scholarly journals A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna

2021 ◽  
Vol 8 ◽  
Author(s):  
Martijn C. Bart ◽  
Meggie Hudspith ◽  
Hans Tore Rapp ◽  
Piet F. M. Verdonschot ◽  
Jasper M. de Goeij

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical coral reefs. In tropical ecosystems, biodiversity and productivity are maintained through efficient recycling pathways, such as the sponge loop. In this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, the sponge-produced detritus serves as a food source for other organisms on the reef. Alternatively, the DOM stored in massive sponges was recently hypothesized to be transferred to higher trophic levels through predation of these sponges, instead of detritus production. However, for deep-sea sponges, the existence of all prerequisite, consecutive steps of the sponge loop have not yet been established. Here, we tested whether cold-water deep-sea sponges, similar to their tropical shallow-water counterparts, take up DOM and transfer assimilated DOM to associated fauna via either detritus production or predation. We traced the fate of 13carbon (C)- and 15nitrogen (N)-enriched DOM and particulate organic matter (POM) in time using a pulse-chase approach. During the 24-h pulse, the uptake of 13C/15N-enriched DOM and POM by two deep-sea sponge species, the massive species Geodia barretti and the encrusting species Hymedesmia sp., was assessed. During the subsequent 9-day chase in label-free seawater, we investigated the transfer of the consumed food by sponges into brittle stars via two possible scenarios: (1) the production and subsequent consumption of detrital waste or (2) direct feeding on sponge tissue. We found that particulate detritus released by both sponge species contained C from the previously consumed tracer DOM and POM, and, after 9-day exposure to the labeled sponges and detritus, enrichment of 13C and 15N was also detected in the tissue of the brittle stars. These results therefore provide the first evidence of all consecutive steps of a sponge loop pathway via deep-sea sponges. We cannot distinguish at present whether the deep-sea sponge loop is acting through a detrital or predatory pathway, but conclude that both scenarios are feasible. We conclude that sponges could play an important role in the recycling of DOM in the many deep-sea ecosystems where they are abundant, although in situ measurements are needed to confirm this hypothesis.

2020 ◽  
Vol 17 (5) ◽  
pp. 1231-1245 ◽  
Author(s):  
Christine Rooks ◽  
James Kar-Hei Fang ◽  
Pål Tore Mørkved ◽  
Rui Zhao ◽  
Hans Tore Rapp ◽  
...  

Abstract. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bioavailable nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with 15NO3--amended oxygen-saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. It was not possible to detect any rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+. Denitrification rates of the different sponge species ranged from below detection to 97 nmol N cm−3 sponge d−1 under oxic conditions, and from 24 to 279 nmol N cm−3 sponge d−1 under anoxic conditions. A positive relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is active and prepared for denitrification. The lack of a lag phase in the linear accumulation of the 15N-labelled N2 gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. Low rates for coupled nitrification–denitrification indicate that also under oxic conditions, the nitrate used to fuel denitrification rates was derived rather from the ambient seawater than from sponge nitrification. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter its origin, is then no longer available as a nutrient for the marine ecosystem. These results suggest a high potential denitrification capacity of deep-sea sponge grounds based on typical sponge biomass on boreal and Arctic sponge grounds, with areal denitrification rates of 0.6 mmol N m−2 d−1 assuming non-pumping sponges and still 0.3 mmol N m−2 d−1 assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. Anthropogenic impact and global change processes affecting the sponge redox state may thus lead to deep-sea sponge grounds changing their role in marine ecosystem from being mainly nutrient sources to becoming mainly nutrient sinks.


2019 ◽  
Author(s):  
Christine Rooks ◽  
James Kar-Hei Fang ◽  
Pål Tore Mørkved ◽  
Rui Zhao ◽  
Hans Tore Rapp ◽  
...  

