Caves

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the complex feedback processes in ecological systems increases, catastrophe theory could become a useful predictive tool. See also: Bifurcation; Chaos; Driver–Pressure–State– Impact–Response; Hysteresis; Mathematical Ecology; Parameters.

Further Reading Adema EB, Grootjans AP, Petersen J, and Grijpstra J (2002) Alternative stable states in a wet calcareous dune slack in the Netherlands. Journal of Vegetation Science 13: 107–114. Arnol’d VI (1992) Catastrophe Theory. New York: Springer. Berry MV and Nye JF (1977) Fine structure in caustic junctions. Nature 267: 34–36. Carpenter SR (2003) Excellence in Ecology 15: Regime Shifts in Lake Ecosystems: Pattern and Variation. Oldendorf/Luhe, Germany: International Ecology Institute.

Casti JL (1994) Complexification: Explaining a Paradoxical World through the Science of Surprise. New York: HarperCollins. Lockwood JA and Lockwood DR (1991) Rangeland grasshopper (Orthoptera: Acrididae) population dynamics: Insights from catastrophe theory. Environmental Entomology 20: 970–980. Mayer AL and Rietkerk M (2004) The dynamic regime concept for ecosystem management and restoration. BioScience 54: 1013–1020. Poston T and Stewart I (1996) Catastrophe Theory and Its Applications. New York: Dover Publications. Rietkerk M, Dekker SC, de Ruiter PC, and van de Koppel J (2004) Selforganized patchiness and catastrophic shifts in ecosystems. Science 305: 1926–1929. Roopnarine PD (2006) Extinction cascades and catastrophe in ancient food webs. Paleobiology 32: 1–19. Scheffer M, Carpenter S, Foley JA, Folke C, and Walke B (2004) Catastrophic shifts in ecosystems. Nature 413: 591–596. Thom R (1975) Structural Stability and Morphogenesis, 1st edn. Massachusetts: W A Benjamin. van Nes EH and Scheffer M (2004) Large species shifts triggered by small forces. American Naturalist 164: 255–266. Weisstein EW (2007) Catastrophe. From MathWorld – A Wolfram Web Resource. http://mathworld.wolfram.com/Catastrophe.html (accessed August 2007)

Caves F G Howarth, Bishop Museum, Honolulu, HI, USA ª 2008 Elsevier B.V. All rights reserved.

Caves Cave Environments Food Resources Cave Communities Adaptations to Cave Life

Other Cave-Like Habitats Case Study: Hawai‘i Perspective Further Reading

Caves

on their size, shape, and interconnectedness, caves develop unique environments that often support distinct ecosystems.

Caves are defined as natural subterranean voids that are large enough for humans to enter. They occur in many forms, and cavernous landforms make up a significant portion of the Earth’s surface. Limestone caves are the best known. Limestone, calcium carbonate, is mechanically strong yet dissolves in weakly acidic water. Thus over eons great caves can form. Caves form in other soluble rocks, such as dolomite (calcium magnesium carbonate), but they are usually not as extensive as those in limestone. Volcanic eruptions also create caves. The most common are lava tubes that are built by the roofing over and subsequent draining of molten streams of fluid basaltic lava. In addition, cave-like voids form by erosion (e.g., sea caves and talus caves) and by melting water beneath or within glaciers. Depending

Cave Environments The physical environment is rigidly constrained by the geological and environmental settings and can be defined with great precision because it is surrounded and buffered by thick layers of rock. Caves can be water-filled or aerial. Aquatic Environments Aquatic systems are best developed in limestone caves since water creates these caves. Debris-laden water in voids in nonsoluble rock will eventually fill caves.

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A significant exception is found in young basaltic lava that has flowed into the sea. Here, subterranean ecosystems develop in the zone of mixing freshwater and salt water within caves and spaces in the lava. The system is fed by food carried by tides and groundwater flow. Frequent volcanism creates new habitat before the older voids fill or erode away. Aquatic cave environments are dark, three-dimensional (3D) mazes, in which food and mates may be difficult to find. In addition, the water can stagnate, locally becoming hypoxic with high concentrations of toxic gases including carbon dioxide and hydrogen sulfide.

