Abstract
Mutualisms enhance ecosystem biodiversity, functioning, and service provisioning through direct and indirect positive interactions. However, invasive species can interrupt mutualisms and disrupt ecosystem functions when they affect foundation species and their keystone mutualist partners. In the southeastern US, mussels aggregate around cordgrass stems, a keystone mutualist-foundation species interaction that controls marsh structure, function, and resilience. Invasive hogs trample cordgrass and consume mussels, yet the multi-scale effects of this mutualism disruption remain uncertain. Here, we quantified the effects of hog-mediated mutualism disruption on four critical ecosystem functions: cordgrass biomass, macroinvertebrate biomass, denitrification, and sediment deposition. We compared a hog-disturbed marsh (27% area disturbed) and a hog-free marsh (0.05% disturbed) and experimentally demonstrated that hog predation causes the observed 93% reduction in mussels on the hog marsh. Plot-scale measurements revealed that hog trampling of cordgrass doubles net denitrification rates but decreases cordgrass biomass, crab biomass, and sediment deposition by 74%, 80% and 55%, respectively, relative to areas without hogs. Mussels stimulate cordgrass biomass, crab biomass, denitrification, and sediment deposition by 19%, 39%, 134% and 140%, effects that are only evident in the mussel-dense hog-free marsh. Using hog damage and mussel cover surveys to extrapolate plot-scale measurements to the 20 m2 scale, we estimate that hogs stimulate cordgrass biomass and denitrification by 27% and 5% but, by driving mussel loss, depress crab biomass and sediment deposition by 48% and 38%. Disruption of the cordgrass-mussel mutualism by invasive hogs alters ecosystem functioning, modifications which will likely affect marsh ecosystem service provisioning and resilience region-wide.
Graphical abstract
Similar content being viewed by others
Data availability
Datasets generated during this study are included as Online Resource 3. At the conclusion of the project, data will be publicly archived with the NOAA Centralized Data Management Office.
References
Albins MA (2015) Invasive pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar Ecol Prog Ser 522:231–243. https://doi.org/10.3354/meps11159
Andresen H, Bakker JP, Brongers M et al (1990) Long-term changes of salt marsh communities by cattle grazing. Vegetatio 89:137–148. https://doi.org/10.1007/BF00032166
Angelini C, Griffin JN, van de Koppel J et al (2016) A keystone mutualism underpins resilience of a coastal ecosystem to drought. Nat Commun 7:12473. https://doi.org/10.1038/ncomms12473
Angelini C, van der Heide T, Griffin JN et al (2015) Foundation species’ overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes. Proc R Soc B: Biol Sci 282:20150421. https://doi.org/10.1098/rspb.2015.0421
Bakker JP, Schrama M, Esselink P et al (2020) Long-term effects of sheep grazing in various densities on marsh properties and vegetation dynamics in two different salt-marsh zones. Estuar Coasts 43:298–315. https://doi.org/10.1007/s12237-019-00680-5
Barbier EB, Hacker SD, Kennedy C et al (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193. https://doi.org/10.1890/10-1510.1
Baron J (1982) Effects of feral hogs (Sus scrofa) on the vegetation of Horn island, Mississippi. Am Midl Nat 107:202–205. https://doi.org/10.2307/2425204
Barrios-Garcia MN, Ballari SA (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14:2283–2300. https://doi.org/10.1007/s10530-012-0229-6
Baustian JJ, Mendelssohn IA, Hester MW (2012) Vegetation’s importance in regulating surface elevation in a coastal salt marsh facing elevated rates of sea level rise. Glob Change Biol 18:3377–3382. https://doi.org/10.1111/j.1365-2486.2012.02792.x
