Tamara B. Robinson

Marine alien species of South Africa — status and impacts

The current status of marine alien species along the South African coast is reviewed and the ecological and economic impacts of these invasions are discussed. In all, 10 confirmed extant alien and 22 cryptogenic species are recorded from the region. All 10 alien species support well-established populations and the majority of these remain restricted in distribution to sheltered bays, estuaries and harbours. Only one species, the Mediterranean mussel Mytilus galloprovincialis, has spread extensively along the coast and caused significant ecological impacts. These include the competitive displacement of indigenous species and a dramatic increase in intertidal mussel biomass. These changes have also increased available habitat for many infaunal species and resulted in enhanced food supply for intertidal predators. Considerable economic benefits have also resulted from this invasion because M. galloprovincialis forms the basis of the South African mussel culture industry.

Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach

Invasion ecology urgently requires predictive methodologies that can forecast the ecological impacts of existing, emerging and potential invasive species. We argue that many ecologically damaging invaders are characterised by their more efficient use of resources. Consequently, comparison of the classical ‘functional response’ (relationship between resource use and availability) between invasive and trophically analogous native species may allow prediction of invader ecological impact. We review the utility of species trait comparisons and the history and context of the use of functional responses in invasion ecology, then present our framework for the use of comparative functional responses. We show that functional response analyses, by describing the resource use of species over a range of resource availabilities, avoids many pitfalls of ‘snapshot’ assessments of resource use. Our framework demonstrates how comparisons of invader and native functional responses, within and between Type II and III functional responses, allow testing of the likely population-level outcomes of invasions for affected species. Furthermore, we describe how recent studies support the predictive capacity of this method; for example, the invasive ‘bloody red shrimp’ Hemimysis anomala shows higher Type II functional responses than native mysids and this corroborates, and could have predicted, actual invader impacts in the field. The comparative functional response method can also be used to examine differences in the impact of two or more invaders, two or more populations of the same invader, and the abiotic (e.g. temperature) and biotic (e.g. parasitism) context-dependencies of invader impacts. Our framework may also address the previous lack of rigour in testing major hypotheses in invasion ecology, such as the ‘enemy release’ and ‘biotic resistance’ hypotheses, as our approach explicitly considers demographic consequences for impacted resources, such as native and invasive prey species. We also identify potential challenges in the application of comparative functional responses in invasion ecology. These include incorporation of numerical responses, multiple predator effects and trait-mediated indirect interactions, replacement versus non-replacement study designs and the inclusion of functional responses in risk assessment frameworks. In future, the generation of sufficient case studies for a meta-analysis could test the overall hypothesis that comparative functional responses can indeed predict invasive species impacts.

Existing and emerging high impact invasive species are characterized by higher functional responses than natives

Predicting ecological impacts of invasive species and identifying potentially damaging future invaders are research priorities. Since damage by invaders is characterized by their depletion of resources, comparisons of the ‘functional response’ (FR; resource uptake rate as a function of resource density) of invaders and natives might predict invader impact. We tested this by comparing FRs of the ecologically damaging ‘worlds worst’ invasive fish, the largemouth bass (Micropterus salmoides), with a native equivalent, the Cape kurper (Sandelia capensis), and an emerging invader, the sharptooth catfish (Clarias gariepinus), with the native river goby (Glossogobius callidus), in South Africa, a global invasion hotspot. Using tadpoles (Hyperolius marmoratus) as prey, we found that the invaders consumed significantly more than natives. Attack rates at low prey densities within invader/native comparisons reflected similarities in predatory strategies; however, both invasive species displayed significantly higher Type II FRs than the native comparators. This was driven by significantly lower prey handling times by invaders, resulting in significantly higher maximum feeding rates. The higher FRs of these invaders are thus congruent with, and can predict, their impacts on native communities. Comparative FRs may be a rapid and reliable method for predicting ecological impacts of emerging and future invasive species.

