Volume 12, Issue 4 (2017)
published November 2017
Contents | |
Research articles |
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Fabio Crocetta, Serge Gofas, Carmen Salas, Lionello Paolo Tringali and Argyro Zenetos
Local ecological knowledge versus published literature: a review of non-indigenous Mollusca in Greek marine waters
(pp 415–434)
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A review of the scientific literature and an analysis of unpublished material identified ~ 50 possible alien molluscs from Greece,
four of which were newly reported here. Records of ~ 100 additional taxa, which would strongly inflate the alien species numbers,
were excluded. Among the ~ 50 candidate species, 43 were confirmed as alien and 12 as cryptogenic. Twenty-nine alien species
were considered established, and four deemed invasive. Our results are consistent with the position of Greece in the east-west
Mediterranean gradient, as well as the Aegean marine environment. The contribution of well-informed citizen scientists appears
to be crucial to our overall knowledge of alien molluscan biotas because only 12 alien taxa were detected during formal research
projects, while 31 were first found by amateurs. No molluscan introductions were confirmed from Greece pre-1960s, and subsequent
periods had variable numbers of introductions, ranging from 0 (1976–1980) to 9.5 (2006–2010). The areas with the highest alien
species concentrations were the Saronikos Gulf, near the Piraeus port area, and the Dodekanisa, near the Levantine coastline.
Despite a general decline in taxonomic expertise and in local knowledge, we show that these are still needed when compiling
and analyzing alien species inventories that subsequently influence policy and management decisions. |
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Florian Roth, Ines Stuhldreier, Celeste Sánchez-Noguera, Susana Carvalho and Christian Wild
Simulated overfishing and natural eutrophication promote the relative success of a non-indigenous ascidian in coral reefs at the Pacific coast of Costa Rica
(pp 435–446)
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Colonial ascidians of the genus Didemnum are common fouling organisms and are typically associated with degraded ecosystems
and anthropogenic structures installed in the sea. In this study, however, the non-indigenous ascidian Didemnum cf. perlucidum
Monniot F., 1983 was discovered in coral reef environments on the Pacific coast of Costa Rica. Its role in the succession of a benthic
community and the impact on biogeochemical features (i.e. reef cementation) was assessed by deploying terracotta settlement tiles
on the reef for 24 weeks. Predator exclusion in experimental plots and naturally elevated nutrient concentrations during seasonal
coastal upwelling gave insights on how settlers of D. cf. perlucidum succeed under projected environmental change.
Exclusion of larger predators and grazers caused an increase of D. cf. perlucidum coverage on tiles from 7 to > 80%.
Due to its rapid proliferation, D. cf. perlucidum grew over calcifying reef organisms, such as barnacles, polychaetes,
and crustose algae, and significantly decreased the accumulation of inorganic carbon on the settlement tiles by one order of magnitude
(4.6 to 0.4 mg C cm-2). The combination of reduced predation and eutrophication revealed negative synergistic effects on the accumulation
of inorganic carbon. The opportunistic reaction of D. cf. perlucidum to environmental changes was further evident by 2-fold
increased growth rates that were positively correlated (r2 = 0.89) to seawater particulate organic matter (POM) concentration during coastal
upwelling. These results suggest that D. cf. perlucidum is a strong spatial competitor in Eastern Tropical Pacific coral reefs
that face changing environmental conditions, e.g. overfishing and eutrophication. The effects of this species on disturbed benthic communities,
but also its potential role as a habitat modifier, is likely significant. Thus, a continuous monitoring of D. cf. perlucidum is
recommended to better understand their effects on post-disturbance dynamics in coral reef ecosystems. |
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Stephanie M. Villalobos, Gretchen Lambert, Noa Shenkar and Susanna López-Legentil
Distribution and population dynamics of key ascidians in North Carolina harbors and marinas
(pp 447–458)
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Ascidians have successfully invaded marinas and harbors around the world. Despite broad knowledge of their global ranges, in some locations,
including the state of North Carolina, U.S.A., little is known about the community composition and distribution of native and introduced ascidians.
