Al·luvial MSS, un nou habitat subterrani.

Primerament la recerca de fauna subterrània és localitzà a les cavitats naturals, aviat és comprovà que igualment colonitzaven altres hipogeus, més recentment la investigació ha anat trobant un altre habitat colonitzat per una part d'aquesta fauna, el MSS (col·luvions, tarteres, pedregars, sols, etc) i ara se'ns presenta un nou terreny de recerca en el medi al·luvial. Els autors ens presenten la seva recerca experimental, material utilitzat i primeres conclusions.

Ortuño VM, Gilgado JD, Jiménez-Valverde A, Sendra A, Pérez-Suárez G, et al.
(2013) The “Alluvial Mesovoid Shallow Substratum”, a New Subterranean Habitat
PLoS ONE 8(10): e76311. doi:10.1371/journal.pone.0076311

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Abstract

In this paper we describe a new type of subterranean habitat associated with dry watercourses in the Eastern Iberian Peninsula, the “Alluvial Mesovoid Shallow Substratum” (alluvial MSS). Historical observations and data from field sampling specially designed to study MSS fauna in the streambeds of temporary watercourses support the description of this new habitat. To conduct the sampling, 16 subterranean sampling devices were placed in a region of Eastern Spain. The traps were operated for 12 months and temperature and relative humidity data were recorded to characterise the habitat. A large number of species was captured, many of which belonged to the arthropod group, with marked hygrophilous, geophilic, lucifugous and mesothermal habits. In addition, there was also a substantial number of species showing markedly ripicolous traits. The results confirm that the network of spaces which forms in alluvial deposits of temporary watercourses merits the category of habitat, and here we propose the name of “alluvial MSS”. The “alluvial MSS” may be covered or not by a layer of soil, is extremely damp, provides a buffer against above ground temperatures and is aphotic. In addition, compared to other types of MSS, it is a very unstable habitat. It is possible that the “alluvial MSS” may be found in other areas of the world with strongly seasonal climatic regimes, and could play an important role as a biogeographic corridor and as a refuge from climatic changes.

Introduction

For nearly eight decades since the appearance of biospeleology as a scientific discipline following the publication of the study by Racovitza [1], classic authors such as Jeannel [2,3], Vandel [4] or Ginet & Decou [5] have been drawing attention to the extent of the subterranean domain in cracks and fissures beneath the soil surface (microcaverns and mesocaverns sensu Howarth [6]), besides the caves accessible to humans. However, it was not until the 1980s that the studies led by Christian Juberthie [7,8] and the observations carried out by Shun-Ichi Uéno [9,10] revealed the extent of the subterranean domain beneath the karst surface shallow, designated Milieu Souterrain Superficiel in French, and later translated to English as Mesovoid Shallow Substratum, abbreviated to MSS. It forms a unique habitat with its own fauna, but can also play the role of an ecotone, in which both epigean and truly subterranean, troglobiont life forms thrive. A continuum of life is established from the surface soil, through the different edaphic horizons and the MSS, and finally, in the deep subterranean environment, as reported in a study by Gers [11].

A basic condition for the existence of the MSS is the presence of rocky deposits that have generated - and preserved - subterranean spaces which life forms can inhabit. There are many diverse forms of the MSS habitat, which arise as the result of several abiotic and biotic factors [12]. To date, three basic types of MSS have been distinguished:

1): Colluvial or slope MSS

This is formed on sloping ground [7], and is the result of the erosion and deposition of rock fragments produced by the mechanical fragmentation of rock walls or the erosive action of continental glaciers. The nature of the rock can be diverse, including calcareous, siliceous and even volcanic rocks. These rocky deposits can be covered by evolving soil (with edaphic horizons) of different thicknesses which often supports dense plant cover. In other cases, the upper level of the MSS is bare, appearing as mountain scree.

2): Bedrock MSS

This is formed by the weathering of much of the bedrock [13], a gradual process that occurs almost simultaneously with the formation of edaphic horizons which seal it off from the external environment. This type of MSS is found in valley bottoms or areas with little or no slope. The nature of the rock may be very diverse, although it is more likely to occur in rocks that are easily altered.

