With preserving the natural state of ecosystems being a priority for conservationists, researchers have attempted to determine which species are critical to their community to focus efforts on species with the most significant impact. Historically, species have been characterized by terms such as dominant, keystone, ecosystem engineer, and structurally based on their characteristics and interactions with community members. The term foundation species has recently propagated through the literature and describes a species that dominates a community in abundance and size, determines the diversity through non-trophic interactions, and controls the fluxes of nutrients and energy at multiple points within the ecosystem (Ellision 2019). Changes in foundation species abundance can affect community structure (Casterani et al., 2018) and habitat value (Haram et al., 2018). As human-induced climate change continues, understanding these foundation species and their range expansion or contraction in response to changes in climatic variables is imperative to conservation, restoration, and understanding the future of these habitats. One current foundation species shift with broad economic and conservation implications is the marsh to mangrove transition currently predicted within the Gulf of Mexico. Through this synthesis, I will introduce mangroves as a foundation species, the factors affecting their invasion of marsh habitat, the implications for mangrove specialists, and the effects of this shift on marsh community members to stress the importance of foundation species as agents of ecological change.
Mangrove forests are tropical coastal ecosystems characterized by salt-tolerant woody trees; the red mangrove (Rhizophora mangle) is considered to be a foundation species of new world mangrove forests with both the black mangrove (Avicennia germinans) and the white mangrove (Laguncularia racemose) when the term is extended to a group of functionally similar taxa. An estimated 35% of mangrove habitat has already been lost due to human activity (reviewed by Valiela et al., 2001). Although these forests have suffered extreme habitat loss, mangrove forests are predicted to expand their current distribution northward due to decreases in freeze events (Cavanaugh et al., 2014) and changes in precipitation (Osland et al., 2017). This expansion may result in a foundation species shift at the northern limits of the mangrove distribution from Spartina alterniflora, the foundation species of coastal marsh, to mangroves. While the expansion of mangroves may be welcomed for their economic services, including acting as nursery habitats for commercial fish, offering storm protection to coastal communities, and sequestering nutrients, the shift will affect communities as mangroves and salt marsh are drastically different in structure, nutrient storage, and habitat value (reviewed by Kelleway 2017).
Cavanaugh et al., 2014 predicts that black and red mangroves will expand northward by 160 and 110 km over the next fifty years, respectively, based on thermal thresholds. This prediction did not account for changes in precipitation, which Osland et al., 2017 suggests is an essential component within these transition zones. Therefore, the expansion of mangroves into marsh habitats may be driven by multiple abiotic factors associated with rapid human-induced climate change. Red mangrove range expansion and contraction are historically common in the higher latitudes of their distribution with lower genetic diversity in these fringe communities (Pil et al., 2011). The low genetic diversity in these populations suggests repeated range contractions leading to small population size and bottleneck effects once mangroves recolonized. While climate variables may govern if mangroves are established in novel locations and colonize marsh habitat, their probability of successful dispersal is both limited and facilitated by ocean currents (Sandoval-Castro et al., 2013). Global ocean dispersal models support the dominance of coastal propagule transport (Stocken et al., 2019); however, more local drivers may also be important such as tides, eddies, and freshwater input. Therefore, understanding the climatic variables governing marsh-mangrove transition is insufficient to predict mangrove expansion when passive dispersal mediates mangrove presence.
