DRAFT 1

Aquatic invasion risks posed by the aquarium trade, aquarists and the internet trade in South Africa

G.D. Martin*

Department of Zoology and Entomology, Rhodes University, Grahamstown, 6140

Abstract

Submerged aquatic invasive plant species are increasingly being recognised as a major threat to South African water ways. Pet stores, aquarists and the internet mediated trade were investigated as vectors for submerged invasive macrophytes introductions into South Africa. Online and manually distributed surveys were used to determine the extent of movement of invasive as well as indigenous submerged plant species in South Africa. Thirty four pet stores and 23 aquarists were interviewed. Results showed that 47% of pet stores sold dense water weed (Egeria densa Planch (Hydrocharitaceae)), 38% sold Canadian water weed (Elodea canadensis Michaux (Hydrocharitaceae)), 43% hornwort (Cabomba caroliniana Grey (Cabombaceae)) and 68% spade sword (Echinodorous cordifolius (L.) Griseb ()). Indigenous species were infrequently sold and traded as substitutes for potentially invasive plant species. 26% of pet store respondents could not successfully identify any submerged invasive species. Misidentification leading to the unintentional sale as well as lack of knowledge regarding preventative regulations was identified as areas of concern. Comparatively, aquarists could identify over 50 % of test species. They also kept a substantial proportion of prohibited species in their planted tanks or aquariums. Aquarists informed of the CARA and NEMBA regulation were predominantly unsatisfied with the regulations and voiced their opinions and recommendations of the regulations. The internet as yet poses an insignificant threat in South Africa as there are very few online South African vendors.

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Introduction

Invasive aquatic pose major threats to aquatic systems throughout the world, including South Africa. Numerous pathways of introduction are responsible for the distribution and spread of many of these species including the horticultural and aquarium trade, dumping of ballast water and more recently the internet trade.

Historically, invasive species such as water hyacinth (Eichhornia crassipes (Martius) Solms- Laubach (Pontederiaceae)), flowering rush (Butomus umbellatus Linnaeus (Butomaceae) and water poppy (Hydrocleys nymphoides (Willd.) Bucherau (Limnocharitaceae) have been transported and traded due to their aesthetic and horticultural value, while others have been traded for their use in the aquarium trade such as hornwort (Cabomba caroliniana Grey (Cabombaceae)), dense water weed (Egeria densa Planch (Hydrocharitaceae)), Canadian water weed (Elodea canadensis Michaux (Hydrocharitaceae)), hydrilla (Hydrilla verticillata (L.f.) Royle (Hydrocharitaceae)) and tape grass (Vallisneria spiralis Linnaeus. (Hydrocharitaceae) (Cook, 1985). Despite stringent import and export regulations, in many countries the movement of potentially invasive plant species still occurs extensively.

The majority of submerged invasive plants in South Africa, USA and New Zealand were introduced via the aquarium trade as ornamental aquarium plants (Dehnen-Schmutz et al. 2007; Champion and Clayton, 2000). For example it is highly likely that hydrilla was introduced into South Africa via the aquarium trade. Genetic analysis of South African hydrilla revealed that it is most closely related to hydrilla from Malaysia and Indonesia (Madeira et al. 2007). Regardless of their status as declared invaders in many countries they continue to be sold, particularly via the internet (Kay and Hoyle 2001).

A more recent aid to introductory pathways is through the easy access that numerous consumers and traders have to the internet and e-commerce. There are numerous listings of online nursery catalogues that contain many invasive aquatic or wetland plants. In the USA, every aquatic wetland plant that is listed as a noxious weed can be found online, while twelve highly invasive species were found to be sold internationally over the internet (Kay & Hoyle, 2001).

There are also inadvertent introductions of aquatic species such as whole plants fragments or rhizomes arriving in ballast water or carried by shipping containers (Ruiz & Carlton, 2003). A variety of unwanted hitchhikers can attach to a variety of objects, for example, species that

2 become attached to legally-imported consignments. One example in New Zealand is yellow floating heart (Nymphoides peltata Kuntze (Nymphaeaceae)), which was found in a Hamilton nursery that cultivated and sold a range of water lily species. The seed or rhizome of this weed species allegedly arrived as a contaminant on the imported water lily rhizomes and has since been spread to numerous lily growers (Champion and Clayton, 2000).

Once in the country, invasive spread of invasive aquatic plants is exacerbated by two primary vectors: the general public as well as plant and aquarium trade dealers (Kay & Hoyle, 2001). In South Africa there are approximately 160 pet traders and aquarium traders registered with the Pet Traders Association (SA Pet Traders Association, 2008). Both the general public and plant dealers often misidentify and/or do not know the repercussions of the species they are dealing with, making them local level introductory vectors.

The lack of knowledge regarding invasive species may result in less care given to the overflowing of ponds or the discarding of unwanted plants, which is often discarded into ponds, ditches, streams and rivers which can result in species escaping, establishment and spread. For example water hyacinth escaped from an overflowing garden pond and established into the Nahoon River, Eastern Cape province (pers. comm. Hill, 2008)

South Africa’s rivers, dams, lakes and irrigation canals have been invaded by a number of aquatic floating macrophysics. In the response to the problem, a combination of programmes has been implemented to control the species to acceptable and manageable levels (Hill, 2003). As control methods of these floating macrophytes have improved, previously disturbed niches have become available for indigenous and introduced pioneer species to establish. Submerged invasive species also pose a significant threat to South African water ways but thus far have been left to spread with little or no control or mitigation. Spiked water milfoil (Myriophyllum spicatum L (Haloragaceae)) and dense water weed were recorded in South Africa in the late 1800 s and 1960 s respectively (SANBI, 2009), whereas Canadian water weed, spade-leaf sword and hydrilla have only been identified in South African water ways within the last 50 years (SANBI, 2009), Fan wort and red-cabomba have also been recorded but under cultivation and have not established in any systems yet. In South Africa it is illegal to possess, import, purchase, transport or introduce invasive species under the Conservation of Agricultural Resources Act (CARA), 1983 (ACT No. 43 of 1983) and Agricultural Pests Act, 1983 (Act 36 of 1983) importation of plants and vegetative propagation material (Table 1).

