Abstract
Many important wetland functions are tied to sediment dynamics, which are influenced by infaunal invertebrate communities. These communities are sensitive to changes in sediment structure and to colonization by non-native species. In a southern California salt marsh, the non-native isopod Sphaeroma quoianum has created dense networks of burrows within the marsh banks. Since this isopod increases erosion in many areas and can change local invertebrate communities, its possible contribution to habitat loss in this already-scarce southern California ecosystem is an important issue. To determine the relationship of S. quoianum to invertebrate community and sediment characteristics, three burrowed transects and one unburrowed transect were surveyed and sampled for invertebrate and sediment cores. This study tested the association between burrows and grain size distribution, sediment carbon content, respiration rates, and invertebrate community composition. Sphaeroma quoianum burrows were correlated with altered invertebrate community composition, decreased carbon content, and steep marsh bluffs. These results highlight the potential susceptibility of salt marsh habitat with steep edges to invasion by non-native species. These results also suggest that S. quoianum invasion of salt marsh habitats can alter native communities and ecosystem functions; thus, incipient invasions should be of concern to managers and ecologists alike.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Sediment parameters (carbon content, respiration rates) and invertebrate parameters (including species list) are available at https://doi.org/10.5281/zenodo.6954329.
Code availability
Not applicable.
References
Anderson M (2008) A new method for non-parametric multivariate analysis of variance. Austral Ecol. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Carlton J (1979) History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. Ph.D. diss, University of California, Davis
Chapman J, Dorman J (1975) Diagnosis, systematics, and notes on Grandidierella japonica (Amphipods: Gammaridea) and its introduction to the Pacific Coast of the United States. Bull South Calif Acad Sci 74:104–108
Coleman D, Hendrix P (2000) Invertebrates as webmasters in ecosystems. CABI Publ, Wallingford UK, p 336
Craft C, Seneca E, Broome S (1991) Loss on ignition and Kjeldahl digestion for estimating organic carbon and total nitrogen in estuarine marsh soils: calibration with dry combustion. Estuaries. https://doi.org/10.2307/1351691
Crooks J (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser. https://doi.org/10.3354/meps162137
Crooks J (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos. https://doi.org/10.1034/j.1600-0706.2002.970201.x
Dauwe B, Herman P, Heip C (1998) Community structure and bioturbation potential of macrofaunal at four North Sea stations with contrasting food supply. Mar Ecol Prog Ser. https://doi.org/10.3354/meps173067
Davidson T (2008) Prevalence and distribution of the introduced burrowing isopod, Sphaeroma quoianum, in the intertidal zone of a temperate northeast Pacific estuary (Isopoda, Flabellifera). Crustaceana 81(2):155–167
Davidson T (2010) Accelerated erosion of saltmarshes infested by the non-native burrowing crustacean Sphaeroma quoianum. Mar Ecology Prog Ser. https://doi.org/10.3354/meps08836
Davidson T, Shanks A, Rumrill S (2010) The composition and density of fauna utilizing burrow microhabitats created by a non-native burrowing crustacean (Sphaeroma quoianum). Biol Invasions. https://doi.org/10.1007/s10530-009-9556-7
Diaz Villanueva V, Albarino R, Canhoto C (2012) Positive effect of shredders on microbial biomass and decomposition in stream microcosms. Freshwater Biol. https://doi.org/10.1111/fwb.12023
Emmerson M (2000) Remedial habitat creation: does Nereis diversicolor play a confounding role in the colonization and establishment of the pioneering saltmarsh plant, Spartina angelica? Helgoland Mar Res. https://doi.org/10.1007/s101520050009
