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EU NON-NATIVE SPECIES RISK ANALYSIS – RISK ASSESSMENT TEMPLATE V1.0

EU NON-NATIVE ORGANISM RISK ASSESSMENT SCHEME

Name of genus: Lepomis (Rafinesque, 1819) - Sunfishes Lepomis auritus (Linnaeus, 1758) – Redbreast Sunfish Lepomis cyanellus Rafinesque, 1819 –Green SunfishLepomis gibbosus (Linnaeus, 1758) – kiver, Pumpkinseed Lepomis gulosus (Cuvier in Cuvier and Valenciennes, 1829) –Warmouth Lepomis humilis (Girard, 1858) – Orangespotted Sunfish Lepomis macrochirus Rafinesque, 1819 –Bluegill Lepomis marginatus (Holbrook, 1855) – Dollar Sunfish Lepomis megalotis (Rafinesque, 1820) –Longear Sunfish Lepomis microlophus (Günther, 1859) –Redear Sunfish Lepomis miniatus (Jordan, 1877) – scarlet sunfish, Redspotted Sunfish Lepomis peltastes Cope, 1870 – Northern Sunfish Lepomis punctatus (Valenciennes in Cuvier and Valenciennes, 1831) – Spotted Sunfish Lepomis symmetricus Forbes in Jordan and Gilbert, 1883 – Bantam Sunfish

Author: Deputy Direction of Nature (Ministry of Agriculture, Fish, Food and Environment of Spain)Risk Assessment Area: EuropeDraft: December 2016

Peer reviewed by: Dr. Carlos Fernández-DelgadoGrupo de Investigación "Aphanius"Departamento de Zoología. Córdoba University.correo-e: [email protected]://www.uco.es/aphaniusLaura Capdevila ArgüellesCoordinator of GEIB - Grupo Especialista en Invasiones Biológicas. correo-e: [email protected]://geib.blogspot.com

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Date of finalisation: 31/01/2017

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EU CHAPPEAU

QUESTION RESPONSE

1. In how many EU member states has this species been recorded? List them. Lepomis auritus (Linnaeus, 1758)

Germany (Holčik, 1991; Elvira, 2001), Italy (Welcomme, 1988, Elvira, 2001; Bianco, 2013), Czech Republic (DAISIE, 2016)

Lepomis cyanellus (Rafinesque, 1819)

Germany (Elvira, 2001; NOBANIS, 2016).

Lepomis gibbosus (Linnaeus, 1758)Austria, Belgium, Bulgaria, Croatia, Czech Republic, Denmark, Estonia, France, Germany, Hungary, Italy, Latvia, Lithuania, Luxembourg, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain, United Kingdom (Elvira, 2001; CABI, 2011; Froese and Pauly, 2009; NOBANIS, 2016); Cyprus (Zogaris et al, 2012) and Greece (Zenetos et al, 2009).

Lepomis megalotis (Rafinesque, 1820)Germany (Geiter, 2002)

There is no information about the introduction of the other species of Lepomis in EU countries.

2. In how many EU member states has this species currently established populations? List them.

Lepomis auritus Germany, Italy (Elvira, 2001)

Lepomis cyanellusGermany (Elvira, 2001)

Lepomis gibbosus is now established in at least 28 countries of Europe and Asia minor (Copp and Fox, 2007). Only in Europe it is established in 23, possibly 24

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https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=168131



countries. These are: Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Latvia, Luxembourg, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain and UK (CABI, 2011, NOBANIS, 2011), Lithuania and possibly Estonia (Elvira, 2001).

It seems that other species of Lepomis are not established in Europe, but most of them demonstrated their invasive character in other parts of the world where introduced (see question 8, Section A).

3. In how many EU member states has this species shown signs of invasiveness? List them.

Lepomis gibbosus is considered a pest anywhere has been introduced. This species is invasive in Netherlands, Portugal, Romania, Spain and UK (CABI, 2011), Austria, Belgium, Denmark, Germany (NOBANIS, 2016), but formed established populations in almost all countries in Europe (Cucherousset et al., 2009).

Lepomis auritus has supplanted the native bleak Alburnus alburnus in some Italian oligotrophic lakes (Elvira, 2001).

L. auritus, L. cyanellus and L. megalotis, are already present or established in Germany; its characteristics of a successful invader increase the possibility of becoming invasive in any country with similar or warmer climate.

There is no evidence of invasiveness of other Lepomis spp in Europe at the moment.

4. In which EU Biogeographic areas could this species establish? Lepomis gibbosus can tolerate a wide range of climatic conditions. It is present in all biogeographic areas: Continental area, Mediterranean area, Atlantic area, Black Sea area, Pannonian area, Alpine area, Macaronesian area, Boreal area and Steppic Area.

5. In how many EU Member States could this species establish in the future [given current climate] (including those where it is already established)? List them.

L. gibbosus established in all biogeographic areas in Europe, so other Lepomis species are likely to establish in any European countries, giving their similar charac-teristics and flexibility in their habitat preferences (Soes et al., 2011).

These countries, including those where at least L. gibbosus is already established, are: Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Latvia, Lithuania, Luxembourg, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain and UK. In the future, L.

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gibbosus could still establish in Estonia (if not already), Malta and Ireland. Finland and Sweden present a lower risk because of colder climate.

In a study realized in Netherlands, Soes et al (2011) indicate a medium or high risk of establishment for six Lepomis species for countries with similar or warmer climate as Netherlands. These countries are: Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Luxembourg, Malta, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain and UK.

6. In how many EU member states could this species become invasive in the future [given current climate] (where it is not already established)?

Lepomis gibbosus is cited as invasive in: Netherlands, Portugal, Romania, Spain and UK (CABI, 2011), Austria, Belgium, Denmark, Germany (NOBANIS, 2016).

At least six Lepomis species could become invasive in any country in Europe in which water temperature would allow reproduction. These countries are: Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Luxembourg, Malta, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain and UK.

