Special Issue:
Behaviour in Aquatic Invasions
published September 2019
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Edited by:
Kit Magellan, University of Battambang, Cambodia
Amy Deacon, The University of the West Indies, Trinidad and Tobago
Marian Wong, University of Wollongong, Australia
and
Mhairi Alexander, University of the West of Scotland, UK
Papers in this Special Issue explore how behaviour contributes to invasion success;
native species’ behavioural strategies that reduce the impacts of invasions; how knowledge of behaviour can enhance management of invasive species;
and potential effects of climate change on the behavioural impacts of aquatic invasive species.
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Editorial |
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Kit Magellan, Mhairi Alexander, Amy Deacon and Marian Wong
Behaviour and Aquatic Invasions in the 21st Century: Progress, Trends and Future Research
(pp 412–416)
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Research articles |
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Edward P. Levri, Rebecca Luft and Xiaosong Li
Predator detection and a possible dispersal behavior of the invasive New Zealand mud snail, Potamopyrgus antipodarum (Gray, 1843)
(pp 417-432)
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Behavior can play a large role in invasion success. Of particular importance may be the ability of an invader to detect and respond
to unfamiliar potential predators. We examined a behavior related to dispersal in populations of the New Zealand mud snail
(Potamopyrgus antipodarum) in response to chemical cues from crayfish and piscine predators. Populations of the snail isolated
from North America and its native New Zealand were used in two separate experiments. In both experiments, groups of snails were placed
in water either with or without predator cues, and the number of snails found floating attached to the surface tension of the water after
ten minutes was noted. In the first experiment, a crayfish odor cue was used (from Procambarus clarkii), and, in the second, two fish,
blacknose dace (Rhinichthys atratulus), and separately zebrafish (Danio rerio), were used to provide the chemical cues.
In both experiments there was significant variation among populations in the proportion of snails that exhibited the floating behavior,
with native populations tending to exhibit less floating behavior. The snails generally increased floating behavior in response to both
crayfish and blacknose dace but not to zebrafish. In addition, we found no differences between populations of snails in their response
to predator cues. Surprisingly, we also found that there were differences in floating proportions between populations of the same invasive
clonal genotypes. These results suggest this behavior, which may be related to dispersal within water bodies, may be important in partially
explaining the invasion success of the most common invasive clones in North America. |
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Natasha Kruger, John Measey, Anthony Herrel and Jean Secondi
Anti-predator strategies of the invasive African clawed frog, Xenopus laevis, to native and invasive predators in western France
(pp 433-443)
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When species are translocated to a novel environment, individuals become exposed to new predators against which they may not express
very efficient defences at least at an initial stage. The strength of anti-predator defence is an important parameter that may
determine the ability of local communities to control the expansion of invasive populations. The African clawed frog,
Xenopus laevis, is a globally invasive amphibian that has successfully established invasive populations on four continents.
In its invasive distribution in western France, X. laevis encounters novel aquatic predators. Some may be related
to the predators in the native range but others may belong to different taxonomic groups and not be functionally or ecologically
equivalent. We tested whether naïve X. laevis tadpoles from the invasive French population exhibit anti-predator response
to local predators, and whether the response depends on the degree of relatedness with predators encountered in the native range
of the frog, or whether individuals may express generic neophobia to any cue they are not familiar with. We exposed naïve lab-reared
tadpoles to a native non-predatory water snail, Planorbarius corneus, a native predatory beetle, Dytiscus dimidiatus,
and an invasive predatory crayfish, Procambarus clarkii. We found that X. laevis tadpoles innately reduce their
activity when exposed to beetle and crayfish stimulus cues, but not to snails. Reducing activity can decrease the probability
of being detected by predators. This demonstrates that invasive tadpoles respond to known and novel predators regardless
of the evolutionary history. Whether the produced response is always effective against a totally novel predator remains
to be tested. |
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Ming-Feng Chuang, Minjee Choe, Hakyung Kang, Amaël Borzée, Ajoung Kim, Sera Kwon, Musung Sung and Yikweon Jang
Microhabitat preference in American bullfrog tadpoles (Lithobates catesbeianus) in relation to predation pressure (pp 444-457)
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Predation risk is among the key forces driving the evolution of escape behaviours and related phenotypes. Successful avoidance of predators results in increased survival rate and fitness.
