2727_C07.fm Page 265 Wednesday, June 30, 2004 12:52 PM SPAWNING AGGREGATIONS OF CORAL REEF FISHES: CHARACTERISTICS, HYPOTHESES, THREATS AND MANAGEMENT JOHN CLAYDON Department of Marine Biology, James Cook University, Townsville, Queensland 4811, Australia E-mail: John.Claydon@jcu.edu.au Abstract Many coral reef fishes migrate to form short-lived aggregations at predictable sites and times in order to spawn For the purposes of this review, such spawning aggregations are defined as any temporary aggregations formed by fishes that have migrated for the specific purpose of spawning Spawning aggregations are known to be formed by 164 species from 26 families of coral reef fishes, but the actual number is likely to be much higher Aggregative spawners share a number of common features (1) All except one species release pelagic eggs (2) They tend to have large body sizes (3) They are more abundant in some phylogenetic groups, such as the Labridae, Scaridae, Serranidae, Acanthuridae, and Lutjanidae, although they are relatively uncommon in all but the least speciose families of Albulidae, Chanidae, Gerreidae, and Scombridae (4) They are more likely to come from large populations with high densities However, these features are not independent and their relative importance is not easily assessed Known spawning aggregations form at the same sites over successive, predictable spawning seasons However, from the limited data presently available, spawning aggregations not appear to form consistently on predictable reef structures The periodicity of spawning aggregations can differ greatly for the same species with relatively small degrees of spatial separation A number of hypotheses have been proposed to explain why, when, and where spawning aggregations are formed These include those that predict that the phenomenon of aggregative spawning (1) reduces predation on spawning adults and their eggs (the predator satiation hypothesis), (2) increases the degree of mate selectivity, and (3) allows individuals to assess sex ratios of populations and make decisions on sex change accordingly Other hypotheses predict that the location and timing of spawning aggregations (1) reduce predation on both eggs (the egg predation hypothesis) and spawning adults (the predator evasion hypothesis), (2) increase the probability that larvae will settle on reefs (the egg dispersal hypothesis and the larval retention hypothesis), and (3) enhance the survival of larvae during their pelagic phase (the pelagic survival hypothesis) However, very little quantitative research addressed at an appropriate scale has been conducted to distinguish among these hypotheses, many of which make common predictions Spawning aggregations of commercially important coral reef fishes have been lost in many locations throughout the tropics because unsustainable fishing targets the spawning aggregations themselves The live reef food-fish trade has proven to be unsustainable in almost all locations in which it has operated, leading to widespread impoverishment and eradication of spawning aggregations Appropriate management, legislation, and enforcement are essential to protect the stocks of commercially important aggregative spawners, as is a more comprehensive understanding of the dynamics of spawning aggregations 0-8493-2727-X/04/$0.00+$1.50 Oceanography and Marine Biology: An Annual Review 2004, 42, 265–302 © R N Gibson, R J A Atkinson, and J D M Gordon, Editors © 2005 by CRC Press LLC 265 2727_C07.fm Page 266 Wednesday, June 30, 2004 12:52 PM 266 J Claydon Introduction Many marine animals migrate to breeding sites at predictable locations and times to form conspecific breeding aggregations A multiphyletic array of animals are known to display this behaviour, including mammals (e.g., gray whales, Jones et al 1984), reptiles (e.g., olive ridley turtles, Plotkin et al 1997), fishes (e.g., salmonids, Groot & Margolis 1991), crustaceans (e.g., the Christmas Island red crabs, Adamczewska & Morris 2001), molluscs (e.g., cuttlefish, Hall & Hanlon 2002), and even polychaetes (e.g., the palolo worm, American Samoa, Caspers 1984) This phenomenon appears to occur when suitable areas for feeding and breeding are spatially separated, and when the costs of migration are outweighed by the benefits of reproducing and feeding in more suitable areas The scale of these migrations ranges from daily over distances of less than a kilometre (e.g., some fish, see Domeier & Colin 1997) to annual migrations over thousands of kilometres (e.g., gray whales, Jones et al 1984) However, we are still in the early stages of understanding why, where, and when breeding aggregations occur Spawning aggregations of fishes are well-known phenomena to fishermen in all of the world’s fished oceans The spatial and temporal predictability of spawning aggregations along with the predictably high yields from low fishing effort (high catch per unit effort) make them attractive targets for fishermen (Johannes 1978, 1981) A wide variety of coral reef fishes are known to form spawning aggregations (Domeier & Colin 1997), and while the size of these spawning aggregations and their migration distances may be smaller than those of pelagic and anadromous fishes, such aggregations are dramatic features of coral reef environments Many spawning aggregations of coral reef fishes have been exploited by commercial and artisanal fishermen for centuries (Johannes & Riepen 1995) However, recent increased fishing efforts along with the efficiency of modern gears are believed to be threatening the existence of these ecologically important phenomena (Sadovy 1994, 1996, Aguilar-Perera & Aguilar-Davilá 1996) Accordingly, interest in and research on spawning aggregations of reef fishes have grown over recent years This growth is mainly in the context of management of commercially exploited species such as many of the large piscivores Although the majority of appropriate publications concern these commercially important species, the fundamental basis of why, where, and when spawning aggregations occur is likely to apply to all species The aims of this review are to (1) define spawning aggregations of coral reef fishes, (2) identify which species of coral reef fishes form spawning aggregations, (3) identify any unifying characteristics these species may have, (4) critically assess the hypotheses explaining why, when, and where spawning aggregations are formed, and (5) assess the importance of management and conservation of spawning aggregations Extensive descriptions of individual species will not be made, as this has been performed comprehensively by Domeier & Colin (1997) What are spawning aggregations? Defining spawning aggregations is problematic and to some extent arbitrary In a review by Domeier & Colin (1997) a spawning aggregation was defined as “a group of conspecific fish gathered for the purpose of spawning with fish densities or numbers significantly higher than those found in the area of aggregation during non-reproductive periods.” Albeit a practical and broadly accepted definition, it may be unnecessarily restrictive It is based around the assumption that aggregative spawners will be present in greater numbers or higher densities than at non-reproductive times, and will exclude species whose behavioural ecology contradicts this assumption Whether species are categorised as forming spawning aggregations by this definition will also vary greatly depending on the scale at which fish densities and numbers are measured The scale of measurement will need to be appropriate for each species in question In order to circumvent these complications and for the purposes of this review, a more simple definition has been adopted: spawning aggregations are any temporary aggregations formed by fishes that