Fee O.H. Smulders

In tropical ecosystems, autotroph organisms are continuously competing for space, with some plant species benefiting from disturbances such as fire, grazing, or bioturbation that clear habitat (Pulsford et al. 2016). These disturbances can open up layers of vegetation, thereby promoting colonization of opportunistic species that would have been competitively inferior without disturbance (Castorani et al. 2018). Opportunistic fast-growing species also include often invasive species that are therefore also likely to increase in dominance after disturbance (Altman and Whitlatch 2007). In seagrass meadows in the southern Caribbean, we observed that the marine invasive plant Halophila stipulacea uses bioturbation mounds, created by burrowing infauna such as sea cucumbers and shrimp (see Suchanek 1983), to colonize new habitats (Figure 1a, b). On Bonaire and Curaçao, in habitats with ~100% native Thalassia testudinum cover, invasive H. stipulacea often at first only occurred on bioturbation mounds that smothered native T. testudinum seagrass, likely due to fragmentation and subsequent settlement (Smulders et al. 2017). These observations suggest that bioturbation mounds serve as starting points for further invasion (Fig. 1c).  

Abstract

Halophila stipulacea, a small seagrass species native to the Indo-Pacific, is a Lessepsian migrant and a high-profile invader that has successfully colonized two exotic regions, the Mediterranean (first observed in 1894) and the Caribbean (2002). In 1961, an intracellular phytomyxid parasite, Marinomyxa marina (SAR: Rhizaria: Endomyxa: Phytomyxea) was discovered in the petioles of H. stipulacea in the Red Sea, and three decades later, it was reported off the coast of Sicily (Mediterranean), suggesting parallel migration of the two organisms. In 2018, infected petioles of H. stipulacea were also observed in St. Eustatius (Caribbean), but the identity of the causative agent remained unresolved. Here, we provide information on four new localities of phytomyxid-infested populations of H. stipulacea in Greece (Mediterranean), and Bonaire and Martinique (Caribbean), including notes on infection prevalence and seasonal dynamics. Using the 18S rRNA barcoding gene, we bring molecular evidence that the disease is caused by a genetically uniform variant of M. marina at all the examined sites. We conclude that the parasite is now widespread throughout both invaded regions and has been present in the Caribbean since 2013 at the latest. For the first time, the production of fruits in infected plants is observed, indicating a non-lethal nature of the symbiosis. While the arrival of M. marina to the Caribbean is unlikely to alleviate the current invasiveness of H. stipulacea, we emphasize the need for its further monitoring since the host-specificity and general biology of seagrass-associated phytomyxids are still poorly understood.

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The success of invasive macrophytes can depend on local nutrient availability and consumer pressure, which may interact. We therefore experimentally investigated the interacting effects of nutrient (nitrogen and phosphorus) addition, the exclusion of large herbivorous fishes and mimicked grazing on the expansion rates of the invasive seagrass Halophila stipulacea. The experiments were established on Bonaire and Aruba, two islands in the southern Caribbean, which differ in fish community structure. We observed that multiple Caribbean fish species feed on H. stipulacea. At both study sites, nutrient enrichment decreased invasive leaf carbon:nitrogen ratios. However only on Bonaire, where herbivore fish abundance was 7 times higher and diversity was 4.5 times higher, did nutrient enrichment result in a significant reduction of H. stipulacea expansion into native Thalassia testudinum meadows. This effect was likely due to increased herbivory on nutrient enriched seagrass leaves, as we found that excluding large herbivorous fish (e.g. parrotfish) doubled invasive expansion rates in bare patches on Bonaire. On Aruba, H. stipulacea expansion rates were higher overall, which coincided with lower abundances and diversity of native fishes, and were limited by mimicked fish grazing. We suggest that top-down control by the native fish community may counteract eutrophication effects by increased grazing pressure on nutrient-rich invasive seagrass leaves. We conclude that diverse and abundant herbivore communities likely play an important role in limiting invasion success and their conservation and restoration may serve as a tool to slow down seagrass invasions.