Volume 10, Issue 4 (2015)
published October 2015
Contents | |
Research articles |
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Ana L. Nunes, Elena Tricarico, Vadim E. Panov, Ana C. Cardoso and Stelios Katsanevakis
Pathways and gateways of freshwater invasions in Europe
(pp 359-370)
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Taking into account the continuous increase in freshwater introductions, and to support the recent European legislation on invasive alien species,
the identification of priority pathways and gateways of introductions is of utmost importance to develop adequate control strategies. The aim of
this paper was to analyse the main pathways and gateways of introductions of freshwater alien species in Europe. Based on a thorough review
of the scientific and grey literature, information on pathways, country and year of initial introduction of all freshwater alien species in Europe,
was retrieved. The spatial and temporal patterns and trends of biological invasions in freshwater ecosystems in Europe, in relation to different
pathways, were assessed. Our results pinpoint the major importance of aquaculture, pet/aquarium trade and stocking activities as pathways
of introduction of freshwater alien species in Europe. For species native to some European countries, shipping and inland canals were
the most important pathways, highly responsible for the entry of many harmful species. Germany, the United Kingdom and Italy were the main
entry gateways of freshwater alien species in Europe. We found a geographical pattern related to some pathways of introduction in Europe:
introductions through inland canals were concentrated in Central/North-eastern Europe, while introductions through pet/terrarium/aquarium
trade were mainly observed in Central/Western Europe. While Chordata species entered Europe mainly through the three major above mentioned
pathways, many harmful Arthropoda and Mollusca entered through shipping and inland canals. The information gathered in this study clearly
indicates the entry routes that should be prioritised by Member States, for which stronger control and management actions should
be implemented and prevention efforts concentrated under the scope of the related new EU Regulation.
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Joanna James, Jo Cable, Graham Richardson, Kate E. Davidson and Andrew S.Y. Mackie
Two alien species of Branchiobdellida (Annelida: Clitellata) new to the British Isles: a morphological and molecular study
(pp 371-383)
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Freshwater ecosystems are particularly vulnerable to the effects of alien species and decapod crustaceans, notably crayfish,
are a principal threat. Although symbiotic fauna may influence the impact and dispersal of introduced species, this is often overlooked.
Here we provide the first record of non-native ecto-symbiotic branchiobdellidan worms on invasive signal crayfish (Pacifastacus leniusculus Dana, 1852)
in the British Isles. Using morphological and molecular techniques we identified and re-described two branchiobdellidan species new to the UK,
Xironogiton victoriensis Gelder and Hall, 1990 and Cambarincola aff. okadai Yamaguchi, 1933, both of which were found at a single
location in the Gavenny River, South Wales. The prevalence of X. victoriensis and C. aff. okadai was 75.34% and 71.23% respectively.
Although the level of X. victoriensis and C. aff. okadai co-infection was high at 75.41% of all infected animals, the two species exhibited
different micro-habitat preferences on the host with the former being found predominantly on the chelae and walking legs and the latter on the carapace and abdomen.
For both branchiobdellidan species, worm burdens were positively correlated with crayfish size. The lack of branchiobdellidan records from signal crayfish in nearby
water bodies, and the reports of native white clawed crayfish (Austropotamobius pallipes) in the Gavenny as recently as 2000, indicates that introduction
of this worm infested population occurred relatively recently, despite stringent legislation banning the import and transportation of non-native crayfish into the UK.
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Claudia Hellmann, Susanne Worischka, Eva Mehler, Jochen Becker, René Gergs and Carola Winkelmann
The trophic function of Dikerogammarus villosus (Sowinsky, 1894) in invaded rivers: a case study in the Elbe and Rhine
(pp 385-397)
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The invasive amphipod Dikerogammarus villosus has become increasingly dominant in German river ecosystems since the River Rhine
invasion in the mid-1990s. Because it is preying on other invertebrate taxa, its appearance is often assumed to be associated with
a drastic decrease in species diversity and changes in natural benthic communities. Despite this, the trophic function of D. villosus
and its predation potential are rarely studied in natural river communities. Here, we assess the trophic function of D. villosus
in two invaded systems, the Elbe River and the River Rhine, using stable carbon and nitrogen isotope analyses. In the two studied river
food webs, D. villosus had a generally low trophic position (TP), indicating a likely function as primary consumer or at most
as an omnivore. The significantly higher TP in the River Rhine (TP = 2.6) than in the Elbe River (TP = 1.9) suggested a partial use
of animal prey in the River Rhine. This was supported by the results of the isotope mixing model SIAR which predicted in addition
to a high importance of herbivory in both rivers a likely feeding on other invasive amphipod species in the Rhine community.
