Sunbleak and Topmouth Gudgeon- two new additions to Britain's freshwater fishes

~ ~ Topmouth Gudgeon Sunbleak Adrian C Pinder and Rodolphe E Gozlan

hroughout the world, it is commonly Globally, among vertebrates, introductions of accepted that the introduction of new freshwater fish species have been among the most T species to a stable ecosystem can upset the numerous (Crivelli 1995), and the introduction of environment and the species already present. non~native fishes to the UK is not a new phenome- Aquatic ecosystems are no exception and, with a non. The Carp Cyprinus carpio was first intro- dramatic increase in world travel and trading over duced for aquaculture in the 15th century (Balon the last century, are increasingly at risk from 1995), and during more recent times introductions biological invasion. that have successfully colonised UK watercourses The various threats posed by the introduction of include the Ide Leuciscus idus, Bitterling Rhodeus alien species are many and can manifest them- sericieus, Zander Sander lucioperca and Pumpkin- selves in the form of direct predation on native seed Lepomis gibbosus. The motives responsible species, competition for food, introduction of new for these introductions vary from ornamental fish- diseases or parasites, or potential to cause change keeping and angling interest to, in the case of to the environment. Grass Carp Ctenopharyngodon idella, their use as

December 2003 British Wildlife 77 Sunbleak and Topmouth Gudgeon

a biological herbicide to control the excessIve Whereas most British freshwater fish grow rela- growth of aquatic weed. tively rapidly for the first few years, until they become sexually mature, in Sunbleak growth is Sunbleakand Topmouth Gudgeon most rapid during the first summer, beyond which This article highlights two of the most recent intro- energy reserves are reallocated from somatic ductions to the fish of : growth towards gonad production, resulting in Topmouth Gudgeon Pseudorasbora parva and Sunbleak becoming sexually mature at one year Sunbleak Leucaspius delineatus. Over the last three old (Gozlan et al. 2003a). years, various aspects of the biology and ecology, During spawning, males, which are smaller than including the reproductive behaviour, females, take up territories around the stems and requirements and early development, and the distri- underside of the leaves of water-lilies and other bution of these two species have been studied by the flat-surfaced structures. The males then clean any authors at the Centre for Ecology and Hydrology in accumulated bio-films from the spawning Dorset. Here, we summarise their fascinating life substrate, using their mouths. The ripe females, histories and assess the current status of these new which develop swollen, distended ovipositors additions to the British aquatic fauna. We also during spawning, join the male and travel at high discuss the future of these species in Britain and the speed across the spawning substrate (Gozlan et al. risks that they pose to our native fishes. 2003b), depositing strips of up to 80 highly adhe- sive eggs. A female Sunbleak can typically deposit a Basicbiology strip of 40 eggs in less than one second. After the Both Sunbleak and Topmouth Gudgeon are small female has spawned, the male guards the eggs and cyprinids possessing highly developed life-history encourages other females to deposit their eggs at strategies which have undoubtedly assisted them the same nest site. The male then guards the eggs in successfully colonising bodies of water in the until they hatch, which takes approximately four . The majority of cyprinid species take days at noc (Pinder & Gozlan in press). 2-4 years to become sexually mature and spawn In contrast to its alien and invasive status in the just once a year. The females scatter many thou- UK, the Sunbleak is considered rare or vulnerable sands of eggs over aquatic macrophytes or gravel, throughout much of its native range (Lelek 1987). and these are then left unguarded and vulnerable It is also listed as protected under Appendix III of to predation. Unusually for cyprinids, both the Bern Convention. Sunbleak and Topmouth Gudgeon become sexu- ally mature at one year old and are batch spawn- TopmouthGudgeon ers, with females laying several batches of eggs, Rarely attaining 8cm in length or living for more between April and July, which are guarded by the than three years, Topmouth Gudgeon predomi- males until they hatch. nantly occupy the bentho-pelagic zone, where This combination of attributes means that a their diet consists of algae, benthic invertebrates, relatively low number of eggs (when compared zooplankton, molluscs and also the eggs and with other cyprinid species) are produced, but larvae of other fish species (Xie et al. 2000). As with the parental care ensuring higher than aver- opportunistic feeders, Topmouth Gudgeon will age hatching rates. Also, as the brood is spread also take food from the )'Vater's surface, where across an extended period, larvae are less vulnera- feeding on terrestrial insects and other floating ble to changes in environmental conditions, thus objects is accompanied by an audible clicking enhancing survival rates (Gozlan et al. 2003a). noise. This behaviour is responsible for these fish being referred to by some as 'clicker barbs'. Sunbleak Topmouth Gudgeon have many life-history char- Sunbleak closely resemble Bleak Alburnus alburnus acteristics in common with Sunbleak. However, in appearance, but are a smaller species not exceed- subtle differences are evident. In contrast to ing 8cm in length and rarely living for more than Sunbleak, male Topmouth Gudgeon are larger than three to four years. They are gregarious and live in the females and exhibit secondary sexual character- large shoals close to the water's surface, where they istics such as tubercles around the mouth, and the typically feed on zooplankton and terrestrial insects. body coloration becomes much darker, particularly

