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Home , Blue hole, Mictacea, Oceanic dispersal, Speleothem, Stygofauna

EOLSS – TO LIFE IN MARINE PAGE 1

ADAPTATIONS TO LIFE IN MARINE CAVES

Thomas M. Iliffe, Department of , Texas A&M University at Galveston, USA

Renée E. Bishop, Department of Biology, Penn State University at Worthington Scranton, USA

Keywords: Anchialine, , caves, , ecology, , , behavior, conservation, endangered , diving, evolution, Crustacea, Remipedia, Tethys Sea.

Contents

1. Introduction 2. Geological origins, age and distribution of anchialine habitats 3. Anchialine cave ecology 4. Biodiversity 5. 6. Evolutionary origins 7. Adaptation to life in anchialine caves 8. Conservation Glossary Bibliography Biographical Sketches

Summary

Inland (anchialine) and submarine caves in and volcanic rock are extreme environments inhabited by endemic, cave-adapted (typically eye and pigment reduced) . Specialized technology is an essential tool to investigate this habitat. A number of new higher taxa are represented with some closely related species inhabiting caves on opposite sides of the Earth suggesting an ancient origin. Because many of these species are found only in a single cave, pollution or destruction of caves will result in their .

1. Introduction ×××

1.1 Definition of anchialine and marine caves

Anchialine caves are partially or totally submerged coastal caves in volcanic or karstic limestone terrain that contain tidal, marine waters having a longer (months to ) residence time with this habitat. Such caves are locally called “” in the Yucatan Peninsula of Mexico and “blue holes” in and . Frequently, they possess highly stratified water masses, with surface layers of fresh or brackish water, separated by a thermo-, chemo- from underlying fully marine, low dissolved waters. restricted to the anchialine habitat show EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 2

pronounced morphological, physiological, biochemical and behavioral adaptations and are termed stygofauna or stygobites. In areas such as Yucatan, both freshwater and marine stygofauna inhabit the same caves.

In contrast, marine caves are located either directly on the coast or wholly submerged beneath the sea floor and contain marine waters that freely exchange with the sea on each tidal cycle. The stygophilic fauna of marine caves can also be found in suitable habitats outside of caves and lack specialized adaptations for subterranean life. Moderate to strong tidal currents are present in many marine caves. As a result, encrusting, filter-feeding animals such as sponges, hydroids, anemones, tube worms and even some corals may completely cover all hard surfaces. Other organisms are swept into caves by tidal currents but which only can survive there for short periods of time are termed accidentals. Some species such as fish, lobster and mysids seek shelter within marine caves but must venture out into open waters to feed and are classified as stygoxenes.

Some extensive marine caves extend far and/or deep enough so that a more or less gradual transition in water residences times takes place and conversion occurs to a true anchialine habitat. Similarly, a number of inland anchialine systems have submerged entrances in the sea with significant water exchange occurring in these sections of the cave but with a transition to anchialine characteristics and fauna taking place as distance from the sea increases and impact of tidal exchanging water declines.

1.2 Biological significance

Anchialine cave contain a rich and diverse, endemic, stygobitic fauna, but, due to the technological demands and potential dangers of cave diving, are relatively unstudied. These habitats serve as refuges to “living fossil” organisms, e.g., members of the class Remipedia, and to animals closely related to deep sea species, e.g., the galatheid crab Munidopsis polymorpha. Such cave animals typically possess regressed features including loss of eyes and pigment. For reasons that are as yet unclear, the invertebrate fauna is dominated by and includes the new class Remipedia, plus 3 new orders, 9 new families, more than 75 new genera and 300 new species. This extraordinary degree of novelty qualifies anchialine habitats as uniquely important. Since anchialine species commonly have a highly restricted distribution, often being found only in a single cave system on one island, pollution or destruction of caves will result in their extinction.

Stygobitic anchialine fauna often show highly disjunct biogeographic distributions, inhabiting caves in isolated locations on opposite sides of the Atlantic and Pacific Oceans, as well as in the Mediterranean, and are considered Tethyan relicts. Various hypotheses have been proposed to explain the origin of anchialine fauna. In general, these involve either vicariance (geological) or dispersal (biological) processes. Perhaps molecular genetic comparisons of cave populations from distant locations may help provide data for determining the age and dispersal sequence of anchialine stygobites.

1.3 Adaptation EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 3

The interactions of freshwater, , and limestone in anchialine caves create a unique set of challenges for the organisms that reside there. Stygofauna have adapted to cope with constant low conditions in an energy limited environment. Additionally, the lack of light results in little or no diurnal or seasonal fluctuation in productivity. Without light, organisms receive no visual information for orientation or communication and must function with an absence of timing mechanisms.

Adaptations to marine caves may be morphological, behavioral and physiological. As a result of both food scarcity and , there is a high selective advantage for economy of energy observed in many phyla. Possible adaptations as a result of this selective are: morphological features resulting in improved food finding capability, starvation resistance, and reduction in energy demand via reduced .

2. Geological origins, age and distribution of anchialine habitats ×××

Anchialine caves occur in both volcanic rock and karstic limestone. caves form during volcanic eruptions of basaltic lava. They typically occur relatively close to the earth’s surface and are thus relatively short lived (thousands to a few tens of thousands of years). Anchialine lava tubes can start on land and extend out past the coastline, beneath the seafloor, or can form from submarine eruptions. Anchialine lava tube caves are known from the Canary Islands, Galapagos Islands, Hawaii and Western Samoa. The longest of these is the Jameos del Agua (Atlantida Tunnel) on Lanzarote in the Canary Islands, the submerged portion of which extends 1.6 km out from the coastline, reaching a depth of 50 m.