3): Volcanic MSS

This is the result of the accumulation of volcanic material [14]. From formation onwards, it contains many interconnected fissures forming a tangled web of micro-spaces, which over time become isolated from the outside due to the development of an edaphic environment [15]. This type of MSS is more ephemeral than others, since deposits of volcanic material are more susceptible to weathering than those composed of more compact rocks such as sedimentary, plutonic or metamorphic rocks.

In this paper, we present a proposal supported by experimental and theoretical arguments for a new type of MSS which we have named “alluvial MSS”, and which corresponds to the crevices (unfilled spaces) which lie beneath the streambeds of temporary watercourses.

Antecedents

The existence of hypogean species in watercourses was already known from occasional citations [16,17], but it was the search for Thalassophilus breuili Jeannel, 1926, endemic to Alicante, that triggered the study which led us to propose a new type of MSS habitat, the “alluvial MSS”. Taking into account that this species was so rare in caves (only three specimens from two caves are known [18,19]) and that the third time it was cited, it was on the banks of a temporary watercourse (the Guadalest River) in Altea (Alicante, Eastern Spain) [17], this suggested the possibility that this species might have been swept away by water from a nearby MSS, and that it might be found in this latter habitat [20]. Given the extraordinary irregularity of the hydrological regime of watercourses in the province of Alicante, it was thought that perhaps T. breuili might live in the substratum of these streambeds. Pursuing this lead, one of the authors (V.M.O.) installed 4 pitfall traps, buried 50-70 cm deep, in the streambed of the watercourse known as the “Barranco de la Cueva de los Corrales” (Xixona, Alicante, Spain). These traps were operated for 4 months (June-September, 2009), collecting a considerable number of arthropods, which abounded in the interstices of the substratum of the watercourse. Although T. breuili was not found, it is worth noting the capture of more than a hundred Speonemadus sp., Coleoptera Leiodidae typical of large subterranean cavities and MSS [21,22]. All these data prompted the launch of a research project aimed, among other objectives, at prospecting and studying the subterranean spaces located among the alluvial deposits of dry watercourses in the province of Alicante. These watercourses are dry for most of the year, carrying water only during very sporadic periods of heavy rainfall. However, this subterranean environment remained damp throughout the year and a priori, its structure, comprising stony debris with an extensive network of crevices, could provide a refuge for terrestrial stenohygrobic fauna.

Experimental approach

Study area

The geographic area selected for our study encompassed the eastern end of the karst reliefs of the Prebetic range, from the centre and north of the province of Alicante to the south of the province of Valencia (Eastern Spain), and was chosen because there are numerous temporary watercourses in the area, thanks to a series of geological, geographical and climatic factors. In the local toponymy, these types of watercourse are termed “rambla” (low, wide channel) and “barranco” or “barranc” (tall, narrow channel), words which reflect cultural and linguistic factors [23,24] rather than a true hydrographic characterisation. Regardless, these dry watercourses are usually dry for most of the year, only carrying water for an average of ten days a year [24,25].

The study area was divided into first-order river basins (Figure 1), following the criterion of IDEJúcar [26], and subsequently, basins in the northern half, the wettest, most mountainous area, were selected. A preliminary selection of promising sites for sampling was made using Sigpac [27] and Google, Earth [28]. Of the 42 sites selected a priori, 16 were considered eligible (Figure 1; Table 1) because the watercourses they contained were dry for most of the year and had thick alluvial deposits with numerous subterranean spaces. The other sites were rejected because they did not present either of the two features mentioned. Many of them overlay inappropriate lithologies, as was the case with the marly series of the Tap [29] which constitute physical barriers to the movement of subterranean fauna [30].

