Benthic Filter Feeders Research Articles

My Favorite Animal, Amphioxus: Unparalleled for Studying Early Vertebrate Evolution

Amphioxus represents the most basally divergent group in chordates and probably the best extant proxy to the ancestor of all chordates including vertebrates. The amphioxus, or lancelets, are benthic filter feeding marine animals and their interest as a model in research is due to their phylogenetic position and their anatomical and genetic stasis throughout their evolutionary history. From the first works in the 19th century to the present day, enormous progress is made mainly favored by technical development at different levels, from spawning induction and husbandry techniques, through techniques for studies of gene function or of the role of different signalling pathways through embryonic development, to functional genomics techniques. Together, these advances foretell a plethora of interesting developments in the world of research with the amphioxus model. Here, the discovery and development of amphioxus as a superb model organism in evolutionary and evolutionary-developmental biology are reviewed.

Ecological Carrying Capacity for Shellfish Aquaculture—Sustainability of Naturally Occurring Filter-Feeders and Cultivated Bivalves

Carrying capacity models for aquaculture have increased in complexity over the last decades, partly because aquaculture growth, sustainability, and licensing are themselves extremely complex. Moreover, there is an asymmetric pattern to all these components, when considered from an international perspective, because of very different regulation and governance of the aquaculture sector in Asia, Europe, and America. Two case studies were used, from Long Island Sound in the United States, and Belfast Lough, in Europe, to examine the interactions between cultivated shellfish and other autochthonous benthic filter-feeders. The objective is to illustrate how such interactions can be incorporated in system-scale ecological models and analyzed from the perspective of ecological carrying capacity. Two different models are described, one based on equations that relate the filtration rate of the hard clam Mercenaria mercenaria to physiological and population factors and one based on a habitat-specific analysis of multiple species of benthic filter-feeders. Both types of models have relative advantages and challenges, and both were integrated in ecosystem modeling frameworks with substantial numbers of state variables representing physical and biogeochemical processes. These models were applied to (1) examine the relative role of the two components (cultivated and wild) in the filtration of particulate organic matter (both phytoplankton and organic detritus), (2) quantify the effect of wild species on harvest of cultivated organisms (eastern oyster and blue mussel), and (3) assess the role of organically extractive aquaculture and other filter-feeders on top–down control of eutrophication.

DPEP1 Balance GSH Involve in Cadmium Stress Response in Blood Clam Tegillarca granosa.

The blood clam, Tegillarca granosa, is a benthic filter feeder with a strong capacity to accumulate and tolerate cadmium (Cd). In our previous study, DPEP1 was shown to be significantly up-regulated under Cd stress based on proteomic analysis. To investigate whether DPEP1 is involved in Cd-induced response, the function of DPEP1 in T. granosa was investigated by integrated molecular and protein approaches. Rapid amplification cDNA end (RACE) assay was established to achieve the complete cDNA sequence of DPEP1 from T. granosa. The full-length cDNA of DPEP1 was 1811 bp, and it contained a 1359-bp open reading frame (ORF), including a 22-amino acid signal peptide. qRT-PCR analysis revealed that DPEP1 was expressed in all examined tissues with the highest expression in gills. At the same time, we investigated DPEP1 gene expression changes after Cd stress at different time points over 96 h. We found that the expression of DPEP1 increased upon initial Cd stress, then it was inhibited, and finally, it was maintained at a low level. Moreover, recombinant DPEP1 showed that higher glutathione (GSH) hydrolysis activity in the temperature range of 30–40°C, and its maximum activity was at pH = 6. Additionally, the results of immunohistochemistry also confirmed that DPEP1 protein was expressed in all test tissues with the highest expression in gills. In addition, there was a positive correlation between QRT-PCR and immunohistochemistry. These results suggested that DPEP1 is probably involved in Cd-induced response by balancing GSH.