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SECTION A – Organism Information and Screening

Stage 1. Organism Information RESPONSE[chose one entry, delete all others]

COMMENT

1. Identify the organism. Is it clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?

This Risk Assessment refers to genus Lepomis and includes information about the most representative species, which have been introduced in Europe and es-tablished populations in at least one country.

Hybridization is common among centrarchid fishes. This makes the task of identifying difficult or almost impossible, and could require using molecular techniques (Soes et al, 2011).

Kingdom: Animalia >> Phylum: Chordata >> Class: Actin-opterygii >> Order: Perciformes >> Family: Centrarchidae

The genus Lepomis (Rafinesque, 1819) is part of Perciformes Order (Perch-likes) and Centrarchidae Family (Sunfishes). This family includes some of the more attractive and brightly colored of the freshwater fishes of North America.

EN: common sunfishes, eared sunfishes

Direct children (from Integrated Taxonomic Information System (ITIS) (http://www.itis.gov):

Lepomis auritus (Linnaeus, 1758) EN:Redbreast Sunfish, ES: mojarra pecho rojo, FR: crapet rouge

Lepomis cyanellus (Rafinesque, 1819)EN: green sunfish, ES: pez sol, FR: crapet vert.

Lepomis gibbosus (Linnaeus, 1758)EN: Pumpkinseed, Sunfish, DE: Sonnenbarsch, FR: Perche

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soleil, IT: Perisco sole, ES: Pez sol, perca sol.

Lepomis gulosus (Cuvier, 1829) – EN: Warmouth, ES: mojarra golosa, FR: crapet sac-à-lait,

Lepomis humilis (Girard, 1858) – EN: Orangespotted Sunfish; ES: Mojarra, FR: crapet menu;

Lepomis macrochirus (Rafinesque, 1819) – EN: Bluegill, ES: mojarra oreja azul, FR: crapet arlequin,

Lepomis marginatus (Holbrook, 1855) – Dollar Sunfish

Lepomis megalotis (Rafinesque, 1820) – EN: Longear Sunfish, ES: mojarra gigante, mojarra orejona, FR: crapet à longues oreilles

Lepomis microlophus (Günther, 1859) – EN: Redear Sunfish, ES : mojarra oreja roja

Lepomis miniatus (Jordan, 1877) – scarlet sunfish, Redspotted Sunfish

Lepomis peltastes Cope, 1870 – EN: Northern Sunfish, FR: crapet du nord

Lepomis punctatus (Valenciennes in Cuvier and Valenciennes, 1831) – EN: Spotted Sunfish, ES: mojarra manchada

Lepomis symmetricus (Forbes in Jordan and Gilbert, 1883) Bantam Sunfish

It is expected that several additional centrarchid species are

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likely to be identified after further research using molecular techniques (Near and Koppelman, 2009), especialy in polymorhic taxa like L. megalotis and L. macrochirus.

2. If not a single taxonomic entity, can it be redefined? (if necessary use the response box to re-define the organism and carry on)

NA

3. Does a relevant earlier risk assessment exist? (give details of any previous risk assessment)

Yes In 2010 Netherlands presented a risk analysis of sunfishes (Centrarchidae) in Netherlands. In this study it is shown that at least another four species of Lepomis, besides L. gibossus, should be considered to be potentially invasive and they are all available for export in North America at least, and have a high probability of establishment based on their thermal biology: L. cyanellus, L. macrochirus, L. megalotis. When considering possible climate change in the period 1990-2050, L. auritus should be included in this list (Soes et al, 2011).

L. gibbosus has been subject to FISK assessment (Copp et al., 2009; Almeida et al., 2013) but there is no Risk assessment specific of the genus Lepomis.

4. If there is an earlier risk assessment is it still entirely valid, or only partly valid?

Yes In the study of Centrarchidae developed in Netherlands, commissioned by the Invasive Alien Species Team of the Food and Consumer Product Safety Authority, a risk analysis was undertaken to provide more insight into the present distribution of Centrarchidae [...], their (potential) impacts, the probability of entry (introduction pathways), the probability of establishment, the probability of further spread and endangered areas. Subsequently, measures are identified to prevent further spread of these species and eradication and physical control methods are described that can be used to reduce their number in The Netherlands.

The FISK assessment developped in UK by Copp et al., 2009; and in Iberia by Almeida et al., 2013 are still valid.

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5. Where is the organism native? Lepomis species are widely distributed throughout the lakes and rivers of the North and Central America.

- Lepomis auritus is native from Atlantic and Gulf Slope drainages, from New Brunswick to central Florida, and west to the Apalachicola and Choctawhatchee drainages, Georgia and Florida (Page and Burr 1991). - Lepomis cyanellus is native to the central plains of North America between the Appalachian and Rocky Mountains, from Ontario (Canada) and New York state in the north to the Gulf Coast and northern Mexico in the south.- Lepomis gibbosus is native to the eastern part of North America, where sunfishes are known to have existed since the Miocene (Scott and Crossman, 1973). - Lepomis macrochirus is native of Mexico, USA and Canada (CABI, 2013).- Lepomis megalotis is native to the Mississippi River basin west of the Appalachian Mountains from Indiana west to eastern Illinois and south to the Gulf of Mexico and to Gulf Slope drainages from the Choctawhatchee River, Florida, west to the Rio Grande, Texas, southern New Mexico, and northeastern Mexico (Page and Burr, 1991; Miller, 2005).

6. What is the global distribution of the organism (excluding Europe)? Lepomis auritus

Dominican Republic, Mexico, Puerto Rico (Froese and Pauly, 2012), USA (introduced in Alabama, Arkansas, Georgia, Kentucky, Louisiana, North Carolina, Oklahoma, Texas, Tennessee, Virginia) (Fuller, 2016).

Lepomis cyanellus This species has been so widely introduced in the USA that it is now present in almost every state, including Atlantic and Pacific slope drainages and Hawaii, except for parts of

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the north-east of the country (Page and Burr, 1991). It was introduced to China in 1999 for use as food (Ma et al., 2003), Philippines where it was introduced from the United States in 1950 for aquaculture purposes, Although there are reports of an established population in Japan (Welcomme, 1988; Froese and Pauly, 2013).

