Volume 11, Issue 4 (2016)
published October 2016
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Letter to the Editor |
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Bella S. Galil, Jacob Douek, Henk K. Mienis and Baruch Rinkevich
Comments on “The Mediterranean Sea as a gateway for invasion of the Red Sea: the case of the Indo-West Pacific head-shield slug
Chelidonura fulvipunctata Baba, 1938” by Manuel António E. Malaquias, Andrea Zamora-Silva, Dyana Vitale, Andrea Spinelli,
Sergio De Matteo, Salvatore Giacobbe, Deneb Ortigosa and Juan L. Cervera, Aquatic Invasions, 2016
(pp 351-354)
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In a recent article, Malaquias et al. (2016) use molecular tools to test the conspecificity of the aglajid sea slug
Chelidonura fulvipunctata Baba, 1938 populations from two sites in the Mediterranean (Cyprus, Italy) and
the Indo-West Pacific (Mozambique, Lizard Island, Australia, and Marshall Islands). The authors then postulate
that the species has entered the Red Sea from the Mediterranean Sea through the Suez Canal, the latter acting
as a “revolving door” that can allow species of Indo-Pacific origin to enter the Mediterranean, and species established
in the Mediterranean to move into the Red Sea. In this response evidence is offered that questions, if not refutes, the authors’ premises.
The veracity and accuracy of the geographic origin and the pathways of introduction are of major importance for management of bioinvasions.
For appropriate management measures to be prioritized, devised, and implemented, care should be taken to provide scientists, regulators
and stakeholders with as accurate information as possible.
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Research articles |
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Rubén Ladrera, Joan Gomà and Narcís Prat
Regional distribution and temporal changes in density and biomass of Didymosphenia geminata in two Mediterranean river basins
(pp 355-367)
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This study aimed to strengthen the knowledge of Didymosphenia geminata distribution in Spain, and to determine which environmental
variables were related to its regional distribution and temporal changes in growth and production in two Ebro River tributary basins
(Iregua and Najerilla¸ La Rioja Region). Living cells of D. geminata were present in 40% of the studied sites of both basins but only
four of the sites developed massive growths. The diatom is widely distributed only in mountain areas of both basins (above 690 masl), which
have low average annual air temperature (8.27 ± 0.28 ºC) and low water Soluble Reactive Phosphorus (SRP) concentration (average value 0.024 ± 0.007 ppm).
Massive growths occur in sites with high light intensity, hydrological regulation of river flow and the lowest measured SRP concentrations
(below 0.018 ppm SRP). We carried out an intensive spatio-temporal survey in the Lumbreras River (Iregua basin), where the first massive growth
was detected in La Rioja Region. The highest cell densities (1.6 × 105 cells cm−2) and biomass values (480 gDWm−2) were recorded
in late summer. An increase in solar radiation and slight rise in water temperature were associated with an increase in biomass over time, but always in waters
with low SRP concentration, the key factor that enhances massive growth development. The alteration of the natural streamflow in the Lumbreras River
by the Pajares Reservoir and the fact that water is discharged from the hypolimnion (which decreases the summer river water temperature) are important
factors in understanding why D. geminata shows such an increase in biomass in a Mediterranean river. This paper provides new insights into
the importance of different factors controlling D. geminata massive proliferations in the Mediterranean climate zone, where it is assumed
that the species should not develop such massive growths, compared to temperate zones where the majority of previous studies have been carried out.
We suggest that changing the reservoir management strategy would be a very important contribution to the control of such significant developments.
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Matthew D. Gunderson, Kevin L. Kapuscinski, Derek P. Crane and John M. Farrell
Habitats colonized by non-native flowering rush Butomus umbellatus (Linnaeus, 1753) in the Niagara River, USA
(pp 369-380)
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During the summer of 2012, we first observed non-native flowering rush Butomus umbellatus (Linnaeus, 1753) in the upper Niagara River, NY, USA,
where this species had previously been undocumented. In a 2013 study, Butomus was present at 33 of 161 (20%) submersed nearshore (≤ 3 m) sites
surveyed.
