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Reviews in Fish Biology and Fisheries

, Volume 26, Issue 2, pp 181–198 | Cite as

The importance of ecological and behavioural data in studies of hybridisation among marine fishes

  • Stefano R. Montanari
  • Jean-Paul A. Hobbs
  • Morgan S. Pratchett
  • Lynne van Herwerden
Reviews

Abstract

Natural hybridisation is a widespread phenomenon, particularly well documented in terrestrial and freshwater ecosystems, where it has been ascribed substantial evolutionary and adaptive relevance. Hybridisation has received comparatively less attention in marine systems, though there has been a recent surge of reported marine hybrids, particularly among corals and fishes. This review summarises the current knowledge of hybridisation in marine fishes, with a focus on ecological and behavioural factors that may play a role in hybridisation processes. Rarity of one or both parental species within the hybrid zone, overlap in habitat use, dietary overlap and the breakdown in assortative mating appear to have a role in facilitating hybridisation. Despite this, most of the recent literature on marine fish hybridisation has a strong genetic focus, with little or no quantitative information about the ecological and behavioural factors that initiate or facilitate hybridisation. Future studies should attempt to gather ecological and behavioural data from hybrid zones, thus teasing out which processes are most relevant to overcoming pre-zygotic barriers to reproductive isolation. Not only will this advance our understanding of the adaptive and evolutionary relevance of hybridisation in marine fishes, but it will also provide unique insights into the maintenance of reproductive isolation and the process of speciation in the marine environment.

Keywords

Diet Ecology Habitat Hybridisation Marine Rarity 

Introduction

Natural hybridisation is the interbreeding of individuals from two genetically distinct species or populations resulting in viable offspring (Arnold 1997). Natural hybridisation has historically been considered infrequent and of limited ecological or evolutionary relevance, mainly because it challenges the biological species paradigm (Mallet 2005). Interestingly, the presumed rarity of natural hybridisation caused it to be marginalised as unimportant (Mayr 1963). In contrast, rare fitness-increasing mutations have been recognised as milestones for adaptive evolution (Arnold 2006). There is increasing recognition that natural hybridisation can have substantial evolutionary and adaptive significance, increasing or decreasing adaptive capacity and species diversity (Arnold 2006; Abbott et al. 2013). To date, more than 25 % of plants and 10 % of animals have been reported to hybridise, but the true proportion of hybridising species is likely to be higher due to difficulties in detecting hybrids (Mallet 2005).

In just a few decades natural hybridisation can lead to evolutionary novelty (Budd and Pandolfi 2010) and increase the adaptability of a population to changing environments (Grant and Grant 2002; Anderson et al. 2009). Furthermore, hybrids have the potential to occupy unexploited ecological niches (Seehausen 2004), and through subsequent reproductive isolation become new species (Smith et al. 2003; Verheyen et al. 2003; Seehausen 2004). Hybridisation can also contribute significantly to the loss of biodiversity through extinction (Rhymer and Simberloff 1996) or reverse speciation (Seehausen 2006; Taylor et al. 2006). Whatever the ultimate outcome, it is clear that hybridisation can play an important role in adaptation and evolution of species.

Most of the research and understanding of natural hybridisation comes from terrestrial and freshwater ecosystems, where there is reportedly a high incidence of hybridisation (Arnold et al. 1993; Cruzan and Arnold 1993; Carney et al. 1994; Nürnberger et al. 1995; MacCallum et al. 1998). Traditionally, hybridisation was considered much less common in the marine environment (Hubbs 1955), but was also less well studied. Since 1995, hybridisation has been documented across a broad range of marine plant and animal taxa (Gardner 1997; van Oppen and Gates 2006; Willis et al. 2006; Yaakub et al. 2006; Hobbs et al. 2009; Richards and Hobbs 2015). As for freshwater and terrestrial environments, there appears to be strong taxonomic bias in hybridisation in marine species. Hybridisation is particularly common in marine fishes (Gardner 1997; Yaakub et al. 2006), as it is for freshwater fishes (Scribner et al. 2000).

The genetic consequences and evolutionary implications of hybridisation in terrestrial and freshwater environments have been widely studied and reviewed (Abbott et al. 2013). Numerous molecular studies have also demonstrated the range of genetic outcomes of hybridisation in marine species—reviewed by Richards and Hobbs (2015). However, less attention has been given to the proximal factors responsible for the breakdown in reproductive isolation that leads to hybridisation. Despite a lack of experimental evidence, a number of ecological and behavioural factors have been suggested to increase the incidence of hybridisation in marine fishes. These include: geographic co-occurrence of recently diverged sister taxa that come into secondary contact (McMillan and Palumbi 1995; Mallet 2005); external fertilisation (Hubbs 1955); the breakdown of assortative mating (McMillan et al. 1999); overlapping spatial or dietary ecologies that increase heterospecific encounters (van Herwerden et al. 2006; Yaakub et al. 2006; Marie et al. 2007; Yaakub et al. 2007; Montanari et al. 2012, 2014; Gainsford et al. 2015). Local rarity of one or both parental species (Gosline 1948; Randall et al. 1977; Frisch and van Herwerden 2006; van Herwerden et al. 2006; Marie et al. 2007; Hobbs and Allen 2014; Montanari et al. 2014) can further favour interbreeding because of the lack of conspecific partners.

Recent reviews have addressed the topic of hybridisation in marine fishes, either to summarise the current knowledge of its consequences and our ability to differentiate it from alternative hypotheses (Richards and Hobbs 2015), or to examine in detail its occurrence in a specific taxon (Hobbs et al. 2013). Here we would like to bring the attention to an aspect of hybridisation that has been, in our opinion, overlooked: that is, the ecological and behavioural mechanisms that initiate hybridisation. To this effect, we: (1) revise estimates of the incidence of hybridisation in marine fishes; (2) provide a summary of the most commonly reported ecological and behavioural factors that facilitate hybridisation among marine fishes; (3) identify areas of study where ecological and behavioural data are needed in marine hybridisation studies; and, therefore, (4) suggest an approach for gathering such data, which are necessary to complement the wealth of genetic information currently available. Further, we argue that complementing genetic studies with ecology and behaviour can, not only shed light on the processes that initiate the formation of mixed social groups (thereby setting the scene for hybridisation), but also help characterise the role of hybrid fish taxa within hybrid zones.

