Shifts in biodiversity and physical structure of seagrass beds across 5 decades at Carriacou, Grenadines

is estimated as 1.1 m based on the slope of the shore across transects at the 6 HWE sites. In any event, it is evident that at HWE sites (with the possible exception of T9), landward migration of seagrass beds has not kept pace with an increase in accommodation space [28] over our study period. At LWE sites, SFI increased in extent at only one site (T2) between 1969 and 2016. The shore at T2 was steeply sloping and naturally fortified with large boulders, compared to the gently sloping, mangrove-lined (T3) or sandy (T10, T14) shores at the other LWE sites, where SFI was effectively stable or decreased between 1969 and 2016. Seawalls reduce sediment sup- ply from the shore and enhance wave reflection and surge levels [86], which likely accounts for the observed expansion of SFI at T2. Erosional scarps occur along the inner margins of seagrass beds where they alternate with gently sloping margins of seagrass growing towards the shore (S3 Fig) [35]. Within seagrass beds “blowouts”—characterized by an erosional scarp, a seagrass-free blowout floor and a gently sloping seagrass-colonized leeward face—form during high wave energy events and their persistence is dependent on recurrent wave- or current-induced erosion at the scarp face (S3 Fig) [35, 87, 88]. Scarps and blowouts generally are absent in more protected, low wave- energy areas [35, 87, 89]. No scarps were observed at LWE sites in 1969 and 1994, but 1 or 2 scarps occurred at 3 of the 4 sites in 2016, suggesting that mean wave energy at those sites had

increased sufficiently to maintain their erosion. At 3 HWE sites (T1, T6, T7), scarp number tri- pled between 1969 and 2016, with most of this increase occurring between 1994 and 2016. At one site (T5), the sediments were scoured down to bedrock between 1994 and 2016, removing the elevated seagrass bed and associated scarps. This is consistent with anecdotal reports by local fishers of a massive break in the barrier reef in this area in the 2000s, after which the area became more turbulent and subject to strong currents. Our findings suggest that the frequency of high wave energy events sufficient to disrupt seagrass beds, particularly those dominated by T. testudinum, increased between 1994 and 2016 compared to 1969 to 1994. This is consistent with a significant increase in Atlantic hurricane activity from 1996 to 2005 (relative to the 1950–2000 average) attributed to local sea surface warming [90]. At the remaining two HWE sites (T8, T9), both in Grand Bay, scarp number changed little over the 3 sampling years. A large increase (27 m) in SFI at T8 between 1969 and 2016 suggests that persistent wave energy at that site had increased, but that scarp-forming, high energy events affecting other HWE sites had less impact at T8, which is partially protected by a head- land to the northeast. At T9, SFI and scarp number decreased between 1994 and 2019. Bottom profiles show little change in depth between 1969 and 1994, and a small increase (30–50 cm) between 1994 and 2019 (S2 Fig), suggesting that, as at T5, there had been an increase in inten-

sity of the wave regime. The seemingly anomalous differences at T9 may be related to a plenti- ful supply of pebble- and cobble-sized materials from eroding banks onshore (https://www. inaturalist.org/observations/32264949), and accretion of a rubble layer, not seen at other HWE sites in 1969 [35] or in 2016. Impacts of reef flattening on lagoonal seagrass beds Increases in SFI and scarp number at HWE sites and their greater magnitude compared to LWE sites, together with greater changes in these parameters between 1994 and 2016 than between 1969 and 1994, are consistent with increased wave forcing associated with degrada- tion of offshore coral reefs between 1994 and 2016 [33, 34]. Observations on shallow reefs dominated by Acropora palmata at Sandy Island on the southwest coast of Carriacou show a progression from healthy A. palmata in 1969 to dead but still standing A. palmata in 1994 [91] —following the spread of white band disease in the Caribbean in the 1970s and 1980s [92]—to PLOS ONE Seagrass bed biodiversity and structure and across 5 decades PLOS ONE | https://doi.org/10.1371/journal.pone.0306897 August 1, 2024 18 / 25

near complete loss of these protective structures by 2016 when we observed these reefs (S4 Fig). In a rapid assessment of the coral reefs of Carriacou in 2005, Kramer and Dowksza [37] noted extensive physical damage caused by hurricanes Ivan (2004) and Emily (2005) to many reefs along the eastern side of the island, and coral bleaching all around the island in fall 2005. These occurrences in Carriacou are consistent with the general pattern of decline in the struc- tural complexity of Caribbean coral reefs described by Alvarez-Filip et al. [33]: a steep decline in rugosity between 1969 and 1985, followed by relative stasis until 1998, and then a resump- tion in decline. These authors attribute the early decline to disease-mediated mortality of the structurally dominant Acroporoids and the latest decline to bleaching events affecting the slower growing massive corals such as Montastrea spp that remained as the major reef builders after the Acroporoid die-off. In Grenville Bay, Grenada, Reguero et al. [93] used wave energy models to explore erosional effects of increases in sea level and wave height between 1950 and 2008. They concluded that these factors were less important than the degradation of adjacent healthy coral reefs in explaining localized erosion within the bay. In a comparison of seagrass beds in three coral reef lagoons of the Veracruz Reef System (SW Gulf of Mexico), Terrados and Ramı´rez-Garcı´a [89] observed that seagrass cover was lowest, and fragmentation and blowout number highest,