have migrated for the specific purpose of spawning © 2005 by CRC Press LLC 2727_C07.fm Page 267 Wednesday, June 30, 2004 12:52 PM Spawning Aggregations of Coral Reef Fishes 267 Domeier & Colin (1997) identified two types of spawning aggregations: resident and transient Resident aggregations are typified by smaller species of locally abundant populations from the same reef (e.g., Thalassoma bifasciatum) Transient aggregations are typified by commercially important species of disperse populations that migrate between reefs (e.g., Epinephelus striatus) However, this distinction is somewhat artificial All spawning aggregations are resident in that all the constituent individuals migrating to an aggregation are, by definition, resident to the spawning aggregation’s catchment area All spawning aggregations are transient because the aggregations are formed briefly during a period of reproductive activity and dissipate afterwards The distinction between resident and transient sensu Domeier & Colin (1997) is simply a matter of scale and whether species migrate between reefs In fact, the same species could be said to form a transient spawning aggregation at one site, but a resident one at another This could arise simply because the former’s catchment area consists of multiple, small, connected reefs (separated by small distances and shallow depths), whereas the latter’s catchment area consists of one large reef isolated by great distance and depth from any others This not unlikely scenario helps to illustrate that while the terms resident and transient may serve to create an artificial distinction between spawning aggregations, they are not intrinsically different Whether resident or transient and regardless of the scale of the migration or the periodicity of spawning aggregation formation, the underlying processes are identical: fishes migrate to form temporary aggregations for the specific purpose of spawning Which species spawn in aggregations? Phylogenetic distribution Globally, 164 species of reef fishes from 26 families have been identified as forming spawning aggregations (see Table 1) The highest numbers of aggregatively spawning species are found in the Labridae, Scaridae, Serranidae, Acanthuridae, and Lutjanidae families (see Table and Figure 1) However, spawning aggregation formation appears to be an uncommon characteristic relative to the total numbers of coral reef species within these families (Figure 1) Similarly, most species known to form spawning aggregations are found within families represented by proportionally few aggregative spawners (Figure 1) Although spawning aggregation formation is known for all coral reef species of Albulidae and Chanidae, as well as high proportions of Gerreidae and Scombridae, these families are represented by very few coral reef species (Figure 1) Body size The majority of aggregatively spawning species are relatively large (Figure 2) and commercially or artisanally important Although around 50% of species forming spawning aggregations are less than 50 cm in maximum total length, the relative proportion of larger reef fishes spawning in aggregations is greater than that of smaller reef fishes, and no species with a maximum total length of less than 10 cm spawn in aggregations (Figure 2) The absence of smaller species from this list of aggregative spawners has been attributed to a hypothesised correlation between size and ability to migrate to form spawning aggregations, with smaller species being unable to afford either the energetic cost of migration (energy spent in movement and time not spent feeding in preferred areas) or the increased risk of predation associated with migration (Domeier & Colin 1997) However, this opinion may attribute too much to the cost of migration Many small species of fishes, especially planktivorous and opportunistic scavenging species, spend the majority of the day moving