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Table 1: Plants currently categorised as declared weeds or that pose a threat to South African water ways and their current establishment status in South Africa.

FAMILY Species COMMON NATURAL CONSERVATION STATUS CURRENT NAME DISTRIBUTION STATUS IN Under Conservation of SOUTH Agricultural Resources Act AFRICA (CARA), 1983 (ACT No. 43 of 1983) and Agricultural Pests Act, 1983 (Act 36 of 1983) importation of plants and vegetative propagation material

Haloragaceae Myriophyllum Spiked Eurasia Invasive. Declared Weed: Established spicatum L. water- Category 1: (CARA (ACT No. milfoil 43 of 1983))

Importation prohibited (APA (Act 36 of 1983))

Hydrocharitaceae Egeria densa Dense Invasive. Declared Weed: Established Planch. water weed Category 1 (CARA (ACT No. 43 of 1983)). Importation prohibited (APA (Act 36 of 1983))

Hydrocharitaceae Hydrilla Hydrilla Australia It has become a very serious Established verticillata India pest in C & N America. none; (one location) (Linnaeus fill) Korea, Democratic SHOULD BE PROHIBITED People's Republic in South Africa, and eradicated of wherever it may occur in Korea, Republic of South Africa ( Henderson & Reunion (La Cilliers 2002) Réunion) Importation prohibited (APA (Act 36 of 1983))

Hydrocharitaceae Elodea Canadian North America Invasive. Declared Weed: Established canadensis water weed category 1 (CARA (ACT No. Michaux 43 of 1983))

Importation prohibited (APA (Act 36 of 1983))

Cabombaceae Cabomba Cabomba, Native to temperate None; should not be Cultivated, caroliniana fan wort and subtropical introduced into Southern not yet Grey America (Ørgard, Africa (Henderson & Cilliers established 1991) 2002).

Importation prohibited (APA (Act 36 of 1983))

Cabombaceae Cabomba Red South America Importation prohibited (APA Cultivated, frucata Schult. cabomba (Ørgard, 1991) (Act 36 of 1983)) not yet established

Alismataceae Echinodorous Spade-leaf Wetlands of Potentially invasive, sold in Established cordifolius (L.) sword Mexico and North aquarium trade (Henderson & (one location) Cilliers, 2002) Importation (pers. comm.

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Griseb America prohibited (APA (Act 36 of D. Bellstedt) 1983))

Very little is known about the movement of aquatic plants in South Africa. Aquatic plants are bought and traded through various organisations and private companies throughout the country. Often these plants are incorrectly labelled and/or unknown. The aim of this study was to determine what role pet stores and planted tank enthusiasts (aquarists) play in the movement and trade of aquatic plants around South Africa.

Methods and Materials

Two desk top surveys were conducted to determine if pet stores and aquarists are possible vectors of submerged aquatic plant invasions in South Africa. This was achieved by creating online surveys to distribute. Pet stores were also investigated for prohibited plant species being sold.

1. Survey development for pet stores and aquarists

The survey software “SurveyMonkey” (SurveyMonkey, 2009) was utilised to create simple, anonymous, easy to use, online questionnaires. The survey presented pet store owners and aquarists with ten questions.

1.1. Selection of test species

Only 12 plant species were chosen for the survey as a comprehensive list of all blacklisted and invasive plants would have proved too cumbersome and time consuming for respondents. The 12 test species selected were derived for the following reasons:

1. Established invader species. Canadian water weed, dense water weed, spiked water-milfoil, hydrilla and spade leaf sword (Echinodorous cordifolius (L.) Griseb (Alismataceae)) are regarded as dangerous invaders to South Africa and have established in South African water ways (Henderson and Cilliers 2001). 2. Potential invader species.

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Red cabomba is often confused with fan wort, and both are potential invader species into South African water ways (Coetzee, 2009; Henderson & Cilliers, 2002). 3. Common aquarium species. Tape Grass (Vallisneria spiralis L. (Hydrocharitaceae)) and hornwort (Ceratophyllum demersum L. var. demersum (Ceratophyllaceae)) common aquarium plants but not classified as invaders. 4. Indigenous alternative species. South African oxygen weed Lagarosiphon major (Ridl.) Moss ex Wager, Lagarosiphon muscoides Harv. (Hydrocharitaceae) and curly pond weed (Potamogeton crispus Linnaeus (Potamogetonaceae)) as they are common indigenous species to South Africa that could easily be utilised as alternative to invasive aquarium species( Cook, 2004) .

All common names, alternate names and scientific names were provided on the questionnaires.

1.2.Pet stores’ questionnaire

The first three questions (question 1,2,3) focussed on identification, stock and opportunity to acquire 12 specifically chosen submerged plant species (test species).The subsequent three questions ( questions 4,5,6) regarded import of, reason for selection and sale of the test species. The next 3 questions (question 7, 8, 9) were concerned with awareness and agreement with the National Environmental Management Biodiversity Act (NEMBA) and Conservation of Agricultural Resources Act (CARA) and the final optional question (question 10) regarded location of enterprise question (Appendix I)

1.3. Aquarists’ questionnaire

The first two questions (question 1, 2) were created to determine the knowledge of the aquarists, if they could successfully identify the test species and whether the species were indigenous or invasive to South Africa. The following three questions (Questions 3, 4, 5) focussed on whether the aquarists had ever had the opportunity to acquire, owned or passed the test species on to either colleagues or friends. The next question (question 6) regarded

6 whether in their opinion the test species posed a threat to South African water ways. The final 4 questions (question 7, 8, 9, 10) were concerned with their awareness and agreement with the National Environmental Management Biodiversity Act (NEMBA) and Conservation of Agricultural Resources Act (CARA).