It was the species of greatest biomass at 27% of the sites where it was collected, and was observed growing at depths > 3 m. Butomus was
disproportionately prevalent in the upper observed ranges of water depth and velocity. Butomus was also closely associated with coarse substrates,
differing from canopy-forming species but not other linear-leaved species. Emergence of Butomus from the sediment generally occurred from late-May
to early-June, with peak coverage and height occurring in mid- to late-July. Coverage was generally minimal by mid-September. Rhizome bulbil
production occurred on specimens as small as 25 cm in length and was first observed in mid-August when water temperatures were about 22.5°C.
Although we did not investigate the ploidy status of Butomus in the Niagara River, the presence of these vegetative reproductive structures
is consistent with reports of genetically diploid Butomus populations in North America. No linear correlations between the biomasses of
Butomus and other species were detected, although the data suggest a possible limiting effect on the biomasses of other species in dense
Butomus stands. Even if emergent Butomus was eradicated from shorelines and wetlands, submersed areas would likely act as a refuge
from which Butomus could continue to distribute viable bulbils and rhizome fragments into the nearshore. Submersed Butomus
is a potential ecosystem engineer because it can colonize barren areas with coarse substrates, reach high densities, and grow to a considerable
height in the water column. Subsequently, deposition and retention of fine sediments may occur, potentially allowing other species to expand
into previously unsuitable areas.
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Ana A. Anđelković, Milica M. Živković, Dušanka Lj. Cvijanović, Maja Z. Novković, Dragana P. Marisavljević, Danijela M. Pavlović and Snežana B. Radulović
The contemporary records of aquatic plants invasion through the Danubian floodplain corridor in Serbia
(pp 381-395)
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Aquatic ecosystems are particularly vulnerable to introductions of non-indigenous species, which potentially lead to major disruptions
in the functioning of these invaluable habitats. Despite the significance of aquatic systems, there is no collated data available
on the aquatic non-native plants in Serbia. Consequently, the aim of this paper is to provide a first overview of the aquatic alien plant
species recorded in Serbia, their origins, current distribution, habitat preferences and invasiveness status. This study comprises
the results of a comprehensive literature review and extensive field research on lake and river systems over a nine year period (2007–2015),
with the addition of data from the IASV database and Joint Danube Surveys 2 & 3. The results of this study show the presence of seven
non-indigenous aquatic plant species in Serbia which, despite being a relatively low number when compared to France and Germany, is in line
with most of the countries of the region (e.g. Croatia, Bulgaria and FYR Macedonia). The majority of the species are native to the Americas,
which concurs with the results of previous studies at the European level, with only one species of Asian origin. The most abundant
of the registered non-natives is Vallisneria spiralis, followed by Azolla filiculoides and Elodea nuttallii, while
Cabomba caroliniana, as the newest registered aquatic alien in Serbia, has the least number of records. All of the registered
non-natives predominantly occur in running waters, including as much as 91% of the records for Elodea canadensis and 85% for
Elodea nuttalli. Vallisneria spiralis is present in five different EUNIS habitat types, while Paspalum distichum
was recorded predominantly along the River Danube, thereby highlighting it as P. distichum's main corridor of spread in Serbia.
The distribution of all the recorded non-indigenous species is primarily linked to the northern, low-lying part of Serbia—i.e. Vojvodina Province.
Such a distribution pattern is concordant with the presence of adequate habitat types, the courses of potential international invasion corridors
in the Sava and Danube rivers and the position of the elaborate irrigation canal network of the Danube-Tisa-Danube Hydrosystem;
but also with the frequency of studies carried out in this region over the years. Of the seven aquatic aliens present in Serbian waterbodies,
three are considered to be highly invasive and one potentially invasive, while two have also been included in the list of 150 most widespread
alien species in Europe.