The behavioural response of individuals under predation pressure has been comparatively well studied, however, most studies focus on specific escape behaviours and not on behavioural plasticity.
The American bullfrog (Lithobates catesbeianus) has been an invasive species in the Republic of Korea since the 1970s and has a negative impact on local species. Here, we evaluated
the functions of microhabitat preference and behavioural plasticity in L. catesbeianus tadpoles through manipulative experiments. In a first experiment, we placed wild-caught tadpoles
with a local predatory fish (Channa argus) into one of three microhabitat treatments: non-vegetated, submerged vegetation, or floating vegetation. The survival rate of tadpoles with submerged
vegetation was significantly higher than that in the non-vegetated microhabitat. In contrast, the survival rates of tadpoles with floating vegetation was not significantly different from the two other
treatments. In the habitat preference experiment, “unhurt” and “wounded” wild-caught tadpoles were given a choice between the three microhabitat treatments. Both types of tadpoles preferentially selected
the submerged vegetation microhabitat compared to the non-vegetated microhabitat. In contrast, only wounded tadpoles significantly preferred floating vegetation over non-vegetated microhabitats.
We conclude that L. catesbeianus tadpoles prefer vegetated microhabitats, and especially submerged vegetation. Furthermore, L. catesbeianus tadpoles can adjust their anti-predatory
behaviour according to previous experience, and thus demonstrate behavioural plasticity by using microhabitats that they do not use in the absence of predators. |
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Matthew J. Greenlees and Richard Shine
Ontogenetic shift in toxicity of invasive cane toads facilitates learned avoidance by native predators
(pp 458-464)
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The ecological impact of an invasive species depends upon many factors. Our experimental studies show that exposure to the tadpoles
of cane toads (containing less toxin), Rhinella marina, induces predatory native frogs, Litoria dahlii, to avoid metamorph cane toads
(containing comparatively more toxin) in subsequent encounters. The frog’s ability to generalise its aversion response from tadpoles to metamorphs,
coupled with the toad’s strong ontogenetic variation in toxin content, which reflects its multiphasic life history, thus play critical roles
in enabling native predatory frogs to survive the cane toad invasion. |
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Tomas Brodin, Sean Fogarty, Andrew Sih and Julien Cote
Personality-dependent survival of the invasive mosquitofish: being social can be deadly (pp 465-477)
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Mosquitofish (Gambusia affinis) are a widespread, invasive species that frequently colonize habitats where they might encounter novel predators.
Earlier work showed that asocial mosquitofish disperse more readily than social fish. Initial colonists to newly invaded, low density sites should thus
be relatively asocial. Here, we tested the hypothesis that asocial mosquitofish should survive better than social fish when exposed to predators at low
mosquitofish density. We used standardized behavioural assays to quantify the individual behavioral type (boldness, sociability, activity, exploratory tendency)
of 224 mosquitofish, and then exposed them to predators in small groups. As predicted, asocial individuals survived exposure to predators better than social individuals.
In addition, while body mass per se did not affect survival, males survived predators better than females. Overall, this study provides an early corroboration
of the general prediction that behavioural types that disperse more readily might also be better at coping with predators at low density. |
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Amy E. Deacon, Susanta K. Ghosh, Anuradha Bhat and Anne E. Magurran
Predatory behaviour of female guppies (Poecilia reticulata) in a mosquito control context: the importance of social and habitat factors (pp 478-489)
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It is vital to consider behaviour when selecting an appropriate biological control agent, as behaviour can affect both the likelihood of the agent successfully
controlling the target organism, and the chance of inadvertent negative effects on native ecosystems. Guppies, Poecilia reticulata, have been introduced widely
outside of their native range for mosquito control, yet very little is known about their feeding decisions when more than one prey species is present, and how these
decisions are mediated by social and physical aspects of the foraging environment. We investigated female guppy foraging behaviour in a two-prey system
(Anopheles and Culex mosquito larvae). When feeding alone, female guppies displayed a preference for Culex larvae. However, the extent of preference
was significantly affected by both the presence of conspecifics and cover, in a non-additive manner. This suggests that the presence of alternative prey will influence
the effectiveness of guppies in biological control, as well as their potential ecological impact. The exact nature of this influence depends on the interaction between
social and habitat factors. |
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Morelia Camacho-Cervantes, Vianey Palomera-Hernadez and Constantino Macías García
Foraging behaviour of a native topminnow when shoaling with invaders
(pp 490-501)
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Individuals join a group when the benefits of doing so outweigh the disadvantages. Typically, groups are composed by individuals of the same species,
as sharing the benefits with relatives dilutes the disadvantages of being part of a group. However, mixed species shoals do occur in the wild.
