Volume 16, Issue 3 (2021)
published September 2021
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Lucas H. Gimenez and Antonio Brante
Do non-native sea anemones (Cnidaria: Actiniaria) share a common invasion pattern? – A systematic review
(pp 365–390)
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A number of cnidarian species are known to have become marine invaders across a diversity of regions and habitats, including sea
anemones of the order Actiniaria. Unfortunately, integrative approaches to identify and describe general patterns and likely drivers
of their invasion process have only been of recent interest. The goal of this systematic review is to summarize and categorize
the literature published on non-native populations of sea anemone species and to assess whether these records exhibit a shared common
invasion pattern. A total of 126 articles were analyzed, in which 11 species presented records of suspected non-native populations.
Our results showed that sea anemone invasions date back to at least the late 1890s and new introductions have recently been reported
for different species in the last five years. Some potential biases in the literature were found in relation to species, marine
realms and study approaches. Most study efforts have been focused on a single species (Diadumene lineata), especially
in the Temperate Northern Atlantic. A seemingly common shared pattern was found and described throughout all stages of the invasion
continuum, but more effort should be focused on the less reported/studied species. Transport has mainly been mediated
by human-associated vectors, such as maritime traffic and aquaculture. Newly arrived individuals colonize mostly natural habitats,
although some species thrive in human-made habitats. A diverse array of traits has been associated with the invasion success
of sea anemones, although the two most frequently reported traits in the literature were abiotic tolerance and the reproductive
strategies. Unlike other benthic invaders, the dispersal mechanisms (both primary and secondary spread) and the ecological
or economic consequences produced by non-native sea anemone populations have been little explored and thus need more attention.
We discuss potential ways to reduce some of the gaps and research biases found and thus develop a better understanding
of the invasion ecology of sea anemones. |
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Research articles |
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Agar Montes, Elsa Vázquez, Laura G. Peteiro and Celia Olabarria
Dynamics and processes influencing recruitment of the invasive mussel Xenostrobus securis and the coexisting indigenous Mytilus galloprovincialis in north-western Spain
(pp 391–414)
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The local extent of populations of invasive species is dependent on coupled dispersal–recruitment dynamics and subsequent interactions with the recipient community
and the local environment. In this study several field experiments were conducted in order to investigate the main factors controlling larval supply
(settlement and recruitment time-series), substrate selection (7 different treatments) and post-recruitment mortality (predation exclusion experiment)
of the invasive mussel Xenostrobus securis and the coexisting, commercially important native mussel Mytilus galloprovincialis. The study aimed
to evaluate differences between the two species in spatio-temporal patterns of recruitment along an estuarine gradient in the Ría de Vigo (NW Spain).
Settlement and recruitment of X. securis were coupled to the distribution of the adult populations and were mainly restricted to the innermost part of
the ria, in direct contrast to the patterns displayed by the native M. galloprovincialis. The recruitment period of the invader in the study area lasted
5 months, partly overlapping with that of M. galloprovincialis. Xenostrobus securis larvae did not display a substrate preference, whereas
M. galloprovincialis larvae preferred substrates with the presence of conspecifics. Although predation pressure was greater on M. galloprovincialis
than on the invader, size-dependent predation pressure was observed in both species, suggesting that smaller individuals are more vulnerable to predators.
Density-dependent processes may also account for recruitment density, especially under low predatory pressure. Despite having life-history traits characteristic
of a successful invader, X. securis populations have remained stable since 2012 and are mainly restricted to the inner part of the Ría de Vigo.
This observation suggests that the species spread may be controlled by seasonal dispersal barriers associated with topographic features. |
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Catherine Kilroy, Amy L. Whitehead, Susanna A. Wood, Marcus J. Vandergoes, Paul Lambert and Phil M. Novis
Predicting the potential distribution of the invasive freshwater diatom Lindavia intermedia in New Zealand lakes
(pp 415–442)
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The freshwater diatom Lindavia intermedia is believed to have been recently introduced to New Zealand lakes. Mucilage (“lake snow”) produced
by L. intermedia can block water intakes and/or degrade recreational values. Because nuisance L. intermedia proliferations and lake snow occur
rarely in lakes overseas, the species was not initially recognised as invasive and knowledge of its ecology and threat to New Zealand lakes remains sparse.
We combined distribution data from several sources with an existing dataset of environmental variables linked to ~ 3800 New Zealand lakes (area > 1 ha) and
used a boosted regression trees modelling approach to: (a) describe the environmental niche occupied by L. intermedia; and (b) predict its potential distribution.
