Latitudinal shifts in coral reef fishes: why some species doand 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

1School 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

AbstractClimate 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 success-

ful establishment of populations in temperate regions. We review the factors likely

to affect population establishment, including larval supply, settlement and post-set-

tlement 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 popula-

tions, 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 reli-

ance on coral resources.

Keywords Climate change adaptation, global warming, range shifts, temperate

reef, tropical reef fishes, tropical vagrant

Correspondence:

David A Feary,

School of the Envi-

ronment, University

of Technology,

Sydney, 123 Broad-

way, NSW 2007,

Australia

Tel.: +61 2 9514

4068

Fax: +61 2 9514

4079

E-mail: david.

feary@uts.edu.au

Received 10 Sep

2012

Accepted 6 Mar

2013

Introduction 2

Scope of this review 2

Section 1 Extrinsic factors regulating arrival of tropical vagrants 4

Oceanographic factors 4

Large-scale ocean currents 4

Ocean eddies 6

Section 2 Intrinsic factors constraining latitudinal population movement 6

Environmental constraints to distributional shifts 6

Population density and latitudinal distribution 7

Life-history traits associated with vagrancy 8

Correlations between species-specific traits in predicting vagrancy 11

© 2013 John Wiley & Sons Ltd DOI: 10.1111/faf.12036 1

F I SH and F I SHER I E S

Resource constraints to vagrant success 11

Habitat association and settlement preferences 12

Dietary preferences and functional groups 13

Section 3 Future research needs 14

Conclusions 15

Acknowledgements 16

References 16

Introduction

A central premise of biogeography is that the natu-

ral distribution of a species is at least partly gov-

erned 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 inci-

dence 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 advan-

tage of high-latitude locations which they could not

otherwise tolerate (Parmesan and Yohe 2003; Hoe-

gh-Guldberg and Bruno 2010).

To date, poleward shifts in species geographical

distribution are most apparent for terrestrial plants

and animals (Parmesan and Yohe 2003; Parme-

san 2006; Burrows et al. 2011). However, there is

increasing evidence of range shifts among marine

fishes and invertebrates, especially at high lati-

tudes in the Northern Hemisphere (Dulvy et al.

2008; Nye et al. 2009; Stefansdottir et al. 2010).

This bias in recorded range shifts (between hemi-

spheres 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

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 (Sei-

del 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 lati-

tudes (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’ dis-

tributional 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 mount-

ing 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 com-

munities (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 et al. 2011), tropical fish species may

be particularly sensitive to increasing temperatures

2 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

as they exist in a relatively thermostable environ-

ment (Hoegh-Guldberg et al. 2007). Most tropical

fishes may not live within environments that are

close to their lethal thermal limits (Mora and

Osp�ına 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 assem-

blages and the potential changes this may have in

the composition and structure of tropical fish com-

munities (Munday et al. 2008a,b). Indeed, there is

mounting evidence to suggest that marine organ-

isms have shown average geographical shifts asso-

ciated with climate-mediated global thermal shifts

from 1.5 to 5 times faster than their terrestrial

counterparts (termed ‘climate velocity’, sensu Bur-

rows et al. 2011). The question then is what are

the factors that may allow tropical coral reef spe-

cies 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. Elasmo-

branchii: Last et al. 2011), these studies are out-

side 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 win-

ter-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 (Figue-

ira and Booth 2010; Booth et al. 2011; Madin

et al. 2012; Soeparno et al. 2012).

We examine both the intrinsic and extrinsic pro-

cesses that likely influence the spatial, temporal

and taxonomic biases in the species-specific struc-

ture 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 deter-

mine 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 tropi-

cal and temperate regions. Determining the intrin-

sic 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 suc-

cessful advection of tropical vagrants into high-lat-

itude temperate regions. Cheung et al. (2010) in

their global analysis on the redistribution of mar-

ine fishes suggested that range shifts are likely to

be constrained by specific resource (prey or habi-

tat) 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 trop-

ical 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’) (Supplemen-

tary Data S1). Despite this, vagrants still appear

relatively uncommon within families (Fig. 2).

Tropical vagrants include a disproportionate num-

ber 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

vagrant surveys, including the Apogonidae, Calli-

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 3

Tropical vagrant fishes D A Feary et al.,

onymidae, 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 major-

ity 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 arrivalof tropical vagrants

Oceanographic factors

Most marine organisms have a bipartite life his-

tory, characterized by a sessile (often reproductive)

phase and highly dispersive (often larval) phase

(Leis et al. 2011). As our knowledge regarding the

physiology and behaviour of larval marine organ-

isms grows, it is becoming increasingly apparent

that contrary to initial speculation, many larvae

possess complex behavioural abilities (including

swimming and orientation behaviour) (Leis and

Carson-Ewart 1998; Leis et al. 2002, 2003,

2007). Indeed, relatively high levels of local larval

retention and self-recruitment (settlement of

locally spawned larvae: up to 40–60%) have been

shown (Jones et al. 1999, 2005; Swearer et al.

1999, 2002; Thorrold et al. 2001; Almany et al.

2007a; Harrison et al. 2012). However, the corol-

lary of this means that 40–60% of a reef fish pop-

ulation may be exported long distances away from

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. orienta-

tion: Paris and Cowen 2004; Dixson et al. 2012).

Overall, however, we can predict that physical dis-

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.

4 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

persal factors may play an important physical role

in determining species-specific differences in move-

ment of larval marine organisms, especially during

the early larval period. Thus, the connectivity

afforded by physical oceanography will play an

important role in structuring shifts in the distribu-

tion of tropical fish populations into temperate

areas.

Large-scale ocean currents

Given the typically large spatial extent covered by

dispersing tropical vagrants (which can be on the

order of 1000s of km) (e.g. Booth et al. 2007;

Booth and Parkinson 2011), large-scale offshore

currents are likely to play a central role in their

transport. This has been suggested for temperate–

tropical connectivity within the Gulf Stream

(McBride and Able 1998; Hare and Cowen 1991;

McBride 1996), the Kuroshio Current (Nakazono

2002), as well as the Leeuwin Current and East

Australian Current (EAC) (Hutchins 1991; Hutch-

ins and Pearce 1994; Figueira and Booth 2010).

These currents are located off the continental

shelf in deep water, largely free of topographical

obstructions, and typically have non-turbulent

unidirectional flow promoting the rapid transport

of entrained particles away from a natal site via

advection (Sponaugle et al. 2002). Sharp density

gradients at current boundaries limit mixing with

surrounding temperate waters, maintaining the

tropical physical environment of these waters.

Although such gradients may also serve as barri-

ers to cross-shelf transport of larvae to inshore

habitat in temperate coastal regions, the degree

to which such limitations can occur will vary.

For instance, along the east coast of Australia,

the EAC has been identified as a relatively strong

barrier to onshore transport (Choukroun et al.

2010; Condie et al. 2011; Roughan et al. 2011).

Figure 2 Estimation of the total number of vagrants

that would be expected by species richness given each

family’s total species number. Lines to the left of the

centre line signify families with a significantly lower

proportion of vagrants than expected; lines to the right

of the centre line signify families with a significantly

higher proportion of vagrants than expected; lines that

cross the centreline signify no significant pattern in

vagrant abundance within families (See Supplementary

Data S2).

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 5

Tropical vagrant fishes D A Feary et al.,

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 trans-

port 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 self-

recruitment 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 cur-

rents, but may also be important in trapping lar-

vae 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 Hat-

teras have been implicated in the transport of lar-

vae towards coastal waters of not only

cosmopolitan temperate fish larvae (Hare and Co-

wen 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 con-

tain larval fish assemblages uniquely different

from the surrounding waters (Keane and Neira

2008; Syahailatua et al. 2011). The dynamic nat-

ure 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).

Section 2: Intrinsic factors constraininglatitudinal population movement

Environmental constraints to distributional shifts

Temperature is one of the primary variables regu-

lating aquatic species bioenergetics (Kitchell et al.

1977). Ambient temperatures substantially deter-

mine physiological processes such as feeding, res-

piration, 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 hab-

itats. We can predict that for warm-adapted tropi-

cal 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 parame-

ters may only be maximized for a short time

frame. Below, we examine the potential impor-

tance of physiological constraints to successful lati-

tudinal extension in tropical reef fish populations.

