The Tropical Seagrass Halophila stipulacea: Reviewing What We Know From Its Native and Invasive Habitats, Alongside Identifying Knowledge Gaps

Halophila stipulacea is a small tropical seagrass, native to the Red Sea, Persian Gulf, and the Indian Ocean. It invaded the Mediterranean Sea 150 years ago as a Lessepsian migrant, but so far has remained in insulated, small populations across this basin. Surprisingly, in 2002 it was reported in the Caribbean Sea, where within less than two decades it spread to most of the Caribbean Island nations and reaching the South American continent. Unlike its invasion of Mediterranean, in the Caribbean H. stipulacea creates large, continuous populations in many areas. Reports from the Caribbean demonstrated the invasiveness of H. stipulacea by showing that it displaces local Caribbean seagrass species. The motivation for this review comes from the necessity to unify the existing knowledge on several aspects of this species in its native and invasive habitats, identify knowledge gaps and develop a critical strategy to understand its invasive capacity and implement an effective monitoring and conservation plan to mitigate its potential spread outside its native ranges. We systematically reviewed 164 studies related to H. stipulacea to create the "Halophila stipulacea database." This allowed us to evaluate the current biological, ecological, physiological, biochemical, and molecular knowledge of H. stipulacea in its native and invasive ranges. Here we (i) discuss the possible environmental conditions and plant mechanisms involved in its invasiveness, (ii) assess the impact of H. stipulacea on native seagrasses and ecosystem functions in the invaded regions, (iii) predict the ability of this species to invade European and transoceanic coastal waters, (iv) identify knowledge gaps that should be addressed to better understand the biology and ecology of this species both in its native and non-native habitats, which would improve our ability to predict H. stipulacea's potential to expand into new areas in the future. Considering the predicted climate change scenarios and exponential human pressures on coastal areas, we stress the need for coordinated global monitoring and mapping efforts that will record changes in H. stipulacea and its associated communities over time, across its native, invasive and prospective distributional ranges. This will require the involvement of biologists, ecologists, economists, modelers, managers, and local stakeholder

Inconclusive evidence of sexual reproduction of invasive Halophila stipulacea : A new field guide to encourage investigation of flower and fruit production throughout its invasive range

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.</p

Growth and recovery after small-scale disturbance of a rapidly-expanding invasive seagrass in St. John, U.S., Virgin Islands

Seagrass meadows evolved in the presence of disturbances and have a wide variance in recovery rate that largely follow a trajectory of re-colonization and succession to pre-disturbance levels. Invasive species may gain a foothold within native seagrass beds after space is opened by disturbances that reduce seagrass cover. Here we use shoot density monitoring data to describe growth of the invasive seagrass Halophila stipulacea in Caribbean bays over a 5-year period and conduct a series of experiments using a combination of mesocosm, seagrass removal plots, and field measurements to quantify vegetative fragment survivorship and recovery after benthic disturbance. Shoot density increased rapidly in invaded bays, reaching average densities of approximately 600 shoots/m2 within 5 years of establishment. Seagrass cover was estimated to recover to pre-disturbance level 17–31 weeks after removal from vegetative propagation of neighboring plants outside the treatment plot. Mesocosm experiments found floating and settled fragments as small as 2 cm in length and containing at least one vertical shoot survived the 4-day trial and increased in both length and biomass. Empirical evidence here demonstrates that H. stipulacea is highly resilient to small-scale disturbance which we suggest is having a transformative impact on Caribbean seagrass communities

An invasive seagrass drives its own success in two invaded seas by both negatively affecting native seagrasses and benefiting from those costs

The nature and strength of interactions between native and invasive species can determine invasion success. Species interactions can drive, prevent or facilitate invasion, making understanding the nature and outcome of these interactions critical. We conducted mesocosm experiments to test the outcome of interactions between Halophila stipulacea, a seagrass that invaded the Mediterranean and Caribbean Seas, and native seagrasses (Cymodocea nodosa and Syringodium filiforme, respectively) to elucidate mechanisms explaining the successful invasions. Mesocosms contained intact cores with species grown either mixed or alone. Overall, in both locations, there was a pattern of the invasive growing faster with the native than when alone, while also negatively affecting the native, with similar patterns for shoot density, aboveground and belowground biomass. In the Caribbean, H. stipulacea increased by 5.6 ± 1.0 SE shoots in 6 weeks when grown with the native while, when alone, there was a net loss of −0.8 ± 1.6 SE shoots. The opposite pattern occurred for S. filiforme, although these differences were not significant. While the pattern in the Mediterranean was the same as the Caribbean, with the invasive grown with the native increasing shoots more than when it grew alone, these differences for shoots were not significant. However, when measured as aboveground biomass, H. stipulacea had negative effects on the native C. nodosa. Our results suggest that a seagrass that invaded two seas may drive its own success by both negatively affecting native seagrasses and benefiting from that negative interaction. This is a novel example of a native seagrass species facilitating the success of an invasive at its own cost, providing one possible mechanism for the widespread success of this invasive species

Little giants: a rapidly invading seagrass alters ecosystem functioning relative to native foundation species

The spread of invasive species is a major component of global ecological change and how and when to manage particular species is a difficult empirical question. Ideally, these decisions should be based on the specific impacts of invading species including both their effects on native competitors and how they may or may not play similar roles in broader ecosystem functioning. Halophila stipulacea is an invasive seagrass currently spreading through the Caribbean, and as seagrasses are foundation species, the effects of invasion have the potential to be particularly far-reaching. To evaluate the impacts of H. stipulacea we quantified spread and potential for displacement of native seagrasses as well as the effects of invasion on multiple ecosystem processes, particularly resource support for higher trophic levels and habitat creation. Long-term monitoring suggested that H. stipulacea likely displaces some native seagrasses (Syringodium filiforme and Halodule wrightii), but not others. Halophila stipulacea had lower N and protein levels and higher C:N ratios than native seagrasses, and as such is a poorer quality resource for consumers. We also observed significantly lower consumption of H. stipulacea than the native S. filiforme but limited differences compared to Thalassia testudinum. We found H. stipulacea created a more nutrient limited environment than T. testudinum and there were significantly distinct invertebrate assemblages in native- and invasive-dominated seagrass beds, but no difference in species richness or invertebrate biomass. These results suggest that the spread of H. stipulacea would impact a variety of ecological processes, potentially restructuring seagrass ecosystems through both direct impacts on environmental conditions (e.g., nutrient availability) and indirect food web interactions