78 British Wildlife December 2003 Sunbleak and Topmouth Gudgeon on the fins. At this time, territo- ries are established which are defended aggressively by the males. Spawning substrata have previously been reported to include the underside of rocks and broadleaved floating macro- phytes. Our studies have shown that, like Sunbleak, Topmouth Gudgeon can successfully spawn on any flat-surfaced object, although they show a preference for structures with a cavity, which are easier to guard from other fish, including their own speCIes. Preliminary investigations into the spawning behaviour, carried out by the Identification authors, suggest that bigger males are most successful in defending territories from Sunbleak conspecifics and in attracting gravid females. This Olive-green back, silver sides and abdomen with iridescent blue sheen along flanks is in agreement with the findings of Katano & Anal fin rays111/10-13 Maekawa (1997), who stated that females choose Distinctly short lateral line terminating before dorsal fin males with larger body size as their mates. Females Upturned mouth

will spawn with several different males in a day, Topmouth Gudgeon depositing several batches of eggs in each terri- 34-38 lateral scales with dark edges tory. Dark band of lateral pigment (often absent in larger The eggs of Topmouth Gudgeon superficially (>Scm) individuals) resemble those of the Sunbleak, but have a thicker Dorsal and anal fins strongly convex Upturned mouth chorion and are encased in a jelly-like substance which is highly adhesive. Eggs are released in In the winter the shoals disperse to deeper water. smaller batches than those of Sunbleak, usually Sunbleak prefer slow-flowing rivers and associ- four to ten at a time. The male guards the eggs ated backwaters, drains, canals and stillwaters, until they hatch. The incubation period of the eggs although fast-flowing rivers have previously been is approximately seven days at 20Ce. Katano & identified as conduits for dispersal. Maekawa (1997) recorded mean fecundity as 1,049 eggs per female, with a maximum of 6,285. Topmouth Gudgeon Internationally, Topmouth Gudgeon are During early development, Topmouth Gudgeon regarded as a highly invasive pest species. disperse from the nest site to the benthos, where they hide between and under stones. It is not until Habitat all the fins are completely formed that they can be Sunbleak found in the open water of shallow marginal habi- During the first few weeks of development, tats. Topmouth Gudgeon are not a closely shoal- Sunbleak are found in shallow marginal ing species and spread themselves across a broad where water temperatures are generally higher, range of the habitat types available to them. They supporting blooms of zooplankton and facilitat- are less specific than Sunbleak in terms of habitat ing optimum growth conditions. As the larvae choice and can thrive in streams, rivers and still- become more developed (around 40 days), these waters, although they are reported to favour shal- marginal habitats are abandoned in favour of deep low, still or slow-running waterbodies, water away from the banks. Here, they form preferentially with macrophyte beds (Adamek et shoals, swimming just below the water's surface. al. 1996).