Environmental temperature is one of the most

important physical variables affecting the perfor-

mance of ectotherms (Hazel and Prosser 1974;

Hurst 2007). Therefore, we can expect that one of

the most important factors in structuring the suc-

cess of tropical vagrants within temperate environ-

ments will be species-specific thermal limits for

minimum environmental temperature (Attrill and

Power 2002; Dulvy et al. 2008; Poertner and Far-

rell 2008). Virtually, all aspects of the behaviour

and physiology of ectotherms are sensitive to envi-

ronmental temperature (Hazel and Prosser 1974;

Poertner and Farrell 2008). Therefore, we can

expect that among tropical vagrants, the predomi-

nant source of mortality in temperate environ-

ments 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

6 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

examining overwintering success have focused on

temperate freshwater or estuarine fishes, examin-

ing 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 damself-

ishes (Pomacentridae), while Figueira et al. (2009)

showed that for the tropical Indo-Pacific sergeant

(Abudefduf vaigiensis, Pomacentridae), water tem-

peratures needed to be �17 °C to cause substan-

tial 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-east-

ern 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 (Fig-

ueira and Booth 2010). In corroboration with this,

low sea surface temperatures (SSTs) at tropical/

temperate transition zones also support the predic-

tion 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 abun-

dant. 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 rela-

tively rare, or locally uncommon, are unlikely to

have high numbers of larvae exported to reefs dis-

tant 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 spe-

cies abundance is associated with geographical

range, with numerous accounts of both spatially

restricted and non-restricted fishes with little differ-

ence in total abundance (Jones et al. 2002; Hobbs

et al. 2010, 2012). To examine whether the abun-

dance of tropical reef fish species within the natal

habitat [southern Great Barrier Reef (GBR)] was

an important predictor of tropical vagrant occur-

rence within the adjacent temperate reef habitat

(NSW), we used a logistic regression analysis and

compared the total abundance of 24 butterflyfish-

es, 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 simi-

larity 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, Chae-

todontidae)), one of the most abundant butterfly-

fish within the Swain sector (i.e. Blackback

butterflyfish (Chaetodon melannotus, Chaetodonti-

dae) was the least abundant species in tropical

vagrant surveys within NSW.

Tropical reef fish populations may be widely dis-

tributed, 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

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 7

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 latitudi-

nal 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 understand-

ing the mechanisms responsible for Rapoport’s

rule, the increase in the latitudinal extents of

occurrence of species towards higher latitudes (Ste-

vens 1989). Although there is evidence to suggest

that species upper thermal limits may show a geo-

graphical variation (Stillman and Somero 2000),

recent work has shown that lower lethal tempera-

tures 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/tem-

perate 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 distribu-

tions truncated in low latitudes are unlikely to

form vagrant communities, while those with distri-

butions 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 abun-

dance of butterflyfishes (as a percentage of total

abundance) surveyed in both high-latitude (Capri-

corn Bunker group) and low-latitude (Lizard

Island/Cooktown Sector) regions (using data from

Emslie et al. 2010) and compared it with butter-

flyfishes surveyed throughout NSW (sensu Booth

et al. 2007) (Table 1). Tropical vagrants surveyed

in NSW were more likely to show higher abun-

dances in high-, than low-latitude regions

(Table 1). Of the seven butterflyfish species sur-

veyed within temperate NSW waters, five species

(Sunburst butterflyfish (Chaetodon kleinii, Chae-

todontidae), Black butterflyfish, Speckled butterfly-

fish (C. citrinellus, Chaetodontidae), Raccoon

butterflyfish (Chaetodon lunula, Chaetodontidae)

and Blackback butterflyfish) were predominantly

the most important butterflyfish species (as a per-

centage of total abundance) surveyed in the high-

latitude region. In comparison, the majority of

tropical vagrants were not abundant in the low-

latitude region, although the Threadfin butterfly-

fish 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, espe-

cially 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 flexi-

bility in their larval dispersal characteristics. For

example, recent work strongly suggests dual strat-

egies in many tropical fish species: that is, local-

ized 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, dis-

persal distance has also been shown to be indepen-

dent of PLD for numerous species in multiple

locations; there are many fish species with rela-

tively 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. Chae-

todontidae) were relatively more common than

taxa with relatively shorter PLDs (e.g. Pomacentri-

dae) 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

8 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

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 non-

vagrant 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 out-

put may substantially increase the probability of

long-distance larval dispersal (Leis 1993; Munday

and Jones 1998). Therefore, to determine whether

body size is associated with vagrants, where possi-

ble, 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 func-

tion 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 spaw-

ners 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; Lo-

Yat et al. 2006). Pelagically spawned larvae are

immediately subject to oceanographic processes,

which may disperse them further than demersally

spawned larvae (Thresher 1984). However, demer-

sally spawned larvae have longer incubation

times, are larger-bodied and have higher developed

sensory and locomotor systems (Thresher 1984;

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 83 C. trifascialis 63.6

C. meyeri 73.9 C. kleinii 49.5

C. reticulatus 72.4 C. flavirostris 38.8

C. ephippium 70.1 C. citrinellus 26.6C. auriga 57.5 C. lunula 16.3

C. bennetti 52.6 C. melannotus 15.3

F. longirostris 51.3 C. rainfordi 15.1

C. lunula 49 C. unimaculatus 13.2F. flavissimus 41.7 C. reticulatus 12.2

C. punctatofasciatus 40.7 F. flavissimus 11.4

C. pelewensis 40.1 C. speculum 11.2

C. ulietensis 38.9 C. ornatissimus 10.2C. vagabundus 38.3 C. plebeius 8.6

C. ornatissimus 35.8 F. longirostris 7.7

C. speculum 33.6 C. lineolatus 7.5C. lunulatus 33 C. pelewensis 6.2

C. plebeius 25 C. lunulatus 6

C. baronessa 23.3 C. auriga 5.4

C. unimaculatus 22.7 C. vagabundus 3.4C. rafflesi 20.1 C. baronessa 2.5

C. aureofasciatus 19.8 C. ephippium 1.2

C. kleinii 17.1 C. rafflesi 0.9

C. trifascialis 15.8 C. aureofasciatus 0.1C. lineolatus 14.6 C. mertensii <0.1

C. mertensii 14.3 C. rostratus 0

C. melannotus 13.1 H. polylepis 0C. rostratus 11.6 C. ulietensis 0

C. rainfordi 7.5 C. punctatofasciatus 0

C. citrinellus 4.9 C. meyeri 0

C. flavirostris 0.8 C. bennetti 0

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 SH and F I SHER IES 9

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 repro-

ductive 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 analy-

sis 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 (Sto-

butzki 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-com-

petent, 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

for retention of fishes within natal waters (Leis

et al. 2011), such differences may also be associ-

ated with potential long-distance dispersal. If swim-

ming ability is associated with potential dispersal,

we can expect tropical vagrants to have greater

larval swimming ability than non-vagrants. There-

fore, 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 criti-

cal speed indicated that fishes with higher swim-

ming 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; McCor-

mick 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 posi-

tively associated with increasing new settler body

size (Sponaugle and Grorud-Covert 2006; Sponau-

gle et al. 2011). We can expect, therefore, that

tropical vagrants may have larger size at settle-

ment 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; Wel-

lington and Robertson 2001; Wellington and Vic-

tor 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 non-

vagrants), seven species (Bicolor chromis (Chromis

margaritifer, Pomacentridae), Nagasaki damsel

(Pomacentrus nagasakiensis, Pomacentridae), Sap-

phire damsel (Pomacentrus pavo, Pomacentridae),Figure 4 Vagrant potential as a function of parental

care type (See Supplementary Data S2).

10 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

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 correla-

tions between traits. For example, temperature is a

major factor determining PLD (O’Connor et al.

2007) and latitudinal range, thus confounding sin-

gle analyses looking at either of these two. In addi-

tion, 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 correla-

tion 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 phylo-

genetic extent of the sample; the potential for a

phylogenetic confound is then potentially high.

Despite these caveats, the need to develop multi-

ple 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: latitudi-

nal 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 ‘fam-

ily’ as a random factor in the binomial GLMM). This

analysis showed that only latitudinal range was sig-

nificant 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 require-

ments (Munday et al. 2008a; Cheung et al. 2010).