The most extensive of the known anchialine habitats are solutionally-developed limestone caves that typically contain both fresh and marine waters. Such caves are sometimes referred to as flank margin caves and were formed by mixing dissolution in a fresh groundwater lens. The largest anchialine cave is located on the coast of the Yucatan Peninsula in Mexico and containing 153.5 km of surveyed underwater passages interconnecting at least 111 entrances. Extensive anchialine limestone caves are also known from the Bahamas, Bermuda, Belize, Dominican Republic, and Bonaire in the Caribbean, plus the Balearic Islands and Sardinia in the Mediterranean. Smaller anchialine caves are present on many islands in the Indo Pacific and in Western Australia.

Limestone caves last much longer than lava tubes and can be hundreds of thousands to many millions of years old. Commonly, sizable underwater and occur to depths in excess of 50 m in coastal limestone caves (Figure 1). Such can only form in air indicating that these caves must have been dry and air-filled for long periods of time when glacial sea levels were as much as 130 m lower than today. The last low stand of Ice Age occurred only 18,000 years ago.

Coastal tectonic faults that extend below sea level constitute another form of anchialine habitat. On Santa Cruz in the Galapagos Islands, vertical faults in coastal volcanic rock are locally called “grietas”. Wedged breakdown blocks have partially roofed over submerged portions of grietas so that are in total darkness. Similar faults are present in Iceland. Fault caves also occur in uplifted EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 4

limestone on the island of Niue in the Central Pacific, produce deep chasms containing anchialine pools. The Ras Muhammad Crack in the Sinai Peninsula consists of a water-filled crack in an elevated fossil reef formed by a 1968 earthquake. Many of the ocean blue holes of the Bahamas consist of submarine faults running parallel to the platform edge. Ocean blue holes typically exhibit exceptionally strong, reversing tidal currents created by an imbalance between on opposite sides of the islands.

Figure 1. Cave divers swim between two enormous submerged stalagmites in Crystal Cave, Bermuda. Since such speleothems only form in air by dripping water, their presence in underwater caves is proof that the caves must have been dry and air-filled for considerable periods of time.

3. Anchialine cave ecology ×××

3.1 Diving investigations EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 5

Since anchialine stygobites are commonly found only at significant depths and/or distances from cave entrances, cave diving is an essential component to collection and study of anchialine fauna. Cave diving requires specialized training, equipment and techniques, since a direct assent to the surface is not possible and divers may be hundreds of meters from access to the surface. In case of equipment failure or loss of air supply, cave divers must have readily available backups. Special techniques for cave diving may include the use of side-mounted instead of back-mounted scuba tanks to allow divers to pass through low bedding plane passages. Closed circuit (Figure 2), which recycle ’s exhaled gases, reduce the amount of percolation, i.e., silt dislodged from cave ceiling or walls by exhaust bubbles produced in conventional, and also lessen contamination of the low dissolved oxygen cave waters. Deeper dives, below 40 m depths, require use of special gas mixtures that replace nitrogen with helium to reduce the effect of . Since many cave dives are for longer durations and/or to deeper depths, they frequently involve long .

Figure 2. A cave diver uses a Megalodon closed circuit with full face mask to collect a small Typhlatya from a cave in Yucatan. Rebreathers recycle expired gas so that no bubbles are produced.

3.2 Physical and chemical characteristics EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 6

A high degree of vertical stratification occurs in most anchialine caves (Figure 3). The largest changes in chemical and physical parameters typically occur at the where fresh or brackish water is separated from underlying fully marine waters. On islands and in some continental regions such as Yucatan and Western Australia, freshwater occurs as in the shape of a lens with thickness increase in a direct relationship with distance inland from the coast. In Yucatan for example, the depth of the halocline and corresponding thickness of the freshwater lens, increases from 10 m at 2 km distance inland to 20 m at 10 km.

Figure 3. Depth profiles of salinity, , dissolved oxygen and pH from an anchialine cave, Cenote 27 Steps, in Akumal, Mexico taken on 7 December 2003 using a YSI 600 XLM multi-parameter water quality monitor. Individual measurements, indicated by ‘ symbol, were taken at 4 second intervals between the surface and 26 m water depth.

Water temperature generally increases with depth, while dissolved oxygen decreases. Warmer waters below the halocline could be due to geothermal heating at depth and/or evaporative cooling at the surface. In the lightless interior of caves, there are no plants and hence no photosynthetic oxygen production, while stable and stratified water masses restrict vertical mixing and exchange of oxygen with surface waters. Where deep, water-filled vertical shafts extend to the surface, such as in many cenotes and blue holes, the input of organic matter has resulted in total depletion of dissolved oxygen and resulting anoxic hydrogen sulfide production. A several meter thick, cloud-like layer of hydrogen sulfide occurs just below the halocline and may reduce underwater visibility to near zero, but water clarity improves considerably below the H2S layer. In some caves, dissolve oxygen levels can recover to 1 mg/l or less and populations of stygobitic fauna occur. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 7

A pH minimum generally occurs at the halocline, possibly arising from microbial oxidation of organic matter suspended at the density interface and resulting CO2 production. Increased acidity at the halocline may explain the dissolution of limestone and resulting development of cave passages at this depth.