We focus our comparison on fishes because hybridisation in this group is common and relatively well studied (Hubbs 1955; Allendorf and Waples 1996; Gardner 1997; Yaakub et al. 2006). Where possible, we include first reports of each hybrid exclusively, and separately cite further work if necessary. This review does not examine physiological and genetic factors implicated in hybridisation: although these have a recognized role in hybridisation, they come into play after the ecological and behavioural factors have initiated the hybridisation process (Fig. 1). Ecological and behavioural factors can also determine the genetic outcome of hybridisation events (Gainsford et al. 2015), however this review will focus on how these factors initiate hybridisation. We have excluded anadromous fishes, some genera of which hybridise extensively—e.g. Oncorhynchus, (Ostberg et al. 2004), because these hybridisation events occur in freshwater streams. Finally, this review focuses only on natural instances of hybridisation, even though anthropogenic influences can cause fish species to hybridise (Scribner et al. 2000; Taylor et al. 2006).
Fig. 1

Provisional framework for examining the initiation of deliberate hybridisation in marine fishes. Biogeographical distribution and ecology/behaviour lay the foundations for hybridisation to occur, before genetic compatibility determines the outcome of hybridisation. Although overlapping geographic distributions is all that is required to initiate hybridisation, ecological (e.g. niche overlap) and behavioural factors increase the likelihood of hybridisation occurring. Highlighted in bold are the aspects of marine fish hybridisation for which data are largely lacking

Hybrid fishes have historically been identified in the field through the observation of aberrant colour patterns, often deemed intermediate between those of the putative parent species (Randall 1956). This approach is still used today, and numerical predictions of hybrid colour patterns (Miyazawa et al. 2010), as well as genetic confirmation of the hybrid status of the intermediate individuals (DiBattista et al. 2012; Bernardi et al. 2013; Coleman et al. 2014; Montanari et al. 2014; Gainsford et al. 2015) have confirmed its validity. Given the universal genetic confirmation of suspected hybrids across a wide range of fishes, we include in this review hybrids that have been reported based on morphology and colouration, but are yet to be genetically confirmed. As is the case in terrestrial and freshwater systems (Mallet 2005), hybrid identification based on phenotypes is likely to significantly underestimate the true incidence of hybridisation. Many more hybrid marine fishes are likely to be detected through genetic analyses, as evidenced by the unintentional discoveries of hybrids in phylogenetic studies (Kuriiwa et al. 2007).

Hybridisation in fishes

Historical notes

Naturally occurring hybrid marine fishes have been reported in the scientific literature since the end of the nineteenth century. Holt (1883), for example, reported probable hybrids between two common flatfishes, turbot (Scophthalmus maximus) and brill (S. rhombus). Since then, at least 111 hybrids, involving 173 marine fish species, have been reported (Table 1). In contrast with the broad temporal distribution of reported occurrences of hybrid freshwater fishes (Scribner et al. 2000), the majority (74 %) of marine fish hybrids have been reported since 1990. The reported number of naturally hybridising marine fish species has more than doubled since the seminal review by Gardner (1997). This suggests that incidence of hybridisation among marine fishes was previously underappreciated due to limited research on this topic, but the recent plethora of reported marine fish hybrids provides a timely opportunity to compare processes of hybridisation between marine and freshwater fishes.
Table 1

Naturally hybridising marine fish species ordered by family

Family

Species 1

Species 2

Location

Climate

Factor

Ecology/behaviour

Source

Acanthuridae

Acanthurus leucosternon

Acanthurus nigricans

Christmas Is.

Tr

R, H

Q

Marie et al. (2007)

Acanthuridae

Acanthurus japonicus

Acanthurus nigricans

Taiwan

Tr

 

N/A

Randall and Frische (2000)

Acanthuridae

Acanthurus achilles

Acanthurus nigricans

Phoenix Is.

Tr

H, D

Q

Randall (1956)

Acanthuridae

Naso elegans

Naso lituratus

Christmas Is.

Tr

R

Q

Hobbs et al. (2009)

Acanthuridae

Acanthurus lineatus

Acanthurus sohal

Socotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Anguillidae

Anguilla anguilla

Anguilla rostrata

Iceland

Te

R

C

Albert et al. (2006)

Atherinopsidae

Menidia menidia

Menidia beryllina

Florida

Te

R, H

C

Gosline (1948)

Balistidae

Melichthys indicus

Melichthys vidua

Christmas Is.

Tr

R

Q

Hobbs et al. (2009)

Chaetodontidae

Chaetodon argentatus

Chaetodon mertensii

N/A

Tr

 

N/A

Allen et al. (1998)

Chaetodontidae

Chaetodon argentatus

Chaetodon xanthurus

N/A

Tr

 

N/A

Kuiter (2002)

Chaetodontidae

Chaetodon auriga

Chaetodon ephippium

Tuamotu

Tr

R

C

Randall et al. (1977)

Chaetodontidae

Chaetodon auriga

Chaetodon fasciatus

Red Sea

Tr

 

N/A 

Gardner (1997)

Chaetodontidae

Chaetodon austriacus

Chaetodon melapterus

N/A

Tr

 

N/A

Allen et al. (1998)

Chaetodontidae

Chaetodon burgessi

Chaetodon tinkeri

N/A

Tr

 

N/A

Allen et al. (1998)

Chaetodontidae

Chaetodon burgessi

Chaetodon flavocoronatus

N/A

Tr

 

N/A

Allen et al. (1998)

Chaetodontidae

Chaetodon daedalma

Chaetodon nippon

N/A

Tr

 

N/A 

Allen et al. (1998)

Chaetodontidae

Chaetodon ephippium

Chaetodon semeion

Marshall Is.

Tr

R

C

Randall et al. (1977)

Chaetodontidae

Chaetodon ephippium

Chaetodon xanthocephalus

N/A

Tr

R

N/A

Kuiter (2002)

Chaetodontidae

Chaetodon guentheri

Chaetodon daedalma

N/A

Tr

 

N/A

Allen et al. (1998)

Chaetodontidae

Chaetodon guentheri

Chaetodon oxycephalus

N/A

Tr

 

N/A

Kuiter (2002)

Chaetodontidae

Chaetodon kleinii

Chaetodon unimaculatus

Marshall Is.