The Mexican Goodeidae are a clade of viviparous topminnows endemic to Central Mexico. Survival of most species is under threat, with some already extinct in nature.
Causes of decline include the introduction of exotic species. These include viviparous topminnows of the Family Poeciliidae, such as the Trinidadian guppy
(Poecilia reticulata Peters, 1859), as well as the twospot- (Pseudoxiphophorus bimaculatus Heckel, 1848) and porthole livebearer
(Poeciliopsis gracilis Heckel, 1848), both native to the Mexican costal slopes but frequently translocated to the central Highlands. Guppies and goodeids
readily associate with each other, and guppies entering such associations improve their foraging efficiency. This has been hailed as evidence of a social skill
that favours the establishment of viable guppy populations across the globe. It is as yet unknown whether this improvement in guppy foraging efficiency comes
at a cost for the interacting goodeids. Here, we investigated how sharing resources with poeciliid invaders affects the foraging efficiency of the goodeid twoline skiffia
(Skiffia bilineata Bean, 1887). We measured the time it took them to locate food and the total time spent eating when part of a mixed species shoal that included
either a species of exotic poeciliids (guppies, twospot- or porthole livebearers), or another goodeid (Goodea atripinnis). We also measured foraging efficiency of twoline
skiffia in single-species (conspecific) shoals as a control. We found that the total foraging time of twoline skiffias is reduced when shoaling with guppies and twospot
livebearers compared to when associating with conspecifics. We provide evidence to support the idea that native species’ fitness is reduced when invaders with similar
ecological requirements occupy their habitats. |
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Kit Magellan, Timothy C. Bonebrake and David Dudgeon
Temperature effects on exploratory behaviour and learning ability of invasive mosquitofish (pp 502-517)
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The success of an invasive species depends on several factors. One of these is behavioural flexibility, which may promote invasions by allowing invaders
to exploit novel foods, habitats and shelters. As behaviour can change rapidly it is an ideal first response to environmental change, including introduction
and spread into a new habitat. Behaviour can be modified by learning, thus facilitating adjustment of existing behaviours to accommodate environmental conditions.
Climate change is also likely to promote the introduction, establishment, and spread of aquatic invasive species. Temperature in particular is vitally important
for ectotherms, directly affecting metabolic rates with consequent changes in behaviour. We evaluated the effects of temperature on the exploration tendency and
learning ability of the western mosquitofish, Gambusia affinis. After acclimating fish to warm, medium and cool temperatures we showed that behaviour
is affected by temperature, and overall warm-acclimated fish outperformed lower temperature fish. Mosquitofish showed remarkably rapid learning ability exhibiting
a clear change within just three days. These effects also differed by fish sex and size. In general, larger females and smaller males were quicker to approach
a novel object, while smaller females and larger males were quicker to find food. Warm-acclimated fish learned to adjust to a novel object more quickly and
warm-acclimated males showed a faster response to food. In contrast, neither males nor females acclimated to warm temperatures appeared to learn to find the food
and it was cool-acclimated females who were both faster to find food and showed the greatest improvement over time. Nonetheless, on both local and global scales,
mosquitofishes’ rapid learning ability and behavioural flexibility, which allows them to adjust to changing temperatures, is likely to augment their success
as invaders in a warming world. |
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Stephanie Cerato, Andrew R. Davis, Daniel Coleman and Marian Y.L. Wong
Reversal of competitive dominance between invasive and native freshwater crayfish species under near-future elevated water temperature
(pp 518-530)
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Biological invasions are a major cause of biodiversity loss and, coupled with climate change, will likely have detrimental impacts
for native species and the functioning of ecosystems. To mitigate such impacts, it is important to elucidate the behavioural mechanisms
underpinning interactions between invasive and native species. Here we examined how competitive interactions between invasive and native
species are modified under conditions of near-future elevated water temperature using freshwater crayfish as a model system. Contest
experiments between the native Euastacus spinifer and invasive Cherax destructor revealed that the competitive advantage
of E. spinifer at current maximum temperatures (22 °C) was reversed at elevated near-future temperatures (26 °C), after controlling
for relative body size. In addition, the native crayfish spent twice as long motionless at 26 °C than C. destructor, consistent with
physiological challenges underpinning this competitive reversal. Most alarmingly, E. spinifer experienced significant mortality
after fighting C. destructor, particularly at 26 °C. Mortality usually ensued two days post-contest even when E. spinifer had won.
