ORIGINAL RESEARCH

 

Alien animals in South Africa - composition, introduction history, origins and distribution patterns

 

 

Mike D. Picker^I; Charles L. Griffiths^{I, II}

^IDepartment of Biological Sciences, University of Cape Town, South Africa
^IICentre of Excellence for Invasion Biology, University of Cape Town, South Africa

Correspondence

 

 

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ABSTRACT

BACKGROUND: There is no comprehensive inventory and analysis of the composition, distribution, origin and rate of introduction of the alien fauna of South Africa.
OBJECTIVES: To provide such an analysis to facilitate effective ecological management, and compile a comprehensive inventory of introduced animal species across major habitats.
METHODS: All available databases and references were used to compile the inventory, forming the basis of subsequent analyses. A graduated map was produced to identify concentrations of alien species
RESULTS: Of the 571 alien animal species analysed, insects comprised the largest component (53%, 300 species), followed by molluscs (9%, 51 species), annelids (8%, 48 species), arachnids (7%, 41 species), vertebrates (7%, 41 species) and crustaceans (6%, 36 species). Vertebrate introductions (88%) were largely intentional, whereas 84% of invertebrate introductions were unintentional.
CONCLUSIONS: Almost all marine and most terrestrial alien species were accidentally introduced, whereas freshwater introductions were almost entirely intentional. Some 13% had not spread significantly, 16% had spread significantly and 71% had become fully invasive. Vertebrate introductions virtually ceased after the 1950s, but rate of introduction of invertebrates remained linear. The overall rate of species accumulation was fairly low until 1880, but accelerated sharply thereafter. Most terrestrial alien species originated from Europe (28.6%) and Asia (25.0%) and the lowest proportion (6.1%) from Africa. Freshwater introductions largely originated from the Americas, with few from Africa. The most invaded areas were around Cape Town, (up to 162 introduced species/half-degree grid cell), followed by Gauteng and Durban.

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Introduction

The distribution patterns and impacts of the approximately 750 tree and 8000 herbaceous plant species that have invaded over 10 million hectares of land in South Africa (Department of Environmental Affairs and Tourism [DEAT] 2006) have been extensively documented (Henderson 2001; Joubert 2009; Macdonald, Kruger & Ferrar 1986; Macdonald et al. 2003; Richardson & Van Wilgen 2004; Wilson et al. 2014). Much less has been published on the introduced fauna, although previous reviews have listed alien animals within some specific habitats or regions or within specific taxonomic groups. These include listings of the introduced fauna of South African aquatic ecosystems (De Moor & Bruton 1988) and South African National Parks (Spear et al. 2011) and several reviews documenting progressively increasing numbers of introductions into the marine environment (Griffiths et al. 1992; Griffiths, Robinson & Mead 2009; Mead et al. 2011a, 2011b; Robinson et al. 2016). Introduction pathways for South African vertebrates, invertebrates and plants have been compared and temporal patterns of invasion via the defined pathways examined (Faulkner et al. 2016). In taxonomic terms, the alien vertebrates have received a fair amount of research interest (Brooke, Lloyd & De Villiers 1986), with various reviews devoted to introduced mammals (Skead 2011), birds (Dean 2000), reptiles (van Wilgen et al. 2010) and fishes (De Moor & Bruton 1988; Ellender & Weyl 2014; Griffiths, Day & Picker 2015). Less attention has been devoted to invertebrate groups, but there have been some attempts to list the introduced species within specific taxa such as terrestrial molluscs (Herbert 2010) and earthworms (Plisko 2010), or functional groups such as biological control agents (Klein 2011). Reviews of the pests of cultivated plants (Annecke & Moran 1982; Prinsloo & Uys 2015; Visser 2009) also incorporate many species that are introduced. However, until recently no attempt had been made to produce an inventory of the entire regional alien fauna. The first such listing appeared in the semi-popular book by Picker and Griffiths (2011). The draft National Environmental Management Biodiversity Act: Alien and Invasive species list (Republic of South Africa 2014, Notice 3: National Lists of Invasive Species, lists 3-10) also provides incomplete listings of various groups of faunal invasives, which in fact also include numerous species that have not yet invaded any part of South Africa. For example, list 5 of the Invasive List (Notice 3) mentions 35 alien reptile species - none which has been recorded as an established alien, but fails to list the single species which is an established invader (Brahminy blind snake, Ramphotyphlops braminus)!