3.3 Trophic relationships

Through selected studies on morphology and gut contents of stygobitic organisms, it is possible to piece together a picture of energy flow in the anchialine system. An examination of stable isotopes in Mexican caves and diver observations present a more complete picture of the trophic ecology of these systems. There are four potential sources of organic matter in Mexican cave systems: the soil from the surrounding jungle, algae from the cenote pool, chemautotrophic bacteria, and to a much lesser extent, organic matter originating from the marine waters.

The paucity of food in anchialine caves drives organisms toward a generalist diet. Mysids and isopods tend toward omnivory, while ostracoda and thermosbaenaceans occupy the roles of detritivores. Tulumella and Typhlatya have modified appendages that allow them to filter out even the tiniest particles. Remipedes, fish and some amphipods, feed on ostracods, thermosbaenaceans, copepods, isopods, amphipods and shrimp, either as top level predators or as scavengers.

4. Biodiversity ×××

4.1 Fish

Sygobitic anchialine fish (Figure 4) are represented in the Family Bythidae (8 species in two genera from the Bahamas, Cuba, Yucatan and Galapagos Islands), Family Eleotridae (1 species from Northwestern Australia), Family Gobiidae (3 species in two genera from the Philippines and Japan) and Family Synbranchidae (2 species in one genus from Northwestern Australia and Yucatan).

EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 8

Figure 4. The Yucatan cave fish Typhliasina pearsei belongs to the Family Bythitidae. It is widely distributed in freshwater cenotes throughout the Yucatan Peninsula.

4.2 Non-crustacean invertebrates

Although most stygobitic anchialine invertebrates are crustaceans, a variety of non-crustacean invertebrate stygofauna have been described. Anchialine species include 4 sponges, 1 turbellarian, 5 gastropods, 10 annelids, 4 chaetognaths, 1 tantulocarids, and 3 water mites. While some of these species are questionable stygobites, several are clearly cave adapted. The polychaetes Gesiella jameensis from the Canary Islands and Pelagomacellicephala iflffei (Figure 5) from the Caicos Islands and Bahamas spend their time slowly swimming in the cave water column. The chaetognath Paraspadella anops from the Bahamas lacks eyes and pigment.

Figure 5. The polynoid polychaete worm Pelagomacellicephala iliffei inhabits anchialine caves in the Bahamas and Caicos Islands. This fragile is typically observed swimming slowly though the water column.

4.3 Crustaceans

Crustaceans are the abundant and diverse group present in both freshwater and anchialine cave habitats. Within the anchialine Crustacea, the largest numbers of species are represented by amphipods, copepods, decapods, ostracods, isopods, mysids and thermosbaenaceans, approximately in that order.

4.3.1 Remipedes

Remipedes are a class of Crustacea originally described from Bahamian caves in 1981. Although their multi-segmented trunk and paired swimming appendages appear primitive, their head and mouth parts are highly specialized. Remipedes have paired hollow fangs for capturing prey and are among the top predators in the anchialine habitat (Figure 6). They are up to 4.5 cm in length, EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 9

usually colorless and blind, with elongate, centipede-like bodies. Seventeen species of remipedes inhabit frilly marine, oxygen-deficient waters in caves from the Bahamas, Caicos Islands, Cuba, Yucatan Peninsula, Canary Islands and Western Australia.

Figure 6. An undescribed species of Remipedia from the genus Speleonected feeds on a Typhlatya shrimp in a Yucatan cave.

4.3.2 Thermosbaenaceans

Thermosbaenaceans (Figure 7) are small (5 mm or less), eyeless or eye-reduced, anchialine and freshwater peracarid crustaceans with a dorsal in females. They include 34 species EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 10

with a wide distribution in caves and thermal springs around the Mediterranean and Caribbean, as well as Australia and Cambodia.

Figure 7. The thermosbaenacean genus Tulumella includes species inhabiting anchialine caves in the Bahamas and the Yucatan Peninsula.

4.3.3 Mictaceans

Micataceans (Figure 8) are small (3-3.5 mm), eyeless and depigmented, non- predatory crustaceans. This peracarid order is represented by only a single species that inhabits anchialine caves in Bermuda.

EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 11

Figure 8. halope from anchialine caves in Bermuda is the sole species in the Order Mictacea. It is classified as critically endangered on the IUCN Red List.

4.3.4 Bochusaceans

Bochusaceans are very small (1.2-1.6 mm), semi-transparent and eyeless peracarid crustaceans that include two anchialine species from the Bahamas and Cayman Islands, plus two deep sea species.

4.3.5 Copepods

Copepods are a large and diverse group, comprising the most common animals in marine plankton. Platycopioid, misophrioid, cyclopoid, harapacticoid, and calanoid (especially epacteriscid and ridgewayiid) copepods inhabit anchialine caves in tropical regions around the globe. They are small (typically 1-2 mm long) and have a short, cylindrical body with head and thorax fused into cephalothorax. Most are planktonic filter-feeders, but some such as the harpacticoids and cyclopoids are benthic, while epacteriscids are predators on other copepods.

4.3.6 Ostracods

Ostracods are small (approximately 0.5-2 mm), benthic or planktonic bivalve crustaceans. Halocyprid ostracods (Figure 9) include anchialine species with a distribution and co-occurrence similar to that of remipedes. More than 300 species of podocopid ostracods have been found in springs, caves and anchialine habitats.

Figure 9. The halocyprid ostracod genus Spelaeoecia inhabits anchialine caves in Bermuda, the Bahamas, Yucatan Peninsula, Cuba and Jamaica.