Habitat, diet, feeding and resting behaviour of the Korean endemic cobitidIksookimia hugowolfeldi(Cobitidae, Pisces) in the wild

A study on the habitat use and diet of Iksookimia hugowolfeldi, which is endemic to Korea, was carried out focusing on feeding and resting behaviour in the wild. This study focused on a valley stream in a forest on Geogeum Island (Eojeon-ri, Geumsanmyeon, Goheung-gun, Jeollanam-do, Korea) with a large population. The bottom substrate of this stream was mud (< 0.1 mm in diameter, 10 % relative abundance), sand (0.1–2 mm, 30 %), gravel (2–16 mm, 20 %), pebbles (16–64 mm, 20 %), cobbles (64–256 mm, 10 %), and boulders (> 256 mm, 10 %), with an Aa-Bb river type and a slow current (0.1 m/s). The food sources analyzed based on the index of relative importance (IRI) included Diptera (70.98 %), Phryganeidae (10.46 %), Branchiopoda (9.74 %), Harpacticidae (8.33 %), Ephemeroptera (0.47 %) and other (0.02 %). As a diurnal and benthic filter feeder, two main feeding behaviours were observed: feeding on surface (sand, cobble) and on sand-cobble digging. Resting behaviour predominantly occurred on the surface of sand and cobbles, and sometimes while buried in the sand. Daily feeding behaviour was more active at the highest water temperature of 22.1– 23.7 °C from 14:00 to 15:00, and feeding behaviour occurred more frequently in July to August, at temperatures as high as 22–24 °C. Meanwhile, while the water temperature is below 8 °C, they are getting around in the water by being hid in or buried in the substrate. In that season, the empty stomach rate was higher than in other seasons.

Shallow water sponges along the south coast of Java, Indonesia

Hadi TA, Hafizt M, Hadiyanto, Budiyanto A, Siringoringo RM. 2018. Shallow water sponges along the south coast of Java, Indonesia. Biodiversitas 19: 535-543. Sponges are the most diverse benthic filter feeders, occupying many different types of marine habitat. The south coast of Java is one such marine habitat, very exposed to the open sea. This study investigated the sponge diversity as well as their morphological characters across the south coast of Java. The observations were carried out from 2011 to 2016 in four different locations, including Pamang Peuk, Gunungkidul, Prigi Bay and Bayuwangi. The study found 96 sponge species, from 15 orders, and described them in terms of nine morphological characters. The most common species included Spheciospongia inconstans, Stylissa massa, Callyspongia sp. and Cinachyrella australiensis, while the most common growth forms were massive and encrusting, accounting respectively for 34.4% and 28.1% of the total number of species. There was a significant difference in the number of species found between sub-tidal and intertidal habitats; subtidal sponges were approximately 50% more diverse than intertidal sponges. Apart from the habitat types, the number of sponges varied in relation to the longitude; east Java had more sponge species with more variations in morphology compared to central and west Java. Encrusting and globular growth forms were the most common characteristics of intertidal sponges in west and central Java, while other growth forms comprised the diverse characteristics of the subtidal sponges in the east Java. This baseline information is essential for management of marine biodiversity hotspots in taking decisions for marine life conservation, because the global trajectory of marine habitat degradation is predicted to rise.

First Evaluation of Microplastic Content in Benthic Filter-feeders of the Gulf of La Spezia (Ligurian Sea)

ABSTRACTThe ingestion and retention of microplastics of filter-feeder organisms represent a risk for the final consumers and the environment. Biomonitoring is necessary to deal with the effects of plastic material pollution. The selection of the monitored organisms strongly affects the relevance of the results and the understanding of the environmental conditions. The results discussed in this paper highlight the differences in the estimate of microplastic pollution depending on the species subject of study. Ascidia spp. specimens retained a value five-fold higher (0.62 MP/g) than bivalve species (Crassostrea gigas 0.11 MP/g; Mytilus galloprovincialis 0.05 MP/g; Anomia ephippium 0.12 MP/g).

A novel Chromatiales bacterium is a potential sulfide oxidizer in multiple orders of marine sponges.

Sponges are benthic filter feeders that play pivotal roles in coupling benthic-pelagic processes in the oceans that involve transformation of dissolved and particulate organic carbon and nitrogen into biomass. While the contribution of sponge holobionts to the nitrogen cycle has been recognized in past years, their importance in the sulfur cycle, both oceanic and physiological, has only recently gained attention. Sponges in general, and Theonella swinhoei in particular, harbour a multitude of associated microorganisms that could affect sulfur cycling within the holobiont. We reconstructed the genome of a Chromatiales (class Gammaproteobacteria) bacterium from a metagenomic sequence dataset of a T. swinhoei-associated microbial community. This relatively abundant bacterium has the metabolic capability to oxidize sulfide yet displays reduced metabolic potential suggestive of its lifestyle as an obligatory symbiont. This bacterium was detected in multiple sponge orders, according to similarities in key genes such as 16S rRNA and polyketide synthase genes. Due to its sulfide oxidation metabolism and occurrence in many members of the Porifera phylum, we suggest naming the newly described taxon Candidatus Porisulfidus.

Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins

Bivalve molluscs are descendants of an early-Cambrian lineage superbly adapted to benthic filter feeding. Adaptations in form and behavior are well recognized, but the underlying molecular mechanisms are largely unknown. Here, we investigate the genome, various transcriptomes, and proteomes of the scallop Chlamys farreri, a semi-sessile bivalve with well-developed adductor muscle, sophisticated eyes, and remarkable neurotoxin resistance. The scallop’s large striated muscle is energy-dynamic but not fully differentiated from smooth muscle. Its eyes are supported by highly diverse, intronless opsins expanded by retroposition for broadened spectral sensitivity. Rapid byssal secretion is enabled by a specialized foot and multiple proteins including expanded tyrosinases. The scallop uses hepatopancreas to accumulate neurotoxins and kidney to transform to high-toxicity forms through expanded sulfotransferases, probably as deterrence against predation, while it achieves neurotoxin resistance through point mutations in sodium channels. These findings suggest that expansion and mutation of those genes may have profound effects on scallop’s phenotype and adaptation.

Water clearance efficiency indicates potential filter-feeding interactions between invasive Sinanodonta woodiana and native freshwater mussels

The Chinese pond mussel (Sinanodonta woodiana Lea, 1834) is a benthic filter-feeder that prefers soft-bottomed freshwater habitats and has successfully spread into both tropical and temperate water bodies outside its natural Southeast Asian range. Due to its preference for nutrient-rich waters with high levels of suspended food particles, the capacity of S. woodiana to influence natural seston concentrations is thought to be relatively low in comparison to that of other invasive bivalves. The experimental quantification of seston removal efficiency reported here demonstrates that S. woodiana is able to reduce seston loads to levels comparable to those by the control native freshwater mussel species Unio tumidus Philipsson, 1788. Moreover, increasing food depletion did not cause detectable changes in the filtration regime of S. woodiana, although the activity of native U. tumidus was significantly reduced. The seston clearance rate (volume of water cleared of particles per unit time) of S. woodiana averaged 9.3 ± 4.0 mL g−1 wet mass h−1, which corresponds to the total daily volume of water filtered being up to several hundreds to thousands L m−2 at the maximal S. woodiana population densities reported in the literature. The observed filtration capacity of S. woodiana and its current invasional spread into areas inhabited by endangered freshwater mussels call for more careful consideration of filter-feeding interactions with native mussels. The potential impacts of S. woodiana should be studied in more detail with respect to available food resources and long-term nutritional needs of native species and reflected in management strategies in the invaded range.

Inter-annual cascade effect on marine food web: A benthic pathway lagging nutrient supply to pelagic fish stock.

Currently, spatial and temporal changes in nutrients availability, marine planktonic, and fish communities are best described on a shorter than inter-annual (seasonal) scale, primarily because the simultaneous year-to-year variations in physical, chemical, and biological parameters are very complex. The limited availability of time series datasets furnishing simultaneous evaluations of temperature, nutrients, plankton, and fish have limited our ability to describe and to predict variability related to short-term process, as species-specific phenology and environmental seasonality. In the present study, we combine a computational time series analysis on a 15-year (1995–2009) weekly-sampled time series (high-resolution long-term time series, 780 weeks) with an Autoregressive Distributed Lag Model to track non-seasonal changes in 10 potentially related parameters: sea surface temperature, nutrient concentrations (NO2, NO3, NH4 and PO4), phytoplankton biomass (as in situ chlorophyll a biomass), meroplankton (barnacle and mussel larvae), and fish abundance (Mugil liza and Caranx latus). Our data demonstrate for the first time that highly intense and frequent upwelling years initiate a huge energy flux that is not fully transmitted through classical size-structured food web by bottom-up stimulus but through additional ontogenetic steps. A delayed inter-annual sequential effect from phytoplankton up to top predators as carnivorous fishes is expected if most of energy is trapped into benthic filter feeding organisms and their larval forms. These sequential events can explain major changes in ecosystem food web that were not predicted in previous short-term models.

