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Mid-ocean isolation and the evolution of Hawaiian reef fishes
TREE vol. 2, no. 7,July
1987
The Hawaiian fish fauna has close afinities with the fauna of the Indo-west Pacific from which it is derived, but is depauperate. It is characterized by a large number of endemic species (30% of inshore fishes), which are often the most a6undant species in their families in Hawaii. Alfhough there is evidence of focal adaptation, there has been no radiation of species within the island chain, as occurs in the terrestrial biota of isolated islands. Three major factors have contributed to these trends: (I ) the geographic isolation of the islands, and oceanographic features, especially current patterns; (2 1the life history characteristics of the fishes, especially their dispersal cupabilities; and (3 1 the extent of aduptive differentiation to environmental conditions after they reached Hawaii.
The Hawaiian archipelago is among the most isolated island groups in the world. The location of the islands with respect to Pacific current patterns contributes to their isolation, and determines the source of the Hawaiian marine fauna. Hawaii does not lie directly in the path of any current system which might quickly transport larval fishes to the islands. The major the affecting current systems Hawaiian islands are the North Pacific Drift’ and the related Kuroshio extension of the North Pacific Equatorial Current2. These have resulted in an inshore Hawaiian fish fauna whose primary affinity is with the Ryukyu Islands and southern japani,‘. Of four current drogues (buoys designed to be transported by subsurface currents) released off Japan, two were drawn into the Kuroshio Current and reached the northwestern Hawaiian islands4. The transport time, however, was over a year longer than the larval life of most fishes. A third current system, the Subtropical Counter-Current, extends from west to east5. Johnston Island lies within this system and may be a stepping stone for fishes colonizing the Hawaiian archipelago 800 km to the northeastb. Fauna] affinities of Johnston tsland with Hawaii rather than the central Pacific, however, suggest that colonization
Mid=ocean Isolationandthe Evolution of HawaiianReefFishes Thomas F. Hourigan and Ernst S. Reese occurred primarily in the opposite direction’,‘. Wind and current patterns around the Hawaiian islands create a system of cyclonic eddy currents downstream of the archipelago7. These may affect the retention of larvae within the archipelagos - an important factor if evolved adaptations to local conditions are to be retained. One cyclonic eddy remained near the island of Hawaii for almost two months, a sufficient time for pelagic larval development to occur7. Its outer swirl swept over the shallow reefs, capturing the larvae of reef fishes in the periphery of the eddy where they could be returned to the reef. Current drogues released where fish spawn were drawn into the eddy, and some were returned close to shore again7. Speculations on the evolutionary history of fishes in Hawaii based on present conditions must be made with caution. The northwestern Hawaiian islands and the Emperor Seamounts are the sunken remnants of islands which existed along the Hawaiian ridge 27 and 70 million years ago respectivelyg, the maximum period during which colonization and evolution of the fish fauna may have occurred. During the glacial recession of the Pleistocene, changes in climate, sea level and water temperatures caused local extinctions of many coral species5 (see also Jokiel, this issue), and probably affected fishes and other organisms, as well as altering current patterns. Unfortunately, no fossil fishes have been found in HawaiilO. In addition to major climatic changes, intermit-
tent phenomena such as El Nifio may also affect current patterns. Life history patterns of reef fishes Trends in the insular evolution of marine animals, compared to their terrestrial counterparts, reflect fundamental differences in life history. Coral reef fishes have relatively sedentary, long-lived adults and large numbers of offspring which are dispersed as pelagic eggs and/ or larvae (Fig. I). This planktonic dispersal stage has allowed the extensive colonization of the reefs of remote islands, and ensures gene flow within the archipelago and also between Hawaii and other fish populations. Tropical marine fishes typically produce hundreds to hundreds of thousands of externally fertilized zygotes at frequent intervals over a breeding season of many months’ l.12. Most spawn pelagic eggs which are fertilized in the water column and dispersed by currents’ l.13. Other reef fishes, especially of families with small body size, lay smaller clutches of demersal eggs, which are defended by one adult or are brooded in the mouth14. Except for one damselfish which broods its young after hatching, demersal egg layers and mouthbrooders also possess a pelagic larval stage. Larval dispersal may be more restricted in fishes with demersal eggs than in those with pelagic eggs14. This would decrease the chances of their reaching Hawaii, and of genetic exchange with the parent populations once they had arrived. The larvae of fishes with pelagic eggs, such as surgeonfishes
(daily, semilunar or lunar over extended
breeding season) Demersal eggs (25-10 000)
(lifespan, 3-20
years)
t
Pelagic eggs (loo- >I00 000). zygotes leave reef
Sexual maturity (i-5 years)
Eggs hatch
ThomasHouriganand Ernst Reese are at the Dept of Zoology, University of Hawaii, Honolulu, Hawaii 96822,USA
Fig. 1. Life cycle of typical coral reef fishes with demersal
or pelagic eggs.
Male guards eggs (2-6 days) c Eggs hatch, larvae leave reef
TREE vol. 2, no. 7, July
1987
Trends in the evolution of the Hawaiian
inshore fish fauna The location of the Hawaiian archipelago and the life history characteristics of reef fishes interact to produce the following trends in the inshore fish fauna:
( I I Low species diversity Range
1Y
2
6
13
3
Pelagic spawners
B
27
2
Demersal spawners
5
Mouth brooders
Fig. 2. Duration of larval life of fishes of nine Indo-west Pacific coral reef fish families. Data are compiled from analyses of daily increments of otoliths of larvae or newly settled juveniles16J7. Numbers indicate the number of species examined.
(Acanthuridae) and butterflyfishes (Chaetodontidae), are generally found farther offshore in Hawaii than the larvae of fishes with demersal eggs such as blennies (Blenniidae) and gobies (Gobiidae)15. The time and place of spawning may also affect larval dispersa18014. The duration of larval life affects the distance of transport and dispersal. The time spent in the plankton ranges from a few days to several months’2.16.17 (Fig. 2); larvae of certain families, e.g. surgeonfishes, butterflyfishes and moray eels (Muraenidae), appear to be especially adapted for longer pelagic larval life12t15. The life history of pelagic larvae with high dispersal capabilities
188
may be adaptive both to remove larvae from the predator-rich environment of the reefs, and to permit dispersal of the young to either suitable pelagic environments for or suitable reef larval growth’8 habitats for adult survival14. Because of the high unpredictable mortality suffered by larvae, there is selection for high fecundity over time, maximizing the chance that some larvae will successfully return to the reef’*. Most reef fishes breed repeatedly, and most live for several years or longerl’,‘9. Long adult life may also favor adaptation of adults to local habitats, especially in terms of resource use, which increases the chances of producing additional clutches.