Once mangroves invade marsh habitats, the community may not be predictable as mangrove dispersal does not represent mangrove-specialists’ strategies. Even species that also utilize ocean currents to disperse, similarly to mangroves, will vary in their ability to survive open water transport. Mangrove propagules have been demonstrated to survive extended periods in open water (Allen & Krauss 2006), enabling long-distance passive dispersal. Mangrove obligates such as crustaceans, gastropods, or mollusks vary in their pelagic larval duration and larval migration patterns, affecting their ability to expand northward with their foundation species. Crustacean larvae in the mangrove ecosystem exhibit vertical migration patterns dependent upon larval stage and species, which may facilitate nearshore retention; therefore, their dispersal to new habitats may be limited through migration to deeper waters or the utilization of inflowing bottom current to return to shore (Morgan & Fisher 2010; Kunze et al., 2013; Miller & Morgan 2013). Oyster larvae swimming behavior changes in response to multiple abiotic variables such as wave, light, and the interaction between the two, which impacts dispersal to new habitats (Fuchs et al., 2015; Wheeler et al., 2017). Furthermore, simulations in oysters from other habitats indicate that species differences in larvae swimming impact dispersal distances, self-recruitment, and connectivity (North et al., 2008). Furthermore, even vertebrates who inhabit mangrove forests may have limited or complex dispersal patterns. Kryptolebias marmoratus, the mangrove killifish, has been shown to have complex patterns of gene flow that are unexplained by distance (Tatarenkov et al., 2012). Additionally, the subspecies Nerodia clarkii compressicauda, the mangrove water snake, has been shown to have limited gene flow and dispersal between mangrove habitat patches (Jansen et al., 2008). The coloration of this subspecies, ranging from rusty orange to black, may contribute to potential costs of dispersal; coloration might camouflage snakes within mangrove forests but likely stands out in open water, thereby increasing predation risk. Understanding if community members who depend on mangroves as their foundation species will track mangrove expansion is essential to allocating conservation resources. Furthermore, suppose mangrove specialists do not follow this foundation species shift. In that case, new novel niche space may become available to salt marsh species which offers a unique opportunity to explore the process of local adaption within a coastal ecosystem.
This foundation species shift from salt marsh to mangrove habitat is accompanied by shifts in communities within these habitats. As the abundance of black mangroves increases, insect abundance and biomass decrease (Loveless & Smee 2019). Additionally, a community shift is observed as wetlands with black mangroves have less predator biomass (Loveless & Smee 2019). In salt marshes bordering mangroves, mangroves have been demonstrated to decrease the abundance and biomass of nekton and infauna while increasing the abundance of crabs and fish (Smee et al., 2017). In commercial shrimp species, shrimp prefer S. alterniflora, marsh cordgrass, over black mangroves, and survive best in medium-density marsh cordgrass patches (Scheffel et al., 2017). Furthermore, the mangrove forest’s structural complexity was previously expected to provide protection from predators, but shrimp prefer marsh cordgrass regardless of predation regime, possibly indicating the importance of Spartina habitat (Scheffel et al., 2017). Black mangroves and marsh cordgrass also have different detrital attributes, which may drive changes in epifauna. While some research indicates black mangrove detritus decomposes 2-4 times faster than marsh cordgrass, most epifaunal taxa do not differ in abundance except crabs, possibly as a factor of the structural attributes of marsh cordgrass (Smith et al., 2019). In opposition to Smith et al., 2019, Macy et al., 2019 suggests black mangrove leaves decompose slower than the marsh cordgrass and are preferable for chewing herbivores. The contradiction points to a complex relationship that must be understood to predict the ramifications of this foundation species shift. The expansion of red mangroves into cordgrass habitat has also been shown to affect Callinectes spp., with individuals preferentially choosing cordgrass over mangroves in the presence of predators (Johnston & Caretti 2017). Wading birds have also shown decreased abundance with increased mangrove cover (Guo et al., 2017). It is not unexpected that a foundation species shift would impact the community dependent upon that species; however, as mangroves encroach into marsh habitat, the current species may suffer. Research already indicates that a variety of taxa are affected by the transition from salt marsh to mangroves, and as mangroves continue to expand northward, understanding the community-level effects of this foundation species shift will be essential to maintain the function of these ecosystems while facilitating the persistence of marsh community members.
While the expansion and contraction of mangrove habitat are not new, the increase in global temperature promotes expansion by decreasing the frequency of freeze events providing mangroves with a competitive advantage over salt marsh plants. The rate of expansion is dependent upon precipitation (Osland et al., 2017), temperature (Cavanaugh et al., 2015), and ocean currents (Sandoval-Castro et al., 2013). Once established, mangroves may cause drastic changes in community structure. However, these changes in community structure may not be attributed to the expansion of mangrove specialists but decreases in habitat suitability for marsh specialists. While mangroves researchers may rejoice as the fragmented and threatened ecosystem expands, the effects on salt marsh species may outweigh the benefits of expansion. Furthermore, the expansion does not guarantee the presence or survival of mangrove community members in need of new habitat. Therefore, understanding the effects of this shift in foundation species is essential for both maintaining the ecosystem services of coastal habitats while protecting resident and obligatory species.
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