Berthelsen AK, Taylor RB (2014) Arthropod mesograzers reduce epiphytic overgrowth of subtidal coralline turf. Mar Ecol Prog Ser 515:123–132. https://doi.org/10.3354/meps11025
Bertness MD (1984) Ribbed mussels and Spartina Alterniflora production in a New England salt marsh. Ecology 65:1794–1807. https://doi.org/10.2307/1937776
Bertness MD, Grosholz E (1985) Population dynamics of the ribbed mussel, Geukensia demissa: the costs and benefits of an aggregated distribution. Oecologia 67:192–204. https://doi.org/10.1007/BF00384283
Bertness MD, Holdredge C, Altieri AH (2009) Substrate mediates consumer control of salt marsh cordgrass on Cape Cod, New England. Ecology 90:2108–2117. https://doi.org/10.1890/08-1396.1
Bilkovic DM, Mitchell MM, Isdell RE et al (2017) Mutualism between ribbed mussels and cordgrass enhances salt marsh nitrogen removal. Ecosphere 8:e01795. https://doi.org/10.1002/ecs2.1795
Bond W, Slingsby P (1984) Collapse of an Ant-plant mutalism: the argentine ant (Iridomyrmex Humilis) and myrmecochorous proteaceae. Ecology 65:1031–1037. https://doi.org/10.2307/1938311
Breland TA, Hansen S (1996) Nitrogen mineralization and microbial biomass as affected by soil compaction. Soil Biol Biochem 28:655–663. https://doi.org/10.1016/0038-0717(95)00154-9
Bromberg Gedan K, Silliman BR, Bertness MD (2009) Centuries of human-driven change in salt marsh ecosystems. Ann Rev Mar Sci 1:117–141. https://doi.org/10.1146/annurev.marine.010908.163930
Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 201–218
Crain CM, Halpern BS, Beck MW, Kappel CV (2009) Understanding and managing human threats to the coastal marine environment. Ann N Y Acad Sci 1162:39–62. https://doi.org/10.1111/j.1749-6632.2009.04496.x
Crotty SM, Pinton D, Canestrelli A et al (2023) Faunal engineering stimulates landscape-scale accretion in southeastern US salt marshes. Nat Commun 14:1–15. https://doi.org/10.1038/s41467-023-36444-w
Crotty SM, Sharp SJ, Bersoza AC et al (2018) Foundation species patch configuration mediates salt marsh biodiversity, stability and multifunctionality. Ecol Lett 21:1681–1692
Dayton PK (1972) Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. In: Proceedings of the colloquium on conservation problems in Antarctica. Blacksberg, VA, p 81–96
Derksen-Hooijberg M, Angelini C, Lamers LPM et al (2018) Mutualistic interactions amplify saltmarsh restoration success. J Appl Ecol 55:405–414. https://doi.org/10.1111/1365-2664.12960
Derksen-Hooijberg M, van der Heide T, Lamers LP et al (2019) Burrowing crabs weaken mutualism between foundation species. Ecosystems 22:767–780
Doane TA, Horwáth WR (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722. https://doi.org/10.1081/AL-120024647
Elschot K, Bouma TJ, Temmerman S, Bakker JP (2013) Effects of long-term grazing on sediment deposition and salt-marsh accretion rates. Estuar Coast Shelf Sci 133:109–115. https://doi.org/10.1016/j.ecss.2013.08.021
Eriksson B, Eldridge DJ (2014) Surface destabilisation by the invasive burrowing engineer Mus musculus on a sub-Antarctic island. Geomorphology 223:61–66. https://doi.org/10.1016/j.geomorph.2014.06.026
Giuliano WM (2010) Wild hogs in Florida: ecology and management. EDIS 2010
Grimes BH, Pendleton EC (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (mid-Atlantic): Atlantic marsh fiddler. The Service
Hay ME, Parker JD, Burkepile DE et al (2004) Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annu Rev Ecol Evol Syst 35:175–197. https://doi.org/10.1146/annurev.ecolsys.34.011802.132357
Hensel MJS, Silliman BR, Hensel E, Byrnes JEK (2021a) Feral hogs control brackish marsh plant communities over time. Ecology. https://doi.org/10.1002/ecy.3572