In particular, for tropical fishes, temperate reefs

will lack a range of settlement substrates, settle-

ment cues or specific dietary components found on

tropical coral reefs (Harriott and Banks 2002).

Temperate reef habitats are not devoid of sclerac-

tinian corals (Rodolfo-Metalpa et al. 2008; Lien

et al. 2012), and it is possible that tropical reef-

building corals may become increasingly estab-

lished beyond their normal latitudinal limits due

to sustained increases in ocean temperature

(Precht and Aronson 2004; Greenstein and Pan-

dolfi 2008; Yamano et al. 2011). Until this hap-

pens, 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 SH and F I SHER IES 11

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; Ems-

lie et al. 2011), we predict that reliance on coral

resources is likely to constrain the shifts of these spe-

cies 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 pro-

portion 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

We can predict that the availability of specific

coral types at settlement will not be the only

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 suc-

cessful 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 preda-

tor 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 habi-

tats (i.e. structurally complex corymbose corals)

are fundamental to successful individual settle-

ment (Holbrook et al. 2002a,b) and post-settle-

ment 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 temper-

ate reef environments. In support, there is little

evidence to suggest that any of the Dascyllus spe-

cies found within the GBR [i.e. Whitetail dascyllus

(Dascyllus aruanus, Pomacentridae), Blacktail hum-

bug (Dascyllus melanurus, Pomacentridae) and

Threespot dascyllus (Dascyllus trimaculatus, Poma-

centridae)] 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 subtrop-

ical coral reef habitats in northern NSW (Scott

and Harrison 2008).

Morphologically, temperate benthic reef systems

are substantially different from their tropical coun-

terparts (Ebeling and Hixon 1991; Kingsford and

Battershill 1998), and we can predict that struc-

tural differences in benthic communities between

temperate and tropical ecosystems will substan-

tially affect the composition of tropical vagrants

0

10

20

30

40

50

60

70

80

90

Low Med High

Prop

ortio

nal a

bund

ance

Coral association

GBR

NSW

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).

12 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

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 sub-

strata 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 topo-

graphical complexity (and therefore fine-scale mi-

croshelter for new settlers) (Kingsford and Carlson

2010). In fact, recent evidence suggests that settle-

ment of tropical vagrants is closely associated with

urchin barren habitats, specifically within fine-

scale 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 habi-

tats 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 feed-

ers, including non-coral benthic invertebrate feed-

ers (Threadfin butterflyfish, Crochet butterflyfish

(C. guentheri, Chaetodontidae), Vagabond butterfly-

fish), soft coral specialists (Blackback butterflyfish)

and generalist benthic foragers (Speckled butterfly-

fish, Black butterflyfish, Sunburst butterflyfish and

Raccoon butterflyfish). Obligate coral-feeding but-

terflyfishes have been sighted (e.g. Blueblotch but-

terflyfish (Chaetodon plebeius, Chaetodontidae));

however, they are exceptionally rare within sur-

veys (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 cer-

tain 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 but-

terflyfish (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 popula-

tions, 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 settle-

ment may take months to years to become appar-

ent. Thus, instead of an immediate reduction in

the abundance of tropical vagrants following set-

tlement, populations may maintain their numbers

over a relatively prolonged time period (Choat

et al. 1988). For example, the Lord Howe Island

butterflyfish (Amphichaetodon howensis, Chae-

todontidae) is a relatively common subtropical spe-

cies 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 evi-

dence to suggest species replenishment is associ-

ated with local reproduction. Rather, population

replenishment appears to be due solely to the

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 13

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 tropi-

cal reef fish species (e.g. larval biology and ecol-

ogy, 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 pro-

vide some of the most extreme examples in geo-

graphical range expansion (Booth et al. 2007;

Figueira et al. 2009) compared with other perci-

form fishes. The most important topics, addressed

in turn, are behavioural ecology and biomechan-

ics, habitat use of subtropical reefs, physiology,

predation and competition with temperate resi-

dents. 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 impor-

tance 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 tropi-

cal 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 sur-

vive and reproduce) may be more likely to settle

and survive within temperate reef systems (see

Section 2). To date, research on the use of sub-

tropical reefs by tropical vagrants has predomi-

nantly 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 over-

lap 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 oceano-

graphic factors than their lower-latitude counter-

parts (Riegl et al. 2011; Feary et al. 2012). In

particular, seasonal variations in seawater temper-

ature of up to 12 °C are relatively common on

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 mech-

anistic basis for the factors that structure tropical

fish communities on these marginal reefs, but will

provide important insights into how reef fish fami-

lies 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’ availabil-

ity per se may not necessarily constrain survivor-

ship (Booth et al. 2007; Figueira et al. 2009).

However, the lack of, or limited availability of, spe-

cific tropical trophic resources (i.e. warm-water

algal species with which the vagrants have histori-

cally co-occurred) may lead to marked physiologi-

cal reductions in fishes condition (Pratchett et al.

2004). In particular, we may expect that for tropi-

cal 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 con-

sideration 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 develop-

ment of most animals, with changes in biota hav-

ing 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 differ-

ences in tropic ecology within these habitats (i.e.

associated with both feeding and nutrient assimila-

tion) may then have substantial effects on popula-

tion persistence and, ultimately, success of these

vagrants.

14 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

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 estab-

lishment 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 tropi-

cal populations (critical period hypothesis, sensu

Suthers 1998). Therefore, we can expect that trop-

ical 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 tem-

perate ‘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 morpho-

logical 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 settle-

ment (mm) (�95% CI) for tropical vagrants was

2.28 (�0.055), while the log mean size at settle-

ment 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 poten-

tial threats (McCormick and Holmes 2006; Loenn-

stedt 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; Man-

assa and McCormick 2012). However, the likeli-

hood 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 behav-

iour 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 rela-

tive 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 interac-

tions 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 site-

attached 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 intrin-

sic processes that are likely to influence the spa-

tial, temporal and taxonomic biases in tropical

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 15

Tropical vagrant fishes D A Feary et al.,

vagrant community structure will be vital in pre-

dicting 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 tropi-

cal species with viable populations near the latitu-

dinal 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 tempera-

ture 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 individu-

als, development of reproductively active individu-

als) 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 Fel-

lowship scheme. OJL was supported by a doctoral

fellowship grant provided by the Sydney Institute

of Marine Science. Thanks to Nicolas Bailly (Fish-

base) for providing data. This paper is contribu-

tion 87 from the Sydney Institute of Marine

Science.

References

Abesamis, R.A. and Russ, G.R. (2010) Patterns of

recruitment of coral reef fishes in a monsoonal envi-

ronment. Coral Reefs 29, 911–921.

Addo-Bediako, A., Chown, S.L. and Gaston, K.J. (2000)

Thermal tolerance, climatic variability and latitude.

Proceedings of the Royal Society London B 267, 739–745.

Almany, G.R. and Webster, M.S. (2004) Odd species out

as predators reduce diversity of coral-reef fishes. Ecol-

ogy 85, 2933–2937.

Almany, G.R., Berumen, M.L., Thorrold, S.R., Planes, S.

and Jones, G.P. (2007a) Local replenishment of coral

reef fish populations in a marine reserve. Science 316,

742–744.

Almany, G.R., Peacock, L.F., Syms, C., McCormick, M.I.

and Jones, G.P. (2007b) Predators target rare prey in

coral reef fish assemblages. Oecologia 152, 751–761.

Attrill, M.J. and Power, M. (2002) Climatic influence on

a marine fish assemblage. Nature 417, 275–278.

Beukers-Stewart, B.D. and Jones, G.P. (2004) The influ-

ence of prey abundance on the feeding ecology of two

piscivorous species of coral reef fish. Journal of Experi-

mental Marine Biology and Ecology 299, 155–184.

Beukers-Stewart, B.D., Beukers-Stewart, J.S. and Jones,

G.P. (2011) Behavioural and developmental responses

of predatory coral reef fish to variation in the abun-

dance of prey. Coral Reefs 30, 855–864.

Bonin, M.C., Srinivasan, M., Almany, G.R. and Jones,

G.P. (2009) Interactive effects of interspecific competi-

tion and microhabitat on early post-settlement survival

in a coral reef fish. Coral Reefs 28, 265–274.

Booth, D.J. (2004) Synergistic effects of conspecifics and

food on growth and energy allocation of a damselfish.