1.4. Pilot testing of the internet surveys

Three aquatic plant dealers\pet store owners and three members of an aquatic plant society completed an initial version of the surveys to ensure the surveys were not biased or in any way offensive. These interested and affected parties were sent an e-mail including an attachment of the survey. They were asked to complete the survey and provide feedback on its content and format. They reported that the content was comprehensive and the format made it easy to complete. In response to their comments, A few minor changes to the wording of questions were made as well as adding red cabomba to the test list, as it was suggested it may be being traded instead of fan wort. The complete questionnaires were then uploaded on to the internet for completion by respondents (appendix I & appendix II).

2. Survey advertisement

2.1. Pet stores

The survey was advertised in the SAPTA news letter (August, 2009), which produced 20 000 copies and was distributed nationally. All members of SAPTA were sent an e-mail message from the SAPTA secretary requesting their co-operation in the survey.

2.2. Aquarists

The survey was advertised on popular aquarist blog pages as well as by word of mouth within the aquarist communities.

3. Survey distribution

3.1. Online distribution

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The questionnaire was distributed through online mailing lists and emailing private companies and individuals, requesting them to open the attached hyperlink and fill in the relevant survey.

3.2. Manual distribution

In order to get a comprehensive idea of the plants being traded in South Africa, the survey was also taken personally to as many pet stores as possible in South Africa. Locations visited included Johannesburg, Pretoria, Port Elizabeth, East London, Bethlehem, and Grahamstown. Cape Town, Durban, Bloemfontein and Pietermaritzburg remain to be surveyed.

The questionnaire was answered by 23 aquarists and 34 pet store owners respectively

4. Internet search

An internet search for prohibited and/or invasive aquatic plants was conducted using common search engines such as Google and Yahoo, and water garden and aquarium businesses selling submerged plant species online were searched and prohibited species were recorded.

The forums on aquatic plant enthusiasts, clubs and societies were also searched to investigate which submerged plants are circulating and what species were available in South Africa.

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Results

1. Pet stores

Thirty four pet stores responded to the questionnaires. Of the pet store respondents, 24 % could not identify a single test plant species presented on the survey. Less than 20% of respondents were able to identify spiked water milfoil, hydrilla and L. muscoides (Fig.1). Tape grass (58%), Canadian water weed (42%) oxygen weed (45%) and hornwort (60%) proved to be the most recognisable species to pet stores, while equal numbers (48%) could differentiate between red cabomba and hornwort (Fig. 1).

100.0 90.0 80.0 70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0

Figure 1: The percentage of pet stores respondents able to successfully identify the test species provided. The species with the lowest percentage score included spiked water milfoil, Lagarosiphon muscoides and hydrilla.

Even though the percentage of pet store owners were able to identify the test species was low, 50 % of pet store owners still had the opportunity to acquire many of the test species (Fig. 2). The least available species included hydrilla (14.8%), L. muscoides (22.6%) and spiked

9 water-milfoil (24.1), whereas tape grass (74.3%) and spade leaf sword (80%) were the most common test species available to pet stores (Fig. 2).

100.0 90.0 80.0 70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0

Figure 2: The percentage of pet store respondents able to acquire the test species. The majority of the test species were available to over 40 % of respondents. Hydrilla, Lagarosiphon muscoides and spiked water milfoil had the lowest percent availability.

Test species stocked by the pet stores showed a similar trend to the test species available for acquisition by pet stores. Test species sold most frequently by pet stores included tape grass (71%), spade-leaf sword (68%), oxygen weed (47%) and hornwort (49%), whereas hydrilla (3%), spiked water milfoil (7%), oxygen weed (21%) and L. muscoides (17%) were stocked the least. Prohibited species Canadian water weed, (38%), fan wort (43%), red cabomba (38 %) and dense water weed (48%) were also stocked regularly by the pet stores.

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100.0 90.0 80.0 70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0

Figure 3: percentage of respondents who stocked the test species. Tape grass and spade-leaf sword were the most frequently stocked. Prohibited species fan wort, red cabomba, Canadian water weed, dense water weed were also shown to be regularly stocked.

The majority of pet stores received their test species from suppliers rather than growing their own plants, mail order or self collection were infrequent modes of plant acquisition (Fig.4).

Mail order

Delivery from companies Self Collection

Self Grown

Other

Figure 4: Modes of acquiring aquatic plant stocks. The majority of pet stores acquired their stock from stocking houses or larger companies.

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The majority of pet stores selected their stock on the availability followed by demand. Only two stores had imported stocked from abroad, one store from the Netherlands and the other from Singapore (Fig.5).

1 1 7 Aesthetic value 9 Availability Demand Hardiness Catalogue 25 Other

Figure 5: Factors determining selection of plants for sale in pet stores

The majority of pet store owners were not aware of the CARA (68%) or the NEMBA (79%) regulations. The respondents that had knowledge of the regulations were not in agreement with the regulations (65%) (Fig. 6).

100 100 100 90 90 90 80 80 80 70 70 70 60 60 60 50 50 50 40 40 40 30 30 30 20 20 20 10 10 10 0 0 0 Yes No Yes No Yes No A. B. C.