The effect of human-mediated spread was incorporated using a binary predictor (road200) indicating the presence or absence of vehicle access. “Niche” models
were developed using absences (non-detections based on a sensitive molecular method) only in lakes with road access, and “spread” models using all absences and
including road200 as a predictor. Lindavia intermedia was observed in 38 lakes, from central North Island to southern South Island, in oligotrophic conditions
(total phosphorus < 0.011 mg L-1, total nitrogen < 0.3 mg
-1) with cool temperatures (mean annual temperature < 11 °C).
All 38 lakes had road access. Likelihood of presence predicted from the combined niche models was lower in North Island lakes (< 1% assessed as vulnerable)
than in the South Island (~ 12.5% vulnerable), highlighting that many additional South Island lakes may be environmentally suitable for L. intermedia.
However, using the spread models, only 46 lakes were assessed as vulnerable nationwide reflecting a lack of road access to most lakes. Lindavia intermedia
was already present in 22 (48%) of the most environmentally suitable lakes with road access. The dataset and models thus implicated humans as important
(but not the only) vectors of this diatom within New Zealand, emphasising the critical role of current New Zealand biosecurity policy for reducing the spread
of freshwater pests. |
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Łukasz Sługocki, Anna Rymaszewska and Lucyna Kirczuk
To fit or to belong: characterization of the non-native invader Eurytemora carolleeae (Copepoda: Calanoida) in the Oder River system (Central Europe)
(pp 443–460)
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The Eurytemora affinis species complex (Copepoda: Calanoida) is widespread in coastal and estuarine waters in the northern
hemisphere. The species Eurytemora carolleeae belongs to this complex. It was recently described and recognized as an invasive
copepod for European waters. Since then, it was found in a few European estuaries. Based on molecular and morphological studies,
we observed that E. carolleeae has expanded into new freshwater habitats in Central Europe. We carried out detailed
morphological analysis for this species which indicates the potential higher stability of the populations in freshwater habitats
compared to brackish waters. Fluctuating asymmetry did not significantly differ between freshwater and brackish water habitats,
but the share of deformed specimens was considerably larger in brackish waters. We also found that season and habitat influenced t
he morphology of Eurytemora. In the molecular analyses, we focused on mitochondrial (COI) as well as nuclear gene markers
(18S rDNA, ITS1-2) in E. carolleeae. In addition, for the first time, we analyzed the cytochrome b gene of the latter species.
A wide distribution of E. carolleeae in the Oder River system in Central Europe indicates that it is a suitable habitat
for the present populations and suggests further expansion of the species into continental waters. |
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Stephanie E. Figary and Kimberly L. Schulz
Spines and surplus: existing inducible defenses and abundant resources may reduce the impacts of Cercopagis pengoi on a likely prey species
(pp 461–481)
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A lack of co-evolved defensive mechanisms can make organisms especially vulnerable to invasive predators. Bosmina longirostris
is an herbivorous zooplankton known to change morphology as an inducible defense mechanism against the native predatory invertebrate
Leptodora kindtii. In 1999, Cercopagis pengoi, another predatory zooplankton, invaded six of the eleven New York Finger Lakes
in which both L. kindtii and B. longirostris co-occur. This created a natural experiment for studying C. pengoi’s
(1) influence on the presence of B. longirostris’ long morphological form, a known inducible defense against predation by native
L. kindtii, (2) consumption rates of B. longirostris using mass-balance equations for several prey preference scenarios,
and (3) overlap with the native predatory cladoceran L. kindtii. B. longirostris densities were lower in the invaded Finger
Lakes and exhibited more long form morphology, with longer percent relative mucro lengths, than in non-invaded lakes (Mann Whitney, p = 0.006).
