Shallow subterranean habitats

Chapter 107

Shallow subterranean habitats Tanja Pipan* and David C. Culver† *Karst Research Institute at ZRC SAZU, Postojna, Slovenia; † American University, Washington, DC, United States

Introduction What are subterranean habitats? Speleobiologists (e.g., Botosaneanu, 1986; Juberthie, 2000) generally recognize two primary categories of subterranean habitats: large cavities (caves) and small interstitial cavities (gravel and sand aquifers, and the soil). These habitats share two important characteristics—the absence of light and the presence of species both limited to and modified for subterranean life. While species in both habitat types are typically without eyes and pigment, large cavity species have elongated appendages while animals limited to interstitial habitats are often miniaturized with shortened appendages (Coineau, 2000). This difference between large and small cavity species makes it relatively easy to separate blind and depigmented species into the appropriate habitat category. An example of these differences is shown for ingolfiellid amphipods in Fig. 1. However, there is one other category—shallow subterranean habitats (SSHs). SSHs are aphotic habitats such as seepage springs, talus slopes, solution pockets, and tubes in epikarst. They are shallow (less than 10 m from the surface), which means that they are much more intimately connected with the surface environment than deeper cavities. They are typically more variable, and with more organic carbon than deeper subterranean habitats. The habitable spaces within these habitats are considerably larger than their inhabitants (Culver and Pipan, 2008). They share with large cavities a habitable space large enough that organisms are not in contact with solid surfaces in all three dimensions. This contrasts with small cavity habitats where cavity size is a major constraint in the evolution of morphology. On the other hand, animals limited to caves and SSHs have similar morphological and ecological characteristics, such as appendage elongation, specialization of extraoptic sensory organs, increased life span, resistance to starvation, reduced aggressive behavior. This set of traits, especially the morphological part, was termed troglomorphy by Christiansen, and this term is widely used to describe the morphological convergence of obligate cave dwellers. SSHs have a number of unique features relative to other subterranean habitats, including: (1) the areal extent of an individual habitat is often small, usually <0.1 km2, but many replicates exist; (2) they are rich in organic matter relative to other subterranean habitats, in part because of their close proximity to the surface; (3) they have intimate connections to the surface resulting in greater environment variation than other subterranean habitats; and (4) they have fauna which includes troglomorphic species, some of which are limited to SSHs (Culver and Pipan, 2014). Among terrestrial SSHs are the spaces between rocks in areas of moderate to steep slope typically stabilized by moss, spaces in bedrock caused by weathering, similar spaces in volcanic terrains, clinker in lava, air-filled epikarst spaces, and sometimes even leaf litter. Juberthie (2000) used the term milieu souterrain superficiel or mesovoid shallow substratum (MSS) for this type of habitat, especially the spaces between rocks, and we follow recent to use MSS as a collective term for these habitats since it is a well-established term in the literature and self-descriptive. Other SSHs include the soil, lava tubes, and iron ore caves. Among aquatic SSHs are epikarst, the uppermost layer of karst with poorly integrated solution cavities; seepage springs, also called the hypotelminorheos; the underflow of streams and rivers, the hyporheos and associated groundwater; and shallow limestone aquifers found in the deserts of Western Australia—calcrete aquifers. For each habitat, we discuss a representative example, give data on environmental variability, and enumerate the fauna (see Culver and Pipan, 2014 for more details).

Aquatic SSHs Seepage springs The hypotelminorheic habitat, or seepage spring (Fig. 2), is (1) a persistent wet spot, a kind of perched aquifer fed by subsurface water in a slight depression in an area of low to moderate slope; (2) rich in organic matter; (3) underlain by a clay layer typically 5–50 cm beneath the surface; (4) with a drainage area typically <10,000 m2; and (5) with a characteristic dark color derived from 896

Encyclopedia of Caves. https://doi.org/10.1016/B978-0-12-814124-3.00107-2 Copyright © 2019 Elsevier Inc. All rights reserved.

Shallow subterranean habitats Chapter 107

897

FIG. 1 Diagrammatic representations of stygobiotic ingolfiellid amphipods. (A) Trogloleleupia leleupi (12–20 mm) from a cave; (B) Ingolfiella sp. (<1 mm) from interstitial habitats, shown at same scale as (A); (C) Trogloleleupia opisthodorus (24–28 mm) from a cave; and (D) Ingolfiella petkovskii (1 mm) from an interstitial habitat. Note the relatively short appendages of I. petkovskii as well as its small size. (From Coineau, N., 2000. Adaptations to interstitial groundwater life. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Subterranean Ecosystems. Elsevier Press, Amsterdam, pp. 189–210. Used with permission of Elsevier Ltd.)

