Rapid global degradation of coastal habitats can be attributed to anthropogenic activities associated with coastal development, aquaculture, and recreational surface water use. Restoration of degraded habitats has proven challenging and costly, and there is a clear need to develop novel approaches that promote resilience to human-caused disturbances. Positive interactions between species can mitigate environmental stress and recent work suggests that incorporating positive interactions into restoration efforts may improve restoration outcomes. We hypothesized that the addition of a potential facultative mutualist, the native hard clam (Mercenaria mercenaria), could enhance seagrass bed recovery from disturbance. We conducted two experiments to examine the independent and interacting effects of hard clam addition and physical disturbance mimicking propeller scarring on mixed community Zostera marina and Halodule wrightii seagrass beds in North Carolina. Adding clams to seagrass beds exposed to experimental disturbance generally enhanced seagrass summer growth rates and autumn shoot densities. In contrast, clam addition to non-disturbed seagrass beds did not result in any increase in seagrass growth rates or shoot densities. Clam enhancement of autumn percent cover relative to areas without clam addition was most prominent after Hurricane Dorian, suggesting that clams may also enhance seagrass resilience to repeated disturbances. By June of the next growing season, disturbed areas with clam additions had greater percent cover of seagrass than disturbed areas without clam additions. Beds that were disturbed in April had higher percent cover than areas disturbed in June of the previous growing season. Our results suggest that the timing and occurrence of physical disturbances may modify the ability of clams to facilitate seagrass resiliency and productivity. Understanding when and how to utilize positive, interspecific interactions in coastal restoration is key for improving restoration success rates.
Special Feature: Honoring Charles H. Peterson, Ecologist
Sarah E. Donaher, Christopher J. Baillie, Carter S. Smith, Y. Stacy Zhang, Anna Albright, Stacy N. Trackenberg, Emory H. Wellman, Nina Woodard, Rachel K. Gittman
A rising awareness of the declining health and functioning of the planet’s coastal ecosystems has occurred in recent years (Jackson et al. 2001, Lotze et al. 2006, Worm et al. 2006, Oliver et al. 2015). Coastal habitat loss is driven in part by an increasing number of natural and anthropogenic disturbances that can hinder ecosystem service provision or result in total ecosystem loss (Short and Wyllie-Echeverria 1996, Halpern et al. 2008). As coastal habitats become increasingly degraded or lost entirely, the need to develop novel and effective restoration techniques is clear (Waycott et al. 2009, Beck et al. 2011, Cullen-Unsworth and Unsworth 2016). To recover vital ecosystem functions and services, researchers and practitioners have invested in a variety of approaches to restore coastal ecosystems, but an understanding of how to ensure long-term sustainment and resilience of restored ecosystems has lagged behind (Lotze et al. 2006, van Katwijk et al. 2009, Zhang et al. 2018).
Improving restoration outcomes for foundation species (sensu Dayton 1972) is of particular interest to restoration ecologists (Byers et al. 2006, van Katwijk et al. 2009, Gedan et al. 2014). Foundation species play a large role in maintaining their habitat, in part by incorporating facilitative and mutualistic interactions to ameliorate abiotic and biotic stressors to create favorable conditions within the system (Dayton 1972). As foundation species, seagrasses benefit both human and natural communities via the provision of many ecological functions, including providing refuge and food for juvenile and adult animals (Heck and Orth 1980, Peterson et al. 1984, Peterson 1986, Heck et al. 1997, Heck and Valentine 2006, Goshima and Peterson 2012); stabilizing sediments and reducing erosion (Fonseca and Fisher 1986, Potouroglou et al. 2017); reducing flow and attenuating wave energy to protect nearshore habitats and infrastructure (Fonseca et al. 1982, Peterson et al. 2004, de Boer 2007); storing carbon (Mcleod et al. 2011, Fourqurean et al. 2012); and reducing human and marine pathogens in the water column (Lamb et al. 2017). Degradation and loss of seagrasses are so severe that it has been dubbed a “global crisis” (Orth et al. 2006); thus, restoration efforts have increased dramatically in recent decades, but seagrass restoration has proven to be both challenging and costly (Cunha et al. 2012, Bayraktarov et al. 2015, van Katwijk et al. 2016).