The isolation of the islands, enhanced by unfavorable current patterns, has resulted in a depauperate fish fauna. About 680 species of fishes occur in Hawaii*O, compared to 817 in the Marshall Island3 and over 2000 in the Philippines, near the center of radiation of the fndowest Pacific reef fish fauna”. Sea water temperatures are lower than in more equatorial areas, which may prevent some tropical species from colonizing the archipelago*l. Indeed, a few species have disjunct distributions, occurring in Hawaii and in the subtropical areas of the southern hemisphere, but not in the tropics22.23. The longitudinal impoverishment due to distance and current patterns, however, is greater than the latitudinal impoverishment due to temperature gradients’ 1. (2) Idiosyncraticspeciescornposition Certain families are well represented in the inshore fish fauna of Hawaii, whereas others are notably missing or poorly represented. Generally, the former are those families characterized by extended larval life. The duration of the pelagic larval stage of species in Hawaii is significantly longer than the mean for most western and central Pacific fishes17. Species which have highly specialized habitat or dietary requirements may be absent because of the unique biotic environment of Hawaii. The anemone fishes of the genus Ampkiprion have ,not become established in Hawaii, perhaps because the anemones with which these species are symbiotic are also rare or absent. However, this species also has the shortest known larval life of any coral reef fish’*. The distribution of the chevron butterflyfish, Ckaetodon trifuscialis, illustrates the interaction of three factors: ocean currents, larval transport and ecological requirements. This fish is widely distributed throughout the Indo-Pacific, including lohnston Island. It is always
TREE vol. 2, no. 7, July
1987
Table I. Representative families of inshore Hawaiian reef Ashes arranged in descending order of endemism Family (common name)
closely associated with the Acroporu corals on which it feeds’9*24. Neither the coral nor the butterflyfish occurs in the waters of the high Hawaiian islands, and it was believed that they simply had not dispersed successfully to Hawaii. Recently, however, both species were reported from the northwestern Hawaiian islands. Acroporucorals reached this area via the Subtropical Counter-Current, but have not spread because water temperatures are too cold for the coral to reproduce5. Larvae of butterflyfishes are specialized for longdistance dispersal, and juvenile C. trifuscialis have been reported in the high island+. Evidently, they have not become established because the Acruporucorals are absent. The abundance of individuals of species established in Hawaii may be high because of the absence of other members in their trophic guild. Certain herbivores, such as the rabbitfishes (Siganidae), are missing from the Hawaiian fauna. Their absence may be partly responsible for the great abundance of acanthurids, the predominant herbivores on Hawaiian reefs25. The native Hawaiian fish fauna is almost wholly lacking in shallowwater groupers and snappers of the families Serranidae and Lutjanidae2’!22. Between 1955 and I96 I, however, I I species were introduced: ten from the Central Pacific and one from Mexico. Recent introductions provide insights into the evolution of native Hawaiian fishes. First, the number of introduced individuals must be large. Of the I I species, only four were introduced in numbers in excess of 2000 individuals, and three of these became established; only one species, Lutjunus kusmiru, has developed large population+. The chance arrival of a small number of individuals may thus be insufficient for a successful invasion. A few thousand arrivals may be necessary for colonization, and with increasing numbers of new arrivals, the probability of a founder effect occurring decreases. In contrast, much of the speciation which occurs in insular terrestrial environments is thought to occur by founder effects (see other articles in this issue). The availability of food resources may affect the success of introduced species. Although the rela-
Serranidae (groupers) Gobiidae (gobies)” Pomacanthidae (angelfishes) Blenniidae (blennies) Pomacentridae (damselfishes) Scaridae (parrotfishes) Labridae (wrasses) Scorpaenidae (scorpionfishes) Apogonidae (cardinalfishes) Chaetodontidae (butterflyfishes) Muraenidae (moray eels) Acanthuridae (surgeonfishes)d Balistidae (triggerfishes)
Total no. of species
26l& 7
No. of endemic species 9 16112) 4
% Endemism
Spawning mode”
Occurrence of protogynyb
62:s) 57
P D P
C C C
14 14
8 7
57 50
D D
? 0
7 41 26
3 16 9
42 39 35
P P D
C C ?
10
2
20
M,D
?
22
3
14
P
N
35 23
4 0
11 0
P P
? N
0
0
D
N
a
‘Spawning mode: P, pelagic eggs; D, demersal eggs; M, mouth brooder. bProtogyny: C, protogynous hermaphroditism is common in family; 0, protogynous hermaphroditism occurs occasionally in family; N, protogynous hermaphroditism not observed; ?, not known. “There are 4 endemic species of freshwater gobies included in the first figure; they are excluded from the second. dThere is one well known subspecies, Acanthurus triostegus sandvicensis, but endemism at the subspecific level is too controversial to be included in the Table.
tive absence of shallow-water groupers and snappers was interpreted as evidence of the existence of an open or underutilized ‘niche’, this may not be the case. Just as these species are notable by their absence, so moray eels (Muraenidae) are notable by their abundance20. Both groups prey on small benthic invertebrates and other fishes. Thus, in Hawaii, moray eels may be successfully exploiting food resources used by groupers and snappers elsewhere. The introduced snapper, Lutiunus kusmiru, feeds extensively on portunid crabs, a diet which shows little overlap with native fishes in Hawaii2$ this may have facilitated its successful colonization and spread.
