Christianen, M.J.A.

Restoration is becoming a vital tool to counteract coastal ecosystem degradation. Modifying transplant designs of habitat-forming organisms from dispersed to clumped can amplify coastal restoration yields as it generates self-facilitation from emergent traits, i.e. traits not expressed by individuals or small clones, but that emerge in clumped individuals or large clones. Here, we advance restoration science by mimicking key emergent traits that locally suppress physical stress using biodegradable establishment structures. Experiments across (sub)tropical and temperate seagrass and salt marsh systems demonstrate greatly enhanced yields when indi- viduals are transplanted within structures mimicking emergent traits that suppress waves or sediment mobility. Specifically, belowground mimics of dense root mats most facilitate sea- grasses via sediment stabilization, while mimics of aboveground plant structures most facilitate marsh grasses by reducing stem movement. Mimicking key emergent traits may allow upscaling of restoration in many ecosystems that depend on self-facilitation for persistence, by constraining biological material requirements and implementation costs.

1. Seagrasses provide an important ecosystem service by creating a stable erosion‐resistant seabed that contributes to effective coastal protection. Variable morphologies and life‐history strategies, however, are likely to impact the sediment stabilization capacity of different seagrass species. We question how opportunistic invasive species and increasing grazing by megaherbivores may alter sediment stabilization services provided by established seagrass meadows, using the Caribbean as a case study.
2. Utilizing two portable field‐flumes that simulate unidirectional and oscillatory flow regimes, we compared the sediment stabilization capacity of natural seagrass meadows in situ under current‐ and wave‐dominated regimes. Monospecific patches of a native (Thalassia testudinum ) and an invasive (Halophila stipulacea ) seagrass species were compared, along with the effect of three levels of megaherbivore grazing on T. testudinum : ungrazed, lightly grazed and intensively grazed.
3. For both hydrodynamic regimes, the long‐leaved, dense meadows of the climax species, T. testudinum provided the highest stabilization. However, the loss of above‐ground biomass by intensive grazing reduced the capacity of the native seagrass to stabilize the surface sediment. Caribbean seagrass meadows are presently threatened by the rapid spread of the invasive opportunistic seagrass, H. stipulacea . The dense meadows of H. stipulacea were found to accumulate fine sediment, and thereby, appear to be effective in reducing bottom shear stress during calm periods. This fine sediment within the invasive meadows, however, is easily resuspended by hydrodynamic forces, and the low below‐ground biomass of H. stipulacea make it susceptible to uprooting during storm events, potentially leaving large regions vulnerable to erosion. Overall, this present study highlights that intensive megaherbivore grazing and opportunistic invasive species threaten the coastal protection services provided by mildly grazed native species.
4. Synthesis . Seagrass meadows of dense, long‐leaved species stabilize the sediment surface and maintain the seabed integrity, thereby contributing to coastal protection. These services are threatened by intensive megaherbivore grazing, which reduces the stability of the surface sediment, and opportunistic invasive species, which are susceptible to uprooting in storms and thereby can leave the seabed vulnerable to erosion.

Ecosystems have been providing our society with useful services to sustain us in our livelihood, survival and health for as long as we exist. Seagrass ecosystems are especially successful in carbon storage, sediment stabilization, and providing food and habitat for fauna (Nordlund et al., 2016). It is important to conserve these ecosystems in order to maintain its high value. 

Human impact is changing the seagrass landscape. One of the biggest impacts of humans on the marine ecosystem is defaunation, the removal of (predatory) fish and large herbivores such as manatees and turtles, that has been ongoing for the past centuries. These large vertebrates have a big impact – either direct or indirect – on foundation species. For instance, moderate turtle grazing can increase plant productivity, but overgrazing by turtles can lead to a collapse of a seagrass meadows (Christianen et al., 2014). In case of an abundant herbivore community, sharks can come to the rescue and either prey on the turtles or create ‘landscapes of fear’ that turtles will avoid and where seagrass can grow (Wirsing et al., 2007). Thus, defaunation likely induces strong alterations in ecosystem functioning and the services they provide. 

