abundance in Glovers Reef,Belize

The proliferation of algae on disturbed coral reefs has often been attributed to (1) a loss of large-bodied herbivorous fishes, (2) increases in sea water nutrient concentrations, particularly phosphorus, and (3) a loss of hard coral cover or a combination of these and other factors. We performed replicated small-scale caging experiments in the offshore lagoon of Glovers Reef atoll, Belize where three treatments had closed-top (no large-bodied herbivores) and one treatment had open-top cages (grazing by large-bodied herbivores). Closed-top treatments simulated a reduced-herbivory situation, excluding large fishes but including small herbivorous fishes such as damselfishes and small parrotfishes. Treatments in the closed-top cages included the addition of high phosphorus fertilizer, live branches of Acropora cervicornis and a third unmanipulated control treatment. Colonization, algal biomass and species composition on dead A. palmata "plates" were studied weekly for 50 days in each of the four treatments. Fertilization doubled the concentration of phosphorus from 0.35 to 0.77 microM. Closed-top cages, particularly the fertilizer and A. cervicornis additions, attracted more small-bodied parrotfish and damselfish than the open-top cages such that there was moderate levels of herbivory in closed-top cages. The open-top cages did, however, have a higher abundance of the chemically and morphologically defended erect algal species including Caulerpa cupressoides, Laurencia obtusa, Dictyota menstrualis and Lobophora variegata. The most herbivore-resistant calcareous green algae (i.e. Halimeda) were, however, uncommon in all treatments. Algal biomass increased and fluctuated simultaneously in all treatments over time, but algal biomass, as measured by wet, dry and decalcified weight, did not differ greatly between the treatments with only marginally higher biomass (p < 0.06) in the fertilized compared to open-top cages. Algal species composition was influenced by all treatments with a maximum between-treatment Bray-Curtis similarity of only 29%. The fertilized cages showed rapid colonization by a mixed turf community largely composed of the filamentous brown (Hincksia mitchelliae) and green (Enteromorpha prolifera) species. Algal cover in the fertilized cages leveled at 80% after 20 days compared to less than 50% in the other treatments. There was no evidence that A. cervicornis suppressed algal colonization compared to the unmanipulated controls. Instead, the herbivore susceptible Padina sanctae-crucis was the most abundant algae followed by Jania capillacea in this treatment in contrast to the more chemically defended Dictyota menstrualis that dominated the unmanipulated controls. We conclude that A. cervicornis was not suppressing algae as a group and its loss cannot account for the observed changes in algal abundance in most reefs except for creating space. In contrast, A. cervicornis appears to attract aggressive damselfish that may reduce herbivory by larger herbivores. Phosphorus enrichment can lead to rapid colonization of space by filamentous turf communities but not high biomass and dominance of erect frondose algae within 50 days. Moderate levels of herbivory by large-bodied herbivores promoted moderately herbivore-resistant erect brown and green algae that are commonly reported on disturbed reefs. Consequently, all the studied factors influenced algal communities but seldom as commonly predicted.     

Effect of nitrogen, phosphorous, and their interaction on coral reef algal succession in Glover's Reef, Belize

Nitrogen and phosphorous fertilizers were used to determine their short-term summer effects on algal colonization, abundance, and species composition in moderate herbivory treatments. Secondary succession of algae on coral skeletons was examined in four treatments: an untreated control, a pure phosphate fertilizer, a pure nitrogen fertilizer, and an equal mix of the two fertilizers. Turf algae cover was the only measure of algae abundance to respond significantly to fertilization. Turf cover was three times higher in treatments with added nitrogen when compared with the pure phosphorus treatment. These turfs were dominated by green and cyanobacteria taxa, namely Enteromorpha prolifera, Lyngbya confervoides, and two species of Cladophora. The phosphate treatment was dominated by encrusting corallines and the cyanobacteria L. confervoides, while the controls had the highest cover of frondose brown algae, namely Padina sanctae-crucis and two species of Dictyota. Results indicate that turf algae were co-limited by nitrogen and phosphorus but enrichment appeared to inhibit brown frondose algae that currently dominate these reefs. Number of species was lowest on the pure phosphorus and nitrogen treatments, highest in the controls and intermediate in the mixed treatments, which suggests that diversity is reduced most by an imbalanced nutrient ratio.     