We conducted field surveys at 16 harbors and marinas along the coast of North Carolina (33–35 ºN) and documented the diversity, distribution and
relative abundance of all ascidian species. Ascidians were identified using morphological observations and barcode sequencing of the mitochondrial
gene cytochrome c oxidase subunit I. Distribution patterns of native and introduced ascidians were analyzed using presence-absence and relative
abundance matrices in relation to latitudinal position (South versus North) and geographic distance among harbors. Finally, we monitored
the dynamics of a well-established ascidian community at Wilmington over 1.5 years using photo transects. For each ascidian species, we calculated
percent cover and abundance and then related those values to temperature fluctuations using cross-correlation analyses. Overall, we found three
introduced, two cryptogenic, and eight native ascidian species. Geographic location and distance between survey sites had no effect on ascidian
community composition in terms of presence-absence of species. However, the relative number of individuals per species present at each harbor was
significantly related to the distance between sites. The ascidian community at Wilmington (three native, one cryptogenic, and one introduced species)
showed some seasonality, with abundance and/or percent cover significantly correlated with temperature values recorded during the same month or
a few months beforehand. |
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Xavier de Montaudouin and Chiara Accolla
Is apparent low productivity of the invasive marine mollusc Crepidula fornicata Linnaeus, 1758 related to biased age determination?
(pp 459–468)
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The slipper limpet Crepidula fornicata Linnaeus, 1758 is a major exotic invader of East North Atlantic coasts. Individuals live
on top of each other and form stacks with the youngest on the top. Earlier studies reported that one individual typically settles per year.
If true, it is a simplified means to provide a “shell length-age” relationship for population dynamics studies, especially Production/Biomass ratio
(P/B) assessment. However, estimated P/B ranges between 0.15 and 0.45 yr-1 seem low compared to those of closely-related marine
invertebrates and considering the invasiveness of C. fornicata in coastal habitats. In this study, we placed artificial substrates
(“tiles”) for one year in the middle of a C. fornicata colony and measured settlement. We sometimes observed more than one individual
settling per stack in a year: 4% of stacks were composed by 3 individuals, 27% by 2 individuals and 69% were single specimen. On this basis,
we formulated a model to better link the position of each C. fornicata within a stack to its age. In addition, the C. fornicata
population was annually sampled for 5 years. Then, population dynamics parameters, density at recruitment, mortality rate, growth performance,
production and P/B were estimated. We compared two cases: (i) individual age was defined by its position in stacks; (ii) individual age was
corrected by the model. Recalculation moderately increased growth performance expectation (+2 to 8% per year) but greatly enhanced production
and P/B (ca. 1.2 to 2.6-fold per year). Recalculated P/B values ranged from 0.55 to 0.72 yr-1. While still low, they were more
consistent with published values for similar large marine invertebrates, in particular for invasive species. |
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Ann Wassick, J. Antonio Baeza, Amy Fowler and Dara Wilber
Reproductive performance of the marine green porcelain crab Petrolisthes armatus Gibbes, 1850 in its introduced range favors further range expansion
(pp 469–485)
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Invasive marine crustaceans can exhibit population-level variation in reproductive traits that are consistent with a response
to stressful conditions near the range edge, or alternatively, that may favor establishing new exotic populations. Reproductive
characteristics of the green porcelain crab Petrolisthes armatus Gibbes, 1850 were not previously known in its invasive range
in the Atlantic waters of the southeastern USA. We compared fecundity estimates, size at sexual maturity, and various other morphological
aspects among crabs collected from two sites at each of four locations spanning approximately 230 km from North Inlet, South Carolina (SC),
to Savannah, Georgia (GA), USA. Reproductive output and smallest ovigerous female sizes within the invaded range also were compared those
in the native range, which extends from the Gulf of Mexico and the Caribbean to Brazil in the Western Atlantic Ocean. Reproductive output
and egg number were higher and female size at maturity was smaller for crabs from more northern locations (North Inlet and Charleston, SC).