Comparisons of benthic filter feeder communities before and after a large-scale capital dredging program

Changes in turbidity, sedimentation and light over a two year large scale capital dredging program at Onslow, northwestern Australia, were quantified to assess their effects on filter feeder communities, in particular sponges. Community functional morphological composition was quantified using towed video surveys, while dive surveys allowed for assessments of species composition and chlorophyll content. Onslow is relatively diverse recording 150 sponge species. The area was naturally turbid (1.1 mean P80 NTU), with inshore sites recording 6.5× higher turbidity than offshore localities, likely influenced by the Ashburton River discharge. Turbidity and sedimentation increased by up to 146% and 240% through dredging respectively, with corresponding decreases in light levels. The effects of dredging was variable, and despite existing caveats (i.e. bleaching event and passing of a cyclone), the persistence of sponges and the absence of a pronounced response post-dredging suggest environmental filtering or passive adaptation acquired pre-dredging may have benefited these communities.

Host-specific assembly of sponge-associated prokaryotes at high taxonomic ranks

Sponges (Porifera) are abundant and diverse members of benthic filter feeding communities in most marine ecosystems, from the deep sea to tropical reefs. A characteristic feature is the associated dense and diverse prokaryotic community present within the sponge mesohyl. Previous molecular genetic studies revealed the importance of host identity for the community composition of the sponge-associated microbiota. However, little is known whether sponge host-specific prokaryotic community patterns observed at 97% 16S rRNA gene sequence similarity are consistent at high taxonomic ranks (from genus to phylum level). In the present study, we investigated the prokaryotic community structure and variation of 24 sponge specimens (seven taxa) and three seawater samples from Sweden. Results show that the resemblance of prokaryotic communities at different taxonomic ranks is consistent with patterns present at 97% operational taxonomic unit level.

Do brachiopods show substrate‐related phenotypic variation? A case study from the Burgess Shale

AbstractAs sessile, benthic filter feeders, brachiopods share an intimate relationship with their chosen substrate. Individuals of Micromitra burgessensis in the Burgess Shale Formation are preserved in life position, attached to a range of hard substrates, including skeletal debris, conspecific brachiopods, sponges and enigmatic tubes. Here we investigate the phenotypic variability of M. burgessensis associated with differing substrate attachments. We apply geometric morphometrics to test for variation by plotting landmarks on the exterior of ventral and dorsal valves of M. burgessensis specimens that are preserved attached to different substrates. Using principal component, canonical variate analyses and anova, we determine that there is some variation in shape related to substrate. Canonical variate analyses, for ventral valves and dorsal valves, indicate that specimens attached to the same substrate are recognizable in shape from specimens attached to other substrate types. The strength of differentiation however, is not robust and combined with our discriminate analysis of separate populations suggests that there is the potential for substrates to exercise only weak control over the morphology of Brachiopoda.

The annual and seasonal variability of the carbonate system in the Bay of Brest (Northwest Atlantic Shelf, 2008–2014)

From 2008 to 2014, the MAREL-Iroise buoy, located in the Bay of Brest, collected high-frequency measurements of partial pressure of CO2 (pCO2) and ancillary hydrographic parameters, in conjunction with a comprehensive sampling regime of two additional carbonate system variables total alkalinity (AT), and dissolved inorganic carbon (DIC). Biological processes drive variations in AT and DIC throughout the year, except in winter, when primary production is negligible and large freshwater inputs occur. Annually, the Bay of Brest generally behaves as a source of CO2 to the atmosphere (0.14±0.20molCm−2yr−1), showing inter-annual variability significantly linked to annual net community production (NCP). The presence of a large community of benthic filter feeders leads to high levels of particulate organic matter (POM) and opal deposition during the spring diatom bloom. Over the following few months, benthic POM remineralisation reduces the spring CO2 deficit relative to the atmosphere, and remineralisation of biogenic silica supplies further late spring primary production. The result is an inverse spring NCP – air-sea CO2 flux relationship, whereby greater NCP in early spring results in lower fluxes of CO2 into the Bay in late spring. This recycling mechanism, or silicic acid pump, also links the spring and summer NCP values, which are both determined by the peak wintertime nutrient concentrations. The carbonate system is further affected by the benthic community in winter, when CaCO3 dissolution is evident from notable deviations in the ΔAT:ΔDIC ratio. This study highlights the necessity of individual study of coastal, temperate ecosystems and contributes to a better understanding of what determines coastal areas as sinks or sources of CO2 to the atmosphere.