Lepomis gibossusNative from the East of North America it has been introduced in Turkey and Georgia in Asia Minor; Congo and Morocco in Africa; Brazil, Chile and Venezuela, Cuba, Guatemala in America, also in the West from EEUU and Canada (CABI, 2011).

Lepomis macrochirusBluegill has been introduced to a number of countries including Iran, Japan, Korea, Philippines, South Africa, Kenya, Morocco, Mauritius, Brazil, Congo, Cuba and Puerto Rico (CABI, 2013).

Lepomis megalotis was largely introduced in the USA. The species that have been repeatedly been introduced outside their native area are L. cyanellus, L. gibbosus and L. macrochirus (Soes et al, 2011).

7. What is the distribution of the organism in Europe? Lepomis auritus

Germany, Italy (Elvira, 2001), Czech Republic (DAISIE, 2016)

Lepomis cyanellus Germany (Elvira, 2001)Also Maitland (1977) (cited in Soes et al., 2011) reported that the introduction of L. cyanellus by aquarists to the Frankfurt area in Germany led to established populations;

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Lepomis gibossusWidely distributed across Europe, only not present in Finland, Sweden, Ireland and Malta.

Lepomis megalotis Germany (Geiter, 2002)

8. Is the organism known to be invasive (i.e. to threaten organisms, habitats or ecosystems) anywhere in the world?

The redbreast sunfish Lepomis auritus has supplanted the native bleak Alburnus alburnus in some Italian oligotrophic lakes (Elvira, 2001).

In streams where L. cyanellus has been introduced in California, it is believed to have helped deplete the California roach, Hesperoleucus symmetricus (CABI, 2013). L. cyanellus along with other predatory fish species is also thought to be responsible for the decline of native frogs and salamanders in the USA (CABI, 2013). L. cyanellus is listed as a major invasive species in parts of Arizona (USDA, 2012) and California (Dill and Cordone, 1997). New Jersey state authorities list it as a potentially dangerous species due to its ability to outcompete native fish species; it is listed as an invasive species of concern in Georgia and Florida (CABI, 2013). Marsh (2010), in a discussion on the advantages of genetic biocontrol in the Colorado River basin system, referred to the species as “one of the most invasive, pervasive, and destructive species in the basin, not even recognized as an invasive species by some states”. Olden and Poff (2005), in a study of long-term trends (> 160 years) of fish species distributions in the Lower Colorado River Basin, to identify those native species exhibiting the greatest rates of decline and those non-native species exhibiting the highest rates of spread, found that L. cyanellus was amongst the fastest expanding invaders in the basin and the most invasive in terms of negative impacts on native fish communities

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L. cyanellus and other introduced predatory centrarchids are also believed to have played a part in the decline of the California tiger salamander (Ambystoma californiense) in California (Hayes and Jennings, 1986; Dill and Cordone, 1997) and the Chiricahua leopard frog (Rana chiricahuensis [Lithobates chiricahuensis]) populations in southeastern Arizona (Rosen et al., 1995). L. cyanellus is not listed as a threatened species in any part of its native range (CABI, 2013).

L. gibbosus is recorded from standing waters, such as moorland pools ponds, lakes, river meanders and canals, but the species is also encountered in streams (Klaar et al. 2004) and rivers (Balon, 1959).

L. gibbosus is listed among the top ten introduced fish species with adverse ecological effects (Casal, 2006). It is considered a threat for native fish species (Welcomme, 1988) through competition for food and predation on eggs and juveniles. Densities decreases of fish species have been reported to regularly coincide with sharp increases in L. gibbosus abundances (Tomoček et al., 2007 and literature therein). The species is also held responsible for the locally strong decline and disappearance of endangered amphibians, such as Pelobates fuscus, Triturus cristatus and Hyla arborea (Bosman, 2003; Soes, 2011) and dragonflies (Janssen, 2000), including several species covered by Natura 2000.

Pumpkinseed is omnivorous and an opportunistic feeder. Prey selection varies with age, prey availability, habitat, season and presence of other fish species. There are two morphological forms of Pumpkinseed; one, with wide short gill rakers that feed mainly on benthic macro invertebrates and, a second, with longer gill rakers, better adapted to feed

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on planktonic prey. Fry feed on zooplankton but Pumpkinseed becomes more piscivorous as it grows larger (DFO, 2011).

Lepomis macrochirus is known to be invasive in Japan, Korea (Kawamura et al., 2006), South Africa (Wellcome, 1988) and some states of the USA (CABI, 2013). In these areas it can overcrowd and stunt the growth of other fish, including native sunfish species, by competing for food and habitat. It may even cause displacement and extinction of native fish. The invasion success of L. macrochirus in Lake Biwa in Japan is attributed to its drastic population growth shortly after its introduction, together with artificial transplantations (Kawamura et al., 2010). They feed on the young of some native fishes, threatening the survival of several species such as the tanago (Acheilognathus melanogaster) and honmoroko (Gnathopogon caerulescens) (CABI, 2013). This species is commonly considered a pest in its introduced range and several countries report it causing negative ecological effects (Myers et al., 2016; Froese and Pauly, 2016). L. macrochirus overcrowd and stunt the growth of other fish and may even be responsible for causing extinctions, such as the extinction of a native fish in Panamá (CABI, 2013)

Lepomis cyanellus and L. macrochirus are mentioned as two of the most commonly reported alien species in US National Parks (Ziska and Dukes, 2014).

In conclusion, like L. gibbosus also other Lepomis species are likely to affect ecosystems mainly by predation (amphibians, smaller fish species, damselflies, etc.) and competition with other predatory fish. Especially ecosystems, lacking comparable native predatory fish species prior to the establishment of such an exotic

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centrarchid, are susceptible to significant ecological impact.

9. Describe any known socio-economic benefits of the organism in the risk assessment area.

Lepomis auritus has been imported as an aquarium fish but not become a great success in aquaristics (Soes, 2011).

