Accelerated biogenic silica dissolution by marine invertebrate digestion: in comparison with phosphorus and iron

Ying WANG; Shaoping KUANG; Guangtao ZHANG

doi:10.1007/s00343-021-1117-7

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Accelerated biogenic silica dissolution by marine invertebrate digestion: in comparison with phosphorus and iron

Continued from the back cover | Updated：2023-05-20

- Accelerated biogenic silica dissolution by marine invertebrate digestion: in comparison with phosphorus and iron
- Journal of Oceanology and Limnology Vol. 40, Issue 3, Pages: 1110-1120(2022)
- Affiliations：
  
  1.Qingdao University of Science and Technology, Qingdao 266000, China
  2.Jiaozhou Bay Marine Ecosystem Research Station, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  3.Laboratory for Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
- Author bio：
  
  Shaoping KUANG, kuangshaoping@126.com
  Guangtao ZHANG, gtzhang@qdio.ac.cn
- Funds：
- DOI：10.1007/s00343-021-1117-7
  CLC：
- Published：2022-03
- Accepted：
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Ying WANG, Shaoping KUANG, Guangtao ZHANG. Accelerated biogenic silica dissolution by marine invertebrate digestion: in comparison with phosphorus and iron[J]. Journal of Oceanology and Limnology, 2022, 40(3): 1110-1120.
DOI：

Ying WANG, Shaoping KUANG, Guangtao ZHANG. Accelerated biogenic silica dissolution by marine invertebrate digestion: in comparison with phosphorus and iron[J]. Journal of Oceanology and Limnology, 2022, 40(3): 1110-1120. DOI： 10.1007/s00343-021-1117-7.

摘要

Abstract

Herbivore digestion in aquatic ecosystems is usually considered a method of nutrient repackaging rather than recycling

as recalcitrant and low-level nutrients are presumed for their egesta. We hypothesize that this opinion holds only for nutrients recycled by excretion and egestion

not for those elements recycled overwhelmingly by fecal decomposition. In this study

we compared the dissolution of biogenic silica (BSi)

phosphorus (P) and iron (Fe) between two food items and fecal pellets of two marine invertebrates fed on artificial seawaters free of bacteria. Relative to raw food materials

the mass proportion in fecal pellets of BSi increased

while that of P and Fe decreased. During the 21 days of incubation

the total dissolution rate of BSi was 13.9–36.0 times higher in fecal pellets than food items

followed by P (1.5–4.2 times) and Fe (1.1–2.4 times). While the dissolution of BSi and Fe occurred mostly in the first few days

P was mostly released in the last ten days. Regarding BSi dissolution

a higher rate was observed in oyster

Crassostrea gigas

than the Echiuran

Urechis unicinctus

but no significant difference was found between fecal pellets in either species under naturally available diatom food (

Phaeodactylum tricornutum

) and introduced terrestrial food (rice husk powder)

respectively. Our results show direct evidence of digestion-associated nutrients mobilization. BSi dissolution after animal digestion may be similarly efficient to that caused by bacteria colonization in natural seawater.

关键词

Keywords

references

Allgeier J E, Burkepile D E, Layman C A. 2017. Animal pee in the sea: consumer-mediated nutrient dynamics in the world's changing oceans. Global Change Biology , 23 (6): 2166-2178, https://doi.org/10.1111/gcb.13625..

Bidle K D, Azam F. 1999. Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature , 397 (6719): 508-512, https://doi.org/10.1038/17351..

Bidle K D, Azam F. 2001. Bacterial control of silicon regeneration from diatom detritus: significance of bacterial ectohydrolases and species identity. Limnology and Oceanography , 46 (7): 1606-1623..

Blackman E, Bailey C B. 1971. Dissolution of silica from dried grass in nylon bags placed in the rumen of a cow. Canadian Journal of Animal Science , 51 (2): 327-332, https://doi.org/10.4141/cjas71-045..

Cabanes D J E, Norman L, Santos-Echeandía J, Iversen M H, Trimborn S, Laglera L M, Hassler C S. 2017. First evaluation of the role of salp fecal pellets on iron biogeochemistry. Frontiers in Marine Science , 3 : 289, https://doi.org/10.3389/fmars.2016.00289..

