INVASION OF THE CRITTERS

I was reading through some of the material that is posted up on GISP, and since I work in a public aquarium, I decided to harp on the subject of aquatic organisms and their role in invasions throughout the world, but particularly here in South Africa. Additionally, for those who have seen my powerpoint presentation, I will also add some additional information on Whitespot or Cryptocaryon irritans as it is known, to add to my justification of its invasive potential.

For those who have fish tanks at home, or a goldfish in a bowl, or a pond outside…here is some food for thought.

Mouton et al. (2001) Indicated that not only is fish keeping in South Africa a very popular pastime, but the majority of the fishes bought in pet shops around the country are imported from areas such as Brazil, Colombia, Indonesia, Malaysia, Peru, Thailand and Sri Lanka (Moravec et al. 1999). As mentioned in my presentation, the South African Government does not have the resource of enough adequately trained staff to implement and police the requirements of the Agricultural Pests Act (Act 36 of 1983), which states that all imported fishes require a period of quarantine though this responsibility falls on the consignee of the shipment (Mouton et al. 2001).

Did you know that there are no guidelines, protocols or legislation suggesting specific requirements of fish quarantine in South Africa, and that there are only a handful of trained and qualified people in aquatic health management in this country? I have been working in this field for nearly 10 years now, and I have also been involved with my own home aquarium, in addition to having the responsibility of the quarantining for both the Two Oceans Aquarium (at present) and Sea World at uShaka Marine World in Durban (from 2003 – 2005). The loophole which is exploited by the pet-trade industry is huge, though in their defence, I am sure the majority of them would prefer to quarantine their fishes correctly prior to release to the general public, if they had the logistical and technical support to do so correctly.

Did you know that goldfish are Cyprinids, a group of the carp-like fishes of which South Africa boast some unique, rare and protected species found nowhere else in the world? Impson et al. (1999) indicates that the Cape Floristic Region, a special conservation concern, has 19 indigenous freshwater fish species of which 16 of them are endemic, and 15 of these are threatened species. They are all Cyprinids. Mouton et al. (2001) indicates that the common goldfish, Carrasius auratus, can happily survive in the temperate regions of South Africa, taking advantage of the same food source as the native Cyprinids, and in fact, a small population was recently discovered on top of Table Mountain! According to “A Complete Guide to the Freshwater Fishes of Southern Africa,” the book by Paul Skelton, the common goldfish can be found as feral populations in the Cape, Port Elizabeth, Pretoria, Kwazulu Natal, and even in Zimbabwe! Other introduced Cyprinids include the common carp, Cyprinus carpio, Grass carp, Ctenopharyngodon idella, Silver carp, Hypophthalmichthys molitrix, and Tench, Tinca tinca.

What is encouraging is the suggestion to prohibit importation of some of these Cyprinids such as the common carp, Cyprinus carpio, but hang on…the Koi is the same species, only a colourful ornamental version, selectively bred over many generations in Japan as not only a form of art, but a serious source of income and industry today. Aquaculture, which includes the South African Koi industry, is one of the fastest growing industries in this country, and responsible for a steady increase in job-creation…Recently this fired up a heated debate, of which the remnants are still available as sections of e-mail between Prof. Paul Skelton, who has been working with the Government to place invasive species into specific categories such as “regulated by area,” “regulated by activity”, and “under surveillance…” The links to the web pages are as follows, and are of particular interest to read:

http://www.happykoi.co.za/Articles/40%20koi%20to%20be%20banned%20in%20south%20africa%20proposed%20legislation.htm
http://www.happykoi.co.za/Articles/41%20koi%20ban%20in%20south%20africa%20follow%20up.htm

So, is it the fishes themselves that are the problem? The answer is both yes and no. Traditionally we have seen the destruction of aquatic biodiversity and macro and micro-habitat disturbance by alien species such as trout, bass and carp, but only now are we beginning to realise just how destructive our ignorance has actually been. All fishes have co-existed and co-evolved with their own set of parasites which they have acquired a certain immunity towards, to allow them to live relatively harmoniously together in normal circumstances. In parasitology, if a naïve host is infected by a parasite for which there is no associated immunity, the results can be the population explosion of the parasite and the possible destruction of the host population in the long term.

Our common goldfish that we keep in our homes are almost always hosts to the monogenean Gyrodactylus gurleyi, G. kobayashii, G. katharineri, and G. medius. Gyrodactylus, though host specific, have the ability to host-swop and can therefore cause potential problems for native Cyprinids in South Africa, not to mention the risk of introducing various Cyprinid-specific viruses to our endemic populations. Remember, one parasite, Gyrodactylus salaris nearly destroyed the entire Norwegian Salmon industry and is still an important threat today! How many goldfish that have died in their bowls have you flushed down the loo? Where do they go, and what hitch-hikers have you potentially introduced to another area? Food for thought.

