Persistent infectivity of a disease-associated herpesvirus in green turtles after exposure to seawater

Herpesviruses are associated with several diseases of marine turtles including lung-eye-trachea disease (LETD) and gray patch disease (GPD) of green turtles (Chelonia mydas) and fibropapillomatosis (FP) of green, loggerhead (Caretta caretta), and olive ridley turtles (Lepidochelys olivacea). The stability of chelonian herpesviruses in the marine environment, which may influence transmission, has not been previously studied. In these experiments, LETD-associated herpesvirus (LETV) was used as a model chelonian herpesvirus to test viral infectivity after exposure to seawater. The LETV virus preparations grown in terrapene heart (TH-1) cells were dialyzed for 24 to 120 hr against aerated artificial or natural seawater or Hank's balanced salt solution (HBBS). Fresh TH-1 cells were inoculated with dialyzed LETV, and on day 10 post-infection cells were scored for cytopathic effect. Virus samples dialyzed up to 120 hr were positive for the herpesvirus DNA polymerase gene by polymerase chain reaction. Electron microscopy revealed intact LETV nucleocapsids after exposure of LETV to artificial seawater or HBSS for 24 hr at 23 C. LETV preparations remained infectious as long as 120 hr in natural and artificial seawater at 23 C. Similar results were obtained with a second culturable chelonian herpesvirus, HV2245. LETV infectivity could not be detected after 48 hr exposure to artificial seawater at 30 C. Since LETV and HV2245 remain infectious for extended periods of time in the marine environment, it is possible that FP-associated and GPD-associated herpesviruses also may be stable. These findings are significant both for researchers studying the epidemiological association of herpesviruses with diseases of marine turtles and for individuals who handle turtles in marine turtle conservation efforts.     

大型海藻的营养盐代谢及其与近岸海域富营养化的关系

大型海藻是近岸海域重要的初级生产者,近年来人们愈来愈认识到大型海藻在近岸海域富营养化生物修复中的重要性,同时,富营养化也可能招致某些机会主义大型海藻种类的爆发生长,因此,进一步理解大型海藻与营养盐供应变化的关系就显得非常重要。本文从大型海藻营养盐代谢与海水中营养盐供应变化(主要是富营养化)的生理生态关系角度对相关问题进行评述,主要包括影响大型海藻营养盐吸收特性的重要因素、海水中营养盐的供应及大型海藻对营养盐的细胞贮存、大型海藻对营养盐的生态需求、大型海藻对近岸海域富营养化的生态响应等问题。文章还对今后的研究提出了展望。     

Influence of salinity, nutrients and light on the germination and growth of Enteromorpha sp. spores

In many shallow coastal areas worldwide, several species of opportunistic macroalgae (mainly Chlorophyta) have an excessive growth, as a consequence of eutrophication processes. Therefore, bloom-forming macroalgae become the dominant primary producers within these coastal systems. However, frequently the ecology and the ecophysiology of adult macroalgae have been insufficient to explain their seasonal abundances. Thus, it is essential to understand the factors that regulate the germination and growth of spores of opportunistic green macroalgae. In the present work, we assessed the effects of nutrients (N and P), salinity and light on the germination and growth of Enteromorpha spores. Overall, the results highlight the fact that, such as for adult macroalgae, spore germination and growth are adversely affected by low salinities. Growth of the spores is significantly decreased at 5 psu, while salinities of 20 and, especially of 35 psu, clearly promote the spore growth. Additionally, Enteromorpha spores seem to be particularly sensitive to PO₄-P limitation and to NH₄-N toxicity, which suggests a higher sensitivity to the variation of external nutrient concentrations than adult macroalgae. The present results contribute to increase the understanding about the factors that control macroalgal growth at its early phases of development. In particular, the results suggest that the growth of spores from opportunistic green macroalgae is strongly salinity-dependent. Consequently, in highly hydrodynamic systems such as most shallow estuaries, salinity variations may play a determinant role in the yearly abundances of green macroalgae, since it controls macroalgal growth from the spores to the adults.     