Hensel MJS, Silliman BR, van de Koppel J et al (2021b) A large invasive consumer reduces coastal ecosystem resilience by disabling positive species interactions. Nat Commun 12:6290. https://doi.org/10.1038/s41467-021-26504-4
Hoogsteen MJJ, Lantinga EA, Bakker EJ et al (2015) Estimating soil organic carbon through loss on ignition: effects of ignition conditions and structural water loss. Eur J Soil Sci 66:320–328. https://doi.org/10.1111/ejss.12224
Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out-compete their native conspecifics? J Appl Ecol 43:940–948
Jordan TE, Valiela I (1982) A nitrogen budget of the ribbed mussel, Geukensia demissa, and its significance in nitrogen flow in a New England salt marsh1. Limnol Oceanogr 27:75–90. https://doi.org/10.4319/lo.1982.27.1.0075
Kana TM, Darkangelo C, Hunt MD et al (1994) Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66:4166–4170. https://doi.org/10.1021/ac00095a009
Lotze HK, Lenihan HS, Bourque BJ et al (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809. https://doi.org/10.1126/science.1128035
Manis JE, Garvis SK, Jachec SM, Walters LJ (2015) Wave attenuation experiments over living shorelines over time: a wave tank study to assess recreational boating pressures. J Coast Conserv 19:1–11. https://doi.org/10.1007/s11852-014-0349-5
McKee KL, Patrick WH (1988) The relationship of smooth cordgrass (Spartina alterniflora) to tidal datums: a review. Estuaries 11:143–151. https://doi.org/10.2307/1351966
Miller-Way T, Twilley RR (1996) Theory and operation of continuous flow systems for the study of benthic-pelagic coupling. Mar Ecol Prog Ser 140:257–269. https://doi.org/10.3354/meps140257
Minchinton TE, Shuttleworth HT, Lathlean JA et al (2019) Impacts of cattle on the vegetation structure of mangroves. Wetlands 39:1119–1127. https://doi.org/10.1007/s13157-019-01143-0
Morales CL, Arbetman MP, Cameron SA, Aizen MA (2013) Rapid ecological replacement of a native bumble bee by invasive species. Front Ecol Environ 11:529–534
Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563. https://doi.org/10.1016/j.tree.2008.06.011
Negrin VL, de Villalobos AE, Trilla GG et al (2012) Above- and belowground biomass and nutrient pools of Spartina alterniflora (smooth cordgrass) in a south American salt marsh. Chem Ecol 28:391–404. https://doi.org/10.1080/02757540.2012.666529
NOAA Tides & Currents Relative Sea Level Trend 8720218 Mayport, Florida
Ogle DH, Doll JC, Wheeler P, Dinno A (2021) FSA: fisheries stock Analysis
Oldfield CA, Evans JP (2016) Twelve years of repeated wild hog activity promotes population maintenance of an invasive clonal plant in a coastal dune ecosystem. Ecol Evol 6:2569–2578. https://doi.org/10.1002/ece3.2045
Paavola M, Olenin S, Leppäkoski E (2005) Are invasive species most successful in habitats of low native species richness across European brackish water seas? Estuar Coast Shelf Sci 64:738–750. https://doi.org/10.1016/j.ecss.2005.03.021
Persico E, Sharp S, Angelini C (2017) Feral hog disturbance alters carbon dynamics in southeastern US salt marshes. Mar Ecol Prog Ser 580:57–68. https://doi.org/10.3354/meps12282
Phiri EE, McGeoch MA, Chown SL (2009) Spatial variation in structural damage to a keystone plant species in the sub-Antarctic: interactions between Azorella selago and invasive house mice. Antarct Sci 21:189–196. https://doi.org/10.1017/S0954102008001569
Power ME, Tilman D, Estes JA et al (1996) Challenges in the quest for keystones. Bioscience 46:609–620. https://doi.org/10.2307/1312990
Reed DJ (1989) Patterns of sediment deposition in subsiding coastal salt marshes, Terrebonne Bay, Louisiana: the role of winter storms. Estuaries 12:222–227. https://doi.org/10.2307/1351901