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Figure 6: A. Percentage of pet store respondents aware of the CARA regulations. B. Percentage of pet store respondents aware of NEMBA regulations. C: Percentage of pet store respondents in agreement with the NEMBA and CARA regulations.

Pet stores’ stock was investigated to note prohibited species being sold. Prohibited species not included in the questionnaire, but available at pet stores are listed:

Anubia barteri Anubia nana Azolla filiculoides Cryptocoryne sp. Cryptocoryne wendtii Trapa natans subulatus

Echinodorus harbich Echinodorus osiris rubra Echinodorus rubin Echinodorus uruguayensis Echinodorus sp Eleocharis parvulus Hygrophila sp. Ludwigia sp. brasiliensis Limnophila sp Vallisneria sp Nymphaea mexicana

Pistia stratiotes Rotala macrandra 'Green' Rotala macrandra

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Sagittaria sp. Salvinia molesta

2. Aquarist Respondents

In contrast to the pet store respondents, aquarists showed that over 50 % of respondents could successfully identify all the species on the test list, with tape grass (91.3%) and hornwort (91.3%) the most frequently positively identified. Lagarosiphon muscoides and curly pondweed species proved to be the most difficult test species to identify for aquarists (Fig. 7).

100 90 80 70 60 50 40 30 20 10 0

Figure 7: The percentage of aquarists able to successfully identify test species. Over 50% of respondents could identify all test species.

All the aquarists had the opportunity to acquire a majority of the test species. Tape grass (87%), dense water weed (70%), Canadian water weed (70%), fan wort (79%), red cabomba (74%), hornwort (96%) and spade leaf sword (78%) were the most prevalent species available to aquarists (Fig. 8). Hydrilla (39%), oxygen weed (34%) and L. muscoides (30%) were the least abundant species available to aquarists (Fig. 8).

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100 90 80 70 60 50 40 30 20 10 0

Figure 8: The percentage of aquarists who had the opportunity to acquire test species. High percentages of respondents were recorded with tape grass, dense water weed, fan wort and hornwort.

There is a similar trend between the opportunity to acquire test species and species owned by aquarists, with L. muscoides (4%) and curly pond weed (21%) being the least kept species. Tape grass (74%), dense water weed (70%), Canadian water weed (56%), fan wort (65%) hornwort (91%) and spade leaf sword (65%) were extensively kept by aquarists (Fig. 9).

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100 90 80 70 60 50 40 30 20 10 0

Figure 9: Percentage of aquarists who had at some stage kept the test species in their aquarium or planted tank. Indigenous species were infrequently kept. Alternatively tape grass, hornwort and some prohibited species were also kept frequently.

Low numbers of the test species were recorded to be traded or passed between colleagues. Less than 30% of aquarists had ever traded or passed on any of the test species, however some of the test species are still traded with tape grass (26%), dense water weed (30 %) and fan wort (30%) being the most common.

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100 90 80 70 60 50 40 30 20 10 0

Figure 10: Percentage of test species traded or passed on between aquarists. The prohibited species fan wort, red cabomba and dense water weed were often traded or passed on.

Aquarists were seen to have a good knowledge regarding the threat that prohibited species pose to South African water ways, indicating in their opinion, hydrilla (65%), spiked water milfoil (65%), dense oxygen weed (65%) and fan wort (65%) pose the most significant threat to South African water ways (Fig. 11). However, they also regard that spade-leaf sword (26%), a potential invader, poses a lesser threat to South African water ways (Fig. 11). It was also noted that no aquarists had ever released any prohibited species into any water ways within the country.

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100 90 80 70 60 50 40 30 20 10 0

Figure 11: Percentage of aquarists who regarded the test species to pose a threat to South African water ways. They regarded the majority of prohibited species to pose significant threats.

In contrast to the pet store respondents, a high proportion of aquarists were familiar with the CARA as well as the NEMBA regulations and the majority of those respondents did not agree with the regulations (Table. 2).

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100 100 100 90 90 90 80 80 80 70 70 70 60 60 60 50 50 50 40 40 40 30 30 30 20 20 20 10 10 10 0 0 0 Yes No Yes No Yes No A B C

Figure 12: A. Percentage of aquarists aware of the CARA regulations. B. Percentage of aquarists aware of NEMBA regulations. C. Percentage of aquarists in agreement with the NEMBA and CARA regulations

Table 2: Responses from aquarists regarding CARA and NEMBA regulations

“Some plants on the list cannot survive in our temperature water and thus are meaningless to keep on the list"

“I have a problem with the restrictive issues relating to the controls against aquarists keeping these species but I don’t know how one effects control in any other way?”

“Planted tank enthusiasts, should be able to apply for a permit to keep invasive plants, as long as they do not distribute them to non-permit holders, and agree to dispose of them responsibly. Similarly to people obtaining permits to keep wild animals etc.”

“I have seen pet shops unpacking newly imported plants with small live snails on them this indicates poor phytosanitary compliance and lack of enforcement.”

“Serious lack of information and research regarding aquatic plants species in South Africa.”

