Deep-sea caging of the mussel Mytilus galloprovincialis: Potential application in ecotoxicological studies

We experimented with caging the Mediterranean mussel (Mytilus galloprovincialis) at various depths for 69 d to measure basic physiological parameters, histological response and bio-accumulation of contaminants in a deep-sea contaminated area. In preliminary experiments, we demonstrated, under artificial pressure conditions, the ability of mussels Mytilus galloprovincialis to tolerate rapid immersion (at a speed of up to 120 m min^?1). In situ experiments were performed using submerged lines enabling mussels to be maintained at depths ranging of 40–1550 m with survival rates ranging from 80 to 38%, respectively. No significant differences in condition indexes were observed between treated and control specimens. However, histological observations demonstrated a clear reduction in thickness of the digestive epithelium with increasing depth exposure. By determining the contaminants in caged mussels, we found the following values for chromium accumulation: 27.4 μg g^?1 dry weight at 580 m depth and 9.8 μg g^?1 dry weight at 1550 m. Selected stations were located downstream of an industrial effluent at 420 m. The biological and environmental consequences of deep-sea contamination demonstrate the suitability of caged mussels for monitoring contaminant accumulation.     

Total body zinc concentration and allometric growth ratios in Mytilus edulis collected from different shore levels

Body zinc concentrations (on a soft parts dry weight basis) in 18 composite collections of mussels (Mytilus edulis) taken from different shore levels within a single mussel bed on the north shore of the Tyne estuary at Tynemouth, on 25 October, 1980, showed highly significant correlations with 4 allometric, size-related factors. A negative correlation was found between body zinc concentration and a flesh condition (FC) index defined as mg dry flesh wt per g dry shell wt. Positive correlations were found between body zinc concentration and width: height ratio, width: length ratio and shell valve inequality index (SVI) defined as the weight of heavier shell valve/weight of lighter shell valve. Unlike earlier observations on a single population taken from a single habitat, this heterogeneous collection showed no significant relationship between body zinc concentration and body size as determined by soft-parts dry weight. Body zinc concentration and allometric ratios were, however, related to position on the shoreline. It is suggested that, where mussels are collected from different habitats, environmental factors probably have a greater influence on body size than age. Therefore, normalization of trace metal concentrations to a standard body weight may not be appropriate where specimens are collected from a variety of habitats. Allometric ratios are related to age, but are independent of absolute size, and may therefore provide a more suitable basis for normalization of trace metal concentration within a monitoring programme.Contribution No. 1222 of the Center for Estuarine and Environmental Studies of the University of Maryland     

Background metal levels determination in bivalves – quality assessment of the European Water Framework Directive

Background levels of metals (Ag, Cd, Cu, Cr, Hg, Ni, Pb and Zn) in biomonitors (Mytilus galloprovincialis mussels and Crassostrea gigas oysters), in estuarine waters within the Basque Country (south-east Bay of Biscay) are estimated using non-parametric statistical tools and data are presented graphically, with the aim of being used in assessing the ecological status, within the European Water Framework Directive (WFD). The basis for this study was the statistical analysis of data compiled from monitoring programmes undertaken along the Basque coast, between 1990 and 2008. For this analysis, a heuristic method was adapted and used. Results showed different metal background ranges throughout the year for both mussels and oysters. Values corresponding to the upper limit of the background range (i.e. value of the upper whisker of the box-plot) are proposed as the ‘high/good’ status boundary, according to the WFD.     

Occurrence of tri-n-butyltin-caused imposex in the North Pacific marine snail Nucella lima in Auke Bay,Alaska