Ecology 85, 2881–2887.

Booth, D.J. and Hixon, M.A. (1999) Food ration and con-

dition affect early survival of the coral reef damselfish,

Stegastes partitus. Oecologia 121, 364–368.

Booth, D.J. and Parkinson, K. (2011) Pelagic larval dura-

tion is similar across 23A degrees of latitude for two

species of butterflyfish (Chaetodontidae) in eastern

Australia. Coral Reefs 30, 1071–1075.

Booth, D.J. and Wellington, G. (1998) Settlement prefer-

ences in coral-reef fishes: effects on patterns of adult

and juvenile distributions, individual fitness and popu-

lation structure. Australian Journal of Ecology 23, 274–

279.

Booth, D.J., Figueira, W.F., Gregson, M.A., Brown, L. and

Beretta, G. (2007) Occurrence of tropical fishes in tem-

perate southeastern Australia: role of the East Austra-

lian Current. Estuarine Coastal and Shelf Science 72,

102–114.

Booth, D.J., Bond, N. and Macreadie, P. (2011) Detecting

range shifts among Australian fishes in response to cli-

mate change. Marine and Freshwater Research 62,

1027–1042.

Brogan, M.W. (1994) Distribution and retention of larval

fishes near reefs in the Gulf of California. Marine Ecol-

ogy Progress Series 115, 1–13.

Brunton, B.J. and Booth, D.J. (2003) Density- and size-

dependent mortality of a settling coral-reef damselfish

16 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

(Pomacentrus moluccensis Bleeker). Oecologia 137,

377–384.

Burrows, M.T., Schoeman, D.S., Buckley, L.B. et al.

(2011) The pace of shifting climate in marine and ter-

restrial ecosystems. Science 334, 652–655.

Caley, M.J., Carr, M.H., Hixon, M.A., Hughes, T.P., Jones,

G.P. and Menge, B.A. (1996) Recruitment and the

local dynamics of open marine populations. Annual

Review of Ecology and Systematics 27, 477–500.

Carnaval, A.C. and Moritz, C. (2008) Historical climate

modelling predicts patterns of current biodiversity in

the Brazilian Atlantic forest. Journal of Biogeography

35, 1187–1201.

Cheal, A., Emslie, M., Miller, I. and Sweatman, H. (2012)

The distribution of herbivorous fishes on the Great

Barrier Reef. Marine Biology 159, 1143–1154.

Cheung, W.W.L., Lam, V.W.Y., Sarmiento, J.L. et al.

(2010) Large-scale redistribution of maximum fisheries

catch potential in the global ocean under climate

change. Global Change Biology 16, 24–35.

Choat, J.H. and Robertson, D.R. (eds.) (2002) Age-Based

Studies on Coral Reef Fishes. Academic Press, San Diego.

Choat, J.H., Ayling, A.M. and Schiel, D.R. (1988) Tempo-

ral and spatial variation in an island fish fauna. Jour-

nal of Experimental Marine Biology and Ecology 121,

91–111.

Choukroun, S., Ridd, P.V., Brinkman, R. and McKinna,

L.I.W. (2010) On the surface circulation in the wes-

tern Coral Sea and residence times in the Great Barrier

Reef. Journal of Geophysical Research-Oceans 115, 1–13.

Condie, S.A., Mansbridge, J.V. and Cahill, M.L. (2011)

Contrasting local retention and cross-shore transports

of the East Australian Current and the Leeuwin Cur-

rent and their relative influences on the life histories of

small pelagic fishes. Deep-Sea Research Part Ii-Topical

Studies in Oceanography 58, 606–615.

Cowen, R.K., Lwiza, K.M.M., Sponaugle, S., Paris, C.B.

and Olson, D.B. (2000) Connectivity of marine popula-

tions: open or closed? Science 287, 857–859.

Cowen, R.K., Paris, C.B. and Srinivasan, A. (2006) Scal-

ing of connectivity in marine populations. Science 311,

522–527.

Danilowicz, B.S. (1997) A potential mechanism for epi-

sodic recruitment of a coral reef fish. Ecology 78,

1415–1423.

Davis, C.C., Bell, C.D., Mathews, S. and Donoghue, M.J.

(2002) Laurasian migration explains Gondwanan dis-

junctions: evidence from Malpighiaceae. Proceedings of

the National Academy of Sciences of the United States of

America 99, 6833–6837.

Dixson, D.L., Munday, P.L., Pratchett, M. and Jones, G.P.

(2012) Ontogenetic changes in responses to settlement

cues by Anemonefish. Coral Reefs 30, 903–910.

Doherty, P.J. and Sale, P.F. (1986) Predation on juvenile

coral reef fishes: an exclusion experiment. Coral Reefs

4, 225–234.

Doherty, P.J., Dufour, V., Galzin, R., Hixon, M.A., Mee-

kan, M.G. and Planes, S. (2004) High mortality during

settlement is a population bottleneck for a tropical sur-

geonfish. Ecology 85, 2422–2428.

Domenici, P., Claireaux, G. and McKenzie, D.J. (2007)

Environmental constraints upon locomotion and pred-

ator-prey interactions in aquatic organisms: an intro-

duction. Philosophical Transactions of the Royal Society

B-Biological Sciences 362, 1929–1936.

Donelson, J.M., Munday, P.L., McCormick, M.I. and Nils-

son, G.E. (2011) Acclimation to predicted ocean warm-

ing through developmental plasticity in a tropical reef

fish. Global Change Biology 17, 1712–1719.

Donelson, J.M., Munday, P.L., McCormick, M.I. and

Pitcher, C.R. (2012) Rapid transgenerational acclima-

tion of a tropical reef fish to climate change. Nature

Climate Change 2, 30–32.

Dulvy, N.K., Rogers, S.I., Jennings, S., Stelzenmuller, V.,

Dye, S.R. and Skjoldal, H.R. (2008) Climate change

and deepening of the North Sea fish assemblage: a bio-

tic indicator of warming seas. Journal of Applied Ecology

45, 1029–1039.

Ebeling, A.W. and Hixon, M.A.. (1991) Tropical and

temperate reef fishes: comparison of community

structures. In: The Ecology of Fishes on Coral Reefs (ed.

P.F. Sale). Academic Press, San Diego, CA, pp. 509–

563.

Eme, J. and Bennett, W.A. (2008) Low temperature as a

limiting factor for introduction and distribution of

Indo-Pacific damselfishes in the eastern United States.

Journal of Thermal Biology 33, 62–66.

Emslie, M.J., Pratchett, M.S., Cheal, A.J. and Osborne, K.

(2010) Great Barrier Reef butterflyfish community

structure: the role of shelf position and benthic com-

munity type. Coral Reefs 29, 705–715.

Emslie, M.J., Pratchett, M.S. and Cheal, A.J. (2011)

Effects of different disturbance types on butterflyfish

communities of Australia’s Great Barrier Reef. Coral

Reefs 30, 461–471.

Emslie, M.J., Logan, M., Ceccarelli, D.M. et al. (2012)

Regional-scale variation in the distribution and abun-

dance of farming damselfishes on Australia’s Great

Barrier Reef. Marine Biology 159, 1293–1304.

Feary, D.A., Almany, G.R., Jones, G.P. and McCormick,

M.I. (2007a) Coral degradation and the structure of

tropical reef fish communities. Marine Ecology Progress

Series 333, 243–248.

Feary, D.A., Almany, G.R., McCormick, M.I. and Jones,

G.P. (2007b) Habitat choice, recruitment and the

response of coral reef fishes to coral degradation. Oeco-

logia 153, 727–737.

Feary, D.A., Burt, J.A., Bauman, A.G., Usseglio, P., Sale,

P.F. and Cavalcante, G.H. (2010) Fish communities on

the world’s warmest reefs: what can they tell us about

the effects of climate change in the future? Journal of

Fish Biology 77, 1931–1947.

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 17

Tropical vagrant fishes D A Feary et al.,

Feary, D.A., Burt, J.A., Cavalcante, G.H. and Bauman,

A.G.. (2012) Extreme physical factors and the struc-

ture of Gulf communities. In: Coral Reefs of the Gulf:

Adaptation to Climatic Extremes (eds B. Riegl and S.

Purkis). Springer, NL, pp. 163–170.