Species like the large serranids (e.g., Epinephelus striatus) are relatively sedentary fishes and migrations will represent a considerable proportion of their energetic budget Additionally, while many small wrasses migrate daily (e.g., Thalassoma bifasciatum, Warner 1995), the © 2005 by CRC Press LLC 2727_C07.fm Page 268 Wednesday, June 30, 2004 12:52 PM 268 J Claydon Table Coral reef species known to form spawning aggregations Acanthuridae Acanthurus bahianus1,2,3 Acanthurus nigrofuscus5,6 Acanthurus coeruleus1,2,3 Acanthurus olivaceus8 Acanthurus lineatus4,5,6,7 Acanthurus triostegus5,7,9,10 Acanthurus mata Acanthurus xanthopterus8 Acanthurus nigricauda Albulidae Albula vulpes4 Balistidae Pseudobalistes flavimarginatus12 Caesionidae Caesio teres13 Pterocaesio digramma14 Carangidae Caranx ferdau4 Caranx melampygus4 Caranx ignobilis4 Elagatis bipinnulata4 Chaetodontidae Chaetodon auriga8 Chaetodon lineolatus8 Chaetodon ephippium Chaetodon melannotus8 Chaetodon kleinii8 Chaetodon rafflesi8 Chanidae Chanos chanos4 Ephippidae Platax orbicularis8 Gerreidae Gerres erythrourus4 Gerres argyreus4 Haemulidae Diagramma pictum8 Plectorhinchus chrysotaenia8 Plectorhinchus chaetodonoides Plectorhinchus flavomaculatus8 Hemiramphidae Rhynchorhamphus georgii4 Labridae Bodianus loxozonus8 Epibulus insidiator8 Cheilinus chlorourus8 Halichoeres hortulanus8 Cheilinus fasciatus8 Halichoeres prosopeion8 Cheilinus undulatus Halichoeres tenuisipinis15 Choerodon anchorago Hemigymnus melapterus8 Cirrhilabrus punctatus8 Macropharyngodon ornatus8 Coris aygula8 Pseudocoris yamashiroi16 Lethrinidae Lethrinus atkinsoni8 Lethrinus lentjan4 Lethrinus harak4 Lethrinus miniatus4 Lutjanidae Aprion virescens4 Lutjanus carponotatus8 Lutjanus analis21,22,23,24,25,26 Lutjanus cyanopterus27 Lutjanus argentimaculatus4 Lutjanus gibbus4,11 4,11 Lutjanus bohar Lutjanus griseus26 30 Lutjanus campechanus Monacanthidae Amanses scopas8 Oxymonacanthus longirostris8 © 2005 by CRC Press LLC Ctenochaetus striatus5,6,9 Naso brevirostris4,8 Naso hexacanthus4 Naso lituratus11 Naso unicornis11 Naso vlamingii8 Zebrasoma scopas9 Zebrasoma veliferum8 Gnathanodon speciosus4 Megalaspis cordyla8 Selar boops4 Chaetodon semeion8 Chaetodon trifasciatus8 Chaetodon unimaculatus8 Chaetodon vagabundus8 Heniochus singularis8 Heniochus varius8 Gerres oblongus4 Plectorhinchus gibbosus8 Plectorhinchus lineatus8 Plectorhinchus obscurus4 Plectorhinchus goldmani4 Stethojulis interrupta15 Stethojulis trilineata17 Thalassoma amblycephalum15 Thalassoma bifasciatum17,18,19,20 Thalassoma hardwicke17 Thalassoma lutescens16 Thalassoma purpureum8 Thalassoma quinquevittatum16 Lethrinus nebulosus1,34,67 Monotaxis grandoculis4 Lutjanus Lutjanus Lutjanus Lutjanus jocu27,31 kasmira8 malabaricus4 sebae4 Lutjanus synagris28 Macolor niger29 Symphorus nematophorus4 Symphorichthys spilurus4 2727_C07.fm Page 269 Wednesday, June 30, 2004 12:52 PM Spawning Aggregations of Coral Reef Fishes 269 Table (continued) Coral reef species known to form spawning aggregations Mugilidae Crenimugil crenilabis4,32 Mullidae Mulloidichthys vanicolensis8 Muraenidae Unidentified spp.35 Pomacanthidae Centropyge bicolor8 Pomacentridae Chromis cinerascens8 Priacanthidae Priacanthus hamrur8 Scaridae Bolbometopon muricatum11 Cetoscarus bicolor8 Chlorurus bleekeri8 Chlorurus gibbus4 Chlorurus sordidus8,37 Hipposcarus harid33,36 Scombridae Acanthocybium solandri4 Serranidae Anyperodon leucogrammicus8 Epinephelus adscencionis40 Epinephelus fuscoguttatus4 Epinephelus guttatus3,21,40,53,54,55,56,57,58,59 Epinephelus itajara3,21,44 Epinephelus malabracus8 Siganidae Siganus argenteus4 Siganus canaliculatus4,67 Sphyraenidae Sphyraena barracuda4 Liza vaigiensis4 Liza macrolepis4 Pseudupeneus maculatus33 Pomacanthus imperator8 Pomacanthus sexstriatus8 Hipposcarus longiceps8 Scarus altipinnis8 Scarus chameleon8 Scarus dimidiatus8 Scarus forsteni8 Scarus Scarus Scarus