“Whilst I agree that it is the person who trades in these plants’ responsibility to find out about regulations, I have heard very confusing messages from friends who have applied and have been granted permits for the importation of aquatic plants. I hear that Hawaiian and Singapore guidelines have been used and that this has lead to the banning of imports of some Cryptocoryne and all Anubias to my knowledge. In Hawaii and Singapore the climate is tropical, hot and humid, whilst here we have frosts in many parts of the country and far lower humidity. In addition, both of these plants grow slowly and are difficult to cultivate and in my opinion pose no threat to natural systems. Instead, I still see Egeria and Elodea being traded in local fish stores and these species are known to be strong growers and hence potentially invasive, yet there seem to be no controls over these. Then I believe that most natural species of Echinodorus (with the exception of E. cordifolius) are permissible, yet hybrids of these, which then have unique names, are not permitted. The hybrids are again much more difficult to grow, yet they are not permitted. This only one with the impression that the persons taking the decisions or making recommendations about imports have no experience of these plants and that suitably knowledgeable aquarists or pet shop owners, of which there are quite a number, are not being consulted or are wilfully excluded. As stakeholders in this industry, there must surely be an effort to communicate with

19 experienced aquarists and I would welcome it if the opportunity was given to make a meaningful contribution to the decision taking process.”

3. Internet Survey

Over 33 invasive species were found to be sold online. However, only eight vendors were found to be selling plants online. Aquarists trading species online for other plants was more common but very difficult to quantify (Table 3).

Table 3: Number of available prohibited species found to being sold online.

Availability i.e. Prohibited species number of vendors

Anubias barteri 5

Egeria densa 4

Cryptocoryne wendtii 3

Echinodorus bathii 3

Hygrophila polysperma 3

Anubias congensis 2

Anubias nana 2

Cabomba caroliniana 2

Cryptocoryne ciliate 2

Eichhornia crassipes 2

Elodea canadensis 2

Hydrocotyle leucocephala 2

Limnophila sessiliflora 2

Myriophyllum spicatum 2

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Pistia stratiotes 2

Salvinia molesta 2

Very few internet sites were actively selling and advertising invasive aquatic plants. Of the sites actively selling plants online, only a single site had a large variety of invasive plants for sale. Invasive species were found online, the most common being Anubias barteri (5) and dense water weed (4) (Fig.13).

35

30

25

20

15

10

5

0 Vendor 1 Vendor 2 Vendor 3 Vendor 4 Vendor 5 Vendor 6 Vendor 7 Vendor 8

Figure 13: Number of blacklisted invasive plants available per online order directory

Discussion

This study has clearly shown that potentially invasive plants, as well as prohibited species are being sold and traded by pet stores as well as aquarists in South Africa, a problem that has been shown in aquarium fish trade as well as aquarium plant trade in other (Champion and Clayton, 2000; Maki & Galatowitsch, 2003; Rixon et al, 2004). Identifying and quantifying the impacts and threats posed by this trade is invaluable, as prevention of introductions is usually more cost effective mechanism than the costs of post introduction control (Coetzee et

21 al, 2009). Reducing the chances of introduction is vital in the prevention of new introductions into South African waters.

Even though the survey only presents a sample of the potentially invasive and prohibited species in South Africa, it gives an adequate representative sample of the variety and quantity of plants moving through the pet stores in South Africa. The survey shows that in South African pet stores, potentially invasive macrophytes and prohibited species such as dense water weed, Canadian water weed, spade leaf sword, fan wort and red cabomba are being extensively sold, and to a lesser extent, hydrilla and spiked water milfoil. Surprisingly, indigenous species that would make suitable alternatives are infrequently sold. Our results of the prohibited species trade are similar to those found to be being traded and introduced in New Zealand (Champion and Clayton 2000)

Other important factors, with regard to possible plant escapes, noted from the survey include misidentification of species which ultimately can lead to the unintentional sale of invasive plants (Maki & Galatowitsch, 2003). In this investigation we showed that there is a high proportion of pet trader respondents unable to identify the majority of invasive species. Of particular concern is that the lowest figures were associated with invasive species already established in South African waters, namely hydrilla and spiked water milfoil.

The lack of knowledge regarding either the CARA or the NEMBA regulations by pet store owners is very worrying as this results in the continued importation and trade of invasive species in South Africa, the most recent example of which is hydrilla in South Africa which has been traced to Malaysian origin.

The majority of species stocked by pet stores are acquired from a few large distributing companies. The primary driver for acquisition by pet stores was availability. Thus, converting the larger distributing companies to grow and sell indigenous and non invasive species would result in the majority of pet stores selling indigenous and non invasive species.

Over the last 30 years, the aquarium industry has boomed, and it is now easier than ever before for aquarists to obtain their equipment, treatments and fish and plants from pet stores and nurseries (Hiscock, 2003). However this is only half of the trading and movement of plant that is occurs within South Africa. Numerous plants are moved behind closed doors between networks of aquarists who often stay in contact via the internet. Aquarists play an

22 import role in the movement of plants in South Africa but this movement of plants is very difficult to quantify or monitor.

The survey quantifies this past time and even though it presents only a sample of the greater community of aquarists, it clearly shows that potentially invasive macrophytes and prohibited species, similar to those sold by pet stores, are moved and traded by aquarists.

The survey shows that aquarists have a far greater knowledge of both indigenous and invasive plant species as they could identify the majority of the test species. The aquarists were far more informed with regard to both the CARA and the NEMBA regulations and were in a position to comment on the regulations. The majority disagreed with the regulations, stating that the regulations were derived from Hawaiian and Singapore regulations and those regulations were not applicable to the South Africa situation. They also felt that numerous plants that were prohibited by the regulations are slow growing and not potentially invasive in South Africa and should not be on the prohibited list.

Aquarists’ knowledge of the dangers associated with invasive species coupled with their greater knowledge of aquarium plants indicates that they pose less of a threat as a vector to introductions, because they are more aware of the dangers of a release into a water system as well as the laws and regulations governing the movement and trade of the plant species. Every respondent had never considered or released a plant species into a water way, whereas pet stores have no control over whom they sell plants to and what will be done with these plants.

