Volume 12, Issue 1 (2017)
published March 2017
Contents | |
Letter to the Editor |
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Manuel António E. Malaquias, Andrea Zamora-Silva, Dyana Vitale, Andrea Spinelli, Sergio De Matteo, Salvatore Giacobbe, Deneb Ortigosa and Juan L. Cervera
The Suez Canal as a revolving door for marine species: a reply to Galil et al. (2016) (pp 1–4)
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In this reply, we address the criticism directed recently to our work (Malaquias et al. 2016) by Galil et al. (2016) dismissing
the hypothesis that the Suez Canal can act as a revolving door allowing marine species to move both ways between the Red Sea
and the Mediterranean Sea. We reiterate that the presence in the Red Sea of the Indo-West Pacific sea slug Chelidonura fulvipunctata
Baba, 1938 is most parsimoniously explained by an invasion from the Mediterranean and highlight several recent studies combing morphology
and molecular phylogenetics where established views about the presence of alien Indo-Pacific / Red Sea species in the Mediterranean were
proven wrong. Caution is suggested when assuming the conspecificity of species between these realms based solely on external features.
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Research articles |
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Lodewijk van Walraven, Rogier Daan, Victor T. Langenberg and Henk W. van der Veer
Species composition and predation pressure of the gelatinous zooplankton community in the western Dutch Wadden Sea before and after the invasion of the ctenophore Mnemiopsis leidyi A. Agassiz, 1865
(pp 5–21)
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The ctenophore Mnemiopsis leidyi A. Agassiz, 1865 is a successful, recent, macroplanktonic invader in European coastal waters,
including the Dutch Wadden Sea. It occurs year-round in substantial numbers. The effect of M. leidyi on structure of the gelatinous
zooplankton community in the Dutch Wadden Sea was studied by comparing data from before and after its introduction. Gelatinous zooplankton
species composition in the western Wadden Sea was largely the same between 1980–1983 and 2009–2012. Only the hydromedusa Eutonina indicans
(Romanes, 1876) was absent in recent years while Cosmetira pilosella Forbes, 1848 and Margelopsis haeckelii Hartlaub, 1897 were rare species
observed only in 2009–2012. M. leidyi was present since 2006, with high densities every year in summer and autumn. Predation pressure
by scyphomedusae, ctenophores, and hydromedusae on fish larvae and zooplankton in 1980–1983 was low because of low densities and a temporal
mismatch between gelatinous zooplankton and their prey. Despite the decrease in abundance of scyphomedusae in recent decades, the introduction
of M. leidyi and its large annual blooms have increased the overall importance of gelatinous zooplankton as predators in the western Wadden Sea,
whereby M. leidyi is responsible for most of the predation pressure on mesozooplankton in the area. Rather than outcompeting local species,
M. leidyi appeared to fill in a previously unoccupied niche in the pelagic western Dutch Wadden Sea in late summer and autumn.
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Daniela Batista, Jose Eduardo Arruda Gonçalves, Héctor Fabian Messano, Luciana Altvater, Rogério Candella, Leandro Machado Calil Elias, Luciana Vicente Resende De Messano, Moacir Apolinário and Ricardo Coutinho
Distribution of the invasive orange cup coral Tubastraea coccinea Lesson, 1829 in an upwelling area in the South Atlantic Ocean
fifteen years after its first record
(pp 23–32)
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A survey of the distribution and abundance of the invasive orange cup coral Tubastraea coccinea Lesson, 1829 was conducted using
photoquadrats during 2014/2015, fifteen years after its first documented introduction in a Cabo Frio upwelling area in the western
South Atlantic (42º00′W–22º44′S). These data were related to local currents and to a dispersion model of particles and with sea surface
temperatures (SST). The objective was to investigate how variations in environmental conditions (local currents and temperatures)
influence the dispersion and survival of T. coccinea. Complementary laboratory experiments were performed to investigate
the effects of low temperatures on the survival of this species. T. coccinea has expanded its distribution and larval
dispersion seems to be driven by the local currents. Furthermore, higher densities of colonies and recruits were observed within
areas with higher water temperatures (>20 °C), while no coral was found in the area of direct upwelling influence, suggesting that
cold waters limited the distribution of T. coccinea. These findings were corroborated by laboratory experiments that showed
a negative effect of cold water (≤ 12.5 °C) on colony survival. The present data contribute to our understanding of the worldwide
geographical expansion of T. coccinea and could be particularly important for management decisions to prevent new invasions.
