Article

THE ZOOGEOGRAPHY OF SPECIALIZED CAVE ANIMALS: A BIOCLIMATIC MODEL

If you want to read the PDF, try requesting it from the authors.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the author.

... As a direct consequence of the lack of solar irradiation, primary phototrophic producers are absent in the deep parts of the caves, with the exception of plant roots growing from the soil into sub-superficial subterranean habitats (Gibert and Deharveng 2002). The permanent darkness below the ground also determines the absence of daily dark-light cycles and a reduced influence of the environmental cyclicity (Poulson and White 1969, Howarth 1980, 1983, two factors which seemingly triggered the reduction in the circadian components of activity of numerous cave-limited species over their evolutionary history (Trajano and Menna-Barreto 1995, Hervant et al. 2000, Trajano et al. 2005, Moran et al. 2014, Espinasa et al. 2016. As such, the subterranean domain is generally regarded as temporally stable. ...
... Aside from the obvious differential daily availability of sunlight, at least in the vicinity of the entrance there were also variation in the climatic conditions, especially in respect to higher moisture content at night. A reduced relative humidity in particular, is a well-known limiting factor for the presence of the subterranean fauna (Howarth 1980, 1983, Sharratt et al. 2000. Pronounced sensitivity to saturation deficit was experimentally demonstrated in subterranean beetles (Boyer-Lefèvre 1971), crickets (Yoder et al. 2011) and spiders (Howarth 1980, Hadley et al. 1981. ...
... A reduced relative humidity in particular, is a well-known limiting factor for the presence of the subterranean fauna (Howarth 1980, 1983, Sharratt et al. 2000. Pronounced sensitivity to saturation deficit was experimentally demonstrated in subterranean beetles (Boyer-Lefèvre 1971), crickets (Yoder et al. 2011) and spiders (Howarth 1980, Hadley et al. 1981. The fact that subterranean species are preferentially associated with humid microhabitats (Howarth 1980(Howarth , 1983, indirectly implies that, at night, the twilight zone should represent a more suitable habitat for the subterranean fauna due to the higher levels of relative humidity -at least in winter and spring. ...
Article
Full-text available
Being characterized by the absence of light and a reduced environmental cyclicity, the subterranean domain is generally regarded as temporally stable. Yet, in the proximity of cave entrances (twilight zones), patterns of sunlight and darkness can be detected within the 24-hour day–night cycle. In parallel, changes in the abiotic and biotic conditions are expected; however, these patterns have been rarely explored in animal communities dwelling in the twilight zone. We performed a biological investigation in a small abandoned mine in the Western Alps, monitoring it once per season, both during the day and at night. At each survey, we collected data on the spatial distribution of the resident species, their activity patterns, and the main microclimatic parameters. We observed significant daily variations in the environmental conditions during winter and spring, namely higher temperature, relative humidity and availability of trophic resources at night. In conjunction with these disparate nocturnal conditions, the abundance of troglophile species was also higher, as well as the activity patterns of one of the most frequent species inhabiting the entrance area – the orb-weaver spider Metamenardi . We further documented temporal changes in the composition of the parietal community, due to species using the mine as a diurnal, nocturnal or overwintering shelter. Overall, our results suggest that the communities of the twilight zone are not temporally stable and we highlight the importance of taking into account not only their seasonal, but also their daily variations.
... Because not all arthropods attracted to pitfall traps will be captured, searches around traps prior to removal have been applied by previous workers (Campbell et al., 2011;Martín & Oromí, 1986;Poulson & Culver, 1969;Wynne, 2013;Wynne et al., 2014). For sampling previously unstudied caves in Hawai'i and Australia, Howarth (1980Howarth ( , 1988 applied a variety of techniques including intensive direct intuitive searches (in promising microhabitats), deploying bait stations (using naturally occurring organic material, tubers, rotting meat, cheese and grains) and to a lesser extent baited pitfall traps-the latter included both live and kill pitfalls. ...
... Cave deep zones were differentially sampled. This environmental zone is characterized by complete darkness, stable temperature, a near-water saturated atmosphere and low to no airflow (as in Howarth, 1980). For select PARA and RAPA caves, we used combined bait sampling (B) and DIS to examine deep zones of three RAPA caves (Q15-074, Q15-076/078 and Q15-113) and two PARA caves (PARA-1001 and PARA-2204). ...
... Schneider and Culver (2004) reported none of their species accumulation curves neared asymp- Boulton, 2009;Howarth, 1982). For example, the desiccating effect of cold dry air on caves (i.e., the winter effect; Barr, 1968;Howarth, 1980) frequently drives cave-adapted organisms into small cracks and fissures where they are more difficult to detect. Thus, sampling for troglomorphic taxa during a less optimal time of year may result in detecting fewer troglomorphic species. ...
Article
Aim: Identify the optimal combination of sampling techniques to maximize the detection of diversity of cave-dwelling arthropods. Location: Central-western New Mexico; northwestern Arizona; Rapa Nui, Chile. Methods: From 26 caves across three geographically distinct areas in the Western Hemisphere, arthropods were sampled using opportunistic collecting, timed searches, and baited pitfall trapping in all caves, and direct intuitive searches and bait sampling at select caves. To elucidate the techniques or combination of techniques for maximizing sampling completeness and efficiency, we examined our sampling results using nonmetric multidimensional scaling (NMDS), analysis of similarity (ANOSIM), Wilcoxon signed-rank tests, species richness estimators and species accumulation curves. Results: To maximize the detection of cave-dwelling arthropod species, one must apply multiple sampling techniques and specifically sample unique microhabitats. For example, by sampling cave deep zones and nutrient resource sites, we identified several undescribed cave-adapted and/or cave-restricted taxa in the southwestern United States and eight new species of presumed cave-restricted arthropods on Rapa Nui that would otherwise have been missed. Sampling techniques differed in their detection of both management concern species (e.g., newly discovered cave-adapted/restricted species, range expansions of cave-restricted species and newly confirmed alien species) and specific taxonomic groups. Spiders were detected primarily with visual search techniques (direct intuitive searches, opportunistic collecting and timed searches), while most beetles were detected using pitfall traps. Each sampling technique uniquely identified species of management concern further strengthening the importance of a multi-technique sampling approach. Main conclusions: Multiple sampling techniques were required to best characterize cave arthropod diversity. For techniques applied uniformly across all caves, each technique uniquely detected between ~40% and 67% of the total species observed. Also, sampling cave deep zones and nutrient resource sites was critical for both increasing the number of species detected and maximizing the likelihood of detecting management concern species.
