Download How do native species respond to invaders? Mechanistic and trait

Biol Invasions
DOI 10.1007/s10530-015-0874-7
PERSPECTIVES AND PARADIGMS
How do native species respond to invaders? Mechanistic
and trait-based perspectives
Katherine Berthon
Received: 28 July 2014 / Accepted: 6 March 2015
Ó Springer International Publishing Switzerland 2015
Abstract Adaptive responses of native species are
important in enabling their persistence in the face of
unprecedented biotic exchange. In the present paper I
discuss how native species respond to invasive species
both from a mechanistic and trait-based perspective.
An earlier review by Strauss et al. (Ecol Lett
9:357–374, 2006) discussed a conceptual model of
native species evolution in which the likelihood of an
evolutionary response to an invader is dependent upon
the strength of the selective pressure imposed (degree
of variation in fitness between genotypes) and the
adaptive capacity of the native (extent of pre-adaptation or genetic diversity). I aim to update and build
upon this framework in light of new information on the
interaction of phenotypic plasticity and evolutionary
processes in adaptive responses of native species.
Phenotypic plasticity can be a precursor to or an
inhibitor of evolutionary responses and, under conditions of strong selection, phenotypic plasticity may
enable adaptation where natives have a low evolutionary capacity. Based on current evidence, it is likely
that phenotypic plasticity is the first front in native
species adaptation, after which genetic changes occur
via a genetic accommodation mechanism. Lastly, I
K. Berthon
Department of Biological Sciences, Macquarie
University, North Ryde, NSW 2109, Australia
K. Berthon (&)
79 Devon Street, North Epping, NSW 2121, Australia
e-mail: [email protected]
review the literature on behavioural, morphological,
physiological and life history trait changes of responding native species in light of this framework.
Knowledge of the genetic and physiological underpinnings of adaptive responses in native species is
limited and would aid in distinguishing the contributions of phenotypic plasticity and evolutionary change
in future studies.
Keywords Evolution Invasion Native species Phenotypic plasticity Response
Introduction
Human activities have led to unprecedented rates of
biotic exchange between previously isolated ecological communities (Strauss et al. 2006; Mooney
and Cleland 2001). This has generated novel species
combinations, enabling interaction of species with no
shared evolutionary history (Mooney and Cleland
2001). In many cases, these altered interactions also
generate changes in environmental conditions with
ramifications for ecosystem function (Wright et al.
2012). Adaptation of exotic species to novel environments and new species interactions is well documented, and much research effort has been placed in
understanding exotic traits or conditions that facilitate
or prevent invasion (reviewed in Mooney and Cleland
2001; Strayer et al. 2006).
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K. Berthon
The research interest in invasive species is fuelled
by the (often negative) impacts of exotics on native
species persistence (Rodriguez 2006). Invasive species impose novel selection pressures on their recipient community through both direct interactions
with native species [predation (Freeman and Byers
2006; Carlsson et al. 2009; Fisk et al. 2007; Latta et al.
2007; Nunes et al. 2014), herbivory (e.g. Lau 2008),
competition (Oduor 2013; Lau 2008; Lankau 2012) or
parasitism (e.g. Patten and Campbell 1998)], and
indirect impacts on ecosystem processes (e.g. Wright
et al. 2012) or trophic cascades (e.g. Knapp et al. 2001)
(Fig. 1). Further, invasive species can cause changes
in the distribution and abundance of resources (Reusch
and Williams 1998) which may provide novel opportunities for native species (Carroll et al. 1997;
Rodriguez 2006). For example, an invasive species
may itself become a valuable food resource for a
native predator (King et al. 2006) or herbivore (Carroll
et al. 1998). The selection pressure exerted by an
invasive species is thus dependent on its trophic
relationship to the native species (Strauss et al. 2006).
Native species that adapt to mitigate the negative
impacts of invasive species or exploit the novel
opportunities they provide will have a fitness advantage over those which do not (Carlsson et al. 2009).
Failure to adapt to the negative impacts of an invasive
species is a major threat to native species persistence,
globally (Rodriguez 2006). However, there is an
increasing body of evidence showing that native
species are able to respond adaptively to the presence
of invaders either through plastic phenotypic responses (Ortega et al. 2013; Latta et al. 2007) or evolutionary processes (Oduor 2013; e.g. Goergen et al. 2011).
A large number of these associations have been found
when investigating insect pests on introduced crop
species (e.g. Zimmerman 1960) and thus have economic as well as ecological implications.