Abstract. Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bio-available nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with 15NO3- – amended oxygen saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. Rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+ could not be detected. Denitrification rates of the different sponge species ranged from 0 to 114 nmol N cm-3 sponge day-1 under oxic conditions, and from 47 to 342 nmol N cm-3 sponge day-1 under anoxic conditions. An exponential relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is both prepared and optimized for denitrification. The lack of a lag phase in the linear accumulation of the 15N labelled N2 gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. High rates for coupled nitrification-denitrification (up to 89 % of nitrate reduction in the presence of oxygen) shows that under these conditions, the NO3- reduced in denitrification was primarily derived from nitrification within the sponge, directly coupling organic matter degradation and nitrification to denitrification in sponge tissues. Under anoxic condition when nitrification was not possible, nitrate to fuel the much higher denitrification rates had to be retrieved directly from the seawater. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter of its origin, is then no longer available as a nutrient for the marine ecosystem. Considering average sponge biomasses on typical boreal and Arctic sponge grounds, our sponge denitrification rates reveal areal denitrification rates of 0.8 mmol N m-2 day-1 assuming non-pumping sponges and still 0.3 mmol N m-2 day-1 assuming pumping sponges. This is well within the range of denitrification rates of continental shelf sediments. For the most densely populated boreal sponge grounds we calculated denitrification rates of up to 2 mmol N m-2 day-1, which is comparable to rates in coastal sediments. Increased future impact of sponge grounds by anthropogenic stressors reducing sponge pumping activity and further stimulating sponge anaerobic processes may thus lead to that deep-sea sponge grounds change their role in the marine ecosystem from nutrient sources to nutrient sinks.


2018 ◽  
pp. 184-200
Author(s):  
Irus Braverman

J Murray Roberts is a professor of applied marine biology and ecology in the School of GeoSciences at the University of Edinburgh, Scotland. His main research focus is deep-sea, or cold-water, corals. I interviewed him by Skype on January 27, 2016, and then over breakfast at a café in Edinburgh on April 20, 2016—in between two of his long excursions into the deep sea. I contemplated joining him on one of these excursions, but after finding out that this might require jumping out of a helicopter into the ocean, I thought better of the idea. I was interested in hearing from Roberts why deep-sea coral reefs were not really recognized as reefs by many coral conservation scientists (in his words, they are “Cinderella species”) and how the material differences between deep- and shallow-water corals play out in terms of regulatory regimes and in the relationship between scientists and lawyers in particular. In his focus on the Cinderella of the coral world, rather than her more glamorous and visible tropical sisters, Roberts’s narrative is an outlier. But then so are all of the other interchapter interviews, in significantly different ways....


Author(s):  
Michel Praet-Van

This ultrastructural investigation of gametogenesis in a deep-sea anemone of the Bay of Biscay trawled around 2000 m depth, contributes to the knowledge of biology and strategy of reproduction of deep-sea benthos.This sea anemone is dioecious. The sperm appears very similar to those of shallow water sea anemones of the genus, Calliactis. The ultrastructural investigation of oogenesis allows the characteristics of the stages of previtellogenesis and vitellogenesis to be defined. The latter begins with a period of lipogenesis correlated with the formation of a trophonema. Mature oocytes measure up to 180 (im in diameter. Study of spermatogenesis and oogenesis reveals that spawning occurs in April/May. In males, the main area of testicular cysts, full of sperm, reaches maximal development from March to May and, in females, the percentage of mature oocytes decreases from 33% in April to 1% in May.Spawning may be induced by the advent in the deep-sea of the products of the spring phytoplankton bloom. This period of spawning, during the increased deposition of organic matter to the deep-sea floor, may be an advantageous strategy for early development of Paracalliactis.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Sandra R. Maier ◽  
Tina Kutti ◽  
Raymond J. Bannister ◽  
James Kar-Hei Fang ◽  
Peter van Breugel ◽  
...  

2014 ◽  
Vol 26 (5) ◽  
pp. 554-562 ◽  
Author(s):  
F. Pasotti ◽  
P. Convey ◽  
A. Vanreusel

AbstractThe meiobenthic community of Potter Cove (King George Island, west Antarctic Peninsula) was investigated, focusing on responses to summer/winter conditions in two study sites contrasting in terms of organic matter inputs. Meiofaunal densities were found to be higher in summer and lower in winter, although this result was not significantly related to the in situ availability of organic matter in each season. The combination of food quality and competition for food amongst higher trophic levels may have played a role in determining the standing stocks at the two sites. Meiobenthic winter abundances were sufficiently high to infer that energy sources were not limiting during winter, supporting observations from other studies for both shallow water and continental shelf Antarctic ecosystems. Recruitment within meiofaunal communities was coupled to the seasonal input of fresh detritus for harpacticoid copepods but not for nematodes, suggesting that species-specific life history or trophic features form an important element of the responses observed.