Mortality was rare when fighting conspecifics. Together, these results suggest that while E. spinifer is more likely to win contests
under current conditions, it could suffer considerable impacts if climate change and the spread of invasive C. destructor continue unabated. |
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Emelia Myles-Gonzalez, Adrienne McLean and Robert McLaughlin
Is there an impact of behaviour on trapping migratory invasive sea lamprey (Petromyzon marinus)?
(pp 531-550)
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Trapping is used to control a variety of invasive species; however, trap encounter and entrance can vary between- and within-species depending
on consistent individual differences in behaviour. We develop a framework for testing how consistent differences in behaviour might be related
to trapping a migratory species. We tested whether adult migrating sea lamprey display consistent individual differences in two behaviours,
boldness (measured as exit time from an enclosure) and activity (measured as the proportion of time spent moving), and whether these differences
were related to trap entrance or timing. We predicted that bolder and more active individuals would migrate sooner and be more likely to be caught
in a trap. We also predicted that early in the migration phenology, trapped individuals would not differ in behaviour from untrapped individuals,
but later in the migration phenology, trapped individuals would be bolder and more active. We determined that sea lamprey exhibit consistent
individual differences in boldness and activity but found no evidence that these differences were related to migratory timing or trap capture A
greater understanding of how individual differences in behaviour influence trapping could help improve the management of invasive species
by allowing for a better estimation of population size and provide insight into how to target different behavioural types. |
Book review |
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Daniel Sol and Judith S. Weis
Highlights and Insights from “Biological Invasions and Animal Behaviour"
(pp 551-565)
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Although behavior has long been considered central in understanding the causes and consequences of animal invasions,
“Biological Invasions and Animal Behaviour” represents the first attempt to summarize the major advances in a single book.
The book is a clear demonstration that behavior influences almost all facets of the invasion process. However, a common theme of the book
is that general rules are rare. The role of behavior changes through the stages of the invasion process and within each stage can be highly
context-dependent, implying that there may be several ways of being a successful invader. Despite the scarcity of general rules, there are two
recurring generalization that emerge from the book. One is the central importance of behavioral plasticity in facilitating establishment and spread.
The other is the appreciation that behavior is part of a suite of traits closely linked to life history, whose effects on population dynamics vary
as a function of population size and degree of adaptive mismatch. Although aquatic ecologists have largely contributed to developing these ideas,
their research has often been restricted to a few study systems and has mostly neglected mechanisms. Aquatic ecologists have, however, led research
on the impact of invaders, using invasions as “unintended” experiments for examining the consequences of novel species interactions. This research
unambiguously demonstrates that behavior is central to understanding how invaders alter native communities, notably by shaping predator–prey interactions.
We believe that aquatic animals can continue providing research opportunities to further improve our understanding of the role of behavior
in biological invasions, and we hope that “Biological Invasions and Animal Behaviour” may serve to encourage new research avenues. |
Last update: 7 September 2019
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© 2019 Regional Euro-Asian Biological Invasions Centre (REABIC)
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