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A. Michaela Harris, Andrea M. Moore, J. Ben Lowen and Claudio DiBacco
Seasonal reproduction of the non-native vase tunicate Ciona intestinalis (Linnaeus, 1767) in Nova Scotia, Canada, in relation to water temperature
(pp 33–41)
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Intra-annual and inter-annual reproductive periodicity for in situ populations of Ciona intestinalis were documented
from October 2013 to August 2015 in the small vessel marina at the Bedford Institute of Oceanography in Dartmouth, NS.
Three metrics of reproduction were monitored: (i) larval settlement, (ii) gonad development and (iii) gamete viability.
In situ settlement was observed between June and November 2014. Gonad development during spring consisted of a sharp
increase in the proportion of males followed by development into hermaphrodites, which resulted in a near entirely-hermaphroditic
population throughout the summer and fall. The proportion of males and hermaphrodites began to decline by late fall;
hermaphrodites were absent by early winter (i.e., late December or January), whereas males persisted at low abundance
throughout the winter. In-vitro fertilization assays demonstrated that gametes became non-viable by early December.
The seasonal changes in development stages were compared with respect to ambient seawater temperature and growing degree days.
The spring maturation in 2014 occurred 3 weeks earlier than observed in 2015 (i.e., May 2014 and June 2015), likely due to
a 2.0 °C higher mean seawater temperature than the same period in 2015. The effect of temperature on development rate was
confirmed in a mesocosm experiment where the 3 °C elevated temperature treatment resulted in earlier sexual maturation
by ten days for males and eight days for hermaphrodites compared to those in the unheated treatment. These results demonstrate
the potential for an extended reproductive window, and perhaps extended geographic range, in response to predicted increases
in ambient sea surface temperatures in Atlantic Canada in the next few decades.
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Martine Wagstaff
Life history variation of an invasive species Botrylloides violaceus (Oka, 1927) between novel coastal habitats in the Gulf of Maine
(pp 43–51)
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Species invasions are characterized by range expansions during which invasive species respond ecologically and evolutionarily
to new environmental conditions. Responses to novel environments often involve shifts in life history traits, which may be due
to phenotypic plasticity, local adaptation, or both. Identifying how species vary across novel habitats can help determine how
invaders integrate themselves into local ecosystems, which is a poorly understood aspect of marine ecology and management.
In the Gulf of Maine, the invasive ascidian Botrylloides violaceus (Oka, 1927) is found on man-made substrates and
has also entered natural subtidal habitats. To investigate if the life history characteristics of B. violaceus vary
across habitats, colonies were grown on polycarbonate plates in floating dock, eelgrass bed, and rocky subtidal habitats,
and life history traits were quantified from settlement until death from June 2012 to July 2013. This was replicated
at three sites along the Massachusetts coast. Settlement density differed among habitats and was highest in floating dock,
lower in eelgrass bed, and least in rocky subtidal habitats. Terminal age was not different among habitats. Terminal size
and maximum growth rates were higher in floating dock and eelgrass bed habitats than in the rocky subtidal habitats.
The duration of colony regression did not differ among habitats. In floating dock habitats, distinct, seasonal cohorts
were observed. These results suggest that B. violaceus is most successful in man-made versus natural habitats.
Its integration into natural habitats may, however, be in an early phase; with B. violaceus still posing
a threat to native species and ecosystems.
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Craig A. Styan, Claire F. McCluskey, Yanan Sun and Elena K. Kupriyanova
Cryptic sympatric species across the Australian range of the global estuarine invader Ficopomatus enigmaticus (Fauvel, 1923) (Serpulidae, Annelida)
(pp 53–65)
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Ficopomatus enigmaticus (Fauvel, 1923) is a reef-building serpulid polychaete that has invaded estuaries worldwide,
causing environmental and economic harm. Although Australia has long been suggested as a place of origin for the species,
this remains unclear. We tested for genetic patterns across the range of F. enigmaticus in southern Australia, predicting
that if the species is an Australian native, it would show evidence of (east-west) phylogeographic patterns often observed in native
marine species in southern Australia. Unexpectedly, concordant patterns from mitochondrial (Cyt B) sequencing and nuclear marker (iSSR)
profiles suggested the presence of at least three genetic groups (putative species), not distributed simply as “east” or “west”.