The aims of this paper are to analyse the most comprehensive available listing of alien animal species of South Africa, that in Picker and Griffiths (2011), in terms of invaded habitat, taxonomic composition of the fauna, proportions of intentionally and unintentionally introduced species, invasion status, historical rate of accumulation of species, geographical origins of the fauna and spatial distribution across the region. These analyses provide baselines against which to measure future rates and patterns of faunal invasion in the region and also allow for comparisons of invasion rates and patterns between the various taxa and across the different habitats examined, as well as between South Africa and other regions. The species listing provided in the Appendix also documents which species have (or have not) in fact been reported in the region and can provide a basis for updated legislation, be used to compare listing from other regions, etc.

 

Methods

This analysis is based entirely on the listing of 571 alien species given in Picker and Griffiths (2011). Species documented after 2011 are excluded, as are translocated species and cryptogenic marine species (as listed by Mead et al. 2011a, 2011b). Data from the Appendix of Picker and Griffiths (2011) were used for the analysis of taxonomic composition, geographical origin and species richness of the South Africa alien fauna. All 571 species listed in the Appendix of Picker and Griffiths (2011) were also used for the analysis of modes of introduction and for the species accumulation curves. The original sources of data from which the listing in Picker and Griffiths (2011) were derived included various earlier reviews (Annecke & Moran 1982; Coates 1970; Herbert 2010; Heyns 1971; Klein 2011; Mead et al. 2011b; Millar 1994; Plisko 2010; Visser 2009) and scattered taxonomic papers as cited under the individual species entries in Picker and Griffiths (2011). In cases where only a subset of the data could be used (viz. Figures 2 and 3), the number of species used and source of data are given in the figure legends.

 

 

 

 

 

When examining the invasion status of species, we followed the framework proposed by Blackburn et al. (2011) and applied these categories to the 220 species featured in Picker and Griffiths (2011) for which we deemed the distribution sufficiently well known to be evaluated. Species were considered to have remained restricted to the site of entry (Category C3) if their distribution was mapped as a point entry (or two points in the case of multiple known sites of introduction, e.g. to two harbours). Species were considered to have 'spread significantly' (Category D) if they had expanded < 100 km from site of entry and to be fully invasive (Category E) if they had spread > 100 km or occupied numerous sites (e.g. several widespread cities). In analysing geographical origin of the alien fauna, we used the seven-continent model. Where the native range of a species spanned two continents, each continent was scored 0.5 for that species, and where the home range spanned three continents, each received a score of 0.33. This accounts for the fractional scores shown in terms of numbers of species originating from the various continents. Assigning a full score to a species that occurs naturally on two continents would effectively bias the scores, as it would assume that the species had been introduced twice, once from each source continent and thus give it a double weighting. For parsimony, the fractional scores assume each species has been introduced from a single continent within its natural range.

When defining the mode of introduction as either intentional or unintentional, we consider species to be unintentional introductions only if they arrived inadvertently into the region, typically through association with crops, on ships' hulls and ballast water, etc. Species are considered as intentional introductions both if purposely introduced directly into the wild, for example, as ornamentals, biological control agents or targets for hunting or fishing, or if introduced intentionally into captivity/aquaculture, from where they subsequently escaped and established in the wild. The mode of introduction was assessed for species in the Appendix of Picker and Griffiths (2011) using original sources of data as listed above.