Putting things back into perspective again, did you know that because terrapins (freshwater turtles) are known carriers of a type of monogenean infecting the urinary bladder, all transportation of all terrapins must be accompanied by a transport permit issued by Cape Nature Conservation, and, if the origin of a terrapin is not known, but has been an illegal pet in someone’s home for a while, not only can it not be re-introduced into the wild, but it is usually destroyed after it has been confiscated? So then why are fishes not treated with the same level of concern?

Late last year I was literally handed two juvenile Red-eared Sliders, an exotic terrapin from America, which came on holiday with their American owners to South Africa and the Waterfront. The terrible twins were placed in a completely transparent plastic box with a sheet of cellophane over the top as a lid, and managed to walk through customs at the Cape Town Docks without any queries, right up to the Two Oceans Aquarium where they were “donated” because they were not wanted anymore! I am just glad they were not just dumped into a drain somewhere. I contacted Dean Impson from Cape Nature Conservation, who explained that this species was black-listed and highly invasive. Luckily they found a home with an approved keeper of illegal exotics by Cape Nature Conservation.

The marine pet-trade is one of serious concern, but also one of the most important industries dealing with the home aquarist. Not only are diseases a common problem as many home aquarists will bear testament to, but what is not fully understood yet is exactly what the potential for invasion this industry has. Most species of marine ornamentals for the aquarium pet-trade are still wild-caught specimens, which are shipped into the country within 18 to 33 hours after packaging from their locations. Many fishes are pre-sold to customers by business owners before they have even landed in the country, and handed out to the purchaser still neatly packaged in their original bags of seawater from all over the world. Though it could be argued that the fishes are only being introduced into home aquaria, and are therefore of low risk, it is the introduction of exotic aquatic diseases and the potential reservoir effect of these home aquaria that threatens our native aquatic biodiversity. Did you know that a main supplier of marine ornamental fishes is the Far East and Sri Lanka, and that the majority of the species brought into our country (without quarantine) are the same species as those that we find in our marine protected areas on the East coast such as Aliwal shoal and Sodwana bay?

So what exactly is the big deal?

Cryptocaryon irritans, the common marine whitespot parasite is thought to be only one worldwide species without variation. Originally, this parasite was though only to be a tropical parasite, preferring temperatures of 22 – 26 Degrees Celsius. Recent studies have indicated that this Ciliophoran parasite is in fact a worldwide group of strains, and these strains have their own adaptations to their native conditions and hosts. Hirazawa et al. (2003) looked at the affects of disinfection using chlorine, benzalkonium chloride and heat treatment as well as increased salinity for the prevention of the spread of Cryptocaryon cysts or tomonts. In their experiment the Cryptocaryon strain used, hatched on the fifth day at 25 Degrees Celsius. A study in progress at the Two Oceans Aquarium has also recently indicated that the Cryptocaryon found off the Cape Town region prefers colder water to warm water, but can actually increase its rate of host re-infestation in unfavourable (warmer) conditions. The local strain of Cryptocaryon began hatching on the fifth day, however the majority hatch only took place on the twelfth and thirteenth days. If the various regions of the South African coastline can expect to be the habitat of specific associated strains of diseases with their own specific host fauna, what impact would the release or introduction of an infected fish from a home aquarium be to our native biodiversity and intricate host-parasite balance? In a review of the mogenean genus Dendromonocotyle from cartilaginous fishes, Chisholm et al. (2004) suggest that previously though worldwide host species, may actually be host-complexes, and if this is so, it can be expected that associated parasite species could have been overlooked. It is therefore of utmost importance not to assume that by purchasing a fish species known from South African waters, it is a lower risk, or that if it becomes too large for the home aquarium, it can be released into the local ocean.

South Africa requires a similar imports risk analysis for the support of improved legislation and training as that implemented by the New Zealand Biosecurity section of the Ministry of Agriculture and Forestry (2005). This risk analysis indicates a strict ban on the Cyprinids discussed above, which is still under debate in this country, and hi-lights the actual disease concerns and previous invasive introductions. The aquatic pet trade is indicated in this risk assessment as one of the main routes of parasitic introduction.

