Crabs assimilating cellulose materials drive the detritus food chain in a mangrove estuary

Kawaida, Shun; Nanjo, Kishio; Ohtsuchi, Naoya; Kohno, Hiroyoshi; Sano, Mitsuhiko

doi:10.1016/j.fooweb.2020.e00180

Cited by 4 publications

(3 citation statements)

References 24 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In addition, endogenous enzymes in the digestive organs have been identified in a wide variety of invertebrates [34,36] including mangrove crabs [37][38][39]. Analysis of sesarmid mangrove crabs has shown that mangrove litter fragments dominate (often over 90%) in stomach contents, and stable isotope technique analysis supported that leaf litter is the main carbon source for sesarmid crabs [11,40,41]. On the other hand, the assimilation efficiency of litter by crabs is not high, and the remaining fragmented matter is released as feces [42][43][44].…”

Section: Introductionmentioning

confidence: 99%

Mangrove crab intestine and habitat sediment microbiomes cooperatively work on carbon and nitrogen cycling

et al. 2021

View full text Add to dashboard Cite

Mangrove ecosystems, where litter and organic components are degraded and converted into detrital materials, support rich coastal fisheries resources. Sesarmid (Grapsidae) crabs, which feed on mangrove litter, play a crucial role in material flow in carbon-rich and nitrogen-limited mangrove ecosystems; however, the process of assimilation and conversion into detritus has not been well studied. In this study, we performed microbiome analyses of intestinal bacteria from three species of mangrove crab and five sediment positions in the mud lobster mounds, including the crab burrow wall, to study the interactive roles of crabs and sediment in metabolism. Metagenome analysis revealed species-dependent intestinal profiles, especially in Neosarmatium smithi, while the sediment microbiome was similar in all positions, albeit with some regional dependency. The microbiome profiles of crab intestines and sediments were significantly different in the MDS analysis based on OTU similarity; however, 579 OTUs (about 70% of reads in the crab intestinal microbiome) were identical between the intestinal and sediment bacteria. In the phenotype prediction, cellulose degradation was observed in the crab intestine. Cellulase activity was detected in both crab intestine and sediment. This could be mainly ascribed to Demequinaceae, which was predominantly found in the crab intestines and burrow walls. Nitrogen fixation was also enriched in both the crab intestines and sediments, and was supported by the nitrogenase assay. Similar to earlier reports, sulfur-related families were highly enriched in the sediment, presumably degrading organic compounds as terminal electron acceptors under anaerobic conditions. These results suggest that mangrove crabs and habitat sediment both contribute to carbon and nitrogen cycling in the mangrove ecosystem via these two key reactions.

show abstract

Section: Introductionmentioning

confidence: 99%

Mangrove crab intestine and habitat sediment microbiomes cooperatively work on carbon and nitrogen cycling

et al. 2021

View full text Add to dashboard Cite

show abstract

“…By shredding or burying leaves (Lee, 1989a;Robertson and Daniel, 1989;Camilleri, 1992;Emmerson and McGwynne, 1992;Skov and Hartnoll, 2002;Mfilinge and Tsuchiya, 2008;Harada and Lee, 2016), they exert great impact on mangrove production and nutrient dynamics, with some species removing large proportions of mangrove leaf litter production (Robertson and Daniel, 1989;Emmerson and McGwynne, 1992;Harada and Lee, 2016). These crabs such as Parasesarma bidens connect mangrove and higher trophic levels by acting as prey to predators such as fish, thus linking mangrove and coastal food chains (Sheaves and Molony, 2000;Kawaida et al, 2021). Alternatively, they transform mangrove production into faecal material with improved nutritional value that may be readily assimilated by deposit-feeders such as fiddler crabs or suspension-feeders such as copepods (Lee, 1997;Werry and Lee, 2005).…”

Section: Introductionmentioning

confidence: 99%

Widespread occurrence of endogenous cellulase production and glycosyl hydrolase in grapsoid crabs along the land-sea transition indicates high potential for mineralisation of mangrove production

Lee

Lee²

2022

Front. Mar. Sci.