FIG. 2 Photograph of the authors at a seepage spring at Scotts Run Park, near Washington, DC, United States. (Photo by W.K. Jones, with permission.)

898

Encyclopedia of Caves

decaying leaves which are usually not skeletonized (Culver et al., 2006). The habitat can occur in a wide variety of geologic settings anywhere outside of arid regions where there is a layer of impermeable sediment but it is probably less common in karst landscapes because of the extensive occurrence of an impermeable clay layer would prevent the downward movement of water and the development of karst landscapes. Most of the available habitat for the animals comprises spaces between decomposing leaves and sediment, and the animals literally live in their food. Chemical and physical conditions vary considerably between sites, but conductivity tends to be high, indicating that the water had been underground for some time. Although oxygen concentrations varied considerably, the fauna does not seem to be especially sensitive to this parameter. There was about 3 mg dissolved organic carbon (DOC)/L in seepage springs in Nanos, Slovenia, several times higher than most cave water. Based on a 10-month monitoring period of a hypotelminorheic habitat in Prince William Forest Park in Virginia, United States, the habitat was temporally variable (Fig. 3). From May to September, hypotelminorheic temperatures were depressed compared to the nearby surface stream, and approximated surface water temperatures for the rest of the year. In spite of the variability, the amplitude of variation in hypotelminorheic temperature is less than that of surface waters. The maximum recorded temperature in the hypotelminorheic was 22°C compared to 28°C in a nearby (<10 m) stream (Table 1). This is a remarkable difference given the superficial nature of seepage springs. The differences may become more important given predictions of climatic variability and change. Based on a study of 50 seepage springs in the lower Potomac River basin that drains hypotelminorheic habitats within a radius of 45 km, a total of 15 macroinvertebrates were recorded, including 12 amphipod, 2 isopod, and 1 gastropod species (Fig. 4). Four FIG. 3 Hourly temperature from April 7, 2007 to February 4, 2008 in a seepage spring and adjoining stream in Prince William Forest Park, Virginia, United States. Because of the scale, line thickness indicates the extent of daily fluctuations.

30

Temperature (°C)

25 20 Seep

15

Stream

10 5 0 A

M

J

J

A

S

O

N

D

J

F

M

Month

TABLE 1 Statistical properties of temperature (in °C) time series for a seepage spring in Prince William Forest Park, Virginia, United States. Seepage Spring

Surface Stream

12.80

15.10

Standard error

0.06

0.09

Standard deviation

4.88

7.51

Coefficient of variation

38.15

49.75

Range

20.03

27.47

Minimum

1.79

1.02

Maximum

21.82

28.49

Count

7274

7274

Mean

Shallow subterranean habitats Chapter 107

899

FIG. 4 Photograph of the stygobiotic hypotelminorheic specialist Stygobromus tenuis, from Scotts Run Park, Fairfax County, Virginia. (Photograph by William K. Jones, used with permission.)

of the amphipods were probably accidentals—they were uncommon and showed no evidence of reproduction. Of the remaining 11 macroinvertebrate species, 7 were species living exclusively in subterranean habitats. Of these seven, five are exclusively found in seeps: they are hypotelminorheic specialists. Five of the seven stygobionts were troglomorphic. Hypotelminorheic sites in Croatia and Slovenia have a similar mixture of specialized and nonspecialized amphipods.