December 2003 British Wildlife 79 Sunbleak and Topmouth Gudgeon

Distributionand currentstatus in the UK d --~ £LV,",". . ~'\. N Figure 1 Present f!;. \J /" The original importation of both species is I~-, ' ) +I distributionSunbleak (black)of I /j~ \ believed to have occurred during the mid-1980s ,~ , h~ 'I. "-. and Topmouth through an ornamental-fish supplier near ;V j) \c;. \ Gudgeon (grey) Romsey, in Hampshire. Figure 1 shows an up-to- } ~ ~ in the UK.The date distribution map for both species and the ~. \ arrow shows only known site of introduction to the DK. ~ . Zr-~ the location of ..\><,..>) J i the original Sunbleak :( I ; importation of ~~I~L ~- both species, Originating from continental and Russia, [F~-.""'" ... -/ ~'J although Sunbleak are well distributed from the Caspian j/ ]~._~ Sunbleak are no Sea to the North Sea and from the Volga to the c<,""~ atlongerthis site.present Alps and Pyrenees. In , initial dispersal from the original location in Hampshire is ofTopmouth Gudgeon in England. believed to have occurred via the River Test, An investigation into the current status of which was used by the fish as a conduit to disperse Topmouth Gudgeon in the DK (Gozlan et al. and subsequently colonise Broadlands Lake 2002) revealed that the original introduction farther down the Test floodplain. At this time, occurred at the same ornamental-fish farm facility Broadlands supplied other fisheries with fry, for in Hampshire as did that of Sunbleak. From this stocking purposes, and this is how the introduc- site the species is now present in Tadburn Lake, a tion to Stoneham Lakes, in the Itchen valley, tributary of the River Test and an ornamental occurred (Farr-Cox et al. 1996). pond in High Wycombe (as reported by The origin of the Somerset population is Domaniewski & Wheeler 1996), and at stillwaters unclear, but the first available record is from in Staffordshire. Since these records were 1990, when Sunbleak first appeared in the Kings published, other populations have now been Sedgmoor Drain. From here they have spread reported at stillwaters in Cumbria and Cheshire rapidly, and are now extremely common through- (J Shelly pers. comm.) and in Epping Forest, out drains, rivers and connected waterbodies of north-east London (G Copp pers. comm.). the Somerset Levels. They are also present in Dispersal several stillwaters in this area and at a complex of fishing lakes near Sherborne in Dorset. The mech- There are many potential modes of dispersal for anisms for dispersal to these stillwaters is both Sunbleak and Topmouth Gudgeon. The unknown, but it is likely that the fish were intro- small adult size of both species means that they duced either unintentionally or intentionally by can easily escape from enclosed stillwaters and man. quickly colonise connected waterbodies. This is how Topmouth Gudgeon have come to be resi- Topmouth Gudgeon dent in Tadburn Lake, which drains the original Native to China, Korea, Japan and the River introduction site and joins the River Test approxi- Amur basin, Topmouth Gudgeon were acciden- mately 4km downstream. The use of a wide range tally introduced into Romania in 1960, mixed of spawning substrata also means that eggs can be with commercial carp species imported to an laid on floating macrophytes. The authors have aquaculture facility bordering the lower River observed lily leaves covered in Sunbleak eggs Danube. From here they quickly dispersed floating over the outflow of Stoneham Lakes, in throughout the Danube system, and within three Hampshire, into the River Itchen catchment. The decades they could be found through much of possibility of spawning on the flat surface of boats Europe and Russia. Today, this species is distrib- or trailing plastic fenders, as discussed by Gozlan uted throughout Europe and is also present in et al. (2003a), also enables both species to disperse North Africa. With this super-fast rate of inva- quickly between catchments via canal networks. sion, it is perhaps not surprising that in 1996 Reports of Sunbleak spawning on angling para- Domaniewski & Wheeler reported the first record phernalia could again result in translocation