Feary, D.A., McCormick, M.I. and Jones, G.P. (2009) Growth

of reef fishes in response to live coral cover. Journal of

Experimental Marine Biology and Ecology 373, 45–49.

Figueira, W.F. and Booth, D.J. (2010) Increasing ocean

temperatures allow tropical fishes to survive overwin-

ter in temperate waters. Global Change Biology 16,

506–516.

Figueira, W.F., Biro, P., Booth, D.J. and Valenzuela, V.C.

(2009) Performance of tropical fish recruiting to tem-

perate habitats: role of ambient temperature and impli-

cations of climate change. Marine Ecology Progress

Series 384, 231–239.

Fisher, R. (2005) Swimming speeds of larval coral reef

fishes: impacts on self-recruitment and dispersal.

Marine Ecology Progress Series 285, 223–232.

Fisher, R., Bellwood, D.R. and Job, S.D. (2000) Develop-

ment of swimming abilities in reef fish larvae. Marine

Ecology Progress Series 202, 163–173.

Fisher, R., Leis, J.M., Clark, D.L. and Wilson, S.K. (2005)

Critical swimming speeds of late-stage coral reef fish

larvae: variation within species, among species and

between locations. Marine Biology 147, 1201–1212.

Francis, M.P., Worthington, C.J., Saul, P. and Clements,

K.D. (1999) New and rare tropical and subtropical

fishes from northern New Zealand. New Zealand Journal

of Marine and Freshwater Research 33, 571–586.

Froese, R. and Pauly, D. (2012) FishBase. World Wide

Web electronic publication. www.fishbase.org, version

(08/2012).

Gardiner, N. and Jones, G.P. (2005) Habitat specialisa-

tion and overlap in a guild of coral reef cardinalfish

(family Apogonidae). Marine Ecology Progress Series

305, 163–175.

Gaston, K.J. and Chown, S.L. (1999) Elevation and cli-

matic tolerance: a test using dung beetles. Oikos 86,

584–590.

Gaston, K.J., Blackburn, T.M. and Spicer, J.I. (1998)

Rapoport’s rule: time for an epitaph? Trends in Ecology

and Evolution 13, 70–74.

Greenstein, B.J. and Pandolfi, J.M. (2008) Escaping the

heat: range shifts of reef coral taxa in coastal Western

Australia. Global Change Biology 14, 513–528.

Guisan, A. and Zimmermann, N.E. (2000) Predictive

habitat distribution models in ecology. Ecological Model-

ling 135, 147–186.

Hare, J.A. and Cowen, R.K. (1991) Expatriation of

Xyrichtys novacula (Pisces, Labridae) larvae – evidence of

rapid cross-slope exchange. Journal of Marine Research

49, 801–823.

Hare, J.A. and Cowen, R.K. (1996) Transport mecha-

nisms of larval and pelagic juvenile bluefish (Pomato-

mus saltatrix) from South Atlantic Bight spawning

grounds to Middle Atlantic Bight nursery habitats.

Limnology and Oceanography 41, 1264–1280.

Hare, J.A., Churchill, J.H., Cowen, R.K. et al. (2002)

Routes and rates of larval fish transport from the

southeast to the northeast United States continental

shelf. Limnology and Oceanography 47, 1774–1789.

Harriott, V.J. and Banks, S.A. (2002) Latitudinal varia-

tion in coral communities in eastern Australia: a quali-

tative biophysical model of factors regulating coral

reefs. Coral Reefs 21, 83–94.

Harrison, H.B., Williamson, D.H., Evans, R.D. et al.

(2012) Larval export from marine reserves and the

recruitment benefit for fish and fisheries. Current Biol-

ogy 22, 1023–1028.

Hazel, J.R. and Prosser, C.L. (1974) Molecular mecha-

nisms of temperature compensation in poikilotherms.

Physiological Reviews 54, 620–677.

Helmuth, B., Mieszkowska, N., Moore, P. and Hawkins,

S.J. (2006) Living on the edge of two changing worlds:

forecasting the responses of rocky intertidal ecosystems

to climate change. Annual Review of Ecology Evolution

and Systematics 37, 373–404.

von Herbing, I.H. (2002) Effects of temperature on larval

fish swimming performance: the importance of physics

to physiology. Journal of Fish Biology 61, 865–876.

Hickling, R., Roy, D.B., Hill, J.K., Fox, R. and Thomas,

C.D. (2006) The distributions of a wide range of taxo-

nomic groups are expanding polewards. Global Change

Biology 12, 450–455.

Hirata, T., Oguri, S., Hirata, S., Fukami, H., Nakamura, Y.

and Yamaoka, K. (2011) Seasonal changes in fish assem-

blages in an area of hermatypic corals in Yokonami, Tosa

Bay, Japan. Japanese Journal of Ichthyology 58, 49–64.

Hixon, M.A. (1991) Predation as a process structuring

coral-reef fish communities. In: The Ecology of Fishes on

Coral Reefs. (ed. P.F. Sale). Academic Press, San Diego,

CA, pp. 475–508.

Hixon, M.A. (2011) 60 years of coral reef fish ecology:

past, present, future. Bulletin of Marine Science 87,

727–765.

Hixon, M.A. and Beets, J.P. (1989) Shelter characteristics

and Caribbean fish assemblages – experiments with

artificial reefs. Bulletin of Marine Science 44, 666–680.

Hixon, M.A. and Beets, J.P. (1993) Predation, prey ref-

uges, and the structure of coral reef fish assemblages.

Ecological Monographs 63, 77–101.

Hobbs, J.-P.A., Jones, G.P. and Munday, P.L. (2010) Rar-

ity and extinction risk in coral reef angelfishes on iso-

lated islands: interrelationships among abundance,

geographic range size and specialisation. Coral Reefs

29, 1–11.

Hobbs, J.-P.A., Jones, G.P., Munday, P.L., Connolly, S.R.

and Srinivasan, M. (2012) Biogeography and the

structure of coral reef fish communities on isolated

islands. Journal of Biogeography 39, 130–139.

18 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

Hoegh-Guldberg, O. and Bruno, J.F. (2010) The impact

of climate change on the world’s marine ecosystems.

Science 328, 1523–1528.

Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J. et al.

(2007) Coral reefs under rapid climate change and

ocean acidification. Science 318, 1737–1742.

Hoey, A.S. and McCormick, M.I. (2004) Selective preda-

tion for low body condition at the larval-juvenile tran-

sition of a coral reef fish. Oecologia 139, 23–29.

Hogan, J.D., Fisher, R. and Nolan, C. (2007) Critical

swimming speed of settlement-stage coral reef fishes

from the Caribbean: a methodological and geographical

comparison. Bulletin of Marine Science 80, 219–231.

Holbrook, S.J. and Schmitt, R.J. (2002) Competition for

shelter space causes density-dependent predation mor-

tality in damselfishes. Ecology 83, 2855–2868.

Holbrook, S.J., Brooks, A.J. and Schmitt, R.J. (2002a)

Predictability of fish assemblages on coral patch reefs.

Marine and Freshwater Research 53, 181–188.

Holbrook, S.J., Brooks, A.J. and Schmitt, R.J. (2002b)

Variation in structural attributes of patch-forming cor-

als and in patterns of abundance of associated fishes.

Marine and Freshwater Research 53, 1045–1053.

Holmes, T.H. and McCormick, M.I. (2009) Influence of

prey body characteristics and performance on predator

selection. Oecologia 159, 401–413.

Holmes, T.H. and McCormick, M.I. (2010) Size-selectivity

of predatory reef fish on juvenile prey. Marine Ecology

Progress Series 399, 273–283.

Hurst, T.P. (2007) Causes and consequences of winter

mortality in fishes. Journal of Fish Biology 71, 315–345.

Hurst, T.P. and Conover, D.O. (2001) Activity-related

constraints on overwintering young-of-the-year striped

bass (Morone saxatilis). Canadian Journal of Zoology-

Revue Canadienne De Zoologie 79, 129–136.

Hutchings, J.A., Myers, R.A., Garcia, V.B., Lucifora, L.O.

and Kuparinen, A. (2012) Life-history correlates of

extinction risk and recovery potential. Ecological Appli-

cations 22, 1061–1067.

Hutchins, J.B. (1991) Dispersal of tropical fishes to tem-

perate seas in the southern hemisphere. Journal of the

Royal Society of Western Australia 74, 79–84.