... The biological importance of cave temperature is less obvious but even small differences in temperature, on the order of 1˚C, can have a major impact on micro-distribution of cave spiders, and an important feature of niche differentiation among competing species [6,7]. Relative humidity is perhaps the most constant of the three, and Howarth [4,8] argues that it is of profound importance as a selective factor, and that the ability of a terrestrial organisms to survive in an atmosphere of 100% RH requires major morphological changes, especially cuticular thinning. Nicolosi et al. [9] show that the cave isopod Armadillium lagrecai was very sensitive to fluctuations in temperature and relative humidity. ...
... Nicolosi et al. [9] show that the cave isopod Armadillium lagrecai was very sensitive to fluctuations in temperature and relative humidity. Howarth [8] showed that longevity for the Hawaiian spider Lycosa howarthi was reduced by 25% as a result of a RH drop to only 90% from saturation. Hadley et al. [10] further showed that the cuticle of cave spiders was thinned, compared to surface relatives. ...
... Hadley et al. [10] further showed that the cuticle of cave spiders was thinned, compared to surface relatives. This reduction allows individuals to survive water saturated environments, but at a cost of desiccation when relative humidity drops below saturation [8,9]. As they point out, at 100% RH, the subterranean terrestrial environment has some features of an aquatic environment and is certainly an extreme environment. ...
Article
Full-text available
Relative humidity (RH) was measured at hourly intervals for approximately one year in two caves at seven stations near Playa del Carmen in Quintana Roo, Mexico. Sistema Muévelo Rico is a 1.1 km long cave with 12 entrances and almost no dark zone. Río Secreto (Tuch) is a large river cave with more than 40 km of passages, and an extensive dark zone. Given the need for cave specialists to adapt to saturated humidity, presumably by cuticular thinning, the major stress of RH would be its deviation from saturation. RH in Río Secreto (Tuch) was invariant at three sites and displayed short deviations from 100% RH at the other four sites. These deviations were concentrated at the end of the nortes and beginning of the rainy season. Three of the sites in Sistema Muévelo Rico showed a similar pattern although the timing of the deviations from 100% RH was somewhat displaced. Four sites in Sistema Muévelo Rico were more variable, and were analyzed using a measure of amount of time of deviation from 100% RH for each 24 hour period. Strong seasonality was evident but, remarkably, periods of constant high humidity were not the same at all sites. In most Sistema Muévelo Rico sites, there was a detectable 24 hour cycle in RH, although it was quite weak in about half of them. For Río Secreto (Tuch) only one site showed any sign of a 24 hour cycle. The troglomorphic fauna was more or less uniformly spread throughout the caves and did not concentrate in any one area or set of RH conditions. Compared to temperature, RH is much more constant, perhaps even more constant than the amount of light. However, changes in RH as a result of global warming may have a major negative effect on the subterranean fauna.
... Apart from thermal tolerance, it is worth noting that air moisture content (i.e. humidity) is one of the most important limiting factors for terrestrial cave obligate species (Howarth, 1980(Howarth, , 1983Simões et al., 2015). For example, Howarth (1980) tested in the laboratory the longevity of spiderlings of Lycosa howarthi Gertsch (Araneae: Lycosidae) at three distinct values of relative humidity (100%, 95%, and 90%). ...
... humidity) is one of the most important limiting factors for terrestrial cave obligate species (Howarth, 1980(Howarth, , 1983Simões et al., 2015). For example, Howarth (1980) tested in the laboratory the longevity of spiderlings of Lycosa howarthi Gertsch (Araneae: Lycosidae) at three distinct values of relative humidity (100%, 95%, and 90%). At 90% the longevity dropped to one-fourth of the mean value at 100% (15.4±0.9 versus 61.8±1.3 days), pointing toward a pronounced sensitivity to saturation deficit. ...
... Accordingly, the maintenance of high humidity levels appears to be essential for the survival of different troglobionts. This is generally explained by the high cuticular permeability of many species, associated with a low resistance to desiccation (Hadley et al., 1981;Howarth, 1980Howarth, , 1983. As previously explained, (2) Niche overlap between congeneric species Mammola and Isaia (2017) in caves from regions with limited water infiltration, relative humidity of cave environments may be reduced as a consequence of the cave temperature increase. ...
Article
Scientists of different disciplines have recognized the valuable role of terrestrial caves as ideal natural laboratories in which to study multiple eco-evolutionary processes, from genes to ecosystems. Because caves and other subterranean habitats are semi-closed systems characterized by a remarkable thermal stability, they should also represent insightful systems for understanding the effects of climate change on biodiversity in situ. Whilst a number of recent advances have demonstrated how promising this fast-moving field of research could be, a lack of synthesis is possibly holding back the adoption of caves as standard models for the study of the recent climatic alteration. By linking literature focusing on physics, geology, biology and ecology, we illustrate the rationale supporting the use of subterranean habitats as laboratories for studies of global change biology. We initially discuss the direct relationship between external and internal temperature, the stability of the subterranean climate and the dynamics of its alteration in an anthropogenic climate change perspective. Owing to their evolution in a stable environment, subterranean species are expected to exhibit low tolerance to climatic perturbations and could theoretically cope with such changes only by shifting their distributional range or by adapting to the new environmental conditions. However, they should have more obstacles to overcome than surface species in such shifts, and therefore could be more prone to local extinction. In the face of rapid climate change, subterranean habitats can be seen as refugia for some surface species, but at the same time they may turn into dead-end traps for some of their current obligate inhabitants. Together with other species living in confined habitats, we argue that subterranean species are particularly sensitive to climate change, and we stress the urgent need for future research, monitoring programs and conservation measures.