Escapa M, Minkoff D, Perillo G, Iribarne O (2007) Direct and indirect effects of burrowing crab Chasmagnathus granulatus activities on erosion of southwest Atlantic Sarcocornia-dominated marshes. Limnol Oceanogr. https://doi.org/10.4319/lo.2007.52.6.2340
Green P, O’Dowd D, Abbott K, Jeffrey M, Retallick K, Mac Nally R (2011) Invasional meltdown: invader-invader mutualism facilitates a secondary invasion. Ecology. https://doi.org/10.1890/11-0050.1
Hass C, Knott B (1998) Sphaeromatid isopods from the Swan River, western Australia: diversity, distribution, and geographic sources. Crustaceana. https://doi.org/10.1163/156854098X00752
Jones C, Lawton J, Shachak M (1994) Organisms as ecosystem engineers. In: Ecosystem Management. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-4018-1_14
Keller J, Takagi K (2013) Solid-phase organic matter reduction regulates anaerobic decomposition in bog soil. Ecosphere. https://doi.org/10.1890/ES12-00382.1
Keller J, Anthony T, Clark D, Gabriel K, Gamalath D, Kabala R, King J, Medina L, Nguyen M (2015) Soil organic carbon and nitrogen storage in two southern California salt marshes: the role of pre-restoration vegetation. Bull South Calif Acad Sci. https://doi.org/10.3160/0038-3872-114.1.22
Kristensen E (2000) Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia. https://doi.org/10.1023/A:1003980226194
Leeper R, Rhodes B, Kirby M, Scharer K, Carlin J, Hemphill-Haley E, Avnaim-Katav S, MacDonald G, Starratt S, Aranda A (2017) Evidence for coseismic subsidence events in a southern California coastal saltmarsh. Sci Rep. https://doi.org/10.1038/srep44615
Matheson K, McKenzie C, Gregory R, Robichaud D, Bradbury I, Snelgrove P, Rose G (2016) Linking eelgrass decline and impacts on associated fish communities to European green crab Carnicus maenas invasion. Mar Ecology Prog Ser. https://doi.org/10.3354/meps11674
McAtee K, Thorne K, Whitcraft C (2020) Short-term impact of sediment addition on plants and invertebrates in a southern California salt marsh. PLoS ONE 15(11):e0240597. https://doi.org/10.1371/journal.pone.0240597
McLain N, Camargo L, Whitcraft C, Dillon J (2020) Metrics for evaluating inundation impacts on the decomposer communities in a Southern California coastal salt marsh. Wetlands. https://doi.org/10.1007/s13157-020-01361-x
Mermillod-Blondin F, Rosenberg R (2006) Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquat Sci. https://doi.org/10.1007/s00027-006-0858-x
Michaels R, Zieman J (2013) Fiddler crab (Uca spp.) burrows have little effect on surrounding sediment oxygen concentrations. J Exp Mar Bio Ecol. https://doi.org/10.1016/j.jembe.2013.06.020
Neira C, Hopner T (1994) The role of Heteromastus filiformis (Capitellidae, Polychaeta) in organic carbon cycling. Ophelia 39:55–73
Nichols F, Pamatmat M (1988) The ecology of soft-bottom benthos of San Francisco Bay: a community profile. Washington, D.C.: U.S. Fish and Wildlife Service Biological Report 85(7.23)
Nordhaus I, Wolff M (2007) Feeding ecology of the mangrove crab Ucides cordatus (Ocypodidae): food choice, food quality and assimilation efficiency. Mar Biol. https://doi.org/10.1007/s00227-006-0597-5
Otani S, Kozuki Y, Yamanaka R, Sasoka H, Ishiyama T, Okitsu Y, Sasaki H, Fujiki Y (2010) The role of crabs (Macrophthalmus japonicus) burrows on organic carbon cycle in estuarine tidal flat, Japan. Estuar Coast Shelf. https://doi.org/10.1016/j.ecss.2009.07.033
Paramor O, Hughes R (2004) The effects of bioturbation and herbivory by the polychaeta Nereis diversicolor on loss of saltmarsh in south-east England. J Appl Ecol. https://doi.org/10.1111/j.0021-8901.2004.00916.x
Pulmanns N, Diele K, Mehlig U, Nordhaus I (2014) Burrows of the semi-terrestrial crab Ucides cordatus enhance CO2 release in a north Brazilian mangrove forest. PLoS ONE. https://doi.org/10.1371/journal.pone.0109532
Reise K (2002) Sediment mediated species interactions in coastal waters. J Sea Res. https://doi.org/10.1016/S1385-1101(02)00150-8
Rosenberg R, Nilsson H, Diaz R (2001) Response of benthic fauna and changing sediment redox profiles over a hypoxic gradient. Estuar Coast Shelf. https://doi.org/10.1006/ecss.2001.0810
