TREE vol. 2, no. 7, July 1987

Charles Darwin offered a standing reward of 50 pounds to any collec- tor who would work in the Hawaiian islands’ His enticement would cer- tainly have been larger had he known what we know today. The biota of the Hawaiian islands in- cludes some 1000 species of flower- ing plants, 2000 lower plants, 7000- 8000 insects, IO00 land snails, 1500 marine mollusks, IOU+ birds, 680 fish, three sea turtles, one bat and one seal. Many of these species are found nowhere else in the world and exhibit traits uncharacteristic of their respective taxa.

Hawaiian Evolutionary Biology: An Introduction

Chris Simon the world, lying 4000 km from the nearest major land mass and 1600 km from the nearest island groups. Individual islands possess habitats ranging from below sea level to 4205 m, and have some of the most dramatic rainfall gradients in the world. Here we find everything from arid lowland forests to high eleva- tion swamps, rocky intertidal areas to deep ocean trenches. Even in one locality, a single mature rain forest tree can encompass a range of habitats: from the epiphytic com- munity of the trunk and canopy to the troglobiontic organisms living among the roots which penetrate lava tube caves.

come seamounts. North of Midway Island, about 3000 km northeast of the island of Hawaii, the chain bends sharply to the north and continues as the Emperor Sea- mounts. Fifteen hundred miles farther north, these seamounts are sequentially subducted into the Kuril-Kamchatka Trench’. The centrepage map illustrates these features. Evolutionary studies of these

novel Hawaiian taxa, many under the auspices of the Hawaiian Evolu- tionary Biology Program, have been instrumental in developing modern theories of speciation and dif- ferentiation. For this reason it is particularly fitting that the Hawaiian islands have been chosen as the subject for the first anniversary issue of this journal. The review articles collected here explore areas of active research in Hawaiian ecology and evolutionary biology. Research to date has been produc- tive and promises significant future rewards. This introduction sets the stage by presenting a sketch of pertinent eco-geological features, constructing a unifying framework, and adding information about less well studied groups not reviewed here.

The Hawaiian archipelago Three characteristics make the

Hawaiian archipelago an exception- al natural laboratory for the study of evolutionary biology: I I) the is- lands are arranged linearly in chro- nological order and are of known ages; (21 there is a large number of endemic species, many of which are numerically dominant and dis- play characteristics unlike those of related taxa; and (3) evolutionary phenomena characteristic of other ‘island’ environments, such as adaptive shifts, loss of dispersal ability, arborescence, etc., are developed to an extraordinary de- gree. The first characteristic is re- lated to the geological formation of the islands; the latter two result from extremes of isolation and habitat diversity.

The Hawaiian archipelago is the most isolated major archipelago in

Chris Simon is at the Dept ot Zoology and the Dept of General Science, UniversEv of Hawaii at Manoa. Honolulu. Hawaii 9b8?7. US4

The linear arrangement of the Hawaiian chain results from the se- quential formation of islands as the Pacific tectonic plate moves north- westward over a volcanic hot spot. The island of Hawaii, which is less than half a million years old and still over the hot spot, includes the active volcanoes of Mauna Loa and Kilauea. A new seamount, Loihi, discovered in the 1950s is forming to the south of the island of Hawaii’,?.

To the northwest of Hawaii island lie four islands - Maui, Molokai, Lanai and Kahoolawe - situated on a common platform. These islands were almost certainly connected during times of lowered sea level; because of this, they function biogeographically as one unit for the more vagile taxa. Oahu (with approximately 80% of the state’s human population) lies to the northwest of the deep Molokai channel, followed by Kauai and Niihau. The two northernmost high islands are approximately five mil- lion years old. The sharp knife- edged ridges of the highly eroded older islands are a dramatic con- trast to the low-sloping domes of the volcanoes of the island of Hawaii3.

