EOLSS – ADAPTATIONS TO LIFE IN MARINE CAVES
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ADAPTATIONS TO LIFE IN MARINE CAVES
Thomas M. Iliffe,
Department of Marine Biology, Texas A&M University at Galveston, USA
Renée E. Bishop,
Department of Biology, Penn State University at Worthington Scranton, USA
Keywords: Anchialine, stygofauna, caves, biodiversity, ecology, adaptation, evolution, behavior,
conservation, endangered species, cave 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. Biogeography
6. Evolutionary origins
7. Adaptation to life in anchialine caves
8. Conservation
Glossary
Bibliography
Biographical Sketches
Summary
Inland (anchialine) and submarine caves in limestone and volcanic rock are extreme
environments inhabited by endemic, cave-adapted (typically eye and pigment reduced) fauna.
Specialized cave diving 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 extinction.
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 years) residence time with
this habitat. Such caves are locally called “cenotes” in the Yucatan Peninsula of Mexico and
“blue holes” in the Bahamas and Belize. Frequently, they possess highly stratified water masses,
with surface layers of fresh or brackish water, separated by a thermo-, chemo-cline from
underlying fully marine, low dissolved waters. Animals restricted to the anchialine habitat show
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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 crustacean 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 crustaceans
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
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The interactions of freshwater, seawater, 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 oxygen 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 hypoxia, there is a high selective advantage for economy of energy
observed in many phyla. Possible adaptations as a result of this selective force are: morphological
features resulting in improved food finding capability, starvation resistance, and reduction in
energy demand via reduced metabolism.
2. Geological origins, age and distribution of anchialine habitats
×
Anchialine caves occur in both volcanic rock and karstic limestone. Lava tube 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 Sistema Sac Actun located on the Caribbean coast of the Yucatan Peninsula in
Mexico and containing 153.5 km of surveyed underwater passages interconnecting at least 111
cenote 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 stalactites and stalagmites occur to depths
in excess of 50 m in coastal limestone caves (Figure 1). Such speleothems 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 sea level
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
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reef 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
tides 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
×
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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
rebreathers (Figure 2), which recycle the diver’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 breathing gas mixtures that replace nitrogen with helium to reduce
the effect of nitrogen narcosis. Since many cave dives are for longer durations and/or to deeper
depths, they frequently involve long decompression.
Figure 2. A cave diver uses a Megalodon closed circuit rebreather with full face
mask to collect a small Typhlatya shrimp from a cave in Yucatan. Rebreathers
recycle expired gas so that no bubbles are produced.
3.2 Physical and chemical characteristics
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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 halocline 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, temperature, 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.
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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).
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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 animal 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,
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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 brood pouch in females. They include 34 species
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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.
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Figure 8. Mictocaris 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
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Mysids are small to medium sized (approximately 3-20 mm), shrimp-like crustaceans including
stygobitic species found in freshwater and anchialine habitats in Africa, 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 South America.
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.
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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 Decapoda). Anomuran crabs
(e.g., hermit, porcelain, mole and sand 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.
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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
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for some time during the Miocene. 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 Holocene carbonate reefs and sediments. Underlying these younger
limestones 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 nature 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 nonrigorous environments. Anchialine habitats on islands and continental margins could be
connected via a continuum of ‘crevicular corridors’ extending from shallow depths to the deep
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sea. However, evidence against a deep-sea origin of cave faunas includes the questionable ability
of deep-sea species to cross the oceanic thermocline, the relatively recent nature of deep-sea
species (due to lack of oxygen in Atlantic bathyal waters during the late Oligocene) and
phylogenetic analyses of morphological characters supporting independent colonization of deepsea 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 arthropods, 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 year. 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.
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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, natural selection 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.
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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 mutation and genetic drift. Features such as eyes and pigment which have
abruptly lost their function and no long protected from what previously would have been lethal
mutations.
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 pressure 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.
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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 lipid 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 buoyancy 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 partial
pressure), a delineation or reduction in the oxygen uptake in the face of declining oxygen
concentrations. 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.
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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 sinkholes 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.
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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 dive light. 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.
Copper 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 concentration 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
rebreather
:a diving apparatus in which all exhaled gas is recycled with carbon
dioxide removed using a chemical scrubber and oxygen added so that no
bubbles are produced
Epigean
:on or near the surface
Flank margin
cave
:cave formed by dissolution at the margin of the freshwater lens, under the
coastal flank of the enclosing landmass
Glycolysis
:first step in cellular respiration 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 solution rather than erosion is the dominant process
Krebs citric acid
cycle
:series of chemical reactions that occur in a cell, second step of three that
involves breaking down glucose into carbon dioxide 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
evolution
:an evolutionary process that results in loss of characters present in the
ancestor species
Speleothem
:mineral deposit formed in caves from the precipitation of calcium
carbonate or calcium sulfate
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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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]