Tr

R

C

Randall et al. (1977)

Chaetodontidae

Chaetodon miliaris

Chaetodon tinkeri

Hawaii

Tr

R

C

Randall et al. (1977)

Chaetodontidae

Chaetodon ornatissimus

Chaetodon reticulatus

N/A

Tr

 

N/A

Allen et al. (1998)

Chaetodontidae

Chaetodon rafflesii

Chaetodon vagabundus

N/A

Tr

 

N/A

Kuiter (2002)

Chaetodontidae

Chaetodon aureofasciatus

Chaetodon rainfordi

GBR

Tr

R

C

Randall et al. (1977)

Chaetodontidae

Chaetodon guttatissimus

Chaetodon punctatofasciatus

Christmas Is.

Tr

H, D, R

Q

Hobbs et al. (2009), Montanari et al. (2014)

Chaetodontidae

Chaetodon punctatofasciatus

Chaetodon pelewensis

GBR

Tr

 

N/A

Randall et al. (1977)

Chaetodontidae

Chaetodon trifasciatus

Chaetodon lunulatus

Christmas Is.

Tr

H, D, R

N/A

Hobbs et al. (2009), Montanari et al. (2012)

Chaetodontidae

Chaetodon ornatissimus

Chaetodon meyeri

Palau; Christmas Is.

Tr

 

N/A

Randall et al. (1977)

Chaetodontidae

Chaetodon auriga

Chaetodon lunula

Red Sea

Tr

 

N/A

Randall et al. (1977)

Chaetodontidae

Chaetodon miliaris

Chaetodon multicinctus

Hawaii

Tr

 

N/A

Randall et al. (1977)

Chaetodontidae

Chaetodon ocellatus

Chaetodon striatus

Puerto Rico

Tr

O

C

Clavijo (1985)

Chaetodontidae

Chaetodon collare

Chaetodon lunula

Socotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Chaetodontidae

Chaetodon gardineri

Chaetodon leucopleura

Socotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Chaetodontidae

Chaetodon melapterus

Chaetodon trifasciatus

Socotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Cirrhitidae

Cirrhitichthys calliurus

Cirrhitichthys oxycephalus

Socotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Clupeidae

Brevoortia patronus

Brevoortia smithi

Florida

ST

R, H

Q

Hettler (1968)

Clupeidae

Brevoortia smithi

Brevoortia tyrannus

Florida

ST

 

N/A

Dahlberg (1969)

Fundulidae

Fundulus majalis

Fundulus similis

Florida

Te

 

N/A

Duggins et al. (1995)

Gadidae

Gadus morhua

Melanogrammus aeglefinus

Nova Scotia

Te

 

N/A

Gardner (1997)

Gadidae

Gadus morhua

Gadus morhua

Baltic Sea; North Sea

Te

 

N/A

Nielsen et al. (2003)

Haemulidae

Anisotremus virginicus

Anisotremus surinamensis

Brazil

ST

 

N/A 

Bernardi et al. (2013)

Haemulidae

Haemulon flaviguttatum

Haemulon maculicauda

Panama

Tr

 

N/A 

Rocha et al. (2008)

Haemulidae

Haemulon bonariense

Haemulon parra

Venezuela

Tr

 

N/A 

Rocha et al. (2008)

Hexagrammidae

Hexagrammos octogrammus

Hexagrammos otakii

Japan

Te

R

C

Munehara et al. (2000), Crow et al. (2010)

Hexagrammidae

Hexagrammos octogrammus

Hexagrammos agrammus

Japan

Te

R

C

Munehara et al. (2000), Crow et al. (2010)

Hexagrammidae

Hexagrammos agrammus

Hexagrammos otakii

Japan

Te

R

C

Munehara et al. (2000), Crow et al. (2010)

Labridae

Bodianus pulchellus

Bodianus rufus

Brazil

Tr

 

N/A

Sazima and Gasparini (1999)

Labridae

Halichoeres garnoti

Halichoeres bivittatus

Belize, Caribbean

Tr

H

C

Yaakub et al. (2007)

Labridae

Notolabrus celidotus

Notolabrus fucicola

NE New Zealand

Te

R

Q

Ayling (1980)

Labridae

Notolabrus celidotus

Notolabrus inscriptus

NE New Zealand

Te

 

N/A

Ayling (1980)

Labridae

Notolabrus fucicola

Notolabrus inscriptus

NE New Zealand

Te

 

N/A

Ayling (1980)

Labridae

Notolabrus fucicola

Notolabrus tetricus

SE Australia

Te

 

N/A

Russell (1988)

Labridae

Thalassoma jansenii

Thalassoma quinquevittatum

Coral Sea

Tr

R, H

Q

Yaakub et al. (2006)

Labridae

Thalassoma hardwicke

Thalassoma quinquevittatum

Saipan

Tr

 

N/A

Myers (1999)

Labridae

Thalassoma lutescens

Thalassoma duperrey

Johnston Atoll

Tr

 

N/A 

Sale (1991), Lobel (2003)

Labridae

Thalassoma nigrofasciatum

Thalassoma quinquevittatum

Coral Sea

Tr

 

N/A

Walsh and Randall (2004)

Merlucciidae

Merluccius capensis

Merluccius paradoxus

South Africa

Te

R

C

Miralles et al. (2014)

Moronidae

Dicentrarchus labrax

Dicentrarchus labrax

Mar Menor

ST

 

N/A

Lemaire et al. (2005)

Pleuronectidae

Isopsetta isolepis

Parophrys vetulus

Puget Sound, WA USA

Te

 

N/A 

Garrett (2005)

Pleuronectidae

Limanda limanda

Platichthys flessus

England

Te

 

N/A

Norman (1934)

Pleuronectidae

Limanda limanda

Pleuronectes platessa

England

Te

 

N/A

Norman (1934)

Pleuronectidae

Platichthys flessus

Pleuronectes platessa

Baltic Sea; England

Te

 

N/A 

Norman (1934)

Pleuronectidae

Platichthys stellatus

Kareius bicoloratus

Japan

Te

R

C

Fujio (1977)

Pleuronectidae

Platichthys stellatus

Parophrys vetulus

Puget Sound, WA USA

Te

H

Q

Schultz and Smith (1936), Garrett et al. (2007)

Pleuronectidae

Pleuronectes platessa

Glyptocephalus cynoglossus

Baltic Sea

Te

 

N/A 

Norman (1934)

Pleuronectidae

Pseudopleuronectes americanus

Limanda ferruginea

New York, NY USA

Te

H

C

Nichols (1918)

Pomacanthidae

Apolemichthys xanthurus

Apolemichthys trimaculatus

Seychelles; Maldives

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Centropyge eibli

Centropyge flavissima

Christmas Is.

