Trophic Dynamics of Cave Ecosystems

Trophic dynamics of cave ecosystems

Department of Biology St. Francis Xavier University Antigonish, Nova Scotia, Canada

Introduction

The trophic-dynamic concept of ecology includes the movement of energy in the form of carbon and nutrients among and between organisms in a given ecosystem

(Chapin, Matson and Mooney 2002). The movement of energy through an ecosystem are easily visible when one looks at food chains. This paper will support the argument that the transfer of energy and materials throughout cave trophic systems are detritus-based, as claimed by Culver in 1982.

I will apply the concept of trophic dynamics to cave ecosystems, with emphasis on their uniqueness as it pertains to (1) sources of energy for cave-dwelling organisms, (2) energy flow through trophic links, (3) community structure as influenced by energy availability, and (4) the energy flow among individuals through their interactions. Within each of these subcategories, I will provide examples of modern research supporting

Culver’s claim.

Detritus-based trophic systems in cave ecosystems

As a general rule, trophic systems are subdivided as either plant-based or detritus- based, and as a consequence are regulated by specific controls to different extents. When compared to plant-based trophic systems, it is seen that detritus-based trophic systems convert a much larger proportion of available energy into production (Figure 1), a direct

1 consequence of their ability to recycle unused organic matter (Chapin, Matson and

Mooney 2002).

Figure 1. Two basic trophic systems in ecosystems as proposed by Heal and Maclean in 1975. Re-printed from Chapin, Matson and Mooney 2002. Uneaten food, feces and dead organisms comprise the soil organic matter and provide a source of energy for decomposers directly, and detritovores indirectly. Efficient recycling of energy occurs at each trophic link (Heal and Maclean 1975).

Within cave ecosystems, the only primary production is by chemosynthetic autotrophic bacteria, which utilize iron and sulfur as electron donors. This is a result of sunlight unavailability. As the amount of energy made available through primary production is minute, we can make the generalization that cave communities are decomposer communities (Culver 1982). The detritus-based, or decomposer food chain is characterized by a series of trophic levels, namely detritus, decomposers, and detritovores. Decomposers include both fungi and bacteria capable of breaking down plant detritus to extract nutrients and organic carbon. Detritovores encompass all those organisms that feed on these decomposers (Figure 1).

2 Sources of food

Cave environments have been classically separated into three separate zones. These zones are the twilight zone near the entrance, a middle zone with complete darkness but variable temperature, and the deep interior which bodes complete darkness with constant temperatures. As green plants cannot live in areas with permanent darkness, trogolobites

(i.e., cave-dwelling organisms) must find other sources of food (Poulson and White

1969).

Food enters cave ecosystems in three main ways through both biological and physical agents, either continuously or in pulses and in a range of spatial patterns (Culver

1982). One way organic matter is brought into the ecosystem directly by either streams or vertical shafts. The receding waters often leave a layer of plant detritus behind them, which is an important reservoir for both aquatic and terrestrial communities within the cave ecosystem. Percolating water through the limestone rock contains dissolved organic matter, bacteria, and protozoa, and the fecal matter of animals regularly entering and leaving the cave is rich in organics. In terrestrial cave ecosystems, bat and cave cricket guano, cave cricket eggs, and microorganisms are additions to those listed above. This is seen within some of the most diverse terrestrial cave communities which are found in areas where the guano from cave crickets is found in abundance, usually splattered on both the walls and floor of the cave (Culver 1982). Also, cave cricket eggs have been shown to be a major dietary item for some beetle species in studies by Mitchell in 1968, and Norton et. al. in 1975.

Plant detritus has been shown to be an important food source in cave ecosystems in studies by Schultz (1970) and Holsinger, Baroody and Culver (1975). These studies show

3 that areas of a cave where mud layers rich in organic matter left by retreating flood waters have a rich fauna, whereas caves that have been subject to severe or rapid flooding are void of this rich mud layer, and as a consequence have distinct fauna that are usually not typically found in cave ecosystems. In stone-bottomed cave streams, most of the food is plant detritus, with microbes only present in low numbers (Culver 1982). Many microorganisms are supported by plant detritus, and are a part of the diet of many terrestrial cave invertebrates (Culver 1982). This is support for the presence of decomposer food chains in cave ecosystems.

There is also support that microfungi, decomposers, are an important trophic level in the decomposer food chain. In a study by Dickson and Kirk in 1976, it was found that an abundance of cave-limited invertebrates was correlated with both an abundance of microfungi, as well as high fungal-bacterial ratios. It was also found that in both mud- bottomed, slow-moving streams and in drip and seep pools, microfungi are more common when compared to other areas of the cave, and are correlated with an abundance of macroscopic invertebrates.

