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My latest paper...the first step to writing up my report on my cute little cave worms

Description of Physiological and Ecological Characteristics of Non-Sulfide Cave Dwelling Animals using Garner Cave: Metaline Falls Washington as a Model

Cave systems are unique environments on the earth, that hold many benefits to those animals that can overcome the challenges. These environments are appreciated by scientists for their unique ability to act as simple natural laboratories for studying communities in toto. (Poulson & White 1969; Culver et al., 2000). They can also work to test hypotheses on evolutionary, ecological and bio-geographic processes (Peck, 1981). Studying evolution in caves can also give insight into the two other environments which are known to be highly stable, the lowland tropics and the deep sea (Poulson & White, 1969). Another important reason to study cave systems is, the aquatic species are highly sensitive to groundwater pollutants and can therefore be used as indicators of the quality of groundwater (Culver et al., 2000). Gardner Cave, in north-eastern Washington, and other small caves are especially important as the urbanization of many of the large rural caves in the United States increases (Poulson & White, 1969).

Cave systems are much more common than once thought, in the US alone there have been over 45,000 caves reported and it is likely that there are many more not yet found because they are entrance-less or two small for human entry (Christman & Culver, 2001). As a whole, karst areas represent 15% of the Earths surface (Pipan & Culver, 2007). Despite the quantity of habitats as a whole, obligate cave species are relatively isolated, from one another and from new cave habitats. As of 2001 there were 1000 described species and subspecies known only from caves and associated subterranean habitat, 973 of those species and subspecies are found in the US (Christman & Culver, 2001). One study by Christman and Culver (2001) showed that of these 973, 61% were located in only one country and 23% were located in only one state.


Although they are relatively stable environments, caves do tend to have rhythms. Many caves breath exhaling cave air from their mouths during summer and inhaling colder, drier air in winter (Barr, 1967). This, and the late winter early spring flooding which many caves experience, is the closest permanently cave-dwelling species come to seasons (Barr, 1967). In north-eastern Washington typically has the highest precipitation in the spring, foresters report the cave rim-pools being full in the late winter through late spring and being completely dry by the beginning of fall. Commonly holes in the cave roves to the surface, and wind at the surface, can cause a chimney effects which changes the barometric pressure inside the caves (Poulson & White, 1969). Gardner Cave has a few small entrances to the surface that are frequented by wood rats; although the change in barometric pressure has not been studies it is likely to be affecting the system.


The sections of the caves are separated by the amount of light is present. The entrance having the most light and is populated by mostly surface animals. The twilight zone, at low light, has the largest and most diverse cave fauna. The deep interior is where the unique aspects of the cave environment and its obligate fauna appear (Poulson & White, 1969). The twilight zone is thought to be the most inhabited because it offers the organic material that is washed in or brought in by pack rats and bats concurrently with the stability and protection of the cave environment (Poulson & White, 1969). Gardner Cave's main entrance is a sink straight down then a 90 degree turn into the main portion of the cave. This configuration creates a very short twilight zone, which could partially be the cause the lack of biological diversity within.


Some organisms take full advantage of the benefits of the cave habitat. The primary benefit of karst habitats is their stability. The overall climate of the cave interior is much less variable than surface environments (Poulson & White, 1969). The air is humid regardless of altitude or latitude (Poulson & White, 1969). The acidity of the water in the cave is maintained at a range of 6.4 to 6.7 in most non-sulfide caves (Wetzel et al., 1999). The temperature inside of caves is very stable at approximately the mean annual temperature of the region in which the cave is located (Barr, 1967). Gardner cave is a constant 5.6 degrees Celsius year round, for example.