Epikarst The epikarst is a perched aquifer, the uppermost layer of rock in karst regions, and the major point of contact and transmission between surface and subterranean water. Water is transmitted vertically either through conduits or through small fissures to the water table. Lateral transmission occurs through poorly integrated cavities. The epikarst stores considerable volumes of water which explains why, during a drought, cave streams take much longer to dry up than surface streams in the same area. Its vertical extent is usually 10 m or less. Its principal characteristic is its heterogeneity, with many solution pockets whose water chemistry is also quite variable. Water dripping from the epikarst (Fig. 5) typically contains about 1.0 mg DOC/L, and while this is relatively low, it is an important carbon source in caves both in the establishment of the biofilm in cave streams and in cave passages without active streams. The epikarst is a nearly universal feature of karst areas, except in arid zones and glaciated areas. Karst areas cover approximately 15% of the earth’s surface, and the epikarst is likely to occur over most of this area. Although epikarst water can usually only be sampled by filtering the dripping and seeping water of caves (Pipan, 2005), it occurs throughout karst areas. Epikarst water shows considerable temperature buffering relative to surface water, and more temperature buffering than hypotelminorheic water. An example is the cave Zˇupanova jama in Slovenia (Fig. 6) where temperature varied by approximately 4°C over a 2-year period. Drip rates of water, however, were highly variable, ranging from <1 mL min 1 to 100 mL min 1; with the seasonal pattern dependent on rainfall, but displaying a lagged response. Even though epikarst water is only a few meters below the surface, its residence time may be weeks or even months. In all of the places where epikarst fauna has been sampled, stygobionts have been found, but the Slovenian assemblages are by far the most diverse (Pipan, 2005). In Zˇupanova jama in Slovenia, a total of 16 copepod species were found in 5 drips and their associated pools, and remarkably 14 of these are stygobionts (Table 2). Seven of these species are epikarst specialists, including five undescribed species, two of which are unique to Zˇupanova jama. Other caves in Slovenia have similar overall epikarst copepod species richness, although with more stygophiles (species that can complete their life cycles in either subterranean or epigean habitats) than Zˇupanova jama.

900

Encyclopedia of Caves

FIG. 5 Photograph of water dripping from epikarst in Organ Cave, West Virginia, United States. (Photograph by Horton H. Hobbs III, used with permission.)

Hyporheic The hyporheic zone, first described by Orghidan (1959), comprised of water-filled spaces between the grains of unconsolidated sediments beneath and lateral to streams, the best studied of all interstitial habitats, is the surface-subsurface hydrological exchange zone beneath and alongside the channels of rivers and streams. The hyporheic of rivers is an ecotone between surface and groundwater. The connection between the hyporheic and permanent groundwater (phreatic water) can be very direct or without any direct connection at all. In the case of direct connections between the hyporheic and permanent groundwater, stygobiotic species are often found. Even though the hyporheic appears to be highly uniform, it actually has a series of upwellings and downwellings. Downwellings typically have higher oxygen levels and more organic matter. The exact position of these upwelling and downwelling zones along the stream course depends on the relative pressure of the subsurface and surface waters, and other hydrological details. When there are unconsolidated sediments along the stream bank, the hyporheic can extend laterally tens of meters from the stream bank. Formed by a meander arm, hyporheic habitats in the Lobau wetlands, are part of the floodplain of the Danube River near Vienna, Austria, and comprise the Danube Flood Plain National Park. This UNESCO Biosphere Reserve, with an area of 0.8 km2, has been extensively sampled for decades. Bou-Rouch pumps, specialized pumps designed for sampling in these habitats and minivideo cameras in shallow wells revealed a complex habitat with areas of differing porosity and permeability, variable oxygen levels, and a rich fauna. A small 900 m2 component of this flood plain, called “Lobau C” is a recent terrace of the backwater system “Ebersch€ uttwasser—Mittelwasser” and is a self-contained ecosystem with clear inputs and outputs because of its position between two channels and a dam. Loosely packed gravel, alternating with a thin layer of finer sediments extends several

Shallow subterranean habitats Chapter 107

901

FIG. 6 Discharge (upper panel) and temperature (lower panel) variation of an epikarst drip in Zˇupanova jama, Slovenia, based on monthly measurements taken over a 2-year period. (Data from Kogovsˇek, J., 1990. The properties of the precipitations seeping through the Taborska jama. Acta Carsol. 19, 139–156.)

TABLE 2 List of species of copepods found in epikarst drips and pools in Zˇupanova jama, Slovenia, according to ecological category, whether they are limited to epikarst, and whether they show troglomorphy. Copepod group

Ecological category

Habitat specialist

Troglomorphic

Number of species

Cyclopoida

Stygobiont

Yes

Yes

1

Cyclopoida

Stygobiont

No

Yes

1

Harpacticoida

Stygobiont

Yes

Yes

6

Harpacticoida

Stygobiont

No

Yes

6

Harpacticoida

Stygophile

No

No

2

Data from Pipan, T., 2005. Epikarst—A Promising Habitat. ZRC Publishing at Karst Research Institute ZRC-SAZU, Postojna-Ljubljana.

meters beneath a thin soil cover. Temperature at a depth of 2 m varied between 3°C and 21°C over a two and a half-year period, while surface water temperatures varied between 1°C and 26°C over the same period (Fig. 7). DOC averaged 3.71 mg C/L (Danielopol et al., 2000). Animals were found throughout the depth of gravel, but were most common 0.5 m beneath the surface, and rare below 2 m. In Lobau C, at least 27 species have been found, 11 of them stygobionts (Table 3). While these species are stygobiotic, they do not in general show the troglomorphic syndrome of size increases and appendage elongation, but rather are miniaturized with shortened appendages (see Fig. 1). Thus, they show more morphological kinship with deep interstitial species rather than species from other SSH habitats.

Encyclopedia of Caves

12

30 SW-T GW-T GW-O2

Temperature (°C)

25

10

20

8

15

6

10

4

5

2

Dissolved oxygen (mg/L)

902

0

0 11.91

01.92

03.92

05.92

07.92

09.92

11.92

01.93

03.93

05.93

FIG. 7 Variation in temperature and oxygen from 1991 through 1993 at site D10 in the Lobau wetlands: surface water temperature (SW-T); ground water € F., temperature at 3.5 m (GW-T), and oxygen concentration at 3.5 m (GW-O2). (Data from Danielopol, D.L., Pospisil, P., Dreher, J., Mosslacher, Torreiter, P., Geiger-Kaiser, M. and Gunatilaka, A., 2000. A groundwater ecosystem in the Danube wetlands at Wien, Austria. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Subterranean Ecosystems. Elsevier Press, Amsterdam, pp. 481–511.)

TABLE 3 Number of species and stygobionts from the “Lobau C” area of Danube Flood Plain National Park, Austria. Group

Number of species

Number of stygobionts

Rotatoria

>1

1

Mollusca

>2

2

Copepoda: Cyclopoida

14

3

Copepoda: Harpacticoida

7

2

Amphipoda

1

1

Isopoda

2

2

Data from Danielopol, D.L., Pospisil, P., 2001. Hidden biodiversity in the groundwater of the Danube Flood Plain National Park, Austria. Biodivers. Conserv. 10, 1711–1721.

Calcrete aquifers Calcrete aquifers are both pedogenic and nonpedogenic deposits in arid terrains. In Western Australia, the only region where they have been extensively studied, they are shallow extensive calcium carbonate deposits that harbor a very rich endemic invertebrate fauna (Humphreys, 2008). Some can be up to 30 m deep, but most especially in the Yilgarn region are less than 10 m in depth. Their formation is complex but ultimately related to drying (Fig. 8). As water moves downstream, salinity increases and they have been called subterranean estuaries. Dozens of these aquifers, many hundreds of square kilometers in size, occur throughout Western Australia. Because of their high salinity and isolation one from the other, the freshwater components of calcrete aquifers are like an archipelago with no dispersal between the virtual “islands.” Although there is little if any data on pore size in calcrete aquifers, the fact that most of the inhabitants are less than 5 mm in length suggests that the cavities are quite small (Culver and Pipan, 2014). Regardless of the habitat size, calcrete aquifers are one of the centers of subterranean biodiversity, harboring both an unusual fauna (e.g., aquatic beetles) and ancient fauna

Shallow subterranean habitats Chapter 107

903

FIG. 8 Stages in development of groundwater calcrete. A. Shallow groundwater system in a broad drainage channel. B. Initial carbonate precipitation. C. Growth of pods and domes. D. Maturation of calcrete and surface reworking. (From Mann, A.W., Horwitz, R.C., 1979. Groundwater calcrete deposits in Australia: some observations from Western Australia. J. Geol. Soc. Aust. 26, 293–303.)

(A)

(B)

(C)

(D) Bedrock

Calcrete

Alluvium/colluvium

Water table

(Bathynellacea). Many of the taxa are undescribed. Three calcrete aquifers near Lake Way in Western Australia have between 9 and 17 species of stygobionts.

Terrestrial SSHs Milieu souterrain superficiel Shallow subterranean terrestrial habitats include the spaces between rocks in areas of moderate to steep slope, spaces in bedrock caused by weathering, similar spaces in volcanic terrains, air-filled epikarst spaces, and even leaf litter. We use the collective term MSS for these terrestrial habitats since it is a well-established term in the literature. Initially, the importance of MSS habitats was thought to be as dispersal corridors between cave regions and did in fact account for some disjunct distributions, but soon it was recognized that the primary habitat for some troglobionts was the MSS, rather than caves. MSS habitats can be thought of as relatively large cavities embedded in a matrix of small cavities, that is, the soil (Gers, 1998). An example is Barranco de los Cochinos, an erosional habitat in lava in a laurel (Laurus) forest at 940 m a.s.l. in the Teno area, northwest Tenerife, Canary Islands. This site is comprised of fragmentized basaltic rocks several million years in age, and covered by 40–60 cm of soil (Fig. 9). The surface is characterized by a dense tree covering, low exposure to the sun, and rather high humidity. Temperatures at a depth of 50 cm ranged from 9.2°C to 16.4°C, compared to a range from 7.9°C to 19.4°C on the surface (Table 4). In fact, the annual pattern of temperature fluctuation was quite similar between surface and MSS (Fig. 9), although there was no detectable daily temperature cycle at the MSS site. The Barranco de los Cochinos site has been exceptionally well studied and a total of 73 invertebrate species have been found. Of these, 41 are generalist species, found both in surface and subterranean habitats. Of the 32 species known only from subterranean habitats, 22 are soil specialists with shortened appendages and small size, and 10 are troglomorphic species, with elongated

904

Encyclopedia of Caves

FIG. 9 Temperature profiles at hourly intervals for an MSS site (dark line) and nearby surface site (light line) in a laurel forest in Teno in northwest Tenerife, Canary Islands.

TABLE 4 Statistical properties of temperature (in °C) time series for an MSS site in Barranco de los Cochinos, Tenerife. Description

Surface

MSS

Mean

12.90

12.50

Standard error

0.025

0.021

Standard deviation

2.51

2.12

Coefficient of variation

19.45

17.00

Range

10.50

7.19

Minimum

7.93

9.24

Maximum

19.43

16.43

Count

10,055

10,055

Data from Pipan, T., Lo´pez, P. Oromı´, S. Polak, Culver, D.C., 2011. Temperature variation and the presence of troglobionts in terrestrial shallow subterranean habitats. J. Nat. Hist. 45, 253–273.

appendages and larger size. The 10 troglomorphic species are not usually found in soil, and the 22 soil specialists may not necessarily be permanent inhabitants of the MSS. The troglobionts include spiders, cockroaches, beetles, millipeds, and pseudoscorpions.

Soil Dating back at least to Racovit¸a˘ (1907), the soil fauna has been excluded from any discussion of the subterranean fauna. Of course, the soil is much more important than any other SSH, and most studies focus on soil fertility and indeed, most species are not troglomorphic. But many are, in particular the fauna of deep soil (Culver and Pipan, 2014). Both Coiffait (1958) and Gers (1998) have implicitly recognized the soil fauna as a subterranean fauna, and pointed out the similarities of troglobionts and edaphobionts (obligate deep soil inhabitants), including loss of eyes and pigment, as well as differences. In contrast to troglobionts, edaphobionts are miniaturized or elongated, with reduced appendages. An extreme case of this is shown in Fig. 10, a nematodelike mite. Both Gers (1998) and Pipan et al. (2011) point out that MSS habitats contain a mixture of troglobionts and edaphobionts, as well as more generalized species. Pore size in soils is a major constraint on the size, and soils with larger particles harbor a wide variety of invertebrates. Light disappears within a few millimeter from the surface, and daily and annual temperature variation declines very rapidly with depth. Relative to other SSHs, soil is often rich in organic matter, a reason that is sometimes used to exclude it from the list of subterranean habitats.

Shallow subterranean habitats Chapter 107

905

FIG. 10 External morphology of the soil mite Gordialycus tuzetae. Overall body length is 2.8 mm and width is 0.05 mm. (From Thibaud, M., Coineau, Y., 1998. Nouvelles stations our le genre Gordialycus (Acarien: Nematalycidae). Biogeographica 74, 91–94.)

The most thorough study of the soil fauna is probably that of Coiffait (1958), who examined from 100 sites in the Pyrenees. Of the 194 beetle species he found, 78 were what he termed edaphobionts, obligate soil inhabitants with morphological modifications including loss of pigment and eyes. He lists six shared features of these edaphobiotic beetles: 1. 2. 3. 4. 5. 6.

reduction in body size flattened or thin body shape reduction in appendage and elytra length disappearance of wing membrane eye loss and sensory compensation disappearance of pigment.

The overall composition of the soil fauna in his study was dominated by Collembola and Acari (Fig. 11), as is generally the case for deep soil communities. Densities of soil inhabitants can be very high; Coiffait (1958) found over 20,000 arthropods in 0.8 m3 of soil.

Lava tubes Lava tubes are by-products of volcanic processes themselves. They form either as the result of surface cooling of lava flows or the result of sequential lava flows, with later flows going underneath the older ones and cavities by a process called inflation. Lava tubes are known throughout the world, in areas of volcanic activity along moving plates of the Earth’s crust. Typically, lava tubes form very close to the surface, and are long tubes of more or less constant diameter. Kazumura Cave in Hawai’i, is the longest known lava tube, with 65 km of passage and 101 entrances, and rarely if ever is more than 10 m below the surface. La Cueva del Viento in the Canary Islands, one of the world most diverse caves with respect to terrestrial troglobionts (Culver and Pipan, 2013), is over 20 km long but is at a depth of between 2.5 and 7 m from the surface. In both the Hawaiian Islands and the Canary Islands, where the fauna has been best studied, roots of trees break through the roof of the lava tubes, and at least in Hawai’i, they are a primary source of food. There are some lava tubes that are deeper than 10 m, and some features of volcanic landscapes, including pit craters and open volcanic conduits are very deep (sometimes greater than 100 m (Palmer, 2007)), but most of what we know about subterranean habitats in lava is from shallow lava tubes and the MSS habitats associated with lava flows. Hence, we include

906

Encyclopedia of Caves

FIG. 11 Pie diagrammatic representations of species composition of soil samples from 100 sites in the Pyrenees Mountains. (Compiled from Coiffait by Culver, D.C., Pipan, T., 2014. Shallow Subterranean Habitats. Ecology, Evolution and Conservation. Oxford University Press, Oxford.)

them as SSHs (Culver and Pipan, 2014). As with other SSHs and caves, environmental variation is reduced in lava tubes. We found that temperature 400 m inside Cueva del Viento varied slightly more than 2°C over the course of year with no detectable daily variation (Culver and Pipan, 2014). In Hawai’i, the food web in many lava tubes is dominated by roots of Metrosideros polymorpha, and its primary herbivore, planthoppers in the genus Oliarus (see Stone et al., 2012). Approximately 40 species of troglobionts are known from the Hawaiian Islands, most of which are ultimately dependent on the roots of Metrosideros. The fauna of the Canary Islands is much more diverse, even though there are fewer visible tree roots in lava tubes there. Nearly 130 troglobiotic species are known from the Canary Islands, and the species composition of the two regions is quite different (Fig. 12). Among the possible reasons for the greater species richness in the Canaries is their greater age and their shallower depth, which may result in more organic matter in the lava tubes in the Canaries. The lava tube fauna is also of general evolutionary interest, because species were not forced into caves by any climatic events such as Pleistocene glaciation, but rather actively invaded caves, in part as a more benign environment than the harsh surface conditions on lava flows (Howarth, 1980).

Iron ore caves A highly unusual type of cave, developed directly in iron ore, has been found in Brazil, where 3000 iron caves over the length of 5 m have been found (Auler et al., 2014). While they can occur at depth, the majority are very close to the surface, at the boundary between a surficial iron-rich breccia (canga) and the band iron formation (BIF). We include them as SSHs because nearly all the fauna is known from shallow caves as well as MSS-like habitats in the upper meter or so of the iron ore fields. They apparently form front the action of iron-reducing bacteria that convert insoluble Fe3+ to aqueous Fe2+, with isostatic rebound moving the cave above the water table (Parker et al., 2013). There is perhaps no other subterranean ecosystem that presents a greater conservation challenge than iron ore caves, located as they are in the midst of one of Brazil’s most important economic resources—iron ore ( Jaffe et al., 2016). Ferreira et al. (2015) report that 150 troglomorphic species are known from iron ore caves and that only 10 of these are described. All of the species are terrestrial, and there are undoubtedly many species yet to be discovered.

Generalities These SSHs share several features. First, all of these habitats, support highly modified troglomorphic species, which have a morphology that in many of its characters is convergent with that of the morphology of related deep cave dwelling species. In smaller cavities, like the soil, the convergent morphology is one of reduction in size and appendage length. Second, all of the superficial subterranean environments have species that are not only obligate subterranean species but are also SSH specialists. Third, SSHs are not generally resource-poor habitats. Fourth, with the exception of light, environmental conditions in SSHs are intermediate between surface conditions and deep subterranean conditions. Fifth, what all these habitats share in common is that they are aphotic. In the case of interstitial and epikarst habitats this is self-evident. In the case of seepage springs, light may be present at the exit of the seep, but the habitat itself—the hypotelminorheic—is without light.

Shallow subterranean habitats Chapter 107

907

FIG. 12 Pie diagrammatic representations of species richness of troglobionts from the Canary Islands and Hawaiian Islands. There were 128 species from the Canary Islands and 37 species from the Hawaiian Islands. (Compiled by Culver, D.C., Pipan, T., 2014. Shallow Subterranean Habitats. Ecology, Evolution and Conservation. Oxford University Press, Oxford.)

Origin of the SSH fauna It might seem curious that any species are ever found in SSHs except for an occasional transient. The dominant paradigm of colonization of deeper subterranean habitats such as caves is that animals were forced into these habitats by the vicissitudes of climate change, such as glaciation, sea level change, and aridity. This may be relevant to SSHs as well, given that temperature extremes are never as high in SSHs relative to surface habitats. If it is temperature extremes that drive species underground, SSHs may be a relatively favorable environment in this respect. In the case of aquatic SSHs (epikarst, hyporheic, and hypotelminorheic) all habitats offer an aquatic environment that is less likely to dry out than some surface habitats. The epikarst retains water long after surface water and some cave streams have dried up and the clay that underlies the hypotelminorheic also retains water during periods of drought. Both habitats may thus be a refuge against climate change. Aside from darkness, it seems likely that conditions in SSHs do not present a formidable barrier to colonization, and may even present some advantages. For example, predators, at least large ones, are absent in most SSHs because the size of the habitat does not provide access. Organic carbon is not scarce, or at least not as scarce as in caves, and all of these habitats have a virtual rain of organic matter—falling and decaying leaves in the hypotelminorheic, DOC in epikarst, organic debris in MSS, and detrital accumulation in the hyporheic.

Evolutionary and biogeographic connections with other subterranean habitats Depending on the proximity of SSHs to deeper subterranean habitats, especially caves, colonization of and subsequent adaptation to SSHs may be an evolutionary pathway to colonization of deeper, more extreme subterranean environments. If this is the case,

908

Encyclopedia of Caves

then a phylogenetic tree of a group with both SSH and deep cave species should have a topology with SSH species more basal than deep cave species. Unfortunately, no detailed phylogenies are available for groups with both SSH and subterranean species. Part of the problem may be classification of the habitat. At first glance, the hypotelminorheic might appear to be a surface habitat, while epikarst species might simply appear to be cave species. In many studies of subterranean fauna, the degree of troglomorphy has been equated with the degree of adaptation to subterranean environments and to the length of time a lineage has been isolated in subterranean environments. We suggest an alternative view—the degree of troglomorphy reflects site-specific differences in the subterranean habitat that the species occupy. Extreme appendage elongation, reduction in metabolic rate, and increased longevity, to cite only a few troglomorphic characters, may occur in organisms in extreme, isolated subterranean environments—deep caves and deep groundwater. More typical troglobionts and stygobionts may be the inhabitants of SSHs. They are not necessarily phylogenetically younger, they are just in a different habitat, one that is dark but neither constant nor extremely food-poor.