80 British Wildlife December 2003 Sun bleak and Topmouth Gudgeon

between catchments, if more than one venue was 300 .. .~... Rudd visited on the same day by an angler. Laboratory 250 "0-" Ro"h .{ experiments have shown that Sunbleak eggs in s .+ .. moo)< S 200 ..0... B",,", .-_!I.' particular exhibit a degree of tolerance of dehy- A 0;, .. o. .. Sunbl,O)< ...0 dration. With the difficulties associated with ..@ ISO ~ 0 distinguishing the early life stages of both species ""' 100 from those of native cyprinids (Pinder 2001), the unintentional transfer along with native species is 50 I"'" '~"":' ':.' ".."".: a real concern. In the case of Sunbleak, further dispersal from 3 4 Nse (years) the current range is restricted by the absence of connecting water bodies from the Somerset Levels Figure 2 Growth in fork length (mm) and standard deviation of Sunbleak from Stoneham Lakes, system arid the Ri~ers Test and Itchen. Further Hampshire, compared with UK growth of Bream, dispersal is, however, likely, either accidentally Roach, Bleak and Rudd. From Gozlan et al. (2003a) with transfers of other species or through inten- tional release into the wild by aquarists. If suggest that this aspect of competition has a signif- Sunbleak were to be introduced to the Bristol icant effect on the recruitment of native species. Avon, which borders the Somerset Levels, this Because of the small size of the species, it is not would open up connections to the UK canal just the young of the year that are competing for network, allowing access to some of the large the same food items as native juveniles. Gozlan et lowland rivers, such as the Thames and Great al. (2003a) demonstrated how the slow growth of Ouse, and the fenland drains of East Anglia, Sunbleak could result in four year-classes of this which support many miles of ideal habitat for this species competing for the same food as young-of- specIes. the-year Roach Rutilus rutilus, Bream Abramis The geographical distance between populations brama, Rudd Scardinius erythrophthalmus and of Topmouth Gudgeon in Britain suggests that Bleak, during a period in their life history when dispersal has occurred almost exclusively by they are at their most vulnerable (Fig. 2). anthropogenic means. Excluding the population Another known risk associated with the intro- in Tadburn Lake, which escaped from the original duction of alien species, is direct predation on stock near Romsey, all other populations appear native species. The introduction of Zander to the to be landlocked with no obvious connections to Great Ouse Relief Channel in 1963 (Wheeler & other waterbodies. On the other hand, if presently Maitland 1973) and the subsequent spread of this unrecognised invasions of the canal/river network species are widely blamed for a decline in the value have already taken place or occur in the future, we of invaded fisheries (Smith & Briggs 1999). Criv- predict that the invasive capabilities that this elli (1995) reported the consequences of the intro- species has already demonstrated across Europe duction of Zander to Lake Egridir, in south-west will result in Topmouth Gudgeon becoming wide- Anatolia, as being rapid and irreversible, resulting spread and very abundant throughout Britain. in the total extinction of several species endemic to this system. Threatsto native fishes Although Sunbleak and Topmouth Gudgeon Various threats have been highlighted regarding may be considered beneficial in terms of providing the introduction of these two species. However, forage species for predatory fishes, they also have no attempts have yet been made to quantify these the potential to prey directly on the larval stages of risks. Because of the very fast reproduction rate of our native stocks, including large predatory both species, population size can explode quickly species 'such as Perch Perca fluviatilis, Zander and and both have the potential to become numeri- Pike Esox lucius, during their early stages of devel- cally dominant over the native species after only opment, and thus have a negative effect on the one year of introduction. recruitment of these species. Various authors have highlighted dietary over- Preliminary investigations by Gozlan et al. lap between. both species and native cyprinids. (2003a) found no evidence of piscivory when However, only anecdotal evidence exists to examining the stomach contents of Sunbleak from

