Cockle Cerastoderma Edule Research Articles

The prevalence of parasitic pea crab Afropinnotheres monodi in mussels depending on the degree of exposure of habitats: implications for mussel culture

XX Iberian Symposium on Marine Biology Studies (SIEBM XX) , Braga, Portugal, 9 Sep - 12 Sep, 2019.

Socioecological changes in data-poor S-fisheries: A hidden shellfisheries crisis in Galicia (NW Spain)

We combined different data sources to analyse key changes in the shellfisheries of Galicia (NW Spain). The shellfishing capacity of this region, a major fishing power in Europe, has been severely reduced in recent decades. The number of vessels has fallen by 13%, vessel length, capacity and engine power have decreased by 10%, 7% and 3%, respectively, while the number of on-foot shellfishers has halved. Landings and sale value of shellfish species have declined in the last decade by 16% and by 13%, respectively. This decline follows a period of recovery from the mid-1980s, when coastal fishery management were transferred from the Spanish to the regional government. Production of local clam species has been progressively abandoned in favour of the foreign Japanese carpet shell Ruditapes philippinarum, leading to losses in sales value and increasing market risks. Overfishing, poaching, degradation of habitats, pollution, disease outbreaks and ocean warming may be responsible for the drop in landings and sales value of key species like edible cockle Cerastoderma edule and Atlantic goose barnacle Pollicipes pollicipes. Despite the development of new fisheries, e.g. algae, anemone and polychaete harvesting, the overall declining trend has important socioecological implications for Galician society, because of the traditional link between shellfishing and coastal communities. The socioecological sustainability of this sector requires policies to be developed by the regional government regarding the support of multidisciplinary research and surveillance, increase control over pollution and poaching, a greater focus on the production of native species and the strengthening of co-management frameworks.

The prevalence and effects of the African pea crab Afropinnotheres monodi on the condition of the mussel Mytilus galloprovincialis and the cockle Cerastoderma edule

Some pea crabs are parasite of bivalves and may cause a significant effect on the host's condition. In this study, the prevalence of the pea crab Afropinnotheres monodi and its effect on host condition are assessed for two commercially important bivalves (the mussel Mytilus galloprovincialis and the cockle Cerastoderma edule) from three natural beds of the Gulf of Cadiz (SW of Iberian Peninsula). The average prevalence of A. monodi ranged from 4.0% (Bay of Cadiz) to 51.4% (Carreras River) for cockles and from 30.5% (Bay of Cadiz) to 45.4% (Carreras River) for mussels. For both hosts, most bivalves were infested by a single pea crab (96.0% of cockles and 92.4% of mussels); among multiple infestations, one male and one female was the dominant combination (72.7% of cockles and 77.8% of mussels). Infested mussels showed a significantly decreased condition index (14.7%, on average), whereas crab infestation did not significantly affect the condition index of cockles (2.2%, on average). When the wet weight of the pea crab represented >5% of the wet weight of the host, an average condition loss of 12.7% and 15.9% were observed for cockles and mussels, respectively. As the relative condition loss of both mussels and cockles was negatively correlated with the relative size of the pea crab, the mentioned interspecific differences in the pea crab effects may be mainly due to the higher prevalence of soft females (larger size and obligatory parasitism) in mussels (70.6%, on average) and of hard females and males (smaller size and facultative parasitism) in cockles (81.1%, on average). This study highlights the importance of knowing the life cycle and host use of the pea crab A. monodi to ascertain the possible negative effect of this parasite on mussel farms and exploited cockle beds.

Facilitation by ecosystem engineers enhances nutrient effects in an intertidal system

AbstractEcosystem engineering research has recently demonstrated the fundamental importance of non‐trophic interactions for food‐web structure. Particularly, by creating benign conditions in stressful environments, ecosystem engineers create hot beds of elevated levels of recruitment, growth, and survival of associated organisms; this should fuel food webs and promote production on the ecosystem scale. However, there is still limited empirical evidence of the influence of non‐trophic interactions on the classical food‐web processes that determine energy transfer, that is, consumer–resource interactions. On the basis of a biomanipulation experiment covering 600 m2 of an intertidal flat, we show that ecosystem engineers influence resource uptake efficiency and the accumulation of algae following nutrient enrichment in a soft‐sediment food web. Nutrient additions increased chlorophyll a concentrations in the sediment by 90%, but only in plots where we also introduced high densities (2000 per m2) of a burrowing bivalve, the common cockle Cerastoderma edule. The artificial cockle beds increased the nutrient uptake efficiency of the biofilm and promoted sediment accumulation, which suggests that the cockles facilitated the sediment‐living algae by increasing sediment stability. This indicates that ecological interactions, rather than the availability of nutrients per se, set the limits for production in this coastal ecosystem. Our results emphasize the need to include facilitation theory and recognize that positive interactions between species are key to understand, manage, and restore ecosystems under human influence.