The list of specific genera and species of fishes admissible to New Zealand, the legislative requirements of quarantine and the actual imporation procedures can be accessed at the following website:

http://www.biosecurity.govt.nz/imports/animals/standards/fisornic.all.htm

Some more invasive parasite examples:

American scientists have discovered an isopod parasite called Orthione griffenis that is destroying the native mud shrimp population in the estuaries of the West coast of the USA. The isopod enters the gills of the shrimp and weakens the shrimp as a result of its feeding habits on the blood tissue. The weakened shrimp cannot reproduce and the population is now in decline. John Chapman from the Oregon Sate University is an invasive species expert who suggests that this isopod parasite is not a native parasite, but could have been introduced to the West coast estuaries through ballast water.

Oysters have been moved around during from one area to another and from place to place all over the world in the name of mariculture for many years. The GISP website article on oysters refers to them as “a kind of sessile sheep” having been moved around for the last 150 years. Through the ignorance of today’s environmental and invasion problems, no prevention of potential oyster diseases was controlled for, and subsequently many different diseases have travelled with the oysters to many regions causing problems in native shellfish populations.
Oyster disease or MSX (Haplosporidium nelsoni) and the microcell disease (Bonamia ostreae), have caused severe problems in shellfish fisheries. A paper by Hine and Jones (1994) identifies Bonamia as primarily parasites of flat oysters, but that Bonamia species are endemic to the Southern Pacific, and make up the natural parasite fauna of New Zealand and Australia. An outbreak of Bonamia in New Zealand was followed by a successful manipulation of the oyster population by dredging a partition between infected and uninfected stock.

In France in 1979, Bonamia ostreae was encountered for the first time in Europe. It spread to various other countries in Europe through the oyster trade and became established in the native populations of bivalves. It is now unfeasible to farm oysters in the affected areas in Europe because of the resultant associated mortality rate of 40% to 60%. A new statement released on 27 July this year by the Fish Health Inspectorate of Scotland explains that this parasite has now only recently been discovered in their native oysters in Loch Sunart. Under the Fish Health Regulations of 1997, the movement of all molluscan is now under strict control. The official notice reads as follows:
“The Fish Health Regulations 1997 No 1881 (as amended) Regulation 14 Notice (No.1) 2006 restricts the movement of any live molluscan shellfish into or out of the designated area without prior consent of Scottish Ministers.
The designated area is the area of water comprising tidal waters (whether forming part of the sea or not) within the seaward limits of the territorial water adjacent to Great Britain, which lies between or within, as the case may be, the limits specified below - The waters of Loch Sunart east of a line drawn south south east from the northernmost tip of Maclean's Nose at NM 532 615 to Auliston Point at NM 546 582.”

The Fish Health Inspectorate is looking at options to eliminate this new outbreak in Scotland.

The monogeneans infesting eels, Pseudodactylogyrus bini, and P. anguillae, were recently discovered on eels in North America, which is the first report of the invasion of these two monogenean species, which are originally from Asia (Hayward et al. 2001). These monogeneans are now infesting the native eel population in North America, and it is suggested in the paper by Hayward et al. (2001) that future invasions of similar parasites of eels could become a reality in other parts of the world.

Similarly, monogeneans found on the skin of an eel species investigated as a possible aquaculture species in Stellenbosch are not native to South Africa (K. Christison pers. com), and in late 2005, a species of anchorworm (Lernaea sp.), which is actually a type of crustacean parasite, was found on a University of Stellenbosch-cultured rainbow trout in the floating cages of Klein plaas dam in the Jonkershoek nature reserve. The significance of this is the fact that firstly, salmonids (trouts and salmon) are not usually known to be hosts of Lernaea sp., but Cyprinids such as the common Carp are known as hosts, and are present in the same dam system, which is fed by the upper Eerste river system. If the Lernaea sp. can infest a salmonid, what potential damage is it doing to the native Cyprinids of the upper Eerste river system and tributaries?

What needs to be done…or is it already too late?

To begin with, legislation cannot be successful without the correct support from trained staff. The South African Government must first put in place measures to train the necessary staff in aquatic health management and the identification of parasitic organisms, with the aid of the available taxonomic keys and of course the correct diagnostic equipment. This would not only provide potential job opportunities in a field which could lend itself to support a growing aquaculture industry, but the support structure for the implementation and policing of legislation would prevent future indiscriminate invasions of parasites.

Evidence needs to be acquired to build a case which would then be submitted to the Governmental Department of Environmental Affairs and Tourism, or the argument that exists now, will continue to provide the opportunity for further procrastination: “We don’t see any invasive parasitic problems in this country…”

All it will take is to prove that Gyrodactylus spp. for example can host switch from one species of introduced Cyprinid to a native species, or, that a known invasive parasite species has been identified and is being harboured in a public aquarium in South Africa. The reciprocal reaction would have to be of a serious nature, or the Governmental Department could be seen to be hypocritical.