Lepomis cyanellus was imported for stock enhancement or ornamental trade but it is a relatively large species with ag-gressive predatory behavior that makes them less suitable for ponds that offer too little space and cover. L. gibbosus is principally a recreational sportfish species, with production in aquaculture facilities for stocking of recreational fishing waters, baitfish production (as a food item for Micropterus salmoides) and scientific research. L. gibbosus are also sold in the aquarium trade.

Lepomis macrochirus Fisheries: minor commercial; aquaculture: commercial; gamefish: yes; aquarium: commercial (Froese and Pauly, 2016). Also commonly stocked as forage for the largemouth bass, Micropterus salmoides (Fuller et al., 1999).

In conclusion, the establishment of larger centrarchid species would have a small, positive social and economic impact to commercial fisheries, the angling society and related business.

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SECTION B – Detailed assessment

PROBABILITY OF ENTRY

Important instructions: Entry is the introduction of an organism into Europe. Not to be confused with spread, the movement of an organism within Europe. For organisms which are already present in Europe, only complete the entry section for current active pathways of entry or if relevant potential future

pathways. The entry section need not be completed for organisms which have entered in the past and have no current pathways of entry.

QUESTION RESPONSE[chose one entry, delete all others]

CONFIDENCE[chose one entry, delete all others]

COMMENT

1.1. How many active pathways are relevant to the potential entry of this organism?

(If there are no active pathways or potential future pathways respond N/A and move to the Establishment section)

Many Moderate L. gibbosus was introduced mainly as an ornamental fish, and stocked in gardens as well as in aquaria, and released through accidental or deliberate releases to different water bodies (Geiter, 2002; Tandon, 1976).

For angling purposes initially was introduced as a sport fish but later as a forage fish for piscivorous fishes (CABI, 2011).

Some authors also assume that L. gibbosus could be introduced unintentionally, for instance with imports of carp fry used in stocking (Tandon, 1976).

L. gibbosus has been intentionally (but illegally) introduced to lakes in Denmark with Onchorhynchus mykiss under the presumption that they would free the Rainbow trout from the fish louse (Argulus sp.) (NOBANIS, 2016)

Lepomis species could entry as ornamental pet and for

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sportfishing.1.2. List relevant pathways through which the organism could enter. Where possible give detail about the specific origins and end points of the pathways.

For each pathway answer questions 1.3 to 1.10 (copy and paste additional rows at the end of this section as necessary).

[Sport Fishing; and Pet-trade]

The main introduction pathways for L. gibbosus was as an ornamental fish including stocking in outdoor ponds as well as in aquaria (e.g. United Kingdom), sport fishing (e.g. France), or for extensive fish culture for use as forage food for largemouth bass (Iberia and Congo) and more recently as a pet fish, i.e. indoor aquaria. Human assistance in the spread of L. gibbosus (e.g. by anglers) appears to be more common in southern Europe than elsewhere, though it is rarely sought after in Europe as an angling amenity in its own right (CABI, 2011).

Fig. 1: The main introduction pathways of aquatic species within Europe (Garcia-Berthou et al, 2005)

Active pathways for any Lepomis species:- ornamental trade by aquarists;- intentional stocking for sportfishing.- introduction as forage fish (Przybylski, et al., 2011).- unintentionally with imports of other species used in stocking (Tandon, 1976).

Pathway name: [Sportfishing activities]

1.3. Is entry along this pathway intentional (e.g. the intentional high Lepomis gibossus has been intentionally imported for

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organism is imported for trade) or accidental (the organism is a contaminant of imported goods)?

(If intentional, only answer questions 1.4, 1.9, 1.10, 1.11)

accidental fishing activities in many parts of Europe, and also as forage food for Micropterus salmoides (Fuller et al., 1999).

The pathway through which L. macrochirus were introduced across the United States is through introduction for recreational fishing also as forage fish for Micropterus salmoides (Kawamura et al. 2010).

Some species (e. g. L. cyanellus) where introduced outside its native area with other intended species as a stock contaminant (CABI, 2013).

In conclusion the entry along this pathway could be intentional but also accidental.

1.4. How likely is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year?

Subnote: In your comment discuss how likely the organism is to get onto the pathway in the first place.

unlikely low Over the course of one year it is not expected that a large number of organism would entry in Europe. Specimens coming from North America is not expected, because anglers take them from established populations in Europe.

But the use of the fish as forage fish makes very easy the introduction in natural habitats.

1.9. How likely is the organism to be able to transfer from the pathway to a suitable habitat or host?

very likely high Once entered it is very likely that the organism transfer to a suitable habitat.

1.10. Estimate the overall likelihood of entry into Europe based on this pathway?

likely medium Even the demand has decresed, Lepomis species could be imported for sportfishing activities.

Pathway name: [Pet-trade ]

1.3. Is entry along this pathway intentional (e.g. the organism is imported for trade) or accidental (the organism is a contaminant of imported goods)?

intentionalaccidental

high Lepomis species are intentionally imported for aquariums or garden lagoons, but demand has decreased.

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They can also be introduced accidentally as a contaminant with other species.

1.4. How likely is it that large numbers of the organism will travel along this pathway from the point(s) of origin over the course of one year?

Subnote: In your comment discuss how likely the organism is to get onto the pathway in the first place.

unlikely medium Over the course of one year it is not expected that a large number of organism would entry in Europe. Entries from North America are very unlikely but trade can be done between European countries.

1.9. How likely is the organism to be able to transfer from the pathway to a suitable habitat or host?

very likely high Pets are released into the wild when owners don’t want to keep them anymore.

1.10. Estimate the overall likelihood of entry into Europe based on this pathway?

unlikely low Trade can be done between European countries.The probability of new entries of Lepomis species as pet-trade from North America is low. .

End of pathway assessment, repeat as necessary.

1.11. Estimate the overall likelihood of entry into Europe based on all pathways (comment on the key issues that lead to this conclusion).

moderately likely medium New entries of other Lepomis species in Europe, as pets or sportfishing activities cannot be discarded.