December 2003 BritishWildlife 81 Sunbleak and Topmouth Gudgeon

Stoneham Lakes. However, Topmouth Gudgeon Table 1 Some hypothesised general attributes of are widely reported in Europe as eating the eggs invasive aquatic species. From Ricardi & Rasmussen and larval stages of other fishes (Xie et al. 2000). (1998). Indeed, in one study, Topmouth Gudgeon were 1 Abundant and widely distributed in original range found to be the second most voracious consumer 2 Wide environmental tolerance of Zander eggs. 3 High genetic variability Perhaps one of the most severe threats associ- 4 Short generation time 5 Rapid growth ated with the introduction of non-native species is 6 Early sexual maturity the inadvertent importation of parasites and 7 High reproductive capacity diseases. Where fish populations have not evolved 8 Broad diet (opportunistic feeding) in the presence of such bacteria, viruses and para- 9 Gregariousness sites, immune systems are too poorly developed to 10 Possessing natural mechanisms of rapid dispersal 11 Commensal with human activity (e.g. transport in respond to these new threats and leave the native ship ballast water, trade of ornamental species for stock vulnerable to infection or infestation. aquarists) To date, there have been no reports of Sunbleak or Topmouth Gudgeon carrying any pathogens many attributes which have enabled them to novel to the British Isles. In Europe, however, establish large populations around the country. Topmouth Gudgeon are reported to act as a Many of these attributes have previously been vector for the parasites Anguillicola crassus and hypothesised by several authors as important Clinostomum complanatum and also as a carrier factors in determining the success of invasive of Pike fry rhabdovirus (PFR). aquatic species, and are summarised in Table 1. Globally and, in particular, in the Great Lakes Current legislation system of North America, the ballast water of As a precautionary approach to control the import ships has been identified as responsible for the vast and future spread of non-native fishes in England majority of aquatic introductions. Transport of and , DEFRA has introduced a licensing species from the inland freshwaters of the Caspian system for the import and keeping of live fish Sea is a particular problem. In Britain, the threat species considered to be undesirable additions to of invasion via this activity is greatly reduced as our native fish fauna. docking of international trading craft is restricted The Prohibition of Keeping or Release of Live to coastal and estuarine waters, thus preventing Fish (Specified Species) Order 1998 made under access to suitable conditions for freshwater the Import of Live Fish (England and Wales) Act species. In Britain, the aquarist trade poses the 1980 includes both Topmouth Gudgeon and biggest threat to freshwater aquatic biodiversity. Sunbleak. This legislation requires any individual In this country, fish are the third most popular wishing to keep any listed species as pets (in either pets after cats and dogs, and it has been estimated aquarium or garden pond), or angling clubs wish- that 3.5 million households (about 13%) own ing to stock a listed species, first to obtain a licence ornamental fish (Elvira 2000). Indeed, both under the Act. Full details of the Act, including Sunbleak and Topmouth Gudgeon are reported to listed species and application procedures, can be have been sold via the ornamental-fish trade obtained from DEFRA or at the website through garden centres (Farr-Cox;ietat. 1996) and www.efishbusiness.co. uk. pet shops. Presently, little is known about the conse- Conclusion quences of such invasions and the potential It must be considered that any species has the impacts on the native ecosystem. To assess potential to establish populations in the wild whether the presence of Sunbleak and Topmouth providing that there is suitable habitat available. Gudgeon is a real threat to our native aquatic However, if an introduced species can exploit an fauna, future research needs to address the follow- empty ecological niche, this greatly enhances its mg: chances of success within the new ecosystem . do dietary overlaps exist between these species (Leveque 2000). and natives? Both Sunbleak and Topmouth Gudgeon possess . do the new species prey directly on the eggs and 82 British Wildlife December 2003 Sunbleak and Topmouth Gudgeon