Bibliography Auler, A., Pilo´, L.B., Parker, C.W., Senko, J.M., Sasowsky, I.D., Barton, H.A., 2014. Hypogene cave patterns in iron ore caves: convergence of forms or processes? In: Klimchouk, A., Sasowsky, I.D., Mylroie, J.E., Engel, S.A., Engel, A.S. (Eds.), Hypogene Cave Morphologies. Karst Waters Institute Special Publication 18, Leesburg, VA, pp. 15–19. Botosaneanu, L. (Ed.), 1986. Stygofauna Mundi. E.J. Brill, Leiden. Coiffait, H., 1958. Les coleopte`res du sol. Vie Milieu Suppl. 7, 1–204. Coineau, N., 2000. Adaptations to interstitial groundwater life. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Subterranean Ecosystems. Elsevier Press, Amsterdam, pp. 189–210. Culver, D.C., Pipan, T., 2008. Superficial subterranean habitats—gateway to the subterranean realm? Cave Karst Sci. 35, 5–12. Culver, D.C., Pipan, T., 2013. Subterranean ecosystems. In: Levin, S.A. (Ed.), Encyclopedia of Biodiversity, second ed. In: vol. 7. Academic Press, Waltham, MA. Culver, D.C., Pipan, T., 2014. Shallow Subterranean Habitats. Ecology, Evolution and Conservation. Oxford University Press, Oxford. Culver, D.C., Pipan, T., Gottstein, S., 2006. Hypotelminorheic—a unique freshwater habitat. Subterranean Biol. 4, 1–8. Danielopol, D.L., Pospisil, P., 2001. Hidden biodiversity in the groundwater of the Danube Flood Plain National Park, Austria. Biodivers. Conserv. 10, 1711–1721. Danielopol, D.L., Pospisil, P., Dreher, J., M€osslacher, F., Torreiter, P., Geiger-Kaiser, M., Gunatilaka, A., 2000. A groundwater ecosystem in the Danube wetlands at Wien, Austria. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Subterranean Ecosystems. Elsevier Press, Amsterdam, pp. 481–511. ´ reas Ferreira, R.L., Oliveira, M.P.A., Silva, M.S., 2015. Biodiversidade subterranea em geossistemas ferruginosos. In: Geossistemas ferruginosos do Brasil: A ´ ´ ´ prioritarias para conservac¸a˜o da diversiadde geologica e biologica, patrim^onio cultural e servic¸os ambientais. Instituto Pristino, Belo Horizonte, pp. 195–231. Gers, C., 1998. Diversity of energy fluxes and interactions between arthropod communities from soil to cave. Acta Oecol. 19, 205–213. Howarth, F.G., 1980. The zoogeography of specialized cave animals: a bioclimatic model. Evolution 34, 394–406. Humphreys, W.F., 2008. Rising from down under: developments in subterranean biodiversity in Australia from a groundwater fauna perspective. Invertebr. Syst. 22, 85–101. Jaffe, R., Prous, X., Zampaulo, R., Giannini, T., Imperatriz-Fonseca, V., Maurity, C., Oliveira, G., Brandi, I., Siqueira, J., 2016. Reconciling mining with the conservation of cave biodiversity: a quantitative baseline to help establish conservation priorities. PLoS One 11, e0168348. Juberthie, C., 2000. The diversity of the karstic and pseudokarstic hypogean habitats in the world. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Subterranean Ecosystems. Elsevier Press, Amsterdam, pp. 17–39. Kogovsˇek, J., 1990. The properties of the precipitations seeping through the Taborska jama. Acta Carsol. 19, 139–156. Mann, A.W., Horwitz, R.C., 1979. Groundwater calcrete deposits in Australia: some observations from Western Australia. J. Geol. Soc. Aust. 26, 293–303. Orghidan, T., 1959. Ein neuer Lebensraum des unterirdischen: der hyporheische Biotop. Arch. Hydrobiol. 55, 392–414. Palmer, A.N., 2007. Cave Geology. Cave Books, Dayton, OH. Parker, C.W., Wolf, J.A., Auler, A., Barton, H.A., Senko, J.M., 2013. Microbial reducibility of Fe (III) phases associated with the genesis of iron ore caves in the Iron Quadrangle, Minas Gerais, Brazil. Fortschr. Mineral. 3, 95–411. Pipan, T., 2005. Epikarst—A Promising Habitat. ZRC Publishing at Karst Research Institute ZRC-SAZU, Postojna-Ljubljana. Pipan, T., Lo´pez, P.O., Polak, S., Culver, D.C., 2011. Temperature variation and the presence of troglobionts in terrestrial shallow subterranean habitats. J. Nat. Hist. 45, 253–273. Racovit¸a˘, E.G., 1907. Essai sur les proble`mes biospeologiques. Arch. Zool. Exp. Gen. 6, 371–488. Stone, F.D., Howarth, F.G., Hoch, H., Asche, M., 2012. Root communities in lava tubes. In: White, W.B., Culver, D.C. (Eds.), Encyclopedia of Caves, second ed. Elsevier/Academic Press, Amsterdam, pp. 659–664. Thibaud, M., Coineau, Y., 1998. Nouvelles stations our le genre Gordialycus (Acarien: Nematalycidae). Biogeographica 74, 91–94.