Effects of algal turfs and sediment on coral settlement

Successful settlement and recruitment of corals is critical to the resilience of coral reefs. Given that many degraded reefs are dominated by benthic algae, recovery of coral populations after bleaching and other disturbances requires successful settlement amidst benthic algae. Algal turfs often accumulate sediments, sediments are known to inhibit coral settlement, and reefs with high inputs of terrestrial sediments are often dominated by turfs. We investigated the impacts of two algal turf assemblages, and of sediment deposits, on settlement of the coral Acropora millepora (Ehrenberg). Adding sediment reduced coral settlement, but the effects of different algal turfs varied. In one case, algal turfs inhibited coral settlement, whereas the other turf only inhibited settlement when combined with sediments. These results provide the first direct, experimental evidence of effects of filamentous algal turfs on coral settlement, the variability in those effects, and the potential combined effects of algal turfs and trapped sediments.     

Bathymetry, biota and sediments on the Hirota Reef, Tane-ga-shima – the northernmost coral reef in the Ryukyu Islands

Abstract Investigations were conducted on bathymetry, reef biota and sediments on the Hirota Reef, Tane‐ga‐shima, North Ryukyus, near the northern limit for coral‐reef formation. A bathymetric profile from shore to the reef edge was depicted along an approximately 420‐m transect on the Hirota Coast of this island. A total of 20 quadrats (1 m × 1 m) were analyzed along the profile at 10‐ or 20‐m intervals to clarify distribution of macrobenthos inhabiting the reef. The Hirota Reef is divided into four geomorphologic zones according to their depth, gradient, surface roughness, substrate and characteristic macrobenthos. They are, from shore to offshore, shallow lagoon, seaward reef flat, reef edge and reef slope. The shallow lagoon comprises a shoreward depression (∼160 m wide on the transect) with a sand/gravel bottom that inclines gently toward offshore, and a seaward patch zone (∼70 m wide). The patches (<2 m high) are covered with fleshy algae, coralline algae and hermatypic corals. The seaward reef flat (∼190 m wide) is a flat plane that is constructed by biogenic carbonates and is covered with turf algae, with hermatypic corals scattered. Although the seaward reef flat of the Hirota Reef cannot be differentiated into different geomorphologic zones, similar seaward reef flat areas in the Central and South Ryukyus can be clearly subdivided into inner reef flat, reef crest and outer reef flat. This difference may be attributed to a lower reef growth rate and/or the later reef formation of the Hirota Reef in Holocene time than the southern examples. The coral fauna on the Hirota Reef is delineated by low diversity and characterized by taxa typical of high‐latitude, non‐reefal communities. The algal flora consists of tropical to subtropical species associated with warm‐temperate species. These faunal and floral characteristics may be related largely to lower water temperature in Tane‐ga‐shima than those in typical coral‐reef regions.     

Macroalgae in the coral reefs of Eilat (Gulf of Aqaba, Red Sea) as a possible indicator of reef degradation

The current state of health of the coral reefs in the northern Gulf of Aqaba (Red Sea), notably the Eilat reefs, is under debate regarding both their exact condition and the causes of degradation. A dearth of earlier data and unequivocal reliable indices are the major problems hinder a clear understanding of the reef state. Our research objective was to examine coral-algal dynamics as a potential cause and an indication of reef degradation. The community structure of stony corals and algae along the northern Gulf of Aqaba reveal non-seasonal turf algae dominancy in the shallow Eilat reefs (up to 72%), while the proximate Aqaba reefs present negligible turf cover (<6%). We believe that turf dominancy can indicate degradation in these reefs, based on the reduction in essential reef components followed by proliferation of perennial turf algae. Our findings provide further evidence for the severe state of the Eilat coral reefs.     

Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis

This paper reviews and evaluates the current state of knowledge on the direct effects of terrestrial runoff on (1) the growth and survival of hard coral colonies, (2) coral reproduction and recruitment, and (3) organisms that interact with coral populations (coralline algae, bioeroders, macroalgae and heterotrophic filter feeders as space competitors, pathogens, and coral predators). The responses of each of these groups are evaluated separately against the four main water quality parameters: (1) increased dissolved inorganic nutrients, (2) enrichment with particulate organic matter, (3) light reduction from turbidity and (4) increased sedimentation. This separation facilitates disentangling and understanding the mechanisms leading to changes in the field, where many contaminants and many responses co-occur. The review also summarises geographic and biological factors that determine local and regional levels of resistance and resilience to degradation. It provides a conceptual aid to assess the kind of change(s) likely to occur in response to changing coastal water quality.     