Effects of bioturbation on the erodibility of cohesive versus non-cohesive sediments along a current-velocity gradient: A case study on cockles

Soft-bottom bioturbators are ecosystem engineers in the sense that they can have considerable effects on sediment erodibility and resuspension. The common cockle Cerastoderma edule is a bioturbating filter feeder that is widespread along the European Atlantic coastline. Its presence and activity can decrease sediment erosion thresholds in cohesive sediments but little is known about its effect on non-cohesive sediments. Using controlled annular flume experiments, we investigated the relative effects of different cockle densities on sediment resuspension in cohesive vs. non-cohesive sediments by assessing the following: (i) the mud and sand burrowing behavior of cockles, (ii) critical erosion thresholds, (iii) the mass of eroded sediment and (iv) erosion rates. Our results show that cockles were more active in non-cohesive sediment compared with cohesive sediment. Despite their lower activity, the presence of cockles in cohesive sediment increased sediment erodibility by reducing the critical erosion threshold (Ucrit) and increasing both the mass of eroded sediment and erosion rate. In contrast, cockles had no effect on erodibility in non-cohesive sediment, especially on the eroded sediment mass and erosion rate. The mass eroded was not significantly different between cohesive and non-cohesive sediments when cockles were present. Our experiments show that the increased erodibility of cohesive sediment due to the bioturbation by cockles is density dependent: higher cockle density results in stronger effects on erodibility. Moreover, this increase in cohesive sediment erosion due to cockle bioturbation was positively correlated with current velocity. In contrast, the erosion of non-cohesive sediment only depended on the current stress and was unaffected by cockle density. Considering the high abundance of C. edule, its widespread distribution and its extensive activities, the results of this study could be widely applicable to intertidal mud flats around the world.

A Minchinia mercenariae-like parasite infects cockles Cerastoderma edule in Galicia (NW Spain).

The cockle Cerastoderma edule fishery has traditionally been the most important shellfish species in terms of biomass in Galicia (NW Spain). In the course of a survey of the histopathological conditions affecting this species in the Ria of Arousa, a haplosporidan parasite that had not been observed in Galicia was detected in one of the most productive cockle beds of Galicia. Uni- and binucleate cells and multinucleate plasmodia were observed in the connective tissue mainly in the digestive area, gills and gonad. The parasite showed low prevalence, and it was not associated with abnormal cockle mortality. Molecular identification showed that this parasite was closely related to the haplosporidan Minchinia mercenariae that had been reported infecting hard clams Mercenaria mercenaria from the Atlantic coast of the United States. The molecular characterization of its SSU rDNA region allowed obtaining a fragment of 1,796bp showing 98% homology with M.mercenariae parasite. Phylogenetic analysis supported this identification as this parasite was clustered in the same clade as M.mercenariae from the United States and other M.mercenariae-like sequences from the UK, with bootstrap value of 99%. The occurrence of M.mercenariae-like parasites infecting molluscs outside the United States is confirmed.

Physiological responses to ocean acidification and warming synergistically reduce condition of the common cockle Cerastoderma edule

The combined effect of ocean acidification and warming on the common cockle Cerastoderma edule was investigated in a fully crossed laboratory experiment. Survival of the examined adult organisms remained high and was not affected by elevated temperature (+3 °C) or lowered pH (−0.3 units). However, the morphometric condition index of the cockles incubated under high pCO2 conditions (i.e. combined warming and acidification) was significantly reduced after six weeks of incubation. Respiration rates increased significantly under low pH, with highest rates measured under combined warm and low pH conditions. Calcification decreased significantly under low pH while clearance rates increased significantly under warm conditions and were generally lower in low pH treatments. The observed physiological responses suggest that the reduced food intake under hypercapnia is insufficient to support the higher energy requirements to compensate for the higher costs for basal maintenance and growth in future high pCO2 waters.