... Regressive evolution is typically associated with shallow subterranean (<10 m) and cave dwelling organisms, and the field of biospeleology (White and Culver 2012;Culver and Pipan 2014). Cave biologists often delineate these variant light environments into discrete photic zones, beginning at the cave "entrance zone" through a series of transitional and increasingly dimmer light zones and culminating in the "dark zone," the deep regions of a cave wherein there is a complete absence of light in addition to relatively constant temperature and humidity levels that are less affected by surface climate variation (e.g., Howarth 1980). Similar parallels can be drawn with transitional light environments at different depths of the water column (e.g., disphotic zone receives light that is insufficient for plants to photosynthesize), as well as transitions from diurnal to nocturnal behavioral activity (Tierney et al. 2017). ...
... These limestone depositions (explained in greater detail below-Unusual Study System section) are relatively shallow (up to 10 m below the surface) compared with most other cave systems. It is plausible that individual calcretes may be subject to surface cracking which would then subject them to light environment categorization akin to Howarth's (1980) zonations. In the majority of cases the stygobiontic beetles are assumed to have evolved in complete darkness, however, it is possible that the beetles may have evolved initially in interstitial environments (e.g., gravels in ephemeral river or creek systems), as evident for several other dytiscid species in Australia (e.g., Watts et al. 2016). ...
Article
Synopsis: Two tribes of subterranean dytiscid diving beetles independently colonised groundwater systems of the Western Australian arid zone, a habitat transition that was most likely driven by the contraction of surface water bodies following late Neogene aridification of the Australian continent. These 'stygofauna' are now trapped within discrete calcrete aquifers that have formed in palaeodrainage valleys, resulting in the world's most diverse radiations of subterranean dytiscid beetles. Approximately 100 species from three genera exhibit partial or fully regressed visual systems and are essentially blind. This unique study system, with multiple independent transitions to subterranean life enables regressive and adaptive evolutionary processes to be studied in parallel at an unheralded comparative scale. Here we provide an overview of the progression of dytiscid beetle research and undertake a literature survey of published research within the field of regressive evolution as it applies to eye loss. We detail our exploration of insect vision genes for signatures of adaptive and neutral evolutionary mechanisms related to eye regression, largely within photoreceptor and eye pigment genes. Our project makes use of transcriptome data from five representative dytiscid beetle species (two surface and three subterranean) in order to design a customized set of RNA baits for use in a hybrid-capture method to target a pool of vision genes sequenced using high-throughput Illumina platforms. This methodological design permits the assessment of modifications in the genomic sequence of beetle vision genes at a much broader scale than Sanger sequencing, enabling a higher number of both target species and genes to be simultaneously assessed relative to research time-investments. Based on our literature search criteria of the research field ('regressive evolution' + 'eyes'), 81 papers have been published since the late 1980's accruing an h-index of 27 and a mean citation rate of 24.57. Collective annual citations for this field of research have surged over the past five years, an indication that broader scientific community interest is gaining momentum. The majority of publications (75%) have focused on the chordate clade Actinopterygii. Historically, research on variant subterranean taxa have faced difficulties inferring the evolutionary mechanisms of eye regression (and vision loss) using molecular approaches because only a handful of target genes could be feasibly addressed within grant funding cycles. From a comparative phylogenetic perspective, next-generation sequencing approaches applied to stygobiontic dytiscid beetles hold the potential to greatly improve our understanding of the genetic mechanisms underlying regressive evolution generally.
... Caves were selected based upon two criteria -sufficient length to support deep zone conditions and the availability of a current cave map. Cave deep zones are defined as completely dark regions with relatively stable temperature, low to no airflow, and a near water-saturated atmosphere with a negligible evaporation rate (Howarth 1980(Howarth , 1982. While we recognize other factors may contribute to the occurrence of cave deep zones (e.g., maze-like and/or constricted passageways, small or partially rock-fall obstructed entrances, and cave structure in general), we used these criteria because logistics prevented us from selecting study caves based upon site visit evaluations. ...
... Terminology.-Cave ecosystems typically consist of four zonal environments (Howarth 1980(Howarth , 1983: (1) entrance zonecombination of surface and cave environmental conditions; (2) twilight zone -both diminished light conditions and influence of (3) transition zone -aphotic, yet barometric and diurnal shifts are observed at a significantly diminished rate approaching near stable climatic conditions; and, (4) deep zone -complete darkness, high environmental stability, constant temperature, and near water-saturated atmosphere with low to no airflow (typically occurs in the deepest portion of the cave). While there are four primary cave specific functional groups generally recognized, the specimens discussed are troglomorphic (cave-adapted) organisms known as troglobionts. ...
Article
Two new troglomorphic pseudoscorpion species, Bisetocreagris maomaotou sp. nov. (Family Neobisiidae) and Tyrannochthonius chixingi sp. nov. (Family Chthoniidae) are described from one cave in the tower karst of northern Guangxi Province, China. This cave is located at close proximity to a village and an adjacent urban area. As with many caves in the South China Karst, this feature occurs at an elevation slightly above agriculture and rural activities; thus, we suggest it may be partially buffered from human activities in the lowland areas. We discuss the likelihood of narrow range endemism and provide research and conservation recommendations to guide future management of these two species.
... Friedrich's (2013) subsequent work suggests that this pattern is widespread among troglobionts. Howarth (1980) proposed that an important aspect of adaptation of terrestrial insects and other arthropods to caves is cuticular thinning to allow the animals to survive in habitats of high or even saturated relative humidity. This situation was first demonstrated for lycosid spiders (Hadley et al. 1981). ...
... Thus, the mean fitness of an individual in a population of surface-and subterranean-dwelling individuals is increased in the subterranean habitat, rather than decreased in the surface habitat. This is what Howarth (1980Howarth ( , 1987 calls the Adaptive Shift Hypothesis, in which some individuals from a population exploit a new habitat or food resource. In his studies of the fauna of Hawaiian lava tubes, Howarth noted that food was in short supply on the surface of lava flows, especially recent ones. ...
Chapter
Full-text available
The first cave‐dwelling invertebrate known to science was the beetle Leptodirus hochenwartii, described by Ferdinand Schmidt in 1832. This chapter presents a discussion of L. hochenwartii. It describes the variety of subterranean spaces, including but not limited to caves, that insects inhabit, the ecological roles of insects in subterranean habitats, and morphological and life‐history adaptations of insects to subterranean life. The L. hochenwartii has many of the features associated with adaptation to subterranean life, including reduced pigment, loss of eyes, and appendage elongation. The chapter shows a number of specialized cave insects, soil insects, and generalists at a milieu souterrain superficiel (MSS) site in Teno, Tenerife, Canary Islands. It also describes probable modes of successful colonization of subterranean spaces, taxonomic and geographic patterns of subterranean insect biodiversity and human utility and protection of cave insects.
