We found a significant impact of hurricanes on fouling communities inhabiting harbors, where non-native species were more resilient and able to recover and recolonize open spaces faster than native ones. Accordingly, when compared with pre-hurricane data, a decrease in the number of native species and an increase of introduced species along the whole North Carolinian coast was observed. Two globally introduced species never reported in N.C. were also observed after Hurricane Florence: the solitary ascidian Styela canopus and the colonial species Distaplia listerianum. In July 2019 (one year after Hurricane Florence), we found thirteen ascidian species in sixteen harbors and marinas along North Carolina’s coast, with five of these species identified as native, two as cryptogenic, four as introduced, and two that were classified only to the genus level. Similarly, thirteen distinct ascidian species were observed by Villalobos et al. (2017) in July 2014. However, not all species observed in 2014 were documented in our study and vice-versa. Three native species Didemnum lutarium (observed in two southern marinas), Distaplia corolla (observed in one northern marina), and Eudistoma capsulatum (occurring in one southern and two northern marinas), and one cryptogenic species Distaplia stylifera (observed in one southern marina) were not retrieved in 2019. On the other hand, four previously unreported species were observed in 2019: the cryptogenic species Eusynstyela tincta, the introduced species Styela canopus, and two uncategorizable species: an Eudistoma and an Aplidium. In both 2014 and 2019, the most abundant and widespread species was the solitary Styela plicata, which has a global distribution and an unknown origin (Barros et al. 2009; Pineda et al. 2011).
Based on presence-absence data, there were significantly more introduced ascidian species in 2019 than 2014, but there was no significant difference in the presence-absence or relative abundance of native species. The greater presence of introduced species in 2019 is likely driven by an increase in the number of harbors containing non-native species, and the appearance of a new introduced solitary species, Styela canopus, in several of the northern harbors. The barcoding sequences obtained here for S. canopus were identical or nearly identical to those reported by Barros and Rocha (2021) for Florida and Georgia (U.S.A.) specimens. Since the species was not observed in the southern-most harbors of N.C., our data suggested that S. canopus was likely introduced by fouling the hull of ships navigating North along the Intracoastal Waterway, rather than by natural range expansion. Independent of its introduction pathway, S. canopus is a species widely introduced across the globe (Barros and Rocha 2021) and thus likely to spread rapidly in N.C.
In this study, the latitudinal location of harbors and the distance among them had a significant effect on community similarity for both presence-absence and relative abundance of ascidian species. This observation contrasted with results reported by Villalobos et al. (2017) for 2014, where only distance between harbors had a significant impact on the relative abundance of ascidians. The most parsimonious explanation for these differences is the varying severity of environmental impacts sustained by each area after Hurricane Florence. Ascidians, as sessile invertebrates unable to avoid local abiotic stressors (e.g. temperature and salinity changes), will be affected more severely than mobile organisms (Patrick et al. 2020) and will likely display varied levels of resilience based on their proximity to a disturbance. Hurricane Florence made landfall in Wrightsville Beach (South) and serious flooding was reported to occur between Wilmington (a mile away from Wrightsville Beach) and New Bern (90 miles North), but sparing the northernmost locations in N.C. Accordingly, we expected ascidian communities in southern harbors to have been impacted differently than those in the North. Support for this expectation included, when examining the southern sites as a whole, a loss of four species: the native species Aplidium stellatum and Didemnum lutarium, and the cryptogenic species Distaplia bermudensis and Distaplia stylifera. Additionally, we observed the disappearance of all species except for S. plicata following Hurricane Florence at Seapath Yacht Club, our southern long-term monitoring site, with colonial species displaying significantly decreased abundance per m2 and percent coverage.
Following Hurricane Florence, the first species to recover its original numbers (and even increase these) at Seapath Yacht Club was the only solitary species in our photo-transects, Styela plicata. This species has a global distribution (Pineda et al. 2011) and is the most common and abundant species in N.C. harbors and marinas (Villalobos et al. 2017, here). In addition, both adults and larvae are known to tolerate a wide range of salinity and temperature conditions (Thiyagarajan and Qian 2003, Pineda et al. 2012a,b) and in other temperate locations, the species is able to reproduce all year long (Pineda et al. 2013). Thus, S. plicata has all the makings of an opportunistic species, and here it was able to rapidly colonize all available substrate left by species that perished as a result of the hurricane.
Similarly, the globally introduced ascidian Diplosoma listerianum (here reported in N.C. for the first time) was the second species recovering from Hurricane Florence at Seapath Yacht Club. D. listerianum was previously documented in the states above (Virginia) and below (South Carolina) N.C. (Pérez-Portela et al. 2013), and was observed here in 2018 and 2019. Thus, although it is possible that the species is a new arrival to N.C., the most parsimonious explanation for the lack of previous observations in N.C. is the species’ life cycle. As shown here, D. listerianum numbers and species coverage were particularly high in fall and winter, with numbers and coverage decreasing in spring and few to no individuals observed in summer. The seasonal life pattern of D. listerianum; however, did not prevent the species from recovering from the drastic environmental changes caused by Hurricane Florence after a few months. In fact, the success of D. listerianum as a wide-spread introduced species is attributed to its ability to produce cross-fertilized zygotes as late as one month after sperm has been stored (Bishop and Ryland 1991), foster diverse genotypes within fused colonies (Sommerfeldt and Bishop 2002), and tolerate a wide range of salinities (Gröner et al. 2011). Thus, the first two species to recolonize available substrate after Hurricane Florence were globally introduced species, which is in agreement with previous studies showing that non-native species are typically opportunistic and more resilient than their native counterparts (Lambert 2005).
All colonial species disappeared during several months after Hurricane Florence and all experienced a significant decrease in abundance and percent cover. Among the colonial ascidians present at Seapath Yacht Club in 2018 and 2019, the native Eudistoma capsulatum was the most severely impacted by Hurricane Florence in terms of number of individuals and coverage. Other species within the Eudistoma genus have displayed decreased settlement success, increased juvenile mortality, and failed metamorphosis to the adult stage at low salinities (Vázquez and Young 2000). The sensitivity of E. capsulatum and other ascidians to changes in abiotic conditions (in particular decreased salinity) is well described in the literature (Vázquez and Young 1996, 2000, Epelbaum et al. 2009, Pineda et al. 2012a, Nagar and Shenkar 2016); thus, further work should focus on establishing why these changes affect native and introduced species differently and the mechanisms behind increased resilience, not only to hurricanes but also to anthropogenic disturbances.