Spatio-temporal variability in the fatty acid profile of the adductor muscle of the common cockle Cerastoderma edule and its relevance for tracing geographic origin

The present study aimed to identify the potential existence of spatio-temporal variability in the fatty acid (FA) profile of the adductor muscle (AM) of a commercially important bivalve, the common cockle Cerastoderma edule, and determine if such variability can be used to trace their geographic origin post-harvesting. Common cockles were sampled in eight ecosystems along the coast of mainland Portugal, as well as in two different channels within one of those ecosystems over two consecutive years. Results showed significant differences in FA profiles among ecosystems, namely due to different levels of eicosapentaenoic acid (EPA; 20:5n-3), arachidonic acid (20:4n-6), ratio of polyunsaturated FA (PUFA) n-3/n-6, monounsaturated FA (MUFA; 18:1n-9 and 20:1n-9/11) and bacterial FA (15:0, 17:0 and 18:1n-7). FA profiles also displayed significant differences between two consecutive years in channels from the same ecosystem. Overall, while the FA profile displayed by the AM of C. edule can be successfully used to trace their geographic origin, the existence of temporal variability requires a periodical verification of FA signatures to identify potential shifts, namely when comparing specimens from the same ecosystem.

Influence of intertidal recreational fisheries and ‘bouchot’ mussel culture on bivalve recruitment

In coastal environments, fishing and aquaculture may be important sources of disturbance to ecosystem functioning, the quantification of which must be assessed to make them more sustainable. In the Chausey Archipelago, France, recreational fishing and commercial shellfish farming are the only two evident anthropogenic activities, dominated by bivalve hand-raking and ‘bouchot’ mussel culture, respectively. This study evaluates the impact of both activities on bivalve recruitment dynamics by comparing primary recruitment intensity (short-term effect) and recruitment efficiency (medium-term effect) by sampling bivalves in reference (undisturbed) and disturbed (i.e. subjected to hand-raking or in ‘bouchot’ mussel culture areas) parcels throughout and at the end of the recruitment season, respectively. Specific hypotheses evaluated were that (H1) bivalve hand-raking negatively affects bivalve recruitment and that (H2) ‘bouchot’ mussel culture promotes bivalve recruitment.Patterns in bivalve community structure in reference parcels (i.e. natural pattern) differed between initial and final recruitment, underlining the great importance of early post-settlement processes, particularly secondary dispersal. Primary recruitment intensity was inhibited in hand-raking parcels whereas it was promoted in ‘bouchot’ mussel culture parcels, but the effect on recruitment efficiency was muted for both activities due to post-settlement processes. Nevertheless, the importance of effects that occur during the first step of recruitment should not be ignored as they may affect bivalve communities and induce immediate consequences on the trophic web through a cascade effect. Finally, it is highlighted that hand-raking damages all life stages of the common cockle Cerastoderma edule, one of the major target species, suggesting that this activity should be managed with greater caution than is currently done.

Changes of paralytic shellfish toxins in gills and digestive glands of the cockle Cerastoderma edule under post-bloom natural conditions

Concentrations of the paralytic shellfish toxins C1+2, C3+4, GTX5, GTX6, dcGTX2+3, dcSTX, dcNEO, GTX2+3, GTX1+4, STX and NEO were determined by LC-FLD in composite samples of digestive glands and gills of Cerastoderma edule cockle. The specimens were sampled in Aveiro lagoon, Portugal, under natural depuration conditions (days 0, 8, 12, 14, 19, 21 and 25) after exposure to a bloom of Gymnodinium catenatum. Individual paralytic shellfish toxins indicated different pathways of elimination and biotransformation in digestive gland and gills. Toxin concentrations in gills were lower than in digestive gland. Most of the quantified toxins in digestive gland decreased during the 25 days of observation according to negative exponential curves, and only GTX5, GTX6 and NEO showed slight irregularities with time. Concentrations of C1+2, C3+4 and dcGTX2+3 in gills decreased progressively, however GTX5, GTX6 and dcSTX showed pronounced increases. Higher concentrations of those toxins in days 8 and 12 in comparison to the initial value (day 0) indicate conversion of other toxins into GTX5, GTX6 and dcSTX during those periods. It appears that inter-conversion of toxins occurs as G. catenatum cells are retained in gills before being transferred to other compartments.