The introduction of exotic species, through increased globalization, is another impact that can have far-reaching consequences on ecosystem services. The spread of invasive species leads to novel ecosystems, where plants and herbivores occur in combinations that are unfamiliar to each other (Williams, 2007). The resulting effect on herbivory rates, food web interactions and ecosystem services are unknown. The PhD project of Fee Smulders will focus on how human impact through defaunation and invasive plant introduction affects ecosystem services in seagrass ecosystems. 

Lac Bay on Bonaire is home to extensive seagrass meadows, dominated by turtlegrass (Thalassia testudinum). This bay provides one of the most important foraging grounds for juvenile green turtles in the Caribbean. The invasive seagrass Halophila stipulacea, native to the Red Sea and the Western Indian Ocean, settled on Bonaire in 2010 and has been increasing throughout the bay ever since (Smulders et al., 2017). Green turtle leaf grazing seems to modify the rate and spatial extent of this invasive species' expansion, due to grazing preferences, and increased space for settlement (Figure 1, Christianen et al., 2018). Defaunation of e.g. predatory sharks could limit the top-down control on sea turtles. This may cause an increase in grazing pressure, and in combination with the fast-growing invasive H. stipulacea may explain the decline of native T. testudinumwe observe in Lac Bay. The ecological effects of this invasion are still largely unknown.

The invasive H. stipulacea is likely to become the dominant species in Lac Bay, and therefore this project aims to quantify and compare the ecosystem services of T. testudinumand H. stipulacea. In this way, potential changes in ecosystem services will be unraveled under the projected species shift. In addition, competition between the native and exotic seagrass species will be investigated. Assessing the impact of the invasion on the ecosystem services of Lac Bay is important for future management and conservation of this protected nature area.

This year, we are collaborating with researchers at 14 other sites in the Caribbean. At all 15 sites, an exclosure experiment will be carried out. We will investigate the effects of nutrient addition and (various levels of) grazing on T. testudinumseagrass structure and function. This large-scale project will give insights in to the tropicalization of turtlegrass. Gradients in grazing intensity, light and temperature may explain differences in ecosystem services across latitudes. Close collaboration with other seagrass scientists will facilitate knowledge exchange across the habitat range of this important seagrass species.

1.Our knowledge of the functional role of large herbivores is rapidly expanding, and the impact of grazing on species co‐existence and non‐native species expansion has been studied across ecosystems. However, experimental data on large grazer impacts on plant invasion in aquatic ecosystems are lacking.

2.Since its introduction in 2002, the seagrass species Halophila stipulacea has rapidly expanded across the Eastern Caribbean, forming dense meadows in green turtle (Chelonia mydas) foraging areas. We investigate the changes in seagrass species co‐existence and the impacts of leaf grazing by green turtles on non‐native seagrass expansion in Lac Bay (Bonaire, Caribbean Netherlands).

3.Green turtle grazing behavior changed after the introduction of non‐native seagrass to Lac Bay in 2010. Field observations, together with time‐lapse satellite images over the last four decades, showed initiation of new grazing patches (65 ha, an increase of 72%). The sharp border between grazed and ungrazed seagrass patches moved in the direction of shallower areas with native seagrass species that had previously (1970‐2010) been ungrazed. Green turtles deployed with Fastloc‐GPS transmitters confirmed high site fidelity to these newly cropped patches. In addition, cafeteria experiments indicated selective grazing by green turtles on native species. These native seagrass species had significantly higher nutritional values compared to the non‐native species. In parallel, exclosure‐experiments showed that non‐native seagrass expanded more rapidly in grazed canopies compared to ungrazed canopies. Finally, in six years from 2011‐2017, H. stipulacea underwent a significant expansion, invading 20 to 49 fixed monitoring locations in Lac Bay, increasing from 6% to 20% in total occurrence. During the same period, native seagrass Thalassia testudinum occurrence decreased by 33%.