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PROBABILITY OF ESTABLISHMENT

Important instructions: For organisms which are already well established in Europe, only complete questions 1.15 and 1.21 then move onto the spread section. If uncertain,

check with the Non-native Species Secretariat.

QUESTION RESPONSE CONFIDENCE COMMENT1.15. How widespread are habitats or species necessary for the survival, development and multiplication of the organism in Europe?

widespread High Opportunistic dietary of the genus and suitable habitats present widely distributed in the Risk As-sessment Area.

The plasticity of this species makes them able to adapt in response to changes in biotic and abiotic conditions. All centrarchidae species are opportun-istic and rather flexible in their diet. This flexibil-ity is well presented by L. gibbosus but it seems that other species of Lepomis have the same suc-cess as invaders (Soes, 2011)

In the case of L. cyanellus, population abundance is positively correlated with percentage vegetative cover (Moyle and Nichols, 1973). It can tolerate turbidity, siltation, intermittent flow, high temperatures, high salt content and low dissolved oxygen.

In conclusion the necessary habitats for survival, development and multiplication are widespread.

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1.21. How likely is it that biological properties of the organism would allow it to survive eradication campaigns in Europe?

Likely high L. cyanellus is described as a very successful invader. Its aggressive nature allows it to quickly dominate wherever it is introduced, taking over in a very short period, and becoming the only species in a particular area, thus posing a major threat to native species (Etnier and Starnes, 2001). As a pioneering species, it is also the first species to find its way to newly created farm ponds and the first to repopulate streams following periods of drought (Tomelleri and Eberle, 1990; Pflieger, 1975, 1997).

The same characteristics of a very adaptative organism are described to other Lepomis species (CABI, 2011; CABI, 2013).

In conclusion in small streams, lakes or ponds, control and eradication techniques could be successfully employed to extirpate or suppress isolated populations (Ling, 2003; Britton et al., 2010; Davies and Britton, 2015). But when it is established in a large river system, Lepomis is nearly impossible to eradicate.

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PROBABILITY OF SPREAD

Important notes: Spread is defined as the expansion of the geographical distribution of a pest within an area.

QUESTION RESPONSE CONFIDENCE COMMENT

2.1. How important is the expected spread of this organism in Europe by natural means? (Please list and comment on the mechanisms for natural spread.)

major medium Escapement of L. gibbosus propagules from hydrologically connected waterbodies has been demonstrated and is likely to increase under climate change scenarios (Fobert et al, 2013).

Additionally, increases in water temperatures, particularly in lentic environment, is likely to facilitate successful reproduction and invasive potential.

When L. macrochirus are newly introduced to an area, they do not need a very high propagule pressure to establish and spread relatively quickly. They have a high morphological, physiological and behavioral adaptability to their new environment (Kawamura et al., 2010).). Once they are introduced, they have a high morphological, physiological, and behavioral adaptability to their new environment (Gross and Charnov, 1980, Ehlinger et al. 1997),

2.2. How important is the expected spread of this organism in Europe by human assistance? (Please list and comment on the mechanisms for human-assisted spread.)

major medium Spread by human assistance could happen because of intentional stocking for sportfishing (Fuller, 2016).The use as forage for fishing and its release in ponds and aquariums may happen even if demand has decreased.

2.3. Within Europe, how difficult would it be to contain Difficult high L. cyanellus is difficult to control once it has become

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the organism? established in ponds. The entire fish population must be eliminated with chemicals, with its contaminant environmental dangers, or the pond drained to eliminate these fish. Sometimes it is possible to control numbers by continuous trapping, or by destroying spawning areas. The removal of vegetation cover will also expose L. cyanellus to predatory fish species (CABI, 2013).

L. gibbosusSubsequent to establishment of L. gibbosus populations in the lotic environment, control and containment would be very difficult. Containment within lakes and ponds is feasible and extirpation of populations in small stream systems, lakes and ponds with hydrological connections is possible (Davies and Britton, 2015), but may incur high costs, financially and ecologically.

L. macrochirus has become an issue in bass-bluegill (Micropterus salmoides-Lepomis macrochirus) population management in the USA (Etnier and Starnes, 2001).

When established, centrarchid populations can in most instances only be eradicated with rigorous measures like dewatering or the use of piscicides. Obviously, the prevention of entries and further spread reduces the need for such actions. The major components of prevention are banning of potential invasive species from trade and educating the public about the impact of centrarchids (Soes at al., 2011).

2.4. Based on the answers to questions on the potential for establishment and spread in Europe, define the area

Most of Europe high Tolerates water temps 4 – 28°C; Some species needs water above 20 °C for reproduction (CABI, 2013).

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endangered by the organism. Centrarchids can experience a broad range of climatic conditions during winter across their range. Pro-nounced latitudinal gradients in winter conditions ex-ist with growing degree days and summer tempera-tures both declining with latitude, while winter sever-ity (i.e., lower daily temperatures) and winter length both increase with latitude.

2.5. What proportion (%) of the area/habitat suitable for establishment (i.e. those parts of Europe were the species could establish), if any, has already been colonised by the organism?

10-33 low Given the high proportion of countries in which it is establish, as well as its adaptability, is considered that it may be of the order of that proportion.

2.6. What proportion (%) of the area/habitat suitable for establishment, if any, do you expect to have been invaded by the organism five years from now (including any current presence)?

10-33 low Given the recent colonization of the species it is estimates that its colonization to five-year view may be of this order.

2.7. What other timeframe (in years) would be appropriate to estimate any significant further spread of the organism in Europe? (Please comment on why this timeframe is chosen.)

40 low There is not a follow-up of its expansion, but considered, given the conditions of expansion in which the species occurs, this can be significant in this period. If taking in consideration climate warming, this interval could be shorter.

2.8. In this timeframe what proportion (%) of the endangered area/habitat (including any currently occupied areas/habitats) is likely to have been invaded by this organism?

10-33 low There is not information about the endangered areas/habitats occupied by the species, but given the endangered situation of the habitats in wetlands and rivers in Europe, it is estimated that it could be of the order of this proportion.