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Antoine Nowaczyk, Valérie David, Mario Lepage, Anne Goarant, Éric De Oliveira and Benoit Sautour
Spatial and temporal patterns of occurrence of three alien hydromedusae, Blackfordia virginica (Mayer, 1910),
Nemopsis bachei (Agassiz, 1849) and Maeotias marginata (Modeer, 1791), in the Gironde Estuary (France)
(pp 397-409)
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The species composition and seasonal abundance patterns of gelatinous zooplankton are poorly known for many European coastal-zone waters.
The seasonal abundance and distribution of the dominant species of hydromedusae along a salinity gradient within the Gironde Estuary,
Atlantic coast of France, were evaluated based on monthly surveys, June 2013 to April 2014. The results confirmed the presence
of three species considered to be introduced in many coastal ecosystems around the world: Nemopsis bachei (Agassiz, 1849),
Blackfordia virginica (Mayer, 1910), and Maeotias marginata (Modeer, 1791). These species were found at salinities
ranging from 0 to 22.9 and temperatures ranging from 14.5 to 26.6 ºC, demonstrating their tolerance to a wide range of estuarine
environmental conditions. There was a clear succession of the three species that was influenced by temperature and salinity.
Blackfordia virginica was the dominant hydromedusae during the warmest months and occurred at very high abundance
(up to 634 individuals.m-3 corresponding to 21.40 g.m-3 as wet weight). The seasonal evolution of the size distribution indicated
an extended period of release of medusae by hydroid polyps, and rapid growth, covering the whole period of occurrence for
B. virginica. Nemopsis bachei also was present during the warmer months but only locally common. In contrast,
Maeotias marginata only occurred in low numbers during autumn and had not been previously detected in the Gironde Estuary.
Non-native jellyfishes clearly represent a prominent component of the Gironde Estuary, and additional work is needed to understand
the potential impacts on the structure and functioning of entire zooplankton community.
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Katherine McFarland, Philippe Soudant, Fred Jean and Aswani K. Volety
Reproductive strategy of the invasive green mussel may result in increased competition with native fauna in the southeastern United States
(pp 411-423)
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Understanding the population dynamics of invasive species, such as the green mussel Perna viridis (Linnaeus, 1758),
can aid in explaining the success of newly introduced populations and help predict the potential for spread. During a two-year
field study of established populations in the invaded region of southwest Florida, year round gametogenesis and continuous spawning
capabilities were observed through histological analysis of mussels collected monthly. This was supported by overall stable energetic
reserves as measured through proximal biochemical composition (protein, glycogen and lipid content). However, egg outputs in the summer
(6.4 × 106 ± 2.6 × 106 eggs / female) were significantly higher than egg outputs of winter-spawned mussels
(7.7 × 104 ± 1.4 × 104 eggs / female). Stability in biochemical composition, suggests temperature and food availability
were sufficient year round, allowing for the maintenance of reserves and active gametogenesis. Protein ranged from 409.0–628.0 mg g−1,
glycogen from 44.3–158.5 mg g−1 and total lipids from 7.4–13.5 mg g−1. Year-round reproductive capabilities supported by sufficient
energy reserves may help explain the rapid colonization and high densities of green mussels along the southeastern United States
and suggests the potential for competition with native species, particularly the eastern oyster Crassostrea virginica.
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Elliot Scanes, Emma L. Johnston, Victoria J. Cole, Wayne A. O’Connor, Laura M. Parker and Pauline M. Ross
Quantifying abundance and distribution of native and invasive oysters in an urbanised estuary
(pp 425-436)
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Human activities have modified the chemical, physical and biological attributes of many of the world’s estuaries. Natural foreshores
have been replaced by artificial habitats and non-indigenous species have been introduced by shipping, aquaculture, and as ornamental pets.