... Caves were selected based upon two criteria -sufficient length to support deep zone conditions, and the availability of a current cave map. Cave deep zones are defined as completely dark region with relatively stable temperature, low to no airflow, and a near water saturated atmosphere with a negligible evaporation rate (Howarth 1980(Howarth , 1982. While we recognize other factors may contribute to the occurrence of cave deep zones (e.g., mazy and/or constricted passageways, small or partially rock-fall obstructed entrances, and cave structure in general), we used this criterion because logistics prevented us from selecting study sites based upon site visit evaluations. ...
... Cave ecosystems typically consist of four zonal environments (Howarth 1980(Howarth , 1983: ...
Preprint
Full-text available
We synthesized the current knowledge of cave-dwelling millipede diversity from Guangxi Zhuang Autonomous Region (Guangxi), South China Karst, China and described six new millipede species from four caves from the Guilin area, northeastern Guangxi. Fifty-two cave-dwelling millipedes are known for the region consisting of 38 troglobionts and 14 troglophiles. Of the troglobionts, 24 are presently considered single-cave endemics. New species described here include Hyleoglomeris rukouqu sp. nov. and Hyleoglomeris xuxiakei sp. nov. (Family Glomeridae), Hylomus yuani sp. nov. (Family Paradoxosomatidae), Eutrichodesmus jianjia sp. nov. (Family Haplodesmidae), Trichopeltis liangfengdong sp. nov. (Family Cryptodesmidae), and Glyphiulus maocun sp. nov. (Family Cambalopsidae). Our work also resulted in range expansions of Pacidesmus trifidus Golovatch & Geoffroy, 2014, Blingulus sinicus Zhang & Li, 1981 and Glyphiulus melanoporus Mauriès & Nguyen Duy-Jacquemin, 1997. As with many hypogean animals in Southeast Asia, intensive human activities threaten the persistence of both cave habitats and species. We provide both assessments on the newly described species’ distributions and recommendations for future research and conservation efforts.
... Such conditions were present near the entrance in spring and summer, which may in turn explain the greater abundance of troglobionts in these seasons. Our findings are in accordance with the generally accepted understanding that troglobionts are adapted to narrow ranges of temperature and humidity (Barr & Kuehnelt, 1971;Howarth, 1980). They are more susceptible to desiccation, owing to their thinner exoskeleton, compared to their surface counterparts (Howarth, 1980). ...
... Our findings are in accordance with the generally accepted understanding that troglobionts are adapted to narrow ranges of temperature and humidity (Barr & Kuehnelt, 1971;Howarth, 1980). They are more susceptible to desiccation, owing to their thinner exoskeleton, compared to their surface counterparts (Howarth, 1980). Furthermore, the higher availability of prey and organic matter deposits in the vicinity of the entrance Tobin et al., 2013) Mammola et al. 2015: Sphodropsis ghilianii). ...
Article
Troglobionts are organisms that are specialized for living in a subterranean environment. These organisms reside prevalently in the deepest zones of caves and in shallow subterranean habitats, and complete their entire life cycles therein. Because troglobionts in most caves depend on organic matter resources from the surface, we hypothesized that they would also select the sections of caves nearest the surface, as long as environmental conditions were favorable. Over 1 year, we analyzed, in monthly intervals, the annual distributional dynamics of a subterranean community consisting of 17 troglobiont species, in relation to multiple environmental factors. Cumulative standardized annual species richness and diversity clearly indicated the existence of two ecotones within the cave: between soil and shallow subterranean habitats, inhabited by soil and shallow troglobionts; and between the transition and inner cave zones, where the spatial niches of shallow and deep troglobionts overlap. The mean standardized annual species richness and diversity showed inverse relationships, but both contributed to a better insight into the dynamics of subterranean fauna. Regression analyses revealed that temperatures in the range 7–10°C, high moisture content of substrate, large cross section of the cave, and high pH of substrate were the most important ecological drivers governing the spatiotemporal dynamics of troglobionts. Overall, this study shows general trends in the annual distributional dynamics of troglobionts in shallow caves and reveals that the distribution patterns of troglobionts within subterranean habitats may be more complex than commonly assumed.
... The existence of gradients in the abiotic and biotic conditions from the surface toward the deepest subterranean sectors, enhance the possibility to use caves as models for ecological studies, e.g. for investigating linear gradients and community turnovers in space. subterranean habitats share some peculiar environmental characteristics, which have been summarised in details by different authors (Barr 1967, Howarth 1980, 1983, Culver 1982, Cigna 2002, Romero 2009, Culver and Pipan 2009, Badino 2010, including Poulson and White themselves (1969). ...
... Classically, it has been observed that the communities of cave twilight zones are usually dominated by trogloxenes and troglophiles species, whereas troglobionts dominate in the deep subterranean sectors (Poulson and White 1969, Culver and Poulson 1970, Howarth 1980, 1983. At a local scale, this spatial heterogeneity in the species distribution has been mostly explained in relation to microclimate (Tobin et al. 2013, Mammola et al. 2015a, Lunghi et al. 2017, light availability (Mulec et al. 2008, Tierney et al. 2017, salinity (Shapouri et al. 2016), invasion history (Fong and Culver 1994), trophic inputs (Gers 1998, Rendoš et al. 2012) and competitive exclusion dynamics (see 'Niche theory and competition'). ...