2.9. Estimate the overall potential for future spread for this organism in Europe (using the comment box to indicate any key issues).

High low Verbrugge et al. (2012) indicate in the comparison of risk classifications for 25 aquatic non-native species using various European risk identification protocols a high risk for Lepomis gibossus.

Soes et al. (2011) identified six Lepomis species as suspected to establish in most European countries (see

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question 2.26).

The spread of the species depends of the different life-history of the different places where it is (Fox et al, 2007), but it has been demonstrate that climate change will help the future spread of these species (Copp et al. (2009), Britton et al. (2010), Zieba et al. (2015).

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PROBABILITY OF IMPACT

Important instructions: When assessing potential future impacts, climate change should not be taken into account. This is done in later questions at the end of the assessment. Where one type of impact may affect another (e.g. disease may also cause economic impact) the assessor should try to separate the effects (e.g. in this

case note the economic impact of disease in the response and comments of the disease question, but do not include them in the economic section). Note questions 2.10-2.14 relate to economic impact and 2.15-2.21 to environmental impact. Each set of questions starts with the impact elsewhere in

the world, then considers impacts in Europe separating known impacts to date (i.e. past and current impacts) from potential future impacts. Key words are in bold for emphasis.

QUESTION RESPONSE CONFIDENCE COMMENTS

2.10. How great is the economic loss caused by the organism within its existing geographic range, including the cost of any current management?

High Moderate There are no studies about the economic loss but most of the states where introduced have complaint.

2.11. How great is the economic cost of the organism currently in Europe excluding management costs (include any past costs in your response)?

Unknown There is no information available regarding the economic impacts of Lepomis spp. in its introduced range but many authors described the important impact of invasive species over the native or endemic species (Elvira, 1997, Doadrio, 2002). The loss of native species that it produced supposes an important economic lost.

The occurrence of fish-predators non-native in Iberian fresh waters, is probably one of the main detrimental factors influencing the survival of endemic species (mostly Cyprinidae an Cobitidae). Lepomis spp became direct competitors or predators over native species as: Anaecypris hispanica, Cobiditis paludica, C. calderoni Salmo trutta etc.

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2.12. How great is the economic cost of the organism likely to be in the future in Europe excluding management costs?

High Moderate There are no studies regarding these economic costs.

2.13. How great are the economic costs associated with managing this organism currently in Europe (include any past costs in your response)?

Unknown In the case of the Italian project “Palata Menasciutto – management and conservation of wet woodlands” (LIFE99 NAT/IT/6253), the eradication of the pumpkinseed sunfish (Lepomis gibbosus) was considered no longer feasible after the start of the activities. The eradication was not possible because the water bodies hosting the two species were lying too close to a river course, and floods, which occur periodically in that area, would have brought about a natural re-colonisation. Another constraint was the lack of species-specific eradication techniques to be applied to fish.

See papers on P. parva eradication in England for piscicide based costs (Britton et al, 2008).

See the case of a fishery in North London that removed A. melas as a cost of approx. £5000.00 (€6356.00). £10,000.00, including manpower costs (APHA, personal comm., 2015).

The eradication of two invasive species (Cyprinus carpio and Gambusia affinis) in an endoreic lagoon (37 Ha) in south of Spain cost about 300.000 € (Fernández-Delgado, comm. pers. 2017).

2.14. How great are the economic costs associated with managing this organism likely to be in the future in Europe?

High Moderate The management of these species will have great economic costs. (See papers on P. parva eradication in England for piscicide based costs (Britton et al, 2008) and Ameiurus melas in North England (APHA, personal comm. 2015). The operation to remove the

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catfish costed approx. £5000.00 (€6356.00) £10,000.00, including manpower costs (APHA, personal comm., 2015).

2.15. How important is environmental harm caused by the organism within its existing geographic range excluding Europe?

Unknown The loss of native species that it produced, supposes an important effect on the function of ecosystems. It affects the quality of the water, increasing the levels of chlorophyll and turbidity and the concentrations of nitrogen and phosphorus (Naspleda et al., 2012).

Lake Biwa catch for native species has dropped from more than 8000 tons in 1972 to 2174 tons in 2000 while experts estimate catch of exotic species (black bass and bluegill) exceeds 3000 tons (Chiba et al., 1989) after the introduction of L. macrochirus.

Attempts to introduce L. cyanellus in tropical Africa have been largely unsuccessful; where it has established itself, occupying smallish, well-vegetated dams and becoming over-populated, it is regarded a pest, according to Jackson (1976).

Many authors mentioned the environmental harm that some Lepomis species brought about regarding the loss of biodiversity in USA. For instance:

L. cyanellus is sometimes deliberately stocked for sport fishing, but its high reproductive potential and tolerance for crowding lead to stunted populations which are unattractive to anglers. Olden and Poff (2005), in a study of long-term trends (> 160 years) of fish species distributions in the Lower Colorado River Basin, to identify those native species exhibiting the greatest rates of decline and those non-native species exhibiting the highest rates of spread, found that the

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green sunfish was amongst the fastest expanding invaders in the basin and the most invasive in terms of negative impacts on native fish communities.

Lepomis macrochirus is commonly considered a pest in its introduced range and several countries report it causing negative ecological effects ((Myers et al., 2016; Froese and Pauly, 2016). L. macrochirus overcrowd and stunt the growth of other fish and may even be responsible for causing extinctions, such as the extinction of a native fish in Panama. It predates on crustaceans and insects, and as a population may consume six times its own weight during a single summer (Gerking, 1962). It competes for food and habitat with native sunfish (Maine's red-breast (Lepomis auritus) and pumpkin seed (Lepomis gibbosus) and preys on native minnow (blacknose dace (Rhinichthys atratulus) (USGS, 2012). It has caused displacement of the native species in Mexico (FAO, 1997) and eliminated native Astyanax kompi (Welcomme, 1988). In Japan it feeds on the young of some native fishes, threatening the survival of several species such as the honmoroko (Gnathopogon caerulescens) and the IUCN red listed tanago (Acheilognathus melanogaster) (Chiba et al., 1989). In California, aggressive bluegill outcompete native Sacramento perch (Archoplites interruptus) (Moyle et al., 1974).