View full text Add to dashboard Cite

Previous studies on mangrove carbon utilisation and mineralisation were focused on mangrove sesarmid crabs (Grapsoidea: Sesarmidae) because they are initial processors of mangrove organic carbon. Grapsoid crabs from other families and habitats were generally ignored although they also perform various levels of herbivory. It remains unclear how the herbivorous crabs utilise the production from mangrove or vascular plants because of the high C/N ratio and high structural carbon content of these materials. In this study, production of cellulase and expression of hepatopancreatic glycosyl hydrolase of grapsoid crabs were investigated in a more extensive way in terms of their taxa (15 species) and habitats (i.e., land margin, mangrove, mudflat, and subtidal area). Generally, low gastric endoglucanase (1.46-2.98 μmol min−1 ml−1) and β-glucosidase (0.06-0.61 μmol min−1 ml−1) activity was detected in 15 grapsoid crabs distributed along the land-sea transition. The activity of both enzymes was significantly affected by the taxonomic affiliation and habitat of the crabs: endoglucanase in sesarmids > varunids > grapsids; and land margin, mangrove and limnic habitats > mudflat and subtidal area. For β-glucosidase: sesarmids > varunids and grapsids; and land and limnic > mangrove and subtidal > mudflat. Our detection of gastric cellulases in mudflat and subtidal grapsoid crabs has rarely been reported. These results show that there is a need to re-evaluate the role of crabs from these habitats in mangrove/vascular plant carbon mineralisation. Further, low cellulase activity could be a common trait among crabs along the land-sea transition and the importance of cellulase in vascular plant carbon utilisation could have been previously over-rated. Glycosyl hydrolase family 9 (GH9) genes were identified in the hepatopancreatic transcriptome of all 15 species, indicating endogenous production of cellulase. In addition, the presence of other digestive carbohydrate-active enzymes (CAZymes), including GH5_10, GH13, GH13_24, and GH16, suggests that a capacity for the utilisation of carbon sources other than cellulose by the grapsoid crabs, which may enable sufficient assimilation of vascular plant carbon despite the low cellulase activity.

show abstract

“…The trophic significance of leaf-eating crabs is twofold: (1) removal of leaves from the forest floor and therefore reduction in tidal export to the estuary, leading to N retention; and (2) processing of leaf litter to fine sized particles, which can more readily be mineralized by microbes and utilized by detritivores (Werry and Lee, 2005). Leaf-eating crabs digesting/assimilating mangrove detritus also play an important role in acting as a trophic intermediate between hard-to-digest detritus and higher-level consumers in mangrove ecosystems, as they are preyed upon by higher consumers such as fish (Sheaves and Molony, 2000;Lee, 2008;Kawaida et al, 2021;Robertson, 2021).…”

Section: Ecological Role Of Sesarmid Crabs In Mangrove N Dynamicsmentioning

confidence: 99%

Feeding Strategies of Mangrove Leaf-Eating Crabs for Meeting Their Nitrogen Needs on a Low-Nutrient Diet

Gao

Lee

2022

Front. Mar. Sci.

View full text Add to dashboard Cite

Sesarmid crabs play an important role in mangrove biogeochemical processes due to their leaf-eating and burrowing activities. How leaf-eating mangrove crabs meet their nitrogen (N) needs remains a puzzle, as N-poor leaf litter (<1% dry weight) cannot support the growth of most macrofauna. Several strategies for overcoming this challenge have been proposed, but the actual mechanisms remain unknown. We identified two categories of leaf-eating crabs according to their feeding habits (1): species active outside their burrows during low tide - we hypothesize that they meet their N needs through consuming the microphytobenthos (MPB) (hypothesis H1); and (2) species spending most of their time inside burrows - we hypothesize that they meet their N needs through N-fixation by associated microbes (H2). To test H1, we conducted a series of feeding experiments on the sesarmid crab Parasesarma affine (model species for category 1) with 13C- and 15N-enriched MPB and mangrove leaves. P. affine relied mainly on mangrove leaves as their C source and MPB as their N source, supporting H1. Two feeding experiments on Neosarmatium smithi (model species for category 2) showed that N limitation could be ameliorated by selecting seasonally available higher-quality food items such as floral parts, or by supplements from the associated nitrogen-fixing bacteria, as identified by genomic analysis. The strategy by which leaf-eating crabs meet their N needs may make significant contribution both to the growth of crabs and to their ecosystem functions of regulating the cycling of significant nutrient elements. The stoichiometric regulations by leaf-eating crabs to meet their N needs, such as food selection, can enhance trophic efficiency and nutrient transfer rate at the community level and ultimately increase nutrient turnover rate at the ecosystem level.

show abstract

Crabs assimilating cellulose materials drive the detritus food chain in a mangrove estuary

Cited by 4 publications

References 24 publications

Mangrove crab intestine and habitat sediment microbiomes cooperatively work on carbon and nitrogen cycling

Mangrove crab intestine and habitat sediment microbiomes cooperatively work on carbon and nitrogen cycling

Widespread occurrence of endogenous cellulase production and glycosyl hydrolase in grapsoid crabs along the land-sea transition indicates high potential for mineralisation of mangrove production

Feeding Strategies of Mangrove Leaf-Eating Crabs for Meeting Their Nitrogen Needs on a Low-Nutrient Diet

Contact Info

Product

Resources

About