tive stream fishes (three gobies and one eleotrid) are endemic, suggesting a greater degree of endemism here than in other habitats; this may reflect greater selective pressure to reduce dispersal and retain adaptive complexes. Adaptation to fresh water did not occur in Hawaii: these species retain a pelagic larval stage and are closely related to other amphidromous gobies in the Indo-west Pacific. The only endemic genus in Hawaii contains a single species, the freshwater goby Lentipes conch-. Most endemic fishes in Hawaii are closely related to Indo-west Pacific species and may be considered sibling species (Table 2). A few endemic species are relics of species with a once wider IndoPacific distribution (e.g. Chuetodon
(3) High endemism at the specieslevel, fremb1ii)20~2’.23. without adaptiveradiation If speciation is dependent on the About 30% of the approximately disruption of gene flow, then fishes 440 inshore fishes in Hawaii are with reduced dispersal should have considered to be endemic at the higher numbers of endemic species species level, with many more in Hawaii. Certain fishes with long showing subspecific variation20r21J3 larval lives, e.g. the pelagic spawn(Table I). This is the highest level ing moray eels and surgeonfishes of endemism in the Indo-west (Fig. 21, do indeed have lower Pacific23 and is similar to the levels of endemism than the de32% endemism reported among mersal spawning damselfishes, Hawaiian marine invertebrates gobies and blennies (Table I), cor(Kay and Palumbi, this issue). It is, responding with the offshore versus however, much lower than the inshore distribution of the larvae of >90% endemism in the native terthese species15. Not all families fit restrial biota27. Four of the five na- this pattern, however: the pelagic 189
TREE vol. 2, no. 7, July 1987 Table2. Common Hawaiian endemicreeffishesandrelatedIndo-Pacific species Family (common name)
Common endemic species
lndo-Pacific sibling species
Chaeotodontidae
Chaetodon miliaris C. multicinctus
C. guntheri C. punctofasciatus
Kuhliidae (flag tails)
Kuhlia sandvicensis
K. marginatus
Labridae (wrasses)
Anampses cuvier Thalassoma duperrey Stethojulis balteata
A. caeruleopunctatus T. lutescens S. bandanensis
Monocanthidae
(butterflyfishes)
(filefishes)
Cantherhines sandwichensis
C. pardalis
Pomacentridae
(damselfishes)
Abudefduf abdominalis Dascyllus albisella
A. saxatilis D. trimaculatus
Tetraodontidae
(puffers)
Canthigaster jactator
C. janthinopterus
spawning angelfishes (Pomacanthidae) have relatively short larval livesI and high levels of endemism, while the demersal spawning triggerfishes (Balistidae) have no Hawaiian endemics (Table 1I. Some pelagic spawners do not have specialized larva1 stages (e.g. groupers, wrasses and parrotfishes)15 and have shorter larva1 lives and higher levels of endemism (Table 1; Fig. 2). Fishes in the eastern Pacific which lay demersal eggs have more restricted distributions and belong to more speciose families than those with pelagic egg+. There is little evidence of interisland variation or adaptive radiation within the Hawaiian archipelago, apparently due to the dispersal capacities of pelagic larvae. The
species : genus ratio is low (2.3 : I for the I3 families in Table I, representing more than 50% of the inshore fishes of Hawaii), not greatly different from that of fishes elsewhere in the PacificlO (3.7 : I, calculated for the same 13 families), but very different from the species : genus ratios of IO : 1 in the Hawaiian terrestrial fauna, which has undergone rapid speciation and radiation27. These patterns suggest that extensive gene flow exists among fish populations within the islands. An electrophoretic study of eight polymorphic loci in the demersal spawning damselfish, Stegastes fasciolatus, collected at sites throughout the Hawaiian archipelago, revealed no evidence of subpopula-
Table3. Abundanceof common Hawaiiin endemic reef fishes by famifyz0,2’J3J5 Family or sub-family
No. of species in Hawaii
Common endemic species Abundance rank in family”
Monocanthinae (filefishes)
6
Acanthurus triostegus (endemic subspecies) Cirripectes obscurus lstiblennius zebra Chaetodon miliaris C. multicinctus C. fremblii Sargocentron xantherythrum Thalassoma duperrey” Stethojulis balteata Pervagor spilosoma
Pomacanthidae (angelfishes) Pomacentridae (damselfishes)
7
Canthigaster sandwichensis Centropyge potteri
23 (surgeonfishes) Blenniidae (blennies)
14
Chaetodontidae (butterflyfishes)
22
Holocentrinae
16
Labridae (wrasses)
41
Scaridae (parrotfishes) Serranidae (groupers) Tetraodontidae (puffers)
14
7 14 10
Chromis hanui C. ova/is Abudefduf abdominalis Scarus dubius S. perspicillatus Anthias thompsoni Canthigaster jactator
l-3
Major habitatb
SCR SCR TP SDR SCR SDR SCR
1 2 1
SCR SCR SCR
2 1
SCR SCR
2-3 3-4 4-5 1 2-3 1 1
SCR SCR SCR SCR SCR DR SCR
“Abundance rank of 1 signifies that the species is the most abundant species of its family in Hawaii. More than one abundance ranking signifies uncertainty or differences among authors. bSCR, shallow coral reefs; TP, tide pools; SDR, shallow and deep reefs; DR, deep reefs. ‘Thalassoma duperrey is the most abundant species of any fish occurring on shallow coral reefs in HawaiV.
190
tion differentiation29. Electrophoretic variation was also studied in milkfish, Chanos chanos, from the islands of Oahu and Hawaii, as well as other sites in the Pacific30. As expected from geographic isolation, the Hawaiian samples showed the greatest divergence from other Pacific samples, as well as some loss of variation at polymorphic loci. There were also, however, significant differences at four loci between fish from the two Hawaiian islands. (4) Local adaptation and the abundance of endemic fishes Many endemic species are the most abundant Hawaiian fishes in their families (Table 3). This trend also occurs in other isolated insular faunas, such as those at Lord Howe Island and Easter Island23. The reasons for differential abundances of species in any ecological community are not well understood, but one may speculate that these species reached the islands earlier than less abundant species, or that some degree of local adaptation has occurred which is responsible for their success. The simplest form of adaptation may involve mechanisms for retention of the larvae within the archipelago. There is evidence that spawning of certain Hawaiian reef fishes is timed to coincide with the season of maximal occurrence of gyres7, I I r3I If the larvae of fish which spawn at other times are likely to be lost, there would be strong selective pressure for local adaptation in spawning season. This in turn would aid the retention of other adaptive complexes, providing a parallel to the reduced dispersal capabilities of terrestrial island organisms. Local adaptation to underutilized food resources may also have occurred. The planktivore assemblage in Hawaii is depauperate, lacking many species which occur on other Indo-west Pacific reefs (e.g. caesionids, shallow-water anthiines, and certain damselfishes). Butterflyfishes of the genus Chaetodon are typically demersal coral feeders, specializing on invertetissue, algae and brateG4.25J*,33. Chaetodon miiiaris, a Hawaiian endemic, is unusual in primarily on that it feeds zooplankton*4~25J4. This change in
TREE vol. 2, no. 7, July
1987
diet is accompanied by morphological adaptations of the feeding apparatus24, and changes from the typical chaetodontid social behavior of pair bonding32, to schooling and group spawning34. Chaetodon miliaris is the most abundant butterflyfish in the Hawaiian islands, and the most abundant fish of any species in depths of 60-I 20 m. This success may be due in part to its adaptation to a locally abundant resource - zooplankton34. These observations suggest that some dietary shifts among fishes may have been due to the absence of interspecific competitors. However, the occurrence and effects of competition in reef fish assemblages are controversial”, and attributing adaptations to an escape from competition is speculative. Shifts to planktivory may occur more easily than other dietary shifts, since most marine fishes are planktivorous as larvae and planktivory may be retained initially as a neotonous condition after metamorphosis.
