Volume 11, Issue 3 (2016)
published July 2016
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Research articles |
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James T. Melton III, Ligia Collado-Vides and Juan M. Lopez-Bautista
Molecular identification and nutrient analysis of the green tide species Ulva ohnoi M. Hiraoka & S. Shimada, 2004
(Ulvophyceae, Chlorophyta), a new report and likely nonnative species in the Gulf of Mexico and Atlantic Florida, USA
(pp 225–237)
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Species level identifications of morphologically simple marine algae have undoubtedly caused biodiversity assessments to be an arduous task.
The green algal genus Ulva L., 1753, is notorious for morphological plasticity and cryptic speciation. We used two chloroplast-encoded
(rbcL and tufA) molecular markers and the nuclear internal transcribed spacer 1 (ITS1) of the ribosomal cistron to detect Ulva ohnoi
M. Hiraoka and S. Shimada, 2004, a species known for forming green tides in Japan, as a new record for the Western Atlantic, including the Gulf of Mexico
(GoMX) and Atlantic coast of Florida. All rbcL sequences from this investigation were identical to reports for U. ohnoi. The Western Atlantic
isolates showed relatively low genetic diversity in tufA and ITS1 sequences, which suggests that this species is not native to the GoMX and
Atlantic Florida. Furthermore, we have identified U. ohnoi as the species that formed an ephemeral, localized overgrowth during July of 2013
in Biscayne Bay, Florida, an area with a persistent bloom of two other green algal species, Anadyomene stellata J. V. Lamouroux, 1812, and
Anadyomene sp., due to eutrophication from anthropogenic nutrient loading near canals. A tissue nutrient analysis of samples from this
overgrowth of Ulva showed that this species has a high affinity for nitrogen, especially ∂15N, which suggests anthropogenic sources
of N. Further investigations are needed to assess the geographical ranges of this species in this region as well as the potential invasiveness of this
alga in the Western Atlantic. It is highly recommended to monitor the abundance of this species in response to nutrient discharges in Biscayne Bay.
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P. Joana Dias, Rosana Rocha, Scott Godwin, María Ana Tovar-Hernández, Maria V. Delahoz, Simon McKirdy, Paul de Lestang, Justin I. McDonald and Michael Snow
Investigating the cryptogenic status of the sea squirt Didemnum perlucidum (Tunicata, Ascidiacea) in Australia based on a molecular study of its global distribution
(pp 239–245)
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Didemnid species are assessed as species with a high invasive potential for Australia and as such are listed as target species for both state
and national monitoring programs. The presence of the sea squirt Didemnum perlucidum (Monniot, 1983) was first documented in Australia
in 2010 and has since then been detected extensively throughout the state of Western Australia and in the Northern Territory. These detections
have raised important questions as to the origin and potential impact of this species in Australia. The current study was initiated to review
the current known global geographic range of D. perlucidum and to obtain specimens that could support molecular studies aimed at evaluating
the potential origin of this species in Australia. Characterization of 5’ COI mitochondrial sequences from 286 specimens revealed a remarkably
low level of genetic diversity across the current known range of D. perlucidum and the existence of one main widespread genetic haplotype.
Such findings suggest that all locations sampled in this study may in fact represent introductions of D. perlucidum and that the natural
native range of the species remains unknown. Our demonstration that specimens (n=187) originating from across a broad expanse of the Australian
West Coast were comprised of a single haplotype also lends support to the hypothesis that D. perlucidum is a species that has been introduced
recently into Australia. This hypothesis is supported by the fact that D. perlucium distribution in Australia is mostly confined to artificial
structures, it has displayed invasive characteristics, and its presence is now being detected across an increasingly wide geographical area. Given
the demonstrated low level of genetic COI variation across its known global distribution, lack of clarity around its native range, and limited
availability of data on this species globally, we recognize the requirement for further work to more fully elucidate the exact origins and patterns
of distribution of D. perlucidum in Australia. This study represents the most comprehensive mapping of the current global distribution
of D. perlucidum conducted to date and will hopefully motivate further studies aimed at elucidating this species biology, origin, high-risk
routes and impacts.