Oysters as vectors of marine aliens, with notes on four introduced species associated with oyster farming in South Africa

Translocated oysters are well known to act as vectors of marine alien species, but to date this topic has received scant attention in South Africa, despite the fact that oysters have been imported into this region since 1894. Surveys of oyster farms in South Africa revealed four newly-recorded alien species: the black sea urchin, Tetrapygus niger, from Chile; the European flat oyster, Ostrea edulis (thought to be extinct since its intentional introduction in 1946); Montagus crab, Xantho incisus, from the North Eastern Atlantic seas of Europe, and the brachiopod Discinisca tenuis from Namibia. Oyster imports are the most likely vector of all these species. The biological attributes of each species, the possible threats posed by their introduction, and the needs for additional control measures to limit or prevent further introduction and spread of alien species via oyster culture are discussed.

NATURALIZED POPULATIONS OF OYSTERS, CRASSOSTREA GIGAS ALONG THE SOUTH AFRICAN COAST: DISTRIBUTION, ABUNDANCE AND POPULATION STRUCTURE

Abstract The Japanese oyster Crassostrea gigas forms the mainstay of the South African oyster farming industry. Despite having been cultured along the South African coast for 30 years, this is the first record of naturalized populations of this well known global invader from the region. DNA sequence data confirmed the presence of C. gigas in the Breede and Goukou estuaries. Populations of 184,206 ± 21 058.9 (SE), 876 ± 604.2 (SE) and 1 228 ± 841.8 (S.E.) individuals were recorded in the Breede, Goukou and Knysna estuaries respectively. No C. gigas were recorded from the open coast. The condition index of oysters in the Goukou and Knysna estuaries differed significantly from those in the Breede Estuary (Kruskal-Wallis ANOVA H = 48.249, P < 0.01) but no difference was found between the Goukou and Knysna estuaries (Kruskal-Wallis ANOVA H = 48.249, P > 0.05). The lower condition index recorded in the Breede Estuary is believed to reflect decreased food supply as a result of the large C. gigas population present in the estuary.

The Status and Distribution of Marine Alien Species in South Africa

No geographcally or taxonomically comprehensive census of marine alien species has ever been undertaken in South Africa and the state of knowledge of the taxonomy of many marine invertebrate groups remains poor in this region (Gibbons 1999), compromising the ability to detect introduced species. Given these constraints, 22 confirmed extant marine aliens, plus 18 cryptogenic species, have been recorded from South African waters to date, with one additional species recently found in on-land mariculture facilities (Simon and Booth, in press). The true number of introduced species may well exceed these estimates by several times (see also Chap. 2, Carlton). All 22 of the marine alien species reported from the wild support wellestablished populations, but the majority of these remain restricted to the few sheltered bays, estuaries and harbours on this wave-exposed coastline. Interestingly, only three species are known to have become invasive (defined here as having spread significantly beyond their points of origin). These are the Mediterranean mussel Mytilus galloprovincialis, the European green crab Carcinus maenas (Griffiths et al. 1992; Robinson et al. 2005a) and the recently detected barnacle Balanus glandula (Laird and Griffiths, 2008). A list of species known to be introduced to the region, and which presently support populations is given in Table 23.1. Sites mentioned in this chapter are shown in Fig. 23.1. The various established species are discussed by taxonomic group below.

Invasion of Langebaan Lagoon, South Africa, by Mytilus galloprovincialis – effects on natural communities

In 1992 the invasive mussel Mytilus galloprovincialis began establishing beds on the centre sandbanks of Langebaan Lagoon. This global invader had previously been restricted to rocky shores along the South African coastline. In order to investigate the effect of the invasion on naturally-occurring communities, a comparative study between invaded areas and areas clear of invasion was conducted. Communities in these areas differed significantly (ANOSIM, R = 0.685, P < 0.01). The biomass supported in invaded areas (53 262 g/m2), was significantly greater than that in clear areas (1133 g/m2), (Mann-Whitney, U = 225, P < 0.001). Invertebrate densities supported in invaded (6780.1 individuals/m2) and clear areas (835 individuals/m2) were also significantly different, (Mann-Whitney, U = 219, P < 0.001). Of the 66 species recorded, only 33 % occurred in both clear and invaded areas (often in very different densities), 41 % occurred exclusively in invaded areas, and 26 % were restricted to non-invaded areas. These figures indicate a replacement of the naturally-occurring sandbank communities by those more typical of rocky shores. It is thus recommended that the invasive mussel beds be removed to conserve the natural biota of the centre banks, which lie within a national park.