Rotramel G (1972) Iais californica and Sphaeroma quoianum, two symbiotic isopods introduced to California (Isopoda, Janiridae, and Sphaeromatidae). Crustaceana, Suppl III 13:193–197
Sasaki A, Nakao H, Yoshitake S, Nakatsubo T (2014) Effects of the burrowing mud shrimp, Upogebia yokoyai, on carbon flow and microbial activity on a tidal flat. Ecol Res. https://doi.org/10.1007/s11284-014-1149-y
Talley T, Crooks J (2007) Habitat conversion associated with bioeroding marine isopods. Ecosystem engineers: plants to protists. Academic Press, Cambridge, pp 185–202
Talley T, Crooks J, Levin L (2001) Habitat utilization and alteration by the invasive burrowing isopod Sphaeroma quoianum, in California salt marshes. Mar Biol. https://doi.org/10.1007/s002270000472
Tolhurst T, Black K, Shayler S, Mather S, Black I, Baker K, Paterson DM (1999) Measuring the in situ erosion shear stress of intertidal sediments with the cohesive strength meter (CSM). Estuar Coast Shelf. https://doi.org/10.1006/ecss.1999.0512
Wasserstein R, Schirm A, Lazar N (2019) Moving to a World Beyond “p < 0.05.” Am Stat. https://doi.org/10.1080/00031305.2019.1583913
West J, Williams G, Madon S, Zedler J (2003) Integrating spatial and temporal variability into analysis of fish food web linkages in Tijuana Estuary. Environ Biol Fish. https://doi.org/10.1023/A:1025843300415
Whitcraft C, Levin L (2007) Regulation of benthic algal and animal communities by salt marsh plants: impact of shading. Ecology. https://doi.org/10.1890/05-2074
Zajac R, Whitlatch R (1982) Response of estuarine infauna to disturbance II: spatial and temporal variation of succession. Mar Ecol Prog Ser. https://doi.org/10.3354/meps010015
Acknowledgements
We wish to acknowledge the Tongva-Gabrieleno and Acjachemen people whose traditional homelands are the site of this research. We thank the Kirby Lab at California State University Fullerton, Valerie Goodwin, Janet Salazar, Molly Burdick-Whipp, Anita Arenas, and Lisa Mastro for field and lab support. Access to the study site was granted by California Fish and Wildlife as well as the State Lands Commission. We are grateful to the two anonymous reviewers whose suggestions greatly improved this manuscript. This publication was prepared with funding from Disney Resort Disney Worldwide Conservation Fund to the Bolsa Chica Conservancy and CSULB. Funding was provided to Brown by The Society of Wetland Scientists, Bolsa Chica Conservancy, and the Southern California Tuna Club.
Funding
Society of Wetland Scientists Graduate Student Award to MB, Bolsa Chica Conservancy (BCC) to CRW and MB, Disney Corporation to BCC, Southern California Tuna Club Graduate Research Award to MB, CSULB Small Faculty Grant to CRW.
Author information
Authors and Affiliations
Contributions
MB was responsible for project conceptualization, data collection and curation, formal analysis, funding acquisition, investigation, development of methodology, writing the original draft, and revising the subsequent drafts. JK was responsible for project conceptualization, supervision of data collection and curation, assistance with formal analysis, development of methodology, writing the original draft, and subsequent drafts. CRW was responsible for project conceptualization, supervision of data collection and curation, assistance with formal analysis, funding acquisition, investigation, development of methodology, project administration, supervision, writing the original draft, and subsequent drafts.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This product was written in my personal capacity and not as a product of the Alaska Department of Environmental Conservation (ADEC) or the State of Alaska. My affiliation with the ADEC is in no way intended to imply that the ADEC sanctions or endorses my personal activities or my personal viewpoints expressed in this paper.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Brown, M.E., Keller, J.K. & Whitcraft, C.R. Relationship of Sphaeroma quoianum to sediment characteristics and invertebrate community. Biol Invasions 24, 3631–3645 (2022). https://doi.org/10.1007/s10530-022-02867-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-022-02867-7