High rates of growth recorded for hawksbill sea turtles in Anegada,British Virgin Islands

Management of species of conservation concern requires knowledge of demographic parameters, such as rates of recruitment, survival, and growth. In the Caribbean, hawksbill turtles (Eretmochelys imbricata) have been historically exploited in huge numbers to satisfy trade in their shells and meat. In the present study, we estimated growth rate of juvenile hawksbill turtles around Anegada, British Virgin Islands, using capture–mark–recapture of 59 turtles over periods of up to 649 days. Turtles were recaptured up to six times, having moved up to 5.9 km from the release location. Across all sizes, turtles grew at an average rate of 9.3 cm year⁻¹ (range 2.3–20.3 cm year⁻¹), and gained mass at an average of 3.9 kg year⁻¹ (range 850 g–16.1 kg year⁻¹). Carapace length was a significant predictor of growth rate and mass gain, but there was no relationship between either variable and sea surface temperature. These are among the fastest rates of growth reported for this species, with seven turtles growing at a rate that would increase their body size by more than half per year (51–69% increase in body length). This study also demonstrates the importance of shallow water reef systems for the developmental habitat for juvenile hawksbill turtles. Although growth rates for posthatching turtles in the pelagic, and turtles larger than 61 cm, are not known for this population, the implications of this study are that Caribbean hawksbill turtles in some areas may reach body sizes suggesting sexual maturity in less time than previously considered.     

Effects of macroalgal identity on epifaunal assemblages: native species versus the invasive species Sargassum muticum

Seaweeds are a refuge from stressful conditions associated with life on rocky intertidal shores, and there is evidence that different macrophytes support different assemblages of mobile epifauna. Introduction of non-indigenous macroalgae may have a great impact on associated epifaunal assemblages and ecosystem processes in coastal areas. Previous studies have reported conflicting evidences for the ability of epifauna to colonize non-indigenous species. Here, we analyzed epifaunal assemblages associated with three species of macroalgae that are very abundant on intertidal shores along the Galician coast: the two native species Bifurcaria bifurcata and Saccorhiza polyschides and the invasive species Sargassum muticum. We collected samples of each species from three different sites at three different times to test whether variability of epifaunal assemblages was consistent over space and time. Epifaunal assemblages differed between the three macroalgae. Results suggested that stability and morphology of habitat played an important role in shaping the structure of epifaunal assemblages. This study also showed that the invasive S. muticum offered a suitable habitat for many invertebrates.     

The Ecological Perspective of Microbial Communities in Two Pairs of Competitive Hawaiian Native and Invasive Macroalgae

Marine macroalgae are known to harbor large populations of microbial symbionts, and yet, microbe symbiosis in invasive macroalgae remains largely unknown. In this study, we applied molecular methods to study microbial communities associated with two invasive algae Acanthophora spicifera and Gracilaria salicornia and the two native algae Gracilaria coronopifolia and Laurencia nidifica at spatial and temporal scales in Hawaiian coral reef ecosystems. Bacterial communities of both the invasive and native macroalgae displayed little spatial and temporal variations, suggesting consistent and stable bacterial associations with these macroalgae. Results of this study identified three types of bacterial populations: nonspecific (present in both algal and water samples); algae-specific (found in all algal species); and species-specific (only found in individual species). The bacterial diversity of invasive algae was lower than that of their native counterparts at phylum and species levels. Notably, the vast majority (71 %) of bacterial communities associated with the invasive algae G. salicornia were representatives of Cyanobacteria, suggesting a potential ecological significance of symbiotic Cyanobacteria.     

Macroalgae Has No Effect on the Severity and Dynamics of Caribbean Yellow Band Disease

By removing herbivores and promoting increases in macroalgae, overfishing is thought to indirectly cause coral disease and mortality. We performed three field manipulations to test the general hypothesis that overfishing and the subsequent alteration of coral reef trophic dynamics are a cause of coral epizootics. Specifically, we asked whether the presence of macroalgae can influence within- and among-colony spread rates of Caribbean Yellow Band Disease in Montastraea faveolata. Macroalgae were placed next to infected and healthy, adult and small coral colonies to measure effects on disease spread rate, coral growth and coral survival. Surprisingly, the addition of macroalgae did not affect disease severity or coral fitness. Our results indicate that macroalgae have no effect on the severity and dynamics of Caribbean Yellow Band Disease and that fisheries management alone will not mitigate the effects of this important epizootic.     