Chen W B, Zhang S S, Sun Y, Tian B, Song L J, Xu Y, Liu T. 2021. Effects of substrate on the physiological characteristics and intestinal microbiota of Echiura worm ( Urechis unicinctus ) juveniles. Aquaculture , 530 : 735710, https://doi.org/10.1016/j.aquaculture.2020.735710..

Fabiano M, Danovaro R, Olivari E, Misic C. 1994. Decomposition of faecal matter and somatic tissue of Mytilus galloprovincialis : changes in organic matter composition and microbial succession. Marine Biology , 119 (3): 375-384, https://doi.org/10.1007/BF00347534..

Freese D, Kreibich T, Niehoff B. 2012. Characteristics of digestive enzymes of calanoid copepod species from different latitudes in relation to temperature, pH and food. Comparative Biochemistry and Physiology Part B : Biochemistry and Molecular Biology , 162 (4): 66-72, https://doi.org/10.1016/j.cbpb.2012.04.007..

Giles H, Pilditch C A. 2006. Effects of mussel ( Perna canaliculus ) biodeposit decomposition on benthic respiration and nutrient fluxes. Marine Biology , 150 (2): 261-271, https://doi.org/10.1007/s00227-006-0348-7..

Grégoire M, Raick C, Soetaert K. 2008. Numerical modeling of the central Black Sea ecosystem functioning during the eutrophication phase. Progress in Oceanography , 76 (3): 286-333, https://doi.org/10.1016/j.pocean.2008.01.002..

Grosell M, Farrell A P, Brauner C J. 2011. The Multifunctional Gut of Fish. Academic Press, Boston.

Halvorson H M, Hall D J, Evans-White M A. 2017. Long-term stoichiometry and fates highlight animal egestion as nutrient repackaging, not recycling, in aquatic ecosystems. Functional Ecology , 31 (9): 1802-1812, https://doi.org/10.1111/1365-2435.12875..

Harris J M. 1993. The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microbial Ecology , 25 (3): 195-231, https://doi.org/10.1007/BF00171889..

Huang D, Qin S, PU Y, Jiao X D. 2020. Advances in studies of artificial breeding and culturing techniques and the comprehensive utilization of Urechis unicinctus . Marine Sciences , 44 (12): 123-131. (in Chinese with English abstract).

Jansen H M, Verdegem M C J, Strand Ø, Smaal A C. 2012. Seasonal variation in mineralization rates (C-N-P-Si) of mussel Mytilus edulis biodeposits. Marine Biology , 159 (7): 1567-1580, https://doi.org/10.1007/s00227-012-1944-3..

Jansen H, Wolf-Gladrow D A. 2001. Carbonate dissolution in copepod guts: a numerical model. Marine Ecology Progress Series , 221 : 199-207, https://doi.org/10.3354/meps221199..

King G M, Judd C, Kuske C R, Smith C. 2012. Analysis of stomach and gut microbiomes of the eastern oyster ( Crassostrea virginica ) from coastal Louisiana, USA. PLoS One , 7 (12): e51475, https://doi.org/10.1371/journal.pone.0051475..

Kitchell J F, O'Neill R V, Webb D, Gallepp G W, Bartell S M, Koonce J F, Ausmus B S. 1979. Consumer regulation of nutrient cycling. BioScience , 29 (1): 28-34, https://doi.org/10.2307/1307570..

Le Mézo P K, Galbraith E D. 2021. The fecal iron pump: global impact of animals on the iron stoichiometry of marine sinking particles. Limnology and Oceanography , 66 (1): 201-213, https://doi.org/10.1002/lno.11597..

Lee B G, Lee J S, Luoma S N, Choi H J, Koh C H. 2000. Influence of acid volatile sulfide and metal concentrations on metal bioavailability to marine invertebrates in contaminated sediments. Environmental Science & Technology , 34 (21): 4517-4523, https://doi.org/10.1021/es001033h..

Luoma S N, Johns C, Fisher N S, Steinberg N A, Oremland R S, Reinfelder J R. 1992. Determination of selenium bioavailability to a benthic bivalve from particulate and solute pathways. Environmental Science & Technology , 26 (3): 485-491, https://doi.org/10.1021/es00027a005..