Aquatic plants are known to be dispatched around the world by mail order. The internet only makes the task of finding and purchasing mail order plants easier (Champion & Clayton, 2000). It has been shown that in US markets, federal noxious weeds are extensively sold online (Maki & Galatowitsch, 2003). In South Africa, invasive species can also be found online however only at from eight sites a far smaller number than in the US. Approximately 40 different prohibited macrophytes could be found on South African sites. This mode of introduction is highly concerning as in other countries it is shown that it is very difficult to control and monitor this trade. Currently, thus far online advertisement and sale is limited in South African markets and thus poses an insignificant threat as a possible vector for invasive introductions.

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In summary, our surveys demonstrate that a variety of invasive plants are sold by pet stores and traded and swapped by aquarists. Lack of knowledge regarding identification as well as regulations is a common trend between both aquarists and pet stores, but more prevalent amongst pet stores in South Africa

The majority of species stocked by pet stores are acquired from a few large distributing companies. The primary driver for acquisition by pet stores was availability. Thus, by converting the larger distributing companies to grow and sell indigenous and non invasive species, the majority of pet stores would be compelled to sell indigenous and non invasive species.

The internet as yet poses an insignificant threat in South Africa, with very few vendors actively selling plants online, but may grow to be a powerful mechanism in the spread of invasive species.

Aquarists informed of the CARA and NEMBA regulation were predominantly unsatisfied with the regulations and voice their opinions and recommendations for the regulations. Comparatively, very few pet stores were aware of the regulations.

The pathways of plant movement should be monitored and controlled with more rigour in South Africa up until the regulations and policies are developed and agreed upon by the majority of vendors and aquarists involved.

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References

Champion PD, Clayton, JS (2000) Border control for potential aquatic weeds––Stage 1 weed risk model, Science for Conservation 141, Department of Conservation Wellington, New Zealand.

Coetzee JA, Hill MP, and Schlange D (2008) Potential spread of the invasive plant Hydrilla verticillata in South Africa based on anthropogenic spread and climate suitability. Biological Invasions 11: 801-812

Cook CDK (1985) Range Extensions of Aquatic Species. Journal. of Aquatic Plant Management 23: 1-6.

Dehnen-Schmutz K, Touza J, Perrings C, Williamson M (2007) A century of the ornamental plant trade and its impact on invasion success, Diversity and Distributions 13: 527–534.

Henderson L (2001) Alien Weeds and Invasive Plants. A Complete Guide to Declared Weeds and Invaders in South Africa. Plant Protection Research Institute, Handbook No. 12, Pretoria, South Africa, 300pp.

Henderson L, Cilliers CJ (2002). Invasive aquatic plants. A guide to the identification of the most important and potentially dangerous invasive aquatic and wetland plants in South Africa. Agricultural Research Council, Pretoria. 30-47 pp.

Hill MP (2003) The impact and control of alien aquatic vegetation in South African aquatic ecosystems. African Journal of Aquatic Science 28: 19–24.

Hiscock P (2003). Encyclopaedia of Aquarium Plants. Interpret publishing. New York. Pp 10-11

Kay SH, and Hoyle ST (2001). Mail order, the Internet, and invasive aquatic weeds. Journal Aquatic Plant Management 39:88-91. Madeira PT, Coetzee JA, Center TD, White EE, Tipping PW, (2007) The origin of Hydrilla verticillata recently discovered at a South African dam. Aquatic Botany 87: 176–180.

Maki K, and Galatowitsch S (2004). Movement of invasive aquatic plants into Minnesota through the horticultural trade. Biological Conservation 118: 389-396

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Orgaard M, (1991) The genus Cabomba (Cabombaceae) - a taxonomic study. Nordic Journal of Botany 11: 179-203

Rixon CAM, Duggan IC, Bergeron NMN, Bergeron NMM, Ricciardi A, MacIsaac HJ (2005) Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes. Biodiversity Conservation 14:1365–1381.

Ruiz GM, Carlton JT, eds (2003) Invasive species, Vectors and management strategies, Island Press, Washington.

S A Pet Traders Association, 2008. [Available at] http://www.sapettraders.co.za/members.html. Accessed [04-11-2008]

SurveyMonkey, 2010 [Available at] http://www.surveymonkey.com/. Accessed [04-11-2008]

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Appendix I

Aquatic Plants South Africa questionnaire for pet stores

From various discussions that we have held we have come to the conclusion that the we actually know very little about the movement of aquatic plants in South Africa.

Aquatic plants are bought and traded through various organisations and private companies throughout the country. Often these plants are incorrectly labelled and/or unknown. The aim of this study is to determine the diversity of the species that are imported into and traded with in South Africa.

This questionnaire gives an opportunity to determine what role, if any, of aquatic plant dealers play in the movement and trade of aquatic plants around South Africa. It also gives members the opportunity to voice their ideas and opinions regarding the trade and movement of aquatic plants around the country.

The questionnaire consists of 9 questions regarding to plant species found and traded in South Africa. It utilises primarily yes/no questions but also gives place for further comment. The questionnaire should take approximately 5 minutes to complete. Responses will be treated confidentially

The questionnaire forms part of a masters Rhodes University project to determine the status of submerged aquatic species in South Africa and the factors that determine their distribution. Should you have any questions regarding the study, please feel free to contact myself, Grant Martin at [email protected] or Dr. Julie Coetzee at [email protected] We can both be reached at the department Zoology and Entomology Rhodes university on: 084 2408170

27

1. Could you successfully identify? 0=NO 5=100% certain

0 1 2 3 4 5

Hydrilla verticillata 0 1 2 3 4 5 (hydrilla)

Vallisneria spiralis 0 1 2 3 4 5 (Tape Grass )