Spatio-Temporal Variation in Effects of Upwelling on the Fatty Acid Composition of Benthic Filter Feeders in the Southern Benguela Ecosystem: Not All Upwelling Is Equal.

Variability in mesoscale nearshore oceanographic conditions plays an important role in the distribution of primary production and food availability for intertidal consumers. Advection of nutrient rich waters by upwelling usually allows the proliferation of diatoms, later replaced by dinoflagellates. We examined upwelling effects on the fatty acid (FA) signature of a benthic intertidal filter feeder to identify its response to pulsed variability in food availability. The study took place in two contrasting seasons and at two upwelling and two non-upwelling sites interspersed within the southern Benguela upwelling system of South Africa. We investigated the FA composition of the adductor muscles and gonads of the mussel Mytilus galloprovincialis to assess how FA are apportioned to the different tissues and whether this changes between upwelling and non-upwelling conditions. In situ temperature loggers used to identify upwelling conditions at the four sites indicated that such events occurred only at the upwelling centres and only in summer. Tissues differed strongly, with gonads presenting a higher proportion of essential FAs. This could reflect the faster turnover rate of gonad tissue or preferential retention of specific FA for reproductive purposes. FA composition did not vary as a direct function of upwelling, but there were strong dissimilarities among sites. Upwelling influenced mussel diets at one upwelling site while at the other, the expected signature of upwelling was displaced downstream of the core of upwelling. Condition Index (CI) and Gonad Index (GI) differed among sites and were not influenced by upwelling, with GI being comparable among sites. In addition, FA proportions were consistent among sites, indicating similar food quality and quantity over time and under upwelling and non-upwelling conditions. This suggests that the influence of upwelling on the west coast of South Africa is pervasive and diffuse, rather than discrete; while nearshore retention or advection of upwelled water is critical and site-specific so that the effects of upwelling differ even among sites categorised as upwelling centres.

TANK-binding kinase-1 broadly affects oyster immune response to bacteria and viruses.

As a benthic filter feeder of estuaries, the immune system of oysters provides one of the best models for studying the genetic and molecular basis of the innate immune pathway in marine invertebrates and examining the influence of environmental factors on the immune system. Here, the molecular function of molluscan TANK-binding kinase-1 (TBK1) (which we named CgTBK1) was studied in the Pacific oyster, Crassostrea gigas. Compared with known TBK1 proteins in other model organisms, CgTBK1 contains a conserved S-TKc domain and a coiled coil domain at the N- and C-terminals but lacks an important ubiquitin domain. Quantitative real-time PCR analysis revealed that the expression level of CgTBK1 was ubiquitous in all selected tissues, with highest expression in the gills. CgTBK1 expression was significantly upregulated in response to infections with Vibrio alginolyticus, ostreid herpesvirus 1 (OsHV-1 reference strain and μvar), and polyinosinic:polycytidylic acid sodium salt, suggesting its broad function in immune response. Subcellular localization showed the presence of CgTBK1 in the cytoplasm of HeLa cells, suggesting its potential function as the signal transducer between the receptor and transcription factor. We further demonstrated that CgTBK1 interacted with CgSTING in HEK293T cells, providing evidence that CgTBK1 could be activated by direct binding to CgSTING. In summary, we characterized the TBK1 gene in C.gigas and demonstrated its role in the innate immune response to pathogen infections.