Like female dog whelks (Nucella lapillus) in the Atlantic Ocean, females of the Pacific gastropod N. lima respond to low concentrations of tri-n-butyltin (TBT) by growing a penis and vas deferens. This condition, termed imposex, was found to occur in N. lima collected from August 1987 to May 1988 along a TBT pollution gradient associated with a marina in Auke Bay, Alaska. The suite of symptoms characteristic of imposex in N. lima was slightly different than in N. lapillus. Imposex, as measured by relative penis size (RPS) of females to males, increased from 0.0 to 34.27 along this gradient and as measured by vas deferens sequenceindex (VDS) increased similarly from 0.0 to 4.29. Concentrations of TBT in N. lima increased from below detection limits (about 0.010 g Sn g^-1 dry tissue wt) to 0.065 g Sn g^-1 dry tissue wt along the gradient. The gradient was determined by measuring TBT in whole-body tissues of bay mussels (Mytilus edulis). Concentrations of TBT in mussels increased from below detection limits to 0.833 g Sn g^-1 dry tissue wt in mussels from within the marina that was the major local source of TBT. Imposex, tissue TBT burden, and position along a TBT pollution gradient are significantly correlated (P<0.01) in N. lima. TBT was tested as a causative agent for imposex by exposing snails at a distant control site to TBT paint. After 1 mo exposure, 33% of the females grew a penis ranging in size from 0.2 to 0.8 mm. Our results generally corroborate those found for N. lapillus and indicate that imposex in N. lima is caused by environmental TBT exposure. We suggest that the RPS in the genus Nucella may be useful in monitoring TBT in coastal waters worldwide.     

Oil pollution monitoring in the Lagoon of Venice using the mussel Mytilus galloprovincialis

Gas chromatographic analyses of mussels, Mytilus galloprovincialis, from different areas of the Lagoon of Venice show that these organisms contain a very complex mixture of hydrocarbons attributable to fuel oil contamination. The measured amounts normally range from 0.8 to 8.7 mg/100 g wet weight, but values as high as 22.0 mg/100 g have been recorded. This high value indicates a saturation limit for these organisms which is considerably higher than those values normally found in mussels from the lagoon. The aliphatic hydrocarbon levels in mussels are related to distance from pollution sources and to the degree of exchange between the sea and the area sampled. On the basis of this relationship between overall hydrocarbon pollution load and level of contamination of M. galloprovincialis, it appears that this bivalve might be effectively utilized as a self-integrating monitoring index of oil pollution in the wasters of the lagoon.     

A multi-scale approach to modelling spatial and dynamic ecological patterns for reservoir's water quality management

With growing levels of urbanization and agriculture throughout the world, it is increasingly important that both research and management efforts take into account the effects of this widespread landscape alteration and its consequences for natural systems. Freshwater ecosystems, namely reservoirs, are particularly sensitive to land use changes. In this context, modelling can be very useful, for decision support, as an investigative tool to forecast the outcome of various scenarios, to guide current management in order to meet future targets and to develop integrated frameworks for management accordingly to the Water Framework Directive (WFD). The present paper examined the applicability of a holistic Stochastic-Dynamic Methodology (StDM), coupled with a Cellular Automata (CA) model, in capturing how expected changes at land use level will alter the ecological status of lentic ecosystems, namely at physicochemical and biological levels. The methodology was applied to Portuguese reservoirs located in the Douro's basin and illustrated with a series of stochastic-dynamic and spatial outputs taking into account expected scenarios regarding land use changes. Overall, the simulation results are encouraging since they seem to demonstrate the tool reliability in capturing the stochastic environmental dynamics of the selected metrics facing spatial explicit scenarios. The ultimate goal was to couple monitoring assessment and the described modelling techniques to ease management and decision making regarding the practical implementation of the WFD, both at the scale of the reservoir body and at the scale of the respective river watershed dynamics.     

Hydrocarbon uptake and loss by the mussel Mytilus edulis

The dynamics of accumulation and elimination of hydrocarbons by the blue mussel Mytilus edulis were studied in a continuous-flow system. Mussels were exposed for as long as 41 days to 200 – 400 g/l of diesel fuel adsorbed on kaolin particles. Hydrocarbons were accumulated in the tissues in excess of 1000 times the exposure levels. Upon termination of dosing, the mussels exhibited a rather rapid loss of hydrocarbons for the first 15 to 20 days (biological half-life=2.7 to 3.5 days). Subsequently, however, elimination was reduced to a minimum and a considerable fraction of the hydrocarbons could be recovered from the tissues after as long as 32 days of depuration. The mussels exhibited definite signs of physiological stress due to chronic exposure to diesel fuel, although recovery was rapid upon termination of dosing. It is concluded that mussels could be utilized as a test organism for monitoring long-term hydrocarbon pollution in marine waters. The implications for the mussel culture industry are discussed.     