Crabs were sexually dimorphic, but population-level differences in overall morphology (e.g., dimensions of the carapace, chelipeds,
and secondary sexual characteristics) were not evident in two populations examined (North Inlet, SC, and Bluffton, SC). Secondary sexual
characteristics (i.e., abdomen length, abdomen width and pleopod length) contributed the most to the morphological differences between
males and females. Using allometric methods, size at sexual maturity was estimated to be 3.99 mm carapace width (CW) for males at North
Inlet and 2.96 mm CW for males at Bluffton. Minimum sizes of ovigerous females at our study sites were smaller (3.0 mm to 4.2 mm CW)
than a published value for a native population (4.0 mm CW). Reproductive output also was higher in the introduced range (0.05–0.11) than
in native populations (0.03–0.07). Along a latitudinal gradient at the northern extent of the invaded range, females allocated more energy
to producing offspring at range-edge locations. These results indicate that both within the introduced range and compared to the native range,
P. armatus exhibits considerable variation in reproductive performance, which may have assisted in the species′ successful invasion
and may aid the species in continuing its range expansion. |
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Kristina Tattersdill, Frauke Ecke, André Frainer and Brendan G. McKie
A head start for an invasive species in a strongly seasonal environment? Growth of Elodea canadensis in boreal lakes
(pp 487–498)
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Many invasive species are expanding northwards into boreal and subarctic habitats, but research on the factors favoring their establishment
in these regions remains limited. In three Swedish lakes we investigated the growth of Elodea canadensis Michx, a highly invasive
macrophyte that is spreading northwards in Europe and Alaska. We conducted an in situ growth experiment, maintained for ten months, in concert
with two field macrophyte surveys, undertaken in summer and spring. We further compared the performance of propagules established during summer
with those established under less favorable conditions in late autumn. We found that E. canadensis grew throughout the autumn, followed
by winter dieback, with regrowth occurring early in the spring when water temperatures remained under 5 °C. Elodea canadensis plants were
frequently found in our spring field survey, soon after ice melt, when almost all other species were still dormant. In the growth experiment,
growth of individual shoots was positively associated with key abiotic variables (especially alkalinity) and also with increasing cover of
E. canadensis. The tendency of propagule shoots to fragment from the main stems was also positively associated with increasing
E. canadensis length and ambient population cover. Although propagules established in November initially did worse the following spring
than those established in August, by the start of the following summer both groups were growing equally well, and had converged in morphology.
The growth of E. canadensis throughout autumn and its early re-growth in spring, the capacity of propagules established even in late autumn
to regrow well the following year, and the apparently self-reinforcing effect of increasing local population size on shoot growth all have
the potential to benefit E. canadensis as it spreads north into boreal and subarctic regions. |
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Edward P. Levri, Sarah Landis, Brittany Smith, Elissa Colledge, Elizabeth Metz and Xiaosong Li
Variation in predator-induced behavioral changes in introduced and native populations of the invasive New Zealand mud snail (Potamopyrgus antipodarum Gray, 1843)
(pp 499–508)
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Predator detection and avoidance can be important factors determining the success of an introduced species. The New Zealand mud snail
(Potamopyrgus antipodarum) exhibits avoidance behaviors when chemically detecting native piscine predators in New Zealand, and
these behaviors appear specific to sympatric fish populations. Here we utilized three different introduced clonal populations of the New
Zealand mud snail from North America, and various clones from New Zealand lakes, to examine the effect of a novel piscine predator,
the blacknose dace (Rhinichthys atratulus), on behavior. Two of the introduced clones in North America are invasive (US1 and US2)
while a third clone (US3) has not exhibited invasive tendencies. In a laboratory setting, we examined geotactic (vertical movement
in response to gravity), photokinetic (differential speeds in response to light), and emergence behaviors of each clonal population
in the presence and absence of a predator chemical cue. Geotaxis was measured by determining the vertical distance traveled in two minutes.
Photokinesis was measured by quantifying the horizontal distance travelled in two minutes in light and dark conditions. Emergence time was
determined by removing individuals from the water for five seconds and then replacing them in water and measuring the time to emerge from
the shell. We found that the two invasive populations of the New Zealand mud snail (US1 and US2) detected and behaviorally responded
to the novel predator utilizing positive photokinesis. The US1 population also showed some evidence of geotactically responding to fish odor.