Rodriguez-Cabal MA, Barrios-Garcia MN, Amico GC et al (2013) Node-by-node disassembly of a mutualistic interaction web driven by species introductions. PNAS 110:16503–16507. https://doi.org/10.1073/pnas.1300131110
Rogers HS, Buhle ER, HilleRisLambers J et al (2017) Effects of an invasive predator cascade to plants via mutualism disruption. Nat Commun 8:14557. https://doi.org/10.1038/ncomms14557
Rogers SG, Targett TE, Van Sant SB (1984) Fish-nursery use in georgia salt-marsh estuaries: the influence of springtime freshwater conditions. Trans Am Fish Soc 113:595–606. https://doi.org/10.1577/1548-8659(1984)113%3c595:FUIGSE%3e2.0.CO;2
Shaffer GP, Day JW, Hunter RG et al (2015) System response, nutria herbivory, and vegetation recovery of a wetland receiving secondarily-treated effluent in coastal Louisiana. Ecol Eng 79:120–131. https://doi.org/10.1016/j.ecoleng.2015.04.001
Sharp SJ, Angelini C (2019) The role of landscape composition and disturbance type in mediating salt marsh resilience to feral hog invasion. Biol Invasions 21:2857–2869. https://doi.org/10.1007/s10530-019-02018-5
Sharp SJ, Angelini C (2016) Whether disturbances alter salt marsh soil structure dramatically affects Spartina alterniflora recolonization rate. Ecosphere. https://doi.org/10.1002/ecs2.1540
Smith JM, Frey RW (1985) Biodeposition by the ribbed mussel Geukensia demissa in a salt marsh, Sapelo island, Georgia. J Sediment Res 55:817–828
Smyth AR, Geraldi NR, Piehler MF (2013) Oyster-mediated benthic-pelagic coupling modifies nitrogen pools and processes. Mar Ecol Prog Ser 493:23–30. https://doi.org/10.3354/meps10516
St Johns River Water Management District (2009) SJRWMD 2009 Land cover land use
Thomsen MS, South PM (2019) Communities and Attachment networks associated with primary, secondary and alternative foundation species; a case study of stressed and disturbed stands of southern bull kelp. Diversity 11:56. https://doi.org/10.3390/d11040056
Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216. https://doi.org/10.1016/j.tree.2006.01.006
Wickham H, Averick M, Bryan J et al (2019) Welcome to the tidyverse. J Open Sour Softw 4:1686. https://doi.org/10.21105/joss.01686
Wood GW, Roark DN (1980) Food habits of feral hogs in coastal south Carolina. J Wildl Manag 44:506–511. https://doi.org/10.2307/3807990
Wu F, Pennings SC, Ortals C et al (2021) Disturbance is complicated: headward-eroding saltmarsh creeks produce multiple responses and recovery trajectories. Limnol Oceanogr Lno. https://doi.org/10.1002/lno.11867
Acknowledgements
Field work assistance from Sydney Williams, Julie Grissett, Kristie Perez, Emory Wellman, Donovan Mitchell, Chloe Schwab, and Jonathan Crabill. Lab assistance from Katie Heiden, Gabriela Reyes, and Heather Donnelly. We thank Andrew Altieri for his comments on the manuscript and an anonymous reviewer for their detailed comments.
Funding
Funded by Florida Sea Grant (PD-21-03) and NSF Career Award (#1652628) to C. Angelini, UF/IFAS Early Career Seed Grant, USDA National Institute of Food and Agriculture (Hatch project FLA-TRC-005764), and NOAA NERR Science Collaborative to A. Smyth, and a Ruth D. Turner Fellowship to H. Fischman.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Data collection was performed by HF and AS. Data analysis was performed by HF. The first draft of the manuscript was written by HF and CA, AS provided edits on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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
Fischman, H.S., Smyth, A.R. & Angelini, C. Invasive consumers provoke ecosystem-wide disruption of salt marsh functions by dismantling a keystone mutualism. Biol Invasions 26, 169–185 (2024). https://doi.org/10.1007/s10530-023-03167-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03167-4