Terrestrial Environments

The subterranean aerial environment is stressful for most organisms. It is a perpetually dark, 3D maze with a water-saturated atmosphere and occasional episodes of toxic gas concentrations. Many of the cues used by surface animals are absent or operate abnormally in caves (e.g., light/dark cycles, wind, sound). Passages can flood during rains, and crevices might drop into pools and water-filled traps. If the habitat is so inhospitable, why and how do surface animals forsake the lighted world and adapt to live there? It is the presence of abundant food resources that provides the impetus for colonization and adaptation.

Food Resources

The terrestrial environment in long caves is buffered from climatic events occurring outside. The temperature stays nearly constant, fluctuating around the mean annual surface temperature (MAST); except passages sloping down from an entrance tend to trap cold air and remain a few degrees cooler than MAST. Passages sloping up are often warmer than MAST. The environment is strongly zonal (Figure 1). Three zones are obvious: an entrance zone where the surface and underground habitats overlap; a twilight zone between the limit of photosynthesis and the zone of total darkness. The dark zone can be further subdivided into three distinct zones: a transition zone where climatic events on the surface still affect the atmosphere, especially relative humidity (RH); a deep zone where the RH remains constant at 100%; and an innermost stagnant air zone where air exchange is too slow to flush the buildup of carbon dioxide and other decomposition gasses. The boundary between each zone is often determined by shape or constrictions in the passage. In many caves, the boundaries are dynamic and change with the seasons.

The main energy source in limestone caves is sinking rivers, which carry-in abundant food not only for aquatic communities but also via flood deposits for terrestrial communities. Rivers are less important in nonsoluble rock, such as lava, but percolating runoff washes surface debris into caves through crevices. Other major energy sources are brought in by animals that habitually visit or roost in caves, plants that send their roots deep underground, chemoautotrophic microorganisms that use minerals in the rock and accidentals that fall or wander into caves and become lost. Generally in surface habitats, accumulating soil filters water and nutrients and holds these resources near the surface where they are accessible to plant roots and surface-inhabiting organisms. However, in most areas with underlying caves, the soil is thin with areas of exposed bare rock because developing soil is washed or carried into underground voids by water or gravity. Soil formation is limited, and much of the organic matter sinks out of the reach of most surface animals.

Entrance zone

Twilight zone

Transition zone

Figure 1 Schematic profile view of the cave habitat showing the location of principal zones.

Deep zone

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Except for guano deposits, flood deposits, scattered root patches, and other point-source food inputs, the defining feature of cave habitats is the appearance of barren wet rock. Visible food resources in the deep cave are often negligible, and what food deposits there are would be difficult for animals to find in the 3D maze. Food resources in the system of smaller spaces is difficult to sample and quantify, but in theory, some foods may be locally concentrated by water transport, plant roots, or micro point source inputs such as through cracks extending to the surface. These deposits would be more easily exploited than would widely scattered deposits. In each biogeographic region, a few members of the surface and soil fauna have invaded cave habitats and adapted to exploit this deep food resource. The colonists usually were pre-adapted; that is, they already possessed useful characteristics resulting from living in damp, dark habitats on the surface.

Cave Communities Guano Communities Many animals live in or use caves. Cave-inhabiting vertebrates are relatively well-known. Cave bats, swiftlets (including the edible-nest swiftlet of Southeast Asia), and the oil bird in South America use echolocation to find their way in darkness. Pack rats in North America, along with cave crickets and other arthropods also roost in caves. Large colonies of these cave-nesting animals carry in huge quantities of organic matter with their guano and dead bodies. This rich food resource forms the basis for specialized communities of microorganisms, scavengers, and predators. Arthropods comprise the dominant group of larger animals in this community, and like their vertebrate associates, most species are able to disperse outside caves to found new colonies. Deep Cave Communities In the deeper netherworld, communities of mysterious, obligate cave animals occur. Most are invertebrates, but a few fishes and salamanders have colonized the aquatic realm. Crustaceans (shrimps and their allies) dominate in aquatic ecosystems, and insects and spiders dominate terrestrial systems. Although a few species are specialists on living plant roots or other specific resources, most are generalist predators or scavengers. The relatively high percentage of predators indicates the importance of accidentals as a food resource. However, many presumed predatory species, such as spiders, centipedes, and ground beetles, will also scavenge on dead animals when available. It is not advantageous to have finicky tastes where food is difficult to find. Thus, the food chain, which

normally progresses from plants through plant feeders, scavengers, and omnivores to predators, more closely resembles a food web with most species interacting with most of the other species in the community.

