A large invasive consumer reduces coastal ecosystem resilience by disabling positive species interactions
1.Vilà, M. et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14, 702–708 (2011).PubMed
Article
PubMed Central
Google Scholar
2.Vitousek, P. M., DAntonio, C. M., Loope, L. L., Westbrooks, R. & D’Antonio, C. M. Biological invasions as global environmental change. Am. Sci. 84, 468–478 (1996).ADS
Google Scholar
3.Pejchar, L. & Mooney, H. A. Invasive species, ecosystem services and human well-being. Trends Ecol. Evol. 24, 497–504 (2009).PubMed
Article
Google Scholar
4.Ehrenfeld, J. G. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Evol. Syst. 41, 59–80 (2010).Article
Google Scholar
5.Doherty, T. S., Glen, A. S., Nimmo, D. G., Ritchie, E. G. & Dickman, C. R. Invasive predators and global biodiversity loss. Proc. Natl Acad. Sci. USA 113, 11261–11265 (2016).CAS
PubMed
PubMed Central
Article
Google Scholar
6.Gallardo, B., Clavero, M., Sánchez, M. I. & Vilà, M. Global ecological impacts of invasive species in aquatic ecosystems. Glob. Change Biol. 22, 151–163 (2016).ADS
Article
Google Scholar
7.Didham, R. K., Tylianakis, J. M., Hutchison, M. A., Ewers, R. M. & Gemmell, N. J. Are invasive species the drivers of ecological change? Trends Ecol. Evol. 20, 470–474 (2005).PubMed
Article
Google Scholar
8.Simberloff, D. How common are invasion-induced ecosystem impacts? Biol. Invasions 13, 1255–1268 (2011).Article
Google Scholar
9.Guy-Haim, T. et al. Diverse effects of invasive ecosystem engineers on marine biodiversity and ecosystem functions: a global review and meta-analysis. Glob. Change Biol. https://doi.org/10.1111/gcb.14007 (2018).10.Vander Zanden, M. J., Casselman, J. M. & Rasmussen, J. B. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401, 464–467 (1999).ADS
Article
CAS
Google Scholar
11.Bartomeus, I., Vilà, M. & Santamaría, L. Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155, 761–770 (2008).ADS
PubMed
Article
PubMed Central
Google Scholar
12.Aizen, M. A., Morales, C. L. & Morales, J. M. Invasive mutualists erode native pollination webs. PLoS Biol. 6, 0396–0403 (2008).CAS
Article
Google Scholar
13.Olesen, J. M., Eskildsen, L. I. & Venkatasamy, S. Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Divers. Distrib. 8, 181–192 (2002).Article
Google Scholar
14.Carvalheiro, L. G., Barbosa, E. R. M. & Memmott, J. Pollinator networks, alien species and the conservation of rare plants: Trinia glauca as a case study. J. Appl. Ecol. 45, 1419–1427 (2008).Article
Google Scholar
15.Anderson, C. B., Griffith, C. R., Rosemond, A. D., Rozzi, R. & Dollenz, O. The effects of invasive North American beavers on riparian plant communities in Cape Horn, Chile. Biol. Conserv. 128, 467–474 (2006).Article
Google Scholar
16.Walsh, J. R., Carpenter, S. R. & Vander Zanden, M. J. Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc. Natl Acad. Sci. USA 113, 201600366 (2016).