Future studies Reef fishes form the most speciose and diverse of vertebrate assemblages, but our current knowledge of their speciation is limited. The inshore fish fauna of the Hawaiian islands presents a case study of evolution in the marine environment. Further research in the following areas would be especially valuable: (I) The means by which small scale physical oceanographic phenomena affect the dispersal of eggs and larvae (e.g. Ref. 7). (21 The factors which determine the time spent by larvae in the plankton, and the extent to which larval behavior may affect dispersal. (3) The effects of interspecific competition on the differential abundance of reef fishes, the invasibility of a community and dietary shifts by fishes in the absence of competitors. (4) The genetic structure of marine fish populations; mitochondrial DNA sequencing techniques may determine the extent of gene flow among populations within and between island groups, and these data can then be compared to current patterns, the geographic separation of populations, and life history characteristics.
Finally, the great diversity of life history patterns among reef fishes offers a unique opportunity to test the interactions of life history traits and speciation. The possible relationship between demersal or pelagic spawning, timing of spawning and length of larval life and levels of endemism has already been noted, and at least one other correlation looks promising: strong sexual selection may favor reproductive isolation and speciation35 (see also Boake and Kaneshiro, this issue). Protogynous hermaphroditism (sex change from female to male) is associated with high levels of sexual selection and is very common, often ubiquitous, among those families which show the highest levels of endemism in Hawaii (Table 1). Further investigation of all these areas should allow their integration into models of speciation. Acknowledgements We would like to thank J. Randall, 8. Carlson, C. Simon, P. Sale, L. Freed, W. Baldwin, T. Telecky and W. Tyler for their comments and assistance with this review.
References
1 Hobson, E.S. ( 1980) in Proceedings of the Symposium on the Status of Resource Investigations in the Northwestern Hawaiian Islands (Grigg, R.W. and Pfund, R.. eds), pp. 57-70, UNIHISEAGRANT-MR-80-04 2 Zinmeister, W.I. and Emmerson, W.K. 11979) Veliger 22,32-40 3 Randall, I.E., Lobel. P.S. and Chave. E.H. (1985) Pac. Sci. 39,24-80 4 McNally, G.1.. Patzert, W.C., Kirwin, A.D., fr and Vastano, AC. (19831 J. Geophys. Res. 88, 7507-7518 5 Grigg, R.W. ( 1981) Pac. Sci. 35, 15-24 6 Gosline, W.A. (1955) Pac. Sci. 9,442-480 7 Lobel, P.S. and Robinson, A.R. f 1986) Deep-
Sea Res. 33,483-500 8 johannes, R.E. (19781 Environ. Biof. Fish. 3. 65-84 9 Dalrymple, G.C., Silver, E.A. and Jackson, E.D. ( 1973) Am. Sri. 61, 294-308 IO Springer, V.G. (19821 Smithson. Contrib. Zoof. 367. I-182 II Sale, P.F. (1980) Oceanogr. Mar. Biol. Annu. Rev. 18, 367-42 I. I2 Thresher, R.E. ( 19841 Reproduction in Reef Fishes, TFH Publications I3 Ehrlich, P.R. 11975) Annu. Rev. Etol. Syst. 6, 2 I l-248 I4 Barlow, C.W. (I981 ) Environ. Biol. Fish. 6, 65-85 I5 Leis, I.M. and Miller, I.M. 11976) Mar. Biol. 36,359-367 I6 Brothers, E.B., Williams. D.McB. and Sale. P.F. (19831 Mar. Biof. 76,319-324 I7 Brothers, E.B. and Thresher, R.E. (1985) in The Ecology o/Coral Reefs (Symp. Ser. Undersea Res. 31 (Reaka.M.L.,ed.t,pp. 53-69, NOAA 18 Doherty, PJ., Williams, D.McB. and Sale, P.F. If9851 Environ. Bio/. Fish. i2,81-90 I9 Reese, ES. ( 1981 I Bull. Mar. Sci. 3 I, 594604 20 Randall, R.E. ( 1985) Guide to Hawaiian Reef Fishes, Harrowood 21 Gosline, W.A. and Brock, V.E. I 1960) HandGooR of Hawaiian Fishes, University of Hawaii Press 22 Randall, I.E. II9821 Pac. Sti. 35, 197-209 1973 23 Randall, J.E. 11976) Colloque Commerson ORSTOM (Travaux et Documents No, 47) 24 Motta, P.J. (1985) Environ. Biof. Fish. 13. 253-276 25 Hobson, ES. t 19741 Fish. Bull. 72,915-1031 26 Oda, D.K. and Parrish, I.D. (I981 I Proc. 4th Int. Coral Reef Symp. I, 59-67 27 Zimmermann, E.C. ( 19481 Insects of Hawaii (Vol. I I, University of Hawaii Press 28 Rosenblatt, R.H. (19671 Stud. Trop. Oceanogr. 5, 579-592 29 Shaklee, 1.B. ( 19841 Copeia 3,629-640 30 Winans, G.A. i 19801 Evolution 34,558-574 31 Walsh, W. Environ. Biol. Fish. (in press) 32 Reese, ES. (19751 Z. Tierpsychol. 37,37-61 33 Hourigan, T.F., Tricas, T.C. and Reese, ES. in Marine Organisms as Indicators (Souie, D.F. and Kleppel, G.P., edsl, Springer-Verlag (in press) 34 Ralston, S. ( 1981 I Eflviron. Biol. Fish. 6, 167-176 35 West-Eberhard, 155-183
M.J. (I9831 0. Rev. Biol. 58,
1987
The Hawaiian fish fauna has close afinities with the fauna of the Indo-west Pacific from which it is derived, but is depauperate. It is characterized by a large number of endemic species (30% of inshore fishes), which are often the most a6undant species in their families in Hawaii. Alfhough there is evidence of focal adaptation, there has been no radiation of species within the island chain, as occurs in the terrestrial biota of isolated islands. Three major factors have contributed to these trends: (I ) the geographic isolation of the islands, and oceanographic features, especially current patterns; (2 1the life history characteristics of the fishes, especially their dispersal cupabilities; and (3 1 the extent of aduptive differentiation to environmental conditions after they reached Hawaii.