4.3.7 Mysids EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 12

Mysids are small to medium sized (approximately 3-20 mm), shrimp-like crustaceans including stygobitic species found in freshwater and anchialine habitats in , the Caribbean, Mediterranean, and India. Their distribution suggests that they were stranded in caves by lowering of sea level in the Tethys and Mediterranean. Recent molecular phylogenies of the mysids suggest that a new order be created for the stygiomysids (Figure 10) which inhabit caves in the Caribbean and Italy.

Figure 10. The mysid genus Stygiomysis is widely distributed throughout the Caribbean but also inhabits a cave in southern Italy.

4.3.8 Isopods

Isopods have a dorsoventrally compressed body (flattened from top to bottom) and occur in terrestrial, freshwater and marine cave habitats. Stygobitic isopods range from several millimeters to several centimeters in length. Anthurid isopods occur in anchialine and freshwater caves in the Canary Islands, Caribbean and Indian Ocean islands, Mexico and . Asellot isopods inhabit anchialine and freshwater caves in the Caribbean, Europe, Galapagos, India, Indonesia, Japan, Malaysia, North and Central America and Polynesia. Cirolanid isopods (Figure 11) have been found in freshwater and anchialine caves clustered in Mexico and the Caribbean as well as in Europe and the Mediterranean. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 13

Figure 11. The cirolanid isopod Bahalana caicasana is known only from two caves in the Caicos Islands at the southern end of the Bahamas archipelago.

4.3.9 Amphipods

Amphipods have a laterally compressed body (flattened from side to side) and occur in freshwater and marine cave habitats. Stygobitic representatives are present in the bogidiellid, crangonyctid, hadziid and niphargid families of the amphipod suborder Gammaridea. They are very widely dispersed with large numbers of species inhabiting caves in Central and Southern Europe, the Mediterranean, eastern and southern North America, and the Caribbean.

4.3.10 Decapods

Decapods possess five pairs of pereiopods or legs (hence the name ). Anomuran crabs (e.g., hermit, porcelain, mole and crabs) inhabit a freshwater cave in Brazil and an anchialine lava tube in the Canary Islands. Brachyuran crabs (i.e., true crabs) are widely distributed from caves in the tropics and subtropics. Stygobitic crayfish are present in caves in North America and Cuba. Caridean shrimp (Figure 12) include numerous freshwater and anchialine species from caves mostly in tropical latitudes. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 14

Figure 12. The hippolytid shrimp Parhippolyte sterreri inhabits anchialine caves in Bermuda, the Bahamas, and the Yucatan Peninsula, while the genus Parhippolyte includes two other species widely distributed in anchialine caves and pools in the Indo-South Pacific region.

4.3.11 Other crustacean stygofauna

One anchialine tantulocarid, an exceptionally tiny (total body length 94 μm) ectoparasite on a harpacticoid copepod, occurs in the Canary Islands. One species of stygobitic nebaliacean inhabits anchialine caves in the Bahamas and Caicos Islands. Several species of cumaceas and tanaidaceans have been collected from anchialine caves in Bermuda and the Bahamas but it is not clear whether they belong to the stygofauna.

5. Biogeography ×××

Upon examining the biogeography of anchialine fauna, extraordinary patterns are evident. A number of anchialine genera, including for example the remipede Lasionectes, ostracod Danielopolina, thermosbaenacean Halosbaena, and misophrioid Speleophria, inhabit caves on opposite sides of the Earth and are believed to be Tethyan relicts whose ancestors inhabited the Tethys Sea during the Mesozoic. Some anchialine taxa are represented in the Mediterranean, but others, notably remipedes and the thermosbaenacean Halosbaena, are absent. The presence of anchialine taxa at all in the Mediterranean is remarkable considering that it was completely dry EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 15

for some time during the . The aytid shrimp Typhlatya shows an especially interesting distribution with 17 know species inhabiting freshwater and anchialine caves in the Mediterranean region, Bermuda and Ascension Island, a number of locations in the Caribbean including Cuba and Yucatan, and the Galapagos Islands. The shrimp family Procaridae contains one genus with species in mid-Atlantic and Caribbean, as well as Hawaii.

Based on species’ abundance, the Bahamian archipelago appears to have been a possible center of origin for anchialine fauna. Among the Remipedia, 13 out of a total of 17 described species inhabit caves in the Bahamas, while among anchialine halocyprid ostracods, Bahamian species account for 4 out of 11 Danielopolina, 6 out of 11 Spelaeoecia and all 8 species of Deeveya.

The Bahamas consist of a series of broad, shallow-water, highly karstified, carbonate platforms rising abruptly from the deep sea. The islands and cays consist of Pleistocene limestone covered by a thin veneer of carbonate reefs and sediments. Underlying these younger is a continuous section of Tertiary and Cretaceous limestones and dolomites exceeding 11 km in thickness. If the position of the tectonic plates prior the development of the Atlantic Ocean are reconstructed, virtually all of the Bahamas overlap onto the African continent and its continental shelf. This suggests that the Bahama platform developed over oceanic crust during the earliest phase of the creation of the Atlantic. The extended shallow water history of the Bahamas, coupled with the cavernous of the limestone, may help to explain its rich and diverse anchialine fauna.

6. Evolutionary origins ×××

A number of theories have been proposed to explain the trans-oceanic distribution of many anchialine taxa. The Vicariance Model suggests that plate tectonics served as a mechanism for the dispersal of anchialine fauna. This model mainly describes the ‘Tethyan track’ of ancient taxa which were rafted on the drifting continents to their present positions. However, the existence of anchialine fauna on mid-ocean islands such as Bermuda, Ascension and Hawaii that have never been part of, or closer to, a continent cannot be explained by this mechanism.

