Hawaiian Islands, Biospeleology

by Francis G. Howarth

The Hawaiian Islands are the emergent summits of massive volcanoes in the North Pacific Ocean. At more than 3500 km from the nearest comparable land, they are the most isolated group of high islands in the world. The eight high islands at the southeast end of the chain range in age from Hawaii at less than one million years to Kauai at nearly 6 million years. Relatively few organisms colonized the islands, but these evolved into a diverse array of native species. Given the isolation and youth of the islands, extreme youth of lava tubes, absence of taxa typically inhabiting continental caves, and rarity of tropical cave species in general, obligate cave species or troglobites were not expected to occur in Hawaii. However, since 1971, more than 70 terrestrial troglobites have been discovered (Table 1). Their study has led to a revision of theories on the evolution and ecology of cave animals (Howarth, 1980; 1993). Although no less interesting, the aquatic cave fauna of Hawaii (Kensley & Williams, 1986; Maciolek, 1986) is restricted to the coastal zone where it is associated with anchialine ecosystems.

Three types of caves support terrestrial troglobites in Hawaii. The most common are lava tubes, which characteristically form in fluid basaltic lava called pahoehoe and which are a common land form on the younger volcanoes on Hawaii, Maui, and Molokai. Remnant lava tubes occur on older volcanoes. Limestone caves formed by dissolution of elevated reefs and lithified sand dunes on the older islands of Oahu and Kauai. Piping (or suffosion) caves formed when water erosion plucked softer material out from under a layer of harder material. In Hawaii, they are best developed beneath montane rainforests on Molokai where a lava flow covers an ash layer. Sea (littoral) caves and talus caves occur on all high islands but rarely support troglobites unless they intersect more extensive cavernous rock strata.

Cave habitats are strongly zonal, and five terrestrial zones are recognized: entrance, twilight, transition, deep, and stagnant air (Howarth, 1993). The surface and underground environments meet in the entrance zone. The twilight zone extends from the boundary of plant life to the limit of light. The transition zone is in total darkness but is subjected to nocturnal desiccating winds caused by cold air sinking into the cave. The deep zone is characterized by total darkness and long-term presence of moisture and saturated atmosphere. The stagnant air zone lies beyond the deep zone and only slowly exchanges air with the surface; therefore decomposition gases, especially carbon dioxide, can accumulate. The stagnant air zone occurs not only in deep caves that trap air masses, but also it is considered to be the characteristic environment of intermediate-sized voids (mesocaverns) in cavernous rock. Troglobites live only in the two inner zones.

The main energy sources in Hawaiian caves are plant roots, especially those of Metrosideros polymorpha, the dominant pioneering tree on lava flows. Additional food energy comes from organic material washing or falling into crevices, surface animals wandering underground, and probably chemoautotrophic bacteria. Native cutworm moths once roosted in caves in huge numbers, but the group has become rare. Cave bats and continental cave crickets do not occur in Hawaii. Cixiid planthoppers and their nymphs feed on living roots by sucking sap with piercing mouthparts. The blind flightless adults wander through subterranean voids in search of mates and roots (Hoch & Howarth, 1993; 1999). Caterpillars of noctuid moths prefer to feed on succulent flushing root tips, but they also scavenge on a variety of foods. The pale adults are flightless or weakly flighted and stay underground. Tree crickets, terrestrial amphipods, and isopods are omnivores but feed extensively on roots. Cave rock crickets are also omnivorous as well as being opportunistic predators. Feeding on rotting organic material and associated microorganisms are millipedes, springtails, and flies. Terrestrial water treaders suck juices from long-dead arthropods. The blind predators include spiders, pseudoscorpions, rock centipedes, thread-legged bugs, and beetles. Most of the cave predators will also scavenge on dead animal material (Howarth, 1987; 1991).

Unlike soil, which acts as a filter trapping nutrients and water, the voids in cavernous rock strata act as conduits that transport organic resources deep underground. Young basaltic flows, like cavernous areas generally, contain a vast anastomosing system of medium to large sized voids. The deeper voids (that is, the deep and stagnant air zones) are stressful environments for most surface organisms, and the food resources there are unavailable to them. Rather than being relicts stranded in caves by changing climate, obligate cave species are highly specialized to exploit abundant energy resources within the medium-sized voids (mesocaverns) and colonize caves (macrocaverns) only where their unique environment is found. Hawaiian troglobites appear to have evolved following an adaptive shift that allowed them to exploit underground environments. Three different surface habitats (moist forests, barren rock, and marine littoral) served as the source for ancestors of the cave species. In many cases, their closest surface relative is still extant in one of these neighboring habitats corroborating the theory that cave species evolved following an adaptive shift, and indicating that the relictualism displayed by some troglobites may be secondary (Howarth, 1993). The adaptations displayed by Hawaiian troglobites are truly remarkable, including such anomalies as blind underground tree crickets, planthoppers, flightless flies, terrestrial water treaders and amphipods, and the epitome of adaptive shifts: the no-eyed, big-eyed hunting spider (Adelocosa anops). Howarth & Mull (1992) show color photographs of many related cave and surface species pairs.