Tr

R

Q

Pyle and Randall (1994), DiBattista et al. (2012)

Pomacanthidae

Centropyge eibli

Centropyge vrolikii

Indonesia

Tr

R

C

Pyle and Randall (1994), DiBattista et al. (2012)

Pomacanthidae

Centropyge flavissima

Centropyge vrolikii

Marshall Is.; Christmas Is.

Tr

R

Q

Pyle and Randall (1994), DiBattista et al. (2012)

Pomacanthidae

Centropyge loricula

Centropyge potteri

Hawaii

Tr

R

C

Pyle and Randall (1994)

Pomacanthidae

Centropyge bispinosa

Centropyge heraldi

Philippines

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Centropyge bispinosa

Centropyge shepardi

Guam

Tr

R

C

Pyle and Randall (1994)

Pomacanthidae

Chaetodontoplus caeruleopunctatus

Chaetodontoplus septentrionalis

Japan

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Chaetodontoplus melanosoma

Chaetodontoplus septentrionalis

Indonesia; Taiwan-S Japan

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Holacanthus bermudensis

Holacanthus ciliaris

Florida

Tr

H, D, R

Q

Feddern (1968)

Pomacanthidae

Paracentropyge multifasciata

Paracentropyge venusta

Philippines

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Pomacanthus arcuatus

Pomacanthus paru

Laboratorya

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Pomacanthus chrysurus

Pomacanthus maculosus

Kenya

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Pomacanthus maculosus

Pomacanthus semicirculatus

Kenya

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Pomacanthus sexstriatus

Pomacanthus xanthometapon

GBR

Tr

 

N/A 

Pyle and Randall (1994)

Pomacanthidae

Pomacanthus navarchus

Pomacanthus xanthometapon

Aquariuma

Tr

 

N/A 

Pyle and Randall (1994)

Pomacentridae

Abudefduf abdominalis

Abudefduf vaigiensis

Hawaii

Tr

R

Q

Maruska and Peyton (2007), Coleman et al. (2014)

Pomacentridae

Acanthochromis polyacanthus

Acanthochromis polyacanthus

GBR

Tr

H

C

Planes and Doherty (1997), van Herwerden and Doherty (2006)

Pomacentridae

Stegastes planifrons

Stegastes leucostictus

Florida

Tr

 

N/A 

Gardner (1997)

Pomacentridae

Amphiprion chrysopterus

Amphiprion sandaracinos

PNG

Tr

R, H

Q

Fautin and Allen (1997), Gainsford et al. (2015)

Pomacentridae

Amphiprion bicicntus

Amphiprion omanensis

Scocotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Pomacentridae

Dascyllus carneus

Dascyllus margintus

Scocotra Archipelago

Tr

R

Q

DiBattista et al. (2015)

Scaridae

Chlorurus perspicillatus

Chlorurus sordidus

Hawaii

Tr

 

N/A 

Randall (2005)

Sciaenidae

Argyrosomus inodorus

Argyrosomus japonicus

South Africa

Te

R

C

Mirimin et al. (2014)

Scombridae

Scomberomorus commerson

Scomberomorus guttatus

India

Tr

R, H, O

C

Rao and Lakshmi (1993)

Scophthalmidae

Scophthalmus maximus

Scophthalmus rhombus

Baltic Sea; North Sea

Te

H

C

Holt (1883), Norman (1934)

Scophthalmidae

Scophthalmus maximus

Scophthalmus maximus

Baltic Sea; North Sea

Te

 

N/A 

Nielsen et al. (2004)

Sebastidae

Sebastes auriculatus

Sebastes caurinus

Puget Sound, WA USA

Te

 

N/A 

Seeb (1998), Buonaccorsi et al. (2005)

Sebastidae

Sebastes auriculatus

Sebastes maliger

Puget Sound, WA USA

Te

 

N/A 

Seeb (1998), Buonaccorsi et al. (2005)

Sebastidae

Sebastes caurinus

Sebastes maliger

Puget Sound, WA USA

Te

 

N/A 

Seeb (1998)

Sebastidae

Sebastes fasciatus

Sebastes mentella

S Newfoundland

Te

R, H

C

Roques et al. (2001)

Serranidae

Hypoplectrus aberrans

Hypoplectrus nigricans

Panama

Tr

H, D

Q

Fischer (1980)

Serranidae

Hypoplectrus unicolor

Hypoplectrus puella

Jamaica

Tr

R, H

Q

Fischer (1980)

Serranidae

Hypoplectrus aberrans

Hypoplectrus puella

Panama

Tr

H, D

Q

Fischer (1980)

Serranidae

Hypoplectrus puella

Hypoplectrus indigo

Panama

Tr

R, D

Q

Fischer (1980)

Serranidae

Plectropomus maculatus

Plectropomus leopardus

GBR

Tr

R, H

Q

Frisch and van Herwerden (2006)

Siganidae

Siganus guttatus

Siganus lineatus

Philippines

Tr

 

N/A 

Kuriiwa et al. (2007)

Siganidae

Siganus doliatus

Siganus virgatus

Philippines

Tr

 

N/A 

Kuriiwa et al. (2007)

Siganidae

Siganus corallinus

Siganus puellus

Palau

Tr

 

N/A 

Kuriiwa et al. (2007)

Siganidae

Siganus fuscescens

Siganus canaliculatus

Japan

ST

 

N/A 

Kuriiwa et al. (2007)

Siganidae

Siganus unimaculatus

Siganus vulpinus

Philippines

Tr

 

N/A 

Kuriiwa et al. (2007)

Soleidae

Solea aegyptiaca

Solea senegalensis

France; Tunisia

ST

 

N/A 

She et al. (1987), Ouanes et al. (2011)

Tetraodontidae

Arothron nigropunctatus

Arothron mappa

Christmas Is.