Lagarosiphon major,

South African oxygen 0 1 2 3 4 5 weed)

Lagarosiphon 0 1 2 3 4 5 muscoides

Egeria densa (Dense 0 1 2 3 4 5 water weed)

Potamogeton crispus 0 1 2 3 4 5 (Curly pondweed)

Elodea canadensis 0 1 2 3 4 5 (Canadian water weed)

Myriophyllum spicatum (Spiked 0 1 2 3 4 5 water-milfoil, Eurasian water-milfoil)

Cabomba caroliniana 0 1 2 3 4 5 (Fan wort)

28

0 1 2 3 4 5

Cabomba furcata (Red 0 1 2 3 4 5 Cabomba)

Ceratophyllum 0 1 2 3 4 5 demersum (hornwort)

Echinodorus cordifolius (Spade-leaf 1 2 3 4 5 Sword, Radicans Sword )

*

2. Have you ever had the opportunity to acquire this species for your business?

Yes No

Hydrilla verticillata Yes No (Hydrilla)

Vallisneria spiralis Yes No (Tape Grass)

Lagarosiphon major,

South African oxygen Yes No weed)

Lagarosiphon Yes No muscoides

Egeria densa (Dense Yes No water weed)

Potamogeton crispus Yes No (Curly pondweed)

29

Yes No

Elodea canadensis Yes No (Canadian water weed)

Myriophyllum spicatum (Spiked water- Yes No milfoil,Eurasian water- milfoil)

Cabomba caroliniana Yes No (Fan wort)

Cabomba furcata (Red Yes No Cabomba)

Ceratophyllum Yes No demersum (hornwort)

Echinodorus cordifolius

(Spade-leaf Sword, Yes No Radicans Sword )

*

3. Do you have this species in stock?

Yes No

Hydrilla verticillata Yes No (Hydrilla)

Vallisneria spiralis Yes No (Tape Grass)

Lagarosiphon major

(South African oxygen Yes No weed)

30

Yes No

Lagarosiphon Yes No muscoides

Egeria densa (Dense Yes No water weed)

Potamogeton crispus Yes No (Curly pondweed)

Elodea canadensis Yes No (Canadian water weed)

Myriophyllum spicatum (Spiked water- Yes No milfoil,Eurasian water- milfoil)

Cabomba caroliniana Yes No (Fan wort)

Cabomba furcata (Red Yes No Cabomba)

Ceratophyllum Yes No demersum (hornwort)

Echinodorus cordifolius

(Spade-leaf Sword, Yes No Radicans Sword )

*

4. How do you acquire your aquatic plants?

31

Mail order

Delivery from companies

Self collection

Self grown

Other

5. How do you select the plants you sell ?

Aesthetic value

Availability

Demand

Hardiness

catalogue

Other

*

6. Have you ever imported aquatic plants from abroad?

Yes

No

*

7. Are you aware of the Conservation of Agricultural Resources Act regarding aquatic plants?

Yes

32

No

*

8. Are you aware of the National Environmental Management Amendment Act (NEMBA)?

Yes

No

9. Do you agree with these regulatory measures and any other comments?

10. Optional, where is you business located?

City/Town:

State/Province:

3. Thank you

I would like to thank you for taking the time to the fill out my questionnaire. Please feel free to e-mail me any questions at [email protected] . The idea is that the results of this study will be used to advise the government authorities about future regulations on aquatic plants in this country, to try make them more fair and reasonable to all parties involved. Regards Grant Martin

33

Appendix II

Aquarists in South Africa

1. Aquatic Plants South Africa

Dear Aquarist,

I would like to ask you to assist me with a few questions about aquatic plants for my Masters project at Rhodes University. From various discussions that we have held we have come to the conclusion that the we actually know very little about the movement of aquatic plants in South Africa. As a result this study was developed and the idea is that the results of this study will be used to advise the government authorities about future regulations on aquatic plants in this country.

Aquatic plants are bought and traded through various organisations and private companies throughout the country. Often these plants are incorrectly labelled and/ or unregistered. The aim of this study is to determine the diversity of the species that are imported into and traded with in South Africa.

This questionnaire gives an opportunity to determine what role, if any, of aquatic plant enthusiasts play in the movement and trade of aquatic plants around South Africa. It also gives members the opportunity to voice their ideas and opinions regarding the trade and movement of aquatic plants around the country.

The questionnaire consists of 11 questions regarding to plant species found and traded in South Africa. It utilises primarily yes/no questions but also gives place for further comment. The questionnaire should take approximately 5 minutes to complete. Responses will be treated confidentially and a compiled report of the findings will be presented on the webpage after we have analysed all the reports. The questionnaire forms part of a masters Rhodes University project to determine the status of submerged aquatic species in South Africa and the factors that determine their distribution. Should you have any questions regarding the study, please feel free to contact myself, Grant

34

Martin at [email protected] or Dr. Julie Coetzee at [email protected] We can both be reached at the department Zoology and Entomology Rhodes university on: 084 2408170

Aquarists in South Africa

2. Section A: Plant Identification

1. Could you successfully identify? Yes No

Hydrilla verticillata Could you successfully Yes No (hydrilla)

Vallisneria spiralis (Tape Yes No Grass )

Lagarosiphon major (African elodea, curly waterweed, ) Yes No oxygen weed, South African oxygen weed )

Lagarosiphon Yes No muscoides

Egeria densa

(Dense water Yes No weed)

35

Yes No

Potamogeton crispus (Curly Yes No pondweed)

Elodea canadensis

(Canadian water Yes No weed)

Myriophyllum spicatum (Spiked water-milfoil, Yes No Eurasian water- milfoil)

Cabomba caroliniana (Fan Yes No wort)