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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 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
(pp 247–255)
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The number of tropical species established in the Mediterranean Sea has risen at an unprecedented rate in the last 40–50 years,
often entering the basin from the Red Sea and to a lesser extent by shipping or mariculture. The taxonomic identity of these alien species
can be difficult to determine and DNA barcoding can help to clarify the status of questionable species. One of these cases is the W-shaped mark
Aglajidae slug usually identified as being the Indo-West Pacific species Chelidonura fulvipunctata Baba, 1938 but was first described
in the Mediterranean Sea as a native species under the name C. mediterranea Swennen, 1961. A Bayesian phylogeny using the barcode marker
cytochrome c oxidase subunit I and an ABGD species delimitation analysis unequivocally showed that specimens from the eastern and central
Mediterranean Sea are conspecific with specimens from the Indian and Pacific Oceans. In this work, we hypothesize that C. fulvipunctata
(presently occurring in the entire Mediterranean Sea and Indo-West Pacific; only once recorded in the Red Sea) has entered the Red Sea through
the Mediterranean Sea. Thus the Red Sea can also be a receiver of tropical species that have arrived in the Mediterranean by other routes than
Lessepsian immigration, with the Suez Canal acting as a “revolving door” allowing both species of Indo-Pacific origin to enter the Mediterranean
and species established in the Mediterranean resilient to tropical/subtropical environmental conditions to move into the Red Sea.
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Nelson A.F. Miranda, Elena K. Kupriyanova, Gavin M. Rishworth, Nasreen Peer, Thomas G. Bornman, Matthew S. Bird and Renzo Perissinotto
An invasive polychaete species found in living marine stromatolites
(pp 257–266)
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This study represents the first report of an invasive species associated with modern, living stromatolites. The presence and potential impacts
of the reef-forming tubeworm Ficopomatus enigmaticus (Fauvel, 1923) in unique stromatolite ecosystems of South Africa are addressed.
Data on F. enigmaticus populations and a suite of environmental variables were collected on a monthly basis in 2014, at three sites along
the Eastern Cape coast. Results are interpreted in terms of known environmental tolerance, reproductive strategy and environmental impacts of
F. enigmaticus around the world. A combination of variables influenced the F. enigmaticus populations, particularly temperature
and the availability of substrates for settlement. Low water temperatures (< 20°C) in winter appeared to limit the species growth and reproduction.
Small populations of adult individuals were however able to persist all year round in habitats that exhibit favourable environmental conditions.
These stromatolite pools appear to function as unique ecosystems that provide refuge for estuarine species, thus acting as stepping stones
facilitating the dispersal and range expansion of estuarine fauna along the coast, including invasive species.
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Lukas De Ventura, Dirk Sarpe, Kirstin Kopp and Jukka Jokela
Variability in phenotypic tolerance to low oxygen in invasive populations of quagga and zebra mussels
(pp 267–276)
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Novel biotic or abiotic conditions can cause invasive species to evolve rapidly in their newly invaded habitats and are important factors
when predicting species invasions. Zebra mussels (Dreissena polymorpha) have a relatively long invasion history in Western Europe,
whereas quagga mussels (Dreissena rostriformis bugensis) began spreading about a decade ago. In a previous invasion to North America,
quagga mussels repeatedly colonized stratified lakes at greater depth than zebra mussels. It would be important to know if the same invasion
pattern is expected to repeat in Western Europe, as the quagga are expected to reach deep stratified lakes in the near future. This might
require quagga mussels to be more tolerant of the low oxygen conditions at depth than zebra mussels. Therefore, using a fully factorial design,
we tested survival of different zebra and quagga mussel populations from Western Europe at four oxygen levels (6%, 33%, 66% and 90%) and two
temperature regimes (11°C and 18°C). Surprisingly, survival differences among oxygen and temperature treatments depended more on population
origin than on species identity. This finding suggests that populations have undergone rapid and convergent adaptation to local conditions
after invasion, in particular to low oxygen. We also found that population-by-environment interactions were more variable among quagga
than zebra mussel populations. Our results suggest that rapid evolutionary adaptation to low oxygen conditions needs to be considered
when predicting the further spread of zebra and quagga mussels.
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Gabriel Iketani, Manoel Alessandro Borges Aviz, Cristiana Maciel, Wagner Valenti, Horacio Schneider and Iracilda Sampaio
Successful invasion of the Amazon Coast by the giant river prawn, Macrobrachium rosenbergii: evidence of a reproductively viable population
(pp 277–286)
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Macrobrachium rosenbergii has been introduced into a number of countries, and in some of these, it has already been frequently
captured in the wild. As for any other exotic species, its success in new habitats is related primarily to its reproductive capacity.
For the present study we evaluated the reproductive capacity of an introduced population of M. rosenbergii in estuaries
of the Amazon Coast, north Brazil. A total of 588 specimens (305 males and 283 females) were captured during 24 months. Of the females,
82 (28.9%) were incubating eggs, and 62 (21.9%) had recently spawned. In addition, more than 70% of the females had mature or maturing gonads.
Mean fecundity was 55,000 eggs, with a minimum of 9,086, and a maximum of 192,172 eggs. Ovigerous females were captured throughout the study period,
indicating continuous reproduction. Adult males are known to present three morphotypes, all of which were observed in the present study,
but with a predominance of the intermediary Orange Claw morphotype (48%). The body length and weight of males were greater than in females.