Description of a New Subterranean Habitat: The “alluvial MSS”

For the most part, the fauna communities found in the alluvial substratum consisted of species belonging to four groups with well-defined ecophysiological characteristics, being geophilic, hygrophilous, mesothermal and/or lucifugous species. These species exhibit a geophilic nature, inhabiting environments closely associated with soil (edaphic horizons or different epiedaphic habitats and biotopes). They can be either totally geophilic, i.e. their entire life cycle occurs in these habitats/biotopes, or partially geophilic, in which only the larval stages inhabit this type of environment, as in the case of Lampyridae species of the genera Nyctophila and Lamprohiza, both frequently observed in the alluvial substratum. The second ecophysiological characteristic is the strongly hygrophilous nature of the species which were well represented in the alluvial substratum. In areas such as that studied, with a Mediterranean climate, these highly hygrophilous species are extremely rare or absent in edaphic/epiedaphic environments. The third characteristic is the mesothermal nature of many of these species, a circumstance that forces them to seek refuge in favourable environments which mitigate the sudden daily and/or seasonal changes in temperature. The last ecophysiological characteristic was the lucifugous nature which, however, only a portion of the ensemble of alluvial substratum fauna exhibited. This characteristic may be expressed to a lesser or greater degree, and thus some species may show a preference for shaded environments (sciophily) whilst others thrive in aphotic environments (a diversity of subterranean environments).

Different species presented different combinations of these characteristics. There were strongly hygrophilous, lucifugous and mesothermal species, all found in caves and other subterranean spaces, such as species belonging to the lineage Trechus martinezi, Lepthyphantes spp. and certain Isopoda Oniscidea, among others, which are considered troglobiont forms. Then there were strongly hygrophilous, mesothermal and sciophilic species (not exclusive to aphotic environments), such as Dysdera spp., Lithobius spp., Porotachys bisulcatus, Ocys harpaloides, Platyderus spp., Speonemadus spp. and some Oniscidea Isopoda, among others, which constitute an ensemble of species which are typically troglophilic. There were also moderately hygrophilous, mesothermal and sciophilic species which may sometimes behave like true troglophiles, such as Dicranolasma soerensenii and Petaloptila spp., and lastly, there were species which were markedly hygrophilous, may or may not be mesothermal and were not lucifugous, as is the case of fauna exhibiting ripicolous behaviour such as Pardosa spp. and some of the Carabidae Bembidiinae species, among others.

Thus, as happens in caves, the alluvial substratum constitutes a habitat occupied by fauna which is exclusively hypogean (troglobionts), frequently hypogean (troglophiles), and where numerous edaphic species occur (Acari and Collembola, among others) to a different degree, in addition to ripicolous and trogloxene fauna. The latter group consisted of species with a small number of individuals belonging to different orders (Diptera and Hymenoptera, among others), for which living conditions in the substratum are not optimal. This group of specimens reached the substratum by accident, either actively, as part of their daily scavenging activities in the edaphic/epiedaphic environment, or passively, usually as a result of hydrochory and also zoochory. Despite being considered species which are not adapted to this environment, they make a vital contribution to the flow of energy in these subterranean habitats [11,58]. Therefore, there is fauna with different ecological roles: some of them shared with caves and other MSSs (troglobionts and trogloxenes), which characterizes this habitat as a true MSS; some others are typical of soil (edaphobionts), which are also frequent in other MSS [59]; epigean fauna (trogloxenes), due to its proximity to the surface and the conditions of temperature and humidity; and finally ripicolous fauna, whose presence would be particularly characteristic of this habitat.

We propose naming these subterranean spaces located in the alluvial substratum “alluvial MSS”, a hypogean habitat composed of cracks and crevices in the substratum that form among the gravel and variously sized pebbles that constitute the alluvial deposits of dry watercourses (Figure 4). To date, all approaches to the study and recognition of fauna in the substratum of watercourses have focused on the hyporheic zone and, collaterally, with certain adjacent biotopes, some of which might fall under the classification of MSS. The hyporheic zone [60,61] is limited to the substratum of active watercourses, through the interstices of which water circulates and provides a habitat for aquatic species, many of which can be described as stygobionts. In addition, the dynamics of the recent past of these rivers has led to the formation of river terraces beneath which groundwater circulates, constituting aquifers (phreatic biotopes) that may be in contact with the waters of rivers and streams; this forms another type of subterranean water environment [61,] where invertebrate stygobionts are also frequently present. With regard to the MSS that is subject to a fluvial influence and whose origin is unrelated to the dynamics of river currents, Uéno [62] revealed the importance of colluvial deposits and slopes that are more or less directly in contact with the waters of rivers with a moderate current.