Mollusc disease situation in Europe : what’s new since 2008 ?

Mollusc disease situation in Europe : what’s new since 2008 ?

Growth, mortality and deformities evolution of the common cockle (Cerastoderma edule L.): suspended culture vs. natural sandflat culture

Growth, mortality and deformities evolution of the common cockle (Cerastoderma edule L.): suspended culture vs. natural sandflat culture

Density dependence of growth and production in a Wadden Sea population of the cockle Cerastoderma edule

In suspension-feeding bivalves, growth rates generally remain at a high level over abroad range of numerical densities. However, data series on growth and production that cover awide density range in a natural marine benthic system appear to be scarce. A long-term monitoringstudy (1973-2013) of zoobenthos on tidal flats in the western Wadden Sea yielded twiceannualdata on numbers and weights of (among others) cockles Cerastoderma edule, allowingestimates of their annual and cohort production by the weight-increment summation method. Innearly all years, cockle densities did not exceed a few 100s m-2, and their individual weight incrementsshowed no significant relationship with density. Only the appearance of one exceptionallystrong year class in 2011 caused higher densities over an extensive area for >1 yr. Growth rates inall cockles were significantly reduced in the second growing season of this strong cohort, whentheir densities amounted to >500 m-2. Seasonal and annual survival did not show a significantrelationship with density. As a consequence of the reduction in growth of its members, productionof the single strong cohort was substantially less than expected on the basis of its initial abundance.In all smaller cohorts, the positive relationship between recruit numbers and cohort productionwas close to linear. However, when the higher density of the one strong year class wasincluded, an inverse-U shaped line would better characterize this relationship. Appearances ofvery strong bivalve cohorts are rare events in the Wadden Sea: bivalve stocks on the tidal flatsusually appear to be far below the carrying capacity of the area for suspension-feeding animals.

Modelling the effect of Cerastoderma edule bioturbation on microphytobenthos resuspension towards the planktonic food web of estuarine ecosystem

Microphytobenthos (MPB) represents an important food source for primary consumers in estuarine ecosystems and the availability of MPB as food items results from complex physical, chemical, and biological interactions. In Baie des Veys (Lower Normandy, France), the common cockle Cerastoderma edule constitutes the major bioturbator in the ecosystem in terms of biomass. In this ecosystem, cockle bioturbation is a key process regulating the MPB erosion flux in the water column. This bivalve intensely modifies the top layer of the sediment by increasing the sediment erodibility and the fluxes of suspended chlorophyll a through the valve movements. More precisely, cockle bioturbation destabilizes the sediment surface by creating a biogenic layer that is easily eroded with tidal hydrodynamic forces. Associated MPB can then be exported to the water column to fuel higher trophic levels of the planktonic food web. The aim of this study was to develop a numerical model that reproduces the export of MPB associated to the biogenic layer erosion. Kinetics of suspended MPB, in response to increasing stress, were obtained from flume experiments in lab controlled conditions and in situ natural conditions. Following this, the suspended MPB were analyzed to respectively parameterize the model by (1) a calibration approach, and (2) an independent validation. The analysis has highlighted that the higher the biomass of cockles, the higher the MPB resuspension rates. Our model consistently reproduces the tendency encountered in laboratory analysis and with in situ natural conditions. During the validation, a small site-specific lack of adjustment was identified, but, among the macrozoobenthic community, the model can be significantly improved by considering the bioturbation activities of another ecosystem engineer, Pygospio elegans. This study thus provides reliable estimates of the daily food availability from benthic primary consumers in an estuarine system where cockles dominate the bioturbating assemblage. This model can be inserted in various model designs (0D, 1D-vertical or 3D).