Adaptations to Cave Life Animals roosting or living in caves must adapt to cope with the unusual environment. Paramount for the caveroosting vertebrates is the ability to find their way to and from their roosts at the correct time. Not surprisingly, the birds and bats display uncanny skill in memorizing the complex maze to and from their cave roosts. Pack rats use trails of their urine to navigate in and out of caves. Species using the twilight and transition zones can use the daily meteorological cycle for cues to wake and leave the cave. Those roosting in the deep zone may rely on accurate internal clocks to know when it is beneficial to leave their roost. Organisms that adapt to live permanently underground must make changes in behavior, physiology, and structure in order to thrive in the stressful environment. They need to find food and mates and successfully reproduce in total darkness. Their hallmark is the loss or reduction of conspicuous structures such eyes, bodily color, protective armor, and wings. These structures are worthless in total darkness, but they can be lost quickly when selection is relaxed because they are expensive for the body to make and maintain. How such losses could happen quickly is demonstrated by the cave-adapted planthoppers (Cixiidae). The nymphs of surface species feed on plant roots and have reduced eyes and bodily color whereas their adults have big eyes, bold colors, and functional wings. The cave-adapted descendents maintain the nymphal eyes, color, and other structures into adulthood, a phenomenon known as neoteny. The high relative humidity and occasional episodes of elevated CO2 concentrations are stressful to cold-blooded organisms. The blood of insects and other invertebrates will absorb water from saturated atmosphere, and the animals literally will drown unless they have adaptations to excrete the excess water. High levels of CO2 force animals to breathe more, which increases water absorption. Cave-adapted insects often have modified spiracles to prevent or cope with their air passages filling with water. Most lava tube arthropods have specialized elongated claws to walk on glassy wet-rock surfaces. Many have elongated legs to step across cracks rather than having to descend and climb the other side. Jumping or falling might land a hapless animal in a pool or water-filled pit or into the clutches of a predator. Small insects are often too heavy or are unable to climb the meniscus at the edge of

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rock pools and will eventually drown. However, many cave-adapted insects have unique knobs or hairs near the base of each elongated claw and modified behavioral traits that allow them to climb the meniscus and escape. Some of the latter are predators or scavengers, who wait on pools for victims.

in the cavernous rock strata. The view is imperfect because the environment is so foreign to human experience.

Case Study: Hawai‘i Food Web

Other Cave-Like Habitats Cavernous rock strata contain abundant additional voids of varying sizes, which may not be passable by humans. These voids are interconnected by a vast system of cracks and solution channels. The smaller capillary-sized spaces are less important biologically because their small size limits the amount of food resources they can hold and transport. Voids larger than about 5 cm can transport large volumes of food as well as serve as habitat for animals. In terms of surface area and extent, these intermediate-size voids are the principal habitat for specialized cave animals. Many aspects of their life history may occur only in these spaces. Some cave species (such as the earwig, Anisolabis howarthi (Figure 2), and sheet web spiders, Linyphiidae, in Hawaiian lava tubes) prefer to live in crevices and are only rarely found in caves. In addition, cave-adapted animals have been found living far from caves in cobble deposits beneath rivers, fractured rock strata, and buried lava clinker in Japan, Hawai‘i, Canary Islands, Australia, and Europe. These discoveries corroborate the view that cave adaptation and the development of cave ecosystems can occur wherever there is suitable underground habitat. Because these smaller voids are isolated from airflow from the surface, the environment resembles the stagnant air zones of caves. Caves serve as entry points and windows in which to observe the fauna living within the voids

Figure 2 The Hawaiian cave earwig, Anisolabis howarthi Brindel (family Carcinophoridae). Photo by W. P. Mull.