The “alluvial MSS” appears in dry watercourses, which appear as scars on the terrain, through which water only flows in times of flood, creating torrential type hydrological regimes. This hydrological dynamic is associated with the Mediterranean climate characteristic of the area, in which maximum rainfall occurs in autumn with a smaller peak in spring, whilst the summer is characterised by a very marked minimum rainfall accompanied by an increase in temperature [24]. Floods occur after irregular, heavy rainfall which starts suddenly and sometimes violently [23,]. However, there are many types of flood, of a diverse nature and intensity [64]. It is of interest to note that those known as flash floods [65] whilst not the only type to occur in the areas studied, have a very significant effect since they can even push solid blocks of a diameter of up to twice the height of the water [24,]. These phenomena may be due to different causes, such as summer convective storms, weather fronts and orographic precipitation [67], and often also to the phenomenon known as “cut-off low” [68-70], responsible for numerous catastrophic episodes of flooding.

Since the watercourses in these areas are dry for most of the year, the fissures in the substratum are not permanently waterlogged. However, they retained sufficient water even when water levels were at their lowest for the stones removed during the installation of the SSDs to be damp (unpublished data), and RHmean levels of 80% and RHmin levels of 46.5% were recorded for some of the SSDs (Table 1, Barranco de la Cueva de los Corrales). This circumstance facilitates the survival of plants growing in the streambed, provides a refuge for hygrophilous terrestrial fauna and supports the presence of both exclusively and frequently hypogean species, rendering this set of spaces among the stones of alluvial debris a new type of MSS.

Formation and structure of the “alluvial MSS”

No single factor determines the presence of temporary watercourses in the Eastern Iberian Peninsula. In other regions of the Mediterranean, the presence of temporary watercourses has been described as the result of a synergy of geological, geomorphological and climatic factors [71]. However, in the case of the study area, there is no clear relationship between the presence of such courses and a given geological substrate or a particular rainfall pattern [23]. Furthermore, it should be noted that not all of the Eastern Iberian watercourses are subject to a seasonal regime, as some have a constant flow of water throughout the annual hydrological cycle, either along the entire course or only a part of it, in which groundwater plays an important role in maintaining a base flow [72]. It should also be noted that the presence of dry watercourses is not a feature unique to the Iberian Peninsula. Rather, they appear in numerous regions of the world with very different climates and geology, receiving different names: the “Chapp” in the Gobi, “Laagate” in the Kalahari, “Wadi” in the Maghreb, “Donga” in South Africa, “Nullah” in India, “Fiumare” in Italy, “Arroyo” in the U.S.A. and Mexico, and “Dry Valley” in England [24,].

With regard to the dry watercourses studied, these are known to have a considerable carrying capacity and thus it is very common to see large boulders, pebbles, gravel and sand on the streambed, forming a very heterogeneous group of rocks from different sources [72]. The loss of the water’s inertia results in the rapid and massive sedimentation of the transported materials [74]. This circumstance converts the lower reaches of these dry watercourses (the low, wide channel known as the “rambla”) into areas where “alluvial MSS” is unlikely to exist because the interstices between the boulders are generally filled (Figure 5a, b). Our field work revealed the existence of “alluvial MSS” in the upper and middle reaches of these watercourses, where the alluvial debris formed by calcareous stones contained a network of empty spaces which had not been filled by sediments, allowing the movement of fauna between these interstices (Figure 6). However, we cannot assert that dry watercourses in different regions of the world behave in the same way.

Although the “alluvial MSS” is not covered by true soil, it is noteworthy that it may have some degree of insulation from the surface as a result of one phenomenon which occurs with relative frequency in these watercourses. This is the phenomenon known as “armouring” [24,], which occurs when flooding ceases and the carrying capacity of the watercourse decreases. At this point, the coarser materials are deposited, forming protective films or “armour”, and the finest materials filter between and rearrange the interstices. Hence, a thin surface layer of silt, sand and gravel is created between the larger stones close to the surface, which contributes to insulating the MSS to a certain extent (Figure 4b, c, d).

In addition, the vegetation that grows not only on the margins of these dry watercourses but also in their channels, plays an important geomorphological role, proffering mechanical resistance to the water and anchoring the alluvial deposits with their roots. Hence, they provide the “alluvial MSS” with greater structural stability against the drag force of torrential waters and favour sedimentation of the particles carried by the water, thus helping to increase the thickness of these deposits [76]. The dry watercourses studied were mostly colonised by oleander formations, shrubs which are characteristic of dry Mediterranean environments and are adapted to withstand both hot drought and the force of floodwaters. Although the oleander (Nerium oleander L.) predominated in these formations, it was often accompanied by various thorny bushes (mostly of the genera Rubus L, Rosa L. and Crataegus L.) and by nitrophilous plants whose growth was favoured by the contribution of organic detritus periodically deposited by floods. When the floods are not very violent or very frequent, it is common for other plants from surrounding plant communities (forest species, mainly) to appear in these streambeds.

The thickness of the alluvial deposits was highly variable, as was the size of the rock fragments of which they were composed, both characteristics being related to the slope and, in general, the orographic and lithological configuration of the site. In some cases, the “alluvial MSS” was no more than 50 cm deep before hitting the bedrock, whilst in other cases its depth exceeded one or one and a half metres (Figure 4).

As already mentioned, the loss of many of the data loggers makes it impossible to generalise the results of the temperature and humidity parameters. Furthermore, the measurements taken corresponded to a depth of between approximately 20 and 30 cm, and it is well known that the physical conditions of temperature and humidity in the substratum change rapidly the further down one goes [77]. However, we can conclude that the “alluvial MSS” is an extremely damp environment, with a RH which is almost constantly in the vicinity of saturation levels. It should be mentioned, however, that the plastic hood in which the data loggers were placed may have produced an overestimation of the RH due to the condensation of water inside. Compared with the external environment, the “alluvial MSS” is very stable as regards temperature [59]. Although the temperature in the MSS showed a pattern (cycle) similar to that of the external environment [59,], values for the mean daily variations in temperature above ground ranged between 10.79-14.78°C, whereas at 20-30 cm deep in the MSS, they ranged between 1.12 and 4.96°C, representing an average of 10°C lower (Figure 3 and Table 2). This is not surprising if we consider that below 50 cm in the substratum, daily temperature variations are usually practically negligible [77], although it may be assumed that in MSS without soil cover, such as the “alluvial MSS”, this depth must be greater [78]. The difference in values between the external environment and the MSS for Tmax and Tmin was around 15°C and 5°C on average, respectively. These data show that although there was an appreciable temperature cycle, the MSS had a more modest variation range than the external environment, and suggest that the MSS was a more effective buffer against maximum temperatures than against minimum temperatures [79,].

Therefore, the “alluvial MSS”, is not only similar in structure to other MSSs (a network of subterranean spaces among rocks and stones), but also in its degree of isolation from surface. However, it has some particularities that differentiate it from other MSSs. The origin of the deposit of stones is alluvial, and the isolation from the surface is not due to a soil layer, but to a layer of silt, sand and gravel (Figure 4b, c, d), and it may eventually have disturbances due to floods of variable intensity.