Tr

R

Q

Hobbs et al. (2009)

Triglidae

Prionotus alatus

Prionotus paralatus

Alabama, USA

ST

 

N/A

McClure and McEachran (1992)

Locations where the hybrids were reported from; general climatic pattern of the waters where the hybridising species are found: tropical (Tr), subtropical (ST) or temperate (Te); ecological factor having a role in the hybridisation, as suggested by the author(s): rarity of one or both parental species (R), overlapping habitat use (H) or dietary overlap (D) of the putative parents and other (O); quantitative ecological/behavioural data are available in the selected hybrid report (Q); circumstantial, anecdotal or hypothetical evidence is provided (C); no ecological/behavioural data are present in the hybrid report (N/A). Sources are mostly first reports: where more than one reference is provided, the more recent studies have further evaluated the same hybrids

aNot included in the summary calculations and discussion presented here, because the hybridisations were not observed in the wild

Taxonomic distribution and genetic relatedness

There is apparent taxonomic bias in the incidence of hybridisation among marine fishes. The families Chaetodontidae and Pomacanthidae account for a combined total of almost 40 % of all marine fishes reported to hybridise (Fig. 2). Even within the Chaetodontidae, there are considerable biases between clades in the proportion of species that hybridise (Hobbs et al. 2013). Of the remaining 26 families of marine fish involved in hybridisation, 12 (Acanthuridae, Clupeidae, Gadidae, Haemulidae, Hexagrammidae, Labridae, Pleuronectidae, Pomacentridae, Scophthalmidae, Sebastidae, Serranidae and Siganidae) had more than one reported natural hybrid (Fig. 2). Taxonomic bias in hybridisation is also evident in freshwater fishes (Scribner et al. (2000): 139 reported hybrids, involving 168 species across 19 families (not including cichlids), two of which, the Cyprinidae (40 %) and Centrarchidae (20 %), accounted for the most hybrids.
Fig. 2

Number of hybrid marine fishes grouped by family. Almost 40 % of the reported hybrids belong to families Chaetodontidae and Pomacanthidae, two taxa characterised by striking colour patterns and that receive disproportionately high attention from SCUBA divers and aquarium enthusiasts

Some genetic factors may explain taxonomic bias in hybridisation incidence. For example, the reported extensive chromosome conservatism of chaetodontids (Molina et al. 2013) may increase genetic compatibility of hybridising species. Families that contain a high proportion of recently diverged species may also be more prone to hybridise when they come into contact. More than 90 % of marine and 68 % of freshwater hybrid fishes were congeneric (Scribner et al. 2000). Intergeneric hybrids represent the minority and are confined to particular families of marine and freshwater fishes: the Pleuronectidae (87 %) and Cyprinidae (96 %), respectively (Scribner et al. 2000). These genetic patterns to hybridisation suggest there may be a divergence threshold beyond which the ability to hybridise is lost, as shown in terrestrial species (Mallet 2005).

Sufficient genetic relatedness is a condicio sine qua non for the successful production of viable hybrids (Mallet 2007). Although it is difficult to summarise the genetic distance between hybridising species, mainly because authors have used different molecular markers in their studies, some examples can provide insights into the range of distances within which hybridisation is successful. In the Chaetodontidae, species diverging as little as 0.7 % (McMillan and Palumbi 1995) and as much as 5 % at the same mitochondrial marker (cytochrome b), have been shown to hybridise successfully and produce viable offspring (McMillan et al. 1999; Montanari et al. 2012). Similarly, in the Labridae, hybridisation occurs between species (Yaakub et al. 2006, 2007), with reported genetic distances ranging from <2 % (Bernardi et al. 2004) to >5.5 % (Barber and Bellwood 2005). Divergences in the order of 1 % (at the molecular markers of focus) are commonly reported for hybridising fishes in some families (e.g. Acanthuridae (Marie et al. 2007) and Serranidae (van Herwerden et al. 2006; Craig and Hastings 2007)). In contrast, menhadens of genus Brevoortia have been reported to hybridise (Hettler 1968; Dahlberg 1969) despite being as much as 20 % divergent (Anderson 2007). Further, reported intergeneric crosses in flatfishes (Norman 1934) involve species as far apart as >25 % (Verneau et al. 1994), however the latter examples represent a minority of the hybridisations reviewed here (Table 1). Examination of families with a high incidence of hybridisation and reliable published phylogenies reveals that hybridisation is prevalent between species and their closest relative: for example, 63 % of cases for the Chaetodontidae (Littlewood et al. 2004; Fessler and Westneat 2007) and 42 % for Pomancanthidae (Hodge et al. 2013; Gaither et al. 2014) (Table 1). Thus, it is clear that marine fishes have a propensity to hybridise that spans across a wide range of genetic distances, however hybridisation is most prevalent among closely related species.

Latitudinal distribution

The plethora of recent studies demonstrating hybridisation in coral reef fishes (Richards and Hobbs 2015) disproves the traditional view that hybridisation is rare on coral reefs (Hubbs 1955). Indeed, the majority (almost 70 %) of marine fish hybrids have been reported from tropical waters (Table 1). This contrasts with the latitudinal distribution of hybrid fishes in freshwater, where over 90 % of the crosses are either temperate or subtropical (Scribner et al. 2000). It is not clear whether there is an underlying reason for this apparent latitudinal bias in marine fish hybrid formation, or whether it is merely a reflection of the higher number of species in the tropics, or greater sampling effort and accessibility to shallow tropical reefs. However, the fact that hybridisation is most prevalent in a high diversity system raises the key question as to whether hybridisation has contributed to this diversity, as is the case for African cichlids (Seehausen 2004), which is a topic worthy of further investigation using molecular approaches.

Ecology of natural hybridisation in fishes

In freshwater fishes, the importance of the ecology of the parent species in facilitating hybridisation has been well documented (Scribner et al. 2000); this may also be true for marine fishes. Ecological factors implicated in 48 % of freshwater fish hybridisation events were grouped into three categories: 1) rarity of parental species; 2) spatial overlap in habitat use by the parental species; 3) habitat loss, range expansion, limited spawning habitat and unspecified natural factors (Scribner et al. 2000). Only one natural hybridisation event in freshwater fish implicated a role for both rarity and overlap in habitat use.