The introduced but likely non-invasive US3 population did not exhibit a detectable response to the odor of fish. Some evidence of photokinetic
behavioral responses to the North American fish odor was also found in New Zealand native populations. Fish odor did not appear to influence
the time it took for any population of snails to emerge from their shells. These results suggest that the ability to detect and respond
to novel predators may be an important trait in the invasion success of New Zealand mud snails by potentially allowing snails to avoid
novel predators. |
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Daniel N. Mills, Michael A. Chadwick and Robert A. Francis
Impact of invasive quagga mussel (Dreissena rostriformis bugensis, Bivalva: Dreissenidae) on the macroinvertebrate community structure of a UK river
(pp 509–521)
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The arrival of invasive quagga mussel (Dreissena rostriformis bugensis) to the UK necessitates rapid study to evaluate its impact
on benthic community structure where colonisation has occurred. In the Wraysbury River (west London), impact on benthic invertebrate community
structure by invasion of quagga mussel was measured by comparing a series of invaded and uninvaded study sites over an annual period of monthly
sampling. It was apparent that despite quagga mussel consistently forming a large proportion of stream biomass in invaded sites, community
taxon richness and composition did not vary significantly in comparison to uninvaded sites. Similarly, total community biomass and density
when excluding quagga mussel was mostly homogeneous across the study reach, with the exception of one site with the highest quagga mussel
biomass and density. If quagga mussel biomass and density increased over time to levels found at this site, more significant changes to native
community structure might be expected. This study represents a first benchmark for understanding the progression and impacts of quagga mussel
invasion in UK rivers and these results will be essential for comparison in evaluating future change and impacts. |
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Eglė Šidagytė, Vladimir Razlutskij, Anatolij Alekhnovich, Aleksandras Rybakovas, Mikhail Moroz, Viktė Šniaukštaitė,
Gintautas Vaitonis and Kęstutis Arbačiauskas
Predatory diet and potential effects of Orconectes limosus on river macroinvertebrate assemblages of the southeastern Baltic Sea basin: implications for ecological assessment
(pp 523–540)
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Invasive crayfish can affect macroinvertebrate assemblages and thus alter conventional macroinvertebrate-based ecological assessment.
We aimed to reveal potential impacts of the North American crayfish Orconectes limosus on river assessment in the Neman River basin
(southeastern Baltic Sea). A laboratory experiment using identical macroinvertebrate assemblages was conducted to compare feeding selectivity
and effects between O. limosus and the European Astacus leptodactylus. Field experiments were conducted to evaluate potential
impacts of O. limosus on disturbed and undisturbed crayfish-free macroinvertebrate assemblages: one dominated by Oligochaeta vs. one
co-dominated by Ephemeroptera-Plecoptera-Trichoptera and Mollusca (EPT-codominated). In the laboratory experiment, both crayfish species
preferred feeding on Diptera (mostly chironomids), but O. limosus also selected Trichoptera and Ephemeroptera. Family richness
did not change, but both species inflated the Shannon Diversity index by reducing Diptera domination. Astacus leptodactylus treatments
had higher Shannon Diversity and percentage of EPT abundance compared to O. limosus treatments. Field experiments indicated (1) negative,
(2) assemblage-specific, or (3) no effects of O. limosus on macroinvertebrate metrics. A negative effect, especially in the undisturbed
assemblage, was observed on simple additive metrics based on taxa presence data, such as total or EPT family richness, or BMWP (Biological
Monitoring Working Party) score. Assemblage-specific effects were indicated for some metrics based on relative abundances.
In the Oligochaeta-dominated assemblage, Shannon Diversity was inflated and the percentage of Oligochaeta abundance was reduced.
In the EPT-codominated assemblage Shannon Diversity was deflated while the relative abundance of Oligochaeta was not affected. No effects
were observed when using the ASPT (Average BMWP Score Per Taxon) or percentage of EPT abundance. We conclude that O. limosus may
have a more diverse predatory diet than A. leptodactylus, and thus can have a stronger effect on macroinvertebrate taxa sensitive
to disturbances. Therefore, the invasion of O. limosus can alter macroinvertebrate assemblages and compromise conventional ecological
assessment, even when it displaces resident Astacus species. |
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Frederic Grandjean, Jonathan Roques, Carine Delaunay, Adam Petrusek, Thomas Becking and Marc Collas
Status of Pacifastacus leniusculus and its role in recent crayfish plague outbreaks in France: improving distribution and crayfish plague infection patterns
(pp 541–549)
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Aphanomyces astaci, the crayfish plague pathogen, is responsible for mass mortalities in native European crayfish stocks.