Two common (and closely related) groups were present across Australia and were often found together in the same aggregations.
A third group was only found in southeast Australia and was morphologically similar to F. uschakovi (Pillai, 1960),
a species previously reported from tropical areas. The discovery of multiple cryptic species with overlapping ranges means
that more work is needed to resolve whether any of the F. enigmaticus sensu lato group has an Australian origin and
to determine how they are related to invasive populations of F. enigmaticus elsewhere.
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Sandra Hudina, Petra Kutleša, Krešimira Trgovčić and Aljoša Duplić
Dynamics of range expansion of the signal crayfish (Pacifastacus leniusculus) in a recently invaded region in Croatia
(pp 67–75)
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The signal crayfish, Pacifastacus leniusculus, is the most widespread and one of the most successful crayfish invaders in Europe.
In 2012 it was recorded in a karstic river in the continental part of Croatia, the Korana River, where it was illegally introduced.
Here, it presents an alarming threat to native crayfish diversity, since three native crayfish species have viable populations
in the Korana River and its tributaries. We explored the dynamics of signal crayfish range expansion in the Korana River,
by i) examining the increase in its range, ii) analysing changes in its relative abundance, size and sex structure at former
invasion fronts in 3 years (since the first study), and iii) examining the status of the native narrow-clawed crayfish
(Astacus leptodactylus) in the area. Signal crayfish range increased 2.5 times since 2012, and currently covers 18.7%
of the entire watercourse. Recorded dispersal rate (2.23 – 2.84 km/year) was similar in upstream and downstream direction.
At both former invasion fronts, increase in the relative signal crayfish abundance by 4.9 – 6.1 times resulted in significant
decrease in the size of signal crayfish individuals, demonstrating the prominent effect of density and competition intensity
on the size structure its populations. The native A. leptodactylus was completely displaced from mixed populations
at former invasion fronts, while at new invasion fronts no narrow-clawed crayfish were recorded. Abundant A. leptodactylus
populations are still present in the Mrežnica and Kupa Rivers, and outside the invaded area in the Korana River. We discuss
these findings in the context of potential management actions and legal requirements for such actions under EU Regulations.
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Jörn Panteleit, Nina Sophie Keller, Harri Kokko, Japo Jussila, Jenny Makkonen, Kathrin Theissinger and Anne Schrimpf
Investigation of ornamental crayfish reveals new carrier species of the crayfish plague pathogen (Aphanomyces astaci)
(pp 77–83)
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Several North American crayfish species have so far been identified as carriers of the crayfish plague agent Aphanomyces astaci.
The pathogen is responsible for the declines of thousands of European crayfish populations. Currently, one of the introduction pathways
of North American crayfish species is the aquarium trade which may sometimes be followed by intentional release or unintentional escape
of the pet species into the wild. We investigated 85 samples of North American and New Guinean species, available through the aquarium trade,
for their possible infection with A. astaci. Crayfish plague infection was examined by applying real-time PCR. Besides morphological
identification, we sequenced a fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene for crayfish species confirmation.
Additionally, sequence analysis of nuclear DNA was conducted to identify the A. astaci lineage of moderate to highly infected crayfish.
A total of 11 of the 85 analyzed crayfish individuals tested positive for an A. astaci infection, of which nine species are for the first
time identified as carriers of A. astaci. No new genetic lineages of A. astaci were identified. The results confirm that, due
to the positive carrier status of tested crayfish, the aquarium trade in Europe can facilitate the spread of A. astaci and can thus
be a significant threat to the indigenous crayfish and the environment.