Marine Turtles as Sentinels of Ecosystem Health: Is Fibropapillomatosis an Indicator?

Marine turtle fibropapillomatosis (FP) is a disease primarily affecting green turtles (Chelonia mydas) that is characterized by multiple cutaneous masses. In addition, the condition has been confirmed in other species of sea turtles. The disease has a worldwide, circumtropical distribution and has been observed in all major oceans. Although reported since the late 1930s in Florida, it was not until the late 1980s that it reached epizootic proportions in several sea turtle populations. Long-term studies have shown that pelagic turtles recruiting to near shore environments are free of the disease. After exposure to these benthic ecosystems, FP manifests itself with primary growths in the corner of the eyes spreading to other epithelial tissue. One or more herpesviruses, a papillomavirus, and a retrovirus have been found associated with tumors using electron microscopy and molecular techniques; however, the primary etiological agent remains to be isolated and characterized. Field observations support that the prevalence of the disease is associated with heavily polluted coastal areas, areas of high human density, agricultural runoff, and/or biotoxin-producing algae. Marine turtles can serve as excellent sentinels of ecosystem health in these benthic environments. FP can possibly be used as an indicator but correlations with physical and chemical characteristics of water and other factors need to be made. Further research in identifying the etiologic agent and its association with other environmental variables can provide sufficient parameters to measure the health of coastal marine ecosystems, which serve not only as ecotourism spots but also as primary feeding areas for sea turtles.     

Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef

 Degradation of coral reefs often involves a “phase shift” from abundant coral to abundant macroalgae. This paper critically reviews the roles of nutrient increases in such phase shifts. I conclude that nutrient overloads can contribute to reef degradation, but that they are unlikely to lead to phase shifts simply by enhancing algal growth rates and hence allowing overgrowth of corals, unless herbivory is unusually or artificially low. Concentrations of dissolved inorganic nutrients are poor indicators of reef status, and the concept of a simple threshold concentration that indicates eutrophication has little validity. I discuss the significance and consequences of these assessments for reef management, focusing on the Great Barrier Reef, and conclude with some specific recommendations, including protection of herbivorous fishes, minimisation of terrestrial runoff, and protection of coastal reefs. Accepted: 13 August 1999     

Metabolic scaling in turtles

Bennett and Dawson (1976) presented an analysis of the relationship of metabolic rate (MR) and body mass among turtles, based on 10 studies, but unlike most of other groups of ectotherms, there has been no update to include the many later reports on turtles. Here I present a review of the data on turtle metabolic rates at 20, 25, and 30 °C, along with regression equations and graphical analyses from a large number of studies. Two generalities emerge: (1) reported metabolic rates for sea turtles are higher than for other chelonians, although it is not certain whether this is an intrinsic characteristic of sea turtles or an artifact related to experimental conditions (such as greater activity of sea turtles in metabolic chambers and the fact that a number of studies were done with the turtles out of water), and (2) the slopes of the log–log plots of metabolic rate (MR) vs. body mass [b in the allometric equation MR = a(mass)^b] are mostly lower than previously reported in smaller studies.     

Effects of herbivory,nutrients, and reef protection on algal proliferation and coral growth on a tropical reef

Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9-46 times, upright macroalgal biomass by 23-84 times, and cyanobacteria cover by 0-27 times, but decreased cover of encrusting coralline algae by 46-100% and short turf algae by 14-39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33-42%) and cyanobacteria (by 71% on the protected reef) when herbivores were excluded. Herbivore exclusion, but not nutrient enrichment, also increased sediment accumulation, suggesting a strong link between herbivory, macroalgal growth, and sediment retention. Growth rates of the corals Porites cylindrica and Acropora millepora were 30-35% greater on the protected versus fished reef, but nutrient and herbivore manipulations within a site did not affect coral growth. Cumulatively, these data suggest that herbivory rather than eutrophication plays the dominant role in mediating macroalgal proliferation, that macroalgae trap sediments that may further suppress herbivory and enhance macroalgal dominance, and that corals are relatively resistant to damage from some macroalgae but are significantly impacted by ambient reef condition.     

Association of herpesvirus with fibropapillomatosis of the green turtle Chelonia mydas and the loggerhead turtle Caretta caretta in Florida.