In caves with large bat colonies, there is an associated large quantity of guano. Thus, food is comparatively abundant and never in short supply. Horst, in 1972, even went so far as to describe bats as primary producers. In the areas of the cave where these colonies reside, there is a much different fauna as compared to the rest of the cave. This is due to the fact that the selective pressures acting on the rest of the cave fauna are alleviated because of a rich and constant supply of food (Culver 1982). Different types of fecal matter, including bat guano, have been shown to have a more or less distinct community associated with each one (Poulson 1978). In 1970, Harris showed that caves associated

4 with large quantities of guano have complex and diverse food webs, and attribute to internal variation in environment by influencing thermal and humidity regimes, as well as gas composition.

Although it has been assumed several times that bat guano is what is the primary energy source of cave food webs, specifically by Poulson in 1972 and Willis in 1984, there are few studies which provide support for this hypothesis, and the evidence which is available contradicts this hypothesis. Studies by Brown in 1996 which looked at total organic carbon concentrations in waters found below and above bat colonies in Logan

Cave showed no significant differences. This is surprising given the fact that thousands of bats occupy Logan Cave in the summer months. If this hypothesis is indeed incorrect, the generalization that cave ecosystems are oligotrophic in their entirety may have some basis.

As a substantial amount of energy available to the fauna within cave ecosystems are dependent not on primary production, but on those mechanisms outlined above, this provides evidence that cave ecosystems are a detritus-based trophic system.

Energy flow through trophic links

The principles that govern energy flow in a plant-based ecosystem are similar in a decomposer-based ecosystem (Chapin, Matson and Mooney 2002). However, a large difference between these systems arises when looking at the flow of energy throughout the system. In a detritus-based trophic system, instead of traveling in a unidirectional flow as in a plant-based trophic system, materials that are not consumed by a particular trophic link returns to the base of the food chain, and are able to be recycled many times

5 before being respired or converted to recalcitrant humus (Heal and MacLean 1975).

Energy flows through the decomposer food chain as one trophic level feeds on the prior. Therefore, it only makes sense that the amount of detritus available at the most basal level of the food chain creates an upper limit on the amount of energy flow throughout the entire chain. This is known as bottom-up control. A related concept is that as energy is lost at each trophic level, it results in a decrease in available energy useable by the next trophic link (Chapin, Matson and Mooney 2002).

Community structure as influenced by available energy

It is generally accepted that productivity, and hence the amount of energy available to an ecosystem, is related to the structure of communities within. The classical view of detritus-based food chains is that because of the efficient use of energy within, a large diversity of animals are able to be supported (Heal and MacLean 1975). However, when viewing the entire cave ecosystem in it's entirety, oligotrophy (i.e. the condition of being nutrient-poor) is quite common, and appears to structure cave communities through competition for food (Culver, 1982).

As shown by Connell and Orias in 1964, as well as Poulson in 1976, a ratio of food payoff/risk is a key aspect in controlling the complexity of communities within cave ecosystems. In communities with high risk and high payoff, short-lived opportunist organisms dominate. In contrast, complex communities composed of long-lived efficiency experts are associated with low payoff and low risk resources. Anthropogenic materials (i.e., those derived from human activities) accumulating in cave ecosystems were found by Poulson in 1976 to favour opportunistic species. In areas of the cave not affected by oligotrophy due to abundant reservoirs of bat guano, changes in community structure

6 due to relaxed selective pressure can be seen. One example includes an addition of species in the community lacking troglomorphic (i.e., cave-adapted) characteristics

(Culver 1982).

Enrichment studies to test theories relating the associated increase in available energy to community structure were proposed by Poulson in 1976. Theories about the effects of eutrophication in cave systems have been also been proposed by Poulson in

1976, as well as Brown et. al. in 1994. These theories propose that eutrophication could favor epigean cave species rather than hypogean species, as well as that enrichment could increase the food supply and payoff for epigean species.

Available energy also influences community structure in relation to the total species richness, as shown by Fichez in 1990. Fichez found a decrease in organic input from the twilight zone of a Mediterranean submarine cave to the interior of the cave, with associated increasingly oligotrophic conditions as distance from the cave entrance increased. He found this to be correlated with a strong zonal decrease in fauna richness.

A specific study concerning specifically bacterial communities within the sediments of

Wind Cave in South Dakota by Chelius et. al. in 2009 arrived at similar conclusions.