In south east Australia, the native Sydney rock oyster Saccostrea glomerata is threatened by pollution, disease and competition
from the invasive Pacific oyster Crassostrea gigas. This study assessed the abundance (as number m-2), size, and distribution of
both invasive and native oyster species at 32 sites in the heavily urbanised Port Jackson Estuary, Australia. We tested the hypotheses
that there would be: (1) a difference in the proportion of C. gigas greater proportion
of C. gigas on artificial compared to natural substrates; (3) a greater numbers of all oysters, with differing size characteristics,
on artificial compared to natural substrates; and (4) that the abundance and size of all oysters would vary among locations along an environmental
gradient. Environmental variables included distance from the estuary mouth and salinity. We found the abundance and size of all oysters differed
among locations; smaller oysters occurred at greater abundances near the mouth of the estuary. Abundance was also higher on artificial, than on
natural substrate. Habitat type, however, had no effect on which species of oyster was present. In contrast, distance from the estuary mouth
strongly influenced the relative proportion of the two species. The invasive C. gigas comprised 16 % of the oysters sampled, and up
to 85 % at some of the upper estuary sites. As predicted, C. gigas was more abundant at locations in the bay ends and upper channel
of the estuary; it was also larger in size than the native S. glomerata. This is the first assessment of oyster distribution
in Port Jackson and provides a solid base for monitoring changes in the estuarine distribution of a globally invasive pest.
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Joop W.P. Coolen, Wouter Lengkeek, Steven Degraer, Francis Kerckhof, Roger J. Kirkwood and Han J. Lindeboom
Distribution of the invasive Caprella mutica Schurin, 1935 and native Caprella linearis (Linnaeus, 1767) on artificial
hard substrates in the North Sea: separation by habitat
(pp 437-449)
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Studying offshore natural and artificial hard substrates in the southern North Sea (51ºN–57ºN/1ºW–9ºE), the invasive introduced Japanese skeleton
shrimp Caprella mutica Schurin, 1935 was found to co-exist with the native Caprella linearis (Linnaeus, 1767) only on near-shore
locations that had an intertidal zone (e.g., wind farm foundations). In contrast, on far offshore and strictly subtidal locations, such as shipwrecks
and rocky reefs, only C. linearis was found. Based on these exploratory observations, we hypothesised that artificial structures that are only
subtidal are inhabited exclusively by C. linearis, and never by C. mutica. To test this hypothesis and understand factors driving each
species’ habitat preferences, habitat suitability models were constructed using generalised additive models, based on samples collected in 2013–2015
from offshore gas platforms, buoys, shipwrecks, and rocky reefs and combined with data from other published and unpublished surveys (2001–2014).
The models showed that the presence of C. mutica is explained by the availability of intertidal and floating hard substrates, suspended
particulate matter density (SPM), mean annual sea surface temperature, salinity, and current velocity. The C. linearis model included subtidal
hard substrates, SPM, salinity, temperature, and current velocity. The modelled distributions showed a significant difference, demonstrating that
C. linearis’ habitat preference does not fully overlap with that of C. mutica. Thus, the native and alien Caprella species
are likely to be able to co-exist in the North Sea.
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Patricia Hale, James Wilson, Zachary Loughman and Sujan Henkanaththegedara
Potential impacts of invasive crayfish on native crayfish: insights from laboratory experiments
(pp 451-458)
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Despite the extreme diversity of crayfish in the Southeastern United States, many taxa are threatened with extinction due
to invasive counterparts. Invasive crayfish alter invaded habitats causing community and population level impacts due to competition,
predation and transmission of diseases. We experimentally evaluated the potential impacts of invasive red swamp crayfish
(Procambarus clarkii) and virile crayfish (Orconectes virilis) on native Piedmont crayfish (Cambarus sp. C)
using size-matched pairs. We tested 1) species-specific aggressive behavior with aggression assays, and 2) survival in sympatry
with survival analysis. Both invasive crayfish species tended to express higher levels of aggression compared to the native counterpart.