To the northwest of the eight major high islands the chain con- tinues with a string of lower islands, atolls, reefs and shoals. Ail of these are of volcanic origin with various degrees of coralline additions (see lokiel, this issue). As the chain progresses northwestward, the is- lands and atolls submerge to be-

This conveyor belt-like progres- sion of islands raises the possibility that islands now eroded and sunk- en could have at one time sup- ported life and provided colonists for newly arising islands to the southeast. If this is true, the age of Kauai and Niihau might not be the maximum age of Hawaiian spe- cies*. Studies designed to answer this question are only just begin- ning (see DeSalle and Hunt, this issue).

“The age oi each island may also not be the maximum age of its endemic species. Species present on one Island may have existed on other islands and since gone extrnct Olson and lames& have shown this to be true for the greater Kona finch.

is

TREE vol. 2, no. 7, July 7987

Biogeography The affinities of the Hawaiian

flora and fauna - both marine and terrestrial - are largely Indo-Pacific. The exceptions among marine in- vertebrates include a small percen- tage of circumtropical species and a few species with eastern Pacific affinities (see Kay and Palumbi, this issue). The inshore fish fauna is probably derived from the Indo- west Pacific, having primary affinity with the Ryukyu Islands and south- ern lapan; but the importance of colonization from the central Pacific remains controversial (Hourigan and Reese, this issue).

There are only a few terrestrial taxa with New World affinities. The most striking botanical examples include the silversword alliance species, all of which came from a single North American ancestor (see Carr, this issue), and the Hawaiian mints (Labiatae) in which only one of the 52 native species had its roots in North America5. The Hawaiian insect fauna was estimated6 to be more than 90% Pacific, the few American elements being mostly large, strong fliers (e.g. a dragonfly, several sphinx moths and several long-horned beetles). The land snails, to a simi- lar degree, are Pacific in origit$.

The biota of the Hawaiian islands is unique. Because of the immense distances that separate the archipelago from both islands and continents, and because some animals and plants are better able to disperse and colonize than are others, the fauna and flora are de- pauperate and distinctive. Com- pared to source area assemblages, certain taxa are well represented while others are notably missing. For example there are no native amphibians, no native terrestrial reptiles? and only one mammal, the Hawaiian bat*; there are no bam- boos or conifers in the flora; among fish there are no snappers or group- ers; and among mollusks no Nautilus or giant clams (Tridacnal.

In groups that are well repre- sented in Hawaii, such as birds, insects and snails, many species are representatives of a very small subset of the world’s higher taxa.

tCeckos may have arrived before the Polynesians iA. Allison. pers. commun I *There is an undescribed fossil bat species IF Howarth. pers c0mmun.l

176

Birds are represented by only I7 of the world’s 150 living families4.7; only four (7%) of the world’s 60 passerine families occur in Hawaii (see Freed, Conant and Fleischer, this issue). Fifteen per cent of the world’s nearly 1000 insect families made their way to HawaiV, while 27% of the 40 land snail families worldwide and 58% of the 19 fami- lies in the Pacific Basin are native to Hawaii6.

Because there are gaps in all its taxonomic assemblages, Hawaii’s biota has been termed ‘disharmonic”J.9. This term is in- appropriate, however, because of its modern connotations of com- petition, discord and imbalance. In- deed it has been suggested that the gaps in the ancestral biota have permitted the spectacular diversi- fication of the Hawaiian biota.

Radiations and adaptive shifts Mueller-Dombois’O aptly de-

scribes the Hawaiian biota as natur- ally depauperate and secondarily enriched. The large numbers of potential habitats created by the varied topography and steep rain- fall gradients in combination with the synergistic effects of co- occurring new species are thought to be contributing factors to specia- tion in Hawaii. In addition, lack of competition and the presence of ‘unfilled ecological niches’ (in the sense of the organism’s role in the environment i I, rather than the ti-dimensional hypervolume of Hutchinson’2), due to missing tax- onomic elements, are often infer- red to be stimuli for radiation and adaptive shiftsl”,13. Recent models of speciation superimpose the genetics and behavior of organisms on the backdrop of these varied potentially isolated environments with their unfilled niches (see Kay and Palumbi, and Kaneshiro and Boake, this issue).