Google Scholar
17.Wiles, G. J., Bart, J., Beck, R. E. & Aguon, C. F. Impacts of the Brown Tree Snake: patterns of decline and species persistence in Guam’s Avifauna. Conserv. Biol. 17, 1350–1360 (2003).Article
Google Scholar
18.Ludyanskiy, M., McDonald, D. & MacNeill, D. Impact of the Zebra Mussei, a Bivalve Invader. BioScience 43, 533–544 (1993).Article
Google Scholar
19.Byrnes, J. E., Reynolds, P. L. & Stachowicz, J. J. Invasions and extinctions reshape coastal marine food webs. PLoS ONE 2, 1–7 (2007).Article
Google Scholar
20.Bruno, J. F., Stachowicz, J. J. & Bertness, M. D. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18, 119–125 (2003).Article
Google Scholar
21.Stachowicz, J. J. Mutualism, facilitation, and the structure of ecological communities. BioScience 51, 235 (2001).Article
Google Scholar
22.Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B Biol. Sci. 273, 2305–2312 (2006).Article
Google Scholar
23.Bulleri, F., Bruno, J. F., Silliman, B. R. & Stachowicz, J. J. Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Funct. Ecol. 30, 70–78 (2016).Article
Google Scholar
24.Angelini, C. et al. 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 (2015).Article
Google Scholar
25.Anthelme, F., Cavieres, L. A. & Dangles, O. Facilitation among plants in alpine environments in the face of climate change. Front. Plant Sci. 5 (2014).26.Angelini, C. & Silliman, B. R. Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree-epiphyte system. Ecology 95, 185–196 (2014).PubMed
Article
PubMed Central
Google Scholar
27.van der Heide, T. et al. A three-stage symbiosis forms the foundation of seagrass ecosystems. Science 336, 1432–1434 (2012).ADS
PubMed
Article
CAS
PubMed Central
Google Scholar
28.Nummi, P. & Holopainen, S. Whole-community facilitation by beaver: ecosystem engineer increases waterbird diversity: ecosystem engineer increases waterbird diversity. Aquat. Conserv. Mar. Freshw. Ecosyst. 24, 623–633 (2014).Article
Google Scholar
29.Rosell, F., Bozser, O., Collen, P. & Parker, H. Ecological impact of beavers Castor fiber and Castor canadensis and their ability to modify ecosystems. Mammal. Rev. 35, 248–276 (2005).Article
Google Scholar
30.He, Q., Bertness, M. D. & Altieri, A. H. Global shifts towards positive species interactions with increasing environmental stress. Ecol. Lett. 16, 695–706 (2013).PubMed
Article
PubMed Central
Google Scholar
31.Schuerch, M. et al. Future response of global coastal wetlands to sea-level rise. Nature 561, 231–234 (2018).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
32.Jackson, J. B. et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).CAS
PubMed
Article
PubMed Central
Google Scholar
33.Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
34.Lotze, H. K. et al. Depletion, degredation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809 (2006).ADS
CAS
Article
Google Scholar
35.Grosholz, E. Ecological and evolutionary consequences of coastal invasions. Trends Ecol. Evol. 17, 22–27 (2002).Article
Google Scholar
36.Syvitski, J. P. M. et al. Sinking deltas due to human activities. Nat. Geosci. 2, 681–686 (2009).ADS
CAS
Article
Google Scholar
37.He, Q. & Silliman, B. R. Climate change, human impacts, and coastal ecosystems in the anthropocene. Curr. Biol. 29, R1021–R1035 (2019).CAS
PubMed
Article
PubMed Central
Google Scholar
38.Barbier, E. B. et al. The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–193 (2011).Article
Google Scholar
39.Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997).ADS
CAS
Article
Google Scholar
40.Angelini, C. et al. A keystone mutualism underpins resilience of a coastal ecosystem to drought. Nat. Commun. 7, 12473 (2016).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
41.Bruno, J. F. & Bertness, M. D. Habitat modification and facilitation in benthic marine communities. in Marine Community Ecology (eds Bertness, M. D., Gaines, S. & Hay, M.) 201–216 (Sinauer, 2001).42.De Fouw, J. et al. Drought, mutualism breakdown, and landscape-scale degradation of seagrass beds. Curr. Biol. 26, 1051–1056 (2016).PubMed
Article
CAS
Google Scholar
43.Ellison, A. M., Farnsworth, E. J. & Twilley, R. R. Facultative mutualism between red mangroves and root‐fouling sponges in belizean mangal. Ecology https://doi.org/10.2307/2265744 (1996).44.Arkema, K. K. et al. Coastal habitats shield people and property from sea-level rise and storms. Nat. Clim. Change 3, 913–918 (2013).ADS
Article
Google Scholar
45.McKee, K. L., Mendelssohn, I. A. & Materne, M. D. Acute salt marsh dieback in the Mississippi River deltaic plain: a drought-induced phenomenon? Glob. Ecol. Biogeogr. 13, 65–73 (2004).Article