Hutchins, J.B. and Pearce, A.F. (1994) Influence of the

current on recruitment of tropical reef fishes at rott-

nest island, Western Australia. Bulletin of Marine Sci-

ence 54, 245–255.

IPCC (2007) Climate change 2007: the physical science

basis. In: Contribution of Working Group I to the Fourth

Assessment. Report of the Intergovernmental Panel on Cli-

mate Change. (eds S. Solomon, D. Qin, M. Manning, Z.

Chen, M. Marquis, K. Averyt, M.M.B. Tignor, H.L.M. Jr

and Z. Chen). Cambridge University Press, Cambridge,

UK, pp. 996.

Jones, G.P., Milicich, M.J., Emslie, M.J. and Lunow, C.

(1999) Self-recruitment in a coral reef fish population.

Nature 402, 802–804.

Jones, G.P., Caley, M.J. and Munday, P.L. (2002) Rarity

in coral reef fish communities. In: Coral Reef Fishes.

Dynamics and Diversity in a Complex Ecosystem (ed. P.F.

Sale), Academic Press, San Diego, pp. 81–102.

Jones, G.P., Planes, S. and Thorrold, S.R. (2005) Coral

reef fish larvae settle close to home. Current Biology

15, 1314–1318.

Jones, G.P., Almany, G.R., Russ, G.R. et al. (2009a) Lar-

val retention and connectivity among populations of

corals and reef fishes: history, advances and chal-

lenges. Coral Reefs 28, 307–325.

Jones, G.P., Russ, G.R., Sale, P.F. and Steneck, R.S. (2009b)

Theme section on “Larval connectivity, resilience and

the future of coral reefs”. Coral Reefs 28, 303–305.

Keane, J.P. and Neira, F.J. (2008) Larval fish assemblages

along the south-eastern Australian shelf: linking meso-

scale non-depth-discriminate structure and water

masses. Fisheries Oceanography 17, 263–280.

Kerrigan, B.A. (1996) Temporal patterns in size and condi-

tion at settlement in two tropical reef fishes (Pomacen-

tridae: Pomacentrus amboinensis and P. nagasakiensis).

Marine Ecology Progress Series 135, 27–41.

Kingsford, M. and Battershill, C. (1998) Studying Temper-

ate Marine Environments. A Handbook for Ecologists.,

Canterbury University Press, Christchurch.

Kingsford, M.J. and Carlson, I.J. (2010) Patterns of distri-

bution and movement of fishes, Ophthalmolepis lineola-

tus and Hypoplectrodes maccullochi, on temperate rocky

reefs of south eastern Australia. Environmental Biology

of Fishes 88, 105–118.

Kitchell, J.F., Stewart, D.J. and Weininger, D. (1977)

Applications of a bioenergetics model to yellow perch

(Perca flavescens) and walleye (Stizostedion vitreum vitre-

um). Journal of the Fisheries Research Board of Canada

34, 1922–1935.

Kokita, T. (2004) Latitudinal compensation in female

reproductive rate of a geographically widespread reef

fish. Environmental Biology of Fishes 71, 213–224.

Last, P.R., White, W.T., Gledhill, D.C. et al. (2011) Long-

term shifts in abundance and distribution of a temper-

ate fish fauna: a response to climate change and

fishing practices. Global Ecology and Biogeography 20,

58–72.

Lawton, J.H. (1999) Are there general laws in ecology?

Oikos 84, 177–192.

Lee, T.N., Rooth, C., Williams, E., McGowan, M., Szmant,

A.F. and Clarke, M.E. (1992) Influence of Florida Cur-

rent, gyres and wind-driven circulation on transport of

larvae and recruitment in the Florida Keys coral reefs.

Continental Shelf Research 12, 971–1002.

Lee, T.N., Clarke, M.E., Williams, E., Szmant, A.F. and

Berger, T. (1994) Evolution of the Tortugas Gyre and

its influence on recruitment in the Florida Keys. Bulle-

tin of Marine Science 54, 621–646.

Lee, T.N., Leaman, K., Williams, E., Berger, T. and Atkin-

son, L. (1995) Florida current meanders and gyre

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 19

Tropical vagrant fishes D A Feary et al.,

formation in the southern straits of Florida. Journal of

Geophysical Research-Oceans 100, 8607–8620.

Leis, J.M. (1993) Larval fish assemblages near indo-paci-

fic coral-reefs. Bulletin of Marine Science 53, 362–392.

Leis, J.M., Sweatman, H.P.A., Reader, S.E. (1996) What

the pelagic stages of coral reef fishes are doing out in

blue water: Daytime field observations of larval beha-

vioural capabilities. Marine and Freshwater Research 47,

401–411.

Leis, J.M. and Carson-Ewart, B.M. (1997) In situ swim-

ming speeds of the late pelagic larvae of some Indo-

Pacific coral-reef fishes. Marine Ecology Progress Series

159, 165–174.

Leis, J.M. and Carson-Ewart, B.M. (1998) Complex

behaviour by coral-reef fish larvae in open-water and

near-reef pelagic environments. Environmental Biology

of Fishes 53, 259–266.

Leis, J.M. and Carson-Ewart, B.M. (2003) Orientation of

pelagic larvae of coral-reef fishes in the ocean. Marine

Ecology Progress Series 252, 239–253.

Leis, J.M. and Goldman, B. (1984) A preliminary distri-

butional study of fish larvae near a ribbon coral-reef in

the great barrier-reef. Coral Reefs 2, 197–203.

Leis, J.M. and McCormick, M.I. (2002) The biology,

behavior, and ecology of the pelagic, larval stage of

coral reef fishes. In: Coral Reef Fishes: Dynamic and

Diversity in a Complex Ecosystem (eds P.F. Sale). Else-

vier, San Diego, CA, USA, pp. 171–199.

Leis, J.M., Carson-Ewart, B.M. and Cato, D.H. (2002)

Sound detection in situ by the larvae of a coral-reef

damselfish (Pomacentridae). Marine Ecology Progress

Series 232, 259–268.

Leis, J.M., Carson-Ewart, B.M., Hay, A.C. and Cato, D.H.

(2003) Coral-reef sounds enable nocturnal navigation

by some reef-fish larvae in some places and at some

times. Journal of Fish Biology 63, 724–737.

Leis, J.M., Hay, A.C., Lockett, M.M., Chen, J.-P. and Fang,

L.-S. (2007) Ontogeny of swimming speed in larvae of

pelagic-spawning, tropical, marine fishes. Marine Ecol-

ogy Progress Series 349, 255–267.

Leis, J.M., Siebeck, U. and Dixson, D.L. (2011) How

Nemo finds home: the neuroecology of dispersal and

of population connectivity in larvae of marine fishes.

Integrative and Comparative Biology 51, 826–843.

Leis, J.M., Sweatman, H.P.A. and Reader, S.E. (1996)

What the pelagic stages of coral reef fishes are doing

out in blue water: Daytime field observations of larval

behavioural capabilities. Marine and Freshwater

Research 47, 401–411.

Lessios, H.A. and Robertson, D.R. (2006) Crossing the

impassable: genetic connections in 20 reef fishes across

the eastern Pacific barrier. Proceedings of the Royal Soci-

ety B-Biological Sciences 273, 2201–2208.

Lien, Y.T., Fukami, H. and Yamashita, Y. (2012) Symbi-

odinium Clade C dominates zooxanthellate corals

(Scleractinia) in the temperate region of Japan. Zoologi-

cal Science 29, 173–180.

Limouzy-Paris, C.B., Graber, H.C., Jones, D.L., Ropke, A.W.

and Richards, W.J. (1997) Translocation of larval coral

reef fishes via sub-mesoscale spin-off eddies from the

Florida current. Bulletin of Marine Science 60, 966–983.

Loennstedt, O.M., McCormick, M.I., Meekan, M.G., Fer-

rari, M.C.O. and Chivers, D.P. (2012) Learn and live:

predator experience and feeding history determines

prey behaviour and survival. Proceedings of the Royal

Society B-Biological Sciences 279, 2091–2098.

Lonnstedt, O.M., McCormick, M.I. and Chivers, D.P.

(2012) Well-informed foraging: damage-released chem-

ical cues of injured prey signal quality and size to pre-

dators. Oecologia 168, 651–658.