Dates of introduction were bracketed by decade. While dates of introduction of vertebrates are generally quite accurately known, the date of discovery for the more cryptic invertebrates commonly postdates the true date of introduction, sometimes by decades. Species accumulation curves were plotted separately in Excel 2013 for invertebrates, for vertebrates and for all taxa combined. The slopes of the fitted curve for all taxa combined were calculated separately for the period 1750-1880, which was a period of limited colonisation, and for the period 1880-2000, which was a period of greater international trade initiated by the discovery of diamonds in Kimberley (1871) and gold in the Witwatersrand (1884), the Anglo-Boer wars (1880-1881; 1899-1902) and by immigration of Indian labourers in 1860 for the growing sugarcane industry in KwaZulu-Natal (Christopher 1994). The 1880-2000 curve was extrapolated in Excel 2013.

A graduated map showing the species richness of the alien fauna per half-degree square in South Africa was generated from Picker and Griffiths (2011), using those 242 species for which adequate distributional data were presented. Hardcopies of individual distribution maps for each of these species were scanned and superimposed over a visual half-degree grid map of matched scale to generate a visual half-degree grid map showing the number of alien species in each grid cell. Marine species were included in cells bordering the coastline, meaning that cells falling over both land and sea contain both terrestrial and marine species. From this visual grid, a half-degree cover was constructed for South Africa, and the species count data were transferred from the Excel grid to the grid feature class in ArcGIS 10.3.1. The grid was then symbolised using the 'Graduated Colour' symbology option with seven classes. This was subsequently converted to greyscale in Corel Photo-Paint X3.

 

Results

Composition of the fauna

Of the 571 alien animal species analysed, the largest taxonomic component comprised the Insecta (300 species; 53% of the fauna), followed by Mollusca (51; 9%), Annelida (48; 8%), Arachnida (41; 7%) and Crustacea (36; 6%). These five groups together comprised 83% of the total introduced fauna (Table 1 and Appendix 1). Vertebrates (sum of Mammalia, Aves, Reptilia and Pisces, there being no alien Amphibia in this region [Measey et al. 2017]) were represented by just 41 species and only accounted for 7% of the alien fauna. Of the species listed, 452 (79%) were terrestrial, 79 (14%) marine and only 40 (7%) freshwater (Table 1 and Appendix 1).

 

 

The taxonomic composition of the introduced fauna varied dramatically across the different habitats. All marine introductions were invertebrates, with typically diverse marine groups, such as Ascidiacea, Crustacea, Annelida, Mollusca and Cnidaria, each well represented (11%-29% of the marine fauna). By far, the most important group in freshwater systems was Pisces (43% of the fauna), followed by Mollusca (20%) and then Crustacea (12%). The terrestrial fauna was dominated by Insecta (65%), followed by Arachnida, Annelida and Mollusca (7%-9% each).

Mode of introduction

The modes of introduction of 571 species could be determined. Of these species 41 were vertebrates, of which 36 (88%) were intentional introductions and only five unintentional (three rodents, one bird and one reptile). By contrast, the 530 invertebrate species comprised 91 (17%) intentional introductions, 82 (16%) of which were introduced as biological control agents, and 439 (83%) unintentional introductions (Table 2).

 

 

When the mode of introduction was separated by habitat (Figure 1), other interesting patterns emerged. The marine fauna comprised almost exclusively accidentally introduced species, the two exceptions being oysters intentionally introduced as aquaculture species but which subsequently escaped from captivity and established feral populations. The terrestrial component comprised about 20% intentional introductions, the majority of which were biological control agents. The freshwater fauna was dominated by fishes or crustaceans that were released intentionally as fishery targets, forage species or as biological control agents, or were intentionally introduced into captivity as ornamentals or aquaculture species, but subsequently escaped to establish feral populations (see Marr et al. 2017 for a proposed risk assessment procedure for future fish introductions).