Despite these benefits there are many obstacles for animals to overcome before they can take advantage of them. Most notably is the absence of light in most of the cave system, this leads to an absents of the most primary producers. Some caves do have primary producers in the form of chemosynthetic autotrophs, but for most, like Gardner, organic material must be imported from the surface (Barr, 1967). Animals at continually move organics into the cave from the surface, such as bats, are key to the community. Decomposers feed on the guano which supplies food for detritus-feeding animals which are then eaten by predators (Barr, 1967). In general the highest number of species is found in the areas of the cave that have the greater amount of organic matter, such as the oligochaetes studies by Wetzel et al (1999) which were primarily found in a well inside the cave and littoral zone, which were both shown to have the highest organics of the available habitats. Also the juvenile stages of blind amphipods studied by Barr (1967) burrowed extensively to eat the clay in the bottom of cave pools.


There is also the problem with the lack of sound, in the majority of caves; there is an unusually high relative humidity which, except near entrances, is accompanied by an exceptionally low rate of evaporation (Barr, 1967). With smaller caves like Gardner the lack of habitat can be a problem Christman and Culver (2001) showed that habitat availability influenced species richness. Compared to the surface and other habitats there is a relatively small number of species and low total biomass involved in even the most complex cave community (Barr, 1967). Often the diversity is related to how interconnected the caves are to one another (Christman & Culver, 2001), how open they are to invasion from the surface, and the balance between colonization and extinction (Poulson & White, 1969). Sub-surface aquatic habitats typically have greater connectivity than sub-surface terrestrial habitats because of the water table flowing between caves (Christman & Culver, 2001). Another factor related to species richness is the geologic history of the cave (Poulson & White, 1969). For example norther caves like Gardner we covered in ice during the last ice age so there has been a relatively short amount of evolutionary time for organisms to invade and adapt. These caves would be expected to have less richness and fewer obligate cave-dwellers. A lack of diversity is not always a problem for a community food supply is usually negatively correlated with diversity (Poulson & White, 1969).


Not only is there a small number of species; simultaneously, the population of each species is small. When speciation happens between the cave-dwellers and their surface ancestors gene flow is often greatly reduced leading to low genetic diversity in cave-dwellers (Christman & Culver, 2001). Barr (1967) studied the speciation of beetles in limestone caves, finding that geographic speciation lead to the smaller geographic ranges in limestone with very thin fissures connecting the cave system, and greater where there are broad, continuous caverniferous limestone. So the less access the beetles had to each other the greater the chance of speciation.
In many habitats temperature is a significant environmental parameter, but this is fairly constant in caves. There, the evaporation rate can be the most significant parameter (Barr, 1967). An example of this stressor is shown near the entrance of Mammoth Cave, where the evaporation rate during the winter is nearly 200 times the rate in mid-summer (Barr, 1967). This high evaporation rate can lead to the dehydration of organisms living in this zone causing harmful cellular shrinkage, cellular proteins denaturation and the cellular membranes losing their normal conformation (Maraldo et al. 2009).
A more modern stressor for cave-dwellers is the tourist industry. Gardner Cave is open for tours four times a day, for thirty minutes each, from May to September. Animals which are only winter dwellers of the cave such as bats are not directly disturbed but invertebrates that live there year round may be affected. Humans are a source of organic debris carried in from the surface and also litter, such as plastic and fibers. In other caves fungal diversity is low in heavily trafficked sites, and increases in moderately visited sites, this may or may not relate to cave animals (Shapiro & Pringle, 2009). Human traffic can introduce new species to caves which may also harm the species already there (Shapiro & Pringle, 2009). In Barbados this was shown to be true with three of the species being introduced by man in a cave that was described as not heavily distributed (Peck, 1981).


Some of the types of animals typically living in cave environments are of Turbellaria, Oligochaeta, Mollusca, Arachnida, Crustacea, Chilopoda, Diplopoda, Insecta, Osteichthyes and Amphibia. Nearly all independently invaded and were then isolated inside their respective cave systems (Christman & Culver, 2001). Although terrestrial animals are less well studied than aquatic cave communities they appears to be generally composed of forest litter species (Peck, 1981; Poulson & White, 1969). Aquatic species are brought into the cave system via in-wash, and sometimes from flooding (Poulson & White, 1969).