Lo-Yat, A., Meekan, M.G., Carleton, J.H. and Galzin, R.

(2006) Large-scale dispersal of the larvae of nearshore

and pelagic fishes in the tropical oceanic waters of French

Polynesia.Marine Ecology Progress Series 325, 195–203.

Lu, J., Deser, C. and Reichler, T. (2009) Cause of the

widening of the tropical belt since 1958. Geophysical

Research Letters 36, L03803.

Madin, E.M.P., Ban, N.C., Doubleday, Z.A., Holmes, T.H.,

Pecl, G.T. and Smith, F. (2012) Socio-economic and

management implications of range-shifting species in

marine systems. Global Environmental Change-Human

and Policy Dimensions 22, 137–146.

Malcolm, H.A., Davies, P.L., Jordan, A. and Smith, S.D.A.

(2011) Variation in sea temperature and the East Aus-

tralian Current in the Solitary Islands region between

2001–2008. Deep-Sea Research Part Ii-Topical Studies in

Oceanography 58, 616–627.

Malcolm, H.A., Gladstone, W., Lindfield, S., Wraith, J.

and Lynch, T.P. (2007) Spatial and temporal variation

in reef fish assemblages of marine parks in New South

Wales, Australia - baited video observations. Marine

Ecology Progress Series 350, 277–290.

Malcolm, H.A., Smith, S.D.A., and Jordan, A. (2010)

Using patterns of reef fish assemblages to refine a Habi-

tat Classification System for marine parks in NSW,

Australia. Aquatic Conservation-Marine and Freshwater

Ecosystems 20, 83–92.

Manassa, R.P. and McCormick, M.I. (2012) Social learn-

ing and acquired recognition of a predator by a marine

fish. Animal Cognition 15, 559–565.

McBride, R. (1996) On the rarity of banded butterfly-

fish in the Mid-Atlantic. Underwater Naturalist 23,

18–20.

McBride, R.S. and Able, K.W. (1998) Ecology and fate of

butterflyfishes, Chaetodon spp., in the temperate, wes-

tern North Atlantic. Bulletin of Marine Science 63,

401–416.

McCormick, M.I. (1998) Condition and growth of reef

fish at settlement: is it important? Australian Journal of

Ecology 23, 258–264.

20 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

McCormick, M.I. and Hoey, A.S. (2004) Larval growth

history determines juvenile growth and survival in a

tropical marine fish. Oikos 106, 225–242.

McCormick, M.I. and Holmes, T.H. (2006) Prey experi-

ence of predation influences mortality rates at settle-

ment in a coral reef fish, Pomacentrus amboinensis.

Journal of Fish Biology 68, 969–974.

Mora, C. and Osp�ına, A.F. (2001) Tolerance to high tem-

peratures and potential impact of sea warming on reef

fishes of Gorgona Island (tropical Eastern Pacific). Mar-

ine Biology 139, 765–769.

Munday, P.L. and Jones, G.P. (1998) The ecological impli-

cations of small body size among coral reef fishes. Ocean-

ography and Marine Biology Annual Review 36, 373–411.

Munday, P.L., Jones, G.P. and Caley, M.J. (1997) Habitat

specialisation and the distribution and abundance of

coral-dwelling gobies. Marine Ecology Progress Series

152, 227–239.

Munday, P.L., Jones, G.P. and Caley, M.J. (2001) Inter-

specific competition and coexistence in a guild of coral-

dwelling fishes. Ecology 82, 2177–2189.

Munday, P.L., Jones, G.P., Pratchett, M.S. and Williams,

A.J. (2008a) Climate change and the future for coral

reef fishes. Fish and Fisheries 9, 261–285.

Munday, P.L., Kingsford, M.J., O’Callaghan, M. and

Donelson, J.M. (2008b) Elevated temperature restricts

growth potential of the coral reef fish Acanthochromis

polyacanthus. Coral Reefs 27, 927–931.

Munday, P.L., Leis, J.M., Lough, J.M. et al. (2009) Cli-

mate change and coral reef connectivity. Coral Reefs

28, 379–395.

Nakazono, A. (2002) Fate of tropical reef fish juveniles

that settle to a temperate habitat. Fisheries Science 68,

127–130.

Nicholson, J.K., Holmes, E., Kinross, J. et al. (2012) Host-

gut microbiota metabolic interactions. Science 336,

1262–1267.

Nye, J.A., Link, J.S., Hare, J.A. and Overholtz, W.J.

(2009) Changing spatial distribution of fish stocks in

relation to climate and population size on the North-

east United States continental shelf. Marine Ecology

Progress Series 393, 111–129.

O’Connor, M.I., Bruno, J.F., Gaines, S.D., Halpern, B.S.

and Lester, S.E. (2007) Temperature control of larval

dispersal and the implications for marine ecology, evo-

lution, and conservation. Proceedings of the National

Academy of Sciences USA 104, 1266–1271.

Oviatt, C.A. (2004) The changing ecology of temperate

coastal waters during a warming trend. Estuaries 27,

895–904.

Paris, C.B. and Cowen, R.K. (2004) Direct evidence of a

biophysical retention mechanism for coral reef fish lar-

vae. Limnology and Oceanography 49, 1964–1979.

Parmesan, C. (2006) Ecological and evolutionary

responses to recent climate change. Annual Review of

Ecology Evolution and Systematics 37, 637–669.

Parmesan, C. and Yohe, G. (2003) A globally coherent

fingerprint of climate change impacts across natural

systems. Nature 421, 37–42.

Parmesan, C., Ryrholm, N., Stefanescu, C. et al. (1999)

Poleward shifts in geographical ranges of butterfly spe-

cies associated with regional warming. Nature 399,

579–583.

Parmesan, C., Gaines, S., Gonzalez, L. et al. (2005)

Empirical perspectives on species borders: from tradi-

tional biogeography to global change. Oikos 108, 58–

75.

Pauly, D. (1997) Geometrical constraints on body size.

Trends in Ecology and Evolution 12, 442–443.

Planes, S. and Lecaillon, G. (2001) Caging experiment to

examine mortality, during metamorphosis of coral reef

fish larvae. Coral Reefs 20, 211–218.

Planes, S., Jones, G.P. and Thorrold, S.R. (2009) Larval

dispersal connects fish populations in a network of

marine protected areas. Proceedings of the National

Academy of Sciences of the United States of America 106,

5693–5697.

Poertner, H.O. and Farrell, A.P. (2008) Physiology and

climate change. Science 322, 690–692.

Pratchett, M.S. (2005) Dietary overlap among coral-feed-

ing butterflyfishes (Chaetodontidae) at Lizard Island,

northern Great Barrier Reef. Marine Biology 148, 373–

382.

Pratchett, M.S., Hoey, A.J., Feary, D.A., Bauman, A.,

Burt, J. and Riegl, B. (2012) Functional composition of

Chaetodon butterflyfishes at a peripheral and extreme

coral reef location, the southern Persian Gulf. Marine

Pollution Bulletin. DOI:10.1016/j.marpolbul.2012.10.

014 [Epub ahead of print].

Pratchett, M.S., Wilson, S.K., Berumen, M.L. and McCor-

mick, M.I. (2004) Sublethal effects of coral bleaching

on an obligate coral feeding butterflyfish. Coral Reefs

23, 352–356.

Pratchett, M.S., Berumen, M.L., Marnane, M.J., Eagle,

J.V. and Pratchett, D.J. (2008a) Habitat associations of

juvenile versus adult butterflyfishes. Coral Reefs 27,

541–551.

Pratchett, M.S., Munday, P.L., Wilson, S.K. et al. (2008b)

Effects of climate-induced coral bleaching on coral-reef

fishes: ecological and economic consequences. Oceanog-

raphy and Marine Biology Annual Review 46, 251–296.

Pratt, T.C. and Fox, M.G. (2002) Influence of predation

risk on the overwinter mortality and energetic rela-

tionships of young-of-year walleyes. Transactions of the

American Fisheries Society 131, 885–898.

Precht, W.F. and Aronson, R.B. (2004) Climate flickers

and range shifts of reef corals. Frontiers in Ecology and

the Environment 2, 307–314.

Ridgway, K.R. and Dunn, J.R. (2003) Mesoscale struc-

ture of the mean East Australian Current System and

its relationship with topography. Progress in Oceanogra-

phy 56, 189–222.