McKindsey C W, Archambault P, Callier M D, Olivier F. 2011. Influence of suspended and off-bottom mussel culture on the sea bottom and benthic habitats: a review. Canadian Journal of Zoology , 89 (7): 622-646, https://doi.org/10.1139/z11-037..

McNaughton S J, Ruess R W, Seagle S W. 1988. Large mammals and process dynamics in African ecosystems. BioScience , 38 (11): 794-800, https://doi.org/10.2307/1310789..

Needham S J, Worden R H, Cuadros J. 2006. Sediment ingestion by worms and the production of bio-clays: a study of macrobiologically enhanced weathering and early diagenetic processes. Sedimentology , 53 (3): 567-579, https://doi.org/10.1111/j.1365-3091.2006.00781.x..

Needham S J, Worden R H, Mcilroy D. 2004. Animal-sediment interactions: the effect of ingestion and excretion by worms on mineralogy. Biogeosciences , 1 (2): 113-121, https://doi.org/10.5194/bg-1-113-2004..

Nelson D M, Tréguer P, Brzezinski M A, Leynaert A, Quéguiner B. 1995. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles , 9 (3): 359-372, https://doi.org/10.1029/95GB01070..

Passow U, Engel A, Ploug H. 2003. The role of aggregation for the dissolution of diatom frustules. Fems Microbiology Ecology , 46 (3): 247-255, https://doi.org/10.1016/S0168-6496(03)00199-5..

Platt T, Rao D V S, Smith J C, Li W K, Irwin B, Horne E P W, Sameoto D D. 1983. Photosynthetically-competent phytoplankton from the aphotic zone of the deep ocean. Marine Ecology Progress Series , 10 (2): 105-110, https://doi.org/10.3354/meps010105..

Pomeroy L R. 1974. The ocean's food web, a changing paradigm. BioScience , 24 (9): 499-504, https://doi.org/10.2307/1296885..

Prins T C, Smaal A C, Dame R F. 1997. A review of the feedbacks between bivalve grazing and ecosystem processes. Aquatic Ecology , 31 (4): 349-359, https://doi.org/10.1023/A:1009924624259..

Ragueneau O, Dittert N, Pondaven P, Tréguer P, Corrin L. 2002. Si/C decoupling in the world ocean: is the Southern Ocean different? Deep Sea Research Part Ⅱ : Topical Studies in Oceanography , 49 (16): 3127-3154, https://doi.org/10.1016/S0967-0645(02)00075-9..

Ragueneau O, Savoye N, Amo Y D, Cotten J, Tardiveau B, Leynaert A. 2005. A new method for the measurement of biogenic silica in suspended matter of coastal waters: using Si: Al ratios to correct for the mineral interference. Continental Shelf Research , 25 (5-6): 697-710, https://doi.org/10.1016/j.csr.2004.09.017..

Ragueneau O, Tréguer P. 1994. Determination of biogenic silica in coastal waters: applicability and limits of the alkaline digestion method. Marine Chemistry , 45 (1-2): 43-51, https://doi.org/10.1016/0304-4203(94)90090-6..

Reinfelder J R, Fisher N S. 1991. The assimilation of elements ingested by marine copepods. Science , 251 (4995): 794-796, https://doi.org/10.1126/science.251.4995.794..

Roubeix V, Becquevort S, Lancelot C. 2008. Influence of bacteria and salinity on diatom biogenic silica dissolution in estuarine systems. Biogeochemistry , 88 (1): 47-62, https://doi.org/10.1007/s10533-008-9193-8..

Saad E M, Pickering R A, Shoji K, Hossain M I, Glover T G, Krause J W, Tang Y Z. 2020. Effect of cleaning methods on the dissolution of diatom frustules. Marine Chemistry , 224 : 103826, https://doi.org/10.1016/j.marchem.2020.103826..

Schmidt K, Schlosser C, Atkinson A, Fielding S, Venables H J, Waluda C M, Achterberg E P. 2016. Zooplankton gut passage mobilizes lithogenic iron for ocean productivity. Current Biology , 26 (19): 2667-2673, https://doi.org/10.1016/j.cub.2016.07.058..