Google Scholar
46.Alber, M., Swenson, E. M., Adamowicz, S. C. & Mendelssohn, I. A. Salt Marsh Dieback: an overview of recent events in the US. Estuar. Coast. Shelf Sci. 80, 1–11 (2008).ADS
Article
Google Scholar
47.Wang, H., Fu, R., Kumar, A. & Li, W. Intensification of summer rainfall variability in the southeastern United States during recent decades. J. Hydrometeorol. 11, 1007–1018 (2010).ADS
Article
Google Scholar
48.Stiven, A. E. & Gardner, S. A. Population processes in the ribbed mussel Geukensia demissa (Dillwyn) in a North Carolina salt marsh tidal gradient: spatial pattern, predation, growth and mortality. J. Exp. Mar. Biol. Ecol. 160, 81–102 (1992).Article
Google Scholar
49.Angelini, C. & Silliman, B. R. Patch size-dependent community recovery after massive disturbance. Ecology 93, 101–110 (2012).PubMed
Article
Google Scholar
50.Mendelssohn, I. & Morris, J. Ecophysiological controls on the productivity of Spartina alterniflora. in Concepts and Controversies in Tidal Marsh Ecology (eds Weinstein, M. & Kreeger, D.) 59–80 (Kluwer Academic Publishers, 1999).51.Bertness, M. D. Ribbed mussels and Spartina alterniflora production in a New England marsh. Ecology 65, 1794–1807 (1984).Article
Google Scholar
52.Siemann, E., Carrillo, J. A., Gabler, C. A., Zipp, R. & Rogers, W. E. Experimental test of the impacts of feral hogs on forest dynamics and processes in the southeastern US. Ecol. Manag. 258, 546–553 (2009).Article
Google Scholar
53.Campbell, T. A. & Long, D. B. Feral swine damage and damage management in forested ecosystems. Ecol. Manag. 257, 2319–2326 (2009).Article
Google Scholar
54.Barrios-Garcia, M. N. & Ballari, S. A. Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol. Invasions 14, 2283–2300 (2012).Article
Google Scholar
55.Graves, H. B. Behavior and ecology of wild and feral swine (Sus-Scrofa). J. Anim. Sci. 58, 482–492 (1984).Article
Google Scholar
56.Wood, G. W. & Roark, N. D. Food habits of feral hogs in coastal South Carolina. J. Wildl. Manag. 44, 506–511 (1980).Article
Google Scholar
57.Sharp, S. J. & Angelini, C. The role of landscape composition and disturbance type in mediating salt marsh resilience to feral hog invasion. Biol. Invasions https://doi.org/10.1007/s10530-019-02018-5 (2019).58.Crotty, S. M. et al. Foundation species patch configuration mediates salt marsh biodiversity, stability and multifunctionality. Ecol. Lett. 21, 1681–1692 (2018).PubMed
Article
PubMed Central
Google Scholar
59.Zhu, Z. et al. Historic storms and the hidden value of coastal wetlands for nature-based flood defence. Nat. Sustain. https://doi.org/10.1038/s41893-020-0556-z (2020).60.Thomsen, M. S. et al. Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integr. Comp. Biol. 50, 158–175 (2010).PubMed
Article
Google Scholar
61.Silliman, B. R. et al. Facilitation shifts paradigms and can amplify coastal restoration efforts. Proc. Natl Acad. Sci. USA 112, 14295–14300 (2015).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
62.Silliman, B. R. et al. Field experiments and meta-analysis reveal wetland vegetation as a crucial element in the coastal protection paradigm. Curr. Biol. 29, 1800–1806 (2019). e3.CAS
PubMed
Article
PubMed Central
Google Scholar
63.Neumann, B., Vafeidis, A. T., Zimmermann, J. & Nicholls, R. J. Future coastal population growth and exposure to sea-level rise and coastal flooding—a global assessment. PLoS ONE 10, e0118571 (2015).PubMed
PubMed Central
Article
CAS
Google Scholar
64.Rogers, K. et al. Wetland carbon storage controlled by millennial-scale variation in relative sea-level rise. Nature 567, 91–95 (2019).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
65.Rogers, H. S. et al. Effects of an invasive predator cascade to plants via mutualism disruption. Nat. Commun. 8, 14557 (2017).ADS
PubMed
PubMed Central
Article
Google Scholar
66.Albins, M. & Hixon, M. Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar. Ecol. Prog. Ser. 367, 233–238 (2008).ADS
Article
Google Scholar
67.Albins, M. Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Mar. Ecol. Prog. Ser. 522, 231–243 (2015).ADS
Article
Google Scholar
68.Ling, S. D. Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156, 883–894 (2008).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
69.Johnson, C. R. et al. Climate change cascades: shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. J. Exp. Mar. Biol. Ecol. 400, 17–32 (2011).Article
Google Scholar