The Hawaiian archipelago is among the most isolated island groups in the world. The location of the islands with respect to Pacific current patterns contributes to their isolation, and determines the source of the Hawaiian marine fauna. Hawaii does not lie directly in the path of any current system which might quickly transport larval fishes to the islands. The major the affecting current systems Hawaiian islands are the North Pacific Drift’ and the related Kuroshio extension of the North Pacific Equatorial Current2. These have resulted in an inshore Hawaiian fish fauna whose primary affinity is with the Ryukyu Islands and southern japani,‘. Of four current drogues (buoys designed to be transported by subsurface currents) released off Japan, two were drawn into the Kuroshio Current and reached the northwestern Hawaiian islands4. The transport time, however, was over a year longer than the larval life of most fishes. A third current system, the Subtropical Counter-Current, extends from west to east5. Johnston Island lies within this system and may be a stepping stone for fishes colonizing the Hawaiian archipelago 800 km to the northeastb. Fauna] affinities of Johnston tsland with Hawaii rather than the central Pacific, however, suggest that colonization
Mid=ocean Isolationandthe Evolution of HawaiianReefFishes Thomas F. Hourigan and Ernst S. Reese occurred primarily in the opposite direction’,‘. Wind and current patterns around the Hawaiian islands create a system of cyclonic eddy currents downstream of the archipelago7. These may affect the retention of larvae within the archipelagos - an important factor if evolved adaptations to local conditions are to be retained. One cyclonic eddy remained near the island of Hawaii for almost two months, a sufficient time for pelagic larval development to occur7. Its outer swirl swept over the shallow reefs, capturing the larvae of reef fishes in the periphery of the eddy where they could be returned to the reef. Current drogues released where fish spawn were drawn into the eddy, and some were returned close to shore again7. Speculations on the evolutionary history of fishes in Hawaii based on present conditions must be made with caution. The northwestern Hawaiian islands and the Emperor Seamounts are the sunken remnants of islands which existed along the Hawaiian ridge 27 and 70 million years ago respectivelyg, the maximum period during which colonization and evolution of the fish fauna may have occurred. During the glacial recession of the Pleistocene, changes in climate, sea level and water temperatures caused local extinctions of many coral species5 (see also Jokiel, this issue), and probably affected fishes and other organisms, as well as altering current patterns. Unfortunately, no fossil fishes have been found in HawaiilO. In addition to major climatic changes, intermit-
tent phenomena such as El Nifio may also affect current patterns. Life history patterns of reef fishes Trends in the insular evolution of marine animals, compared to their terrestrial counterparts, reflect fundamental differences in life history. Coral reef fishes have relatively sedentary, long-lived adults and large numbers of offspring which are dispersed as pelagic eggs and/ or larvae (Fig. I). This planktonic dispersal stage has allowed the extensive colonization of the reefs of remote islands, and ensures gene flow within the archipelago and also between Hawaii and other fish populations. Tropical marine fishes typically produce hundreds to hundreds of thousands of externally fertilized zygotes at frequent intervals over a breeding season of many months’ l.12. Most spawn pelagic eggs which are fertilized in the water column and dispersed by currents’ l.13. Other reef fishes, especially of families with small body size, lay smaller clutches of demersal eggs, which are defended by one adult or are brooded in the mouth14. Except for one damselfish which broods its young after hatching, demersal egg layers and mouthbrooders also possess a pelagic larval stage. Larval dispersal may be more restricted in fishes with demersal eggs than in those with pelagic eggs14. This would decrease the chances of their reaching Hawaii, and of genetic exchange with the parent populations once they had arrived. The larvae of fishes with pelagic eggs, such as surgeonfishes
(daily, semilunar or lunar over extended
breeding season) Demersal eggs (25-10 000)
(lifespan, 3-20
years)
t
Pelagic eggs (loo- >I00 000). zygotes leave reef
Sexual maturity (i-5 years)
Eggs hatch
ThomasHouriganand Ernst Reese are at the Dept of Zoology, University of Hawaii, Honolulu, Hawaii 96822,USA
Fig. 1. Life cycle of typical coral reef fishes with demersal
or pelagic eggs.
Male guards eggs (2-6 days) c Eggs hatch, larvae leave reef
TREE vol. 2, no. 7, July
1987
Trends in the evolution of the Hawaiian
inshore fish fauna The location of the Hawaiian archipelago and the life history characteristics of reef fishes interact to produce the following trends in the inshore fish fauna:
( I I Low species diversity Range
1Y
2
6
13
3
Pelagic spawners
B
27
2
Demersal spawners
5
Mouth brooders
Fig. 2. Duration of larval life of fishes of nine Indo-west Pacific coral reef fish families. Data are compiled from analyses of daily increments of otoliths of larvae or newly settled juveniles16J7. Numbers indicate the number of species examined.
(Acanthuridae) and butterflyfishes (Chaetodontidae), are generally found farther offshore in Hawaii than the larvae of fishes with demersal eggs such as blennies (Blenniidae) and gobies (Gobiidae)15. The time and place of spawning may also affect larval dispersa18014. The duration of larval life affects the distance of transport and dispersal. The time spent in the plankton ranges from a few days to several months’2.16.17 (Fig. 2); larvae of certain families, e.g. surgeonfishes, butterflyfishes and moray eels (Muraenidae), appear to be especially adapted for longer pelagic larval life12t15. The life history of pelagic larvae with high dispersal capabilities
188
may be adaptive both to remove larvae from the predator-rich environment of the reefs, and to permit dispersal of the young to either suitable pelagic environments for or suitable reef larval growth’8 habitats for adult survival14. Because of the high unpredictable mortality suffered by larvae, there is selection for high fecundity over time, maximizing the chance that some larvae will successfully return to the reef’*. Most reef fishes breed repeatedly, and most live for several years or longerl’,‘9. Long adult life may also favor adaptation of adults to local habitats, especially in terms of resource use, which increases the chances of producing additional clutches.