Sea turtle fibropapillomatosis (FP) is a disease marked by proliferation of benign but debilitating cutaneous fibropapillomas and occasional visceral fibromas. Transmission experiments have implicated a chloroform-sensitive transforming agent present in filtered cell-free tumor homogenates in the etiology of FP. In this study, consensus primer PCR methodology was used to test the association of a chelonian herpesvirus with fibropapillomatosis. Fibropapilloma and skin samples were obtained from 17 green and 2 loggerhead turtles affected with FP stranded along the Florida coastline. Ninety-three cutaneous and visceral tumors from the 19 turtles, and 33 skin samples from 16 of the turtles, were tested. All turtles affected with FP had herpesvirus associated with their tumors as detected by PCR. Ninety-six percent (89/93) of the tumors, but only 9% (3/33) of the skin samples, from affected turtles contained detectable herpesvirus. The skin samples that contained herpesvirus were all within 2 cm of a fibropapilloma. Also, 1 of 11 scar tissue samples from sites where fibropapillomas had been removed 2 to 51 wk earlier from 5 green turtles contained detectable herpesvirus. None of 18 normal skin samples from 2 green and 2 loggerhead turtles stranded without FP contained herpesvirus. The data indicated that herpesvirus was detectable only within or close to tumors. To determine if the same virus infected both turtle species, partial nucleotide sequences of the herpesvirus DNA polymerase gene were determined from 6 loggerhead and 2 green turtle samples. The sequences predicted that herpesvirus of loggerhead turtles differed from those of green turtles by only 1 of 60 amino acids in the sequence examined, indicating that a chelonian herpesvirus exhibiting minor intratypic variation was the only herpesvirus present in tumors of both green and loggerhead turtles. The FP-associated herpesvirus resisted cultivation on chelonian cell lines which support the replication of other chelonian herpesviruses. These results lead to the conclusion that a chelonian herpesvirus is regularly associated with fibropapillomatosis and is not merely an incidental finding in affected turtles.     

Recombinant Murine Gamma Herpesvirus 68 Carrying KSHV G Protein-Coupled Receptor Induces Angiogenic Lesions in Mice

Human gamma herpesviruses, including Kaposi’s sarcoma-associated herpesvirus (KSHV) and Epstein-Barr virus (EBV), are capable of inducing tumors, particularly in in immune-compromised individuals. Due to the stringent host tropism, rodents are resistant to infection by human gamma herpesviruses, creating a significant barrier for the in vivo study of viral genes that contribute to tumorigenesis. The closely-related murine gamma herpesvirus 68 (γHV68) efficiently infects laboratory mouse strains and establishes robust persistent infection without causing apparent disease. Here, we report that a recombinant γHV68 carrying the KSHV G protein-coupled receptor (kGPCR) in place of its murine counterpart induces angiogenic tumors in infected mice. Although viral GPCRs are conserved in all gamma herpesviruses, kGPCR potently activated downstream signaling and induced tumor formation in nude mouse, whereas γHV68 GPCR failed to do so. Recombinant γHV68 carrying kGPCR demonstrated more robust lytic replication ex vivo than wild-type γHV68, although both viruses underwent similar acute and latent infection in vivo. Infection of immunosuppressed mice with γHV68 carrying kGPCR, but not wild-type γHV68, induced tumors in mice that exhibited angiogenic and inflammatory features shared with human Kaposi’s sarcoma. Immunohistochemistry staining identified abundant latently-infected cells and a small number of cells supporting lytic replication in tumor tissue. Thus, mouse infection with a recombinant γHV68 carrying kGPCR provides a useful small animal model for tumorigenesis induced by a human gamma herpesvirus gene in the setting of a natural course of infection.     

Technical note: side-scan sonar enables rapid detection of aquatic reptiles in turbid lotic systems

Monitoring rare aquatic reptiles in turbid rivers and lagoons is complicated by low detection rates due to low visibility. We tested the use of side-scan sonar as a simple, rapid method for detecting turtles and identifying areas of high activity that could then be targeted with capture methods. We compared detection rates of turtles (Dermatemys mawii and Trachemys venusta venusta) in the New River Lagoon, Belize, using sonar, visual surveys, trammel nets, and baited traps. Sonar surveys detected 0.75 turtles/h (daytime) and 4 turtles/h (nocturnal surveys). In comparison, visual surveys detected 0 turtles/h; hoop traps detected 0.003 turtles/h; and trammel netting detected 1.75 turtles/h. Sonar surveys also detected Crocodylus moreletii (0.28 crocodiles/h). Sonar surveys do not directly facilitate capture and identification, and the efficacy of this method varies with the depth and substrate of the survey area. Sonar surveys are a useful preliminary detection tool for large aquatic reptiles in turbid waterways with soft substrate, allowing rapid, preliminary presence–absence surveys and identification of activity hotspots.     