Cabomba furcata Yes No (Red Cabomba)

Ceratophyllum demersum Yes No (hornwort)

Echinodorus cordifolius

(Spade-leaf Yes No Sword, Radicans Sword )

*

2. Is it indigenous and/or invasive Indigenous Invasive

36

Indigenous Invasive

Hydrilla verticillata Indiginous Invasive (Hydrilla)

Vallisneria spiralis (Tape Indiginous Invasive Grass)

Lagarosiphon major (African elodea, curly waterweed, Indiginous Invasive oxygen weed, South African oxygen weed)

Lagarosiphon Indiginous Invasive muscoides

Egeria densa

(Dense water Indiginous Invasive weed)

Potamogeton crispus (Curly Indiginous Invasive pondweed)

Elodea canadensis

(Canadian water Indiginous Invasive weed)

Myriophyllum spicatum (Spiked ) Indiginous Invasive water- milfoil,Eurasian

37

Indigenous Invasive water-milfoil)

Cabomba caroliniana (Fan Indiginous Invasive wort)

Cabomba furcata Indiginous Invasive (Red Cabomba)

Ceratophyllum demersum Indiginous Invasive (hornwort)

Echinodorus cordifolius

(Spade-leaf Indiginous Invasive Sword, Radicans Sword )

*

3. Have you ever had the opportunity to acquire this species? Yes No

Hydrilla verticillata Yes No (Hydrilla)

Vallisneria spiralis (Tape Yes No Grass)

Lagarosiphon major (African Yes No elodea, curly waterweed,

38

Yes No oxygen weed, South African oxygen weed)

Lagarosiphon Yes No muscoides

Egeria densa

(Dense water Yes No weed)

Potamogeton crispus (Curly Yes No pondweed)

Elodea canadensis

(Canadian water Yes No weed)

Myriophyllum spicatum (Spiked water- Yes No milfoil,Eurasian water-milfoil)

Cabomba caroliniana (Fan Yes No wort)

Cabomba furcata Yes No (Red Cabomba)

Ceratophyllum demersum Yes No (hornwort)

39

Yes No

Echinodorus cordifolius

(Spade-leaf Yes No Sword, Radicans Sword )

*

4. Do you or have you ever had this species in you aquarium/tank? Yes No

Hydrilla verticillata Yes No (Hydrilla)

Vallisneria spiralis (Tape Yes No Grass)

Lagarosiphon major (African elodea, curly waterweed, Yes No oxygen weed, South African oxygen weed)

Lagarosiphon Yes No muscoides

Egeria densa

(Dense water Yes No weed)

Potamogeton Yes No crispus (Curly

40

Yes No pondweed)

Elodea canadensis

(Canadian water Yes No weed)

Myriophyllum spicatum (Spiked water- Yes No milfoil,Eurasian water-milfoil)

Cabomba caroliniana (Fan Yes No wort)

Cabomba furcata Yes No (Red Cabomba)

Ceratophyllum demersum Yes No (hornwort)

Echinodorus cordifolius

(Spade-leaf Yes No Sword, Radicans Sword )

*

5. Do you or have you ever passed this species on to colleague or friend? Yes No

Hydrilla Yes No verticillata

41

Yes No

(Hydrilla)

Vallisneria spiralis (Tape Yes No Grass)

Lagarosiphon major (African elodea, curly waterweed, Yes No oxygen weed, South African oxygen weed)

Lagarosiphon Yes No muscoides

Egeria densa

(Dense water Yes No weed)

Potamogeton crispus (Curly Yes No pondweed)

Elodea canadensis

(Canadian water Yes No weed)

Myriophyllum spicatum (Spiked water- Yes No milfoil,Eurasian water-milfoil)

42

Yes No

Cabomba caroliniana (Fan Yes No wort)

Cabomba furcata Yes No (Red Cabomba)

Ceratophyllum demersum Yes No (hornwort)

Echinodorus cordifolius

(Spade-leaf Yes No Sword, Radicans Sword)

*

6. In your opinion does this species pose a threat to our water systems? Yes No

Hydrilla verticillata Yes No (Hydrilla)

Vallisneria spiralis (Tape Yes No Grass)

Lagarosiphon major (African elodea, curly Yes No waterweed, oxygen weed, South African

43

Yes No oxygen weed)

Lagarosiphon Yes No muscoides

Egeria densa

(Dense water EYes No weed)

Potamogeton crispus (Curly Yes No pondweed)

Elodea canadensis

(Canadian water Yes No weed)

Myriophyllum spicatum (Spiked water- Yes No milfoil,Eurasian water-milfoil)

Cabomba caroliniana (Fan Yes No wort)

Cabomba furcata Yes No (Red Cabomba)

Ceratophyllum demersum ) Yes No (hornwort)

Echinodorus Yes No cordifolius

44

Yes No

(Spade-leaf Sword, Radicans Sword)

*

7. Are you aware of the Conservation of Agricultural Resources Act regarding aquatic plants? Are you aware of the Conservation of Agricultural Resources Act regarding aquatic plants?

Yes

No

8. Are you aware of the National Environmental Management Amendment Act (NEMBA)? Are you aware of the National Environmental Management Amendment Act (NEMBA)?

Yes

No

9. Do you agree with these regulatory measures?

Do you agree with these regulatory measures?

10. Any other comments regarding aquatic plants and /or their regulation in South Africa

45

3. Thank you

I would like to thank you for taking the time to the fill out my questionnaire. Please feel free to e-mail me any questions at [email protected] . The idea is that the results of this study will be used to advise the government authorities about future regulations on aquatic plants in this country, to try making them more fair and reasonable to all parties involved. Regards Grant Martin

46