Wind cave is a dry cave in the temperate region, and thus is an energy-starved system

(Chelius et. al. 2009). The organisms inhabiting these caves are low in diversity and structurally simple, and exhibit sensitivity towards changes in external inputs of organic matter (Chelius et. al. 2009). The results of the study showed increases in bacterial biomass in regions of the cave that had received an external input of foreign organic matter. It was also shown that the increase in foreign organic matter compromises significantly the stability of the native populations of bacteria.

7 From the above examples we can see the influences that the amount of energy available can have on community composition. Particulate organic matter is the chief source of energy in cave ecosystems, and is often the agent of increased system stability and persistence, having great effects on both trophic structure and biodiversity (Moore et. al. 2004). This is supported through the evidence mentioned above, and results obtained through manipulation of the availability of organic matter to the cave ecosystem provides more verification for the view of cave ecosystems as detritus-based.

New studies by Issartel et. al. used aspers to measure physiological and metabolic adaptations to food deprivation (2010). Phylogenic and biogeographic data allow conclusions to be made that aspers experienced a rapid selection of adaptive traits that can be related to fasting. The overall results of the study indicate that colonization by organisms in cave ecosystems induces a decreased metabolism with a coupled high capacity to accumulate energy reserves, which together allow the organism to compensate for the oligotrophic conditions of cave ecosystems as well as unpredictable fasting periods (Issartel et. al. 2010).

The structure and function of cave communities may be disrupted by a change in quality or quantity of allochtonous leaf litter entering caves (Hills et. al. 2008). The main findings of Hills et. al's study were that cave invertebrate assemblages differ between native leaf litter and exotic leaf litter in limestone caves in the Jenolan Caves Karst

Conservation Reserve in Australia. Foreign litter was deposited in both the twilight zone and deep within the caves, resulting in a greater richness and abundance of invertebrates in the twilight zone (Hills et. al. 2008).

8 Interactions within communities and potential energy exchange

The exchange of materials through trophic links is correlated to some extent to the interactions within and among individuals of cave communities. An interaction occurring very frequently in nature is that of parasitism. Parasitism has been shown to be a very important agent of population control. When looking at energy flow through the effects of parasitism, it may not matter if the total flux is small. However, the role parasites have in the structure and function of communities is grossly underestimated (Price 1980), particularly in cave ecosystems, as extremes of parasitic specializations often occur

(Culver 1982). In 1975, studies done by Keith in Murray Spring Cave in Indiana shown that nearly all Pseudanophthalmus tenuis beetles were infected with a particular fungal parasite. On average, fifteen infestations of this parasite were found per beetle. Another example of parasitic specialization was documented by Matjasic in 1958, in which seven species from several genera of parasitic platyhelminth worms were found only on the cave shrimp Trogocaris schmidti.

Mutualism has been documented by Hobbs (1973, 1975) between entocytherid ostracods living on exoskeletons of cave crayfish. These ostracods can only complete their life cycle while associated with their crayfish host, and feed on the microbes and detritus that accumulates on the host exoskeleton.

Studies by Christiansen and Bullion in 1978 on competition and predation among terrestrial cave fauna resulted in the conclusion that competition is more important than predation in determining community structure. One could relate this to the oligotrophic conditions primarily found in caves, as a selective pressure is felt by trogolobites to acquire limited resources. Controversially, studies by Kane in 1974 of terrestrial cave

9 communities resulted in the conclusion that predation is a large control on community structure, as supported by large, constant ratios of predator to prey species within experimental units enriched with leaf litter.

Conclusions and future studies

Cave ecosystems are detritus-based trophic systems. The trophic dynamics of cave ecosystems are controlled by a variety of factors. Looking at the detritus-based food chain allows for easy determination of energy flow through the system. The major driving force behind the utilization of a detritus-based trophic system is the unavailability of sunlight, and thus the absence of primary production as an energy base. Consequently, cave-dwelling organisms must derive their energy, nutrients, and carbon from particulate organic matter. Cave ecosystems tend to be oligotrophic, with high diversity being found in areas where pools of organic matter are found. The classic example is areas with high concentrations of bat guano. As evidence to the contrary has arisen in regards to bat guano being a sole source of primary production to fauna found within the cave, this is an area which requires more attention, specifically in material usage and exchange.

The structures of cave communities are influenced by the energy available to the organisms comprising those communities. Also, energy flows through the ecosystem through the interactions between and among members of these communities. The extent to which these interactions influence overall energy availability and movement is poorly known, and is an area which should be addressed in future studies.

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