New Zealand, I believe has taken the initiative and the authority to control this potential problem. Although there is a ban on the importation of certain Cyprinid species into New Zealand, they do allow the trading and breeding of certain ornamental species, though kept controlled by permits. This is the way South Africa should be looking regarding the Koi industry. It could be argued that the gene pool for the breeding of show-quality Koi would be compromised without the importation of brood stock from Japan or other countries, which could impact the sale of high-end show Koi. More realistically though, this argument is refuted by the fact that fertilised ova from high quality Koi could be shipped to this country to be raised in hatcheries where the fry would be naïve to parasitic infestation. All accompanying water shipped with the fertilised ova would be affectively sterilised after the transfer of ova to the hatchery (as also indicated as a protocol for New Zealand). In fact it can then be argued that it is in fact beneficial and feasible. Equally, the breeding of high-quality Koi in this country does not have to continuously rely on the importation of winning brood stock from overseas, and the breeders need to distinguish between responsible biosecurity for our native biodiversity and their role in this, and managing acceptable profit margins. A balance must be reached, or the Koi industry may run the risk of being seen as income-orientated rather than conservation-orientated. With their support instead of criticism thereof, the Biodiversity Act (2004) can be supported.

Quarantine measures

Quarantine is defined in the dictionary as being a period of isolation for forty days, though this should not be an excuse to include all possible invasive pathogens within the same preventative time frame. Work needs to be done to understand the risks of specific disease-causing organisms that can be introduced with aquatic livestock. Species-specific quarantine regimes need to be implemented using the known information of the biology and ecology of these organisms to be most successful. To achieve an effective quarantine for fishes, Integrated Pest Management (IPM) is the only affective tool. IPM used within a species-specific host-parasite profile, would be most effective in reducing potential invasion risks of parasites, and would also reduce not only the risk of potential medication-resistant strain creation, but reduce the amount of medication or therapies used in total, a general cost saving.

Public aquaria have a responsibility as the perceived “Big Brother” of the aquarium world, to lead by example, and I believe that together with the relevant Governmental Departments, the conservation mandate of public aquaria could be shown to provide potential solutions and even logistical support for the implementation of such a quarantine programme.

David Vaughan
Senior aquarist, Quarantine
Two Oceans Aquarium
Cape Town, South Africa
dvaughan@aquarium.co.za


Picture credits isopod shrimp parasite:

http://oregonstate.edu/dept/ncs/newsarch/2005/Aug05/isopod.htm

Picture credit Bonamia 1:

http://www.ices.dk/marineworld/fishdiseases/map8_5.htm

Picture credit Eel:

http://www.fotograf.nu/special/images/eel.jpg

References

International Council for the Exploration of the Sea (ICESCIEM) [Internet] [cited 10 Aug 06 10:54] Available from: http://www.ices.dk/indexfla.asp

Confirmation of Bonamia in Loch Sunart [Internet] [Cited 10 Aug 06: 11:07] Available from: http://www.scotland.gov.uk/News/Releases/2006/07/27154609

Chisholm L. A., Whittington I. D., Fischer A. B. P. 2004. A review of Dendromonocotyle (Monogenea: Monocotylidae) from the skin of stingrays and their control in public aquaria. Folia Parasitologica 51: 123 – 130.

Hayward, C. J., Iwashita M., Crane J. S., Ogawa K, 2001. First report of the invasive eel pest Pseudodactylogyrus bini in North America and in wild American eels. Diseases of Aquatic Organisms 26; 44(1):53-60

Hines P. M., Jones J. B. 1994. Bonamia and other aquatic parasites of importance to New Zealand. New Zealand Journal of Zoology 21: 49 – 56.

Hirazawa N., Goto T., Shirasu K. 2003. Killing effect of various treatments on the monogenean Heterobothrium okamotoi eggs and oncomiracidia and the ciliate Cryptocaryon irritans cysts and theronts. Aquaculture 223: 1 – 13.

Impson N. D., Bills I. R., Cambray J. A., Le Roux A. 1999. The primary freshwater fishes of the Cape Floristic Region: Conservation needs for a unique and highly threatened fauna. Stellenbosch: Cape Nature Conservation.

Moravec F., Wolter J., Korting W. 1999. Some nematodes and acanthocephalans from exotic ornamental freshwater fishes imported into Germany. Folia Parasitologica 46: 296 – 310.

Mouton A., Basson L., Impson D. 2001. Health status of ornamental freshwater fishes imported to South Africa: a pilot study. Aquarium Sciences and Conservation 3: 327 – 333.