Metallothioneins and lysosomes in metal toxicity and accumulation in marine mussels: the effect of cadmium in the presence and absence of phenanthrene

It has been confirmed that metallothioneins play an important role in the accumulation of cadmium (Cd) in the digestive gland cells of mussels (Mytilus galloprovincialis Lam.). The content of Cd in the tissue of mussels exposed for 9 d to the metal (estimated dosage of 180 g Cd mussel^-1 d^-1) was 66.2 ppm. This value is about the same as the metal content found in the digestive gland of Cd-exposed mussels kept in clean water for a recovery period of 28 d. At the end of the recovery period, however, the Cd bound to thionein had increased by approximately 250%. Our data demonstrate that the stability of lysosomes, a biological parameter adopted as a cellular stress index, is extremely low in mussels exposed to Cd for 9 d, but returns to control values in the digestive gland cells of mussels allowed to recover for 28 d in uncontaminated sea water. At this point most of the Cd present in the cytosol is bound to thionein. These data demonstrate the importance of metallothionein induction in the reduction of the cytotoxic effects exerted by high levels of Cd accumulation. The results of tests designed to clarify the reasons for the long biological half-life of Cd demonstrated that, in the digestive gland of mussels, the lysosomes are not able to eliminate Cd either bound to insoluble thionein polymers or to lipid peroxidation products such as lysosomal lipofuscin, both of which are apparently involved in the elimination of copper. The absence of these two mechanisms of metal sequestration and elimination via excretion of residual bodies (tertiary lysosomes) is in agreement with the persistence of cadmium in the digestive gland of mussels. Finally, the results also demonstrate that simultaneous exposure of mussels to Cd and phenanthrene, an established lysosomal membrane destabilizer, did not significantly alter the accumulation of Cd or the kinetics of the metal in mussels.     

Sedimentary records of anthropogenic contribution to heavy metal content in Oum Er Bia estuary (Morocco)

Levels of heavy metals (Cd, Hg, Cr, Cu, Fe, Mn, Ni, Pb and Zn), organic carbon content and textural characteristics in the superficial and cored sediments of Oum Er Bia estuary have been studied. The anthropogenic fluxes of heavy metals were determined in two sediment cores collected in the estuary, facing urban sewages. A dated estuarine core from the inter-tidal area was assessed using ²¹⁰Pb and ¹³⁷Cs data. These data indicate that the mean sedimentation rates are 0.38–68 cm year^?1. The analytical results and the radio-dating of sediment cores show extremely high concentrations of Zn, Pb and Cu in the sediments that can be ascribed mostly to the discharge of the liquid effluent from the sewage since the late 1960s, decreasing towards the present day. The pollution intensity of the estuary is determined by the enrichment factors, which show that the Oum Er Bia estuary is moderately polluted to polluted.     

Toxic substances: Measures and measurements†

The formulation of a sound policy for environmental protection and toxic substances control requires knowledge of the presence and concentration of environmental contaminants. For this reason monitoring programs have been set up in the Netherlands for water, drinking water, and air pollution. The Netherlands system for air pollution, monitoring of the substances SO2, NOχ, CO, O₃ is now fully automated. Some examples will be given to show the acquisition and management and interpretation of air pollution measurements.

Various smaller projects, supported by the Department of Health and Environmental Protection include measurement of indoor air‐contaminants, contaminants in soil and hazardous waste sites, and contaminants in biotic samples such as for instance PCB's in eels and seals and mussels. Moreover a Coordinating Committee regularly collects measurements from various sources in the Netherlands regarding pesticide residues and contaminants in food.

For cost‐effective monitoring the accuracy of the measurements must be chosen with regard to the biological effect concentration of the pollutant. The necessity of proper control measurements to establish background levels and the necessity of ring‐tests to increase interlaboratory reproducibility is discussed. In cost‐effective monitoring the minimum number of measurements, which are necessary to check the effect of environmental protection measures, must be defined through proper sampling.     