by a reef that had been used as a source of building materials. They attribute this to increasing wave exposure in the lagoon through a direct anthropogenic reef-flattening effect. The stability of seagrass ecosystems, and their associated ecosystem services, including accu- mulation and long-term storage of carbon in associated sediments, has been highlighted as a key unknown in blue carbon science [16, 94]. Our 47-year long dataset suggests persistence of seagrass beds in Carriacou, although observations of increased blowouts and shifts in dominant seagrass species may indicate possible threat to carbon storage capacity. The availability of new accommodation space with sea level rise recently has been recognized as a potential mechanism of expansion of coastal wetlands [28] and blue carbon stores [19, 29]. Limiting development of new anthropogenic barriers to inland wetland migration or removing existing barriers could enable the persistence of coastal wetlands and associated benefits [28, 95]. Such barriers did not exist at the Carriacou HWE sites. Yet, our observations suggest that the potential of landward migration of seagrass to increase cover and enhance carbon stocks of reef-protected seagrass beds under rapidly rising sea levels in future [29] is unlikely to be realized at Carriacou, barring a significant reversal in the processes that have caused reef flattening. Supporting information S1 Table. Transect and station geographic information. Locations and sites (with GPS coor-

dinates) for (A) 10 transects and (B) 17 stations sampled between 1969 and 2016. The number- ing system follows that used in our paper on distribution of the invasive seagrass Halophila stipulacea in Carriacou (Scheibling et al. 2018), in which positions of transects and stations were numbered sequentially around the island. (This included 3 transects conducted in 2016 only and not shown here.) Also given are direction from shore, depth (m) at 50 m offshore, and relative wave exposure (low, LWE; high, HWE) for transects; and distance offshore (m), depth (m, chart datum) at sampling grid, habitat descriptions for stations, and the iNaturalist Observation Number for photographs of species and sites. Link directly to the Observation Number or append it to: https://inaturalist.org/observations/. View iNaturalist Project at: https://inaturalist.org/projects/seagrass-bed-flora-fauna-of-carriacou-grenada-2016. (DOCX) S2 Table. Species or species groups (denoted *, see footnotes) categorized by broad taxo- nomic group. Presence of species or species group in at least one station (1) or none (0), PLOS ONE Seagrass bed biodiversity and structure and across 5 decades PLOS ONE | https://doi.org/10.1371/journal.pone.0306897 August 1, 2024 19 / 25

number of stations out of 17 at which the species/group was recorded, and mean frequency of occurrence (%) in 12 quadrats per station across all stations in 1969, 1994 and 2016. For addi- tional notes on occurrence and natural history of these species and associated photographic records, see iNaturalist Project https://www.inaturalist.org/projects/seagrass-bed-flora-fauna- of-carriacou-grenada-2016. (PDF) S3 Table. Multivariate analysis of seagrass bed community composition. Results of a one factor permutational multivariate analysis of variance (PERMANOVA) based on a Bray–Cur- tis similarity matrix generated from arcsine sqrt transformed frequency of abundance of spe- cies/groups in stations (n = 17) in 1969, 1994 and 2016. Year is a fixed factor and all tests used 9999 permutations and unrestricted permutation of raw data and Type III partial sums of squares. Pairwise tests and average similarity are shown for communities between years. (PDF) S1 Fig. Wave exposure for transects. Relative Exposure Index (REI) for transects at Low Wave Energy (LWE, n = 4) and High Wave Energy (HWE, n = 6) sites. (TIFF) S2 Fig. Depth profiles for transects at 6 HWE sites and 4 LWE sites in 1969 and 2016, and 3 HWE sites and 1 LWE site in 1994. Extent of seagrass-free inshore zone shown as dashed line at start of transects. Scarps (depth measured at base and peak) shown as circles. (TIFF) S3 Fig. Photographs illustrating blowout and scarps in seagrass beds at Carriacou. A. Typi- cal blowout. B. Actively eroding scarp. C. Old scarp, non-eroding; new growth of seagrass on

blowout floor and over scarp face. (Photographs by David Patriquin). (PDF) S4 Fig. Photographs of Acropora palmata-dominated fringing reef on seaward side of Sandy Island (12.4855, -61.4829), Carriacou, illustrating the process of reef flattening between 1969 and 2016. 1969: Intact, living A. palmata reef. 1996: A. palmata entirely dead but mostly still in-place following die-off from White Band Disease in late 1970s/early 1980s; a few small colonies of a new generation of A. palmata were present. 2016: Original A. palmata framework reduced to rubble, no substantive replacement by newer colonies. (Photographs by David Patriquin.) For details of changes from 1969 to 1996, see Patriquin DG, Hunte W. Pre- liminary observations of the status of shallow water reefs at Sandy Island, Carriacou, Grenada. Report to the Grenada Board of Tourism and the Kido Project Environment Station, Carria- cou. 1997. Available at: https://dalspace.library.dal.ca/handle/10222/82532. (PDF) Acknowledgments Graham Patriquin and Lotus Vermeer assisted with field sampling in 1994. Coy Coy McLaren in 1969 and 1994, and Ivan McLaren in 2016, provided able boat assistance to reach offshore sites. Nina Patriquin provided essential support throughout. Author Contributions Conceptualization: David Patriquin, Robert E. Scheibling. Data curation: David Patriquin, Karen Filbee-Dexter. PLOS ONE Seagrass bed biodiversity and structure and across 5 decades PLOS ONE | https://doi.org/10.1371/journal.pone.0306897 August 1, 2024 20 / 25

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