Several studies have reviewed evidence for species
adaptations generally (Strauss et al. 2006), as well as
within the context of individual ecological interactions
(Carlsson et al. 2009; Strauss et al. 2006), or with a
focus on particular taxa (Bezemer et al. 2014; Oduor
2013; Shine 2012). These studies highlight four main
aspects of native species biology that are altered under
selection from invaders: behaviour, morphology,
physiology and life history traits. However, a full
synthesis of how these traits change across trophic
relationships has not yet been performed. Further,
previous studies have focused on evolutionary processes as mechanisms for native species adaptation to
invaders. While such reviews do discuss plasticity and
its contribution to evolution (e.g. Strauss et al. 2006),
plasticity, particularly maladaptive changes, has not
Invader Impact
(A)
(B)
Direct
Novel
Competitor
Novel
Predator
Indirect
Novel
Prey
Trophic
Interaction
Environment
Modification
(C)
Life History
Physiological
Behavioural
Morphological
Nov. Competitor
15
7
4
2
Nov. Predator
7
7
16
9
Fig. 1 Selection imposed by invasive species. An invasive
species imposes selection pressure on its recipient community
either a directly through interaction with native species or
b indirectly through alteration of trophic linkages between
species or changes in environmental conditions. c Four aspects
of a species’ biology are impacted: life history, physiology,
behaviour and morphology. The number of cases for each trait
123
Nov. Prey
7
2
12
7
Trophic
Env. Mod.
1
1
1
change under each context are given based on analysis of 77
cases compiled from the literature. No references were found for
native species altering their behaviour or morphology in the face
of a novel competitor. Environmental effects were only found
for morphological traits. The terms ‘‘predator’’ and ‘‘prey’’ are
used generically and include herbivore-plant interactions.
Further details are given in Table 1
Mechanistic and trait-based perspectives
been explicitly incorporated into models of native
adaptation. Considering recent advances in our understanding of the contribution of phenotypic plasticity to evolution (Schlichting and Wund 2014;
Ghalambor et al. 2007a; Trussell and Smith 2000;
Nylin et al. 2014), a mechanistic understanding of how
native species respond adaptively to invaders should
incorporate phenotypically plastic responses.
In the present review, I aim to generate a comprehensive mechanistic understanding of how native
species respond to invasive species. I begin by
building upon a conceptual framework by Strauss
et al. (2006) which outlines the conditions under which
native species adaptation occurs (Fig. 2) and relate
this to different types of selection pressure imposed by
invaders (Fig. 1). Using this framework I discuss the
interaction between phenotypic plasticity and evolutionary processes in adaptive responses of natives to
invaders. I then review the literature on behavioural,
morphological, physiological and life history trait
changes of responding native species in light of this
framework. This review is not exhaustive, but aims to
synthesise information to cover all factors affecting
how native species respond to invasive species.
Mechanisms for adaptation: phenotypic plasticity
or evolution?
Selective pressure and capacity for evolution
Selecve Impact of Invader
(trophic interacons, resource distribuon changes)
Capacity for Evoluon
(genec diversity, pre-adaptaon)
Low
High
a
Minimal
Effect
c
Phenotypic
b
Stable
d
Plascity
(Co-)Evoluon
Phenotype
High
Fig. 2 How native species adapt to invaders. The likelihood
that a native species will adaptively respond to an invasive
species is dependent on the strength and direction of selection
imposed by the invader (i.e. the degree to which genotypes are
differentially affected), and the capacity of the native for
evolution. Four, non-mutually exclusive scenarios are possible.
a If the ecological impact of the invader is weak and the adaptive
capacity of the native species is low, the invasive will exert little
selective pressure on native species primarily through lack of
interaction. b Even if the native species has a large capacity for
evolution, i.e. a high genetic diversity, pre-adaptation to the
invader may result in minimal change in the native phenotype.
c Under strong selection pressure and low adaptation capacity,
native species are only able to respond using phenotypic
plasticity. d Native species with a high capacity for evolution
can respond adaptively to high selection pressure. This
interaction may be two-sided if the invasive species is similarly
capable of adapting. If the native species is able to adapt
effectively, and the invader selection remains constant, the
impact of the invader will decrease over time (red arrow).
However, if the selection pressure is too strong, or the induced
phenotype is initially maladaptive, the native species population
may decline too rapidly to enable adaptation (blue arrow).
Figure modified from Strauss et al. (2006)
Native species may respond to the novel selection
pressures imposed by invasive species using already
existing phenotypes in relevant traits (Strauss et al.
2006). For example, species that respond to broad cues
for anti-predator response may be more likely to
respond to a novel predator (Nunes et al. 2014). The
presence of such pre-adaptations to invader interactions is more common when the two species share
some evolutionary history [e.g. through the presence
of a phylogenetically similar host plant in the recipient
ecosystem (Bezemer et al. 2014; Tuda et al. 2014), or
an evolutionary history of exposure to other toxic prey
(Llewelyn et al. 2011)]. In these instances, the
selective impact of an invader may be small and the
invader may readily integrate into the ecosystem
without much change in trait frequencies of the native
(Strauss et al. 2006; Figs. 2b, 3a). Alternatively, such
pre-adaptations may hinder establishment of an
invader through competitive exclusion or predation
(Levine et al. 2004).
In many cases, invasive species represent novel
selection pressures for which species are not preadapted (Cox 2004; Strauss et al. 2006). Where the
native species possesses inducible or heritable variation
in traits that are involved in interaction with invaders,
selective pressures imposed by invaders may result in
differential fitness of different genotypes and consequently evolution (Fig. 2d; Strauss et al. 2006). The
strength of the selection pressure is dependent on
trophic relationships (e.g. direct predation risk versus
optional novel prey [Robbins et al. 2013)] and extent to
which the invader modifies environmental conditions
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K. Berthon
New phenotypic opmum
b
Phenotypic Change
+
c
a
0
Ancestral phenotype
e
d
–
Time
Invasion
Fig. 3 Adaptive and maladaptive phenotypic changes of
species exposed to invaders. a No change in phenotype either
because the invader has no impact or because the existing
phenotype enables the species to respond adaptively. b Where
the ancestral phenotype is below a new phenotypic optimum, the
species may adaptively change its phenotype. If this new
phenotype is near the optimum there is likely to be no
evolutionary change. c Most phenotypically plastic responses
are incomplete leading to selection towards the new phenotypic
optimum and the most rapid rates of evolution. Alternatively,
the species may be trapped into displaying maladaptive
phenotypes in the presence of the invader. Species may recover
to more adaptive phenotype (e), or ultimately go extinct (d)
[e.g. changes in nutrient availability (Reusch and
Williams 1998) vs. habitat construction (Wright et al.
2012)] (Fig. 1). The stronger selection is on certain
genotypes, the greater the fitness disparity between
them, and the more likely it is a native species will
evolve (Strauss et al. 2006; Fig. 2).
The result of interaction between native and
invasive species is not always one sided, with selection
favouring both species adapting to better exploit,
avoid or outcompete the other (Lankau 2012). In some
cases, this interaction may be facultative for the native
(Dijkstra et al. 2013) or the invader (e.g. Quinos et al.
1998). Such dynamics are important in determining
the success of species invasion (Mooney and Cleland
2001), and the long-term consequences for ecosystem
function thereafter (Strayer et al. 2006).This coevolution can lower the selective impact of invaders
over time and allow for their integration into the
ecosystem to a point where they may be considered
‘native’ (Carthey and Banks 2012). However, the
point at which an invader becomes an integral part of
an ecosystem is unclear, and any facultative interactions invasives have with native species are hotly
debated in light of their frequently negative impacts
(Rodriguez 2006).
Due to the magnitude of human induced environment changes, many native species are impacted by
123
multiple threats and are already genetically impoverished (Strauss et al. 2006). A low genetic diversity,
usually coupled with a low population size, confers a
low capacity for an evolutionary response, as genotypes are either equally affected by the selection
pressure, or are otherwise dominated by stochastic
effects (an ‘ecological response’ as in Strauss et al.
2006; Fig. 2c). For some species, phenotypically
plastic responses may aid in buffering against strong
negative selection pressure from invaders (Brown
2012; Ghalambor et al. 2007a), as it allows for rapid
responses to invasion without underlying genetic
variation (Brown 2012; Schlaepfer et al. 2010). If
these new phenotypes are close to the new phenotypic
optimum (i.e. the fitness of individuals is maintained
as close as possible to if not higher than that before
invasion, Fig. 3b), phenotypic plasticity can decouple
the selected phenotype from genotype frequencies,
and may actually prevent formation of evolutionary
responses (Schlichting and Wund 2014; Ghalambor
et al. 2007a). In reality, most phenotypic responses are
incomplete and do not fully restore native fitness in the
face of the new invader (Ghalambor et al. 2007b;
Fig. 3c). If, within the presence of the invader, the new
phenotype has a higher fitness value than the ancestral
state (i.e. the phenotype is adaptive), selection may act
to increase the efficacy with which a preferred
phenotype is produced. Hence, the phenotypic response facilitates a genetic response [‘genetic accommodation’, (Schlichting and Wund 2014; Ghalambor
et al. 2007b)]. This may mean a loss of plasticity such
that successful phenotypes become fixed in the
population (e.g. Scoville and Pfrender 2010). Similarly, increasing instability of environments and species
exchanges may favour increased capacity for phenotypically plastic responses [e.g. evolving an increased
ability to learn (Caller and Brown 2013)].
Alternatively, phenotypic responses that are reliably produced within the presence of an invader may
decrease the fitness of individuals, causing them to
become ‘trapped’ into expressing maladaptive traits
(Schlaepfer et al. 2005; Fig. 3d). The most commonly
studied examples of this are in host plant selection for
native insects where invaders are readily colonised but
have poor nutritional quality compared to native hosts
(e.g. Carroll et al. 1998). This may be because native
insects are unable to discriminate between chemical
cues of the invader and the native host, a key aspect of
host recognition (Fox and Lalonde 1993). Similarly,
Mechanistic and trait-based perspectives
the similar appearance of the toxic cane toad (Bufo
bufo) to native Australian frogs has caused several
native predators to be decimated due to misrecognition
of prey (Phillips and Shine 2006). In this way,
phenotypically plastic responses may lower a species’
capacity for adaptation to invaders by moving the
phenotype further from the optimum (Ghalambor et al.
2007b). Ultimately, such ecological traps may lead to
extinction (Schlaepfer et al. 2005).
However, evidence shows that species may not
always be doomed to extinction by such evolutionary
traps. For example, soapberry bugs have evolved to
exploit novel hosts in spite of initial decreases in
fitness (Carroll et al. 1997). Similarly, selection has
favoured changes in snake morphology to overcome
detrimental impacts of cane toad toxins [discussed
below (Phillips and Shine 2006)]. Studies into genetic
mechanisms have shown that trait phenotypes evolve
independently (Carroll et al. 2003) but may be
influenced by other traits (Lau 2008). Therefore,
maladaptive phenotypic responses in one trait (e.g.
host selection) may act to magnify selection pressure
on another related trait (e.g. feeding morphology),
thereby potentially increasing the rapidity of evolutionary change and releasing them from the trap (e.g.
adoption of a new host) (Fig. 3e).
Interactions of plastic and evolutionary changes
As phenotypic plasticity and evolutionary responses
are not mutually exclusive, there has been some
interest in investigating the contribution of plasticity
to rapid adaptive evolution (Scoville and Pfrender
2010; Trussell and Smith 2000; Latta et al. 2007;
Ghalambor et al. 2007b; Hendry et al. 2008). Several
studies have showed the importance of initial plasticity (Carroll et al. 1997; Latta et al. 2007; Nylin et al.
2014; Scoville and Pfrender 2010), but only one study
has successfully quantified its relative contributions to
adaptive responses in a native species (Latta et al.
2007). This study found that while phenotypic plasticity was important in the early stages of adaptation, it
only explained 11 % of the change in phenotype.
Similarly, studies of soapberry bugs (Carroll et al.
1997) have showed naı̈ve ancestral populations capable of responding plastically in the same direction as
genetically distinct experienced populations. Interestingly, these populations also show a predominance of
non-additive genetic mechanisms (Carroll et al. 2003),
indicating a strong role of gene expression (and hence
plasticity) in adaptation. Further, wider investigations
of adaptive evolution have shown a large role of
phenotypic plasticity in producing rapid rates of
evolution (Hendry et al. 2008). Taken together, this
suggests a genetic accommodation mechanism for
native species adaptation, where initial phenotypic
plasticity determines the evolutionary trajectory of the
species (Schlichting and Wund 2014; Ghalambor et al.
2007a). Even in cases of maladaptive plasticity,
evolution is rapid (Carroll et al. 2003) and the
contribution of plasticity is likely to vary depending
on the system (Hendry et al. 2008). Therefore,
understanding the time scale of plastic and genetic
processes and being able to distinguish between them
may allow us to better track the adaptation process in
native species and predict species capable of persistence in the face of invaders.
Changes to species traits
Selective pressure from invasive species alters native
species biology in four ways (Fig. 1). Natives may
alter their behaviour, morphology, physiology or lifehistory traits in order to reduce contact with or better
exploit the opportunities presented by an invader
(Strauss et al. 2006). A total of 77 cases of native
species adaptation were compiled from searches of
online databases and review articles (Table 1). Each
native/invasive species pair was treated as a separate
case, such that a native and/or invasive species may be
involved in several cases. Trends in species trait
changes were categorised in relation to different
trophic interactions (Fig. 1).
Behavioural changes
Change in the anti-predator or foraging behaviours of
native species is the most commonly studied form of
adaptation (Strauss et al. 2006; Fig. 1c). Studies have
shown adaptive changes in predator avoidance tactics
(Berger et al. 2007; Whitlow et al. 2003; Vanderwerf
2012), dietary preferences (Robbins et al. 2013;
Zimmerman 1960; Carroll et al. 1998; King et al.
2006; Dijkstra et al. 2013), prey handling methods
(Carlsson et al. 2009; Robbins et al. 2013; Beckmann
and Shine 2011; Phillips and Shine 2006), and habitat
choice (Vanderwerf 2012). A large amount of this
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K. Berthon
Table 1 List of species found to respond adaptively to invasive species
Native Species
Non-native
Selection
Plastic
Achilea millefoliuma
Achilea millefoliuma
Holcus lanatus
Thymus
pulegioides
Centaurea
maculosa
Thymus
pulegioides
Thymus
pulegioides
Cenchrus ciliaris
Competition
Competition
X
X
X
X
Strauss et al. in Oduor (2013)
Grøndahl and Ehlers (2008)
Competition
X
X
Lesica and Atthowe (2007)
Competition
X
X
Jensen and Ehlers (2010)
Competition
X
X
Jensen and Ehlers (2010)
Competition
X
Agropyron
spicatuma
Agrostis capillarisb
Campanula
rotundifollaa
Cercidium
microphyllum
Coregonus hoyib
Genetic
M
B
LH
P
X
Eilts and Huxman (2013)
Alosa
pseudoharengus
Bombus tectorum
Centaurea
maculosa
Acroptilon repens
Competition
X
X
Competition
Competition
X
X
X
Competition
X
X
Mealor and Hild (2007)
Cirsium arvense
Competition
X
X
Ferrero-Serrano et al. (2011)
Competition
Competition
X
X
X
X
Cipollini and Hurley (2008)
Dostál et al. (2012)
Salvelinus
fontinalisb
Sporobolus airoidesa
Alliaria petiolata
Impatiens
parviflora
Medicago
polymorpha
Alliaria petiolata
Bombus tectorum
Salmo trutta
Oncorhynchus
mykiss
Catostomus
commersoni
Acroptilon repens
Sporobolus airoidesa
Stipa occidentalisa,b
Elymus multisetus
Festuca
idahoensisa, b
Hesperostipa
comataa
Hesperostipa
comatea
Impatiens capensisa
Impatiens nolitangerea
Lotus
wrangelianusa,b
Pilea pumila
Poa secundaa
Salmo salar
Salmo salar
Onychomys
leucogasterb
Anadara trapezia
Zostera marina
Cirsium canescensb
Gentianella
campestrisb
Lotus wrangelianusb
123
X
References
Crowder (1986)
X
X
Competition
X
X
Competition
Competition
Competition
Competition
X
X
X
X
X
Competition
X
X
X
X
Rowe and Leger (2011)
Callaway et al. (2005)
X
Lau (2006, 2008)
X
Lankau (2012)
Goergen et al. (2011)
van Zwol et al. (2012)
van Zwol et al. (2012)
X
X
X
Bourke et al. (1999)
Competition
X
X
Cirsium arvense
Competition
X
X
Centaurea
maculosa
Yersinia pestis
Competition
X
X
Ferrero-Serrano et al. (2011)
and Bergum et al. (2012)
Ferrero-Serrano et al. (2011)
and Sebade et al. (2012)
Callaway et al. (2005)
Disease
X
X
Thomas et al. (1988)
Caulerpa
taxifolia
Musculista
senhousia
Rhinocyllus
conicus
Livestock
Environmental
modification
Environmental
modification
Novel
herbivore
Novel
herbivore
Novel
herbivore
Hypera
brunneipennis
X
X
X
Wright et al. (2012)
X
Ruesch and Williams (1998)
X
X
Rose et al. (2005)
X
X
X
X
Lennartsson et al. (1997)
X
Lau (2006, 2008)
Mechanistic and trait-based perspectives
Table 1 continued
Native Species
Thuja plicata
b
Cassida piperata
Colias philodiceb
Euphydryas edithab
Jadera
haematolomab
Leptocoris
tagalicusb
Lycaeides Melissab
Ostrinia nubilalisb
Papilio zelicaonb
Pieris napib
Prodoxus
quinquepunctellusb
Rhagoletis
pomonellab
Polioptila
californicab
Alytes muletensisb
Amblyrhynchus
cristatus
Amblyrhynchus
cristatus
Anolis sagreib
Daphnia retrocurvab
Daphnia magnab
Daphnia melanica
Limnodynastes
convexiusculus
Melanotaenia
duboulayi
Mya arenaria
Mytlius edulisb
Nesameletus
ornatusb
Nucella lapillusb
Perameles nausta
Perameles nausta
Non-native
Selection
Odocoileus
hemionus
Alternathera
spinosus
Medicago sativa
Plantago
lanceolata
Koelreuteria
elegans
Cardiospermum
grandiflorum
Medicago sativa
Zea maus
Ammi visnaga
Novel
herbivore
Novel host
Plastic
Genetic
M
B
LH
X
X
Novel host
Novel host
P
References
X
Vourc’h et al. (2001)
X
X
X
Dai et al. (2014)
X
X
X
X
X
Tabashnik (1983)
Thomas et al. (1988), Singer
et al. (1993)
Carroll et al. (1997, 1998,
2003)
Carroll et al. (2005)
Novel host
X
X
X
Novel host
X
X
X
Novel host
Novel host
Novel host
X
X
X
X
Alliaria petiolata
Yucca aloifolia
Novel host
Novel host
X
X
Malus pumila
Novel host
X
Molothrus ater
Novel parasite
Natrix maura
Canis lupus
familiaris
Felis catus
Novel predator
Novel predator
X
X
X
X
Griffiths et al. (1998)
Berger et al. (2007)
Novel predator
X
X
X
Berger et al. (2007)
Leiocephalus
carinatus
Alosa
pseudoharengus
Introduced fish
Salmanoid fish
Novel predator
X
X
Losos et al. (2004)
Novel predator
X
X
Wells (1970)
Novel predator
Novel predator
X
Rhinella marina
Novel predator
X
Bufo marinus
Novel predator
Carcinus maenus
Hemigrapsus
sanguineus
Salmo trutta
Novel predator
Novel predator
Carcinus maenus
Canis lupus
familiaris
Felis catus
Novel predator
Novel predator
Novel predator
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Novel predator
X
X
X
X
Cousyn et al. (2001)
Thomas et al. (1988) and Singer
et al. (1993)
Greenlees et al. (2014)
Caller and Brown (2013)
X
X
Smith et al. (1995)
Dai et al. (2014)
X
X
Nice et al. (2002)
Malausa et al. (2005)
Shapiro as in Strauss et al.
(2006)
Courant (1994)
Groman and Pellmyr (2000)
Whitlow et al. (2003)
Tabashnik (1983)
X
Mcintosh and Townsend (1994)
X
X
Vermeij (1982)
Carthey and Banks (2012)
X
X
Carthey and Banks (2012)
X
X
123
K. Berthon
Table 1 continued
Native Species
Non-native
Selection
Plastic
Pseudacris regilla
Procambarus
clarkii
Rana catesbeiana
Lepomis
macrochrius
Procambarus
clarkii
Rana catesbeiana
Introduced fish
Introduced fish
Bufo marinus
Novel predator
X
Novel predator
Novel predator
Novel predator
Pseudacris regillab
Rana aurora
aurorab
Rana aurora
aurorab
Rana aurorab
Triturus alpestrisb
Triturus helveticusb
Denrelaphis
punculatusb
Egretta garzetta
Haliastur sphenurus
Milvus migrans
Nycticorax
caledonicus
Porphyrio porphyrio
Pseudechis
porphyriacusb
Sceloporus
undulates
Vestiaria coccineab
M
B
X
X
Pease and Wayne (2014)
X
X
X
Chivers et al. (2001)
Pearl et al. (2003)
X
X
Pearl et al. (2003)
X
Novel
Novel
Novel
Novel
predator
predator
predator
prey
Novel
Novel
Novel
Novel
prey
prey
prey
prey
X
X
X
X
Bufo marinus
Bufo marinus
Novel prey
Novel prey
X
Solenopsis invicta
Novel prey
X
Feral ungulates
Trophic
cascades
Bufo
Bufo
Bufo
Bufo
marinus
marinus
marinus
marinus
Genetic
X
X
X
X
LH
X
X
X
X
X
X
P
References
Kiesecker (1997)
Denoel et al. (2005)
Denoel et al. (2005)
Phillips and Shine (2004)
X
X
X
X
Beckmann
Beckmann
Beckmann
Beckmann
et al. (2011)
and Shine (2011)
and Shine (2011)
et al. (2011)
X
X
X
X
Beckmann et al. (2011)
Phillips and Shine (2004, 2006)
X
X
X
X
X
Robbins et al. (2013);
Langkilde (2009)
Smith et al. (1995)
Native and non-native species pairs, are listed by their trophic interaction as in Strauss et al. (2006). Both phenotypically plastic and
genetic responses are given. Responses are marked according to the aspect investigated in each case study and absence of a mark does
not indicate the absence of a genetic or plastic response. This list is not exhaustive, but is likely representative of current case studies.
This list was used to inform Fig. 1
M morphological trait changes, B behavioural trait changes, LH life history trait changes, P physiological trait changes
a
References cited in Oduor (2013)
b
References cited in Strauss et al. (2006)
behavioural change appears to result from phenotypic
plasticity, primarily the ability of species to learn
(Caller and Brown 2013; Brown 2012; Beckmann and
Shine 2011; Vanderwerf 2012). Behavioural flexibility enables a rapid response that is often advantageous
when a species is presented with the novel challenges
of an invader (Brown 2012; Strauss et al. 2006). For
example, the endangered Hawaiian forest bird (Chasiempis ibidis) has altered its nest placement behaviour
in response to nest predation by introduced black rats
(Rattus rattus), which has a clear fitness advantage
(Vanderwerf 2012).
However, all behaviours have an innate (genetic)
component which usually relates to the stimuli
required to initiate a particular behavioural response
(Brown 2012). Examples may include particular cues
123
for host plant recognition that form the basis of host
plant preference (Bezemer et al. 2014; Tuda et al.
2014), or predator recognition (Nunes et al. 2014).
These innate elements may restrict the ability of
species to respond behaviourally (Brown 2012). For
example, species may be unable to recognise chemical
cues of a novel predator and hence not display
appropriate anti-predator behaviours (Freeman and
Byers 2006). The innate elements of a species’
behaviour may be altered under selection (Brown
2012) and there is evidence that this is the case for
invasive species responses (Caller and Brown 2013;
Bourdeau 2013). For example, Caller and Brown
(2013) showed that crimson spotted rainbow fish
(Melanotaenia duboulayi) from sites with a history of
cane toad invasion had an increased capacity for
Mechanistic and trait-based perspectives
aversion learning compared to their naive counterparts. Therefore, the capacity for phenotypic plasticity, and hence the tendency to display behavioural
responses to novel invaders, can itself evolve (Brown
2012).
Most behavioural studies have focused on the
ability of species to learn to recognise and respond to
predatory cues (e.g. Carthey and Banks 2012) or avoid
toxic prey items (e.g. Caller and Brown 2013). The
limited empirical evidence for predators responding to
exploit novel prey (reviewed in Carlsson et al. 2009) is
proposed to be an artefact of the strength of selection
pressure. That is, the cost for an organism of losing a
foraging opportunity is not as great as losing its life
(Beckmann and Shine 2011), leading to a decreased
tendency of adaptive change in predators compared to
prey. However, a number of insect herbivores have
evolved to utilise novel hosts (e.g. Carroll et al. 1998;
Tuda et al. 2014) and there is evidence to suggest that
vertebrate predators change their foraging behaviour
to reduce consumption of prey toxins (Beckmann and
Shine 2011; Robbins et al. 2013). Therefore, it is
possible that the gap in empirical evidence for predator
behavioural changes actually reflects a paucity of data
rather than the rarity of the phenomena.
Morphology changes
Morphological changes in native species have been
shown to occur under the same scenarios (such as
predator–prey interaction) but are not as commonly
documented as behavioural changes (Strauss et al.
2006; Fig. 1c). Similar to behavioural responses, these
may be a consequence of phenotypic plasticity (e.g.
induced anti-predator defences in the native mollusc,
Mya arenaria, Freeman and Byers 2006). However,
such changes form a part of organismal development
and are often irreversible (Nunes et al. 2014; Freeman
and Byers 2006) in contrast to more flexible behavioural plasticity.
In some instances, morphological change has
resulted in an alteration of native species’ adult body
patterns, with a strong genetic basis (Langkilde 2009).
For example, consumption of the toxic cane toad Bufo
marina has led to selection in Australian snakes for a
smaller gape size and longer body length (Phillips and
Shine 2006). This new body plan limits the amount of
toxin ingested by limiting the size of prey consumed,
while increasing the resistance to the toxin based on
body size. Similarly, the lizard (Sceloporus undulates), has evolved longer hind limbs in response to fire
ant invasion (Langkilde 2009) and soapberry bugs
show remarkably rapid changes in beak length to
exploit the different fruit sizes of invasive species
compared to natives (Carroll 2008; Carroll et al. 1997,
1998).
Interestingly, indirect changes in the environment
as a result of invasion have also led to altered
morphology. For example, the native bivalve (Anadara trapezia) has been shown to have increased shell
breadth in response to the altered water conditions
produced by the introduced seaweed Caulerpa taxifolia (Wright et al. 2012). Indirect impacts of invaders
are hard to predict as well as difficult to study, and
therefore present a challenging area of future research.
Changes in life history traits
Life history strategy changes appear to be important in
response to competition from invasive species (Oduor
2013), or predator–prey interactions (e.g. Nunes et al.
2014; Fisk et al. 2007; Fig. 1c). For example, plants often
increase their growth rate or reproduction in response to
competition (Oduor 2013). Alternatively, altered timing
of reproductive events is beneficial in reducing the
interaction of natives with their novel predators (Nunes
et al. 2014) or competitors (Oduor 2013).
Interestingly, life history traits have been found to
be more readily modified than morphological traits
under altered predation pressure (Nunes et al. 2014).
Developmental elements of life history (such as time
to maturity and growth rates) are strongly linked to
environmental factors and have high fitness value
(Fisk et al. 2007; Nunes et al. 2014). Life-history traits,
therefore, may be more readily modified because they
are under stronger selection pressure and evolve more
rapidly. On the other hand, a strong linkage with
environmental cues may indicate an important role of
phenotypic plasticity in shaping trait optima. Contrastingly, requirements for specific developmental
plans may buffer against environmental influence and
prevent adaptation (Ghalambor et al. 2007b).
Life history traits are often linked to morphology
changes, especially body size (Blueweiss et al. 1978).
It should not be surprising, then, that species which
have altered morphology often have altered life
history traits as well. For example, zooplankton
display both a smaller body size and the production
123
K. Berthon
of fewer, smaller offspring in the presence of a novel
predator (Fisk et al. 2007).
Physiological changes
Physiological changes in response to invasive species
are intimately linked to changes in a species’ life
history (Nunes et al. 2014), or morphology (Berger
et al. 2007, Freeman and Byers 2006) and are hence
rarely studied explicitly. However, physiological
changes can exist without a visible change in phenotype such as metabolic pathways for increased resistance to herbivory (Lau 2006) or disease (Thomas
et al. 1988), and tolerance to allelopathic compounds
(Callaway et al. 2005) or toxic prey (Phillips and Shine
2006). In most cases, the chemical mechanisms
underlying these processes are poorly understood
(Strauss and Agrawal 1999).
Future directions
Understanding the conditions under which native
species respond to invaders is important in understanding the long-term impacts of current invasions (Strayer
et al. 2006; Carthey and Banks 2012), as well as
determining the future susceptibility of recipient communities to invasion (Mooney and Cleland 2001).
Adaptive responses of native species also have economic implications either as pests of commercial crops
(e.g. Zimmerman 1960) or as biological control agents
(Flower et al. 2014). Though it is now clear that native
species can and do respond adaptively to invasive
species, little work has been done on the genetic
mechanisms underlying these changes (Carroll 2007).
It is becoming increasingly apparent that adaptive
responses are the result of complex interactions
between phenotypic plasticity and evolutionary processes. In many cases evolutionary adaptation is
inferred based on population-specific differences in
traits without directly testing for underlying genetic
changes (Strauss et al. 2006; Fisk et al. 2007). A lack of
explicit genetic approaches has led to misinterpretation
of phenotypically plastic responses as evolved patterns
(Trussell and Smith 2000). Considering the proliferation of cheap and accessible genetic techniques,
there is promise that quantitative measures of genetic
change may be readily integrated into future studies of
native species, as they have been for invasive species
123
(reviewed in Lee 2002). Contrastingly, much has been
gained by way of reciprocal transplant experiments
(e.g. Lau 2006) and hybridization techniques (e.g.
Carroll et al. 2003). Integrating both new and old
techniques would allow for investigation of the interaction between phenotypic plasticity and evolutionary
responses, and enable direct testing of genetic accommodation hypotheses to progress our understanding of
the mechanisms of native species adaptation.
In most of the above cases, more than one aspect of
a species’ biology is altered in response to invaders. In
combination these form complex adaptive strategies.
For example, the longer hind limbs of S. undulates
individuals is hypothesised to enhance the effectiveness of escape behaviours (Langkilde 2009), while
alteration in foraging behaviours (i.e. eating passing
fire ants) is likely to reduce incidence of predation at
the risk of toxicity (Robbins et al. 2013). An understanding of the physiology underlying these changes
may aid in linking these traits in terms of resource or
energy trade-offs. However, our knowledge of the
mechanisms of physiological change is severely
lacking and should be a topic of further research.
Finally, multi-species introductions are common and
complicate the selective pressure experienced by native
species. Additional invaders may modify the interactions between natives and existing invaders (Lau 2008)
or between native species (Lankau 2012). However,
only one study has directly compared responses of a
native species exposed to multiple invasive species (Lau
2008). This study found that the response of a native
plant to an introduced herbivore was altered depending
on the presence of an introduced competitor. Therefore,
understanding the true impact of invasive species as a
result of multiple species interactions is crucial for
adaptive management of invaded areas in future.
Acknowledgments I would like to thank Michelle Leishman,
David Nipperess and Culum Brown for their helpful comments
and ideas which greatly improved this manuscript. Thanks also
to two anonymous reviewers whose critical eye greatly
strengthened the arguments given.
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