Speciation rates have been very different for marine and terrestrial Hawaiian systems. Thus, although species endemism in marine in- vertebrates and inshore fishes is high (30-32%) compared to other marine faunas, it is dramatically lower than the 90-99% endemism found in terrestrial invertebrates, birds and plants.

Endemic terrestrial Hawaiian taxa are often characterized by ram- pant speciation within lineages, re-

sulting in complexes of closely re- lated species. Among the best known of these radiations are those of the insect genus Drosopkifa, the land snails, the honeycreepers, and several groups of Hawaiian plants.

Drosophila meluflogdster is perhaps the world’s most famous insect. Both the genus Drosophila and the family Drosophilidae are, however, peculiarly Hawaiian. There are more endemic species in Hawaii than in the rest of the world com- bined: 346 described species in the genus Drosopkila and more than 700 Hawaiian species (estimated) in the family Drosophilidae.

There are two Hawaiian droso- philid lineages: the scaptomyzoids and the drosophiloids. Species of the former group are well differenti- ated in terms of internal (particu- larly reproductive) morphology, but conservative in external morphol- ogy and mating behavior. The drosophiloid species tend to be conservative in genital morphology, but exhibit complex external mor- phology and some astonishing pat- terns of mating behavior. The simi- larities between Drosopkila and Scap- tornyza are such that entomologists suggest that Scaptomyza may have evolved from DrosopIiila in Hawaii and colonized other islands in the Pacific and even New World continents’4-‘6. Aspects of the evolution of Hawaiian drosophilids based on cytological, behavioral and molecular data are reviewed by Carson, Kaneshiro and Boake, and DeSalle and Hunt (this issue1 respectively.

There are many more insect genera which remain to be studied. Of these, at least seven have more than 100 species: the moth Hypos- mocoma (350 spp.); the beetles ProterrIGtius ( I8 I I and Plagithrnyslrs (1401; the wasps Sierola (182) and Odynerus ( 1051; the flies Lispocepltafa ( 1051, Campsicnemus (136) and Scap- tomyza ( I I9)8.17-20.

Hawaii’s best known land snails are the brightly colored arboreal achatinelline snails (family Tor- natellinidae, subfamily Achatinelli- nae). Partltlina is the most speciose with 44 species, Achatiflella only slightly less so with 42 species. The oldest of the land snails in the islands may be the endemic ground-living family Amastridae, which has two subfamilies: one which gives birth to live young, the

TREE vol. 2, no. 7, July 1987

other which produces eggs. The amastrids are especially diversified with respect to shell shape, sculp- ture and size. Small rotund shells are represented on all the islands; minute discoid shells, Armisiellu, are found on Oahu; the ‘giants’, Carelia, IO cm in length, occur only on Kauai6.21.

Among vertebrates, the Hawaiian honeycreepers with 43 species (27 extant + 16 fossil species) are a better example of radiation than the 14 extant Galdpagos finch spe- cies (no species known from fos- sils). In numbers, bill morphology, plumage coloration and behavior, the honeycreepers are much more complex. The adaptive radiation of Hawaiian birds goes well beyond the traditional trophic characters (beaks and tongues) which have received so much attention. Recent investigations have shown that bird subspecies on different islands, and even populations on the same island, vary considerably in charac- ters such as interspecific flocking, male coloration relative to females, and nest morphology and position (see Freed, Conant and Fleischer, this issue).

Hawaiian plants exhibit some spectacular examples of radiation. The best studied are members of the silversword alliance described by Carr (this issue). Others, crying out for study, include the Hawaiian lobeliads with six endemic genera out of seven. Five of these - com- prising 90 species - arose from one colonizer; the largest of these five genera, Cyanea, has 52 species rang- ing in habit from shrubs to trees22. The Pacific genus Cyrtandru in the African violet family (Gesneri- aceae), with 53 endemic Hawaiian species, was thought to have come from a single ancestor and was cited by Carlquist13 as an example of non-adaptive radiation because ‘most species differ by features which have no obvious adaptive value’. Recent taxonomic compari- sons of Hawaiian Cyrtandru with Malesian and other Pacific island Cyrtandra, however, suggest that there were four or five separate introductions rather than a single radiating ancestor, thus explaining more simply the co-occurence of very different form+.