The percent relative mucro length was positively correlated with predator densities, particularly those of C. pengoi
(Spearman, r = 0.812, p < 0.001), consistent with C. pengoi predation on B. longirostris as a potential driver of this
inducible defense expression. Mass balance calculations estimated predation by C. pengoi could reduce B. longirostris
densities by 10–100% during peak C. pengoi densities if the latter only consumed the former or preferentially selected large
zooplankton from the available prey assemblage. Additionally, C. pengoi and L. kindtii populations overlapped temporally
in the invaded lakes, suggesting that their prey species were abundant enough to support both populations. This study indicates that
(1) B. longirostris likely produce an inducible defense protective against native predators in response to invasive C. pengoi,
and (2) C. pengoi distribution overlaps with L. kindtii in invaded lakes. |
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Ana Dobrović, Ivana Maguire, Marija Boban, Dorotea Grbin and Sandra Hudina
Reproduction dynamics of the marbled crayfish Procambarus virginalis Lyko, 2017 from an anthropogenic lake in northern Croatia
(pp 482–498)
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Despite the growing number of established populations in Europe, the reproduction dynamics of parthenogenetic marbled crayfish,
Procambarus virginalis Lyko, 2017, from populations in the wild is currently understudied. In this study, we performed
a systematic seven-month long monitoring of the reproduction dynamics of marbled crayfish population in an anthropogenic lake
in continental Croatia. Crayfish were caught monthly by applying the baited stick catch method. We recorded pleopodal fecundity
and the number of hatched juveniles in each monthly catch and a random selection of individuals (20 per month) was dissected
to determine the ovarian fecundity. Obtained fecundity parameters were correlated with crayfish size (total length, weight and pleon
size), body condition (Fulton’s condition factor), organosomatic indices (hepatosomatic index: HSI and gonadosomatic index: GSI)
and compared with available literature data on marbled crayfish from laboratory-reared or wild populations. Based on the obtained
data, we identified two potential reproductive peaks in early summer and mid autumn. However, the continuous presence of individuals
with mature ovarian eggs and glair glands throughout almost the entire monitoring period indicates potential reproduction throughout
June to November. Ovarian egg number and number of hatched juveniles was significantly correlated with crayfish size and Fulton’s
condition factor, while GSI exhibited significant variations among analyzed months and was positively correlated with HSI.
The number of hatched juveniles in our study was significantly lower compared to literature data for marbled crayfish
from populations in the wild and laboratory-reared populations. Collected data offer insights into the understudied reproduction
dynamics of marbled crayfish in the wild and represent baseline information for predicting its invasion dynamics and risks of its
further spread in this region. |
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Tomáš Jůza, Petr Blabolil, Daniel Bartoň, Martin Čech, Vladislav Draštík, Jaroslava Frouzová, Michaela Holubová, Henk A.M. Ketelaars, Luboš Kočvara, Jan Kubečka, Milan Muška, Marie Prchalová, Milan Říha, Zuzana Sajdlová, Marek Šmejkal, Michal Tušer, Mojmír Vašek, Lukáš Vejřík, Ivana Vejříková, Arco J. Wagenvoort and Jiří Peterka
Recovery of the ruffe (Gymnocephalus cernua) population after an invasion boom of round goby (Neogobius melanostomus) in De Gijster Lake (the Netherlands)
(pp 499–511)
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Studies dealing with invasive species usually focus on changes caused by invasion, however, natural recovery of the system after
the initial population explosion (boom) has been much less studied. Ruffe dominated the benthic fish community in De Gijster Lake
(Biesbosch National Park, the Netherlands) before a round goby invasion indicated by catches in both seines and gillnets. In 2012,
the round goby was found for the first time and it was observed to undergo a boom in 2014, when ruffe almost completely disappeared.
Nevertheless, gillnet sampling in 2016 indicated a decreasing trend in the number of round gobies and an increase in ruffe. These
changes were confirmed during monitoring in 2019, when the density of round goby decreased seven times in comparison with 2014
indicated both in seine and gillnet catches. At the same time, the density of ruffe increased six times in gillnets and from zero
to 396 ind/ha in seine catches. Densities of both species were clearly negatively correlated and the approximate theoretical
threshold-values for coexistence of both species were estimated as 750 ind/ha in the littoral zone and 120–140 ind/1000 m²
of standard CEN gillnets. Our results show the recovery of a native fish population after a natural decline of the invasive species
density, which could be important when considering the management of invasive species. |
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Pamela J. Schofield, Quenton M. Tuckett, Daniel H. Slone, Kristen M. Reaver and Jeffrey E. Hill
Invasion frustration: can biotic resistance explain the small geographic range of non-native croaking gourami Trichopsis vittata (Cuvier, 1831) in Florida, USA?
(pp 512–526)
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Croaking gourami Trichopsis vittata is a non-native fish species that has maintained a reproducing population in Florida, USA, since at least the 1970s.