Establishment category

Of the 240 species assessed (Table 3), only 13% remained restricted to their site of origin (Category C3), 16% had spread significantly (Category D) and 71% were fully invasive at multiple sites (Category E). These proportions varied considerably between taxa and systems. Site-restricted forms made up the highest proportions among marine invertebrates (many of which remain confined to the harbours to which they were introduced) and among terrestrial vertebrates. Category D species were most common among vertebrate groups, especially freshwater ones (which often occupy delimited habitats such as dams). Fully invasive species were particularly dominant among the terrestrial and marine invertebrates, both of which are characterised by high mobility (via flight in the case of insects and pelagic larval stages in the case of marine invertebrates).

Date of introduction

Few introduced species were detected prior to the 1880s, although many, including crop pests and marine fouling species, may have been introduced well before that date. Vertebrate introductions, almost all of which were intentional (see above) occurred steadily since that time, but became rare after the 1950s (Figure 2a). By contrast, the rate of introduction of invertebrates has remained virtually linear since the late 1800s, when proper documentation began (Figure 2a). When the rate of detection curve was broken into two components - an early phase of invasion history (1800-1880) and a period of burgeoning international travel and trade (1880-2000) - the fitted curves showed markedly differing slopes, with the more recent period having a much steeper slope (0.65) than the earlier period (0.16). The extrapolated curve maintained the steep slope and predicts a high future rate of accumulation of alien species (Figure 2b), the great majority of which are likely to be invertebrates.

Geographical origin of the South African alien fauna

For the terrestrial fauna, the majority of species were derived from Europe (28.6%) and Asia (25.0%), with the lowest proportion (6.1%) from other parts of Africa (Figure 3, cf. Faulkner et al. 2017). The component derived from Australia (9.3%) mostly comprised biological control agents. In contrast, the introductions of freshwater alien fauna originated mostly from North America (32.4%), South America (23.5%) and Asia (23.5%). The other continents contributed far fewer species (< 5%) each respectively (Figure 3). The areas of origin of the marine fauna are based on a different set of oceanic, rather than continental, bioregions and have previously been plotted by Mead et al. (2011a), so are not re-examined here.

Intensity of faunal invasion across South Africa

The highest densities of introduced animal species (130-162/half-degree grid cell) occurred in the extreme south-western parts of the Western Cape Province, near Cape Town, followed by the highly populated regions around Gauteng and Durban (Figure 4). The southern and eastern coastal regions, as well as the summer rainfall regions in the Northeast, also had fairly high alien animal species richness. The lowest number of alien species (46-57/half-degree grid cell) occurred in the north-western semi-arid interior of the country. Because coastal cells contain both marine and terrestrial species, this accounts for some increase in the number of species in those cells, but in fact marine species represent a relatively low proportion of the total, except in a few harbour cities, such as Cape Town (42 marine species), Durban (31), Saldanha and Port Elizabeth (both 25) (Mead et al. 2011a).

 

 

Discussion

The 571 alien animal species in South African analysed here certainly represent an underestimation of the true number of alien animals present in the region. Newly introduced species are constantly invading the region and several such new invasions are reported each year. In addition, long-established historical invasions are also being revealed as a result of new ecological surveys or taxonomic revisions, for example, Mead et al. (2011a) uncovered several marine invasions that were associated with dry ballast or wooden vessels and had thus probably remained undiscovered for a century or more. Species may of course also be lost from the fauna, if local populations that were recorded as introduced in South Africa in the historical literature become locally extinct. Such losses can be difficult to detect, but see documentation of the recent local extinction of an alien sea urchin by Mabin, Wilson and Robinson (2015).