In conclusion there is an important impact due to Lepomis spp. in the ecosystems indicated by many authors i.e. van Kleef et al, (2008), Dill and Cordone (1997), Rosen et al. (1995), Casal (2006), Kawamura et al. (2006), added to the high costs of its eradication.

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2.16. How important is the impact of the organism on biodiversity (e.g. decline in native species, changes in native species communities, hybridisation) currently in Europe (include any past impact in your response)?

Major high Lepomis species are likely to affect ecosystems mainly by predation (amphibians, smaller fish species, damselflies, etc.) and competition for food and as a predator of fish breeding and adults (Wiesner et al. 2010). Especially ecosystems, lacking comparable native predatory fish species prior to the establishment of such an exotic centrarchid, are susceptible to significant ecological impact.

Some of the negative impacts are: decline in native species, changes in communities (vegetation, water quality, macroinvertebrate populations etc.), supplantion of many native species in the areas where introduced. In some Italian oligotrophic lakes the redbreast sunfish Lepomis auritus has supplanted the native bleak Alburnus alburnus (Elvira, 2001).

As described by many authors Lepomis species have a major impact on biodiversity in Europe (Elvira, 1997, 2001; Holčík, 1991, Clavero, 2004, Almeida et al. 2013, Van Kleef et al, 2008)..

Introduction of L. gibbosus into Iberia saw aggression on native lotic species (Almeida et al. 2013), Van Kleef et al. (2008) demonstrated impacts on macroinvertebrate fauna in waterbodies in the Netherlands, albeit in a highly modified environment, (as shown in question 8, Section A).

The main response of the recipient species to aggression from all sizes of L. gibbosus was retreat, specifically with no return (i.e. the strongest behavioural impact of the aggression) when aggressors were medium or large pumpkinseed. These results highlight the true potential for adverse impact of L. gibbosus through behavioural interference, resulting in

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the physical displacement of native species from essential resources (e.g. food or habitat), with the subsequent expenditure of energy to avoid the aggressor. In relation to recipient species, the results of the study carried out by the authors (Almeida et al., 2014) showed that L. gibbosus, particularly medium and large sizes, can display aggression on a wide range of taxonomic groups with different ecological requirements, including species at the stream margins (mosquitofish, frog), in the water column (calandino, chub) or on the river bed (crayfish, loach). Previous studies have also shown impacts of pumpkinseed on a variety of functional groups, including zooplankton (Angeler DG et al 2002), macrobenthos (Van Kleef et al 2008), crayfishes (Bramard et al 2006), fishes (Declerck et al 2006) and amphibians (Hartel et al 2007).

2.17. How important is the impact of the organism on biodiversity likely to be in the future in Europe?

major medium Some of the species of this genus are already established in Europe and it is difficult to apreciate its future impact, especially in rivers and lotic ecosystems where the impact could increase.

The prevention of entries and further spread are the only measures to avoid future impact. The major components of such prevention are banning potential invasive species from trade and educating the public about when such centrarchids are actually obtained for e.g. aquaria, garden ponds or fish ponds (Soes et al, 2011).

2.18. How important is alteration of ecosystem function (e.g. habitat change, nutrient cycling, trophic interactions), including losses to ecosystem services,

major high The loss of native species that it produced, supposes an important effect on the function of ecosystems. It affects the quality of the water, increasing the levels of

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caused by the organism currently in Europe (include any past impact in your response)?

chlorophyll and turbidity and the concentrations of nitrogen and phosphorus. This suggests that the introduction of this species in wetlands can be a threat to the functioning of ecological processes that occur within these wetlands (Naspleda et al., 2012).

L. gibbosus has been shown to enhance water turbidity and concentrations of phosphorus and nitrogen (An-geler et al., 2002). As these substances are important nutrients for plant growth, increased concentrations can lead to shifts in plant species composition and changes in ecosystem functioning.

During a pilot study in the moorland pool “Zwart wa-ter” in Flanders (Unpublished data H. van Kleef) demonstrated that nesting activity resulted in the desta-bilizing of Littorella uniflora plants, an endangered species in the Netherlands (Soes et al., 2011).

2.19. How important is alteration of ecosystem function (e.g. habitat change, nutrient cycling, trophic interactions), including losses to ecosystem services, caused by the organism likely to be in Europe in the future?

major medium Increased negative effects on ecosystem functions is likely, with climate change scenarios facilitating Lepomis spp survival and growth. Trophic cascades (via increased numbers of the predatory Lepomis spp), dietary shifts of native species and increased competition is likely.

2.20. How important is decline in conservation status (e.g. sites of nature conservation value, WFD classification) caused by the organism currently in Europe?

major high The Lepomis species are found in areas of high value for the conservation of nature, so the loss of biodiversity supposes a high decline in the conservation status of these areas. Depredation of macro-invertebrates and predation of native species could contribute to the decline in conservation status of a waterbody.

2.21. How important is decline in conservation status (e.g. sites of nature conservation value, WFD classification)

major high Likelihood of declines in conservation status is increased in the future due to the trophic interactions

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caused by the organism likely to be in the future in Europe?

and ecosystems alteration caused by these species.

2.22. How important is it that genetic traits of the organism could be carried to other species, modifying their genetic nature and making their economic, environmental or social effects more serious?

minimal medium There is no evidence of possibility of hybridisation with native species but hybridisation within species of the same family ocurre, making its impact more serious and more difficult to distinguish between species (Misra and Holdsworth. 1972)

2.23. How important is social, human health or other harm (not directly included in economic and environmental categories) caused by the organism within its existing geographic range?

minimal medium Within recreational fisheries Lepomis populations may lead to a decrease in participation by anglers, as they are seen as a pest species.