Scarus Scarus Grammatorcynus bicarinatus4 Scomberomorus commersoni4 Epinephelus merra4 Epinephelus polyphekadion11 Epinephelus striatus40,41,42,43,44,45,46,47,48,49 Gracila albomarginata8 Mycteroperca bonaci31,44,45,52 Mycteroperca microlepis46,60,61,62 Mycteroperca phenax46,60,61,62 Mycteroperca tigris45,52,66 Mycteroperca venenosa44,45,46,49,50,51,52,55, 66 Paranthias furcifer52 Plectropomus areolatus63 Plectropomus leopardus4,63,64,65 Pseudanthias pleurotaenia8 Pseudanthias tuka8 Siganus lineatus4 Siganus punctatus4 Siganus spinus4 frenatus8 ghobban8 globiceps8 iseri17,33,38 microrhinos8 Pygoplites diacanthus8 Scarus niger8 Scarus oviceps8 Scarus rubroviolaceus8 Scarus schlegeli8 Sparisoma rubripinne17,38,39 Sphyraena genie4 Note: 1Colin 1985; 2Colin & Clavijo 1988; 3Colin 1994; 4Johannes 1981; 5Robertson 1983; 6Myrberg et al 1988; 7Randall et al 1990; 8Squire and Samoilys, unpublished; 9Randall 1961a; 10Randall 1961b; 11Johannes et al 1999; 12Gladstone 1994; 13Bell & Colin 1986; 14Thresher 1984; 15Nakazono 1979; 16Colin & Bell 1991; 17Randall & Randall 1963; 18Warner & Robertson 1978; 19Warner & Hoffman 1980; 20Warner 1988; 21Schroeder 1924; 22Rojas 1960; 23Craig 1966; 24Claro 1981; 25Mueller 1994; 26Domeier et al 1996; 27Domeier & Colin 1997; 28Reshetnikov & Claro 1976; 29Myers 1989; 30Moe 1963; 31Carter & Perrine 1994; 32Helfrich & Allen 1975; 33Colin & Clavijo 1978; 34 Ebisawa 1990; 35 Kuiter & Debelius 1994; 36Gladstone 1996; 37Yogo et al 1982; 38Colin 1978; 39Colin 1996; 40Colin et al 1987; 41Smith 1972; 42Carter 1988a; 43Carter 1988b; 44Carter 1989; 45Fine 1990; 46Colin 1992; 47Tucker et al 1993; 48Aguilar-Perera 1994; 49Carter et al 1994; 50Olsen & LaPlace 1979; 51Bannerot 1984; 52Fine 1992; 53Burnett-Herkes 1975; 54Garciá-Moliner 1986; 55Beets & Friedlander 1992, 1998; 56Bullock et al 1992; 57Shapiro & Rasotto 1993; 58Shapiro et al 1993; 59Sadovy et al 1994a; 60Gilmore & Jones 1992; 61Coleman et al 1996; 62Koenig et al 1996; 63Johannes 1988; 64Samoilys & Squire 1994; 65Samoilys 2000; 66Sadovy et al 1994b; 67Hasse et al 1977 © 2005 by CRC Press LLC 2727_C07.fm Page 270 Wednesday, June 30, 2004 12:52 PM 270 J Claydon A 25 Frequency 20 15 10 % Coral reef species in family B 100 75 50 25 e da hi e nt ida ca tr ia en Pr ac dae ae m i id Po aen ph ur m M ira ae em id H ipp e h a Ep nid e a C istid l ae ae Ba lid id bu en Al yra e h e da Sp lida thi ul an M ac idae on n M sio dae ae ri C mb e o a Sc i l i d e ae u g a id M reid nth er a G ac e m a Po nid ae ga id Si rin ae th id Le ang dae ae ar li id C mu ont ae d H eto e da e C ani rida tj u Lu th e an ida Ac ran r e Se rida a e Sc rida b La Figure (A) The number of species of coral reef fishes known to form spawning aggregations from the 26 families identified in Table (B) The percentage of coral reef fishes in each family known to form spawning aggregations The total numbers of coral reef fishes in each of the 26 families were compiled from data found in Froese & Pauly (2000) larger species may migrate monthly during a limited spawning season The cumulative distances migrated annually by smaller daily spawning species can be equal to or higher than that of their larger transient counterparts (Figure 3) Whereas the ability to migrate is an important prerequisite for spawning in aggregations, a species’ size may not be a good determinant of this ability The prevalence of larger species may be attributable to sampling artefact Information about spawning aggregations has originated primarily from fishermen (see Johannes 1981) Therefore, it is to be expected that most species identified as being aggregative spawners are commercially or artisanally important, and thus tend to be larger fishes More non-commercial species of aggregative spawners are likely to be identified in the future as research continues (Domeier & Colin 1997) Spawning mode The lack of species from smaller size classes (