The isolation of the islands, enhanced by unfavorable current patterns, has resulted in a depauperate fish fauna. About 680 species of fishes occur in Hawaii*O, compared to 817 in the Marshall Island3 and over 2000 in the Philippines, near the center of radiation of the fndowest Pacific reef fish fauna”. Sea water temperatures are lower than in more equatorial areas, which may prevent some tropical species from colonizing the archipelago*l. Indeed, a few species have disjunct distributions, occurring in Hawaii and in the subtropical areas of the southern hemisphere, but not in the tropics22.23. The longitudinal impoverishment due to distance and current patterns, however, is greater than the latitudinal impoverishment due to temperature gradients’ 1. (2) Idiosyncraticspeciescornposition Certain families are well represented in the inshore fish fauna of Hawaii, whereas others are notably missing or poorly represented. Generally, the former are those families characterized by extended larval life. The duration of the pelagic larval stage of species in Hawaii is significantly longer than the mean for most western and central Pacific fishes17. Species which have highly specialized habitat or dietary requirements may be absent because of the unique biotic environment of Hawaii. The anemone fishes of the genus Ampkiprion have ,not become established in Hawaii, perhaps because the anemones with which these species are symbiotic are also rare or absent. However, this species also has the shortest known larval life of any coral reef fish’*. The distribution of the chevron butterflyfish, Ckaetodon trifuscialis, illustrates the interaction of three factors: ocean currents, larval transport and ecological requirements. This fish is widely distributed throughout the Indo-Pacific, including lohnston Island. It is always
TREE vol. 2, no. 7, July
1987
Table I. Representative families of inshore Hawaiian reef Ashes arranged in descending order of endemism Family (common name)
closely associated with the Acroporu corals on which it feeds’9*24. Neither the coral nor the butterflyfish occurs in the waters of the high Hawaiian islands, and it was believed that they simply had not dispersed successfully to Hawaii. Recently, however, both species were reported from the northwestern Hawaiian islands. Acroporucorals reached this area via the Subtropical Counter-Current, but have not spread because water temperatures are too cold for the coral to reproduce5. Larvae of butterflyfishes are specialized for longdistance dispersal, and juvenile C. trifuscialis have been reported in the high island+. Evidently, they have not become established because the Acruporucorals are absent. The abundance of individuals of species established in Hawaii may be high because of the absence of other members in their trophic guild. Certain herbivores, such as the rabbitfishes (Siganidae), are missing from the Hawaiian fauna. Their absence may be partly responsible for the great abundance of acanthurids, the predominant herbivores on Hawaiian reefs25. The native Hawaiian fish fauna is almost wholly lacking in shallowwater groupers and snappers of the families Serranidae and Lutjanidae2’!22. Between 1955 and I96 I, however, I I species were introduced: ten from the Central Pacific and one from Mexico. Recent introductions provide insights into the evolution of native Hawaiian fishes. First, the number of introduced individuals must be large. Of the I I species, only four were introduced in numbers in excess of 2000 individuals, and three of these became established; only one species, Lutjunus kusmiru, has developed large population+. The chance arrival of a small number of individuals may thus be insufficient for a successful invasion. A few thousand arrivals may be necessary for colonization, and with increasing numbers of new arrivals, the probability of a founder effect occurring decreases. In contrast, much of the speciation which occurs in insular terrestrial environments is thought to occur by founder effects (see other articles in this issue). The availability of food resources may affect the success of introduced species. Although the rela-
Serranidae (groupers) Gobiidae (gobies)” Pomacanthidae (angelfishes) Blenniidae (blennies) Pomacentridae (damselfishes) Scaridae (parrotfishes) Labridae (wrasses) Scorpaenidae (scorpionfishes) Apogonidae (cardinalfishes) Chaetodontidae (butterflyfishes) Muraenidae (moray eels) Acanthuridae (surgeonfishes)d Balistidae (triggerfishes)
Total no. of species
26l& 7
No. of endemic species 9 16112) 4
% Endemism
Spawning mode”
Occurrence of protogynyb
62:s) 57
P D P
C C C
14 14
8 7
57 50
D D
? 0
7 41 26
3 16 9
42 39 35
P P D
C C ?
10
2
20
M,D
?
22
3
14
P
N
35 23
4 0
11 0
P P
? N
0
0
D
N
a
‘Spawning mode: P, pelagic eggs; D, demersal eggs; M, mouth brooder. bProtogyny: C, protogynous hermaphroditism is common in family; 0, protogynous hermaphroditism occurs occasionally in family; N, protogynous hermaphroditism not observed; ?, not known. “There are 4 endemic species of freshwater gobies included in the first figure; they are excluded from the second. dThere is one well known subspecies, Acanthurus triostegus sandvicensis, but endemism at the subspecific level is too controversial to be included in the Table.
tive absence of shallow-water groupers and snappers was interpreted as evidence of the existence of an open or underutilized ‘niche’, this may not be the case. Just as these species are notable by their absence, so moray eels (Muraenidae) are notable by their abundance20. Both groups prey on small benthic invertebrates and other fishes. Thus, in Hawaii, moray eels may be successfully exploiting food resources used by groupers and snappers elsewhere. The introduced snapper, Lutiunus kusmiru, feeds extensively on portunid crabs, a diet which shows little overlap with native fishes in Hawaii2$ this may have facilitated its successful colonization and spread.