Despite the recent surge in reported cases of natural hybridisation in marine fishes, the majority of studies lack quantitative data on the role of ecological factors (Table 1). Ecological factors are quantified in only 24 % of hybrid cases, while circumstantial evidence or hypothetical statements are presented in 22 % of cases (Table 1). Where ecological factors were implicated, rarity of one or both parent species was indicated as the primary factor promoting hybridisation in 81 % of the reports on hybrid marine fishes (Table 1). In the remaining cases, habitat use overlap was invoked 54 % of the time, often in combination with diet overlap. Dietary overlap has received some attention for facilitating marine fish hybridisation (15 % of reported cases), always in association with another ecological driver (Table 1). Specific evidence for each of these factors (rarity of parental species, habitat overlap and dietary overlap) is discussed in turn.

Rarity of parental species

Rarity of the putative parental species has been indicated as a facilitator of hybridisation in marine fish since the early work of Hubbs (1955). Intuitively, a lack of conspecific partners increases the chance that an individual will mate with a heterospecific partner (Hubbs 1955). For hybridising marine species, rarity of parent species has been reported in tropical (24 cases), temperate (nine cases) and subtropical (one case) waters (Table 1) (Gosline 1948; Hettler 1968; Fujio 1977; Ayling 1980; Roques et al. 2001; Crow et al. 2010; Miralles et al. 2014; Mirimin et al. 2014). Most studies on the hybridisation of fishes do not however, explicitly consider the local abundance of putative parent species (Feddern 1968; Fischer 1980; Frisch and van Herwerden 2006; Yaakub et al. 2006; Marie et al. 2007; Maruska and Peyton 2007; Hobbs et al. 2009; Montanari et al. 2012; Coleman et al. 2014; Montanari et al. 2014; DiBattista et al. 2015), which makes it difficult to comprehensively assess the importance of mate scarcity in the hybridisation of fishes.

Hybridisation in marine fishes is particularly prevalent at the intersection of biogeographic regions, where species often come into contact with sister species (Hobbs et al. 2009; Hobbs and Allen 2014; DiBattista et al. 2015; Richards and Hobbs 2015). A notable hotspot for hybridisation is Christmas Island (Indian Ocean), where there is overlap of Pacific and Indian Ocean fauna (Hobbs and Salmond 2008). Of the 681 fish species that have been reported at Christmas Island, 286 (42 %) are considered rare (<2 individuals per 3000 m2) (Hobbs et al. 2014), which may promote high levels of hybridisation at this location. Moreover, at least 80 % (12 out of 15) of the putative parental species of commonly observed hybrid fishes recorded from this location are rare (Hobbs and Allen 2014). Species are often rare at the extremes of their geographical ranges, but parental rarity can facilitate hybridisation even when the hybrid zone is more central to the species’ ranges (Hettler 1968).

In some instances, extreme rarity of a hybridising species results from vagrants (Hobbs et al. 2013). Species not known to hybridise within their normal geographic ranges may hybridise as vagrants. Vagrant fishes, straying from their distributional ranges, may hybridise with allopatric sister species or endemics (Severns and Fiene-Severns 1993; Maruska and Peyton 2007; Craig 2008). Parental rarity has also been shown to favour hybridisation at several spatial scales, from individual coral heads to entire sections of the reef (Feddern 1968). The range of magnitudes and spatial scales at which rarity can play a role in initiating hybridisation in tropical marine fishes requires further investigation (Epifanio and Nielsen 2000). Although hybridisation is reportedly common when one parent species is rare, there are several instances where both parent species are common (Hobbs et al. 2009, 2013; Coleman et al. 2014). Thus factors other than rarity of a parent species may also play a role in hybridisation.

The lack of a conspecific partner appears to promote hybridisation across the range of mating systems exhibited by marine fishes including: pair spawning, haremic and mass spawning. Hybridisation has been reported in monogamous anemonefishes (Gainsford et al. 2015) and pair-forming butterflyfishes (Hobbs et al. 2013; Montanari et al. 2014). Pygmy angelfishes tend to spend their lives in harems, and hybridising species are often observed in heterospecific harems and interbreeding (Moyer et al. 1983; Hobbs et al. 2009; Hobbs and Allen 2014). Some species only form harems during spawning times, and these species may also hybridise (Frisch and van Herwerden 2006). For mass-spawning species, Gosline (1948) suggested that congeneric mating might occur where there are too few of one species to initiate reproductive behaviour. Thus, in a range of mating systems, species are deliberately choosing to mate with another species.

Rarity has also been reported to act in synergy with some degree of niche overlap (either spatial or dietary) between the two parent species to breakdown reproductive isolation—e.g. Hypoplectrus spp., (Fischer 1980)—(Table 1). In another case of serranid hybridisation, rarity of one species was reported to promote hybridisation in synergy with habitat overlap at several locations along a latitudinal gradient (Frisch and van Herwerden 2006). The concomitant effect of rarity of the parental species and habitat overlap has also been shown to favour hybridisation in the Labridae (Yaakub et al. 2006), Acanthuridae (Fig. 3) (Marie et al. 2007) and Chaetodontidae (Montanari et al. 2012; Hobbs et al. 2013; Montanari et al. 2014) (Table 1). Further ecological assessment of reef fish hybrid zones is required to quantify the relative importance of ecological factors promoting hybridisation. In particular, to determine if local rarity of one or both parental species has a role in initiating hybridisation, abundance surveys should be routinely conducted in the context of hybridisation studies (Fig. 1). This type of survey is inexpensive and time efficient, especially when combined with necessary sampling for genetic analyses, and it can further provide a direct estimate of hybrid prevalence. The presence of marine suture zones (Remington 1968), biogeographic borders where multiple species pairs come into secondary contact and hybridise (Hobbs et al. 2009), provides the opportunities to investigate the relative contribution of ecological promoters of hybridisation across multiple taxa in the same setting.
Fig. 3

Acanthurus leucosternon (a) in a multispecies roving school with A. nigricans (b). Hybridisation between these two species at Christmas Island is mediated by rarity of one parent species and some degree of niche overlap (habitat and diet) (Marie et al. 2007)

Niche overlap

Even if species co-occur within the same geographic location, inter-specific reproduction will be conditional on some level of niche overlap, such that interbreeding individuals co-occur in the same space concurrently. For extreme habitat-specialists, such as anemone fishes or coral-dwelling fishes, inter-breeding species must co-habit the same specific habitat type (Gainsford et al. 2015). Anemone fishes have species-specific preferences for their host anemones, and the control of this limiting resource can lead to strong interspecific competition (Gainsford et al. 2015). To cohabit an anemone, two species must have the same preference and also be willing to disregard interspecific competition (Gainsford et al. 2015). As such, hybridisation among anemonefishes may be somewhat constrained by species-specific use of different microhabitats (Gainsford et al. 2015). For more generalist or wide-ranging species, niche overlap may be structured by depth distributions or large-scale habitat preferences. This is important because changes in habitat availability, due to either acute disturbances or sustained degradation of natural ecosystems (Mullen et al. 2012), may bring species together that normally occupy very distinct habitats, thereby facilitating hybridisation (Yaakub et al. 2006).