Article
Full-text available
The use of semi‐isolated habitats such as oceanic islands, lakes and mountain summits as model systems has played a crucial role in the development of evolutionary and ecological theory. Soon after the discovery of life in caves, different pioneering authors similarly recognized the great potential of these peculiar habitats as biological model systems. In their 1969 paper in Science, ‘The cave environment’, Poulson and White discussed how caves can be used as natural laboratories in which to study the underlying principles governing the dynamics of more complex environments. Together with other seminal syntheses published at the time, this work contributed to establishing the conceptual foundation for expanding the scope and relevance of cave‐based studies. Fifty years after, the aim of this review is to show why and how caves and other subterranean habitats can be used as eco‐evolutionary laboratories. Recent advances and directions in different areas are provided, encompassing community ecology, trophic‐webs and ecological networks, conservation biology, macroecology, and climate change biology. Special emphasis is given to discuss how caves are only part of the extended network of fissures and cracks that permeate most substrates, and thus their ecological role as habitat islands is critically discussed. Numerous studies have quantified the relative contribution of abiotic, biotic and historical factors in driving species distributions and community turnovers in space and time, from local to regional scales. Conversely, knowledge of macroecological patterns of subterranean organisms at a global scale remains largely elusive, due to major geographical and taxonomical biases. Also, knowledge regarding subterranean trophic webs and the effect of anthropogenic climate change on deep subterranean ecosystems is still limited. In these research fields, the extensive use of novel molecular and statistical tools may hold promise for quickly producing relevant information not accessible hitherto.
... Cave entrances typically appear as warm features in thermal imagery acquired at night and cool features in midday imagery (e.g., [1,36,47,48]) because cave entrances are generally characterized by smaller diurnal temperature changes than the surrounding surface rock. Deep interior cave temperatures are typically stable (e.g., [49,50]) due to diurnal surface temperatures, which are dampened via thermal conduction of the geologic substrate [51,52]. As this occurs, the diurnal temperature variations of cave entrances may also be diminished. ...
... These include shallow through caves (or tunnels), shelter-like features extending ~10 meters to caves tens of meters in length with multiple collapse pit entrances. Given the exploratory nature of this study, we did not attempt to differentiate between shallow caves and caves with a deep zone environment (refer to [49,50]). Thus, we considered all features, regardless of size that permitted access to the subterranean realm, as caves. ...
Article
Full-text available
Since the initial experiments nearly 50 years ago, techniques for detecting caves using airborne and spacecraft acquired thermal imagery have improved markedly. These advances are largely due to a combination of higher instrument sensitivity, modern computing systems, and processor intensive analytical techniques. Through applying these advancements, our goals were to: (1) Determine the efficacy of methods designed for terrain analysis and applied to thermal imagery; (2) evaluate the usefulness of predawn and midday imagery for detecting caves; and (3) ascertain which imagery type (predawn, midday, or the difference between those two times) was most informative. Using forward stepwise logistic (FSL) and Least Absolute Shrinkage and Selection Operator (LASSO) regression analyses for model selection, and a thermal imagery dataset acquired from the Mojave Desert, California, we examined the efficacy of three well-known terrain descriptors (i.e., slope, topographic position index (TPI), and curvature) on thermal imagery for cave detection. We also included the actual, untransformed thermal DN values (hereafter "unenhanced thermal") as a fourth dataset. Thereafter, we compared the thermal signatures of known cave entrances to all non-cave surface locations. We determined these terrain-based analytical methods, which described the "shape" of the thermal landscape hold significant promise for cave detection. All imagery types produced similar results. Down-selected covariates per imagery type, based upon the FSL models, were: Predawn-slope, TPI, curvature at 0 m from cave entrance, as well as slope at 1 m from cave entrance; midday-slope, TPI, and unenhanced thermal at 0 m from cave entrance; and difference-TPI and slope at 0 m from cave entrance, as well as unenhanced thermal and TPI at 3.5 m from cave entrance. Finally, we provide recommendations for future research directions in terrestrial and planetary cave detection using thermal imagery.
... Howarth developed a bioclimatic model to explain the occurrence and evolution of cave species (Howarth, 1980). Five zones can be characterized by their abiotic and biotic environments: Entrance, Twilight, Transition, Deep Cave and Stagnant Air Zones (Howarth, 1993). ...
... Two contrasting theories attempt to explain the origin and the distribution of the subterranean fauna Pipan 2009, 2010). The theory of the active colonization (Rouch and Danielopol 1987) or adaptive shift hypothesis (Howarth, 1980) puts great emphasis on the process of active colonization of the hypogean domain, with species being driven by the opportunity to occupy new, unexploited ecological niches. On the other hand, the theory of relicts and refuges (Botosaneanu and Holsinger 1991) invokes long-term climatic changes, such as glaciation cycles and other large-scale climate upheavals, as the main factors that prompted the colonization of the subterranean habitat and causing the obliteration of surface-dwelling populations (Holsinger 1988, Botosaneanu andHolsinger 1991). ...
Article
Full-text available
Subterranean ecosystems present ideal opportunities to study mechanisms underlying responses to changes in climate because species within them are often adapted to a largely constant temperature. We have characterized the thermal conditions of caves in the Western Alps, and related these hypogean climate data to the occurrence of Troglohyphantes spiders (Araneae, Linyphiidae). Our data indicated that present distributions reflect Pleistocene glaciation events and also pointed to specific responses as a consequence of changes in temperature. Constant temperatures recorded inside caves provide an approximation of the mean annual temperature outside, thus we extended the results to a regional scale. We used ecological niche modeling to predict habitat suitability both in the Pleistocene and under future global warming scenarios. These analyses pointed toward a future decline in habitat suitability for subterranean spiders and the potential extinction of the most restricted endemic species. When compared with other species that live in confined habitats such as islands and mountains, we expect cave species to be as much, if not more, vulnerable to climate change.
... Although natural cavities (e.g., caves) can be formed by various mechanisms (e.g. volcanic, glacial, mechanical and erosion/ solution processes) in different climates, rock formations, and biogeographical regions, most of them share abiotic characteristics, such as limitation of light, stable and narrow ranges of temperatures, and often high relative humidity (Howarth, 1993(Howarth, , 1983(Howarth, , 1980Howarth and Moldovan, 2018;Mammola, 2019;Poulson and White, 1969). The communities of these habitats are strongly shaped by environmental filtering and can include species with different levels of affinities and adaptations to the subterranean habitats. ...
Article
Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also constitutes a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.