4.Synthesis. Our results provide first‐time evidence of large scale replacement of native seagrasses by rapidly colonising H. stipulacea in the Caribbean and add a mechanistic explanation for this invasiveness. We conclude that green turtle leaf grazing may modify the rate and spatial extent of this invasive species’ expansion, due to grazing preferences, and increased space for settlement. This work shows how large herbivores play an important but unrecognized role in species co‐existence and plant invasions of aquatic ecosystems.

Raw dataset: Christianen, M. J. A. (Creator) (28 Jun 2018). Megaherbivores may impact expansion of invasive seagrass in the Caribbean. Wageningen University & Research. 10.4121/uuid:772a6bcf-983d-4be5-96bf-ba6175df5634

From Bonaire, we here provide the first documented case of the green turtle feeding on the invasive seagrass, Halophila stipulacea, in the Caribbean. The seagrass is rapidly invading existing seagrass meadows and altering key foraging habitat of this endangered marine reptile throughout the eastern Caribbean. We expect that more records of green turtles feeding on this invasive species will gradually follow from throughout the region and that the green turtle might alter its foraging behavior in response to the changing species composition of its foraging habitat. 

Early in 2015 the research project “Ecology and conservation of green and hawksbill turtles in the Dutch Caribbean” started funded by NWO. 

The six Dutch Caribbean islands (Aruba, Curaçao, Bonaire, Saba, St. Maarten and St. Eustatius) are home to nesting populations and foraging grounds of the endangered green turtle, Chelonia mydas, and the critically endangered hawksbill turtle, Eretmochelys imbricata. The known threats in the Caribbean are: egg poaching, pollution, incidental catches, and habitat degradation. The Dutch Ministry of Economic Affairs’ “Nature Policy Plan Dutch Caribbean” flags sea turtles as a high conservation priority, yet no (governmentally supported) coordinated conservation program has been implemented. The development of an effective and well-founded conservation program is hampered by the incomplete and disparate knowledge of basic sea turtle ecology. This project aims to provide a solid ecological foundation upon which to base management strategies for green and hawksbill turtles in the Dutch Caribbean, such as gaps of knowledge on the migration routes, population demographics and habitat use of sea turtles within the Caribbean. 

This news article was published in BioNews 20

BioNews is produced by the Dutch Caribbean Nature Alliance and funded by the Ministry of Economic Affairs.

The management of small rookeries is key to conserving the regional genetic diversity of marine turtle populations and requires knowledge on population connectivity between breeding and foraging areas. To elucidate the geographic scope of the populations of marine turtles breeding at Bonaire and Klein Bonaire (Caribbean Netherlands) we examined the post-breeding migratory behavior of 5 female loggerheads Caretta caretta, 4 female green turtles Chelonia mydas, and 2 male and 13 female hawksbill turtles Eretmochelys imbricata during the years 2004-2013. After leaving Bonaire, the 24 tracked turtles frequented foraging grounds in 10 countries. The distances swum from Bonaire to the foraging areas ranged from 608 to 1766 km for loggerhead turtles, 198 to 3135 km for green turtles, and 197 to 3135 km for hawksbill turtles, together crossing the waters of 19 countries. Males represented the minority in this study, but we made 2 key observations that require further research: males remained in the vicinity of the breeding area for 3-5 mo, which is 2-5 times longer than females, and males migrated greater distances than previously recorded. Although the turtles dispersed widely across the Caribbean, there appeared to be 2 benthic foraging areas of particular importance to all 3 species of marine turtles breeding at Bonaire, namely the shallow banks east of Nicaragua and Honduras (n = 8 tracked turtles) and Los Roques, Venezuela (n = 3). Marine turtles breeding at Bonaire face threats from legal turtle harvesting, illegal take, and bycatch in the waters that they traverse across the Caribbean.