Smulders, F.O.

The dioecious seagrass species Halophila stipulacea reproduces mainly through fast clonal growth, underlying its invasive behavior. Here, we provide morphological evidence to show that the first findings of fruits in the Caribbean were misidentified. Consequently, H. stipulacea reproduction is likely still only asexual in the Caribbean. Therefore, we introduce an identification key of H. stipulacea reproductive structures to encourage careful identification and quantification throughout its invasive range. Until large-scale seed production in invaded habitats is reported, the apparent low rate of sexual reproduction needs to be considered in current studies investigating the invasion capacity of this species.

Native to the Red Sea and Western Indo-Pacific, the seagrass Halophila stipulacea (Forsk.) Ascherson, was reported to have invaded the Mediterranean Sea in 1894 (Lipkin 1975) and the Caribbean in 2002 (Ruiz and Ballantine 2004), after which it spread successfully in both regions (Winters et al. 2020). Similar to many invasive macrophytes, H. stipulacea expands mainly through asexual clonal growth and fragmentation (Lipkin 1975; Smulders et al. 2017), a feature believed to characterize the colonization of multiple Caribbean islands (Willette et al. 2014).

Sexual reproduction increases the genetic variability and dispersal potential of seagrasses, which is important for long-term stability of populations under dynamic change (Ackerman 2006). In its native range, Halophila stipulacea flowers predictably with both female and male flower production, followed by seed formation within 1–2 months after fertilization (Dural 2020; Malm 2006; Nguyen et al. 2018 see Figure 1A and B). Male flowering has commonly been reported throughout its invasive range; both in the Mediterranean as well as in the Caribbean (Chiquillo et al. 2019; Dural et al. 2020; Gambi et al. 2018; Procaccini et al. 1999; Vera et al. 2014). In contrast, documentation of female flowers and fruits is rare, and was limited to four studies in the Mediterranean (Dural et al. 2020; Gerakaris and Tsiamis 2015; Lipkin 1975; Nguyen et al. 2018), until a recent report of fruits in the US Virgin Islands (Chiquillo et al. 2019).

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.

The non-native seagrass species Halophila stipulacea has spread throughout the Eastern Caribbean since 2002, and could potentially impact the functioning of local seagrass ecosystems. Important characteristics for invasiveness, such as dispersal, recruitment and expansion of H. stipulacea at a local scale, are unknown. We assessed H. stipulacea expansion rates within Lac Bay, Bonaire, Dutch Caribbean (7 km2), since its establishment in 2010 and tested the settlement potential of uprooted vegetative fragments of H. stipulacea. Using 49 fixed locations, we observed that between 2011 and 2015 the occurrence of H. stipulacea in the bay increased significantly from 6% to 20% while native Thalassia testudinum occurrence decreased significantly from 53% to 33%. Free-floating H. stipulaceafragments that were collected and tethered above the sediment rooted within 10 days with a settlement success rate of 100%. The growth of settled fragments was on average 0.91 shoots d−1. The ongoing shift from native T. testudinum to introduced H. stipulacea dominated meadows may have important consequences for multiple Caribbean seagrass ecosystem functions. Given the large difference in size between the two seagrass species, functions such as coastal protection, habitat structure, food availability, and the stability and resilience of these systems can be altered. The next steps towards modelling future expansion of H. stipulacea throughout the Caribbean and beyond should include the assessment of fragment viability and dispersal distance, and the impacts of natural and anthropogenic disturbance on vegetative fragment density, dispersion and settlement by this species.