Species found in caves are categorized based on where they live in the cave and their dependence on the cave as a habitat. Troglobites are terrestrial species found only in caves. Troglophiles are found in caves and other similar habitats, they survive at the entrance and the deep interior (Moseley, 2009). Trogloxenes use the cave as a shelter at night but most of their life in spent outside of the cave environment (Barr, 1967). Stygobites are similar to troglobites, but are aquatic (Christman & Culver, 2001). Phreatobites live exclusively in ground water, including cave waters, subterranean wells and pools (Barr, 1967). Edaphobites live in deep soil and caves (Barr, 1967). The last group is called accidentals which can be terrestrial or aquatic and are brought into the cave by mechanical action (Barr, 1967).
The vertebrate animals found in caves are rarely troglobites; although, caves with non-ethereal waters can provide habitat for stynobite fishes. As with many caves Gardner is the part time home for wood rats and bats. Sometimes the cave bat populations are seasonal inhabitants, as it is with Gardner cave in the winter, and caves studied by Barr (1967), in the summer months. The Gardner Cave wood rats surprisingly do not only use the twilight zone, but also the deep interior although it is not yet clear why they do this (Clark et al. 1994). Both bats and wood rats are important sources of organic matter with in their systems (Peck, 1981; Clark et al. 1994). In fact, it was shown in one cave that the prime interaction was between the guanophages and their food resource (Peck, 1981).

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Invertebrates constitute the bulk of the species living in caves. Gardner, like the caves in Nova Scotia studied by Moseley (2009), was formerly glaciated during the last ice age. These caves are interesting because they are composed almost entirely of species in the early stages of colonization (Moseley, 2009). Exploration of Gardner cave has resulted in the identification of species of Ceratopogonidae flies stuck to the fresh calcite flows like fly-paper. A beetle Coleoptera staphylinidea was an expected find, in most non-sulfide caves, beetles dominate the terrestrial fauna (Christman & Culver, 2001). 73% of the described troglobite insects are from the Coleoptera order (Moseley, 2009). C. staphylinidea specifically has been found in formerly glaciated caves other than Gardner (Moseley, 2009). The beetle species is possibly Quedius s. spelaeus which is a subterranean species that has almost never been found outside caves (Moseley, 2009).


An Oligochaeta was found that is currently still under taxonomic investigation. These worms could be having a positive impact on the C. staphylinidea population. In Moseley's (2009) study larvae of the beetles were found living in the organic material of the worm casts. Although it is unclear whether or not these oligochaetes are aquatic or not there is evidence that aquatic oligochaetes are pre-adaptive to living in cave systems (Creuze Des Cha Telliers et al., 2009). Currently these oligochaetes are thought to be either Enchytraeidae or Lumbricidae. Enchytarids are small, highly sensitive to low moisture, and usually live in soil (Maraldo et al. 2009). Lumbricids are the dominant worm family in both North America and Europe (Cook, 1975). Both families have been shown to live in cave habitats in the United States, along with Haplotaxidae, Naididae, Tubificidae, and Ocnerodrilidae (Wetzel et al., 1999; Peck, 1981; Cook, 1975). These worms most likely contribute to the productivity of the Gardner cave system by preforming the same role as other earthworms, modifying the substrate physically, chemically, and biologically; meanwhile, they themselves are a rich food source for predators (Creuze Des Cha Telliers et al., 2009, Cook, 1975).


With all of the difficulties associated with living in caves these simple communities have managed to find successful strategies for working around the stressors. Some of the typical cave- associated strategies are the lowering of population size, reproductive rate, and metabolic rate and toward the lengthening of life and development (Poulson & White, 1969). Organisms also have a tendency to loose their ability to adjust to variable conditions, because of the stability of the cave environment (Poulson & White, 1969).


