Corresponding author: Tamara B. Robinson ( firstname.lastname@example.org )
Academic editor: Gregory Ruiz
© 2017 Tamara B. Robinson, Brendan Havenga, Marlene van der Merwe, Sue Jackson.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Robinson TB, Havenga B, van der Merwe M, Jackson S (2017) Mind the gap – context dependency in invasive species impacts: a case study of the ascidian Ciona robusta. NeoBiota 32: 127-141. https://doi.org/10.3897/neobiota.32.9373
In the face of increasing invasions and limited resources, appropriate management of invasive species requires prioritisation of species for management action. This process often relies on knowledge of species specific impacts. However, as studies explicitly measuring impact of marine alien species are rare, prioritisation of management actions is often based on studies from outside the geographic area of interest. Further, few impact studies account for context dependency (e.g. seasonal variability or distinct environmental regimes), raising the question of how transferrable knowledge about the impact of a species is between invaded ranges. This study addressed this question by using the widespread invasive solitary ascidian Ciona robusta as a case study for assessing impacts across two invaded regions: South Africa and California, USA. We replicated a previously conducted experiment from California that showed that C. robusta depresses local species richness in San Francisco Bay. Our South African experiment showed no effect of C. robusta on species richness, the Shannon-Weiner diversity index or community composition, despite experiments being carried out over two years and at two depths. While these results may reflect strong density dependency in the impact of C. robusta, they serve to highlight context dependency in invasive species impacts. This suggests that until studies of impact in marine systems become common place, context dependency should be explicitly addressed as a source of uncertainty during the prioritisation of species for management action.
Ciona robusta, community structure, fouling, impacts, management, species richness
The increasing rate at which alien species are being spread across the globe is well acknowledged (
Such management challenges can be particularly relevant in developing nations. For instance, 89 non-indigenous marine species are known from South Africa (
Due to their prevalence in fouling communities, and the reported ecological or economic impacts of some species, ascidians are often a focal group in marine invasion studies (e.g.
Previously referred to as C. intestinalis, C. robusta has been known from South Africa for more than 50 years (
This study took place at two locations, Yacht Port Marina (33°01'36"S; 17°57'40"E) in Saldanha Bay on the South African west coast and Gordons Bay Yacht Club (34°09'52"S; 18°51'42"E) in False Bay on the south coast (Figure
Sites along the South African coast where the ecological impacts of Ciona robusta were quantified.
During the austral winter of 2012 and 2014, 18 experimental arrays were deployed in Saldanha Bay and False Bay. This season was chosen as this is when the peak settlement of C. robusta occurs in this region (
Species richness (i.e., total number of species) and the Shannon-Wiener diversity index (H’), which incorporates both species richness and evenness (
Ciona robusta only settled on experimental plates in Saldanha Bay, despite pre-experiment surveys recording this ascidian in Gordons Bay and the presence of low densities of adults on marina infrastructure during the experiment. As such Gordons Bay was excluded from all analyses. In Saldanha Bay, both the number and biomass of individuals removed from the treatment plates were affected by ‘depth’ (density: F1,21=24.32, p<0.0001, biomass: F1,21=24.16, p<0.0001) with significantly lower abundances occurring on shallow plates (density: t=-2.16, p<0.05; biomass: t=-1.71, p<0.05) (Figure
In total, 58 fouling species were recorded in our study, of which 57% were only present in 2012. While a total of seven non-indigenous species were recorded, only C. robusta, the colonial bryozoan Bugula neritina and the lightbulb ascidian Clavelina lepadiformis were present in both years, while the remaining four species (the ascidian Diplosoma listerianum, the amphipod Jassa marmorata, the hydrozoan Obelia dichotoma and the bryozoan Waterspora suborquata) were present only in 2014, despite fewer species being recorded in that year. Only one species, C. lepadiformis, was restricted to removal treatment plates. There was a significant effect of ‘year’ on species richness and a significant interaction between ‘year’ and ‘depth’ (Table
Changes in diversity. Mean (±SE) species richness and Shannon-Wiener index (H’) recorded in 2012 (a, b) and 2014 (c, d). Both measures of diversity were significantly affected by year (p<0.01) and a significant interaction between year and depth (p<0.01).
GLM results considering the effect of ‘year’, ‘depth’ and ‘treatment’ on (a) species richness and (b) the Shannon-Wiener diversity index (H’). ns = non-significant.
|Factor||df Effect||Null deviance||F-ratio||p-value|
|(a) Species richness|
|Year × Treatment||2||3.1||1.1||ns|
|Year × Depth||1||12.8||9.3||p<0.01|
|Treatment × Depth||2||0.4||0.2||ns|
|Year × Treatment × Depth||2||2.6||0.9||ns|
|Year × Treatment||2||0.2||1.2||ns|
|Year × Depth||1||1.2||15.4||p<0.001|
|Treatment × Depth||2||0.009||0.1||ns|
|Year × Treatment × Depth||2||0.2||1.3||ns|
Community assemblages differed significantly among years and were affected by an interaction between ‘year’ and ‘depth’ (Table
Community composition. Multi-dimensional scaling (MDS) plots of community assemblages formulated using fouling (a) biomass and (b) % cover of treatment, treatment control and control panels in two years at two depths.
Test statistics for a main effects PERMANOVA considering the effect of year, treatment and depth on fouling (a) biomass and (b) % cover. ns = non-significant.
|Year × Treatment||2||2506||1253||1.2||ns|
|Year × Depth||1||5032||5032||4.8||p<0.001|
|Treatment × Depth||2||2493||1246||1.9||ns|
|Year × Treatment × Depth||2||1291||646||0.6||ns|
|(b) % cover|
|Year × Treatment||2||3803||1969||1.8||ns|
|Year × Depth||1||6712||5644||9.4||p<0.05|
|Treatment × Depth||2||2113||1746||2.1||ns|
|Year × Treatment × Depth||2||1394||452||0.3||ns|
Alien species can have ecological, socio-economic and human health impacts in recipient regions (
Although previous studies have recorded dense settlement of C. robusta in Saldanha Bay (in 1994 an average density of more than 1000 individuals/m2 was recorded at a depth of 3m (
While the impacts of alien species are often measured at different locations within a region (e.g.
Yacht Port Marina and Gordons Bay Yacht Club are thanked for allowing us to run the fieldwork component of this project in their marinas. Jonathan Jonkers and Koebraa Peters are thanked for help in the field. BH and MvdM gratefully acknowledge bursaries from the DST-NRF Centre of Excellence for Invasion Biology and the Department of Botany and Zoology, Stellenbosch University respectively. Running costs were provided by DST-NRF Centre of Excellence for Invasion Biology. SJ gratefully acknowledges a grant from the Marine Living Resources Fund.