However, we failed to detect any statistically significant differences. During survival experiments, the proportional survival of native
Cambarus sp. C in sympatry with invasive O. virilis was significantly lower than that of invasive O. virilis.
However, we did not find a significant difference in the proportional survival between invasive P. clarkii and native
Cambarus sp. C. These experiments demonstrate inconsistent and limited negative impacts of two invasive crayfish species
on a native species, when size-matched. Therefore, in order to make novel and effective decisions in managing these invasive species,
it is critical to understand species-specific invasion dynamics and size-dependent potential impacts of invasive crayfish on native taxa.
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Agata Mrugała, Lukáš Veselý, Adam Petrusek, Satu Viljamaa-Dirks and Antonín Kouba
May Cherax destructor contribute to Aphanomyces astaci spread in Central Europe?
(pp 459-468)
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Transmission of the crayfish plague pathogen Aphanomyces astaci endangers native European crayfish. This pathogen, spread mainly
by its natural hosts, North American crayfish, has also been detected in the aquarium trade in Europe. As the trade in ornamental crayfish
is nowadays considered a key introduction pathway of non-European crayfish, it may contribute to crayfish plague spread. Non-American crayfish
have been assessed as highly susceptible to the pathogen, and thus unlikely to participate in A. astaci spread from aquarium facilities.
However, moderate resistance to this disease has been suggested for the Australian yabby Cherax destructor. This widely traded crayfish
species exhibits high potential to establish in Central Europe, and has been assessed as a high-risk species with regards to its invasiveness.
We investigated resistance of juvenile C. destructor towards three A. astaci strains differing in virulence (representing genotype
groups A, B and E), present in Central European waters. Cherax destructor was exposed to two doses of A. astaci zoospores
(10 and 100 spores ml-1) and its mortality was further compared with that of the juvenile European noble crayfish Astacus astacus.
While some survival among C. destructor individuals was observed after exposure to the least virulent A. astaci strain
(genotype group A), total mortality of Australian crayfish was noted after infection with the two more virulent strains. However, in contrast
to A. astacus, the mortality of C. destructor was significantly delayed. These results suggest that under favourable conditions
C. destructor may contribute to crayfish plague spread in Central Europe.
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Joseph D. Lechelt and Przemyslaw G. Bajer
Elucidating the mechanism underlying the productivity-recruitment hypothesis in the invasive common carp
(pp 469-482)
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Across-ecoregion analyses showed that the recruitment of common carp, Cyprinus carpio (Linnaeus 1758), a globally invasive fish,
is strongly influenced by lake productivity: while recruitment was frequent in hypereutrophic lakes, it was invariably absent in oligotrophic
lakes. This led to a hypothesis that common carp larvae might have faster growth rates in productive lakes that allow them to outgrow native predators,
whereas larvae might encounter nutritional bottlenecks in oligotrophic lakes. We shed some light on this hypothesis by documenting how zooplankton
communities found in oligo-, meso-, and eutrophic lakes in Minnesota, USA affected larval carp survival, growth and diet composition. We cultured
larval carp in tanks fed zooplankton at naturally occurring densities from three lakes of varying trophic states for 20 days during two consecutive
springs. The growth rates were significantly higher (up to 5 times) among larvae fed zooplankton from the eutrophic lake and lowest in larvae fed
zooplankton from the oligotrophic lake. Despite their small size (~6 mm), carp larvae selected large zooplankton (0.3–0.6 mm), primarily
Bosmina spp., even on the first day of exogenous feeding. This pattern was consistent across all treatments. Rotifers were generally not found
in the stomachs of larval carp, despite their high abundance, even if other food items were scarce. The densities of cladocera were highest
in the productive lake, especially during one of the two years when larval carp showed very rapid growth rates. Our study shows that larval
carp have well defined dietary preferences and that common carp recruitment might be especially likely to occur in productive systems with abundant
cladocera populations in which carp larvae are expected to be more likely to escape gape-limited, native predators.
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