... Thus, caves in very cold or desert regions have a markedly depauperated or even inexistent fauna, and besides direct bioclimatic reasons (Howarth, 1980;Culver et al., 2006), some authors have argued that this may be caused by the fact that organic matter hardly ever reaches the deep layers in these environments . As in caves nutrient input is allochthonous (Culver, 1982;Howarth, 1983; but also see, for instance, Sarbu, 2000or Hutchins, Engel, Nowlin, & Schwartz, 2016, subterranean species richness variation is related to primary productivity at the surface, as suggested by the high biodiversity spots located in highly productive latitudinal bands (Culver et al., 2006;Gibert & Deharveng, 2002). ...
Article
Full-text available
The aim of this study was to unravel the relative role played by speleogenesis (i.e., the process in which a cave is formed), landscape-scale variables, and geophysical factors in the determination of species richness in caves. Biological inventories from 21 caves located in the southeastern Iberian Peninsula along with partial least square (PLS) regression analysis were used to assess the relative importance of the different explanatory variables. The caves were grouped according to the similarity in their species composition; the effect that spatial distance could have on similarity was also studied using correlation between matrices. The energy and speleogenesis of caves accounted for 44.3% of the variation in species richness. The trophic level of each cave was the most significant factor in PLS regression analysis, and epigenic caves (i.e., those formed by the action of percolating water) had significantly more species than hypogenic ones (i.e., those formed by the action of upward flows in confined aquifers). Dissimilarity among the caves was very high (multiple-site β sim = 0.92). Two main groups of caves were revealed through the cluster analysis, one formed by the western caves and the other by the eastern ones. The significant-but low-correlation found between faunistic dissimilarity and geographical distance (r = .16) disappeared once the caves were split into the two groups. The extreme beta-diversity suggests a very low connection among the caves and/or a very low dispersal capacity of the species. In the region under study, two main factors are intimately related to the richness of terrestrial subterranean species in caves: the amount of organic material (trophic level) and the formation process (genesis). This is the first time that the history of a cave genesis has been quantitatively considered to assess its importance in explaining richness patterns in comparison with other factors more widely recognized.
... This relative constancy of the environment may also be a selective factor in the evolution of subterranean species, especially in having to cope with the absence of daily cycles (Poulson, 1963). Howarth (1980) argues that relative humidity itself is an important selective factor and a factor that isolates animals in caves because of cuticular thinning. More generally, reduced organic matter and nutrients have been invoked as important selective factors in the evolution of reduced metabolic rate (Hüppop, 2000), foraging behavior (Bilandžija et al. 2013), and increased egg size (Rouch, 1968). ...
Article
Full-text available
Sistema Muévelo Rico is a 1.2 km long cave in Quintana Roo, less than 2 km from the Caribbean Sea. We measured illuminance to a level of 0.1 lux, organic matter (weight loss on ignition), temperature, and relative humidity. The last two were measured at hourly intervals for nearly one year. Approximately one-third of the cave has illuminance values greater than 0.01 lux, and most of the rest of the cave has light as well. Temperature and relative humidity were relatively constant, but they showed a daily cycle at all stations, albeit with different strengths. Organic matter averaged 8%, intermediate in value between surface and aphotic zones. Both eyeless species and eyed predators occurred throughout the cave. Their occurrence can best be explained by their foraging for organic matter and incurring an increased risk of predation.
... During the evolution of troglobitic species, other adaptations besides the reduction in thickness of the integument likely also occur. The high air humidity in the cave environment (Howarth, 1980;Sp€ otl et al., 2005) can be expected to contribute to the reduction of structures limiting water vapor permeability of the integument, as evaporative water loss is a minor problem to subterranean animals. It is known that troglophilic and troglobitic terrestrial arthropods may possess smaller amounts of cuticular lipids than epigean species (Hadley et al., 1981) and display greater cuticular water permeability (Ahearn and Howarth, 1982). ...
... Identified zones include the entrance zone, where there is direct light and climate influence from the exterior; the twilight zone, where there is no direct incidence of solar light; and the aphotic zone, where there is a total and permanent absence of light. The aphotic zone is the least affected by surface conditions (Poulson and White 1969;Howarth 1979). ...
Article
The subterranean environment has a set of unique characteristics, including low thermic variation, high relative humidity, areas with total absence of light and high dependence on nutrient input from the epigean environment. Such characteristics promote distinct ecological conditions that support the existence of unique communities. In this work, we studied seven caves in the Presidente Olegário municipality, Minas Gerais state, Southeast Brazil, to determine their richness of predatory species, to understand how they are spatially distributed in the cave and whether their distribution is influenced by competition and/or predation. We carried out five surveys of the caves, with each cave divided into sampling plots. We collected fauna within the plots using a manual search method. The collected animals were fixed in 70% ethanol for later identification. We performed a canonical correspondence analysis to verify the spatial distribution and substrate preference of each species, and selected five species for agonistic interaction testing in the laboratory. We found a great richness of predators in the caves, with 79 species distributed among 22 families of spiders, five families of pseudoscorpions, three families of chilopods, two families of opilionids and one family each of scorpions and heteroptera. Spiders were the most species diverse and abundant of all arthropods we found in the caves. We recorded evidence of competition among some pairs of species but, in general, the spatial distribution of the predatory community in the interior of the caves seems to be unrelated to interspecies competition. The laboratory pairings support our field observations that most species merely share space, rather than exhibiting aggressive or predatory behaviour.
... The role of relative humidity as an important limiting factor for the subterranean fauna is widely recognized (e.g. Boyer-Lef evre, 1971;Howarth, 1980;Tobin et al., 2013;Mammola et al., 2015b). Accordingly, the local low microclimatic suitability during drier periods likely determined a significant reduction in the dimension of the realized niche of the two species. ...
... For example, many recent debates focus on the mechanism responsible for regressive evolution such as the reduction and loss of eyes (Culver and Wilkens 2000, Christiansen 2012, Klaus et al. 2013, Krishnan and Rohner 2016). An old but still unsettled question concerns the apparent higher diversity of troglomorphic animals in temperate rather than in tropical regions (Howarth 1980, Culver and Sket 2000, Deharveng and Bedos 2012. And quite mysterious is the fact that only certain groups in any major taxon have entered caves and adapted to subterranean life while close relatives present in the same region have not (e.g., 91% of cave beetles are members of only two out of 166 beetle families; Moldovan 2012; see also Christiansen 2012). ...