Its persistence and spread across Europe has been facilitated by the presence of invasive North American crayfish species, which act
as asymptomatic vectors of this pathogen. In France, some recent mass mortalities have involved the pathogenic strain harboured
by the invasive signal crayfish, Pacifastacus leniusculus, which may share habitats with the autochthonous white-clawed crayfish,
Austropotamobius pallipes. To improve the efficiency of conservation management of A. pallipes, we have (i) updated information
on the distribution of P. leniusculus populations in France based on data collected by the ONEMA (French National Agency for Water and
Aquatic Environments), (ii) studied the distribution and prevalence of the crayfish plague pathogen within P. leniusculus populations
throughout the country, and finally (iii) genotyped the strains responsible for several recent mass mortalities in A. pallipes populations.
In total, 1658 populations of the signal crayfish were recorded in France; 1554 of these in streams and 104 in ponds. In 2014, this species was
present in 80 of 95 French departments. Among the 1131 analyzed P. leniusculus individuals from 94 localities, 255 individuals (23%)
tested positive for A. astaci presence. Infected individuals were detected in 63% of studied populations. Local prevalence varied highly
among populations, ranging from 0% (no detection of A. astaci) up to 90% in the most infected ones. Out of five mass mortalities characterized
in France in 2014–2015, four involved the strain from genotype group B, specific to P. lenisuculus. Our results confirm that the widespread
signal crayfish serves as a key reservoir of A. astaci in France and therefore represents a serious danger for native crayfish species,
especially the white-clawed crayfish. |
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Michal Janáč, Josef Bryja, Markéta Ondračková, Jan Mendel and Pavel Jurajda
Genetic structure of three invasive gobiid species along the Danube-Rhine invasion corridor: similar distributions, different histories
(pp 551–564)
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Ponto-Caspian gobiids have expanded their ranges throughout Europe since the 1990s. While genetic studies have been widely used to assess
the invasion history of gobiids in North America, complex genetic studies involving multiple sites and species have been less common in Europe,
severely limiting our understanding of invasion processes along navigable rivers and their tributaries. In this study, we used both nuclear
and mitochondrial markers to assess genetic diversity and structure in native and non-native Western tubenose goby Proterorhinus semilunaris,
round goby Neogobius melanostomus and bighead goby Ponticola kessleri sampled from the main areas of their joint distribution, i.e. the lower
Danube, middle Danube and lower Rhine. Additionally, we describe expansion into Danubian tributaries and provide early genetic data for
N. melanostomus from the River Elbe. Our data revealed i) a founder effect in non-native P. semilunaris, ii) an increase in genetic diversity
in non-native N. melanostomus samples from the Rhine and Elbe, and iii) no genetic structuring in P. kessleri. This suggests greater initial
propagule pressure in P. kessleri; strong propagule pressure with introductions from multiple sources followed by admixture for N. melanostomus
in the Rhine and Elbe; and one or very few introduction events for P. semilunaris. We provide further support for the Danubian origin of all three
goby species in the Rhine and document lower genetic diversity in fish colonising non-navigable tributaries. Our results illustrate how the ranges
of invasive species can become sympatric, despite clear differences in their invasion histories. |
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Francisco D. Moreira, Raquel Marques, Monica Sousa and Rui Rebelo
Breeding in both lotic and lentic habitats explains the invasive potential of the African clawed frog (Xenopus laevis) in Portugal
(pp 565–574)
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The African clawed frog is a successful invader in several countries throughout the world. Although it may be found
in both lentic and lotic habitats, its use of both habitats for breeding has not been documented. Nonetheless,
in its Portuguese invasive range this frog was found to breed in small streams, as well as in ponds. We recorded
all the sites where Xenopus laevis bred during a 7-year period (2010–2016) in the entire Portuguese invasive range.
In 2015 and 2016, we measured snout-vent length of 970 tadpoles from eleven sites, and the size and body condition
at the end of metamorphosis of 91 metamorphs from four sites. To assess the size at which reproductive investment begins,
we dissected and weighed the gonads of 409 juveniles and small adults. We found that the species can produce metamorphs
in both habitats, but their numbers were much higher in lentic sites. Furthermore, tadpoles and metamorphs from lentic
sites were much larger than those from lotic sites. Body condition of metamorphs was similar across all sites.
Gonad development was size-dependent, and we estimate that larger metamorphs from lentic sites will mature sooner
and may reproduce in the following year, while smaller metamorphs will need an extra year. Our results suggest that
while lentic sites are most likely to be responsible for population booms, the hitherto unknown reproduction in lotic
sites may contribute to the maintenance of the invasive population even in the absence of lentic sites. |
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