larvae of native species? tion records, and to Henry Arnold and the Biolog- . do the new species compete for habitat and ical Records Centre (CEH, Monks Wood) for space with the native species? providing distribution maps. We also wish to . how does the recruitment success of the new thank all the angling clubs and fisheries that species compare with that of natives? assisted us by returning Sunbleak awareness and . does the presence of Topmouth Gudgeon or distribution questionnaires. Sunbleak have a negative or positive effect on References the recruitment, growth and population health of natives? Adamek, Z, Navratil, S, Palikova,M, &Siddiqui,MA 1996 Pseudorasb- ora parva Schlegel, 1842: Biology of non-native species in the Czech In the case of Sunbleak, since this species is Republic. In Proceedings of scientific papers to the 75th Anniversary of Foundation of the Research Institute of Fish Culture and Hydrobi- established throughout the connected waterbodies ology (ed. Martin Flajshans), pp. 143-152 of the Somerset L,evels, it is undoubtedly here to Balon, E K 1995 Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers. Aquacul- stay, as any att~inpt to control or eliminate it ture 129: 3-48 would be futile. The fact that Topmouth Gudgeon Crivelli, A J 1995 Are fish introductions a threat to endemic freshwater fishes in the northern Mediterranean region? Bioi. Conserv. 72: 311- are currently believed to be restricted to enclosed 319 stillwaters allows some scope for the control or Domaniewski, J, & Wheeler, A 1996 The topmouth gudgeon has arrived. Fish 43: 40 total eradication of this species. If unintentional or Elvira, B 2000 Identification of non-native freshwater fishes established intentional introductions of either species should in Europe and assessment of their potential threats to biological occur within the interconnected canal/river diversity. Convention on the conservation of European wildlife and natural habitats. 27st meeting Strasbourg, 26-30 November 2007 network of Britain, however, we predict that, p.35 Farr-Cox, F, Leonard, S, & Wheeler, A 1996 The status of the recently because of their unusual life-history strategies and introduced fish Leucaspius delineatus (Cyprinidae) in Great Britain. broad range of environmental tolerance limits, Fisheries Management and Ecology 3: 193-199 Gozlan, R E, Pinder, A C, & Shelley, J 2002 Occurrence of the Asiatic they will become widespread and very abundant cyprinid Pseudorasboraparva in England.1. Fish Bioi. 61' 298-300 within the right habitats. Gozlan, R E, Pinder, A C, Durand, S, & Bass, J 2003a Could the small If the British populations of these alien species size of Leucaspius delineatus (Pisces, Cyprinidae) be an ecological advantage in invading British waterbodies? Folio Zoologica 52 (1): are found to prey opportunistically on the eggs 99-108 Gozlan, R E, Flower, C J, & Pinder, A C 2003b Reproductive success in and larvae of other species, then their spread to male sunbleak, a recent invasive fish species in the UK. 1. Fish Bioi. natural lakes such as Windermere, in the Lake 63: 1-13 District, could prove devastating to the already Katano, 0, & Maekawa, K 1997 Reproductive regulation in the female Japanese minnow, Pseudorasbora parva (Cyprinidae). Env. Bioi. Fish. endangered populations of native whitefish in that 49 (2): 197-205 Lelek, A 1987 The freshwater fishes of Europe. Threatened fishes of region. Europe. AULA-Verlag Wiesbaden 9 The driving motive behind the production of Leveque, C 2000 L'histoire des milieux modele les especes. La this article has been to raise awareness of these Recherche 333: 56-57 Pinder, A C 2001 Keys to larval and juvenile stages of coarse fishes species, with a view to gaining a better picture of from freshwaters in the British Isles. Scientific Publication no. 60 the true distribution of these two new additions to p.134. Freshwater Biological Association, Ambleside Pinder, A C, & Gozlan, REin press Early ontogeny of Sunbleak the aquatic fauna of Britain. Leucaspiusdelineatus. 1. FishBioi. Ricardi, A, & Rasmussen, J B 1998 Perspectives: Predicting the identity Any reports of the further spread of either and impact of future biological invaders: a priority for aquatic species, or the occurrence of any unidentified resource management. Can.1.Fish.Aquat. Sci. 55: 1759-1765 Smith, P, & Briggs, J 1999 Zander - The hidden invader. British Wildlife fishes from British fresh waters, would be 11: 2-8 welcomed by Adrian Pinder at the Centre for Ecol- Wheeler, A, & Maitland, PS 1973 The scarcer freshwater fishes of the BritishIsles1 Introduced species.J.FishBioi.5: 49-68 ogy and Hydrology, Winfrith Technology Centre, Xie, S, Cui, Y, Zhang, T, & Li, Z 2000 Seasonal patterns in feeding ecol- Winfrith Newburgh, Dorchester, Dorset DT2 ogy of three smallfishes in the Biandantang Lake,China.1. FishBioi. 57: 867-880 8ZD (e-mail: [email protected]).

Acknowledgements The authors are grateful to Eastleigh and District Angling Club for its continued co-operation in allowing us to carry out our research at Stoneham Both Adrian C Pinder and Dr Rodolphe E Gozlan are Lakes, to Mark Stollery for providing historical fish ecologists based at CEHDorset, specialising in the impacts of alien introductions and the early information and samples of Topmouth Gudgeon, development of fishes. to Jon Shelley (Environment Agency) for distribu-

December 2003 British Wildlife 83