The Regression Model suggests that sea-level regressions, caused by tectonic uplift or eustatic glacial lowering of sea levels, ‘stranded’ crevicular or interstitial marine littoral species which subsequently adapted to brackish or freshwater conditions. This is supported by the observed correlation between the distribution patterns of numerous, marine-derived cave organisms and the position of shorelines during the Late Mesozoic or Tertiary seas. Nevertheless, the presence of anchialine fauna in caves that were completely dry and air-filled (as evidenced by their now submarine speleothems) less than 10,000 years ago indicates that these animals can migrate vertically with raising post-glacial sea levels. Also, small islands such as Bermuda offer little chances for marine species to be stranded.

A Deep-Sea Origin has been proposed for some anchialine species having close relatives that inhabit bathyal depths. Both caves and the deep sea are old, climatically stable, lightless and non- rigorous environments. Anchialine habitats on islands and continental margins could be connected via a continuum of ‘crevicular corridors’ extending from shallow depths to the deep EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 16

sea. However, evidence against a deep-sea origin of cave includes the questionable ability of deep-sea species to cross the oceanic , the relatively recent nature of deep-sea species (due to lack of oxygen in Atlantic bathyal waters during the late ) and phylogenetic analyses of morphological characters supporting independent colonization of deep- sea and anchialine habitats.

The Active Migration Model involves the inland dispersal and colonization of subterranean habitats by expansionistic marine species with a high degree of salinity tolerance. This process is independent of climatological and geological variations.

Passive Oceanic Dispersal of larval and/or postlarval stages of anchialine species by currents could explain the wide distribution of some anchialine shrimp species within the Indo-Pacific. Rafting on floating objects, e.g., wood, algae, kelp and coconuts, or on mobile and migratory animals, e.g., sea turtles, fishes and larger , could disperse anchialine species, even those without a free-larval stage. But oceanic dispersal is unlikely for many anchialine groups which produce few offspring and/or have narrow physiological tolerances.

7. Adaptation to life in anchialine caves ×××

7.1 Behavioral adaptations

Behavioral adaptations are the most immediate adaptations for survival and colonization in cave systems. Cave organisms, in particular amblyopsid cave fish, use a glide and rest technique to conserve energy in their search for food. Remipede locomotion is also designed for the economy of movement. Remipedes swim relatively slowly, using less energy for the same distance than if they swam at higher speeds. The power stroke produces drag by individual legs but the recovery stroke is completed with the legs folded with other legs to reduce water resistance.

The stygobitic galatheid crab Munidopsis polymorpha (Figure 13) inhabiting an anchialine lava tube in the Canary Islands has a number of specialized behaviors. These small crabs are most abundant in a dimly illuminated pool where they hide in rock crevices during the day but come out at night to feed on diatoms. Due to the large numbers of individuals in this pool, they spread in an almost regular pattern determined by the length of the second antenna. Munidopsis remain aggressive throughout the . They detect intruders from water movements and attack with extended chelipeds. Male crabs are attracted by a molting hormone released by females. To prevent the females from fleeing, males rhythmically move their chelipeds as they approach, until the female responds by vibrating one of her chelipeds. The male then seems to turn the female over on their back to initiate insemination. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 17

Figure 13. The galatheid crab Munidopsis polymorpha inhabits an anchialine lava tube on Lanzarote, Canary Islands. It uses its large cheilipeds to pluck diatoms off rock surfaces in a dimly illuminated portion of the caves.

In fresh water hypogean habitats, some cave fish and salamanders exhibit reduced territorial and antagonistic behavior as well as disturbance resistance.

7.2 Morphological adaptations

7.2.1 Regressive features

The loss of features that have no longer have a function, such as eyes and pigment in organisms from the cave environment, is regarded as regressive evolution (Figure 14). There are two main theories explaining the driving force for regressive evolution. In an environment with a depauperate food supply, should favor reallocating energy from unused features such as eyes and pigment to growth and survival. Examining a simplification of the energetics equation demonstrates this phenomenon: I = G + E+ M. In this equation, I represents the energy that must be ingested, G is growth, either in development of features or reproduction, E is excretion and M is the energy involved in metabolism. Any reduction in the energy demands on the right side of the equation will result in the need for less food or an energy reserve that can be allocated to reproduction. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 18

Figure 14. The amphipod Pseudoniphardus grandimanus from Bermuda caves is eyeless and colorless. Its closest relative’s inhabit inland groundwater around the Mediterranean basin, along the Atlantic coast of Portugal and Spain, in the Azores, Canary and Balearic Islands, and Morocco and France.

A second explanation is that regressive evolution may be the result of non-selective processes such as neutral and . Features such as eyes and pigment which have abruptly lost their function and no long protected from what previously would have been lethal .

Unfortunately, there are very few experimental data demonstrating the theory of energy economy by character reduction on stygobites and none applied to anchialine stygobites, yet the anchialine environment is dominated by blind, de-pigmented organisms.

7.2.2 Constructive features

In the case of constructive features, priority is given to life history, metabolism, development and starvation resistance, with sensory development such as mechano- and chemo- receptors being subordinate. For troglomorphy to occur, two factors must be present: 1. selective in favor of the development; 2. genetic, physiological or behavioral ability of the organism to respond to the selective pressure. A prerequisite for constructive traits is their genetic availability in epigean forms — if traits are not present in epigean ancestors, they will not be present in hypogean descendants. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 19

There are several areas of the body where constructive features occur. In crustaceans, appendages may be elongated, in particular the antennae, and in fish, the head may become enlarged or flattened. Corresponding to the morphological changes, there is an increased sensitivity to chemical and mechanical stimulants. As a result of compensatory enhancement of extraocular senses, the signal processing structures in the brain are altered.