Widespread and enduring demographic collapse of invasive common carp (<Emphasis Type="Italic">Cyprinus carpio</Emphasis>) in the Upper Mississippi River System

Populations of invasive species that undergo rapid expansions after establishment in a new system can also be subject to collapse. Although the dynamics of the establishment and expansion phases and their ecological effects are well documented, substantially fewer studies document collapses despite their importance for understanding invasion dynamics. Two long-term fish monitoring programs sample the fish assemblage of the Upper Mississippi River System. These data provide an opportunity to document the collapse of common carp (Cyprinus carpio), a globally invasive freshwater fish species. Here we describe their population trajectory over several decades and examine several hypotheses to explain the decline, including: boom-bust population dynamics; suppression by native predators; resource exhaustion; improvements in environmental conditions; and disease. The observed trends appear to be most consistent with the hypothesis that disease was the most important factor contributing to the collapse. In particular, cyprinid herpesviruses have been shown to affect common carp in a manner consistent with the observed decreases in catch rates and increases in size distributions. The apparent role of a viral agent in causing the decline of common carp across one of the largest river basins in North America suggests similar collapses may occur elsewhere.     

Past, current and future thermal profiles of green turtle nesting grounds: Implications from climate change

Sex determination and hatching success in sea turtles is temperature dependent and as a result global warming poses a threat to sea turtles. Warmer sand temperatures may skew sea turtle population′s sex ratios towards predominantly females and decrease hatching success. Therefore, understanding the rates at which sand temperatures are likely to increase as climate change progresses is warranted. We recorded sand temperature and used historical sea surface and air temperature to model past and to predict future sand temperature under various scenarios of global warming at key sea turtle nesting grounds (n = 7) used by the northern Great Barrier Reef (nGBR) green turtle, Chelonia mydas, population. Reconstructed temperatures from 1990 to the present suggest that sand temperatures at the nesting sites studied have not changed significantly during the last 18 years. Current thermal profile at the nesting grounds suggests a bias towards female hatchling production into this population. Inter-beach thermal variance was observed at some nesting grounds with open areas in the sand dune at northern facing beaches having the warmest incubating environments. Our model projections suggest that a near complete feminization of hatchling output into this population will occur by 2070 under an extreme scenario of climate change (A1T emission scenario). Importantly, we found that some nesting grounds will still produce male hatchlings, under the most extreme scenario of climate change, this finding differs from predictions for other locations. Information from this study provides a better understanding of possible future changes in hatching success and sex ratios at each site and identifies important male producing regions. This allowed us to suggest strategies that can be used at a local scale to offset some of the impacts of warmer incubating temperatures to sea turtles.     

Algal assemblages associated with Stegastes sp. territories on Indo-Pacific coral reefs: Characterization of diversity and controls on growth

Herbivorous fish occupy an important niche in coral reef ecosystems. Specifically, damselfish of the genus Stegastes have been shown to have a significant impact on coral community structure and algal assemblages. This study investigated the algal communities associated with Stegastes territories of the Indo-Pacific (Fiji, Solomon Islands, and Tonga), while concurrently examining the effects of nutrient enrichment and herbivore exclusion (alone and in unison) on these communities. Results evidenced differences in species composition, percent cover, and algal growth rate between Stegastes territories and non-Stegastes sites and between control sites and treatment sites. Stegastes territories consistently displayed a greater abundance of turf algae than non-Stegastes sites; the two main genera of turf algae observed at all sites were Polysiphonia and Ceramium. Although non-Stegastes sites in Fiji, the Solomon Islands, and Tonga showed a greater percent coverage of macroalgae, they contained fewer algal species compared to Stegastes territories. In Fiji, red macroalgae decreased in the herbivore exclusion treatments, while brown macroalgae increased significantly in the herbivore exclusion and nutrient treatments. The combined effect of the herbivore exclusion and nutrient treatment at this location yielded a significantly increased turf algae growth rate compared to control sites. Growth rates of turf algae in the Solomon Islands and Tonga increased significantly in caged treatments, suggesting that damselfish of the genus Stegastes can play an important role in maintaining cropped algal beds. In summation, the results demonstrated that Stegastes sustains distinct algal assemblages which may be disrupted by reduced grazing and/or eutrophication.     