We conclude that D. villosus has a variable but mostly low predacious behaviour, probably depending on the benthic community structure.
To allow more realistic trophic analyses for D. villosus in the field, we determined the trophic enrichment factors (TEFs) for nitrogen
and carbon isotopes of two diet types in the tissue of D. villosus in an eight-week laboratory experiment. The carbon isotope enrichment
(13C) from the chironomid diet was negative in the consumer (-1.75 ‰), whereas the carbon from leaf litter was enriched positively in the tissue
(3.27 ‰). The TEFs for nitrogen (15N) were more similar for plant and animal diet (leaf litter: 3.56 ‰, chironomids: 2.29 ‰). Because of the high
specificity of the enrichment factors with respect to species and food source, we recommend their use in further trophic analyses.
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Katri Aarnio, Anna Törnroos, Charlotta Björklund and Erik Bonsdorff
Food web positioning of a recent coloniser: the North American Harris mud crab Rhithropanopeus harrisii (Gould, 1841) in the northern Baltic Sea
(pp 399-413)
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Identifying resource use and functional traits of non-indigenous species are promising means to increase the ability to predict ecological consequences of invasions.
One of the most widely spread brachyuran crab species, and a recent invader in the northern Baltic Sea, is the North American Harris mud crab, Rhithropanopeus harrisii
(Gould, 1841). Although spread, establishment, and population structure have been studied for this species, little is known about its role and impact in a new environment.
We investigated the position and role of R. harrisii in the coastal food web by combining spatial and temporal estimates of trophic position using stable isotopes
(δ13C and δ15N), with short-term food- and habitat-choice experiments. We observed a stable pattern in the trophic position between two environmentally different locations
in the Archipelago Sea over the production season. The identification of a natural breakpoint in carbon stable isotopes at the size of 12 mm carapace width suggested
a presence of an ontogenetic diet shift, which was confirmed by isotope signatures positioning large R. harrisii among secondary consumers and small individuals
with primary consumers. The generalist consumer nature of R. harrisii and preference for structured habitat was supported by an active habitat and food choice,
revealing no preference for prey species (polychaetes versus amphipod), but selection of brown algae over bare mud. To broaden the understanding of the functional role
of R. harrisii, we combined our findings with other known biological and ecological traits of the species and qualitatively compared these to characteristics
of other benthic organisms in the northern Baltic Sea, suggesting a general similarity in traits.
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Stella Redón, Andy J. Green, Boyko B. Georgiev, Gergana P. Vasileva and Francisco Amat
Influence of developmental stage and sex on infection of the American brine shrimp Artemia franciscana Kellogg, 1906 by avian cestodes in Ebro Delta salterns, Spain
(pp 415-423)
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The American brine shrimp Artemia franciscana Kellogg, 1906 is invasive in the Mediterranean region where it has displaced native populations
of sexual A. salina and clonal A. parthenogenetica from many hypersaline wetlands. Brine shrimps are intermediate hosts of several
cyclophyllidean avian cestodes, whose effects have been studied in native Artemia. However, determinants of these infections in the alien
invader remain unknown. We present the most detailed study to date of parasitism of A. franciscana by cestodes in its invasive range,
conducted in the Ebro Delta salterns (NE Spain) over a 33 month period, when a total of 9,293 A. franciscana adults and 8,902 juveniles
were studied. We examined for first time whether host age and sex influence infection rates. Ten cestode species were recorded, with a total
prevalence of 11.1% in adults and 2.7% in juveniles. The most abundant cestodes were Eurycestus avoceti (in adults) and
Flamingolepis flamingo (in juveniles). Prevalence, abundance and intensity of infection were significantly higher in adults for four cestode
species (Flamingolepis liguloides, Wardium stellorae, E. avoceti and Anomotaenia microphallos), and significantly higher in juveniles
for F. flamingo. Mean cestode species richness was four times higher in adults. One cestode species (F. liguloides), was significantly
more abundant in adult females than in adult males. Host age influences infection patterns which seem to be strongly related to the feeding behaviour
of avian final hosts (filtering versus picking), suggesting complex ecological interactions among predators, prey and their parasites, with important
implications for native biodiversity and ecosystem stability.