While the number of alien vertebrates (41; 7% of all alien species) is considered to be relatively well documented (Picker and Griffiths 2011), the tally of alien invertebrates is certainly a considerable underestimation linked to South Africa's relatively low 'country development status' (McGeoch et al. 2010), which results in resource limitation constraining the state of knowledge of biological invasions. This is best illustrated by comparing the inventory presented here with that produced by the DAISIE Project (Delivering Alien Invasive Species Inventories for Europe), one of the most comprehensive and detailed inventories of any alien fauna. The DAISIE Project records 2740 terrestrial invertebrate species in Europe compared to only 441 species for South Africa (DAISIE 2008). A similar situation exists in the marine environment. Although the number of recorded alien animals in the South African marine environment has increased dramatically in recent years, from 22 species reported by Griffiths et al. (2009) to 79 species recorded here, this is still far less than the 986 alien marine species recorded for Europe (Hulme et al. 2009). This is because many marine habitats (e.g. soft sediments of harbours) and taxa (e.g. Nematoda, Copepoda, Ostracoda and many parasitic taxa) remain poorly sampled for introduced species in South Africa and surely contain many more alien species. Additional factors, such as different duration and intensity of introduction histories and differences in the diversity of available habitats, may also contribute towards these regional differences.

The differences in the composition of the introduced faunas among major habitat types reflect (1) natural differences in biodiversity and faunal composition of terrestrial, marine and freshwater faunas and (2) differences between vectors that have transported these species. The dominance of the alien terrestrial fauna by insects is a reflection not only of the enormous natural diversity and species richness of this group in terrestrial systems but also of their importance as crop pests and their frequent use as biological control agents. Similarly, ascidians, echinoderms, bryozoans and cnidarians are all overwhelmingly marine groups and hence feature more prominently in the marine listing. However, it is of interest to note that no marine fishes have been introduced to South Africa, and no introduced marine nematodes have been reported, despite their high diversity in marine habitats. The latter is probably an artefact of poor sampling and lack of taxonomic expertise in marine nematodes, as numerous invasive nematodes have been reported from other regions, such as Europe (DAISIE). The high diversity of fishes among freshwater introductions stems from their frequent intentional introduction as sport-fishing targets, ornamental and forage species, or as biological control agents. This pattern was not paralleled in marine habitats, where sport-fishing targets are common among the indigenous fish fauna and no intentional alien fish introductions have taken place (other than of species that remain restricted within aquaculture facilities).

Our analysis of degree of establishment of species within the alien fauna suggests that 13% of analysed species have failed to spread from their sites of introduction, 16% have spread significantly (< 100 km) and 71% are fully invasive. However, as this analysis is based on species featured as full entries in the review by Picker and Griffiths (2011), it is (apart from the vertebrates) biased in favour of 'important' invasions, which also tend to be those that have spread widely. In addition, species with wider distributions are more likely to have been discovered, and their distribution is more likely to have been mapped when compared to those that remain localised. Thus, we suspect that that species in the early stages of invasion in fact make up a larger component of the fauna than this analysis suggests.

The initial rate of accumulation of the South African alien fauna was slow. During this period of early colonialism, the first Dutch settlers gradually expanded settlements into the interior and eastern parts of South Africa, with the last frontiers of the Northern and Eastern Cape and northern KwaZulu-Natal being breached by colonialists around 1900. During the last decades of the 19th century (1880 onwards), the numbers of alien species increased steeply, with the slope of the accumulation curve increasing from 0.16 to 0.65. This coincided with the discovery of diamonds in Kimberley (ca. 1871) and then gold on the Witwatersrand (1884) - both events galvanising urbanisation, international travel and trade links, which led to increased immigration rates (Christopher 1994; Deacon 1986). The dramatic increase in trade because of the mining industry was also associated with the industrialisation of ports. All these factors contributed to the steep increase in the number of alien animals since 1880. It should be noted that while these figures were derived from species whose invasion history is well known, many (invertebrate) species are only being discovered long after their first date of introduction, and some species may have multiple dates of introduction. The pattern of invasion by alien species in Europe differs in many respects from that in South Africa. In Europe, there was no noticeable increase in the number of new species between the period 1951-1970 and the period 1971-1990 in marine and freshwater habitats, apart for marine invertebrates, which had a steep increase during the period 1951-2007 (Hulme et al. 2009). No new alien birds or mammals colonised Europe after 1951, comparable with the situation in South Africa, where few new alien vertebrates colonised after 1930. However, the number of escapee species appears to be increasing with time (Faulkner et al. 2016). In Europe there was a fairly steep increase in the number of new alien insects after 1951 and a flatter curve for new alien non-insect arthropods. In South Africa the curve was linear and steep after 1890. Roques et al. (2009) estimated that 60% of the alien insect fauna of Europe only established in the last 50 years. A similar trend is evident for South Africa (Figure 2), where approximately 50% of invertebrate introductions occurred prior to 1960. The major pathways for the introduction of South African alien invertebrates (besides deliberate release as biocontrol agents) were as contaminants and stowaways with the number of released biocontrol agents increasing sharply after 1970 (Faulkner et al. 2016). In contrast, the introduction of invertebrates as stowaways and contaminants was gradual in the 1900s and accelerated in the 2000s (Faulkner et al. 2016). The curve may thus not have been influenced to a large degree by biocontrol agents, as few had been introduced at the beginning of the 20th century and comprised only 21% of the 530 alien invertebrates considered here. See also Faulkner et al. (2017) for a discussion of introductions from other African countries.