Restoration is particularly difficult in areas where seagrass has been entirely lost or where environmental quality has degraded to the point that the site is no longer suitable for the establishment of seagrasses (van Katwijk et al. 2009). Attempts to restore or accelerate recovery in seagrasses impacted by small-scale disturbances, such as propeller scarring, have included nutrient addition, supplemental planting of colonizing species, and biophysical stabilization, with varied success (Hall et al. 2006, Marion and Orth 2010, Kenworthy et al. 2018). Although often relatively small in scale, propeller scarring in seagrass beds can cause substantial economic and ecological losses, particularly when beds are exposed to repeated scarring events or to both scarring and major storms, such as hurricanes (Fonseca and Bell 1998, Whitfield et al. 2002, Engeman et al. 2008, Orth et al. 2017). For example, propeller scars in Florida exposed to a strong hurricane grew in size by 63% and only 11% of the seagrass coverage returned five years after the hurricane (Whitfield et al. 2002). These repeated disturbances can create physical instability in seagrass beds by uprooting shoots and severing rhizome connections, making them more vulnerable to further disturbances. For these beds, recovery is often slower than the initial decline, in some cases making it nearly impossible for a seagrass bed to recover naturally (Scheffer et al. 2001, Beisner et al. 2003, O’Brien et al. 2017). It is therefore critical to develop and rigorously test conservation approaches which improve local environmental conditions and promote the resilience of existing habitats to disturbance in order to maintain the ecosystem’s ecological and economic value (Reynolds et al. 2016).
There is a growing movement among coastal restoration researchers and practitioners to understand which ecological relationships and functions provide innate resiliency and prevent significant degradation and loss of habitats experiencing stress (Silliman et al. 2015, Derksen-Hooijberg et al. 2017, Renzi et al. 2019). For example, several studies have shown that mussels promote saltmarsh resiliency to and recovery from physical and climatic disturbances via deposition of nutrient-rich waste and providing structure which reduces soil salinity stress and enhances water storage capacity (Angelini et al. 2016, Derksen-Hooijberg et al. 2017). Many of the seagrass restoration strategies most widely employed today, including large-scale planting or seeding (Marion and Orth 2010) and use of laboratory-germinated seeds (Bird et al. 1994), are reactive practices designed to be implemented after the habitat has already been severely degraded or lost entirely. However, the proactive incorporation of positive, interspecific interactions into seagrass conservation and restoration (Zhang et al. 2021) after small-scale disturbances may have the potential to change the trajectory of recovery for seagrass ecosystems.
Several seagrass and bivalve species interact positively with one another as facultative mutualists (Boström et al. 2006). Seagrass beds benefit associated bivalves by serving as a refuge from predation, providing a source of sediment oxygen, and minimizing exposure to bacterial pathogens (Peterson et al. 1984, Wall et al. 2008, Goshima and Peterson 2012, Lamb et al. 2017). The hard clam, Mercenaria mercenaria, has been shown to have elevated survivorship and densities within Zostera marina beds relative to those within adjacent unvegetated substrate (Peterson et al. 1984, Peterson 1986, Irlandi 1997). Bivalves, in turn, have been shown to increase seagrass productivity and survivorship in some cases (Reusch et al. 1994, Peterson and Heck 2001a, Gagnon et al. 2020). Bivalves benefit seagrasses by enhancing sediment nutrient content via the biodeposition of feces and pseudofeces, thereby potentially fertilizing seagrasses (Reusch et al. 1994, Peterson and Heck 1999, 2001b, Newell and Koch 2004, Lotze et al. 2006). Bivalves also enhance water column clarity via suspension feeding, which allows for increased light penetration and higher seagrass photosynthetic and growth rates (Wall et al. 2008). Additionally, by providing habitat for epiphytic grazers and directly feeding on epiphyte propagules in the water column, bivalves can also help control eutrophication and algal blooms, thereby reducing deleterious fouling on seagrass blades (Peterson and Heck 2001a, Cerrato et al. 2004). In some seagrass beds, lucinid bivalves host sulfide-oxidizing bacteria in their gills which reduces the levels of toxic sulfide in the sediment and enhances seagrass aboveground biomass by alleviating sulfide intrusion (van der Heide et al. 2012, van der Geest et al. 2020).
To determine whether artificial enhancement of the densities of M. mercenaria, a bivalve commonly found in seagrass beds within North Carolina’s estuarine waters (Peterson et al. 1984), could facilitate seagrass bed resilience to disturbance, we conducted two experimental studies examining the independent and interacting effects of bivalve facilitation and physical disturbance on seagrass productivity and recolonization of disturbed areas. We proposed the following hypotheses: (1) The addition of M. mercenaria to undisturbed beds would increase seagrass productivity relative to control beds; (2) the addition of M. mercenaria to disturbed beds would increase seagrass productivity relative to disturbed beds without M. mercenaria addition; and (3) seagrass with clam additions would recolonize disturbed areas more rapidly and extensively than seagrass in disturbed areas without clam additions. Further, because past studies have confirmed that severe storms can act as repeated disturbances that cause propeller scars to expand or persist (Fonseca and Bell 1998, Whitfield et al. 2002), we also sampled before and after Hurricane Dorian, a Category 1 hurricane, to determine how seagrass percent cover was affected by the storm in our experimental treatments.