Satellite imaging coral reef resilience at regional scale. A case-study from Saudi Arabia

We propose a framework for spatially estimating a proxy for coral reef resilience using remote sensing. Data spanning large areas of coral reef habitat were obtained using the commercial QuickBird satellite, and freely available imagery (NASA, Google Earth). Principles of coral reef ecology, field observation, and remote observations, were combined to devise mapped indices. These capture important and accessible components of coral reef resilience. Indices are divided between factors known to stress corals, and factors incorporating properties of the reef landscape that resist stress or promote coral growth. The first-basis for a remote sensed resilience index (RSRI), an estimate of expected reef resilience, is proposed. Developed for the Red Sea, the framework of our analysis is flexible and with minimal adaptation, could be extended to other reef regions. We aim to stimulate discussion as to use of remote sensing to do more than simply deliver habitat maps of coral reefs.     

Sealevel history recorded in the Pleistocene carbonate sequence in IODP Hole 310‐M0005D,off Tahiti

Material cored during the Integrated Ocean Drilling Program (IODP) Expedition 310 ‘Tahiti Sea Level’ revealed that the fossil reef systems around Tahiti are composed of two major stratigraphic sequences: (i) a last deglacial sequence; and (ii) an older Pleistocene sequence. The older Pleistocene carbonate sequence is composed of reef deposits associated with volcaniclastic sediments and was preserved in Hole 310‐M0005D drilled off Maraa. Within an approximately 70‐m‐thick older Pleistocene sequence (33.22–101.93 m below seafloor; 92.85–161.56 m below present sealevel) in this hole, 11 depositional units are defined by lithological changes, sedimentological features, and paleontological characteristics and are numbered sequentially from the top of the hole downward (Subunits P1–P11). Paleowater depths inferred from nongeniculate coralline algae, combined with those determined by using corals and larger foraminifers, suggest two major sealevel rises during the deposition of the older Pleistocene sequence. Of these, the second sealevel rise is associated with an intervening sealevel drop. It is likely that the second sealevel rise corresponds to that during Termination II (TII, the penultimate deglaciation, from Marine Isotope Stages 6 to 5e). Therefore, the intervening sealevel drop can be correlated with that known as the ‘sealevel reversal’ during TII. Because there are limited data on the Pleistocene reef systems in the tropical South Pacific Ocean, this study provides important information about Pleistocene sealevel history, the evolution of coral reef ecosystems, and the responses of coral reefs to Quaternary climate changes.     

The 1997/1998 mass mortality of corals: effects on fish communities on a Tanzanian coral reef

The abnormally high surface temperatures in the world's oceans during 1997/1998 resulted in widespread coral bleaching and subsequent coral mortality. An experiment was performed to study the effects of this coral mortality as well as the influence of the structural complexity on fish communities on a Tanzanian coral reef. Changes in fish communities were investigated on plots of transplanted corals after 88% of these corals had died. A distinct shift in fish community composition was found, although diversity was not affected. Fish abundance rose by 39% mostly due to an increase in herbivores, which seemed to benefit from enhanced algal growth on the dead corals. Fish abundance, species diversity and community composition were also strongly influenced by the structural complexity provided by the live and dead corals. This suggests that a coral reef can support abundant and diverse fish populations also after the corals have died as long as the reef structure is sustained.     

Coral death from sewage and phosphate pollution at Aqaba,Red Sea

Localized pollution of coral reef areas is occurring at Aqaba, Red Sea, as a result of sewage discharge, and as a result of spillage of phosphate dust during loading of phosphate mineral onto ships. The rate of death of colonies of the coral Stylophora pistillata was found to be 4–5 times as great in the polluted area as in a control area. Coral damage in the control area is generally caused by grazing or by extreme low tide, but the cause of coral death in the polluted area was not readily apparent. The growth of algae, both on the damaged corals, and on glass slides placed out in the reef, was greatly stimulated in the polluted area, but it appeared that such algal growth was not the direct cause of coral death. Corals in the polluted area may be under stress because of reduced light intensity, inhibition of calcification by excess phosphate, and increased sediment load. It was found that in the polluted area there was a greater weight of sediment settling on the glass slides for a given weight of algae. But in addition, since algal growth was faster in the polluted area, the sediment load was increased by the sediment trapping capacity of the enhanced algal growth. Thus it is suggested that increased algal growth stimulated by increased nutrient concentrations may be important in greatly increasing the sediment load experienced by corals.     