However, unlike most other non-native fishes in Florida, T. vittata has not spread beyond its very small (ca. 5 km²) range. We suspected the inability
of T. vittata to colonize new habitats may be due to biotic resistance by the native eastern mosquitofish Gambusia holbrooki. In laboratory experiments,
we show that G. holbrooki causes physical damage to T. vittata and that T. vittata’s growth is reduced in the presence of G. holbrooki.
While the effects of G. holbrooki on T. vittata were sub-lethal, they were severe enough to hamper its growth and could affect recruitment in the wild.
These results support the hypothesis that small non-native fishes may be excluded from establishment or may only establish small ranges due to pressure from
G. holbrooki. Biotic resistance may reduce invasion success and thus consideration of species interactions is useful for natural resource managers trying
to evaluate the potential risk of new invaders. |
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James E. Whitney, Joshua A. Holloway, Jake T. Wright, Kali L. Boroughs, Robin E. Goodreau, Ashton L. McManis, Adam B. Pistorius, Deaundre K. Puritty, Michael A. Ramirez and Rachel A. Styers
Assessing the invasion history and contemporary diet of nonnative redear sunfish (Lepomis microlophus Günther, 1859) in an ecotonal riverscape
(pp 527–541)
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The redear sunfish (Lepomis microlophus Günther, 1859) is widely-introduced as a sportfish in the United States and globally. The redear sunfish
can become invasive when introduced to lentic waterbodies, but the outcome of lotic introductions has received less attention. As such, we evaluated trends
in the distribution and abundance of introduced redear sunfish throughout the Spring River subbasin (SRS) of southeastern Kansas during 1962–2019 using five
separate datasets. We also examined contemporary diet of the redear sunfish in the SRS during 2018 at sites where it was most abundant to determine if its diet
differed from the native range. The SRS included low-velocity, turbid streams draining the Cherokee Lowlands and Osage Cuestas physiographic regions
and high-velocity, clear streams flowing through the Ozark Plateau. Streams across all physiographic regions in the SRS are ill-suited to the Redear Sunfish,
which prefers low water velocity coupled with high water clarity. We found that the redear sunfish exhibited a restricted distribution with low relative abundance
in the SRS throughout the entire study period. Furthermore, its contemporary diet was dominated by non-biting midge larvae (Chironomidae), seed shrimp (Ostracoda),
fingernail clams (Sphaeriidae), and snails (Gastropoda), similar to its diet in the native range. The inability of redear sunfish to achieve widespread prevalence
in the SRS at least 50 years after introduction likely stems from habitat in the SRS being a poor match to its niche requirements. However, future environmental
alterations resulting from human activity and climate change (e.g., dewatering and lentification in streams of the Ozark Plateau) could make conditions
in the SRS more suitable for redear sunfish. As such, continued monitoring will be necessary to determine if the prevalence of the redear sunfish
in the SRS of Kansas changes in the future. |
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Charles A. Drost, Jeffrey E. Lovich, Philip C. Rosen, Matthew Malone and Steven D. Garber
Non-native pond sliders cause long-term decline of native Sonora mud turtles: a 33-year before-after study in an undisturbed natural environment
(pp 542–570)
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Using a before-after study design in a stable, largely undisturbed pond habitat and a dataset spanning 33 years, we document and describe the decline of native
Sonora mud turtles (Kinosternon sonoriense) after the introduction of non-native pond sliders (Trachemys scripta). The Sonora mud turtle population
in Montezuma Well in central Arizona, USA, declined to less than 25% of previous numbers, from 372 ± 64 in 1983 to 80 ± 21 in 2011. We trapped and removed
the non-native turtles between 2007 and 2012 and after removal of the non-natives, the Sonora mud turtle population increased to 139 ± 34 in 2015.
The native turtles also significantly increased basking activity after removal of the non-natives, paralleling results of small-scale mesocosm studies showing
that pond sliders negatively affect basking rates of native turtle species. Reproductive rates of female Sonora mud turtles (numbers of females with eggs)
were lower during the period of peak non-native turtle abundance, and increased after removal of the non-native turtles. We hypothesize that the reduction
in effective reproductive rate links interference competition (reflected in reduced basking rates) to the long-term decline of the native mud turtles.
Results from the undisturbed natural system of Montezuma Well provide new insights on the overall occurrence, magnitude, and mechanisms of negative effects
of introduced pond sliders on native turtle species. Sonora mud turtles are very different in their morphology, behavior, and ecology from pond sliders
and from native turtles in other studies, suggesting that impacts of non-native pond sliders are more pervasive than previously thought. |
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