Despite being a necessary precursor to hybridisation, habitat overlap has been articulated only in 20 cases of marine fish hybridisation, almost 28 % of which contained no indication of another ecological driver acting in synergy with habitat overlap to facilitate the hybrid formation process (Table 1) (Nichols 1918; Norman 1934; Schultz and Smith 1936; Yaakub et al. 2006, 2007; Mullen et al. 2012; Gainsford et al. 2015). Fisheries catch and observational data indicated an overlap in the depth range and substrate use of the hybridising species in early works on flatfishes (f. Pleuronectidae) (Nichols 1918; Norman 1934; Schultz and Smith 1936). More recently, in their molecular genetic assessment of a hybrid between the two Caribbean wrasses Halichoeres garnoti and H. bivittatus, Yaakub et al. (2007) indicated that this hybridisation event might have been driven mainly by habitat use overlap in concomitance with synchronous spawning events (Table 1).

Habitat overlap can increase the likelihood of hybridisation in marine fishes at several spatial scales (Feddern 1968). In hamlets (f. Serranidae), species with broad, fully overlapping depth distributions have been found to hybridise just as readily as species that only share a narrow depth range (Fischer 1980). Broadly overlapping habitats have been shown to promote hybridisation between the menhadens Brevoortia patronus and B. smithi (f. Clupeidae) (Hettler 1968), as well as the surgeonfishes Acanthurus achilles and A. nigricans (f. Acanthuridae) (Randall 1956). Conversely, in another case of hybridisation between the surgeonfishes Acanthurus leucosternon and A. nigricans, the species involved shared a very narrow depth range, where they were also observed foraging together, indicating a possible dietary overlap (Marie et al. 2007). Acanthurus nigricans is able to setup and defend territories, but may also form roving schools (Marie et al. 2007). These are often multispecies assemblages, not formed to defend a resource (Fig. 3). Having the same dietary preferences aids in keeping the multispecies groups together, because individuals share a common goal (Fig. 3). Avoiding territorial defence and moving in a roving school may, therefore, create opportunities for hybridisation (Marie et al. 2007). Habitat overlap can favour hybridisation even when two species have markedly different distributions on a reef: for instance if one species occurs exclusively on the reef flat, where it encounters individuals of the second species straying from their normal reef crest habitat (Yaakub et al. 2006). Habitat modifications (e.g. breakwater structures) can lead to hybridisation because species occupying discrete depth zones and habitats come into close proximity and interact (Kimura and Munehara 2010).

Aside from spatial overlap and co-occurrence of interbreeding species, the capacity to hybridise may also be facilitated by the timing of reproduction (Schultz and Smith 1936; Frisch and van Herwerden 2006). Regardless of the reproductive mode, spatial and temporal overlap of spawning events facilitate hybridisation in compatible species (van Herwerden and Doherty 2006). In 73 % of the reported cases, parental habitat overlap was said to be a factor for marine fish hybridisation in synergy with parental rarity, dietary overlap or a combination of the two. In all but two cases (Gosline 1948; Rao and Lakshmi 1993), the authors included quantitative data to illustrate habitat overlap (Randall 1956; Feddern 1968; Hettler 1968; Fischer 1980; Frisch and van Herwerden 2006; Yaakub et al. 2006; Marie et al. 2007; Montanari et al. 2012; Mullen et al. 2012; Hobbs et al. 2013).

If inter-breeding species co-occur, it does not seem necessary that they also exploit the same dietary resources. However, high levels of dietary overlap may increase encounters between potential heterospecific partners (Grant and Grant 2002). Conversely, very high levels of dietary overlap may lead to levels of inter-specific competition (Blowes et al. 2013) that may reinforce reproductive isolation. To assess if this is the case, where possible, competitive interactions between potentially hybridising species should be recorded from the hybrid zone (Fig. 1). Among the Chaetodontidae, Hobbs et al. (2013) suggested that specialist coral-feeding species were less likely to hybridise than generalist feeders, which may well reflect strong inter-specific competition among species that are coral-feeding specialists. Even so, dietary overlap is suggested to be an important facilitator of hybridisation for at least seven pairs of marine fishes, always in combination with another ecological process (Table 1). In all of these studies, the diets of the putative parents were deemed essentially the same (Randall 1956; Feddern 1968; Fischer 1980; Montanari et al. 2012, 2014). Generalist corallivorous butterflyfishes of genus Chaetodon come into contact frequently as they are feeding on the same resources and hybridise (Montanari et al. 2012, 2014). Some Chaetodontids are territorial and defend food resources, but these two pairs of hybridising sister species are willing to share the same food source, instead of competitively excluding one another (Montanari et al. 2012, 2014). Analogous to the research on terrestrial species that identified a threshold for successful hybridisation as less than 10 % genetic divergence (that is, >90 % overlap) between parent species, documentation of habitat and dietary preference data within the hybrid zone (Fig. 1) would be helpful in determining the degree of niche overlap that is required for successful hybridisation in marine fishes. Field-based experiments that involve manipulating the amount of food or habitat resources available could be used to identify these thresholds.