7.3 Physiological adaptations

7.3.1 Adaptations to a low food environment

Food in the stygobitic environment may be in general scarce or at best patchy, therefore, the stygofauna need to cope with temporal periodicity of food availability and potentially tolerate long periods of starvation. This is done through adaptations, in particular accumulation and energy economy.

An examination of the proximate composition of anchialine organisms reflects their adaptations to the cave environment. The energy content of lipid per gram is approximately two times that of carbohydrate or protein resulting in more energy to fuel the metabolism. In comparison with mesopelagic crustaceans, anchialine crustaceans sacrifice protein mass for increased lipid stores.

Increased lipid stores may serve a two-fold purpose in some of the stygobites. Lipid provides neutral without energy expenditure. Lipid globules observed throughout the bodies of remipedes also can serve as an energy reserve when food is limiting and facilitate a substantial reduction in activity. The combination of lower metabolic rates and lower energy-density allows the stygobites to allocate a greater fraction of their ingested food energy to growth, much like deeper-living midwater fishes do.

Anchialine stygobites tend to be more diminutive than their epigean counterparts. Their small size is a mechanism for energy economy. The metabolic rate of organisms is not directly proportional to body mass but related to mass by the equation: Metabolism = aMb; where a is the intercept, M is the body mass and b is the slope. Small overall body size of stygobites provides the advantage of less energy needed overall, but necessitates a greater energy demand per unit of mass.

7.3.2 Adaptation to hypoxia and anoxia

Hypogen organisms tend to have substantially lower oxygen consumption rates than their epigean phylogenetic relatives. In addition, anchialine crustaceans have no critical p02 (oxygen ), a delineation or reduction in the oxygen uptake in the face of declining oxygen . These organisms are oxyregulators and are capable of maintaining constant oxygen consumption under hypoxic conditions as opposed to many epigean crustaceans that show a significant decline in oxygen consumption with declining oxygen concentrations. This regulation indicates better adaptation to low 02 concentrations and allows the organisms to maintain an aerobic metabolism for longer periods of time before switching to the less efficient anaerobic metabolism. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 20

Remipedes may also be using strategies similar to Gnathophausia ingens, a deep-sea mysid, to efficiently extract oxygen from their environment. Remipedes do not have specialized respiratory structures such as gills, but their broad paddle-like trunk appendages could serve as respiratory surfaces. Several species of remipede, including Godzilliognomous frondosus, have been observed pumping water anally. Anal intake of water has been reported for a number of small crustaceans and is considered to be a respiratory adaptation particularly for organisms inhabiting water deficient in dissolved oxygen. Remipedes use hemocyanin to further facilitate the utilization of oxygen.

7.4 Biochemical adaptations

As mentioned earlier (see Physical and Chemical Characteristics), the anchialine environment is frequently hypoxic and in some areas anoxic. Many organisms are capable of obtaining energy when faced with a reduction or absence of oxygen but few are able to survive indefinitely without a return to oxygen. When the oxygen supply becomes inadequate, organisms switch to anaerobiosis to compensate for ATP demand. This can happen if the ATP demand in an organism exceeds aerobic capacity due to physiological activity (functional anaerobiosis) or if oxygen availability is reduced to values preventing the maintenance of cell functions aerobically. The latter is referred to as environmental anaerobiosis.

Organisms are able to conserve their energy stores during periods of environmental anaerobiosis by a loss in physiological functions such as motility, ingestion, and digestion, combined with a dramatic depression of their energy (ATP) demand. There are three ways organisms can increase their metabolic efficiency: 1. maximize the amount of energy they get from their food; 2. maximize the energy they get for the amount of 02 used; 3. maximize the amount of work they can do for each unit of energy (ATP).

When oxygen is temporarily unavailable to serve as the terminal electron acceptor in the electron transport chain, many organisms switch to anaerobic glycolysis. But anaerobic glycolysis is a fundamentally inefficient metabolic strategy, generating maximally 15% of the aerobic potential of an organism. For organisms that remain in a hypoxic environment indefinitely in a food poor environment, this would be particularly inefficient route to follow.

By examining the activities of enzymes critical to metabolism and energy conversion, it is possible to determine the rate at which food is converted to cellular energy. Citrate synthase (CS), located at the beginning of the Krebs citric acid cycle, is an indicator of an organism’s maximum aerobic potential, or how fast an organism can convert glucose to energy. Malate dehydrogenase (MDH) plays a dual role in facultative anaerobes. In the presence of oxygen, malate dehydrogenase functions in the Krebs citric acid cycle to oxidize pyruvate completely to CO2 and H20. In anaerobic conditions, malate dehydrogenase can catalyze reactions in the opposite direction, resulting in the generation of more ATP than by glycolysis alone. Lactate dehydrogenase (LDH) is the terminal enzyme in glycolysis that contributes to both aerobic and anaerobic metabolic pathways and serves as indicator of glycolytic potential.

In crustaceans, there is a direct correlation between an organism’s ability to withstand temporary anaerobiosis and values of MDH:LDH; the higher the ratio, the greater an organism’s tolerance EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 21

to hypoxia. To maximize the amount of ATP obtained per meal, there needs to be a shift toward aerobic (high ATP yield) over anaerobic (low ATP yield) pathways. One way to do this is to use malate dehydrogenase.