Hawaiian species are of interest from an evolutionary standpoint not only because they are diverse

but also because many of them have diverged substantially from their presumed ancestors. Many cases of ‘adaptive shifts’ have been documented where newly evolved species exhibit characteristics and assume ecological roles unknown in other parts of their respective taxa. Geometrid caterpillars are well known herbivores on the North American continent; in Hawaii, some geometrid caterpillars in the genus Eupithecia are carnivorous - the only predatory lepidopteran larva in the world24. Spiders are known for eating flies; in Hawaii, in an apparent case of evolutionary revenge, the scaptomyzoid T&flu- chaeta has adopted the habit of preying on spider eggs. Lygaeid bugs elsewhere feed on seeds; in Hawaii some are scavengers. The nymphs of a variety of genera of dragonflies and damselflies (order Odonata) all over the world live in flowing water or in still water, in leaf axils, in leaf litter, and under or on wet rocks; in Hawaii, a single damselfly genus Meg&g& has species which have radiated into all of these kinds of habitats8.

Among the land snails, members of the family Succineidae, which live in marshes and on stream banks elsewhere, came to roost in the damp axils of plants and on the leaves of bushe+. Similarly, ground dwelling achatinelline snails be- came arboreal achatinelline snails2’. Among birds, honeycreep- ers - descended from a finch-like insectivorous ancestor - have adopted highly specialized methods of nectar, seed and insect eating (see Freed, Conant and Fleischer, this issue).

Non-speciose lineages It is important to point out that

not all successful Hawaiian colon- ists produced many descendant species. Why should one genus be monotypic while another produces hundreds of species? Carson25 compiles genus : species ratios for selected Hawaiian taxa and de- scribes genetic conditions which could result in speciose versus non-speciose lineages. For most Hawaiian taxa, not enough is known about their genetic structure to decipher the reasons behind the presence or absence of specific diversity. Most studies reviewed

in this issue, therefore, merely describe patterns.

One remarkably clear pattern is that marine ancestors, unlike their terrestrial counterparts, did not give rise to speciose lineages; the marine invertebrate genera with Hawaiian endemics mostly contain only one or two endemic species. The largest number of congeneric endemic marine invertebrate spe- cies is seven (Kay and Palumbi, this issue). Among terrestrial Hawaiian invertebrates it is not uncommon to find genera with more than 100 endemic specie+. Genera which are themselves endemic are not uncommon in the terrestrial biota? in contrast, there are no endemic marine genera and there has been little radiation of species within genera (Kay and Palumbi, and Hourigan and Reese, this issue).

The ubiquitous Hawaiian forest tree Metrosideros polymorpha may rep- resent an intermediate condition with regard to speciose versus non- speciose lineages. It is highly vari- able in growth form and occurs in an enormous number of habitats. It appears to have radiated without speciating. Mueller-Dombois (this issue) describes ‘successional varieties’ of this species, which have both genetically and environ- mentally influenced distinguishing characteristics.

Fragility, introductions and extinctions It is the extraordinary features of

island biotas which make them in- teresting to evolutionary biologists. At the same time it is these very features which are the basis for the fragility of island life: specializa- tion, limited ranges, loss of disper- sal ability, flightlessness and lack of defenses (e.g. toxins and thorns) are among these influential charac- teristics.

Most Hawaiian endemic species are restricted to single island@. In the Hawaiian picture-wing Drosophila only two (D. grimshawi and D. cru- cigera) of the more than 100 de- scribed species are known to occur

on more than one island -and they may yet be split by taxonomists into single island endemics. Of the

QFerns are notable exceptions to this rule Of the total of II8 endemic species, only 20 116.9%1 are single Island endemics. This can probably be explained by the ready dispersal of small wind-borne spores IW H Wagner, )r, pers c0mmun.l

177

TREE vol. 2, no. 7, July 1987

222 described carabid beetle spe- cies, only five are found on more than one island. Many insect and snail species are restricted to indi- vidual mountains or valleys. The limited ranges and specialized habits of these species make them especially vulnerable to disturb- ance.