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Samuel P. Iglésias and Lou Frotté
Alien marine fishes in Cyprus: update and new records
(pp 425-438)
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The Mediterranean Sea, due to its connection to the Red Sea via the Suez Canal, its heavy maritime traffic, and the effects of climate change
is a hotspot of invasion by alien species. A survey carried out around Cyprus during September 2014 documented the occurrence of 25 alien fishes.
Seven Lessepsian migrants (Hippocampus fuscus Rüppell, 1838, Nemipterus randalli Russell, 1986, Ostorhinchus fasciatus (Shaw, 1790),
Parupeneus forsskali (Fourmanoir & Guézé, 1976), Pomadasys stridens (Forsskål, 1775), Sphyraena obtusata Cuvier, 1829 and
Spratelloides delicatulus (Bennett, 1832)) were recorded for the first time, increasing to 35 the number of alien fishes recorded around the island.
Four of these first records can be considered as 'established', whereas the 2013 first record of Pterois volitans/miles is confirmed by new
findings placing the species as newly 'established' in Cyprus. All the recorded alien fishes of Cyprus are Lessepsian migrants, 80% of which can be
considered established and four of them are invasive. The rapid increase of alien fish species over time in Cyprus supports the accelerating
tropicalisation process observed elsewhere in the Mediterranean over the last decades. Furthermore, the new finding of the tropical Atlantic
immigrant Enchelycore anatina (Lowe, 1839) is documented.
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Marco Milardi, Mattia Lanzoni, Mikko Kiljunen, Jyrki Torniainen and Giuseppe Castaldelli
Natural recruitment contributes to high densities of grass carp Ctenopharyngodon idella (Valenciennes, 1844) in Western Europe
(pp 439-448)
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Introductions of grass carp, well known for their potentially negative ecosystem effects, have been performed in several countries around the world.
As the species was considered unable to reproduce naturally under non-native environmental conditions, little attention was initially given to its
invasive potential. We studied an area in northern-Italy where, contrary to expectations, introductions that were performed in the early 80s still
exert a considerable pressure on aquatic macrophytes. In order to reveal whether the observed population dynamics are the result of natural events
or stocking we analysed the density, age- and size-structure of the grass carp population and the migration pathways available to it. Telephone
surveys were also used to check for fish transport from national and international suppliers. We also sampled potential spawning and nursery areas
for young individuals and, when some were captured, we applied stable isotope analyses to discriminate their origin. We found that the population
of large individuals likely originated solely from early stocking. We also documented the first analytical evidence of grass carp recruitment
in the study area and, to our knowledge, in Western Europe. Therefore the species has the potential to become invasive in these areas and more
detailed studies are needed to assess this potential. Further management should account at least for natural recruitment and potential negative
environmental effects, controlling the species where needed.