Patterns of genetic variation across the distribution range of the cockle Cerastoderma edule inferred from microsatellites and mitochondrial DNA

The edible cockle Cerastoderma edule is an ecologically and economically important species found along the northeastern Atlantic coast. In this study, microsatellite and mitochondrial cytochrome b (cyt b) gene variation was examined in 19 localities across the species’ distribution range to test whether the patterns of genetic diversity, population structure and demographic inferences deduced from the cytochrome oxidase I gene in a previous study were supported by these molecular makers. High levels of genetic diversity were detected, with allelic richness, heterozygosity and haplotype diversity, showing different geographic patterns. Through Bayesian clustering analysis, Fst estimates and AMOVA, microsatellites indicated the existence of a southern group of populations that expands up to France, a northern one composed of localities from Denmark to Russia plus one from Scotland, and a third central group comprising localities from Ireland, Great Britain and southern North Sea. Regarding the cyt b gene, Fst data supported the pattern inferred from microsatellites, but haplotype distribution and AMOVA revealed a different three-group scenario where the central group includes only the southern North Sea localities. Both marine currents and historical processes, such as a recent population expansion of the southern group, the existence of northern cryptic refugia during Pleistocene glaciations and secondary contact between the southern and northern groups of populations, may explain the genetic composition of C. edule populations. Overall, the available data suggest that in C. edule nuclear markers and even different mitochondrial genes reacted differently to the same population history.

Changes in small scale spatial structure of cockle Cerastoderma edule (L.) post-larvae

Understanding the spatial structure of populations at different scales can help reveal the processes controlling abundance and distribution. For species with a pelagic larval stage and highly mobile post-larval stage, such as the common cockle Cerastoderma edule, changes in spatial distribution from settlement through to juvenile stages are likely to occur at various spatial scales influencing the population dynamics observed. To record such changes a small-scale high-resolution field survey of C. edule post-larvae over an area of 60×80m of tidal mudflat was conducted using a spatially-explicit staggered-nested design in the Dee estuary, UK. The survey was repeated three times from initial settlement in June 2011 to March 2012. Changes in spatial structure were described using Moran's I correlograms and prediction mapping, with analysis of correlations between cockle cohorts and sediment composition. At the first sampling event in June 2011, when initial settlement was occurring, post-larvae were highly aggregated in patches of 10–14m in size and 16–20m apart. By October 2011 the post-larvae had become more evenly dispersed with some small scale (<4m) random patchiness and a gradient in post-larval density. This spatial structure was maintained into March 2012 but with increased patchiness. At settlement post-larval density showed no correlation with adult abundance or sediment mud content, but by October 2011 and March 2012 there was a strong positive correlation with adult abundance. Such changes in spatial structure, abundance and adult association after settlement show the likely importance of small scale (metres to tens of metres) processes on post-larval survival from predation and adult interactions, thereby potentially shaping adult distributions. Small scale patchiness in post-larvae can be created at settlement; however the distribution and association with adults change over time.

Multi‐scale habitat modification by coexisting ecosystem engineers drives spatial separation of macrobenthic functional groups

By changing habitat conditions, ecosystem engineers increase niche diversity and have profound effects on the distribution and abundances of other organisms. Although many ecosystems contain several engineering species, it is still unclear how the coexistence of multiple engineers affects the physical habitat and the structure of the community on a landscape scale. Here, we investigated through a large‐scale field manipulation how three coexisting engineers on intertidal flats (cockles Cerastoderma edule; lugworms Arenicola marina; blue mussels Mytilus edulis) influence the functional composition of the local macrobenthic community and what the consequences are at the landscape level. By using biological trait analysis (BTA), we show that on the local scale biogenic changes in sediment accumulation and organic matter content translated into specific shifts in the distribution of functional traits within the community. At a landscape scale, the co‐occurrence of multiple ecosystem engineers resulted in the spatial separation of different functional groups, i.e. different functional groups dominated unique complementary habitats. Our results emphasize the role of co‐occurring multiple engineers in shaping natural communities, thus contributing to a better knowledge of community assembly rules. This understanding can profitably be used to improve ecosystem‐based management and conservation actions.

A preliminary threshold model of parasitism in the Cockle Cerastoderma edule using delayed exchange of stability