Article
Full-text available
Pholcidae are ubiquitous spiders in tropical and subtropical caves around the globe, yet very little is known about cave-dwelling pholcids beyond what is provided in taxonomic descriptions and faunistic papers. This paper provides a review based on a literature survey and unpublished information, while pointing out potential biases and promising future projects. A total of 473 native (i.e. non-introduced) species of Pholcidae have been collected in about 1000 caves. The large majority of cave-dwelling pholcids are not troglomorphic; a list of 86 troglomorphic species is provided, including 21 eyeless species and 21 species with strongly reduced eyes. Most troglomorphic pholcids are representatives of only two genera: Anopsicus Chamberlin & Ivie, 1938 and Metagonia Simon, 1893. Mexico is by far the richest country in terms of troglomorphic pholcids, followed by several islands and mainland SE Asia. The apparent dominance of Mexico may partly be due to collectors’ and taxonomists’ biases. Most caves harbor only one pholcid species, but 91 caves harbor two and more species (up to five species). Most troglomorphic pholcids belong to two subfamilies (Modisiminae, Pholcinae), very few belong to Smeringopinae and Arteminae, none to Ninetinae. This is in agreement with the recent finding that within Pholcidae, microhabitat changes in general are concentrated in Modisiminae and Pholcinae.
... For site 1 on SMMR this result suggests that its relatively low levels of genetic diversity are due to prolonged isolation rather than a recent population reduction. In general, cave environments are relatively stable (Howarth 1980), which might minimize the likelihood of bottleneck events. ...
Article
Full-text available
Cave ecosystems supporting a variety of endemics depend on the carbon, nitrogen, and nutrients brought into caves by trogloxenic species, such as the secret cave cricket (Ceuthophilus secretus). Surface movements of trogloxenes may comprise the strongest ecological connections among caves. Our objective was to better understand dispersal patterns in C. secretus in order to inform management of this species and the cave endemics that depend upon them. We used microsatellite loci to estimate gene flow and genetic diversity among 42 karst features supporting C. secretus on the Fort Hood Military Reserve, Texas, USA. This sampling was used to assess the influences of karst topography and other landscape features on genetic diversity and population structure. Cave populations did not exhibit evidence of recent bottlenecks and genetic diversity was similar among sites, with the exception of one sample from an isolated cave. Samples exhibited a strong pattern of isolation by distance, but karst topology was also influential, with genetic differentiation being much higher between samples from separate ridges than among those on the same ridge. It appears that co-location on a ridge was an important factor facilitating dispersal among karst features. There was little evidence that other surface features such as forest cover, roads or streams influenced gene flow and genetic differentiation. The low genetic connectivity among ridges suggests that isolated caves on ridges where cricket habitat is uncommon or degraded might not be easily recolonized after extinction events, with potentially negative consequences for associated cave communities.
... Until relatively recently the groundwater fauna of Australia was very poorly known (Marrnonier et al. 1993), and that mostly from the investigation of cave faunas in the eastern portion of the continent (Thurgate et al. 200la;2001b). Western Australia has been considered to have poor prospects for supporting subterranean faunas, owing to the lack of water and low nutrient input from xeric plant communities (Moore 1964;Hamilton-Smith 1967;Barr 1973;Howarth 1980). Knowledge of this region, however, has developed substantially in the last decade, such that it is now recognized to include one of the world's most diverse and notable subterranean faunas (Holthuis 1960;Humphreys 1992, 1998;Wilson and Ponder 1992;Bartsch 1993;Humphreys 1993aHumphreys , 1993bHumphreys , 1993cHumphreys , 2000Humphreys , 2001Bruce and Humphreys, 1993;Harvey et al. 1993;Aubrecht and Kozur 1995;Baltanas and Danielopol 1995;Yager and Humphreys 1996;Bradbury and Williams 1996a, 1997a, 1997bHarvey 1998;Knott and Halse 1999;Bradbury 2000Bradbury , 2002Watts and Humphreys 2000, 2001, 2003Moore et al. 2001;Marrnonier 2002, 2003). ...
... From this, we can conclude that the long-term stable areas of high precipitation were important for subterranean terrestrial fauna. In such areas, humidity in subterranean habitats could remain high and constant over time, which is important for maintaining life functions (Racovitza, 1907;Howarth, 1980), especially in cave beetles, which have thinner cuticles than their epigean counterparts (Moldovan, 2012). Additionally, longterm stable areas of high precipitation can present larger input of organic matter going underground (Culver et al., 2006). ...
... Caves are zonal environments often consisting of four principal zones: (1) an entrance (or light) zone representing a combination of both surface and cave climatic conditions; (2) a twilight zone where light is diminished and surface climate conditions are progressively dampened; (3) a transition zone characterized by complete darkness with a further diminished influence of surface climate conditions; (4) a deep zone (usually the deepest portion of the cave) where environmental conditions (e.g., complete darkness, temperature, and air flow) remain relatively stable over time and the evaporation rate is negligible (Howarth 1980(Howarth , 1982. We provide zone designations for all Collembola specimens in the Material Examined section. ...
Article
Full-text available
Disparrhopalites naasaveqw n. sp. is described from a cave at Wupatki National Monument, Arizona. It differs from D. patrizii (Cassagnau & Delamare Deboutteville, 1953) in having pigment and a well-developed ungual cavity, and from D. tergestinus Fanciulli, Colla & Dallai, 2005 by having pigment, 8+8 eyes and a well-developed ungual tunica. Dietersminthurus enkerlinius Palacios-Vargas, Cuéllar & Vázquez, 1998 is transferred to Disparrhopalites Stach, 1956 as D. enkerlinius (Palacios-Vargas, Cuéllar & Vázquez, 1998) n. comb. The sminthurid subfamily Songhaicinae Sánchez-García & Engel, 2016 (type genus Songhaica Lasebikan, Betsch & Dallai, 1980) is redefined and the genera Disparrhopalites, Gisinurus Dallai, 1970, Soqotrasminthurus Bretfeld, 2005 and Varelasminthurus Da Silva, Palacios-Vargas & Bellini, 2015 are transferred to this subfamily. A key is provided for separation of included genera. Effects of climate change on presumed cases of cave restriction in the American Southwest are discussed.