Effects of salinity stress on neurotransmission, energy metabolism, and anti-oxidant biomarkers of Carcinus maenas from two estuaries of the NW Iberian Peninsula

This study investigated the effects of salinity on biomarkers of oxidative stress, energy metabolism, and neurotransmission of Carcinus maenas from an estuary low impacted by pollution and from an estuary under chemical stress in the NW Iberian Peninsula. Crabs were collected in the field and, following an acclimation period, they were exposed for 7 days to five salinity levels ranging from 4 to 45 psu. At the end of the exposure period, stress biomarkers were determined in samples of muscle and digestive gland. The biomarkers assessed in the muscle were the activities of the enzymes cholinesterases (ChE), of which acetylcholinesterase is involved in neurotransmission, and lactate dehydrogenase (LDH) and isocitrate dehydrogenase (IDH) that are involved in energy metabolism. The biomarkers assessed in the digestive gland were (1) the activities of the enzymes glutathione S-transferases (GST), glutathione reductase (GR), and glutathione peroxidase (GPx), involved in phase II biotransformation and the anti-oxidant defence system; (2) the levels of total glutathiones (TG), also belonging to the anti-oxidant system; and (3) the levels of lipid peroxidation as a measure of oxidative damage. The results showed a significant influence of salinity on neurotransmission, energy metabolism, anti-oxidant status, and oxidative damage of C. maenas. For some biomarkers, this influence was dependent on whether the crabs were collected at the low-polluted estuary or at the contaminated estuary. In particular, crabs collected at the low-polluted estuary showed altered neurotransmission and anti-oxidant defences (GR). Crabs collected at the impacted estuary showed alterations in neurotransmission, energy metabolism (IDH and LDH), biotransformation, and anti-oxidant defences (GST, GR, GPx, and TG), as well as in oxidative damage, indicating that salinity change superimposes higher stress on these organisms. For ChE, IDH, and TG, altered responses were induced by both hypo- and hypersalinity.     

Biotic indexes reveal the impact of harbour enlargement on benthic fauna

Environmental effects of enlargement works in Puerto Calero (Lanzarote, Canary Islands) were analysed in the sediments using abiotic variables (total hydrocarbons, polyaromatic hydrocarbons, organic matter and granulometry) and three biotic indexes (AMBI, M-AMBI and BENTIX). A before–after/control–impact (BACI) design was developed with four sampling campaigns, before (November 2004), during (March and July 2005) and after (July 2006) works. Inner stations were characterised by high concentrations of pollutants (total hydrocarbons and polyaromatic hydrocarbons). A temporal trend (2004–2006) was observed in macrofaunal assemblage structure, and thus in AMBI, M-AMBI and BENTIX indexes. Macrobenthic assemblages also mirrored the pollution gradient, with bioindicator species in inner stations (the polychaete Pseudopolydora paucibranchiata and the mollusc Abra alba), sensitive species (the sipunculid Aspidosiphon muelleri, the crustacean Pariambus typicus and the polychaete Aponuphis bilineata) in outer stations and ubiquitous species (the polychaetes Aricidea assimilis and Armandia polyophthalma) in both stations (inner and outer).     

Assessing water quality in the Ceyhan River basin (Turkey) with the use of aquatic macrophytes

As a major biotic component of many lotic ecosystems, macrophytes consist a major component of running waters are often used as indicators within the European Water Framework Directive (WFD) to establish ecological quality. In this study, we investigated macrophyte community structure (e.g. composition, abundance and diversity) in Ceyhan River Basin located in the Southeastern Anatolian Region in Turkey. Data was collected during 2014–2015 from river sites located throughout the basin to evaluate the relationship between aquatic vegetation and river physico-chemical factors. The ecological status of the river basin was also calculated based on Macrophyte Biological Index for River (IBMR). In total, 33 macrophyta taxa were observed. According to their biological classification (life form), filamentous algae (FA), free floating (FF), floating leaved (FL) and submersed (S) macrophytes reached their maximum abundance value in summer, while emergent (E) macrophytes were at their maximum abundance in both summer and autumn. The ecological status of the Ceyhan River basin ranged from moderate to bad. The values found are reasonably comparable to IBMR scores recorded in rivers of other Mediterranean countries. IBMR index may be suitable to some extent to establish a basis for ecological quality assessment in Turkish River systems.     