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Simon Jungblut, Jan Beermann, Karin Boos, Reinhard Saborowski and Wilhelm Hagen
Population development of the invasive crab Hemigrapsus sanguineus (De Haan, 1853) and its potential native competitor Carcinus maenas (Linnaeus, 1758) at Helgoland (North Sea) between 2009 and 2014
(pp 85–96)
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The Asian shore crab Hemigrapsus sanguineus (De Haan, 1853) has recently established populations in the North Sea and now occurs
within the native ranges of the green crab Carcinus maenas (Linnaeus, 1758). To determine potential competitive effects and to assess
the progress of the invasion, species-specific population characteristics (numerical abundances, biomasses, and size distributions) of the two
species around the island of Helgoland (German Bight, southern North Sea) were compared for surveys conducted in 2009 and 2014. Sampling sites
were chosen based on accessibility and differed in their topography and wave exposure, which allowed testing for the influence of these factors
on the establishment success of H. sanguineus. The numerical abundance and biomass of H. sanguineus increased markedly and approached
those of C. maenas in 2014. At a sheltered site, H. sanguineus even outnumbered C. maenas, whereas the converse was observed
at a site exposed to strong winds and waves. Although such contrasting abundance patterns between the native and the introduced shore crab may be
the result of direct interference, the dominance of H. sanguineus at the sheltered site may also be explained by enhanced larval settling
rates caused by odors of conspecifics. The results suggest that the invasion of H. sanguineus has not yet reached its equilibrium, and
population abundances in the North Sea are expected to further increase in the future.
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Mari Taniguchi, Jeffrey E. Lovich, Kanako Mine, Shintaro Ueno and Naoki Kamezaki
Unusual population attributes of invasive red-eared slider turtles (Trachemys scripta elegans) in Japan: do they have a performance advantage?
(pp 97–108)
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The slider turtle (Trachemys scripta Thunberg in Schoepff, 1792) is native to the USA and Mexico. Due to the popularity
of their colorful hatchlings as pets, they have been exported worldwide and are now present on all continents, except Antarctica.
Slider turtles are well-established in Japan and occupy aquatic habitats in urban and agricultural areas, to the detriment of native
turtles with which they compete. We asked the overall question, do slider turtles in Japan have a performance advantage because
they are liberated from the numerous competing turtle species in their native range and released from many of their natural predators?
Traits compared included various measures of adult body size (mean, maximum), female size at maturity as measured by size of gravid females,
clutch size, population density and biomass, sex ratio, and sexual size dimorphism, the latter two a partial reflection of growth and maturity
differences between the sexes. We sampled slider turtle populations in three habitats in Japan and compared population attributes with published
data for the species from throughout its native range in the USA. Mean male body sizes were at the lower end of values from the USA suggesting
that males in Japan may mature at smaller body sizes. The smallest gravid females in Japan mature at smaller body sizes but have mean clutch
sizes larger than some populations in the USA. Compared to most populations in the USA, slider turtles achieve higher densities and biomasses
in Japanese wetlands, especially the lotic system we sampled. Sex ratios were female-biased, the opposite of what is reported for many populations
in protected areas of the USA. Sexual size dimorphism was enhanced relative to native populations with females as the larger sex. The enhanced
dimorphism is likely a result of earlier size of maturity in Japanese males and the large size of mature (gravid) Japanese females. Slider
turtles appear to have a performance advantage over native turtles in Japan, possibly as a result of being released from competition with
numerous sympatric turtle species in their native range, and the absence of many co-evolved predators and parasites in Japan. This slight
competitive edge, coupled with the catholic diet and broad tolerance of varying aquatic habitats of slider turtles, is reflected in their
dominance over native and naturalized Japanese turtles in altered aquatic habitats.
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Wen Xiong, Chunyan Shen, Zhongxin Wu, Huosheng Lu and Yunrong Yan
A brief overview of known introductions of non-native marine and coastal species into China
(pp 109–115)
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Non-native marine species have attracted a great deal of attention due to wide distribution and potential harmful impacts
on ecosystems and economies. However, relatively little information exists about non-native marine species in China.
This study provides an inventory of non-native marine and coastal species (213 species) reported to date in China
(including the Bohai Sea, the Yellow Sea, the East China Sea, and the South China Sea). The main source regions were
the Atlantic, Pacific, Indo-Pacific, and Indian Oceans (196 species in total, or 92.0% of species). Over one-third
of non-native marine species (74 species) have established self-sustaining populations, and nearly half of the non-native
species (93 species) caused negative ecological and economic impacts. The main introduction pathways of the known
non-native species are ornamental trade (74 species, 34.7%), followed by aquaculture (69 species, 32.4%), shipping
(65 species, 30.5%), and ecological restoration (5 species, 2.3%). The number of non-native marine species is higher
in the northern sea than that in the southern sea of China. Non-native marine species have caused significant positive
and negative impacts on China’s environment and economy. Clearly, future studies need to focus on detecting and managing
non-native marine species in China.
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