In Hawaii we find unique species even in the most unlikely places. Extreme (high stress) environments were until recently thought to be exceptions to the pattern of rapid evolution of species. In fact, they were believed to be devoid of life. Exploration of lava tubes, marine caves, high altitude cinder fields and new lava flows has turned up a surprising array of endemic taxa; Howarth (this issue) reviews the recent literature and discusses the vulnerability of these ecosystems.

Life history patterns also affect the sensitivity of organisms to changing environments and to com- petition and predation. Hadfield and coworkers2L28, studying land snails, have elucidated life history patterns which serve as clues to the vulnerability of the group. Both genera they have studied, Acha- tinella and Parfufirra, are late in maturing (6-7 years) and have low fecundity (one offspring per year in Achatinella mustelina; 6-7 in Partulina proximal; P. proxima has been esti- mated to live for 18-19 years. When compared with the life history char- acteristics of the predatory snail Euglandina - less than a year to maturity and > 600 eggs per year with a life span of up to five years - it is easy to see why the native snails are being decimated by in- troduced predators.

Freed, Conant and Fleischer (this issue) point out that 68% of the original land bird fauna is extinct today and that new fossils may in- crease the known number of extinc- tions. The birds are typical of a wider phenomenon in Hawaii.

Hawaiian taxa are disappearing and, sadly, remain largely unstud- ied from an ecological and evolu- tionary perspective. To illustrate the magnitude of the loss, consider that of the 210 native genera of flowering plants, only six (all in the family Compositae; discussed by Carr, this issue), and two genera of ferns (Diellia29 and Sadleria? have been studied in any detail; studies of a few other taxa are just begin- ning. Nearly one third of the native species of flowering plants are threatened or endangered (W.L. Wagner, pers. commun.).

The major causes of extinction in Hawaii are habitat conversion and introduction of alien predators, competitors and diseases. Land conversion is almost complete in the lowlands and was begun by the first Polynesian settlers, who brought dogs, pigs, rats and about a dozen plant species which they cultivated3’. Since that time, more than 2000 arthropods, 50 land birds, 18 mammals and 600 plants have been introduced to Hawaii32. Of these, a handful - those with the ability to spread rapidly - have done the majority of the damage. Vitousek, Loope and Stone (this volume) review the biological effects of these invasive species and discuss how studies of exotics can contribute to our understand- ing of ecological and evolutionary processes, and perhaps help to preserve the remaining native taxa.

The opportunities for evolution- ary studies in the Hawaiian archipelago are unique. Nowhere else in the world can one find such a rich ‘natural laboratory’ in close proximity to modern university and museum facilities. We cannot offer 50 pounds to any researcher willing to come and study the Hawaiian biota but we can make the assur- ance that the scientific rewards of such studies will be considerable.

Acknowledgements I would like to thank the following people

for information and/or helpful suggestions: S. Conant, C. Carr, H.L. Carson, N. Evenhuis, R. Fleischer, L. Freed, D. E. Hardy, F. Howarth, K. Kaneshiro, A. Martin, S. Palumbi, W.H. Wagner, fr, W.L. Wagner, and especially E.A. Kay.