Changes in octocoral communities and benthic cover along a water quality gradient in the reefs of Hong Kong

Cover of the main reef benthic groups, and abundances and taxonomic richness of octocorals were surveyed in the reefs of Hong Kong, and related to spatial and water quality gradients. Nutrient and particle concentrations are high throughout the area, with concentrations declining from the south towards the north-eastern region. Regression tree analyses showed that hard coral cover was most strongly related to water clarity, that macroalgal cover was highest in areas with high wave action and high water clarity, and that crustose coralline algae were negatively related to sedimentation. Octocoral communities (42 species in 23 genera) were dominated by zooxanthellae-free taxa; those few species with zooxanthellae were restricted to reefs with low wave action and high water clarity in the north-eastern region. The water quality gradient spans from conditions that are marginal for zooxanthellate octocorals while still supporting diverse scleractinian communities, towards an estuarine endpoint where zooxanthellate octocorals cease to exist and hard coral communities are reduced to a few resilient colonies. The data suggest that the types, abundances and richness of zooxanthellate octocorals, and the shift from zooxanthellate to azooxanthellate octocoral communities, may act as useful indicators of water clarity in regions where long-term water quality data are unavailable.     

Metal contents in Porites corals: Anthropogenic input of river run-off into a coral reef from an urbanized area, Okinawa

In order to monitor pollutants from urban areas to coral reefs, metal contents in Porites coral samples collected from the Hija River mouth and at nearby sites from the estuary were analyzed. The corals were cleaned by oxidative and reductive treatments to effectively eliminate detritus and organic materials. Metal-to-calcium (Me/Ca) ratios in the samples were determined by ICP-MS. Filtered samples of river water were also measured similarly for metal concentrations. The extent of anthropogenic contribution by riverine input was assessed by comparing the Me/Ca values in corals to those of Rukan-sho, an unpolluted coral reef. High riverine inputs of Mn, Cd, Zn and Ag were observed from Me/Ca values in the coral samples. Manganese in the coral samples showed strong dependence on salinity, varying inversely to the distance from terrestrial sources. Considering a lead background of 25.0 nmol/mol measured in the Rukan-sho corals, Pb/Ca in corals of the Hija River estuary that are two and three times higher may indicate lead enrichment in the river mouth. Because Pb is only moderately high in the Hija River water compared to its concentration in surface seawater, lead may have accumulated in the estuarine water and sediments, resulting in an elevated concentration of lead available for coral uptake.     

Benthic status of near-shore fishing grounds in the central Philippines and associated seahorse densities

Benthic status of 28 near-shore, artisanal, coral reef fishing grounds in the central Philippines was assessed (2000-2002) together with surveys of the seahorse, Hippocampus comes. Our measures of benthic quality and seahorse densities reveal some of the most degraded coral reefs in the world. Abiotic structure dominated the fishing grounds: 69% of the benthos comprised rubble (32%), sand/silt (28%) and dead coral (9%). Predominant biotic structure included live coral (12%) and Sargassum (11%). Rubble cover increased with increasing distance from municipal enforcement centers and coincided with substantial blast fishing in this region of the Philippines. Over 2 years, we measured a significant decrease in benthic 'heterogeneity' and a 16% increase in rubble cover. Poor benthic quality was concomitant with extremely low seahorse densities (524 fish per km(2)). Spatial management, such as marine reserves, may help to minimize habitat damage and to rebuild depleted populations of seahorses and other reef fauna.     