The highest concentration of marine alien species in South Africa occurs in the vicinity of major urban areas, especially ports, which were the entry point for many groups of alien invaders, including plants (Deacon 1986). For animals, the highest density of terrestrial alien species (130-162 species/half-degree grid square) occurs in the metropolitan area of Cape Town. This area is the oldest port in South Africa, and its Mediterranean-type climate also provides a suitable eco-climatic match for alien fauna from the temperate regions of Europe and North America, with which the developing colony conducted most of its trade (Tribe & Richardson 1994). Interestingly, some alien vertebrates, such as the grey squirrel and European chaffinch, both introduced to Cape Town in the 1890s, have not managed to substantially extend their ranges further into the fynbos biome in over 100 years.

The least invaded region, with less than 50 introduced species per half-degree cell, is restricted to the arid, low population density areas of the Northern Cape in the interior of the country. Many of the alien species here are widely distributed species associated with human habitation, such as mice, house sparrows, cockroaches, booklice and pests of domestic stock and stored products (see individual maps in Picker & Griffiths 2011). The low densities of alien animals in the semi-arid interior may also be related to low habitat diversity and poor ecoclimatic matching of that area. Most of the country has 50-100 introduced animal species per half-degree grid square. Areas with more than 100 species comprise the urban centres surrounding Johannesburg, Pretoria and Durban, plus a broad coastal swath running from Port Elizabeth to Cape Town. Cape Town and its close surrounds stand out as the only region with over 150 species (largely invertebrates) and represent by far the most heavily invaded area of the country. This is similar to the situation in Europe, where both alien plants and insects were found to be associated most closely with urban habitats (parks and gardens), followed by cultivated lands (Pyšek et al. 2010). Sampling intensity may also play some role here, as urban habitats also tend to be adjacent to research institutions and this may result in their being more intensively surveyed than more remote regions of the country.

 

Acknowledgements

Our thanks to the specialist authors of chapters in the book 'Alien and Invasive animals - a South African perspective', without whose input this paper would not have been possible. Shona Troost assisted with the extraction of mapping data, and Thomas Slingsby and Nick Lindenberg provided valuable advice and assistance with the mapping. Three anonymous reviewers are thanked for their useful comments on earlier drafts of the manuscript.

Financial support for this study and towards publication of the book on which this analysis is based was provided by the National Research Foundation-Department of Science and Technology Centre of Excellence for Invasion Biology.

Competing interests

The authors declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.

Authors' contributions

M.D.P. and C.L.G. contributed equally to the compilation of the inventory, data analysis and writing of the manuscript.

 

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Correspondence:
Mike Picker
mike.picker@uct.ac.za

Received: 05 Aug. 2016
Accepted: 31 Oct. 2016
Published: 31 Mar. 2017

 

 

 Note: This paper was initially delivered at the 43rd Annual Research Symposium on the Management of Biological Invasions in South Africa, Goudini Spa, Western Cape, South Africa on 18-20 May 2016.

 

 

Appendix 1

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