Ecological importance of the “alluvial MSS”

It is well known that plant and animal species associated with temporary watercourses in arid and semi-arid regions have developed adaptive strategies that allow them to survive water stress [81,]. Watercourses subject to natural spatial and temporal environmental disturbances have been described by Margalef [82] as dynamic evolutionary elements that favour the dynamic processes of species colonisation and expansion [,]. In this paper, we show that this happens not only on the surface and banks of the fluvial network (which includes the edaphic environment), but also in the hypogean environment closely associated with alluvial deposits. In line with the above, the alluvial plains subject to periodic flooding are increasingly being studied as a whole, rather than from an exclusively terrestrial or aquatic perspective [87] As with the “alluvial MSS”, this periodic flooding constitutes a “pulse” that disrupts the dynamic equilibrium these systems had reached before the flood. It is precisely because of these disturbances that it seems difficult to conceive of the existence of terrestrial fauna living in the “alluvial MSS” when, periodically, these channels are completely flooded (Figure 5c-f). However, these apparently catastrophic episodes do not appear to represent an obstacle to the survival of subterranean communities, whose members show very different degrees of adaptation to hypogean life. The proof of this lies in the terrestrial life forms collected in the MSS only days after heavy rainfall. The high speed at which the water flows in the upper and middle sections of these channels may facilitate the retention of large pockets of air within the spaces inside the “alluvial MSS”, and thus, the survival of the terrestrial fauna. The high carrying capacity of these watercourses suggests the possibility that hydrochory events could occur, “seeding specimens” in other sections of the channel suitable for hypogean life [88].

The fauna results obtained show that despite the structural instability of this MSS, the underground spaces in the area studied constituted a habitat that was sufficiently suitable for colonisation both by exclusively hypogean fauna (species only known caves in the area) and frequently hypogean fauna (“troglophile” species sensu Sket [89]). This habitat also acts as a “refuge” for epiedaphic, hygrophilous fauna that are capable of occupying these spaces when necessary to shelter from the seasonal fluctuations in temperature and humidity. Therefore, this subterranean environment must be considered an important habitat due to the role it plays in the conservation of fauna. Furthermore, it represents a new source of information for determining the real biodiversity of sites which, until now, had only been explored above ground and provides data which contribute to improving knowledge of the real distribution of hypogean and epigean species. Lastly, the possibility must also be raised that this new type of MSS may act as an ecological corridor for both hypogean and epiedaphic, hygrophilous fauna.

Synthesis of characteristics of the “alluvial MSS”

The “alluvial MSS” is a type of terrestrial shallow subterranean habitat that consists of a network of spaces which forms among the alluvial deposits of temporary watercourses, and which may be covered or not by a more or less evolved soil on which some herbaceous or woody plants may manage to grow.

Structure.

the “alluvial MSS” forms within alluvial deposits of any type of lithology, and has a thickness which ranges from a few decimetres to several metres deep, overlying the bedrock. Among the gravel (a few millimetres in diameter) and rocks (of up to several decimetres in diameter) that comprise this habitat, empty micro and mesovoids can form which facilitate colonisation by, or provide refuge for, terrestrial fauna presenting very diverse ecological preferences.

Origin.

this habitat is formed as the result of the accumulation of eroded rock fragments (principally pebbles) in dry watercourses, which have been carried there by periodic flooding of the channels.

Abiotic factors.

it moderates the temperature with respect to the external environment, presents high humidity and, below a certain depth, constitutes an aphotic environment. This habitat is usually affected by sporadic, short-lived and temporary flooding.

Energy Sources.

nutrients (organic detritus of animal and vegetable origin) transported by floodwater or from the banks by surface runoff, waste products resulting from the metabolism of the animals inhabiting the MSS and plant remains from vegetation growing on the banks and plants growing in the channel itself (grasses and shrubs).

Fauna.

animals, generally invertebrates and principally arthropods, of different taxa and diverse ecological roles, including epiedaphic, sub-lapidicole, hygrophilous, subterranean (endogean and even hypogean) and ripicolous species. During flooding, it may also contain species which are typically aquatic.

Evolution.

this subterranean environment appears to be more dynamic and unstable than other types of MSS. Floods encourage the periodic creation and destruction of this habitat’s structure, and it is the uppermost layers of the alluvial deposit which are the most unstable. In addition, the alluvial deposit may also be affected by two different processes that are closely related to the transportation of sediment by water: a periodical washing away of sediments or a process whereby the interstices of the alluvial deposit become filled with sediment.

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