In addition to the ecological impact of naturalized fishes outlined above, some species have also on occasion been of socio-economic significance. This is especially so when a naturalized species not favoured for human consumption replaces a popular food species. This phenomenon commonly occurs in not developed countries and is still rare in Europe (Elvira, 2001).

2.24. How important is the impact of the organism as food, a host, a symbiont or a vector for other damaging organisms (e.g. diseases)?

moderate low There is evidence of alien parasites, which could have an impact on native species (Wiesner et al., 2010), Hockley et al. (2011) detected a non-native parasite on introduced L. gibbosus, which was not found on native species within the waterbody.

2.25. How important might other impacts not already covered by previous questions be resulting from introduction of the organism? (specify in the comment box)

NA

2.26. How important are the expected impacts of the organism despite any natural control by other organisms, such as predators, parasites or pathogens that may already be present in Europe?

Moderate medium Despite of any predators, parasites and pathogens present in Europe, L. gibossus had a very successful evolution in most part of Europe as described previously.

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As demonstrated by Soes et al. (2011) at least L. auritus, L. cyanellus, L. macrochirus, L. megalotis and L. peltastes could have the same success in Europe.

The Largemouth (Micropterus salmoides) is an important predator of the species, but also of native species in Europe, so it should not be used for that purpose. Native species within the introduced range of Lepomis spp could be used to control populations (c.f. Davies and Britton, 2015) and reduce impacts.

2.27. Indicate any parts of Europe where economic, environmental and social impacts are particularly likely to occur (provide as much detail as possible).

[In all its distribution area]

medium Environmental impacts in all its distribution area where it is established.

In addition to the ecological impact of naturalized fishes outlined above, some species have also on occa-sion been of socio-economic significance. This is espe-cially so when a naturalized species not favoured for human consumption replaces a popular food species. This phenomenon commonly occurs in not developed countries and is still rare in Europe (2001).

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RISK SUMMARIES

RESPONSE CONFIDENCE COMMENTSummarise Entry likely high At least four species of the genus Lepomis are already

present in Europe: .L. gibbosus, L. auritus, L. cyanellus and L. megalotis,

New entries are possible if not taking preventive measures. It is necessary to prevent through banning of potential invasive species from trade and educating the public about its impact.

Summarise Establishment very likely high Lepomis auritus Germany, Italy (Elvira, 2001)

Lepomis gibbosus is now established in at least 28 countries of Europe and Asia minor (Copp and Fox, 2007). Only in Europe it is established in 23, possibly 24 countries. These are: Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, France, Germany, Greece, Hungary, Italy, Latvia, Luxembourg, Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain and UK (CABI, 2011), Lithuania and possibly Estonia (Elvira, 2001). The species is established almost exclusively in lacustrine ecosystems in northern Europe. Whereas in southern latitudes, in particular in Iberia, L. gibbosus populations establish easily in regulated rivers and reservoirs.

Summarise Spread rapidly medium The expansion depends on ecological conditions of river basins in which it is introduced, but if it finds good conditions it can be easier. Once established in closed waters is easy its natural expansion. Verbrugge et al.

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(2012) classified it as a high risk invasive species. The progressive warming of water in ponds and rivers, facilitates the expansion of the species and changes in precipitation amount and intensity could lead to the further dispersal. (Fobert et al. 2013)

Summarise Impact high high Loss of biodiversity or impacts on native species and threats to ecosystem function occurred and is expected to grow.

Conclusion of the risk assessment high high The further dispersal (via natural and/ or anthropogenic means) is likely. Coupled with the plasticity of Lepomis species life-history traits and environmental tolerances, increased impacts on ecosystem function and native biota is expected. The effect of climate change will encourage their further expansion.

The effects of introducing species in an area other than their origin are generally unpredictable, and although not always invasive, precautionary measures are required. And its entry, voluntary or involuntary, has had transcendental, sometimes disastrous, consequences throughout history.

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ADDITIONAL QUESTIONS - CLIMATE CHANGE3.1. What aspects of climate change, if any, are most likely to affect the risk assessment for this organism?

[Climate directly]

High Verbrugge et al. (2012) indicate in the comparison of risk classifications for 25 aquatic non-native species using various European risk identification protocols a high risk for this species. The progressive warming of water in ponds and rivers, facilitates the expansion of the species.

The further dispersal of Lepomis spp. is likely, due to increased water temperatures facilitating Y-O-Y survival and growth. Changes in precipitation amount and frequency could also contribute to elevated water-levels and facilitate dispersal into lotic environments. Additionally, increases in water temperatures, particularly in lentic environment, is likely to facilitate successful reproduction and increase invasive potential.

Whilst not currently considered to be invasive at more northerly latitudes, including the U.K., L. gibbosus is predicted to become invasive under conditions of cli-mate warming (Britton et al., 2010); this is expected to result in earlier reproduction (Zieba et al., 2010), en-hanced recruitment (Zieba et al., 2015) and subsequent greater dispersal (Fobert et al. 2013). These traits are then anticipated to result in adverse impacts on native species and ecosystems (e.g. Angeler et al., 2002; Van Kleef et al., 2008).

3.2. What is the likely timeframe for such changes? 20 years low Aquatic environments are particularly affected by climate change.

3.3. What aspects of the risk assessment are most likely to change as a result of climate change?

[Increase suitability of the habitat for the species].

medium Increased water temperatures as a result of climate change will extend the reproductive season of Lepomis species and likelihood of progeny survival. Larger body sizes and increased growth rates may also lead to a

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greater impact on native fauna (Eaton, 1996)

ADDITIONAL QUESTIONS - RESEARCH4.1. If there is any research that would significantly strengthen confidence in the risk assessment please summarise this here.

The impact to native fauna should be further investigated]

medium Confidence in the risk assessment is high for establishment and furtherspread of L. gibbosus. Further research on the impact of Lepomis specieswithin different countries and environments (lentic and lotic) of their invaded range would be beneficial. Dietary analysis would reveal the degree of competition with native fish species and likelihood of native species displacement/ depredation by Lepomis. Additionally, species-specific control measures should be identified, where possible and mechanisms of Lepomis species control/ extirpation investigated.

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