Different size classes were observed for both sexes during the study period suggesting a continued recruitment of new individuals
to the population over the time. The species has been harvested from the wild for more than ten years, being interrupted during
the period when the river is flooded. This may function as a natural interval for the recovery of stocks, which may favor
the establishment of a sustainable population over the long term. We conclude that the exotic population of M. rosenbergii
in eastern Amazonia is capable of reproducing itself and probably has the capacity to persist over future generations, causing a strong
impact on native species. Given this, it is important to continue monitoring the progress of this species and its potential effects
on the biodiversity of the Amazon basin.
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Kelley L. Kroft and April M.H. Blakeslee
Comparison of parasite diversity in native panopeid mud crabs and the invasive Asian shore crab in estuaries of northeast North America
(pp 287–301)
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Numerous non-indigenous species (NIS) have successfully established in new locales, where they can have large impacts on community
and ecosystem structure. A loss of natural enemies, such as parasites, is one mechanism proposed to contribute to that success.
While several studies have shown NIS are initially less parasitized than native conspecifics, fewer studies have investigated whether
parasite richness changes over time. Moreover, evaluating the role that parasites have in invaded communities requires not only
an understanding of the parasite diversity of NIS but also the species with which they interact; yet parasite diversity in native
species may be inadequately quantified. In our study, we examined parasite taxonomic richness, infection prevalence, and infection
intensity in the invasive Asian shore crab Hemigrapsus sanguineus De Haan, 1835 and two native mud crabs (Panopeus herbstii
Milne-Edwards, 1834 and Eurypanopeus depressus Smith, 1869) in estuarine and coastal communities along the east coast of the USA.
We also examined reproductive tissue allocation (i.e., the proportion of gonad weight to total body weight) in all three crabs to explore
possible differences in infected versus uninfected crabs. We found three parasite taxa infecting H. sanguineus and four taxa infecting
mud crabs, including a rhizocephalan castrator (Loxothylacus panopaei) parasitizing E. depressus. Moreover, we documented
a significant negative relationship between parasite escape and time for H. sanguineus, including a new 2015 record of a native
microphallid trematode. Altogether, there was no significant difference in taxonomic richness among the crab species. Across parasite taxa,
H. sanguineus demonstrated significantly lower infection prevalence compared to P. herbstii; yet a multivariate analysis
of taxa-specific prevalence demonstrated no significant differences among crabs. Finally, infected P. herbstii had the highest
proportion of gonad weight to total body weight. Our study finds some evidence for lower infection prevalence in the non-native versus
the native hosts. However, we also demonstrate that parasite escape can lessen with time. Our work has implications for the understanding
of the potential influence parasites may have on the future success of NIS in introduced regions.
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Nelson A.F. Miranda, G. John Measey, Nasreen Peer, Jacqueline L. Raw, Renzo Perissinotto and Christopher C. Appleton
Shell crushing resistance of alien and native thiarid gastropods to predatory crabs in South Africa
(pp 303–311)
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The successful invasion of freshwater and coastal lakes of South Africa by the recently introduced thiarid snail Tarebia granifera
may be due in part to release from predatory pressure. This study aimed to determine the comparative vulnerability of T. granifera
and the widespread native aquatic thiarid Melanoides tuberculata to predation. These species also account for many thiarid invasions
in the Americas, Europe and parts of Africa. We quantified the shell crushing resistance of these snails, as well as the maximal shell crushing
capability of native freshwater crab predators, Potamonautes sidneyi and P. perlatus. Using an Instron isometric transducer,
we showed that Tarebia granifera shells were significantly stronger than Melanoides shells, and exceeded the crushing strength
we documented for both potential predatory crabs. The greater shell strength of Tarebia granifera was due to shape, sculpture and thickness
characteristics. Shell strength of Melanoides, however, remained within the range of crushing strength of their potential predators.
Assuming crushing to be the main form of crab predation on snails, we inferred T. granifera to be less vulnerable to durophagous attack
and that their population growth is thus not limited by predation pressure.