References 1 Darwin, C.R. (19721 in A Natural History of tke Hawaiian Islands: Selected Readings (Kay, E.A.. ed.1. University of Hawaii Press

2 Clague, D.A. and Dalrymple, G.B. ( 19871 in Volcanism in Hawaii (Decker, R.W., Wright, T.L. and Stauffer, P.H., edsl. pp. 5-54. US Govt Printing Office 3 Nonark, W.R., Clague, D.A. and Moore. LG. (1982) Nat. Hist. 91,68-71 4 Olson, S.L. and fames, H.F. (1982) Smitlison. Contrib. Zoof. 365, l-59 5 Epling, C. (19481 Brittonia 6, 352-364 6 Zimmerman, E.C. ( 19481 Insects of Hawaii (Vol. I I, University of Hawaii Press 7 Austin, OJ., fr II9851 Families of Birds, Golden Press 8 Simon, C., Gagne, W., Howarth, F. and Radovsky, F. f 1984) Bull. Entomof. Sot. Am. 30, a-17 9 Hubble, T.H. (1972) in A Natural History of the Hawaiian Islarrds: Selected Readings (Kay, E.A., ed.), pp. 385-395, University of Hawaii Press 10 Mueller-Dombois, D. I I9671 in bland Ecosystems: Biological Organization in Selected Hawaiian Communities (Mueller-Dombois, D., Bridges, K.W. and Carson, H.L., eds), pp. 502-520, Hutchinson-Ross II Krebs, C. (1972) Ecology: Tke Experimental Analysis of Distri6ution and AGundance. Harper G Row I2 Hutchinson. G.E. ( 1957) Cold Spring Harbor Symp. Quant. Biol. 22,415-427 13 Carlquist, S.1. II9801 Hawaii, a Natural History, Pacific Tropical Botanical Garden (Lawai, Kauail I4 Carson, H.L., Hardy, DE., Spieth, H.T. and Stone, W.S. t 1970) in Essays in Honor of Tti. Dobzkansfry (Hecht. M.K. and Steere. W.C., edsl, pp. 436-543, Appleton-Century-Crofts I5 Carson, H.L. and Kaneshiro, K.Y. (1976) Annu. Rev. Ecol. Syst. 7, 31 l-345 16 Hardy, D.E. and Kaneshiro, K.Y. (1981) in The Genetics and Biology of Drosophila (Ashburner, M., Carson, H.L. and Thompson, J.N.. Jr, edst, pp. 309-342, Academic Press 17 Hardy, D.E. ( 1964) Insects of Hawaii (Vol. I I I, University of Hawaii Press 18 Hardy, D.E. II9651 Insects of Hawaii (Vol. 121, University of Hawaii Press I9 Tenorio, ).M. (1969) Insects of Hawaii (Vol. I I Suppl.) University of Hawaii Press 20 Hardy, D.E. (1981 I Insectsof HawaiifVol. 141, University of Hawaii Press 21 Cooke, C.M., fr and Kondo, Y. II9601 Bernite P. Bishop Mus. Bull. 22 I, l-303 22 Rock, I. (1919) Mem. Bernice P. Bishop Mus. 712). l-395 23 Wagner, W.L. (19861 Am. I. Bot. 73,792-793 24 Montgomery, S.L. II9751 Proc. Hawaii. Entomol. Sot. 22, 65-102 25 Carson, H.L. (1987) in Colonization, Succession, and Stability (Proc. Brit. Etol. Sot. Symp. 26) 187-206 (Gray, A.f., Crawfey. M.f. and Edwards, P.f., edsf, pp. 187-206, Blackwell Scientiffc Publications 26 Hadffeld, M. (1980) Par. Sri. 34,345-358 27 Hadffeld, M. (1986) Malacologia 27,67-81 28 Hadfield, M. and Miller, S. in Molluscs as Threatened Species: Their Exploitation and Conservation (9th Annual Meeting of tke International Malacological Union, Edinburgh, Scotland, September 1986) (in press) 29 Wagner, W.H., Ir (1952) Univ. Cafif. PubI. Bot. 26, I-212 30 Lloyd, R.M. and Holbrook-Walker, S. II9731 Bot.1. Linn. Sot. 67, 157-174 31 Kirch. P. (19821 Pac. Sci. 36, l-14 32 Stone, C.P. and Scott, I.M., eds 11985) Hawaii’s Terrestrial Ecosystems: Preservation and Management, University of Hawaii Press for Cooperative National Park Resources Study Unit

178