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Allison W. Lenaerts, Alison A. Coulter, Zachary S. Feiner and Reuben R. Goforth
Egg size variability in an establishing population of invasive silver carp Hypophthalmichthys molitrix (Valenciennes, 1844)
(pp 449-461)
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Reproductive investment (e.g., egg size) is generally critical for the successful establishment of invasive species, with high variability
often positively influencing success. Silver carp Hypophthalmichthys molitrix (Valenciennes, 1844) are highly successful invasive fish
on a global scale and threaten biodiversity in a wide range of freshwater habitats. However, factors influencing egg size variability in silver carp
are not fully understood. We collected drifting silver carp eggs from the Wabash River, Indiana (USA) throughout the 2012 and 2013 spawning seasons
to examine egg diameter variation was related to environmental factors and across time. The Wabash River is largely unregulated with few backwater habitats,
and the resident silver carp population is relatively new. As a result, the Wabash River offers the opportunity to observe an expanding silver carp population
in a river with a comparatively “natural” flow regime. Egg size was positively correlated with both embryo total length and yolk sac volume, indicating larger
silver carp eggs contain larger, better-provisioned embryos at a given developmental stage. Eggs collected in 2013 were significantly larger than those collected
in 2012 despite a decline in mean length of mature females. Relationships between egg diameter and environmental factors appear complex, with relationships varying
between years. Silver carp eggs displayed high variability in diameter, with a mean coefficient of variation of 9.5%. This high variation may reflect a diverse
population of spawning females, but it may also constitute a reproductive strategy to facilitate egg transport across habitats and potentially reduce intraspecific
competition. Such reproductive plasticity in silver carp and other invasive species is likely to be key for achieving reproductive success in newly invaded ecosystems
despite the species’ naivety with novel and unpredictable environmental conditions therein.
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Melanie M. Perello, Thomas P. Simon, Hilary A. Thompson and Douglas D. Kane
Feeding ecology of the invasive round goby, Neogobius melanostomus (Pallas, 1814), based on laboratory size preference and field diet in different habitats in the western basin of Lake Erie
(pp 463-474)
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The round goby, Neogobius melanostomus, is an invasive benthic fish species in the Laurentian Great Lakes that is threatening native fish
populations through competition, predation, and trophic dynamic change. This study examined the trophic dynamic plasticity of round goby along
a depth gradient based on laboratory and field observations to determine prey species consumed and mussel prey size selection. Prey size selection
in the laboratory was assessed by presenting individual round goby with quagga mussels (Dreissena rostriformis bugensis) of various class sizes
(i.e., 6.0–9.9 mm, 10.0–12.9 mm, 13.0–15.9 mm, and 16.0–18.9 mm in length). Round goby exhibited a selection preference for small sized quagga mussels,
although in individual trial events, mussels were consumed from all four size classes. Prey species consumed from shallow and deep sites in the western
basin of Lake Erie were assessed using individual gut contents to calculate measures of prey importance, diversity, and dominance. Based on the Index
of Relative Importance (IRI), Cladocera was found to be the most consumed prey item for both males and females and between study sites. Both sexes consumed
a variety of prey items although females exhibited greater prey dominance or reliance on one prey item. Round goby individuals at the shallow, natural shoreline
site had the highest trophic diversity, while individuals at the deep site exhibited the highest prey dominance. Diet of round goby in the western basin
of Lake Erie are mainly dominated by just a few prey items.
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Olatz San Sebastián, Eudald Pujol-Buxó, Núria Garriga, Álex Richter-Boix and Gustavo A. Llorente
Differential trophic traits between invasive and native anuran tadpoles
(pp 475-484)
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How trophic resources are managed is a key factor in our understanding of the success of invasive species.
In amphibians that usually occupy ephemeral ponds, the capacity to acquire resources and food selection
are especially important because as a pond dries, the larval density increases and food resources are limited.
Abundant and high-quality food can increase the final size and reduce the duration of development of amphibians.
The aim of this work was to assess the trophic traits of tadpoles of the invasive (originally North African) anuran
Discoglossus pictus compared to those of native European Epidalea calamita tadpoles under laboratory
conditions. Food of two different levels of quality was supplied, and the feeding activity and food preference
of the two species were analysed alone and in co-occurrence. D. pictus was capable of modifying its behaviour
and food preferences; while E. calamita displayed much milder differences between treatments. Both alone and
in co-occurrence with the native species, the invasive tadpoles obtained higher feeding activity values and showed
a stronger preference for high-quality food. Additionally, when high densities of the two species shared food resources,
the feeding activity results indicated potential displacement of the native tadpoles to low-quality resources.
D. pictus thus presents trophic traits that are favourable for invasion and could limit the fitness of
E. calamita when resources are limited or there is a risk of pond desiccation.
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