Schmitz O J, Hawlena D, Trussell G C. 2010. Predator control of ecosystem nutrient dynamics. Ecology Letters , 13 (10): 1199-1209, https://doi.org/10.1111/j.1461-0248.2010.01511.x..

Smaal A C, Verbagen J H G, Coosen J, Haas H A. 1986. Interaction between seston quantity and quality and benthic suspension feeders in the Oosterschelde, the Netherlands. Ophelia , 26 (1): 385-399, https://doi.org/10.1080/00785326.1986.10422002..

Štrus J, Žnidaršič N, Mrak P, Bogataj U, Vogt G. 2019. Structure, function and development of the digestive system in malacostracan crustaceans and adaptation to different lifestyles. Cell and Tissue Research , 377 (3): 415-443, https://doi.org/10.1007/s00441-019-03056-0..

Sun X L, Olofsson M, Andersson P S, Fry B, Legrand C, Humborg C, Mörth C M. 2014. Effects of growth and dissolution on the fractionation of silicon isotopes by estuarine diatoms. Geochimica et Cosmochimica Acta , 130 : 156-166, https://doi.org/10.1016/j.gca.2014.01.024..

Tande K S, Slagstad D. 1985. Assimilation efficiency in herbivorous aquatic organisms—The potential of the ratio method using 14 C and biogenic silica as markers. Limnology and Oceanography , 30 (5): 1093-1099, https://doi.org/10.4319/lo.1985.30.5.1093..

Tang K W, Glud R N, Glud A, Rysgaard S, Nielsen T G. 2011. Copepod guts as biogeochemical hotspots in the sea: evidence from microelectrode profiling of Calanus spp. Limnology and Oceanography , 56 (2): 666-672, https://doi.org/10.4319/lo.2011.56.2.0666..

Tirelli V, Mayzaud P. 2005. Relationship between functional response and gut transit time in the calanoid copepod Acartia clausi : role of food quantity and quality. Journal of Plankton Research , 27 (6): 557-568, https://doi.org/10.1093/plankt/fbi031..

Tsuchiya M. 1980. Biodeposit production by the mussel Mytilus edulis L. on rocky shores. Journal of Experimental Marine Biology and Ecology , 47 (3): 203-222, https://doi.org/10.1016/0022-0981(80)90039-8..

Valdés V P, Fernandez C, Molina V, Escribano R, Joux F. 2017. Dissolved compounds excreted by copepods reshape the active marine bacterioplankton community composition. Frontiers in Marine Science , 4 : 343 https://doi.org/10.3389/fmars.2017.00343..

Van Broekhoven W, Jansen H, Verdegem M, Struyf E, Troost K, Lindeboom H, Smaal A. 2015. Nutrient regeneration from feces and pseudofeces of mussel Mytilus edulis spat. Marine Ecology Progress Series , 534 : 107-120, https://doi.org/10.3354/meps11402..

Van Broekhoven W, Troost K, Jansen H, Smaal A. 2014. Nutrient regeneration by mussel Mytilus edulis spat assemblages in a macrotidal system. Journal of Sea Research , 88 : 36-46, https://doi.org/10.1016/j.seares.2013.12.007..

Vandevenne F I, Barão A L, Schoelynck J, Smis A, Pyken N, Van Damme S, Meire P, Struyf E. 2013. Grazers: biocatalysts of terrestrial silica cycling. Proceedings of the Royal Society B Biological Sciences , 280 (1772): 2013-2083, https://doi.org/10.1098/rspb.2013.2083..

Vanni M J. 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics , 33 : 341-370, https://doi.org/10.1146/annurev.ecolsys.33.010802.150519..

Wang J, Wang W X. 2016. Novel insights into iron regulation and requirement in marine medaka Oryzias melastigma . Scientific Reports , 6 (1): 26615, https://doi.org/10.1038/srep26615..

Wang W X, Fisher N S. 1999. Delineating metal accumulation pathways for marine invertebrates. Science of the Total Environment , 237-238 : 459-472, https://doi.org/10.1016/S0048-9697(99)00158-8..

Wang W X, Qiu J W, Qian P Y. 1999. The trophic transfer of Cd, Cr, and Se in the barnacle Balanus amphitrite from planktonic food. Marine Ecology Progress Series , 187 : 191-201, https://doi.org/10.3354/meps187191..

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