Biological Invasions

Abstract

The seagrass Halophila stipulacea is native to the Red Sea. It invaded the Mediterranean over the past century and most of the Caribbean over the last two decades. Understanding the main drivers behind the successful invasiveness of H. stipulacea has become crucial. We performed a comprehensive study including field measurements, a mesocosm experiment, and a literature review to identify ‘superior growth traits’ that can potentially explain the success story of H. stipulacea. We assessed meadow characteristics and plant traits of three invasive H. stipulacea populations growing off the Island of Sint Eustatius (eastern Caribbean). We compared similar parameters between native (Eilat, northern Red Sea) and invasive (Caribbean) H. stipulacea plants in a common-garden mesocosm. Lastly, we compared our field measurements with published data. The newly arrived H. stipulacea plants from St. Eustatius were characterized by higher percent cover, higher below- and above-ground biomasses, more apical shoots, and faster leaf turnover rates than those measured in both native and older invaded habitats. These results were further confirmed by the mesocosm experiment where the invasive H. stipulacea plants grew faster and developed more apical shoots than the native plants. Results suggest that increased growth vigour is one of the main invasive traits that characterize successful invasive H. stipulacea populations in the Caribbean and potentially in other invaded areas. We encourage long-term monitoring of H. stipulacea in both native and invaded habitats to better understand the future spread of this species and its impacts on communities and their ecosystem functions and services.

Prey naïveté, or the failure of prey to recognize non-native predators due to a lack of co-evolutionary history, is thought to underpin the large impact of invasive Indo-Pacific lionfish (Pterois sp.) on coral reef fish populations in the western Atlantic. Most previous studies of lionfish recognition have taken place in experimental tanks that did not mimic natural conditions or used bottle or cage field designs that constrained natural behaviour. To alleviate these issues, we compared the homing patterns of experimentally translocated Caribbean bicolor damselfish (Stegastes partitus) in the presence and absence of standardized models of a lionfish, of an ecologically similar native piscivore (black grouper; Mycteroperca bonaci), and of a native non-piscivore (French grunt, Haemulon flavolineatum) in the field. The native grouper model elicited a strong predator avoidance response: translocated damselfish became unlikely to home when released beyond ~ 2 m from their territory and took longer to do so. In contrast, damselfish facing a lionfish model exhibited similar homing behaviours to those of damselfish in the presence of a non-piscivorous grunt and in the absence of any model. Fish length and translocation distance also influenced homing: damselfish stopped homing when released more than 5.6 m away from their territory and larger individuals crossed wider sand gaps. Overall, our findings are consistent with the idea that bicolor damselfish are naïve to the threat of predation presented by lionfish, but also with the notion that damselfish might be assessing, but deeming to be low, the threat of a stalking predator hunting over open sand. Both mechanisms point to inaccurate risk perception in relation to invasive lionfish. More broadly, we highlight a novel experimental translocation approach to evaluate behavioural responses of native prey species to novel predators under realistic field conditions.

The loss of biodiversity by the replacement of invasive species could lead to the loss of functional traits that maintain certain ecosystem services (ES). The ES method provides a conceptual framework to value changes of functional traits related to this loss of biodiversity. The Caribbean Sea offers a multifaceted seascape to evaluate this approach as native seagrass species (Thalassia testudinum, Syringodium filiforme or Halodule wrightii) cohabit this region together with the invasive seagrass Halophila stipulacea, native to the Indian Ocean. The functional traits of native seagrass species in the Caribbean are compared to different traits of H. stipulacea observed worldwide with the aim of evaluating the dimensions of this change in terms of the ES that seagrass meadows provide in the Caribbean. Under a changing seascape due to climate change and anthropogenic pressures that have driven the disappearance of most seagrass meadows in the Caribbean, we explore how this invasive seagrass could play a role in restoration attempts as a pioneer species where native species have been lost. The potential unintended consequences of the presence of H. stipulacea to replace services of native species are also noted.

The detrimental effects of invasive lion- fishes (Pterois volitans and Pterois miles) on western Atlantic shallow reefs are well documented, including declines in coral cover and native fish populations, with disproportionate predation on critically endan- gered reef fish in some locations. Yet despite individ- uals reaching depths [100 m, the role of mesophotic coral ecosystems (MCEs; reefs 30–150 m) in lionfish ecology has not been addressed. With lionfish control programs in most invaded locations limited to 30 m by diving restrictions, understanding the role of MCEs in lionfish distributions remains a critical knowledge gap potentially hindering conservation management. Here we synthesise unpublished and previously published studies of lionfish abundance and body length at paired shallow reef (0–30 m) and MCE sites in 63 locations in seven western Atlantic countries and eight sites in three Indo-Pacific countries where lionfish are native. Lionfish were found at similar abundances across the depth gradient from shallow to adjacent MCEs, with no difference between invaded and native sites. Of the five invaded countries where length data were avail- able three had larger lionfish on mesophotic than shallow reefs, one showed no significant difference while the fifth represented a recently invaded site. This suggests at least some mesophotic populations may represent extensions of natural ontogenetic migra- tions. Interestingly, despite their shallow focus, in many cases culling programs did not appear to alter abundance between depths. In general, we identify widespread invasive lionfish populations on MCE that could be responsible for maintaining high densities of lionfish recruits despite local shallow-biased control programs. This study highlights the need for manage- ment plans to incorporate lionfish populations below the depth limit of recreational diving in order to address all aspects of the local population and maximise the effectiveness of control efforts. 

The invasion by Indo-Pacific lionfish (Pterois volitans and P. miles) of the western Atlantic, Caribbean and Gulf of Mexico is emerging as a major threat to coral reef communities across the region. Comparing native and introduced populations of invasive species can reveal shifts in ecology and behaviour that can accompany successful invasions. Using standardized field surveys replicated at multiple sites in Kenya and the Bahamas, we present the first direct comparisons of lionfish density, body size, biomass and behaviour between native and invaded coral reefs. We found that lionfish occur at higher densities with larger body sizes and total biomass on invaded Bahamian coral reefs than the ecologically equivalent species (P. miles) does on native Kenyan reefs. However, the combined average density of the five lionfish species (Pterois miles, P. antennata, P. radiata, Dendrochirus brachypterus and D. zebra) on Kenyan reefs was similar to the density of invasive lionfish in the Bahamas. Understanding the ecological processes that drive these differences can help inform the management and control of invasive lionfish.

The rapid invasion of lionfish into the Western North Atlantic and Caribbean will undoubtedly affect native reef fishes via processes such as trophic disruption and niche takeover, yet little is known about the dynamics of this invasion. We constructed a stage-based, matrix population model in which matrix elements were comprised of lower-level parameters. Lionfish vital rates were estimated from existing literature and from new field and laboratory studies. Sensitivity analysis of lower-level parameters revealed that population growth rate is most influenced by larval mortality; elasticity analysis of the matrix indicated strong influence of the adult and juvenile survival elements. Based on this model, approximately 27% of an invading adult lionfish population would have to be removed monthly for abundance to decrease. Hierarchical modeling indicated that this point estimate falls within a broad uncertainty interval which could result from imprecise estimates of life-history parameters. The model demonstrated that sustained removal efforts could be substantially more effective by targeting juveniles as well as adults.