The main energy sources in Hawaiian lava tube ecosystems are tree roots, which penetrate the lava for several decameters; organic matter, which washes in with percolating rainwater; and accidentals, which are surface and soil animals blundering into the cave. Both living and dead roots are utilized, and this source is probably the most important. Furthermore, both rainwater and accidentals often use the same channels as roots to enter caves, so that root patches often provide food for a wide diversity of cave organisms. The importance of roots in the cave ecosystem makes it desirable to identify the major species. This has become possible only recently by using DNA-sequencing technology. The most important source of roots is supplied by the native pioneer tree on young lava flows; Metrosideros polymorpha. Cocculus orbiculatus, Dodonaea viscosa, and Capparis are locally important in drier habitats. Several different slimes and oozes occur on wet surfaces and are utilized by scavengers in the cave. They are mostly organic colloids deposited by percolating groundwater, but some may be chemoautotrophic bacteria living on minerals in the lava. Cave-roosting vertebrates do not occur in Hawai‘i. Native agrotine moths once roosted in caves in large colonies, but the group has become rare in historic times. The composition of the community their colonies once supported is unknown. Feeding on living roots are cixiid planthoppers (Oliarus). Their nymphs suck xylem sap with piercing mouthparts. The blind flightless adults wander through subterranean voids in search of mates and roots. Caterpillars of noctuid moths (Schrankia) prefer to feed on succulent flushing root tips, but they also occasionally scavenge on rotting plant and animal matter. Tree crickets (Thaumatogryllus), terrestrial amphipods (Spelaeorchestia), and isopods (Hawaiioscia and Littorophiloscia) are omnivores but feed extensively on roots. Cave rock crickets (Caconemobius) are also omnivorous as well as being opportunistic predators. Feeding on rotting organic material and associated microorganisms are millipedes (Nannolene), springtails (Neanura, Sinella, and Hawinella), and phorid flies (Megaselia). Terrestrial water treaders (Cavaticovelia aaa) suck juices from long-dead arthropods. Feeding in the organic oozes growing on wet cave walls are larvae of craneflies (Dicranomyia) and biting midges (Forcipomyia pholeter). The blind predators include spiders (Lycosa howarthi, Adelocosa anops (Figure 3), Erigone, Meioneta, Oonops, and Theridion), pseudoscorpions (Tyrannochthonius), rock centipedes (Lithobius), thread-legged bugs (Nesidiolestes), and beetles (Nesomedon, Tachys, and Blackburnia). Most of the cave predators will also scavenge on dead animal material.

540 Ecosystems | Caves

Figure 3 The no-eyed big-eyed hunting spider, Adelocosa anops Gertsch (family Lycosidae) from caves on the island of Kaua‘i. Photo by the author.

Nonindigenous Species Several invasive nonindigenous species have invaded cave habitats and are impacting the cave communities. The predatory guild is the most troublesome, with some species being implicated on the reduction of vulnerable native species. Among these, the nemertine worm (Argonemertes dendyi) and spiders (Dysdera, Nesticella, and Eidmanella) have successfully invaded the stagnant air zone within the smaller spaces. The colonies of cave-roosting moths disappeared from the depredations of the roof rat (Rattus rattus) on their roosts and from parasites purposefully introduced for biological control of their larvae. Many non-native species (such as Periplaneta cockroaches, Loxosceles spiders, Porcellio isopods, and Oxychilus snails) survive well in larger accessible cave passages, where they have some impact, but they appear not to be able to survive in the system of smaller crevices. A few alien tree species also send roots into caves, creating a dilemma for reserve managers trying to protect both cave and surface habitats since their roots support some generalist native species but not the host-specific planthoppers.

Succession Inhabited Hawaiian lava tubes range in age from 1 month on Hawai‘i Island to 2.9 million years on O‘ahu Island. On Hawai‘i Island colonization and succession of cave ecosystems can be observed. Crickets and spiders arrive on new flows within a month of the flow surface cooling. They hide in caves and crevices by day and emerge at night to feed on windborne debris. Caconemobius rock

crickets are restricted to living only in this aeolian (wind-supported) ecosystem and disappear with the establishment of plants. The obligate cave species begin to arrive within a year after lava stops flowing in the caves. The predatory wolf spider, Lycosa howarthi, arrives first and preys on wayward aeolian arthropods. Other predators and scavenging arthropods – including blind, cave-adapted Caconemobius crickets – arrive during the next decade. Under rainforest conditions, plants begin to invade the surface after a decade, allowing the root feeding cave animals to colonize the caves. Oliarus planthoppers arrive about 15 years after the eruption and only 5 years after its host tree, Metrosideros polymorpha. The cave-adapted moth, Schrankia species, and the underground tree cricket, Thaumatogryllus cavicola, arrive later. The cave species colonize new lava tubes from neighboring older flows via underground cracks and voids in the lava. Caves between 500 and 1000 years old are most diverse in cave species. By this time the surface rainforest community is well-developed and productive, while the lava is still young and maximal amount of energy is sinking underground. As soil formation progresses, less water and energy reaches the caves, and the communities slowly starve. In highest rainfall areas, caves support none or only a few species after 10 000 years. Under desert conditions, succession is prolonged for 100 000 years or more. Mesic regimes are intermediate between these two extremes. New lava flows may rejuvenate some buried habitat as well as create new cave habitat.