Carbon and nitrogen cycling in the Zhubi coral reef lagoon of the South China Sea as revealed by 210Po and 210Pb

The radionuclides (210)Po and (210)Pb were examined to trace the cycling of particulate organic carbon (POC) and particulate organic nitrogen (PON) in the Zhubi coral reef lagoon. The net export flux of POC to the open sea is 14 mg Cm(-2) d(-1). However, the net exchange of PON has not yet been observed. On average, the vertical export fluxes in the lagoon of POC and PON, as derived from (210)Po/(210)Pb disequilibria, are 43 mg Cm(-2) d(-1) and 13.8 mg Nm(-2) d(-1), respectively. The deficit of (210)Po relative to (210)Pb in particulate matter provides evidence for the degradation of particulate organic matter. According to the mass balance budgets, 310 mg Cm(-2) d(-1) and 121 mg Nm(-2) d(-1) were recycled into dissolved fractions. Based on a first-order kinetics model, the degradation rate constants of POC and PON are 0.28 and 0.30 m(-1), respectively. Thus, (210)Po and (210)Pb can quantify the cycling of carbon and nitrogen in this coral lagoon.     

In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon

Our view of how water quality effects ecosystems of the Great Barrier Reef (GBR) is largely framed by observed or expected responses of large benthic organisms (corals, algae, seagrasses) to enhanced levels of dissolved nutrients, sediments and other pollutants in reef waters. In the case of nutrients, however, benthic organisms and communities are largely responding to materials which have cycled through and been transformed by pelagic communities dominated by micro-algae (phytoplankton), protozoa, flagellates and bacteria. Because GBR waters are characterised by high ambient light intensities and water temperatures, inputs of nutrients from both internal and external sources are rapidly taken up and converted to organic matter in inter-reefal waters. Phytoplankton growth, pelagic grazing and remineralisation rates are very rapid. Dominant phytoplankton species in GBR waters have in situ growth rates which range from approximately 1 to several doublings per day. To a first approximation, phytoplankton communities and their constituent nutrient content turn over on a daily basis. Relative abundances of dissolved nutrient species strongly indicate N limitation of new biomass formation. Direct ((15)N) and indirect ((14)C) estimates of N demand by phytoplankton indicate dissolved inorganic N pools have turnover times on the order of hours to days. Turnover times for inorganic phosphorus in the water column range from hours to weeks. Because of the rapid assimilation of nutrients by plankton communities, biological responses in benthic communities to changed water quality are more likely driven (at several ecological levels) by organic matter derived from pelagic primary production than by dissolved nutrient stocks alone.     

Monitored and modeled coral population dynamics and the refuge concept

With large-scale impacts on coral reefs due to global climatic change projected to increase dramatically, and suitability of many areas for reef growth projected to decrease, the question arises whether particular settings might serve as refugia that can maintain higher coral populations than surrounding areas. We examine this hypothesis on a small, local scale in Honduras, western Caribbean. Dense coral thickets containing high numbers of the endangered coral Acropora cervicornis occur on offshore banks while being rare on the fringing reef on nearby Roatán. Geomorphological setting and community dynamics were evaluated and monitored from 1996 to 2005. A model of population dynamics was developed to test assumptions derived from monitoring. Coral cover on the fringing reef declined in 1998 from >30% to <20%, but the banks maintained areas of very dense coral cover (32% cover by A. cervicornis on the banks but <1% on the fringing reef). Bathymetry from satellite images showed the banks to be well-separated from the fringing reef, making asexual connectivity between banks and fringing reef impossible but protecting the banks from direct land-runoff during storms. Exposure to SE tradewinds also causes good flushing. Only four A. cervicornis recruits were recorded on the fringing reef over 6 years. Runoff associated with hurricanes caused greater mortality than did bleaching in 1998 and 2005 on the fringing reef, but not on the banks. Since 1870, our analysis suggests that corals on the banks may have been favored during 17 runoff events associated with tropical depressions and storms and potentially also during five bleaching events, but this is more uncertain. Our model suggests that under this disturbance regime, the banks will indeed maintain higher coral populations than the fringing reef and supports the assumption that offshore banks could serve as refugia with the capacity to subsidize depleted mainland populations.     

Genesis of marine terrace soils,Barbados, West Indies: Evidence from mineralogy and geochemistry

Well-developed, clay-rich soils dominated by interstratified kaolinite-smectite are found on the uplifted coral reef terraces on the island of Barbados. The reef limestone is unlikely to have been the soil parent material however, because it is 98 per cent CaCO₃ and geomorphic evidence argues against the 20 m of reef solution required to produce the soils by this process. The mineralogy of the sand, silt, and clay fractions of the soils, and trace element geochemistry, suggest that aeolian materials carried on the trade winds from Africa, volcanic ash from the island of St. Vincent, and quartz from Tertiary bedrock on the island itself are the parent materials for the soils.     

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.