Cave species evolved independently on five islands, indicating that cave adaptation is a general process and that they can evolve wherever there has been suitable habitat and available resources for a sufficient time. The degree of convergence in morphology, behavior and physiology among the independently derived fauna on different islands is striking but can be understood as adaptations to cope with the stressful underground environment. Surprisingly, the degree of cave adaptation is not correlated with either island or cave age, but with environmental factors and size of the available habitat (Howarth, 1993; Taiti & Howarth, 1998; Hoch & Howarth, 1999). In fact, Hawaii, the largest and youngest island, supports the largest number of cave-adapted species (Table 1). The diversity of cave species may be much higher than currently recognized. Recent morphological, behavioral, and molecular studies of several troglobitic groups on Hawaii Island have demonstrated that each cave may harbor unique populations or species. Hoch and Howarth (1993) showed that each cave population of Oliarus polyphemus studied has a unique mating song and small but consistent differences in morphology. Even the mating calls in neighboring lava tubes were distinct, and some had diverged sufficiently to appear to be reproductively isolated (i.e., distinct biological species). Otte (1994) confirmed that the rock cricket Caconemobius varius also represented a complex of species. Different cave populations of moths and millipedes can also be distinguished morphologically, but the species have not been formally described.

Hawaiian caves are island-like habitats within islands, and like other Hawaiian environments, cave communities are threatened, both by direct disturbance from visitors and indirectly from activities on the surface. Caves are used as refuse dumps; vegetation over caves is cleared; rocks surrounding caves are mined; ground water is polluted, and alien plants and animals disrupt cave ecosystems. Human visitors may break plant roots, kill blind animals, trample bones, and damage other values. Only two Hawaiian cave species currently enjoy formal protection as federally listed endangered species: the no-eyed, big-eyed hunting spider and the terrestrial sandhopper, both of which are known from a small area of remnant caves on Kauai. Many other species deserve conservation initiatives. Most Hawaiian caves remain unsurveyed, and many more endemic animals remain to be discovered, especially since many apparent widespread taxa may in fact represent species complexes. Effective conservation is predicated on accurate systematics studies. There is a dilemma: publicity featuring caves can increase visitation rates, leading to increased damage in caves; but if caves and their values are not made known, their resources may be destroyed through ignorance during changes in land use (Howarth, 1983). If these cave ecosystems had been destroyed before discovery, it would be difficult to speculate that they ever existed.

Works Cited

Hoch, H. & Howarth, F.G. 1993. Evolutionary dynamics of behavioral divergence among populations of the Hawaiian cave-dwelling planthopper Oliarus polyphemus (Homoptera: Fulgoroidea). Pacific Science, 47: 303-318.

Hoch, H. & Howarth, F.G. 1999. Multiple cave invasions by species of the planthopper genus Oliarus in Hawaii (Homoptera: Fulgoroidea: Cixiidae). Zoological Journal of the Linnean Society, 127(4): 453-475.

Howarth, F.G. 1980. The zoogeography of specialized cave animals: a bioclimatic model. Evolution, 34: 394-406.

Howarth, F.G. 1983. The conservation of cave invertebrates. In: Proceedings first International Cave Management Symposium held at Murray, Kentucky, July, 1981, edited by J.E. Mylroie, Copyright 1983 J.E. Mylroie, Murray, KY

Howarth, F.G. 1987. Evolutionary ecology of aeolian and subterranean habitats in Hawaii. Trends in Ecology Evolution, 2:220-223.

Howarth, F.G. 1993. High-stress subterranean habitats and evolutionary change in cave-inhabiting arthropods. American Naturalist, 142: S65-S77.

Howarth, F.G. & Mull, W.P. 1992. Hawaiian Insects and Their Kin. University of Hawaii Press, Honolulu

Kensley, B. & Williams, D. 1986. New shrimps (families Procarididae and Atyidae) from a submerged lava tube on Hawaii. Journal of Crustacean Biology, 6:417-437.

Maciolek, J.A. 1986. Environmental features and biota of anchialine pools on Cape Kinau, Maui, Hawaii. Stygologia, 2(1/2): 119-129.

Otte, D. 1994. The Crickets of Hawaii. Academy of Natural Sciences, Philadelphia, PA.

Taiti, S. & Howarth, F.G. 1998. Terrestrial isopods (Crustacea: Oniscidea) from Hawaiian caves. Memoires de Biospeologie, 24:97-118.

Further Reading

Ahearn, G.A. & Howarth, F.G. 1982. Physiology of cave arthropods in Hawaii. Journal of Experimental Zoology, 222: 227-238.

Camacho, A.I. (editor). 1992. The Natural History of Biospeleology. Monografias, Museo Nacional de Ciencias Naturales. Madrid.

Culver, D.C. 1982. Cave Life Evolution and Ecology. Harvard Univ. Press, Cambridge.

Howarth, F.G. 1981. Community structure and niche differentiation in Hawaiian lava tubes. In: Island Ecosystems: Biological Organization in Selected Hawaiian Communities. US/IBP Synthesis Series. Vol. 15, edited by D. Mueller-Dombois, K.W. Bridges, & H.L. Carson, Hutchinson Ross Publishing Co., PA.

Howarth, F.G. 1983. Ecology of cave arthropods. Annual Review Entomology, 28:365-389.

Howarth, F.G. 1983. Bioclimatic and geologic factors governing the evolution and distribution of Hawaiian cave insects. Entomologia Generalis, 8:17-26.

Howarth, F.G. 1988. The evolution of non-relictual tropical troglobites. International Journal of Speleology, 16:1-16.

Howarth, F.G. 1991. Hawaiian Cave Faunas: macroevolution on young islands. In: The Unity of evolutionary biology, Vol. 1, edited by E. C. Dudley, Dioscorides Press, Portland, OR

Wilkens, H., Culver, D.C. & Humphries, W.F. (editors.). 2000. Subterranean Ecosystems. Elsevier Science B.V., Amsterdam.