Thresholds occur, and play an important role, in the dynamics of many biological communities. In this paper, we model a persistence type threshold which has been shown experimentally to exist in hyperparasitised flukes in the cockle, a shellfish. Our model consists of a periodically driven slow-fast host-parasite system of equations for a slow flukes population (host) and a fast Unikaryon hyperparasite population (parasite). The model exhibits two branches of the critical curve crossing in a transcritical bifurcation scenario. We discuss two thresholds due to immediate and delayed exchange of stability effects; and we derive algebraic relationships for parameters of the periodic solution in the limit of the infinite ratio of the time scales. Flukes, which are the host species in our model, parasitise cockles and in turn are hyperparasitised by the microsporidian Unikaryon legeri; the life cycle of flukes includes several life stages and a number of different hosts. That is, the flukes-hyperparasite system in a cockle is, naturally, part of a larger estuarine ecosystem of interacting species involving parasites, shellfish and birds which prey on shellfish. A population dynamics model which accounts for one system of such multi-species interactions and includes the fluke-hyperparasite model in a cockle as a subsystem is presented. We provide evidence that the threshold effect we observed in the flukes-hyperparasite subsystem remains apparent in the multi-species system. Assuming that flukes damage cockles, and taking into account that the hyperparasite is detrimental to flukes, it is natural to suggest that the hyperparasitism may support the abundance of cockles and, thereby, the persistence of the estuarine ecosystem, including shellfish and birds. We confirm the possibility of the existence of this scenario in our model, at least partially, by removing the hyperparasite and demonstrating that this may result in a substantial drop in cockle numbers. The result indicates a possible significant role for the microparasite in this estuarine ecosystem.

BACI monitoring of effects of hydraulic dredging for cockles on intertidal benthic habitats of Dundalk Bay, Ireland

Hydraulic dredging for bivalves, such as cockles (Cerastoderma edule), has the potential to cause significant impacts on marine intertidal benthos. Although this fishing activity is common in northern European Natura 2000 sites such impacts may be incompatible with conservation objectives for designated habitats and species within these sites. In 2009–2010 a spatially nested control-impact study was undertaken before (t0), 8–9 days after (t1) and 4 months (t2) following dredging and extraction of 108 tonnes of cockles from a standing stock of 2158 tonnes in Dundalk Bay. This study failed to detect significant effects on benthic sediments, or the overall community structure. However, a fishing effect on the target species C. edule in one sampling area and a short lived effect on the bivalve Angulus tenuis were identified. Significant spatial and temporal variability in abundance of species and taxonomic groups, unrelated to fishing effects, was observed. Previous studies on the effects of fisheries on marine intertidal benthos have reported variable results, related to study design and objectives and the physical characteristics of the study site. Site specific studies, relative to the intensity and frequency of proposed fishing activity, may be required to adequately inform managers whether such activities are compatible with specific conservation objectives for Natura 2000 sites.

Size, distribution and sediment biodeposition of prolific bivalves in small estuaries

The growth and distribution of bivalves in estuaries is generally driven by access to food, hydrodynamic forces and sedimentary conditions that facilitate recruitment and allow persistent settlement. Factors such as site elevation or sediment properties have a significant impact, but there are few studies quantifying the relative importance of different factors in an entire estuary. We carried out an estuary-wide survey of the cockle Cerastoderma edule L. by sampling 343 sites in a small estuary, the Burry Inlet in South Wales, UK. We determined the extent to which site elevation, as an indicator for the duration of feeding, sediment properties and position inside the estuary, explained variation in the size and density of the bivalve. We also analysed the production of faeces and pseudo-faeces per cockle. The population consisted almost entirely of 1-year old cockles, the average size was 14.7 ± 2.7 mm and the average density was 56 ± 189 cockles 0.1 m−2 (mean ± SD). Altogether 37% of the variation in size was explained by two factors: elevation of site (15%) and amount of clay & silt in sediments (22%). Variation in density appeared to play no significant role in determining size. Density was significantly linked to sediment properties (32%) and position inside the estuary (4%). Sediment biodeposition, the amount of material discharged per cockle, was 0.032 ± 0.017 g dry weight, the whole population thereby producing an estimated 387 tonnes of faeces and pseudo-faeces in the entire estuary per day. The study confirmed that access to food is a principal driver of growth, but the relatively small proportion of the variation in size explained by site elevation highlights that other factors play an important role. Sediment characteristics in particular were of importance to variation in size as well as density. It seems plausible that sediment properties were a proxy for factors such as bedload movement and exposure, which are more likely causal factors for distribution patterns. However, the bivalves may also actively favour certain sediment compositions for ease of burrowing and food availability. We suggest that the role of active and passive movement of bivalves within an estuary needs further clarification, which would affect individual growth rates and spatial size distribution patterns. The considerable amount of mucus bound material discharged by cockles suggests that the contribution of prolific bivalves to habitat properties of small estuaries is under-estimated.