tive stream fishes (three gobies and one eleotrid) are endemic, suggesting a greater degree of endemism here than in other habitats; this may reflect greater selective pressure to reduce dispersal and retain adaptive complexes. Adaptation to fresh water did not occur in Hawaii: these species retain a pelagic larval stage and are closely related to other amphidromous gobies in the Indo-west Pacific. The only endemic genus in Hawaii contains a single species, the freshwater goby Lentipes conch-. Most endemic fishes in Hawaii are closely related to Indo-west Pacific species and may be considered sibling species (Table 2). A few endemic species are relics of species with a once wider IndoPacific distribution (e.g. Chuetodon
(3) High endemism at the specieslevel, fremb1ii)20~2’.23. without adaptiveradiation If speciation is dependent on the About 30% of the approximately disruption of gene flow, then fishes 440 inshore fishes in Hawaii are with reduced dispersal should have considered to be endemic at the higher numbers of endemic species species level, with many more in Hawaii. Certain fishes with long showing subspecific variation20r21J3 larval lives, e.g. the pelagic spawn(Table I). This is the highest level ing moray eels and surgeonfishes of endemism in the Indo-west (Fig. 21, do indeed have lower Pacific23 and is similar to the levels of endemism than the de32% endemism reported among mersal spawning damselfishes, Hawaiian marine invertebrates gobies and blennies (Table I), cor(Kay and Palumbi, this issue). It is, responding with the offshore versus however, much lower than the inshore distribution of the larvae of >90% endemism in the native terthese species15. Not all families fit restrial biota27. Four of the five na- this pattern, however: the pelagic 189
TREE vol. 2, no. 7, July 1987 Table2. Common Hawaiian endemicreeffishesandrelatedIndo-Pacific species Family (common name)
Common endemic species
lndo-Pacific sibling species
Chaeotodontidae
Chaetodon miliaris C. multicinctus
C. guntheri C. punctofasciatus
Kuhliidae (flag tails)
Kuhlia sandvicensis
K. marginatus
Labridae (wrasses)
Anampses cuvier Thalassoma duperrey Stethojulis balteata
A. caeruleopunctatus T. lutescens S. bandanensis
Monocanthidae
(butterflyfishes)
(filefishes)
Cantherhines sandwichensis
C. pardalis
Pomacentridae
(damselfishes)
Abudefduf abdominalis Dascyllus albisella
A. saxatilis D. trimaculatus
Tetraodontidae
(puffers)
Canthigaster jactator
C. janthinopterus
spawning angelfishes (Pomacanthidae) have relatively short larval livesI and high levels of endemism, while the demersal spawning triggerfishes (Balistidae) have no Hawaiian endemics (Table 1I. Some pelagic spawners do not have specialized larva1 stages (e.g. groupers, wrasses and parrotfishes)15 and have shorter larva1 lives and higher levels of endemism (Table 1; Fig. 2). Fishes in the eastern Pacific which lay demersal eggs have more restricted distributions and belong to more speciose families than those with pelagic egg+. There is little evidence of interisland variation or adaptive radiation within the Hawaiian archipelago, apparently due to the dispersal capacities of pelagic larvae. The
species : genus ratio is low (2.3 : I for the I3 families in Table I, representing more than 50% of the inshore fishes of Hawaii), not greatly different from that of fishes elsewhere in the PacificlO (3.7 : I, calculated for the same 13 families), but very different from the species : genus ratios of IO : 1 in the Hawaiian terrestrial fauna, which has undergone rapid speciation and radiation27. These patterns suggest that extensive gene flow exists among fish populations within the islands. An electrophoretic study of eight polymorphic loci in the demersal spawning damselfish, Stegastes fasciolatus, collected at sites throughout the Hawaiian archipelago, revealed no evidence of subpopula-
Table3. Abundanceof common Hawaiiin endemic reef fishes by famifyz0,2’J3J5 Family or sub-family
No. of species in Hawaii
Common endemic species Abundance rank in family”
Monocanthinae (filefishes)
6
Acanthurus triostegus (endemic subspecies) Cirripectes obscurus lstiblennius zebra Chaetodon miliaris C. multicinctus C. fremblii Sargocentron xantherythrum Thalassoma duperrey” Stethojulis balteata Pervagor spilosoma
Pomacanthidae (angelfishes) Pomacentridae (damselfishes)
7
Canthigaster sandwichensis Centropyge potteri
23 (surgeonfishes) Blenniidae (blennies)
14
Chaetodontidae (butterflyfishes)
22
Holocentrinae
16
Labridae (wrasses)
41
Scaridae (parrotfishes) Serranidae (groupers) Tetraodontidae (puffers)
14
7 14 10
Chromis hanui C. ova/is Abudefduf abdominalis Scarus dubius S. perspicillatus Anthias thompsoni Canthigaster jactator
l-3
Major habitatb
SCR SCR TP SDR SCR SDR SCR
1 2 1
SCR SCR SCR
2 1
SCR SCR
2-3 3-4 4-5 1 2-3 1 1
SCR SCR SCR SCR SCR DR SCR
“Abundance rank of 1 signifies that the species is the most abundant species of its family in Hawaii. More than one abundance ranking signifies uncertainty or differences among authors. bSCR, shallow coral reefs; TP, tide pools; SDR, shallow and deep reefs; DR, deep reefs. ‘Thalassoma duperrey is the most abundant species of any fish occurring on shallow coral reefs in HawaiV.
190
tion differentiation29. Electrophoretic variation was also studied in milkfish, Chanos chanos, from the islands of Oahu and Hawaii, as well as other sites in the Pacific30. As expected from geographic isolation, the Hawaiian samples showed the greatest divergence from other Pacific samples, as well as some loss of variation at polymorphic loci. There were also, however, significant differences at four loci between fish from the two Hawaiian islands. (4) Local adaptation and the abundance of endemic fishes Many endemic species are the most abundant Hawaiian fishes in their families (Table 3). This trend also occurs in other isolated insular faunas, such as those at Lord Howe Island and Easter Island23. The reasons for differential abundances of species in any ecological community are not well understood, but one may speculate that these species reached the islands earlier than less abundant species, or that some degree of local adaptation has occurred which is responsible for their success. The simplest form of adaptation may involve mechanisms for retention of the larvae within the archipelago. There is evidence that spawning of certain Hawaiian reef fishes is timed to coincide with the season of maximal occurrence of gyres7, I I r3I If the larvae of fish which spawn at other times are likely to be lost, there would be strong selective pressure for local adaptation in spawning season. This in turn would aid the retention of other adaptive complexes, providing a parallel to the reduced dispersal capabilities of terrestrial island organisms. Local adaptation to underutilized food resources may also have occurred. The planktivore assemblage in Hawaii is depauperate, lacking many species which occur on other Indo-west Pacific reefs (e.g. caesionids, shallow-water anthiines, and certain damselfishes). Butterflyfishes of the genus Chaetodon are typically demersal coral feeders, specializing on invertetissue, algae and brateG4.25J*,33. Chaetodon miiiaris, a Hawaiian endemic, is unusual in primarily on that it feeds zooplankton*4~25J4. This change in
TREE vol. 2, no. 7, July
1987
diet is accompanied by morphological adaptations of the feeding apparatus24, and changes from the typical chaetodontid social behavior of pair bonding32, to schooling and group spawning34. Chaetodon miliaris is the most abundant butterflyfish in the Hawaiian islands, and the most abundant fish of any species in depths of 60-I 20 m. This success may be due in part to its adaptation to a locally abundant resource - zooplankton34. These observations suggest that some dietary shifts among fishes may have been due to the absence of interspecific competitors. However, the occurrence and effects of competition in reef fish assemblages are controversial”, and attributing adaptations to an escape from competition is speculative. Shifts to planktivory may occur more easily than other dietary shifts, since most marine fishes are planktivorous as larvae and planktivory may be retained initially as a neotonous condition after metamorphosis.