Behaviour of hybridising marine fishes

Most marine fishes spawn gametes resulting in external fertilization and interbreeding between species can occur accidently or deliberately. Accidental hybridisation occurs when two species mate homospecifically at the same time and place and the gametes from different species inadvertently mix, resulting in fertilisation and viable offspring. Accidental hybridisation may be common in other marine groups—e.g. corals (Willis et al. 2006), however only three studies explicitly implicate its role in marine fish hybridisation (Gosline 1948; Frisch and van Herwerden 2006; Yaakub et al. 2007). For marine fishes, multi-species spawning aggregations do exist (Heyman and Kjerfve 2008; Karnauskas et al. 2011) and although accidental hybridisation has occasionally been suggested, no conclusive evidence has been provided (Frisch and van Herwerden 2006; Yaakub et al. 2007).

Deliberate interbreeding has been more commonly reported for hybridising marine fishes (16 studies in Table 1). Although this can occur through the deliberate choice of one species and not the other—e.g. sneak spawning (Frisch and van Herwerden 2006), more commonly reported is the formation of heterospecific social groups where both species choose to interbreed. For example, pygmy angelfishes form harems and two species may accept each other in the harem and choose to interbreed (Moyer et al. 1983; Hobbs and Allen 2014). Similarly, hybridising butterflyfishes are often observed as a long-lasting heterosexual breeding pair (Hobbs et al. 2013; Montanari et al. 2014). In damselfishes that lay demersal eggs, not only does hybridisation represent a deliberate choice by both species during courtship and spawning, but it also represents a deliberate choice by a male to care for, and guard, the eggs of another species (Maruska and Peyton 2007; Gainsford et al. 2015). Thus, hybridisation in many marine fishes is due to a breakdown in assortative mating through deliberate choices made by both parent species. These choices may be influenced by local conditions (e.g. a lack of conspecific partners). It is therefore important to carefully document the abundance and temporal stability of mixed social groups (Fig. 1), to determine how and to what extent their offspring will influence the hybrid zone population.

Conclusions and future directions

Natural hybridisation among marine fishes has been underestimated and perhaps overlooked until very recently. In terrestrial and freshwater systems, by contrast, hybridisation is recognised as being not only highly prevalent, but also important in speciation (Seehausen 2004), extinction (Rhymer and Simberloff 1996) and adaptability to novel environments (Grant and Grant 2002). The literature on marine fish hybrids has been dominated by studies documenting hybrids, or more recently, determining the genetic consequences of hybridisation. Much less research has focused on determining the causes of hybridisation. This review has identified the ecological and behavioural processes that have most frequently been ascribed a role in the initiation of hybridisation in marine fishes, and highlighted a general lack of quantitative ecological and behavioural data from within fish hybrid zones. Understanding how ecological and behavioural processes enable species to overcome the barriers to reproductive isolation (e.g. assortative mating) will prove useful in contextualizing the consequences of hybridisation in the marine environment.

Despite being widely acknowledged (Albert et al. 2006), the need for quantitative ecological and behavioural data is rarely met in marine fish hybridisation studies (but see (Frisch and van Herwerden 2006; Yaakub et al. 2006; Marie et al. 2007; Montanari et al. 2012, 2014; DiBattista et al. 2015; Gainsford et al. 2015). Figure 1 provides a framework for gathering ecological and behavioural data at the critical steps in initiating hybridisation and overcoming pre-zygotic barriers to reproductive isolation. Mate choice experiments would be required to test which factors are most important to the breakdown in assortative mating. Surprisingly, there has been a lack of mate choice experiments on hybridising marine fishes, and the approach used in McMillan et al. (1999) illustrates how to test the role of mate choice in the breakdown in assortative mating.

As described above, niche overlap (particularly habitat/microhabitat and diet) has been identified in several hybrid reports as a factor increasing heterospecific encounters between potentially hybridising species. In situ surveys documenting habitat and dietary preferences of parental species (Fig. 1) can help to quantify the degree of such overlap. Quantification would in turn provide a means to differentiate between species that rarely come into contact within the hybrid zone—leading to rare, evolutionarily irrelevant hybridisation events (Yaakub et al. 2007)—and species that, conversely, spend most of their lives together in heterospecific social groups, thereby producing a large number of viable hybrid offspring with rapid evolutionary and adaptive consequences (Taylor et al. 2006).

Field studies that document key ecological and behavioural factors (Fig. 1) are required to identify the proximal cause for hybridisation in marine fishes. Previous work on hybridising Galapagos finches provides an example of a successful approach. Careful documentation of abundance (and diet) through time enabled the authors to show that hybrid numbers rapidly fluctuated in response to resource availability, resulting in the persistence of the population in times of scarcity (Grant and Grant 2002; Grant et al. 2005; Grant and Grant 2008). Similarly, it was thanks to abundance data that the mechanism underlying mixed pair formation was elucidated, namely the choice to mate with more abundant heterospecific partners in response to conspecific rarity mediated by a lack of food resources (Grant and Grant 2002). Further, careful documentation of the ecology and behaviour of hybridising and non-hybridising relatives within the hybrid zone is required to tease out which factors are most important to initiating hybridisation. Similarly, comparisons between ecological conditions inside and outside a hybrid zone will help determine what facilitates hybridisation between sympatric species in some parts of the range but not elsewhere. It is also important to test predictions by considering ecological similarities among closely related species that do not hybridise, despite opportunities to interbreed when co-occurring. Finally, experiments involving the manipulation of abundance, availability of adult mates, amount and type of food or habitat, could be used on suitable species (e.g. anemonefish) to determine the relative importance of different ecological and behavioural factors in facilitating hybridisation. Determining what conditions cause hybridisation in marine fishes is critical to understanding how marine fishes achieve reproductive isolation and thus initiate the speciation process. Finally, elucidating the causes of hybridisation is necessary to predicting how changing environmental conditions will affect hybridisation.

Notes

Acknowledgments

This work was financially supported by AIMS@JCU (SRM). We thank two anonymous reviewers for comments that improved this manuscript.

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Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Stefano R. Montanari
    • 1
    • 2
  • Jean-Paul A. Hobbs
    • 3
  • Morgan S. Pratchett
    • 4
  • Lynne van Herwerden
    • 2
    • 5
  1. 1.College of Marine and Environmental SciencesAustralian Institute of Marine Science, James Cook University (AIMS@JCU)TownsvilleAustralia
  2. 2.Centre for Sustainable Tropical Fisheries and AquacultureJames Cook UniversityTownsvilleAustralia
  3. 3.The Oceans Institute and School of Plant BiologyUniversity of Western AustraliaCrawleyAustralia
  4. 4.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  5. 5.College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia

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