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Paul H. Evangelista, Nicholas E. Young, Pamela J. Schofield and Catherine S. Jarnevich
Modeling suitable habitat of invasive red lionfish Pterois volitans (Linnaeus, 1758) in North and South America’s coastal waters
(pp 313–326)
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We used two common correlative species-distribution models to predict suitable habitat of invasive red lionfish Pterois volitans (Linnaeus, 1758)
in the western Atlantic and eastern Pacific Oceans. The Generalized Linear Model (GLM) and the Maximum Entropy (Maxent) model were applied using
the Software for Assisted Habitat Modeling. We compared models developed using native occurrences, using non-native occurrences, and using both
native and non-native occurrences. Models were trained using occurrence data collected before 2010 and evaluated with occurrence data collected
from the invaded range during or after 2010. We considered a total of 22 marine environmental variables. Models built with non-native only or both
native and non-native occurrence data outperformed those that used only native occurrences. Evaluation metrics based on the independent test
data were highest for models that used both native and non-native occurrences. Bathymetry was the strongest environmental predictor for all models
and showed increasing suitability as ocean floor depth decreased, with salinity ranking the second strongest predictor for models that used native
and both native and non-native occurrences, indicating low habitat suitability for salinities < 30. Our model results also suggest that red lionfish
could continue to invade southern latitudes in the western Atlantic Ocean and may establish localized populations in the eastern Pacific Ocean.
We reiterate the importance in the choice of the training data source (native, non-native, or native/non-native) used to develop correlative species
distribution models for invasive species.
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Meagan N. Schrandt, Laura C. Stone, Brian Klimek, Saara Mäkelin, Kenneth L. Heck Jr., Johanna Mattila and Heidi Herlevi
A laboratory study of potential effects of the invasive round goby on nearshore fauna of the Baltic Sea
(pp 327–335)
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In the Baltic Sea, species diversity is relatively low and the introduction of new predator species can have large direct
and indirect impacts on native species – both prey and potential competitors. The alien round goby Neogobius melanostomus
Pallas, 1811 was introduced to the Baltic Sea in the early 1990s and is now well-established. We examined the feeding habits
of male round gobies from the Åland Islands, Finland, where round gobies were first recorded in 2011. Specifically, we tested
whether small round gobies (≤165 mm TL) showed size and/or species preferences (using Manly’s selectivity index) for two abundant
bivalve prey items, the blue mussel Mytilus trossulus Gould, 1850 and the Baltic clam Macoma balthica Linnaeus, 1758.
When offered two sizes of clams, small round gobies did not show a prey preference. When offered two sizes of mussels, round gobies
selected for small mussels (6 – 9 mm) and against large (10 – 13 mm) mussels. When offered both bivalve species and sizes simultaneously
(four prey options), round gobies selected for small blue mussels and against large clams. Combined, these results suggest that small
round gobies will selectively feed on the preferred prey if available and if not, their feeding will reflect the availability of various
prey items in the environment. In addition, round gobies consumed small (≤ 38 mm TL) individuals of the native flounder
Platichthys flesus Linnaeus, 1758. Round goby and flounder have the potential to overlap in habitat use and previous literature
has suggested a diet overlap between the two; however, this is the first evidence of direct predation on flounder by round gobies.
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Vanessa Y. Rubio, Melissa A. Gibbs, Kirsten A. Work and Clifford E. Bryan
Abundant feces from an exotic armored catfish, Pterygoplichthys disjunctivus (Weber, 1991), create nutrient hotspots and promote algal growth in a Florida spring
(pp 337–350)
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Florida springs are relatively unique, stable systems that have experienced increasing and synergistic threats from reductions in water flow,
nutrient additions, and invasions of exotic species. The purpose of this study was to evaluate the effects of the egesta of one common exotic
loricariid catfish species on nutrient availability and periphyton growth in a central Florida spring. Pterygoplichthys disjunctivus
produces copious feces that, unlike excreted nutrients, continue to contribute to nutrient loading when the fish are not present. Fecal abundance,
measured using photographs of randomly distributed quadrats, was found to be high in the spring run (total estimates for the spring run averaged
6.1 × 105 cm3 feces). We measured extractable fecal nutrients (N-NO3-, P-PO43-) from feces collected both
from the guts of live fish and from the spring benthos, and leaching rates of nutrients from feces in laboratory flumes. We also measured direct
algal growth of feces incubated in nutrient broth and the potential of fecal nutrients to stimulate algal growth downstream in arrays deployed in situ.
We found that although each fecal sample leached minute quantities of nutrients, the total quantity of nutrients released in the spring run from local
accumulations of feces was substantial. Furthermore, even the relatively small quantities of nutrients released from fecal material from one fish were
sufficient to increase algal growth in the in situ experimental arrays. Leachate from P. disjunctivus fecal deposition could create transient
biogeochemical hotspots lasting considerably longer than those described for excreta. Although the contributions of the extractable fecal nutrients
were small relative to the overall nutrient load to the spring (TKN = 0.18–3.64%, P-PO43- = 2.78–22.2%), these fecal hotspots
typically occurred in low-flow areas with structure where algae tend to accumulate and nutrient influx of spring water is slow. Therefore, it is
likely that P. disjunctivus fecal leachate significantly alters nutrient availability for algae in this spring system.
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