Investigation of metallothionein level,reduced GSH level,MDA level,and metal content in two different tissues of freshwater mussels from Atatürk Dam Lake coast,Turkey

Atatürk Dam Lake is one of the important freshwater ecosystems in the world in terms of the size of the surface area and the biodiversity. The objective of this study was to determine the effects of metal pollution in the Atatürk Dam Lake on some biochemical markers in the gills and digestive glands of mussels (Unio mancus). Mussel samples were collected in July-2018 from four stations. The metal residues (Cd, Cu, Pb, Zn, and Ni) in the tissues were determined by ICP-MS. The MT, reduced GSH, and MDA levels were analysed using the proposed spectrophotometric methods. According to the results, toxic metals such as Cd and Pb in both tissues were determined mostly in mussels collected from St1. The highest MT and MDA levels in the gills were determined in St3 and St2 respectively, while the highest MT and MDA levels in the digestive glands were determined in St1. Although there was no significant difference in the reduced GSH level in the gills among the stations, the highest reduced GSH level in the digestive glands was determined in St4. These results indicated that mussels are appropriate sentinel organisms for metal contamination with effects on oxidative stress and metal exposure biomarkers.     

Combining heat-transfer and energy budget models to predict thermal stress in Mediterranean intertidal mussels

Recent studies have emphasised that organisms can experience physiological stress well within their geographic range limits. Developing methods for mechanistically predicting the presence, absence and physiological performance of organisms is therefore important because of the ongoing effects of climate change. In this study, we merged a biophysical–ecological (BE) model that estimates the aquatic (high tide) and aerial (low tide) body temperatures of Mytilus galloprovincialis with a Dynamic Energy Budget (DEB) model to predict growth, reproduction and mortality of this Mediterranean mussel in both intertidal and subtidal environments. Using weather and chlorophyll-a data from three Mediterranean sites along the Italian coasts, we show that predictions of sublethal and lethal (acute) stress can potentially explain the observed distribution (both presence and absence) of mussels in the intertidal and subtidal zones, and the maximum size of animals in the subtidal zones. Importantly, our results suggest that different mechanisms limit the intertidal distribution of mussels, and that these mechanisms do not follow a simple latitudinal gradient. At the northernmost site (Palermo), M. galloprovincialis appears to be excluded from the intertidal zone due to persistent exposure to lethal aerial temperatures, whereas at the southernmost sites (Porto Empedocle and Lampedusa) sublethal stress is the most important driver of mussel intertidal distribution. Our predictions provide a set of hypotheses for future work on the role of climate change in limiting intertidal distribution of mussels in the Mediterranean.     

Microprofiles of oxygen in epiphyte communities on submerged macrophytes

Mussels (Mytilus edulis) transferred in net bags from clean to chronically mercury polluted water readily accumulated mercury during an exposure period of three months. Growth of the transplanted mussels had a diluting effect on the mercury concentration, but the absolute weight of mercury uptake increased throughout the entire period, though there was a tendency for decreased efficiency of the removal of mercury per liter of water filtered by the mussels. Mussels were also translocated from polluted to clean (laboratory) water to depurate mercury. The biological half-lives of mercury was 293 d for M. edulis from the chronically polluted area in contrast to only 53 d for mussels from a temporary massive mercury polluted area near a chemical deposit. In both cases about 75% of the total mercury in the mussels was inorganic, and it is suggested that both inorganic and organic mercury species were immobilized in mussels from the long-term mercury polluted area, whereas the immobilization capacity was exceeded in the short-term mercury exposed mussels near the chemical deposit. Very slow elimination of mercury was observed in the deposit-feeding bivalve Macoma balthica from the chronically polluted area, and about 6% of the total mercury was methyl-+phenyl-mercury. This is more than three times lower than found in M. edulis from the same collecting site. A pronounced difference in the mercury speciation (i.e., total mercury, total organic mercury, methyl-mercury and phenyl-mercury) in M. edulis from the two mercury polluted areas is thought to reflect the different character of the mercury pollution in the two areas.     

Effects of chemical contaminants on the health of Mytilus edulis from Puget Sound,Washington. II. Cytochemical detection of subcellular changes in digestive cells

Activities of the enzymes NADPH-dependent ferrihemoprotein reductase (NFR), NADH-dependent DT-diaphorase (DTD), gamma-glutamyl transpeptidase (GGT), and catalase (CAT) and peroxisome proliferation (PP) in the digestive cells of Mytilus edulis from nine sites in Puget Sound, Washington (USA) sampled in September 1992 were measured cytochemically using image analysis. Mussels from these areas are known to be exposed to a wide range of chemical contaminants. At urban-associated sites, mussels generally showed increased activities of NFR, DTD, and CAT, suppressed GGT activity, and peroxisome proliferation, relative to mussels from the non-urban reference sites. Significant positive relationships were observed between tissue concentrations of polyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs) and DDTs and activities of NFR, DTD, CAT, and peroxisome proliferation. Structural changes in the digestive gland of mussels also appear to be more responsive to chemical contaminant exposure than changes in enzyme activity. These relationships suggest that NFR, CAT, and the induction of peroxisome proliferation represent complimentary indicators of biological effects from chemical-contaminant exposure in the marine bivalve M. edulis. The current findings support the use of selected cytochemically measured subcellular responses as biomarkers of contaminant exposure in environmental monitoring programs.     