70.Ling, S. D., Johnson, C. R., Frusher, S. D. & Ridgway, K. R. Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc. Natl Acad. Sci. USA 106, 22341–22345 (2009).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
71.Persico, E. P., Sharp, S. J. & Angelini, C. Feral hog disturbance alters carbon dynamics in southeastern US salt marshes. Mar. Ecol. Prog. Ser. 580, 57–68 (2017).ADS
CAS
Article
Google Scholar
72.Shaffer, G. P. et al. System response, nutria herbivory, and vegetation recovery of a wetland receiving secondarily-treated effluent in coastal Louisiana. Ecol. Eng. 79, 120–131 (2015).Article
Google Scholar
73.Fleming, P. A. et al. Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function?: loss of Australian digging mammals and ecosystem function. Mammal. Rev. 44, 94–108 (2014).Article
Google Scholar
74.Woinarski, J. C. Z., Burbidge, A. A. & Harrison, P. L. Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc. Natl Acad. Sci. USA 112, 4531–4540 (2015).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
75.Croll, D. A. Introduced predators transform subarctic islands from grassland to tundra. Science 307, 1959–1961 (2005).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
76.Siero, E. et al. Grazing away the resilience of patterned ecosystems. Am. Nat. 193, 472–480 (2019).PubMed
Article
PubMed Central
Google Scholar
77.Crotty, S. M. & Angelini, C. Geomorphology and species interactions control facilitation cascades in a salt marsh ecosystem. Curr. Biol. 30, 1562–1571.e4 (2020).CAS
PubMed
Article
PubMed Central
Google Scholar
78.Geisser, H. & Reyer, H.-U. Efficacy of hunting, feeding, and fencing to reduce crop damage by wild boars. J. Wildl. Manag. 68, 939–946 (2004).Article
Google Scholar
79.Engeman, R. M. et al. Feral swine management for conservation of an imperiled wetland habitat: Florida’s vanishing seepage slopes. Biol. Conserv. 134, 440–446 (2007).Article
Google Scholar
80.Bevins, S. N., Pedersen, K., Lutman, M. W., Gidlewski, T. & Deliberto, T. J. Consequences associated with the recent range expansion of nonnative feral swine. BioScience 64, 291–299 (2014).Article
Google Scholar
81.McClure, M. L. et al. Modeling and mapping the probability of occurrence of invasive wild pigs across the contiguous United States. PLoS ONE 10, 1–17 (2015).
Google Scholar
82.Oldfield, C. A. & Evans, J. P. 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 (2016).PubMed
PubMed Central
Article
Google Scholar
83.Ford, M. A. & Grace, J. B. Effects of vertebrate herbivores on soil processes, plant biomass, litter accumulation and soil elevation changes in a coastal marsh. J. Ecol. 86, 974–982 (1998).Article
Google Scholar
84.Hensel, M. J. S. & Silliman, B. R. Consumer diversity across kingdoms supports multiple functions in a coastal ecosystem. Proc. Natl Acad. Sci. USA 110, 20621–20626 (2013).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
85.Silliman, B. R. et al. Are the ghosts of nature’s past haunting ecology today? Curr. Biol. 28, R532–R537 (2018).CAS
PubMed
Article
PubMed Central
Google Scholar
86.Morse, N. B. et al. Novel ecosystems in the Anthropocene: a revision of the novel ecosystem concept for pragmatic applications. Ecol. Soc. 19, art12 (2014).Article
Google Scholar
87.Goigel Turner, M. Effects of grazing by feral horses, clipping, trampling, and burning on a Georgia salt marsh. Estuaries. 10, 54–60 (2014).Article
Google Scholar
88.Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.4.4. https://CRAN.R-project.org/package=DHARMa (2021).89.R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2017).90.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article
Google Scholar
91.Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article
Google Scholar
92.AgiSoft PhotoScan Professional. (AgiSoft, 2016).93.Rasband, W. S. ImageJ. (U.S. National Institutes of Health, 1997).94.Kuenzler, E. J. Structure and energy flow of a mussel population in a Georgia salt marsh. Limnol. Oceanogr. 6, 191–204 (1961).ADS
Article
Google Scholar
95.Length, R. V. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.0. https://CRAN.R-project.org/package=emmeans (2021).96.Guichard, F., Halpin, P. M., Allison, G. W., Lubchenco, J. & Menge, B. A. Mussel disturbance dynamics: signatures of oceanographic forcing from local interactions. Am. Nat. 161, 889–904 (2003).PubMed
Article
PubMed Central
Google Scholar
97.Silliman, B. R., van de Koppel, J., Bertness, M. D., Stanton, L. E. & Mendelssohn, I. A. Drought, snails, and large-scale die-off of southern U.S. salt marshes. Science 310, 1803–1806 (2005).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar More