Download Latitudinal shifts in coral reef fishes: why some species do and

F I S H and F I S H E R I E S , 2014, 15, 593–615
Latitudinal shifts in coral reef fishes: why some species do
and others do not shift
David A Feary1, Morgan S Pratchett2, Micheal J Emslie3, Ashley M Fowler1, Will F Figueira4, Osmar J Luiz5,
Yohei Nakamura6 & David J Booth1
1
School of the Environment, University of Technology, 123 Broadway, Sydney, NSW 2007, Australia; 2ARC Centre of
Excellence for Coral Reef Studies, James Cook University, Townsville, Qld. Q4811, Australia; 3Australian Institute of
Marine Science, PMB No.3, TMC, Townsville, Qld. 4810, Australia; 4School of Biological Sciences, University of Sydney,
Sydney, NSW 2006, Australia; 5Department of Biological Sciences, Macquarie University, Sydney, NSW 2109,
Australia; 6Graduate School of Kuroshio Science, Kochi University, 200 Monobe, Nankoku, Kochi 783-8502, Japan
Abstract
Climate change is resulting in rapid poleward shifts in the geographical distribution
of many tropical fish species, but it is equally apparent that some fishes are failing
to exhibit expected shifts in their geographical distribution. There is still little
understanding of the species-specific traits that may constrain or promote successful establishment of populations in temperate regions. We review the factors likely
to affect population establishment, including larval supply, settlement and post-settlement processes. In addition, we conduct meta-analyses on existing and new data
to examine relationships between species-specific traits and vagrancy. We show
that tropical vagrant species are more likely to originate from high-latitude populations, while at the demographic level, tropical fish species with large body size,
high swimming ability, large size at settlement and pelagic spawning behaviour are
more likely to show successful settlement into temperate habitats. We also show
that both habitat and food limitation at settlement and within juvenile stages may
constrain tropical vagrant communities to those species with medium to low reliance on coral resources.
Correspondence:
David A Feary,
School of the Environment, University
of Technology,
Sydney, 123 Broadway, NSW 2007,
Australia
Tel.: +61 2 9514
4068
Fax: +61 2 9514
4079
E-mail: david.
[email protected]
Received 10 Sep
2012
Accepted 6 Mar
2013
Keywords Climate change adaptation, global warming, range shifts, temperate
reef, tropical reef fishes, tropical vagrant
Introduction
594
Scope of this review
594
Section 1 Extrinsic factors regulating arrival of tropical vagrants
596
Oceanographic factors
596
Large-scale ocean currents
597
Ocean eddies
598
Section 2 Intrinsic factors constraining latitudinal population movement
598
Environmental constraints to distributional shifts
598
Population density and latitudinal distribution
599
Life-history traits associated with vagrancy
600
Correlations between species-specific traits in predicting vagrancy
603
© 2013 John Wiley & Sons Ltd
DOI: 10.1111/faf.12036
593
Tropical vagrant fishes D A Feary et al,
Resource constraints to vagrant success
603
Habitat association and settlement preferences
604
Dietary preferences and functional groups
605
Section 3 Future research needs
606
Conclusions
607
Acknowledgements
608
References
608
Supporting Information
615
Introduction
A central premise of biogeography is that the natural distribution of a species is at least partly governed by climate (Guisan and Zimmermann 2000;
Parmesan et al. 2005; Soberon 2007; Sunday et al.
2012). Therefore, we can expect to see major
changes in the distribution of species associated
with changes in global climate (IPCC 2007). The
fossil record (Davis et al. 2002; Carnaval and Moritz
2008) and recent observed trends (Parmesan et al.
1999; Thomas and Lennon 1999; Hickling et al.
2006; Burrows et al. 2011) attest to increased incidence of natural populations showing both range
expansion and contraction during periods of rapid
climate change. Metabolism, growth, reproduction
and ultimately survival of all organisms are tightly
linked to temperature, and there are both upper and
lower limits within which organisms can survive
(Hurst 2007). During warming periods, organisms
move poleward either to escape deleterious effects of
high temperatures at low latitudes or to take advantage of high-latitude locations which they could not
otherwise tolerate (Parmesan and Yohe 2003; Hoegh-Guldberg and Bruno 2010).
To date, poleward shifts in species geographical
distribution are most apparent for terrestrial plants
and animals (Parmesan and Yohe 2003; Parmesan 2006; Burrows et al. 2011). However, there is
increasing evidence of range shifts among marine
fishes and invertebrates, especially at high latitudes in the Northern Hemisphere (Dulvy et al.
2008; Nye et al. 2009; Stefansdottir et al. 2010).
This bias in recorded range shifts (between hemispheres and among latitudes) is consistent with
higher rates of temperature change recorded in
Northern Hemisphere, high-latitude regions (IPCC
2007). However, large-scale changes in ocean
temperature are also taking place at low latitudes,
characterized by a widening of the tropical belt
(Seidel et al. 2008; Lu et al. 2009). Such changes
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have been linked to poleward expansions in the
distribution of many tropical organisms (Booth
et al. 2007, 2011; Madin et al. 2012).
The distribution of tropical marine organisms has
been substantially affected by changes in both
ocean temperatures and major ocean currents (Seidel et al. 2008; Lu et al. 2009). Since 1900, surface
waters associated with western boundary currents
(e.g. Gulf Stream, Agulhas Current) have increased
in temperature 2–3 times faster than the global
mean surface ocean warming rate (Wu et al.
2012). Such warming of surface currents has also
been associated with a poleward shift in the extent
of these boundary currents and substantial change
in the distribution and extent of tropical benthic
species (Oviatt 2004; Helmuth et al. 2006; Yamano
et al. 2011). Such poleward shifts in warm currents
have also had important effects on tropical reef fish
larvae, which can frequently be transported 100–
1000s of kilometres from tropical to temperate latitudes (e.g. Booth et al. 2007; Figueira et al. 2009;
Hirata et al. 2011; Soeparno et al. 2012).
Scope of this review
There is increasing evidence that climate change is
leading to rapid changes in marine species’ distributional envelope, with such range shifts expected
to increase in strength and intensity as global climatic conditions change (Booth et al. 2011; Madin
et al. 2012). While there is mounting evidence that
benthic marine communities are showing substantial changes in their distribution and boundaries
(Greenstein and Pandolfi 2008; Yamano et al.
2011), relatively less is known of the potential
impacts on the associated fish communities (Munday et al. 2008a, 2009; but see Burrows et al.
2011). Although climate-mediated shifts in the
geographical range of temperate and subtropical
fish species are expected, and indeed have been
shown in several regions (Sorte et al. 2010; Last
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Tropical vagrant fishes D A Feary et al.,
et al. 2011), tropical fish species may be particularly sensitive to increasing temperatures as they
exist in a relatively thermostable environment
(Hoegh-Guldberg et al. 2007). Most tropical fishes
may not live within environments that are close to
their lethal thermal limits (Mora and Ospına
2001), but we can expect that elevated ocean temperature may have substantial effects on individual
performance, with potential implications for population shifts (Munday et al. 2008a, 2009). Despite
this, there is little predictive framework to understand whether species-specific traits may structure
range shifts within tropical fish assemblages and
the potential changes this may have in the composition and structure of tropical fish communities
(Munday et al. 2008a,b). Indeed, there is mounting
evidence to suggest that marine organisms have
shown average geographical shifts associated with
climate-mediated global thermal shifts from 1.5 to
5 times faster than their terrestrial counterparts
(termed ‘climate velocity’, sensu Burrows et al.
2011). The question then is what are the factors
that may allow tropical coral reef species to track
‘climate velocity’ closely? Within this review, we
argue that species-specific demographic traits (e.g.
body size, post-larval duration, size at settlement,
reproductive behaviour) are likely to be important
in structuring such geographical shifts in coral reef
fish species. An understanding of how such traits
may differ between tropical fish species is lacking in
tropical reef science and is the focus of this review.
Within this review, we focus solely on marine
ray-finned fishes (Class Actinopterygii) that breed
within tropical coral reef habitats (dominated by
reef building, scleractinian reefs), and their larvae
show or have shown settlement into temperate
reef habitats (hereafter termed ‘tropical vagrants’).
Although there is increasing awareness that other
groups of mobile tropical organisms are showing
shifts in their latitudinal distribution (i.e. Elasmobranchii: Last et al. 2011), these studies are outside the scope of this review. All of the tropical
vagrants identified in this review, despite being
found within temperate habitats, show substantial
reductions in abundance associated with low winter-water temperatures (e.g. Choat et al. 1988;
Francis et al. 1999; Booth et al. 2007; Figueira
and Booth 2010). However, as global sea surface
temperature increases are associated with climate
warming scenarios (IPCC 2007), we predict that
for a suite of tropical vagrants being advected into
high-latitude regions, survival, adaptation and
population development may occur rapidly (Figueira and Booth 2010; Booth et al. 2011; Madin
et al. 2012; Soeparno et al. 2012).
We examine both the intrinsic and extrinsic processes that likely influence the spatial, temporal
and taxonomic biases in the species-specific structure of tropical vagrant populations (Fig. 1). It is
assumed a priori that extrinsic processes (i.e.
oceanographic factors) will interact with inherent
differences in the life histories of fishes to determine which species settle, as well as when and
where (see also Munday et al. 2009). Therefore,
we first examine the oceanographic factors that
may facilitate physical connectivity between tropical and temperate regions. Determining the intrinsic processes that may facilitate or constrain
latitudinal movement is expected to be key to
understanding which tropical species may be
increasingly susceptible to sustained and ongoing
climate change (Cowen et al. 2000, 2006; Jones
et al. 2005, 2009a; Almany et al. 2007a; Hobbs
et al. 2010, 2012). Therefore, within this review,
we examine the potential physiological constraints
to successful settlement and recruitment of tropical
vagrants in temperate regions. We then consider
pre-settlement mechanisms associated with successful advection of tropical vagrants into high-latitude temperate regions. Cheung et al. (2010) in
their global analysis on the redistribution of marine fishes suggested that range shifts are likely to
be constrained by specific resource (prey or habitat) requirements for some fishes. Thus, we also
examine the potential importance of resource
requirements in successful settlement and survival
of tropical vagrants within temperate habitats.
Finally, albeit not exhaustive, we highlight the
array of research questions that will be vital in
understanding the role of increasing climate
change in structuring the range expansion of tropical coral reef fishes into temperate environments.
A total of 360 species of tropical fishes (within
the Class Actinopterygii) from 55 different families
have been recorded settling into temperate regions
(hereafter termed ‘tropical vagrants’) (Supplementary Data S1). Despite this, vagrants still appear
relatively uncommon within families (Fig. 2).
Tropical vagrants include a disproportionate number of species from the families Acanthuridae,
Balistidae, Chaetodontidae, Cirrhitidae, Labridae,
Lutjanidae, Mullidae, Pomacentridae and Scaridae
(Fig. 2). In comparison, several common tropical
families are extremely under-represented within
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
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Tropical vagrant fishes D A Feary et al,
Figure 1 Schematic of factors potentially limiting the range expansion of tropical fishes in temperate habitats during
three stages of the expansion process (natal, larval and novel environments). Factors discussed and/or tested in this
study are indicated by the section number in parentheses.
vagrant surveys, including the Apogonidae, Callionymidae, Gobiesocidae, Gobiidae, Serranidae,
Syngnathidae and Tripterygiidae (Fig. 2). It is
important to note that the majority of these
under-represented families predominantly hold
small, relatively cryptic species (see Munday and
Jones 1998), which may result in such species
being missed in vagrant surveys, rather than not
tending to be vagrants (see Section 2). However,
as the majority of families that hold vagrants are
also relatively small-bodied species, and the majority of vagrant survey data comprise surveys of
new recruit and early-stage juveniles (~2–3 cm
TL), other ecological traits may also be important
in structuring vagrant success (see Section 2).
Section 1: Extrinsic factors regulating arrival
of tropical vagrants
Oceanographic factors
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596
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local reef area (Leis et al. 2011). In addition, while
larval marine organisms, and fish in particular,
can attain impressive swimming and orienting
abilities, the onset of this ability may be species
specific and form gradually (i.e. swimming ability:
Fisher et al. 2000) or relatively rapid (i.e. orientation: Paris and Cowen 2004; Dixson et al. 2012).
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On the west coast, the Leeuwin Current actually
seems to promote it (Condie et al. 2011). Thus,
the highly coherent nature of these large-scale
boundary currents, which may effectively transport larvae over great distances, may also impede
the ability of those larvae to reach viable inshore
habitat.
Ocean eddies
Recirculating current features, or eddies, have
commonly been proposed as mechanisms that
may retard, rather than encourage, long-distance
transport of larva from a natal area (Sponaugle
et al. 2002). For instance, eddies forming in the
wake of islands may concentrate eggs or larvae
(e.g. Wing et al. 1998) preventing their dispersal.
Such recirculation may then result in the selfrecruitment of larvae, as has been suggested for
the Tortugas Gyre and other spin-off eddies of the
Florida Current (Lee et al. 1992, 1994, 1995;
Limouzy-Paris et al. 1997). However, while eddies
retain larvae near a natal site, they may also be
extremely important for larval transport where
individuals are entrained in large-scale ocean currents, but may also be important in trapping larvae when they arrive at new locations. Due to a
complex mix of factors (e.g. topography, density
gradients), eddies are commonly shed from ocean
currents and may migrate, transporting the water
masses they contain. For example, warm-core
eddies shed by the Gulf Stream north of Cape Hatteras have been implicated in the transport of larvae towards coastal waters of not only
cosmopolitan temperate fish larvae (Hare and Cowen 1996; Hare et al. 2002), but also tropical fish
(Hare et al. 2002). The EAC separates from the
east Australian coast at ~32°S latitude, shedding
a series of cold- and warm-core eddies (Ridgway
and Dunn 2003; Choukroun et al. 2010). The
tropical water masses contained within the EAC
and its resultant eddies have been shown to contain larval fish assemblages uniquely different
from the surrounding waters (Keane and Neira
2008; Syahailatua et al. 2011). The dynamic nature of the eddy field south of the separation zone
results in episodic patterns of tropical larval
recruitment (Booth et al. 2007). A similar process
occurs within the Leeuwin Current on the west
Australian coast, where eddies greatly facilitate
on-shelf transport of water masses (Condie et al.
2011).
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Section 2: Intrinsic factors constraining
latitudinal population movement
Environmental constraints to distributional shifts
Temperature is one of the primary variables regulating aquatic species bioenergetics (Kitchell et al.
1977). Ambient temperatures substantially determine physiological processes such as feeding, respiration, faecal egestion rates and ultimately
growth (von Herbing 2002; Domenici et al. 2007).
Even within their natal ranges, newly recruited
fishes will experience a range of temperatures,
both spatially and temporally, due to behavioural
activities and in situ environmental fluctuations
(Danilowicz 1997; Sponaugle and Grorud-Covert
2006; Abesamis and Russ 2010). Such changes in
temperature can have substantial effects on fish
physiology, defining species thermal geographical
boundaries, even within relatively open-water habitats. We can predict that for warm-adapted tropical vagrants within cooler waters, thermal optima
for physiological mechanisms may exist for limited
periods during the year (i.e. warm summer
months), and therefore, key bioenergetic parameters may only be maximized for a short time
frame. Below, we examine the potential importance of physiological constraints to successful latitudinal extension in tropical reef fish populations.
Environmental temperature is one of the most
important physical variables affecting the performance of ectotherms (Hazel and Prosser 1974;
Hurst 2007). Therefore, we can expect that one of
the most important factors in structuring the success of tropical vagrants within temperate environments will be species-specific thermal limits for
minimum environmental temperature (Attrill and
Power 2002; Dulvy et al. 2008; Poertner and Farrell 2008). Virtually, all aspects of the behaviour
and physiology of ectotherms are sensitive to environmental temperature (Hazel and Prosser 1974;
Poertner and Farrell 2008). Therefore, we can
expect that among tropical vagrants, the predominant source of mortality in temperate environments will be an individual’s inability to maintain
cellular and organismal homoeostasis during
winter (Hurst 2007). Although there is an
increasing array of studies determining the upper
thermal physiological limits within tropical fishes
(Munday et al. 2008b; Donelson et al. 2011,
2012), there is comparatively little information on
lower thermal limits. The majority of studies
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examining overwintering success have focused on
temperate freshwater or estuarine fishes, examining survival within lakes or estuaries that have a
partial or full winter freeze of surface waters (e.g.
Hurst and Conover 2001; Pratt and Fox 2002).
Recent work has shown that tropical fishes may
be able to effectively withstand water temperatures
much lower than predominantly found in tropical
latitudes. Eme and Bennett (2008) found that
water temperatures of ~15 °C were the critical
thermal minimum for eight Indo-Pacific damselfishes (Pomacentridae), while Figueira et al. (2009)
showed that for the tropical Indo-Pacific sergeant
(Abudefduf vaigiensis, Pomacentridae), water temperatures needed to be 17 °C to cause substantial population loss within field surveys. Figueira
et al. (2009) also demonstrated in aquaria trials
that individuals of the Indo-Pacific sergeant were
able to withstand water temperature down to
16 °C. However, such thermal ability may vary
among tropical fish families and even species.
Visual surveys of tropical vagrants in south-eastern Australia revealed that populations of four
damselfish species tolerated temperatures down to
17 °C, while two butterflyfish species populations
tolerated water temperatures down to 19 °C (Figueira and Booth 2010). In corroboration with this,
low sea surface temperatures (SSTs) at tropical/
temperate transition zones also support the prediction that tropical fishes may be able to withstand
low winter-water temperatures. For example, at
the Solitary Islands [northern New South Wales
(NSW)], winter SSTs regularly drop to 16.6 °C
(Malcolm et al. 2011). Despite this, these islands
support a large breeding colony of the tropical
Threespot damselfish (Dascyllus trimaculatus,
Pomacentridae) (HA Malcolm pers comm), while
more than 50% of the species within the Solitary
Islands are regarded as tropical (Malcolm et al.
2010).
Population density and latitudinal distribution
The likelihood of tropical fish larvae dispersal into
temperate regions is likely to be associated with
population abundance: that is, species that are
extremely rare at the current latitudinal extremes
of their distribution, or may be non-reproductive
at these limits, will ultimately have lower numbers
of larvae available to disperse away from source
locations than species that are exceedingly abundant. Although there is limited data on the rarity
and/or fecundity of species throughout their
range, we can potentially use species population
abundance at southern limits of coral development
as a proxy for these processes. We can expect,
therefore, that tropical vagrants may be among
those with the highest population abundance on
tropical reefs. In comparison, species that are relatively rare, or locally uncommon, are unlikely to
have high numbers of larvae exported to reefs distant from natal sources (Jones et al. 2002). One of
the most common macro-ecological patterns
reported is a positive correlation between local
abundance of a species and geographical range
(Lawton 1999; Roughgarden 2009). However,
there is little evidence to suggest that tropical species abundance is associated with geographical
range, with numerous accounts of both spatially
restricted and non-restricted fishes with little difference in total abundance (Jones et al. 2002; Hobbs
et al. 2010, 2012). To examine whether the abundance of tropical reef fish species within the natal
habitat [southern Great Barrier Reef (GBR)] was
an important predictor of tropical vagrant occurrence within the adjacent temperate reef habitat
(NSW), we used a logistic regression analysis and
compared the total abundance of 24 butterflyfishes, 19 surgeonfishes and 42 damselfishes surveyed
within the Swain sector (southern GBR) with the
total abundance of these same species observed
within NSW over the same 5-year period (2003,
2004, 2005, 2007 and 2009). This analysis found
that species abundance in the southern GBR was
not significantly associated with species abundance
in NSW (P = 0.334). Overall, there was little similarity in tropical vagrant abundance between the
Swain sector and NSW sites; although the most
abundant tropical vagrant butterflyfishes (surveyed
in NSW) showed some of the highest densities
within the Swain group (i.e. Black butterflyfish
(Chaetodon flavirostris, Chaetodontidae) and the
Threadfin butterflyfish (Chaetodon auriga, Chaetodontidae)), one of the most abundant butterflyfish within the Swain sector (i.e. Blackback
butterflyfish (Chaetodon melannotus, Chaetodontidae) was the least abundant species in tropical
vagrant surveys within NSW.
Tropical reef fish populations may be widely distributed, encompassing the entire latitudinal
extent of coral reefs. Conversely, they may have
truncated distributions, being predominantly found
in a narrow band near the equator or occurring
only in high-latitude regions (Choat and Robertson
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Tropical vagrant fishes D A Feary et al,
2002; Jones et al. 2002; Emslie et al. 2010, 2012;
Cheal et al. 2012). Such differences in the latitudinal extent of coral reef fishes may be an important
predictor in understanding vagrancy within coral
reef fishes, and we found latitudinal extent to be
significantly associated with vagrants (P = 0.000).
Indeed, there is increasing interest in understanding the mechanisms responsible for Rapoport’s
rule, the increase in the latitudinal extents of
occurrence of species towards higher latitudes (Stevens 1989). Although there is evidence to suggest
that species upper thermal limits may show a geographical variation (Stillman and Somero 2000),
recent work has shown that lower lethal temperatures decline with latitude (Gaston et al. 1998,
Gaston and Chown 1999, Addo-Bedaiko et al.
2000). Therefore, although there is little data to
examine this (see Eme and Bennett 2008; Figueira
et al. 2009), we can predict that differences
between vagrant and non-vagrant fishes in their
latitudinal extent (i.e. abundance in tropical/temperate transition region) may be associated with a
wider thermal tolerance for lower temperatures
within vagrants (Addo-Bedaiko et al. 2000).
However, more important in predicting the
extent of vagrancy among coral reef fishes may be
the geographical distance between a population’s
tropical source and its temperate sink (Sorte et al.
2010). We can expect that species with distributions truncated in low latitudes are unlikely to
form vagrant communities, while those with distributions that are closer to temperate regions are
more likely to form them (Munday et al. 2008a).
To test the role of latitude, and therefore distance
from source to sink in structuring tropical vagrant
communities, we examined the proportional abundance of butterflyfishes (as a percentage of total
abundance) surveyed in both high-latitude (Capricorn Bunker group) and low-latitude (Lizard
Island/Cooktown Sector) regions (using data from
Emslie et al. 2010) and compared it with butterflyfishes surveyed throughout NSW (sensu Booth
et al. 2007) (Table 1). Tropical vagrants surveyed
in NSW were more likely to show higher abundances in high-, than low-latitude regions
(Table 1). Of the seven butterflyfish species surveyed within temperate NSW waters, five species
(Sunburst butterflyfish (Chaetodon kleinii, Chaetodontidae), Black butterflyfish, Speckled butterflyfish (C. citrinellus, Chaetodontidae), Raccoon
butterflyfish (Chaetodon lunula, Chaetodontidae)
and Blackback butterflyfish) were predominantly
600
the most important butterflyfish species (as a percentage of total abundance) surveyed in the highlatitude region. In comparison, the majority of
tropical vagrants were not abundant in the lowlatitude region, although the Threadfin butterflyfish and Raccoon butterflyfish were relatively
important (Table 1). In corroboration with this,
recent research has shown that there is very little
exchange in surface circulation between the
northern (north of 18°S) and southern GBR
(Choukroun et al. 2010), further supporting the
potential importance of high-latitude populations
as sources for tropical vagrants.
Life-history traits associated with vagrancy
Among species, a positive relationship has been
shown between pelagic larval duration (PLD) and
dispersal distance (e.g. Shanks 2009). We may,
therefore, expect taxa with long PLDs to be more
prevalent in expatriated larval assemblages, especially further from tropical sources (Booth and
Parkinson 2011). However, this prediction may be
overly simple as the phylogeographical literature
has shown that reef fish have a great deal of flexibility in their larval dispersal characteristics. For
example, recent work strongly suggests dual strategies in many tropical fish species: that is, localized dispersal that ensures retention in the
immediate natal area and long-distance dispersal
to geographically distant areas (Jones et al. 1999,
2005, 2009b; Planes et al. 2009). In addition, dispersal distance has also been shown to be independent of PLD for numerous species in multiple
locations; there are many fish species with relatively low PLDs, which regularly cross the East
Pacific barrier each way (c. 5000 km of deep
water separating the Eastern from the Central
Pacific) (Lessios and Robertson 2006; Leis et al.
2011), while others with relatively high PLDs can
show exceptionally high levels of self-recruitment
(i.e. Vagabond butterflyfish (Chaetodon vagabundus,
Chaetodontidae) Almany et al. 2007a). Despite
this, taxa with relatively longer PLDs (e.g. Chaetodontidae) were relatively more common than
taxa with relatively shorter PLDs (e.g. Pomacentridae) among a suite of tropical vagrant species in
south-eastern Australia (Booth et al. 2007). To
examine whether PLD is associated with successful
long-distance dispersal of vagrants, where possible,
we compared the mean PLD (in days) of tropical
vagrant (n = 109) and tropical non-vagrant fishes
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
Tropical vagrant fishes D A Feary et al.,
(n = 214). We found no relationship between
vagrants and mean PLD, with both high and low
PLD values found for both vagrant and nonvagrant species (P = 0.782).
Life-history
theory
predicts
relationships
between numerous life-history traits and body size
of fishes (Hutchings et al. 2012). Among these is a
positive relationship between body size and lifetime
reproductive output, with larger fishes producing
far more gametes and higher lifetime reproductive
output than smaller-bodied fishes (Weatherly
1972; Thresher 1984). We can expect then that
such size-mediated differences in reproductive output may substantially increase the probability of
Table 1 Distribution of Chaetodontidae as a percentage
of total abundance between Lizard Island/Cooktown and
Capricorn Bunker sectors (Emslie et al. 2010). Species in
bold denote species that have been surveyed within NSW
waters (sensu Booth et al. 2007).
Species
Lizard
Island/
Cooktown
Sector
Species
Swain
sector
H. polylepis
C. meyeri
C. reticulatus
C. ephippium
C. auriga
C. bennetti
F. longirostris
C. lunula
F. flavissimus
C. punctatofasciatus
C. pelewensis
C. ulietensis
C. vagabundus
C. ornatissimus
C. speculum
C. lunulatus
C. plebeius
C. baronessa
C. unimaculatus
C. rafflesi
C. aureofasciatus
C. kleinii
C. trifascialis
C. lineolatus
C. mertensii
C. melannotus
C. rostratus
C. rainfordi
C. citrinellus
C. flavirostris
83
73.9
72.4
70.1
57.5
52.6
51.3
49
41.7
40.7
40.1
38.9
38.3
35.8
33.6
33
25
23.3
22.7
20.1
19.8
17.1
15.8
14.6
14.3
13.1
11.6
7.5
4.9
0.8
C. trifascialis
C. kleinii
C. flavirostris
C. citrinellus
C. lunula
C. melannotus
C. rainfordi
C. unimaculatus
C. reticulatus
F. flavissimus
C. speculum
C. ornatissimus
C. plebeius
F. longirostris
C. lineolatus
C. pelewensis
C. lunulatus
C. auriga
C. vagabundus
C. baronessa
C. ephippium
C. rafflesi
C. aureofasciatus
C. mertensii
C. rostratus
H. polylepis
C. ulietensis
C. punctatofasciatus
C. meyeri
C. bennetti
63.6
49.5
38.8
26.6
16.3
15.3
15.1
13.2
12.2
11.4
11.2
10.2
8.6
7.7
7.5
6.2
6
5.4
3.4
2.5
1.2
0.9
0.1
<0.1
0
0
0
0
0
0
long-distance larval dispersal (Leis 1993; Munday
and Jones 1998). Therefore, to determine whether
body size is associated with vagrants, where possible, we compared the maximum body size (cm TL)
of vagrant vs. non-vagrant tropical fishes
(n = 341 vagrants, n = 4060 non-vagrants).
Logistic regression of vagrant potential as a function of body size illustrates that fishes with larger
body size are significantly more likely to have
expatriated larval assemblages than smaller-sized
fishes (P = 0.000). In fact, there is a threshold at
which species are more likely to show vagrancy:
within tropical fishes with body size larger than
10.95 cm TL, 12% are tropical vagrants, while
within fishes smaller than 10.95 cm TL, only
0.02% are vagrants (Fig. 3).
Coral reef fishes vary in the degree of parental
care invested in their offspring. Broadcast spawners release gametes into the water column with
very little investment, while demersal spawners
invest vast resources into building and defending
nest sites where eggs are laid and protected until
hatching (Thresher 1984). We can expect that
such differences in spawning mode may influence
larval dispersal (Thresher 1984; Brogan 1994; LoYat et al. 2006). Pelagically spawned larvae are
immediately subject to oceanographic processes,
which may disperse them further than demersally
spawned larvae (Thresher 1984). However, demersally spawned larvae have longer incubation
times, are larger-bodied and have higher developed
sensory and locomotor systems (Thresher 1984;
Figure 3 We identified the threshold of body size effect
on vagrancy by fitting a binary recursive partitioning,
which splits the data successively and selects the split
that maximally distinguishes the response variable above
and below a given value.
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
601
Tropical vagrant fishes D A Feary et al,
Leis 1993). Therefore, demersally spawned larvae
may have a greater ability to control their position
within the water column, thereby influencing the
potential for dispersal (Leis and Goldman 1984;
Leis 1993; Brogan 1994; Lo-Yat et al. 2006). To
examine whether spawning mode is associated
with vagrancy, we compared the reproductive
strategies of 4665 species of tropical fish (n = 330
vagrant species, n = 4335 non-vagrant species)
and classified them into one of three distinct reproductive guilds, each exhibiting different levels of
parental care: (i) non-guarders (low care: pelagic
spawner), (ii) guarders (moderate care: guarding
and caring for eggs spawned into a demersal nest)
and (iii) bearers (high care: brooding). This analysis showed that both high and medium levels of
parental care were negatively associated with
vagrant potential, while low levels of parental care
were positively associated with vagrant potential
(Fig. 4).
Species-specific differences in larval swimming
behaviour have been implicated in the dynamics
of dispersal within a range of reef fish larvae (Stobutzki and Bellwood 1994, 1997; Leis et al. 1996;
Leis and Carson-Ewart 1997, 2003; Fisher 2005).
Although there is considerable variation among
taxa, recent work on late-stage, or settlement-competent, larvae of coral reef fishes shows them to be
outstanding swimmers both in terms of swimming
speed and endurance (Fisher 2005; Fisher et al.
2005; Leis et al. 2011). Although species-specific
differences in swimming ability may be important
Figure 4 Vagrant potential as a function of parental
care type (See Supplementary Data S2).
602
for retention of fishes within natal waters (Leis
et al. 2011), such differences may also be associated with potential long-distance dispersal. If swimming ability is associated with potential dispersal,
we can expect tropical vagrants to have greater
larval swimming ability than non-vagrants. Therefore, we compared the potential swimming ability
of tropical vagrants vs. non-vagrants using (Ucrit),
the average critical speed (cms 1) as a proxy for
swimming ability. Ucrit data were available for a
total of 31 tropical vagrants vs. 32 non-vagrants,
mostly from the Pomacentridae, Apogonidae and
Chaetodontidae (using Fisher et al. 2005; Hogan
et al. 2007; Leis et al. 2011). A logistic regression
of vagrant potential as a function of average critical speed indicated that fishes with higher swimming ability were more likely to show vagrancy
than those with lower swimming ability
(P = 0.015).
There is a substantial literature showing that
factors operating within the early life history of
coral reef fishes (e.g. feeding, growth rate, size)
may have substantial flow-on effects to juvenile
growth and ultimately survival (Brunton and
Booth 2003; Hoey and McCormick 2004; McCormick and Hoey 2004). One of the most important
factors in determining the survival of early history
stages of coral reef fishes is size at settlement, as
survival and longevity of new recruits are positively associated with increasing new settler body
size (Sponaugle and Grorud-Covert 2006; Sponaugle et al. 2011). We can expect, therefore, that
tropical vagrants may have larger size at settlement than non-vagrants. Therefore, to examine
whether body size at settlement is an important
predictor of the diversity of tropical vagrant fishes,
we compared the size at settlement of tropical
vagrant and non-vagrant damselfishes (using
Kerrigan 1996; Thresher and Brothers 1989; Wellington and Robertson 2001; Wellington and Victor 1989). Logistic regression of vagrant potential
as a function of size at settlement illustrated that
fishes with larger size at settlement were more
likely to have expatriated larval assemblages than
species with smaller-sized settlers (P = 0.045). In
fact, of the 51 species of damselfish for which
average size-at-settlement data were available
(n = 15 tropical vagrants, n = 36 tropical nonvagrants), seven species (Bicolor chromis (Chromis
margaritifer, Pomacentridae), Nagasaki damsel
(Pomacentrus nagasakiensis, Pomacentridae), Sapphire damsel (Pomacentrus pavo, Pomacentridae),
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
Tropical vagrant fishes D A Feary et al.,
Speckled damselfish, (Pomacentrus bankanensis,
Pomacentridae), Ward’s damsel (Pomacentrus
wardi, Pomacentridae), Neon damsel (Pomacentrus
coelestis, Pomacentridae) and Yellowtail demoiselle
(Neopomacentrus azysron, Pomacentridae)) settled
between 13 and 15 mm TL, which was in the top
17% of values for settlement size. In comparison,
the majority of non-vagrant Pomacentrid species
larvae settled at sizes below 13 mm TL.
Correlations between species-specific traits in
predicting vagrancy
Within this review, we have focused on examining
whether single species-specific traits may be useful
in predicting vagrant potential. However, there is
also the need to examine whether there are correlations between traits. For example, temperature is a
major factor determining PLD (O’Connor et al.
2007) and latitudinal range, thus confounding single analyses looking at either of these two. In addition, body size may co-vary with abiotic factors
(e.g. temperature); warmer water species tend to
have smaller body size than colder water species
because of oxygen and thermal capacity limitation
(Pauly 1997). However, when undertaking correlation analyses encompassing a number of species
traits, there are several caveats that need to be
addressed. Firstly, although coral reef fishes are
among the best-studied teleost assemblages, there
remain considerable gaps in our knowledge of their
biology and ecology (Pratchett et al. 2008b).
Therefore, there will be always limited information
on specific traits within this fauna. For example,
when comparing the Ucrit values between vagrant
and non-vagrant fishes, our analyses comprised 31
species of vagrant fishes (encompassing 9 families)
and 32 non-vagrant fishes (encompassing nine
families). Secondly, there is a substantial bias in the
phylogenetic extent of research undertaken on
coral reef fish communities, with the butterflyfishes
and damselfishes the most well-researched groups
(Sale 1991, 2002). Therefore, for any particular
trait, the potential analysis between vagrants and
non-vagrants may be affected by the limited phylogenetic extent of the sample; the potential for a
phylogenetic confound is then potentially high.
Despite these caveats, the need to develop multiple trait correlations will be important in developing
the range of traits that will aid in predicting
vagrancy within coral reef fishes. Therefore, we
undertook a logistic regression using three traits in
which there was sufficient data available: latitudinal range, body size and reproductive mode [all
data sourced from Fishbase (Froese and Pauly
2012)]. For this analysis, there were 290 species
(encapsulating surgeonfishes, butterflyfishes and
damselfishes, 97 species were vagrants) for which
values for all three traits were available (with ‘family’ as a random factor in the binomial GLMM). This
analysis showed that only latitudinal range was significant in predicting vagrancy (P <0.000,
z = 6.307). We then extended this analysis and
included all data available on PLD (which reduced
the available dataset to 129 species, 61 species were
vagrants). As PLD and reproductive mode were
highly correlated (Spearman’s correlation = 0.8),
we excluded reproductive mode from this analysis.
However, the results also showed that latitudinal
range was the only significant factor that predicts
vagrancy (P <0.000, z = 3.735). Therefore,
although such correlative analyses at present are
limited by available data, and potentially have a
phylogenetic bias, they will be useful in developing
a predictive framework for understanding vagrancy
within tropical reef fishes. We have shown that the
present latitudinal range of tropical reef fishes may
be a suitable predictor of vagrancy: the higher the
latitudinal range, the more likely that the species
will have expatriated larval assemblages.
Resource constraints to vagrant success
We can expect that tropical range shifts are likely
to be limited by species-specific resource requirements (Munday et al. 2008a; Cheung et al. 2010).
In particular, for tropical fishes, temperate reefs
will lack a range of settlement substrates, settlement cues or specific dietary components found on
tropical coral reefs (Harriott and Banks 2002).
Temperate reef habitats are not devoid of scleractinian corals (Rodolfo-Metalpa et al. 2008; Lien
et al. 2012), and it is possible that tropical reefbuilding corals may become increasingly established beyond their normal latitudinal limits due
to sustained increases in ocean temperature
(Precht and Aronson 2004; Greenstein and Pandolfi 2008; Yamano et al. 2011). Until this happens, however, it is likely that the lack of tropical
corals, the resources associated with a coral reef
or the types of habitat available within a coral reef
will significantly limit the successful recruitment
and thereby the range extensions of coral reef
fishes into temperate environments.
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
603
Tropical vagrant fishes D A Feary et al,
Approximately 10% of coral reef fishes can be
classified as coral dependent at some part of their life
stage (Pratchett et al. 2008b). These fishes include
obligate coral settlers or dwellers (Munday et al.
1997; Gardiner and Jones 2005; Feary et al. 2007b)
and corallivores (Pratchett 2005). As reductions in
coral cover nearly always cause corresponding
declines in the abundances of such coral-dependent
species (Wilson et al. 2006; Feary et al. 2007a; Emslie et al. 2011), we predict that reliance on coral
resources is likely to constrain the shifts of these species into temperate reef habitats (Fig. 5). In addition,
some reef fish families as a whole are more reliant
on live coral cover than others, with a higher proportion of species in diverse reef fish families such as
the butterflyfish (Chaetodontidae), cardinalfish
(Apogonidae) and gobies (Gobiidae) known to be
closely associated with live coral cover (Pratchett
2005; Pratchett et al. 2008b). If the degree of live
coral cover is important in structuring settlement, or
early survival of these families, we can expect these
families to show the lowest levels of abundance and
diversity within temperate reef habitats.
Habitat association and settlement preferences
Proportional abundance
We can predict that the availability of specific
coral types at settlement will not be the only
90
GBR
80
NSW
70
60
50
40
30
20
10
0
Low
Med
High
Coral association
Figure 5 Coral habitat association between tropical
vagrants and tropical non-vagrants (using Wilson et al.
2006; Froese and Pauly 2012) comparing fishes
surveyed within the Swain sector within the Australian
Institute of Marine Science Long Term Monitoring
Project (AIMS LTMP unpublished data) and tropical
vagrant surveyed throughout NSW (D.J. Booth,
unpublished data). Coral habitat association is divided
into three categories: (i) those that settle, dwell or feed
on the reef (‘high’ association), (ii) those that are
associated with the reef structure (‘medium’ association)
and (iii) those that are not associated with the reef (‘low’
association).
604
factor limiting the success of tropical vagrants in
colonizing temperate reef habitats. There are a
range of factors, independent of live coral cover,
which can be used to potentially predict the successful settlement and recruitment of tropical reef
fish assemblages (Caley et al. 1996; Booth and
Wellington 1998; Leis and McCormick 2002).
These factors include, but are not limited to, the
availability of suitable trophic resources (Booth
and Hixon 1999), habitat complexity (Holbrook
et al. 2002b), prior resident density (Sweatman
1988; Booth 2004) and the composition of predator assemblages (Beukers-Stewart and Jones 2004;
Beukers-Stewart et al. 2011). Understanding the
role of such factors in structuring species-specific
settlement in tropical assemblages will be vital in
predicting potential vagrant species.
Tropical species that show distinct settlement
preferences (i.e. settlement habitat specialists)
would be expected to be much more limited in
their ability to utilize habitats and environments
beyond their normal latitudinal limits, compared
with more generalized settlement resource use (i.e.
settlement habitat generalists). For example,
within a range of group-forming planktivorous
damselfishes (e.g. Dascyllus complex), specific habitats (i.e. structurally complex corymbose corals)
are fundamental to successful individual settlement (Holbrook et al. 2002a,b) and post-settlement survival (Holbrook and Schmitt 2002). For
these species, we can predict that the lack of these
specific habitats may result in low or non-existent
settlement of this species complex within temperate reef environments. In support, there is little
evidence to suggest that any of the Dascyllus species found within the GBR [i.e. Whitetail dascyllus
(Dascyllus aruanus, Pomacentridae), Blacktail humbug (Dascyllus melanurus, Pomacentridae) and
Threespot dascyllus (Dascyllus trimaculatus, Pomacentridae)] settle and survive in habitats within
temperate NSW (Booth et al. 2007), despite being
found in relatively high abundances throughout
the southern limits of the GBR and within subtropical coral reef habitats in northern NSW (Scott
and Harrison 2008).
Morphologically, temperate benthic reef systems
are substantially different from their tropical counterparts (Ebeling and Hixon 1991; Kingsford and
Battershill 1998), and we can predict that structural differences in benthic communities between
temperate and tropical ecosystems will substantially affect the composition of tropical vagrants
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
Tropical vagrant fishes D A Feary et al.,
settling in temperate reefs. Shallow temperate
reefs, especially within south-east Australia, form
a mosaic of habitats, dominated by large stands of
laminarian and fucoid algae (e.g. Ecklonia radiata,
Sargassum species) and relatively barren rocky substrata with low coralline turfing or crustose algal
populations (termed ‘urchin barrens’) (Underwood
et al. 1991). We may predict that tropical vagrant
larvae may show avoidance behaviour towards
habitats dominated by macroalgae, due to both
the physical movement of such habitats associated
with wave action and relatively low levels of topographical complexity (and therefore fine-scale microshelter for new settlers) (Kingsford and Carlson
2010). In fact, recent evidence suggests that settlement of tropical vagrants is closely associated with
urchin barren habitats, specifically within finescale cracks and crevices where urchins have
cleared algae (H.J. Beck, unpublished data). Such
habitats are also preferred settlement habitats
within a range of temperate reef fish species
(Kingsford and Carlson 2010).
Dietary preferences and functional groups
Although the availability of habitat resources may
be important in constraining vagrant success
within temperate systems, resource requirements
will be further constrained by specific dietary
requirements. Obligate coral-feeding butterflyfishes,
for example, will be unlikely to recruit into habitats devoid of extensive cover of preferred coral
species (Pratchett et al. 2008a). Accordingly, the
overwhelming majority of Chaetodon butterflyfishes
recorded in surveys of vagrant fishes along the
NSW coast are non-coral or facultative coral feeders, including non-coral benthic invertebrate feeders (Threadfin butterflyfish, Crochet butterflyfish
(C. guentheri, Chaetodontidae), Vagabond butterflyfish), soft coral specialists (Blackback butterflyfish)
and generalist benthic foragers (Speckled butterflyfish, Black butterflyfish, Sunburst butterflyfish and
Raccoon butterflyfish). Obligate coral-feeding butterflyfishes have been sighted (e.g. Blueblotch butterflyfish (Chaetodon plebeius, Chaetodontidae));
however, they are exceptionally rare within surveys (D.J. Booth, unpublished database) despite
their high relative abundance in the southern
GBR (i.e. Swain sector). This suggests that the
availability of specific prey will strongly constrain
range extensions for highly specialized reef fishes,
but three mechanisms may occur: these fishes
may have limited larval dispersal to reefs devoid of
coral, or not settle on these reefs, or experience
rapid early post-settlement mortality if settlement
occurs on reefs devoid of coral.
For some tropical reef fish species, differences in
the availability of specific prey resources may not
necessarily constrain settlement and immediate
survivorship (Booth et al. 2007; Figueira et al.
2009), but the lack or limited availability of certain resources may lead to marked physiological
changes (e.g. growth and development) or reduced
fitness. For example, Pratchett et al. (2004) found
little change in the population abundance of an
obligate coral-feeding butterflyfish, the Oval butterflyfish (Chaetodon lunulatus, Chaetodontidae),
two years after extensive coral loss on reefs in the
central GBR. However, there were significant
declines in the physiological condition of populations, likely to have resulted from declines in the
quantity and quality of available coral prey
(Pratchett et al. 2004). Likewise, Feary et al.
(2009) found little effect on individual persistence
following experimental coral loss within groups of
two planktivorous damselfish species (Goldtail
demoiselle (Chrysiptera parasema, Pomacentridae)
and Blacktail humbug). However, growth rates of
both species (quantified over a 29-day period)
were directly related to percentage live coral cover;
individuals within colonies with reduced live coral
exhibited slower morphometric growth than those
within colonies with high live coral cover (Feary
et al. 2009). Therefore, although tropical fishes
may be able to successfully settle and persist
within suitable temperate reef habitats (Booth
et al. 2007; Figueira et al. 2009), the full impact
on each species population following such settlement may take months to years to become apparent. Thus, instead of an immediate reduction in
the abundance of tropical vagrants following settlement, populations may maintain their numbers
over a relatively prolonged time period (Choat
et al. 1988). For example, the Lord Howe Island
butterflyfish (Amphichaetodon howensis, Chaetodontidae) is a relatively common subtropical species found within the northern islands of the Poor
Knights Islands, New Zealand. Although paired
individuals of the Lord Howe Island butterflyfish
have been consistently surveyed since the early
1970s (e.g. Russell 1971), there is still no evidence to suggest species replenishment is associated with local reproduction. Rather, population
replenishment appears to be due solely to the
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
605
Tropical vagrant fishes D A Feary et al,
continual immigration of larvae from tropical and
subtropical locations.
Section 3: Future research needs
Aside from established topics of research on traits
that may facilitate or impede range shifts of tropical reef fish species (e.g. larval biology and ecology, post-settlement resource use), there are
several other key areas of future research needed
to understand range shifts among tropical species.
This is predominantly because tropical fishes provide some of the most extreme examples in geographical range expansion (Booth et al. 2007;
Figueira et al. 2009) compared with other perciform fishes. The most important topics, addressed
in turn, are behavioural ecology and biomechanics, habitat use of subtropical reefs, physiology,
predation and competition with temperate residents. This is by no means a comprehensive list of
potential future research topics, but we present
these topics with the hope of stimulating even
more research on tropical vagrant fishes.
There is still little understanding of the importance of subtropical (i.e. marginal) coral reefs in
providing a ‘habitat refuge’ from the impacts of
climate change for coral reef fish communities.
Although this review has focused on temperate
reef habitats, there is considerable overlap in tropical and subtropical reef fish community structure
(Malcolm et al. 2007, Malcolm et al. 2010). We
may expect that tropical vagrants that successfully
utilize subtropical reef systems (i.e. are able to survive and reproduce) may be more likely to settle
and survive within temperate reef systems (see
Section 2). To date, research on the use of subtropical reefs by tropical vagrants has predominantly focused on how the structure and
composition of these populations vary between
tropical and subtropical reef systems. Such studies
have shown that while there is considerable overlap in community structure between these systems,
marginal reefs typically have lower abundance
and, more notably, lower diversity than tropical
reef systems (Feary et al. 2010; Pratchett et al.
2012). Such differences in community structure
may be partly associated with subtropical reefs
having greater seasonal variation in oceanographic factors than their lower-latitude counterparts (Riegl et al. 2011; Feary et al. 2012). In
particular, seasonal variations in seawater temperature of up to 12 °C are relatively common on
606
subtropical and high-latitude reefs (i.e. Japan: 16–
28 °C; Lord Howe Island: 17–27 °C; Gulf of
Oman: 22–32 °C). Therefore, understanding how
such extremes in oceanographic variables affect
the resource acquisition (i.e. feeding rates,
resource use and competition) (Pratchett et al.
2012), and energy demands and physiology (e.g.
metabolic rates and swimming abilities) of tropical
fishes on such reefs may not only provide a mechanistic basis for the factors that structure tropical
fish communities on these marginal reefs, but will
provide important insights into how reef fish families may acclimate or adapt to environmentally
extreme ecosystems.
Successful establishment of certain tropical reef
fishes within temperate regions may be associated
with specific dietary requirements (see Section 2
above). For tropical herbivorous fishes, the often
high abundance of micro- and macroalgae within
temperate reef habitats means that ‘food’ availability per se may not necessarily constrain survivorship (Booth et al. 2007; Figueira et al. 2009).
However, the lack of, or limited availability of, specific tropical trophic resources (i.e. warm-water
algal species with which the vagrants have historically co-occurred) may lead to marked physiological reductions in fishes condition (Pratchett et al.
2004). In particular, we may expect that for tropical fishes evolved to utilize specific tropical algae,
the use of temperate algal species may affect their
physiological condition. This may happen directly
through novel chemical defences of the new foods
or reduction in assimilation rates, or it may be
mediated by changes in gut microflora, a key consideration for almost all herbivorous consumers,
including humans (e.g. recent studies of the
human gut ‘microbiome’: Nicholson et al. 2012).
An established gut microbiota is essential for the
healthy physiological and immunological development of most animals, with changes in biota having substantial effects on nutrient utilization and
therefore physiological performance. Therefore,
although tropical fishes may be transported to and
successfully settle within temperate habitats
(Booth et al. 2007; Figueira et al. 2009), to persist
they must be able to consume dietary resources
that are suboptimal or novel. Species-specific differences in tropic ecology within these habitats (i.e.
associated with both feeding and nutrient assimilation) may then have substantial effects on population persistence and, ultimately, success of these
vagrants.
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
Tropical vagrant fishes D A Feary et al.,
Predation is a major source of mortality for
early life stages of tropical fish (Hixon and Beets
1993; Planes and Lecaillon 2001; Doherty et al.
2004), and minimizing lethal interactions with
predators is critical to successful population establishment in temperate areas. Predation within the
first 7 days accounts for up to 78% mortality of
recently settled juveniles in tropical reef fishes
(Doherty and Sale 1986; Victor 1986; McCormick
1998), and mortality during this period is likely to
have a disproportionate effect on the size of tropical populations (critical period hypothesis, sensu
Suthers 1998). Therefore, we can expect that tropical fish species that are relatively successful at
avoiding temperate predators, both during and
immediately following settlement, are more likely
to survive in temperate systems. This will be
important given that for tropical vagrants, all temperate ‘predators’ within temperate environments
will be novel, with the potential for substantial
predation risk within temperate environments.
However, the traits that may influence predation
risk of juvenile tropical reef fish still remain poorly
understood (McCormick 1998). Selective mortality
has been linked to variation in numerous morphological and physiological traits (Hixon 1991,
2011). Although contradictory evidence exists
(Holmes and McCormick 2009, 2010), numerous
studies have reported enhanced survival of recruits
and juveniles that were larger for a given age
(Sponaugle and Grorud-Covert 2006; Sponaugle
et al. 2011). Tropical vagrant species with larger
size at settlement may therefore be more likely to
succeed within temperate environments. To test
whether size at settlement differs between tropical
vagrants and temperate residents, where possible
we compared the log mean size at settlement of
tropical vagrant (n = 15) and temperate residents
(n = 41). We found that there was no substantial
difference between groups; log mean size at settlement (mm) (95% CI) for tropical vagrants was
2.28 (0.055), while the log mean size at settlement for temperate residents was 2.47 (0.065).
Predator recognition by juvenile reef fish is a
vital factor affecting the outcome of predator–prey
interactions (Almany and Webster 2004; Almany
et al. 2007b), with higher mortality observed in
individuals with reduced ability to identify potential threats (McCormick and Holmes 2006; Loennstedt et al. 2012). The majority of research
focusing on tropical fishes has examined the effect
of prior experience on subsequent predator
recognition (learned responses) and has indicated
that individuals previously exposed to visual and
chemical cues associated with predators have a
greater chance than naive individuals of surviving
predatory encounters (Lonnstedt et al. 2012; Manassa and McCormick 2012). However, the likelihood that initial (non-learned) abilities to
recognize predators may vary among tropical
vagrants suggests that predation risk during initial
predatory encounters will also substantially differ
among species settling in temperate environments.
Although based on a relatively small subset of
tropical vagrant species, recent work has shown
that there are substantial changes in the behaviour of tropical species when exposed to temperate
predators, including reduced feeding rates and
increased sheltering (H.J. Beck, unpublished data).
We predict that tropical vagrants that are initially
better at recognizing temperate predators, or learn
to recognize them more rapidly, may experience
reduced predation risk during settlement and early
recruitment and are able to successfully establish
temperate populations.
Despite the increasing abundance of tropical fish
species within temperate reef systems, little is
known of their competitive abilities in temperate
environments. Recent evidence suggests that relative activity levels and feeding rates of tropical
range-shifting species compared with temperate
residents are dependent on habitat availability and
temperature fluctuations (H.J. Beck, unpublished
data). Therefore, research into competitive interactions between temperate and tropical species and
how these interactions may be influenced and
mediated by temperature and habitat availability
is necessary. As space limitation is important in
determining juvenile abundance in numerous siteattached tropical fish species (Hixon and Beets
1989; Munday et al. 2001; Holbrook and Schmitt
2002; Bonin et al. 2009), we hypothesize that
competition for temperate macroalgal resources
both during and following settlement may have
substantial consequences for the abundance and
diversity of tropical range-shifting species within
temperate ecosystems and the potential impact on
the temperate resident fishes.
Conclusions
An understanding of both the extrinsic and intrinsic processes that are likely to influence the spatial, temporal and taxonomic biases in tropical
© 2013 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 15, 593–615
607
Tropical vagrant fishes D A Feary et al,
vagrant community structure will be vital in predicting the repercussions for tropical fishes with
increased changes in global climate. It can be
assumed that extrinsic processes (e.g. currents,
environmental temperature) will interact with
inherent differences in the life histories of fishes to
determine what species settle into temperate
regions, when these species settle and where.
However, intrinsic processes constraining the
movement and population success of tropical
vagrants are key to understanding which species
will move and which will not and which species
will become susceptible to sustained and ongoing
climate change. This review has shown that tropical species with viable populations near the latitudinal margins of reef development (high-latitude
reefs) will be expected to show substantial changes
in distribution. In this respect, we can also expect
that adaptation to changes in local water temperature may occur more rapidly in small-bodied,
short-lived species, where selection can operate
over a large number of generations. Larger species,
with much longer generation times, may have
reduced ability to adapt to temperate regions. To
our knowledge, successful reproduction in tropical
vagrants has not occurred within temperate
regions, with all observed population expansion
driven solely by larval input from tropical sources
(however, see Kokita 2004). However, with
increasing warming of waters, we can expect that
the physical variables constraining reproduction
will reduce (i.e. increased growth rates in individuals, development of reproductively active individuals) and viable breeding populations of tropical
vagrants will increase within temperate regions.
Acknowledgements
DAF was funded by the University of Technology,
Sydney, under the Chancellors Postdoctoral Fellowship scheme. OJL was supported by a doctoral
fellowship grant provided by the Sydney Institute
of Marine Science. Thanks to Nicolas Bailly (Fishbase) for providing data. This paper is contribution 87 from the Sydney Institute of Marine
Science.
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Supporting Information
Additional Supporting Information may be found
in the online version of this article:
Data S1. Full list of all tropical reef associated
fish species (Family and species) that have been
identified as utilising temperate reef habitats
within larval, sub-adult or adult phase.
Data S2. Methods for logistic analyses.
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