Classification and ordination of benthic samples from Bedeque Bay,an estuary in Prince Edward Island,Canada

An attempt was made to identify the causes of the distribution of benthos within Bedeque Bay using multivariate techniques programmed for the computer. Both classification by a hierarchical cluster analysis, and ordination by principal components analysis suggested that a large proportion of the variance in the data was directly or indirectly correlated with a salinity gradient. Classification divided the species into two main groups, a in the upper half of the estuary where lower salinities and larger salinity fluctuations occurred, and group b in the lower half of the estuary with a more stable salinity regime. The group b species were further subdivided into those preferring soft mud and those preferring sandier sediments. The group a species were divided into a well-developed oyster association and various sub-groups less strongly associated with oysters. Five principal components were required to account for 50% of the variance in the data. The first axis accounted for 20% of the variance and was shown by a non-parametric test to be correlated with the salinity gradient. Axes II to V could not be interpreted, but possibly represented complex species interactions. By providing hard substrates and altering the natura of the sediment, oysters and mussels produced conditions suitable for many other species.     

流域水体污染的生态学效应及监测预警

从流域生态系统的结构与功能出发,分述流域水体污染引起的生态学效应(结构与功能效应),并归纳目前国内外生物、生态监测预警的特点.生态监测经历了以敏感和耐污种类比例为主的传统简单指数、以群落结构变化为主的单一指数到以群落结构、营养结构为主要特征的复合多参数指数的发展过程.生物预警利用在线生物监测技术,主要形成了鱼类、无脊椎动物和微生物的三大类生物预警系统.目前,生物完整性指数能从群落水平较好地指示水体污染状况,生态预警则缺乏生态系统水平的研究.因此提出以群落结构为主的生态监测以及生态系统整体水平上的生态预警是未来研究方向的重点.     

Local extinction of a foundation species in a hypoxic estuary: integrating individuals to ecosystem

We integrated across individual, population, community, and ecosystem levels to understand the impact of environmental stress by tracking the foundation species Mytilus edulis in the hypoxic estuary Narragansett Bay, Rhode Island, USA. Our initial surveys revealed that the mussels occurred in nine extensive (2-28 ha) dense (814-9943 individuals/m2) subtidal reefs that attracted a diverse suite of predators (sea stars, crabs, gastropods). Hypoxia occurred in the summer of 2001, and a mussel transplant experiment revealed overall reduced growth rates of individuals, and higher mortality rates among larger mussels. At the population level, large decreases in densities and cover of mussels were correlated with dissolved oxygen concentrations, leading to extinction at one site and reductions of over an order of magnitude at others. Within one year, seven of the eight remaining populations were edged to extinction, and the previously extinct population was recolonized. At the community level, a predator exclusion experiment indicated that predation was an unimportant source of mussel mortality during the hypoxic period, in part due to the emigration of sea stars, as predicted by the Consumer Stress Model. However, mussels were too intolerant to hypoxia to have a net benefit from the predation refuge. The seasonal (summer) occurrence of hypoxia allowed sea stars to return following a lag, as predicted by a stress return time model, and the resumption of predation contributed to the subsequent extinction of mussel populations. At the ecosystem level, the initial filtration rate of the mussel reefs was estimated at 134.6 x 10(6) m3/d, equivalent to filtering the volume of the bay 1.3 times during the 26-d average residence time. That function was reduced by >75% following hypoxia. The effect of hypoxia on each level of organization had consequences at others. For example, size-specific mortality and decreased growth of individuals, and reduced filtration capacity of reefs, indicated a loss of the ability of mussels to entrain planktonic productivity and potential to control future eutrophication and hypoxia. Our study quantified patterns of loss and identified pathways within an integrative framework of feedbacks, summarized in a conceptual model that is applicable to similar foundation species subjected to environmental stress.