Metabolic rate changes are crucial when living in an environment that has so little in the way of organic material. Efficiency in using and finding the available food resources is a common strategy for stygobites and troglobites (Poulson & White, 1969). In a Poulson and White (1969) study they showed that a stygobitic fish had a fourfold increase in metabolic rate with a rise of temperature form 10 to 15 degrees Celsius; as opposed to, a closely related troglophilic species who's metabolic rate had a one to two fold increase. The stygobitic fish also searched 30 times as much water as the troglophilic fish when searching for food; however, the longer fins allow it to move twice the distance for each coordinated pectoral caudal fin stroke. (Poulson & White, 1969). When prey items were introduced to both the troglophilic and the stygobitic fish in the laboratory the troglophilic fish found the prey sooner when there was more prey in less water, but when there was more water and fewer prey the stygobitic fish found it's prey hours before the troglophilic fish (Poulson & White, 1969).
Life history traits are also shown to be influenced by the cave environment. There are many species that use strategies including reduction in the rate of population growth, parental care, longer maturation, longer life, and smaller population size (Poulson & White, 1969). Once again the stygobitic fish from the Poulson and White (1969) show more cave associated traits than the troglophilic fish. The stygobitic fish have a reduced caloric cost of egg production because they produce fewer of them and the production of those eggs is also more metabolically efficient (Poulson & White, 1969). Once hatched and living in the mothers gill cavity, they develop much slower than the troglophilic fry and are less susceptible to cannibalism (Poulson & White, 1969). These stygobitic and troglobitic organisms that produce few young in the short term have longer life spans and can therefore produce more young in the long term (Culver et al., 2000). They are also implementing a circandian rhythm strategy to their reproduction due to the lack of seasonal changes within caves (Poulson & White, 1969).


Desiccation is a real problem for animals in cave like Gardner that have no steady supply of water. The high evaporation rate also contributes to the rapid loss of moisture in some caves. The oligochaetes are especially susceptible to desiccation because they breathe through their skin, even mild drought conditions can have negative effects on earthworm reproduction and survival (Maraldo et al., 2009). When there is long term or reoccurring stress many earthworms delay their development in response, this strategy is called diapause (Maraldo et al. 2009). On a cellular level, enchytraeids in particular, use two compatible osmolytes, glucose and alanine, to give them high osmotic pressure which maintains their cell volume in conditions with reduced water (Maraldo et al. 2009). If this is not enough to prevent desiccation enchytraeids have two behavioral strategies to help them survive in dry conditions, the first strategy is not an option for the Gardner cave worms, which is avoidance of dry conditions by migrating to moister substrates. The second strategy is the use of more desiccation tolerant cocoons, and the behavior of covering those cocoons with sand and debris (Maraldo et al. 2009). Maraldo et al.(2009) discussed the way the cocoons become equalized with the environmental water potential and accumulates osmolytes (glucose and sorbitol) in response to dehydration.


The most intriguing cave-associated characteristic is the loss or reduction of morphological traits. Of all of the cave-limited species most display unique cave-associated traits such as eye and pigment loss, elaboration of extra-optic sensory structures, and a delicateness of form. (Culver et al., 2000). These highly modified organisms typically invaded their home cave as long ago as 100 million years (Poulson & White, 1969). Due to the fact that Gardner Cave was only recently (on an evolutionary time scale) available to invasion it is not likely that there are any organisms with these types of trogolmorphisms. Stygobitic fish typically show a reduction or complete loss of eyes while their lateral-line becomes more sensitive and tactile receptors on their heads become more abundant (Poulson & White, 1969). A consequence of living in total darkness is a separation from the diurnal or nocturnal life styles. Loss of circadian activity rhythms was observed in Poulson and White's (1969) study of stygobitic fish, although the oxygen consumption circadian rhythm was retained. These same fish also seemed to have lost their escape responses, and their resistance to pathogens, greatly increasing their vulnerability (Poulson & White, 1969).


Cave systems although prevalent are also inhabited by narrowly dispersed fauna. They are incredibly stressful places to live, despite the relative stability of the environment. Cave communities are simple because of the low diversity and low population sizes, hence they can act as model systems for study of more complex systems. Adaptations and exaptations give animals strategies to survive in conditions with little food, low light to complete darkness conditions, high evaporation rates, and lack of seasonal changes. Continued biological study of Gardner Cave should reveal more information about cave oligochaetes as a whole and may help us discover if the worms living there are troplobites or troglophiles.