Future studies Reef fishes form the most speciose and diverse of vertebrate assemblages, but our current knowledge of their speciation is limited. The inshore fish fauna of the Hawaiian islands presents a case study of evolution in the marine environment. Further research in the following areas would be especially valuable: (I) The means by which small scale physical oceanographic phenomena affect the dispersal of eggs and larvae (e.g. Ref. 7). (21 The factors which determine the time spent by larvae in the plankton, and the extent to which larval behavior may affect dispersal. (3) The effects of interspecific competition on the differential abundance of reef fishes, the invasibility of a community and dietary shifts by fishes in the absence of competitors. (4) The genetic structure of marine fish populations; mitochondrial DNA sequencing techniques may determine the extent of gene flow among populations within and between island groups, and these data can then be compared to current patterns, the geographic separation of populations, and life history characteristics.
Finally, the great diversity of life history patterns among reef fishes offers a unique opportunity to test the interactions of life history traits and speciation. The possible relationship between demersal or pelagic spawning, timing of spawning and length of larval life and levels of endemism has already been noted, and at least one other correlation looks promising: strong sexual selection may favor reproductive isolation and speciation35 (see also Boake and Kaneshiro, this issue). Protogynous hermaphroditism (sex change from female to male) is associated with high levels of sexual selection and is very common, often ubiquitous, among those families which show the highest levels of endemism in Hawaii (Table 1). Further investigation of all these areas should allow their integration into models of speciation. Acknowledgements We would like to thank J. Randall, 8. Carlson, C. Simon, P. Sale, L. Freed, W. Baldwin, T. Telecky and W. Tyler for their comments and assistance with this review.
References
1 Hobson, E.S. ( 1980) in Proceedings of the Symposium on the Status of Resource Investigations in the Northwestern Hawaiian Islands (Grigg, R.W. and Pfund, R.. eds), pp. 57-70, UNIHISEAGRANT-MR-80-04 2 Zinmeister, W.I. and Emmerson, W.K. 11979) Veliger 22,32-40 3 Randall, I.E., Lobel. P.S. and Chave. E.H. (1985) Pac. Sci. 39,24-80 4 McNally, G.1.. Patzert, W.C., Kirwin, A.D., fr and Vastano, AC. (19831 J. Geophys. Res. 88, 7507-7518 5 Grigg, R.W. ( 1981) Pac. Sci. 35, 15-24 6 Gosline, W.A. (1955) Pac. Sci. 9,442-480 7 Lobel, P.S. and Robinson, A.R. f 1986) Deep-
Sea Res. 33,483-500 8 johannes, R.E. (19781 Environ. Biof. Fish. 3. 65-84 9 Dalrymple, G.C., Silver, E.A. and Jackson, E.D. ( 1973) Am. Sri. 61, 294-308 IO Springer, V.G. (19821 Smithson. Contrib. Zoof. 367. I-182 II Sale, P.F. (1980) Oceanogr. Mar. Biol. Annu. Rev. 18, 367-42 I. I2 Thresher, R.E. ( 19841 Reproduction in Reef Fishes, TFH Publications I3 Ehrlich, P.R. 11975) Annu. Rev. Etol. Syst. 6, 2 I l-248 I4 Barlow, C.W. (I981 ) Environ. Biol. Fish. 6, 65-85 I5 Leis, I.M. and Miller, I.M. 11976) Mar. Biol. 36,359-367 I6 Brothers, E.B., Williams. D.McB. and Sale. P.F. (19831 Mar. Biof. 76,319-324 I7 Brothers, E.B. and Thresher, R.E. (1985) in The Ecology o/Coral Reefs (Symp. Ser. Undersea Res. 31 (Reaka.M.L.,ed.t,pp. 53-69, NOAA 18 Doherty, PJ., Williams, D.McB. and Sale, P.F. If9851 Environ. Bio/. Fish. i2,81-90 I9 Reese, ES. ( 1981 I Bull. Mar. Sci. 3 I, 594604 20 Randall, R.E. ( 1985) Guide to Hawaiian Reef Fishes, Harrowood 21 Gosline, W.A. and Brock, V.E. I 1960) HandGooR of Hawaiian Fishes, University of Hawaii Press 22 Randall, I.E. II9821 Pac. Sti. 35, 197-209 1973 23 Randall, J.E. 11976) Colloque Commerson ORSTOM (Travaux et Documents No, 47) 24 Motta, P.J. (1985) Environ. Biof. Fish. 13. 253-276 25 Hobson, ES. t 19741 Fish. Bull. 72,915-1031 26 Oda, D.K. and Parrish, I.D. (I981 I Proc. 4th Int. Coral Reef Symp. I, 59-67 27 Zimmermann, E.C. ( 19481 Insects of Hawaii (Vol. I I, University of Hawaii Press 28 Rosenblatt, R.H. (19671 Stud. Trop. Oceanogr. 5, 579-592 29 Shaklee, 1.B. ( 19841 Copeia 3,629-640 30 Winans, G.A. i 19801 Evolution 34,558-574 31 Walsh, W. Environ. Biol. Fish. (in press) 32 Reese, ES. (19751 Z. Tierpsychol. 37,37-61 33 Hourigan, T.F., Tricas, T.C. and Reese, ES. in Marine Organisms as Indicators (Souie, D.F. and Kleppel, G.P., edsl, Springer-Verlag (in press) 34 Ralston, S. ( 1981 I Eflviron. Biol. Fish. 6, 167-176 35 West-Eberhard, 155-183
M.J. (I9831 0. Rev. Biol. 58,