All anchialine organisms examined so far have been anaerobically poised with LDH:CS values greater than one. Remipedes were consistently found to have the lowest CS activities indicating a reduced reliance on aerobic metabolism. Additionally, MDH:LDH were also consistently greater than one. Anchialine organisms are obtaining more energy using MDH than through glycolysis alone, indicating a biochemical adaptation to the cave environment.

8. Conservation ××× Over the last 25 years, more than 400 new species of anchialine stygobites have been discovered and described. A high percentage of these species are known only from a single cave or cave system. Even within caves, species are characteristically found only at specific depths or locations as defined by a narrow range of environmental parameters. In many parts of the world, tourist developments, limestone quarries and groundwater pollution are either destroying or grossly polluting numerous caves, resulting in extinction of untold numbers of species.

Anchialine species qualify for inclusion on endangered species lists due to their limited distribution and the declining environmental quality of their habitat. In Bermuda, 25 cave species are on the IUCN Red List of endangered species. Other cave species from the Yucatan Peninsula are on the official Mexican list of threatened and endangered species.

Maintaining groundwater quality is essential to the environmental health of the subterranean environment. For example, the small oceanic island of Bermuda is the third most densely populated country in the world and has the largest number of private cesspits per capita. Disposal of sewage and other waste water into cesspits or by pumping down boreholes is contaminating the ground and cave water with nitrates, detergents, toxic metals and pharmaceuticals; depleting the very limited amounts of dissolved oxygen in cave water; and generating toxic levels of hydrogen sulfide.

Some ocean caves such as the Blue Holes of the Bahamas have strong tidal currents sweeping through them for very considerable distances. In one such cave, plastic bottles and other trash have been observed littering the floor of the cave nearly a mile back into previously unexplored passage. Far too many caves and are viewed as preferred locations for the dumping of garbage and other waste products.

Another serious environmental problem concerns the destruction of caves by limestone quarries (Figure 15) or construction activities. Half a dozen or more Bermuda caves have been totally destroyed by two limestone quarries which produce crushed aggregate for construction purposes. Untold other caves have been lost to enormous limestone quarries in the Yucatan Peninsula. Many caves have been filled and built over by golf courses, hotels and housing developments in Bermuda. Recently, a series of luxury town homes were built directly on top of the largest cave lake in Bermuda. EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 22

Figure 15. Limestone quarries such as this one from Bermuda have destroyed numerous caves. A remnant of a cave can be seen in the cliff face in the center of the photograph, while Admiral’s Cave, one of the largest and most historic in Bermuda, is located on the hillside to the right of the quarry.

Sometimes even seemingly innocent activities can threaten caves and cave animals. Along the Caribbean coast of the Yucatan Peninsula, many open water cenote pools are inhabited by freshwater fish. Some of these fish have learned to follow divers into caves, moving in front of the dive team and voraciously darting in to consume any animals that are illuminated by the beam of a . Considering the many thousands of cave divers who use these systems each year, it is not surprising that the caves most heavily visited by tourist divers are now essentially devoid of life.

Even the gas exhaled by divers may have adverse effects on cave animals. Since anchialine caves waters typically contain extremely low levels of dissolved oxygen, exhaust bubbles from open circuit scuba could have profound effects on the cave ecosystem. Several anchialine caves in Western Australia with unique fauna are currently off limits to open circuit divers and may only be visited by those using rebreathers.

Some anchialine caves in Bermuda, the Canary Islands and Mallorca have been developed into commercial tourist attractions. Unfortunately, many of the tourists visiting these sites have viewed the deep clear water cave pools as natural wishing wells in which to throw a coin or two. coins tend to rapidly deteriorate and dissolve in salt water, producing high levels of toxic EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 23

copper ions in the cave waters. In one such cave in the Canary Islands, the endemic crab Munidopsis polymorpha has show a marked decline in abundance over the last decade or more, probably in response to high levels of copper in the cave water.

Glossary ×××

Accidentals :animals accidentally fallen or washed into caves but not able to survive there for long

Anaerobiosis :cellular processes necessary for supporting life that occur without oxygen

Anchi(h)aline :tidal, marine or brackish water bodies, existing either in caves or as open pools which show subsurface hydrologic connections to the sea

Anoxic :without oxygen, or where the oxygen is too low for organisms to utilize

Benthic :bottom dwelling in an aquatic environment

Blue hole :water-filled sinkholes in Belize and the Bahamas, occurring both on land and beneath the sea floor

Cave :a natural passage into the earth

Cenote :bodies of water contained in natural cavities within limestone bedrock, especially in the Yucatan Peninsula of Mexico

Cheliped :decapod appendage that ends in a pincer-like structure

Closed circuit :a diving apparatus in which all exhaled gas is recycled with carbon rebreather dioxide removed using a chemical scrubber and oxygen added so that no bubbles are produced

Epigean :on or near the surface

Flank margin :cave formed by dissolution at the margin of the freshwater lens, under the cave coastal flank of the enclosing landmass

Glycolysis :first step in cellular where glucose is broken into 2 pyruvate, can occur without the presence of oxygen

Halocline :area of rapid vertical changes in salinity

Hypogean :beneath the earth’s surface EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 24

Ilypoxic :oxygen present but at extremely low concentrations

Karst :terrain in which rather than erosion is the dominant process

Krebs citric acid :series of chemical reactions that occur in a cell, second step of three that cycle involves breaking down glucose into and water

Lava tube :natural conduits through which lava travels beneath the surface of a lava flow; when the eruption stops, lava in the tube system drains downslope and leaves tunnels beneath the ground