The diet composition of immature loggerheads: Insights on trophic niche, growth rates, and fisheries interactions

For immature animals, diet quality and composition influence expression of life history traits such as growth rates and ultimately life stage duration and age to maturity. Circumglobally distributed loggerhead turtles (Caretta caretta) exhibit a multi-decade immature stage that generally occupies neritic habitats and is characterized by slow growth and an omnivorous diet. Although adult nesting populations are geographically distinct, foraging areas for immature loggerheads show a high degree of mixing of individuals that originate from multiple nesting stocks. Furthermore, despite their generalist foraging ecology, immature loggerheads have been observed to supplement their natural diets with fish from fishery discards and/or caught in fishing gear. However, whether trophic opportunism results in variation in loggerhead growth rates within or among feeding areas has not been investigated. In Core Sound, North Carolina (NC), USA, immature loggerheads demonstrate highly variable size-specific growth rates, in contrast to other studies that report discernible somatic growth functions in immature marine turtles. To determine whether inter-individual variation in growth rates at this site was due to variation in diet composition, and specifically variation in consumption of fish, we analyzed carbon and nitrogen stable isotope ratios of loggerhead blood plasma and of tissue samples of putative loggerhead prey, as well as commercially important fish species. Our results indicated that growth rates were not related to trophic levels at which individual turtles fed, but rather probably reflected inter-individual variation in overwintering or foraging behavior (i.e. nearshore vs. offshore). Furthermore, loggerhead diets were highly diverse, and comprised mainly blue crabs and/or whelks, as well as small proportions of cannonball jellies. Fish were unimportant dietary components for loggerheads. Although loggerheads in NC do not appear to feed on fish catch or discards, immature turtles showed dietary preferences for prey items that are also valuable to or are commonly taken as bycatch in commercial fisheries (e.g. blue crabs and whelks, respectively) in the region. Thus, the status of these prey items/fishery stocks as well as trends in loggerhead populations should be monitored to mitigate potential competitive interactions between fisheries activities and loggerhead turtles.     

Response of ecological indices to nutrient and chemical contaminant stress factors in Eastern Mediterranean coastal waters

Environmental data produced throughout monitoring activities in the framework of the implementation of Water Framework Directive 2000/60/EC (WFD) in Eastern Mediterranean (Greece) were used to assess the sensitivity and response of ecological indices against trace metals, eutrophication and multiple stress factors. The applied ecological indices include multi-metric eutrophication indices, a physicochemical status index applied for the first time in the Greek marine area, benthic indices, phytoplankton biomass index, and integrated status indices assessed through the application of the decision tree integration scheme. To investigate the exceedances in the eco-stoichiometric relationship between nutrients, considered a stressing factor, all physicochemical elements influenced directly or indirectly by eutrophication, such as nutrient concentrations, water transparency, oxygen saturation, particulates concentration, and sediment organic content, were related to ecological indices. Also, chemical contaminant stress factors represented by heavy metal concentrations in the water, as well as multiple stress factors represented by a pressure index, were related to ecological indices. A graphical visualization multivariate tool and statistical correlations were used to evaluate the sensitivity or explanatory power of the tested ecological indices against single and multiple stress factors. Results showed a strong response of all ecological indices to stress factors, although a diversification of sensitivity was evident. Primary production-related indices, i.e., macroalgae and chlorophyll-a indices, are more sensitive to particulates and nitrogen, while secondary production-related indices, i.e., benthic macroinvertebrates indices and eutrophication indices, including nutrients, are more sensitive to phosphates in the water column. The macroalgae index shows the strongest sensitivity to multiple stress factors. Among metals, mostly cadmium seems to match all indices⿿ performance. Nutrient relationships were shown as critical to eutrophication and ecological status.