Autochthony, allochthony and the role of consumers in influencing the sensitivity of aquatic systems to nutrient enrichment

Primary consumers may mitigate or exacerbate the effects of nutrient enrichment by grazing on plant matter and recycling nutrients. Few studies have quantified these effects for a suite of consumers and in the context of other processes regulating plant standing crop and nutrient supply. We quantified the abundance, feeding and diet of zooplankton, benthic filter-feeders, and planktivorous and detritivorous fish in the James River Estuary and found that consumer-mediated fluxes of CHLa and N were small in comparison to other fluxes regulating phytoplankton abundance (production, respiration, advection) and N availability (external inputs, internal recycling). Chlorophyll-a ingestion by consumers was equivalent to 15% of daily phytoplankton production and N recycling by consumers corresponded to 29% of phytoplankton N demand. The bulk of phytoplankton production (74%) was lost to autotrophic and heterotrophic respiration. Recycling of N contained in autochthonous and allochthonous organic matter was sufficient to meet 100% of phytoplankton N demand with external inputs corresponding to 39% of phytoplankton N demand. Experiments using 2000L outdoor mesocosms with natural plankton communities showed that the presence of consumers (shad) resulted in higher N availability, elevated CHLa and reduced macrozooplankton abundance. Overall, our study showed that the direct effect of consumers on fluxes of CHLa and N was small as the bulk of phytoplankton biomass and N passed to microbial decomposers. However selective grazing by planktivorous fishes reduced zooplankton densities resulting in greater phytoplankton yield at lower nutrient concentrations.

Bivalve Grazing Can Shape Phytoplankton Communities

The ability of bivalve filter feeders to limit phytoplankton biomass in shallow waters is well-documented, but the role of bivalves in shaping phytoplankton communities is not. The coupled effect of bivalve grazing at the sediment-water interface and sinking of phytoplankton cells to that bottom filtration zone could influence the relative biomass of sinking (diatoms) and non-sinking phytoplankton. Simulations with a pseudo-2D numerical model showed that benthic filter feeding can interact with sinking to alter diatom:non-diatom ratios. Cases with the smallest proportion of diatom biomass were those with the fastest sinking speeds and strongest bivalve grazing rates. Hydrodynamics modulated the coupled sinking-grazing influence on phytoplankton communities. For example, in simulations with persistent stratification, the non-sinking forms accumulated in the surface layer away from bottom grazers while the sinking forms dropped out of the surface layer toward bottom grazers. Tidal-scale stratification also influenced vertical gradients of the two groups in opposite ways. The model was applied to Suisun Bay, a low-salinity habitat of the San Francisco Bay system that was transformed by the introduction of the exotic clam Potamocorbula amurensis. Simulation results for this Bay were similar to (but more muted than) those for generic habitats, indicating that P. amurensis grazing could have caused a disproportionate loss of diatoms after its introduction. Our model simulations suggest bivalve grazing affects both phytoplankton biomass and community composition in shallow waters. We view these results as hypotheses to be tested with experiments and more complex modeling approaches.

Hierarchical effects of biogeography and upwelling shape the dietary signatures of benthic filter feeders

Hierarchical effects of biogeography and upwelling shape the dietary signatures of benthic filter feeders

Does proximity to urban centres affect the dietary regime of marine benthic filter feeders?

Threats to marine ecosystems include habitat destruction and degradation of water quality, resulting from land- and ocean-based human activities. Anthropogenic input causing modification of water quality, can affect primary productivity and thus food availability and quality for higher trophic levels. This is especially important for sedentary benthic intertidal communities, which rely on local food availability. We investigated the effect of urbanization on the dietary regime of four species of intertidal filter feeders (three barnacles and one mussel) at sites close to high-density cities and at sites far from heavily urbanized areas using fatty acid and stable isotope techniques. δ15N was significantly higher at urbanized sites compared to their corresponding control sites for all species with few exceptions, while no effect on δ13C was recorded. Barnacle fatty acid profiles were not affected by cities, while mussels from sites close to cities had fatty acid signatures with a higher proportion of polyunsaturated fatty acids (PUFA). We suggest that the enrichment in δ15N at urbanised sites reflects the influence of anthropogenically derived nitrogen directly linked to wastewater input from domestic and industrial sewage. Linked to this, the high proportion of PUFA in mussels at urbanized sites may reflect the influence of increased nitrogen concentrations on primary production and enhanced growth of large phytoplankton cells. The results indicate that anthropogenic effects can strongly influence the diets of benthic organisms, but these effects differ among taxa. Changes in the diet of such habitat forming species can affect their fitness and survival with potential effects on the populations associated with them.