Living fossil :organisms which have primitive features, no close living relatives, limited geographic distribution and small population sizes

Marine cave :caves on the coastline or in the sea floor containing marine waters that freely exchanges with the sea on each tidal cycle

Oxyregulator :organism whose oxygen consumption rate remains constant with declining environmental oxygen levels

Planktonic :organisms that drift or weakly swim in a freshwater or saltwater environment

Regression :retreating sea level converting marine to freshwater habitats

Regressive :an evolutionary process that results in loss of characters present in the evolution ancestor species

Speleothem : deposit formed in caves from the precipitation of or

Stygobite :obligatory aquatic organisms that show some sort of specialization to the underground environment

Stygofauna :aquatic fauna inhabiting the subterranean environment

Stygophile :aquatic organisms that can live in caves but is also found in suitable habitats outside them

Stygoxenes :aquatic organisms that inhabit caves but regularly come out, especially to feed

Tethys Sea :a Mesozoic era ocean that existed between the continents of Gondwana (Antarctica, South America, Africa, Australia and India) and Laurasia (North America, Europe and Asia) EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 25

Troglomorphy :process of adaptation to the cave environment usually involving the reduction or loss of eyes or pigment

Vicariance :separation or division of a group of organisms by a geographic barrier resulting in differentiation of the original group into new varieties or species

Bibliography ×××

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Culver, D.C. (1982). Cave Lfe. Harvard University Press, Cambridge, Massachusetts. [This book integrates empirical knowledge of cave-dwelling organisms with basic principles of ecology and .]

Culver, D.C., T.C. Kane, & D.W. Fong (1995). Adaptation and Natural Selection in Caves, Harvard University Press, Cambridge, MA. [Focusing on the amphipod Gammarus minus, this book shows that cave dwelling animals can provide a valuable empirical model for the study of evolution and adaptation.]

Hochachka, P.W., & P.L. Lutz (2001). Mechanism, origin and evolution of anoxia tolerance in animals. Comparative Biochemistry and Physiology B 130:435-459. [This article is a review of the hypoxia detection and tolerance evolution in turtles and fish.]

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Iliffe, T.M. (1991). Anchialine cave fauna of the Galapagos Islands. In: Galapagos Marine Invertebrates, M.J. James, ed., Plenum Press, New York, p. 209-231. [Biodiversity, ecology and evolutionary origins of anchialine fauna in the Galapagos Islands.]

Iliffe, T.M. (2000). Anchialine cave ecology. Pages 59-76 in: Ecosystems of the World. 30. Subterranean Ecosystems, H. Wilkens, D.C. Culver, & W.F. Humphreys (eds.), Elsevier Science, Amsterdam. [Distribution, hydrological properties and biodiversity of anchialine habitats.]

Iliffe, T.M. (2004). Anchialine caves, biodiversity in. Pp. 24-30 in Encyclopedia of Caves, D.C. Culver and W.B. White, eds., Elsevier, Burlington, MA. [Biodiversity, adaptations and biogeography of anchialine fauna.] EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES PAGE 26

Parzefall, J. (1992). Behavioural aspects in animals living in caves. Pages 325-376 in: The Natural History of , AT. Camacho (ed.), Museo Nacional de Ciencias Naturales, Madrid. [Comparison of behavioral patterns in hypogean populations and their epigean relatives.]

Parzefall, J. (2000). Ecological role of aggressiveness in the dark. Pages 22 1-228 in: Ecosystems of the World. 30. Subterranean Ecosystems, H. Wilkens, D.C. Culver, & W.F. Humphreys (eds.), Elsevier Science, Amsterdam. [Comparison of aggressive competition for food, mates and space in hypogean and epigean populations.]

Pohlman, J.W., L.A. Ciftientes, & T.M. Iliffe (2000). Food web dynamics and biogeochemistry of anchialine caves: a stable isotope approach. Pages 345-357 in: Ecosystems of the World 30. Subterranean Ecosystems, H. Wilkens, D.C. Culver, & W.F. Humphreys (eds.), Elsevier Science, Amsterdam. [Use of stable isotopes to investigate trophic structure and ecology of anchialine fauna.]

Riedel, R. (1966). Biologic der Meereshohlen. Paul Parey, Hamburg & Berlin, 636 pp. [This lavishly illustrated monograph is the first comprehensive treatment of the biology of submarine caves.]

Romero, A., ed. (2001). The Biology of Hypogean Fishes. Dordrecht: Kluwer. [This volume contains 29 papers dealing with the ecology and evolution of cave dwelling fish.]

Sket B. (1996). The ecology of the anchihaline caves. Trends in Ecology & Evolution, 11:221- 225. [Ecology and adaptations of anchialine fauna with special reference to abiotic conditions of the cave habitat.]

Biographical Sketches ×××

Thomas M. Iliffe is a Professor of Marine Biology at Texas A&M University at Galveston. His main research interest is diving based biodiversity, ecology and conservation investigations of anchialine and marine caves.

Renée E. Bishop is an Assistant Professor of Biology at Penn State University at Worthington Scranton. Her research interests involve the ecological physiology of organisms in extreme environments.

To cite this chapter Thomas M. Iliffe and Renée E. Bishop, (2007), ADAPTATIONS TO LIFE IN MARINE CAVES, in Fisheries and Aquaculture, [Ed. Patrick Safran], in Encyclopedia of Life Support Systems (EOLSS), Developed under the Auspices of the UNESCO, Eolss Publishers, Oxford, UK, [http://www.eolss.net] [Retrieved September 25, 2007]