Perspective The fauna of a large percentage of the world’s cave habitats remain unknown to science, and new species continue to be discovered in well-studied caves. Additional biological surveys are needed to fill gaps in knowledge and improve our understanding of cave ecosystems. Improved methods for sampling the inaccessible smaller voids are needed. The cave environment is a rigorous, high-stress one, which is difficult for humans to access and envision because it is so foreign to human experience. Working in caves can be physically challenging. However, recent innovations in equipment and exploration techniques allow ecologists to visit the deeper, more rigorous environments. In spite of the difficulties of working in the stressful environment, several factors make caves ideal natural laboratories for research in evolutionary and physiological ecology. Since cave habitats are buffered by the surrounding rock, the abiotic factors can be determined with great precision. The number of species in a community is usually manageable and can be studied in total. Questions that are being researched are how organisms

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adapt to the various environmental stressors; how communities assemble under the influence of resource composition and amount; and how abiotic factors affect ecological processes. For example, a potential overlap between cave and surface ecological studies occurs in some large pit entrances in the tropics. The flora and fauna living in these pits frequently experience CO2 levels 25–50 times ambient.

See also: Colonization; Rocky Intertidal Zone; Soil Ecology.

Further Reading Camacho AI (ed.) (1992) The Natural History of Biospeleology. Madrid: Monografias, Museo Nacional de Ciencias Naturales. Chapman P (1993) Caves and Cave Life. London: Harper Collins Publishers. Culver DC (1982) Cave Life. Cambridge, MA: Harvard University Press.

Culver DC, Master LL, Christman MC, and Hobbs HH, III (2000) Obligate cave fauna of the 48 contiguous United States. Conservation Biology 14: 386–401. Culver DC and White WB (eds.) (2004) The Encyclopedia of Caves. Burlington, MA: Academic Press. Gunn RJ (ed.) (2004) Encyclopedia of Caves and Karst. New York: Routledge Press. Howarth FG (1983) Ecology of cave arthropods. Annual Review Entomology 28: 365–389. Howarth FG (1993) High-stress subterranean habitats and evolutionary change in cave-inhabiting arthropods. American Naturalist 142: S65–S77. Howarth FG, James SA, McDowell W, Preston DJ, and Yamada CT (2007) Identification of roots in lava tube caves using molecular techniques: Implications for conservation of cave faunas. Journal of Insect Conservation 11(3): 251–261. Humphries WF (ed.) (1993) The Biogegraphy of Cape Range, Western Australia. Records of the Western Australian Museum, Supplement no.45. Perth: Western Australian Museum. Juberthie C and Decu V (eds.) (2001) Encyclopaedia Biospeologica Vol III. Moulis, France: Socie´te´ de Biospe´ologie. Moore GW and Sullivan N (1997) Speleology Caves and the Cave Environment, 3rd edn. St. Louis, MO: Cave Books. Wilkins H, Culver DC, and Humphreys WF (eds.) (2000) Ecosystems of the World, Vol. 30 Subterranean Ecosystems. Amsterdam: Elsevier Press.

Cellular Automata A K Dewdney, University of Western Ontario, London, ON, Canada ª 2008 Elsevier B.V. All rights reserved.

Introduction Cellular Automata in General History of Cellular Automata

Applications in Ecology Further Reading

Introduction

crucial point is discussed in the final section of this article.

Somewhere between ecology and computer science a nascent science struggles to be born. Cellular automata provide a simple, yet flexible platform for simulating a large variety of phenomena, some of which resemble ecological processes, at least in a wider sense. One thinks of chemical oscillators, seashell patterns, and epidemics, among other things. Whether one is discussing lively chemical solutions, seashell patterns, or epidemics, the question inevitably arises as to what degree cellular automata model ecological processes in a useful (i.e., predictive) manner. This

Cellular Automata in General The term ‘cellular automaton’ hints at the marriage of two concepts, automata and cellular space, the latter being essentially an infinite square lattice. Automata per se have been the subject of a vast amount of research into their computing powers, particularly the languages they produce or recognize. The theory of automata has been a core subject in computer science from the beginning. It