A Brief History of Marine Bio-Invasions in South Africa

Marine species have been introduced continuously into South Africa for more than 400 years, since the arrival of the first European explorers. Various waves of introduction can be identified over this period, each associated with a different mix of vectors. Early wooden vessels carried specialized wood-boring species, a rich external fouling community, plus semi-terrestrial species associated with dry ballast. Modern steel vessels continue to import fouling species, despite the use of anti-fouling paints, and may ply new routes, bringing additional introductions from novel locations. More modern waves of introduction are associated with use of ballast water and with marine aquaculture. Research on marine bio-invasions in South Africa has a short history, marked by a rapid rate of discovery of introductions. Some 86 marine species are currently regarded as introduced to the region, with a further 39 considered cryptogenic, but this number is increasing rapidly. Moreover, many taxa and regions still remain inadequately explored, indicating that the current list remains far from complete. The reasons for under-reporting of introduced populations are discussed and include lack of sample coverage, misidentification of aliens as native species and erroneous redescriptions of aliens as new, indigenous species. However, the lack of taxonomic expertise across large sections of the biota remains the greatest impediment to progress.

Patterns of endemicity and range restriction among southern African coastal marine invertebrates

Southern Africa supports a rich marine biota of 12 734 currently described marine species. Although the distribution and overall species-richness patterns of several component taxa are well documented, studies considering range sizes are absent. This study considers range size frequencies and distribution patterns of seven major marine invertebrate taxa. The most commonly observed pattern of size frequency distributions is bimodal, with a predominance of species with either small or large range sizes, and few taxa with intermediate-sized ranges. This pattern is displayed by prosobranch and opisthobranch molluscs, polychaetes and amphipods, and for all invertebrate taxa examined combined. Peaks in small range sizes are likely a reflection of the numerous poorly sampled and/or endemic species in the region, while the high number of species with large range sizes can be attributed to the large proportion of widespread tropical Indo-Pacific species within the regional fauna. Overall, the largest peaks of range-restricted endemic species occurred around False Bay, Port Elizabeth, Durban, St Lucia and Maputo Bay. These areas are all situated at or adjacent to recognised biogeographic breaks for invertebrate assemblages, but coincidentally also tend to also be areas of enhanced research and shipping activity. The Cape Point region supports the highest number of endemics, with 73 species restricted to ranges of <100 km and 28 species to ranges <200 km.

Changes in habitat complexity resulting from sequential invasions of a rocky shore: implications for community structure.

Worldwide, marine rocky shores are being modified by alien species, but their successive impacts are rarely recorded. We documented sequential invasions of Marcus Island on the west coast of South Africa by comparing communities from 1980 (pre-invasion), 2001 (after invasion by the mussel Mytilus galloprovincialis) and 2012 (following invasions by another mussel, Semimytilus algosus, and the barnacle Balanus glandula). Their influence on habitat complexity was measured with a novel technique enabling retrospective calculation of historical complexity. In 1980, habitat complexity, invertebrate abundance and species richness decreased from the low-shore to the high-shore, but homogenised in 2001 after M. galloprovincialis elevated habitat complexity across most of the shore. In 2012, these variables returned to pre-invasion patterns, after M. galloprovincialis declined in the high-shore and was replaced there by B. glandula. With the first mussel invasion, several indigenous species extended up the intertidal, but retreated once M. galloprovincialis receded. Community composition differed significantly among nearly all years and zones, irrespective of whether the alien species were included in the analyses or not. Some once-dominant native species were negatively affected by the invasions: one indigenous mussel, Choromytilus meridionalis, disappeared by 2012, and another, Aulacomya atra, declined. The abundance of recruits of the limpet Scutellastra granularis rose and fell with the arrival and recession of M. galloprovincialis, but adults were adversely affected. Changes to habitat complexity induced by sequential invasions supported hypothesised changes in invertebrate abundance and species richness, but could not alone predict changes in community composition, which were also influenced by zonation.