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 21

Tropical vagrant fishes D A Feary et al.,

Riegl, B.M., Purkis, S.J., Al-Cibahy, A.S., Abdel-Moati,

M.A. and Hoegh-Guldberg, O. (2011) Present limits to

heat-adaptability in corals and population-level

responses to climate extremes. PLoS ONE 6, e24802.

Rodolfo-Metalpa, R., Reynaud, S., Allemand, D. and Fer-

rier-Pages, C. (2008) Temporal and depth responses of

two temperate corals, Cladocora caespitosa and Oculina

patagonica, from the North Mediterranean Sea. Marine

Ecology Progress Series 369, 103–114.

Roughan, M., Macdonald, H.S., Baird, M.E. and Glasby,

T.M. (2011) Modelling coastal connectivity in a Wes-

tern Boundary Current: seasonal and inter-annual var-

iability. Deep-Sea Research Part Ii-Topical Studies in

Oceanography 58, 628–644.

Roughgarden, J. (2009) Is there a general theory of

community ecology? Biology and Philosophy 24, 521–

529.

Russell, B.C. (1971) A preliminary annotated checklist of

fishes of the Poor Knights Islands. Tane 17, 81–90.

Sale, P.F. (ed.) (1991) The Ecology of Fishes on Coral

Reefs. Academic Press, New York, 754 pp.

Sale, P.F. (ed.) (2002) Coral Reef Fishes. Dynamics and

Diversity in a Complex Ecosystem. Academic Press, San

Diego, 549 pp.

Scott, A. and Harrison, P.L. (2008) Larval settlement

and juvenile development of sea anemones that pro-

vide habitat for anemonefish. Marine Biology 154,

833–839.

Seidel, D.J., Fu, Q., Randel, W.J. and Reichler, T.J. (2008)

Widening of the tropical belt in a changing climate.

Nature Geoscience 1, 21–24.

Shanks, A.L. (2009) Pelagic larval duration and dispersal

distance revisited. Biological Bulletin 216, 373–385.

Soberon, J. (2007) Grinnellian and Eltonian niches and

geographic distributions of species. Ecology Letters 10,

1115–1123.

Soeparno, Nakamura, Y., Shibuno, T. and Yamaoka, K.

(2012) Relationship between pelagic larval duration

and abundance of tropical fishes on temperate coasts

of Japan. Journal of Fish Biology 80, 346–357.

Sorte, C.J.B., Williams, S.L. and Carlton, J.T. (2010) Mar-

ine range shifts and species introductions: comparative

spread rates and community impacts. Global Ecology

and Biogeography 19, 303–316.

Sponaugle, S. and Grorud-Covert, K. (2006) Environmen-

tal variability, early life-history traits, and survival of

new coral reef fish recruits. Integrative and Comparative

Biology 46, 623–633.

Sponaugle, S., Cowen, R.K., Shanks, A. et al. (2002) Pre-

dicting self-recruitment in marine populations: bio-

physical correlates and mechanisms. Bulletin of Marine

Science 70, 341–375.

Sponaugle, S., Boulay, J.N. and Rankin, T.L. (2011)

Growth- and size-selective mortality in pelagic larvae

of a common reef fish. Aquatic Biology 13, 263–273.

Stefansdottir, L., Solmundsson, J., Marteinsdottir, G.,

Kristinsson, K. and Jonasson, J.P. (2010) Groundfish

species diversity and assemblage structure in Icelandic

waters during recent years of warming. Fisheries

Oceanography 19, 42–62.

Stevens, G.C. (1989) The latitudinal gradients in geo-

graphical range: how so many species co-exist in the

tropics. American Naturalist 133, 240–256.

Stillman, J. and Somero, G.N. (2000) A comparative

analysis of the upper thermal tolerance limits of east-

ern Pacific porcelain crabs, genus Petrolisthes: Influ-

ences of latitude, vertical zonation, acclimation, and

phylogeny. Physiological and Biochemical Zoology 73,

200–208.

Stobutzki, I.C. and Bellwood, D.R. (1994) An analysis of

the critical swimming abilities of pre- and post-settle-

ment coral reef fishes. Journal of Experimental Marine

Biology and Ecology 175, 275–286.

Stobutzki, I.C. and Bellwood, D.R. (1997) Sustained

swimming abilities of the late pelagic stages of coral

reef fishes. Marine Ecology Progress Series 149, 35–41.

Sunday, J.M., Bates, A.E. and Dulvy, N.K. (2012) Ther-

mal tolerance and the global redistribution of animals.

Nature Climate Change 2, 686–690. doi:10.1038/NCLI-

MATE1539.

Suthers, I.M. (1998) Bigger? Fatter? Or is faster growth

better? Considerations on condition in larval and juve-

nile coral-reef fish. Australian Journal of Ecology 23,

265–273.

Swearer, S.E., Caselle, J.E., Lea, D.W. and Warner, R.R.

(1999) Larval retention and recruitment in an island

population of a coral-reef fish. Nature 402, 799–802.

Swearer, S.E., Shima, J.S., Hellberg, M.E. et al. (2002)

Evidence of self-recruitment in demersal marine popu-

lations. Bulletin of Marine Science 70, 251–271.

Sweatman, H. (1988) Field evidence that settling coral-

reef fish larvae detect resident fishes using dissolved

chemical cues. Journal of Experimental Marine Biology

and Ecology 124, 163–174.

Syahailatua, A., Roughan, M. and Suthers, I.M. (2011)

Characteristic ichthyoplankton taxa in the separation

zone of the East Australian Current: larval assemblages

as tracers of coastal mixing. Deep-Sea Research Part

Ii-Topical Studies in Oceanography 58, 678–690.

Thomas, C.D. and Lennon, J.J. (1999) Birds extend their

ranges northwards. Nature 399, 213.

Thorrold, S.R., Latkoczy, C., Swart, P.K. and Jones, C.M.

(2001) Natal homing in a marine fish metapopulation.

Science 291, 297–299.

Thresher, R. (1984) Reproduction in Reef Fishes. TFH Pub-

lications, Neptune City.

Thresher, R.E. and Brothers, E.B. (1989) Evidence of

intra- and inter-oceanic regional differences in the

early life history of reef-associated fishes. Marine Ecol-

ogy Progress Series 57, 187–205.

22 © 2013 John Wiley & Sons Ltd, F ISH and F ISHER IES

Tropical vagrant fishes D A Feary et al,

Underwood, A.J., Kingsford, M.J. and Andrew, N.L.

(1991) Patterns in shallow subtidal marine assem-

blages along the coast of New South Wales. Australian

Journal of Ecology 6, 231–249.

Victor, B.C. (1986) Larval settlement and juvenile mor-

tality in a recruitment-limited coral-reef fish popula-

tion. Ecological Monographs 56, 145–160.

Weatherly, A.H. (1972) Growth and Ecology of Fish

Population. Academic Press, London.

Wellington, G.M. and Robertson, D.R. (2001) Variation in

larval life-history traits among reef fishes across the

Isthmus of Panama. Marine Biology 138, 11–22.

Wellington, G.M. and Victor, B.C. (1989) Planktonic lar-

val duration of one hundred species of Pacific and

Atlantic damselfishes (Pomacentridae). Marine Biology

101, 557–567.

Wilson, S.K., Graham, N.A.J., Pratchett, M.S., Jones, G.P.

and Polunin, N.V.C. (2006) Multiple disturbances and

the global degradation of coral reefs: are reef fishes at

risk or resilient? Global Change Biology 12, 2220–2234.

Wing, S.R., Botsford, L.W., Ralston, S.V. and Largier, J.L.

(1998) Meroplanktonic distribution and circulation in

a coastal retention zone of the northern California

upwelling system. Limnology and Oceanography 43,

1710–1721.

Wu, L.X., Cai, W.J., Zhang, L.P. et al. (2012) Enhanced

warming over the global subtropical western boundary

currents. Nature Climate Change 2, 161–166.

Yamano, H., Sugihara, K. and Nomura, K. (2011) Rapid

poleward range expansion of tropical reef corals in

response to rising sea surface temperatures. Geophysical

Research Letters 38, L04601.

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.

© 2013 John Wiley & Sons Ltd, F I SH and F I SHER IES 23

Tropical vagrant fishes D A Feary et al.,