2021 ◽  
Author(s):  
◽  
Joseph Marlow

<p>Coral reefs are among the most diverse ecosystems on the planet, yet they are also sensitive to anthropogenic disturbances that can degrade these systems. On many degraded reefs, large increases in bioeroding sponge abundance have occurred. On healthy reefs these sponges contribute to species diversity and habitat complexity, however there is growing concern that their proliferation on degraded reefs could lead to a state of net-erosion. In the Southeast Asian Indo-Pacific, the ecology of bioeroding sponges in relation to coral degradation has been poorly studied compared to other coral reef regions. This thesis aims to increase our understanding of the ecology of these sponges in the Wakatobi region of Indonesia, and their likely trajectory if reefs continue to degrade in the region.  My first research chapter aimed to identify the common bioeroding sponge species of the Wakatobi. This was achieved through in-water surveys, and subsequent spicule and phylogenetic analysis. This resulted in the identification of eight commonly occurring Wakatobi bioeroding sponge species, two of which are described for the first time. The assemblage composition was distinctly different from the only other bioeroding sponge study in Indonesian waters (Calcinai et al. 2005), highlighting the need for more clionaid taxonomic information from the region.  Having identified the common bioeroding sponge species in the region, my second chapter assessed the major environmental drivers of the abundance and assemblage composition of these sponges. Abundance surveys were conducted at 11 reef sites characterised by different environmental conditions and states of reef health. Bioeroding sponges occupied 8.9% of suitable substrate, and differences in abundance and assemblage composition were primarily attributed to differences in the availability of dead substrate. However, abundance was lowest at a sedimented and turbid reef, despite abundant dead substrate availability. This indicates a limited resilience in some species to conditions associated with terrestrial run-off and that not all forms of reef degradation are beneficial for bioeroding sponges. The capacity to increase spatial occupation of degraded reefs is also dependent upon larval recruitment and my third chapter was a two year recruitment study using in situ experimental calcareous blocks. Recruitment occurred rapidly and consistently with bioeroding sponges recruiting to approximately 70% of experimental blocks and exhibiting a preference for settlement on uncolonised dead calcareous substrates. The importance of substrate settlement cues and extent of larval dispersal appeared to differ between species, indicative of different recruitment mechanisms. Any significant increase in the availability of exposed calcareous substrate (e.g. following a mass coral bleaching event) is therefore likely to result in widespread increases in bioeroding sponge recruitment.  Surveys conducted in my second research chapter revealed that two of the three locally abundant zooxanthellate bioeroding species were absent from a highly turbid reef, Sampela. My fourth research chapter investigated whether this was due to light limitation by examining the photoacclimatory capabilities of the Symbiodinium photosymbionts of Cliona aff. viridis n. sp. A. PAM chlorophyll fluorometry was employed in a 25 day shading experiment and Symbiodinium of C. aff. viridis n. sp. A demonstrated an ability to photoacclimate to extreme light reduction and recover quickly when conditions returned to normal. My results demonstrate that the absence of this species at Sampela is not due to light limitation but possibly due to other stressors associated with turbidity, e.g. suspended sediment.  My final chapter was an assessment of the environmental drivers of rates of bioerosion in Spheciospongia cf. vagabunda, a common species in the Wakatobi. Erosion rates were determined from changes in dry-weight of calcareous substrates with attached grafts of S. cf. vagabunda after a year deployment across seven reef sites. The average bioerosion rate was 12.0 kg m⁻² sponge tissue yr⁻¹ (± 0.87 SE), but differed between sites and was negatively correlated with settled sediment depth. Bioerosion by this species can play a significant part in the carbonate budget on reefs where it is abundant (up to 20% of available substrate on some reefs in the Wakatobi) but is likely reduced on highly sedimented reefs.  In summary, the Wakatobi bioeroding sponge assemblage is diverse and overall, both adult abundance and recruitment are primarily driven by the availability of dead calcareous substrates. Therefore, further coral mortality and a subsequent rise in the availability of dead substrate in the region is likely to result in increased abundance of bioeroding sponges. However, not all forms of reef degradation will benefit these sponges; turbid and sedimented reefs will likely constitute stressful habitats for some bioeroding sponge species and assemblages in these environments will be comprised of fewer more resilient species.</p>


Science ◽  
2013 ◽  
Vol 342 (6154) ◽  
pp. 108-110 ◽  
Author(s):  
Jasper M. de Goeij ◽  
Dick van Oevelen ◽  
Mark J. A. Vermeij ◽  
Ronald Osinga ◽  
Jack J. Middelburg ◽  
...  

Ever since Darwin’s early descriptions of coral reefs, scientists have debated how one of the world’s most productive and diverse ecosystems can thrive in the marine equivalent of a desert. It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna. This “sponge loop” was confirmed in aquarium and in situ food web experiments, using 13C- and 15N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as coral reefs persist in oligotrophic seas—the reef’s paradox—and has implications for reef ecosystem functioning and conservation strategies.


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