... As reviewed by Peck and Finston (1993) for Hawaii, Galapagos, and Canarys there are many sister species and on this basis researchers have championed habitat shift colonization with parapatric speciation. 6. Pioneering work by Howarth et al. (1980) in pointing out high tropical Hawaiian troglobite diversity, as opposed to some views that tropical caves have few troglobites. 7. ...
... Biospeleology Terminology Cave systems generally consist of four zonal environments (Howarth 1980(Howarth , 1983: (1) entrance zone -a combination of surface and cave environmental conditions; (2) twilight zone -both diminished sunlight and dampened influence of surface environment; (3) transition zone -completely dark, but where surface weather and diurnal changes influence the cave environment; and, (4) deep zone -complete darkness, high environmental stability, constant temperature, and near water-saturated atmosphere with low to no air flow (typically occurs in the deepest portion of the cave). Cave-dwelling taxa fall broadly into four functional groups (from Barr 1968;Howarth 1983): (1) troglobiontobligate cave dwellers who only complete their life cycle within the deepest most stable reaches of the cave and exhibit morphological characteristics of adaptation to the cave environment; ...
Technical Report
Full-text available
This work represents the first large scale cave biological inventory of caves in Sierra de las Nieves Natural Park, Andalucía, Spain. We sampled seven caves (three low and four high elevation caves) from 22 June through 01 July 2017. We have preliminarily identified at least 42 morphospecies and 13 coarse-level taxonomic groups (i.e., Order or higher) of cave-dwelling arthropods including the relict springtail species, Onychiurus gevorum Arbea 2012. Bats were detected in two of three low elevation caves; a bat roost of unknown type consisting of approximately 100 bats was observed in one cave, and one bat (Myotis sp.) was found torporing in another cave. The common toad (Bufo bufo (Linnaeus, 1758)) was identified in two low elevation caves. We also provide recommendations for additional research to aid in the future management of these resources.
... This is not surprising as it has been amply demonstrated that terrestrial cave animals are often stenothermic and react to temperature differences already at the smallest of scales (e.g. [21][22][23][24]. ...
Article
Full-text available
Terrestrial life typically does not occur at depths greater than a few meters. Notable exceptions are massifs of fissured rock with caves and hollow spaces reaching depths of two kilometres and more. Recent biological discoveries from extremely deep caves have been reported as sensations analogous to wondrous deep sea creatures. However, the existence of unique deep terrestrial communities is questionable when caves are understood as integral parts of a bedrock fissure network (BFN) interconnecting all parts of a massif horizontally and vertically. We tested these two opposing hypotheses – unique deep cave fauna vs. BFN – by sampling subterranean communities within the 3D matrix of a typical karst massif. There was no distinction between deep core and shallow upper zone communities. Beta diversity patterns analysed against null models of random distribution were generally congruent with the BFN hypothesis, but suggested gravity-assisted concentration of fauna in deep caves and temperature-dependent horizontal distribution. We propose that the idea of a unique deep terrestrial fauna akin to deep oceanic life is unsupported by data and unwarranted by ecological considerations. Instead, the BFN hypothesis and local ecological and structural factors sufficiently explain the distribution of subterranean terrestrial life even in the deepest karst massifs.
... For example, during warmer and more humid seasons (spring and summer) many obligate and non-obligate subterranean taxa will forage in these ecotones and then move deeper into the subterranean environment during cooler and drier seasons (winter and fall). These movements are especially prevalent in obligate subterranean species as many have thinner cuticles which increases integument permeability and thus cannot tolerate low humidity environments (Howarth, 1980). The cavities that connect surface and subterranean environments also direct the flow of water across terrestrial subterranean environments. ...
Chapter
This article reports the current knowledge of trophic dynamics in both aquatic and terrestrial subterranean communities. Scarcity of nutrients characterizes subterranean food web interactions and drives opportunistic adaptive strategies. However, recent research contrasts the archetype of poorly structured food chains against emerging convoluted mechanisms sustaining a great range of biotic diversity and functional complexity. Novel analytical designs described in this work provide important new perspectives into the investigation of these key ecological dynamics, which, together with future advances, will enable the understanding of the immense conservational value of these often overlooked ecosystems.
... There are different hypotheses available to explain it. Simply put, animals either colonise caves to avoid harsh surface conditions (climate change, predation) or to exploit new resources provided by caves (Howarth 1980(Howarth , 1987Peck and Finston 1993;Danielopol and Rouch 2005;Culver and Pipan, 2009;Romero 2009). In both cases, colonisers are expected to show high innovativeness, especially when the most important resource, food, is completely novel in the colonised cave. ...
Article
Full-text available
Behavioural innovativeness is important for colonising new habitats; however, it is also costly. Along the colonisation event of a simple, stable and isolated habitat offering only new food sources, one could hypothesize that the colonising individuals are more innovative than the average in their source population, showing preference to the new resource, while after colonisation, the adapted population will lose its innovativeness and become specialised to the new resource. To test this hypothesis, we compared food preference and food type innovation of a cave-dwelling waterlouse ( Asellus aquaticus ) population (genetically isolated for at least 60 000 years) to three surface-dwelling populations, also sampling individuals that have recently entered the cave (‘colonists’). In the cave, the only food sources are endogenous bacterial mats, while surface populations feed on various living and dead plant material together with their fungal and bacterial overgrow. We assayed all populations with the familiar and unfamiliar food types from the natural habitats and two novel food types not occurring in the natural habitats of the species. We found that all populations preferred surface to cave food and consumed the unnatural novel food types. Surface populations avoided cave food and colonists spent the most time with feeding on surface food. We conclude that the cave population maintained its preference for surface food and did not lose its food type innovativeness. We suggest that adapting to the special cave food was a major challenge in colonising the cave. Significance statement Behavioural innovativeness is a key trait for adapting to environmental changes or to colonise new habitats. However, it has developmental and maintenance costs due to the high energy need of the necessary sensory and neural organs. Therefore, we asked whether behavioural innovativeness decreases after colonising an isolated, stable and highly specialised habitat. By comparing food type innovativeness of surface-dwelling populations of waterlouse ( Asellus aquaticus ) to a population that has colonised a cave at least 60 000 years ago, we found that the high innovativeness towards unnatural food was retained in the cave population. Further, all populations preferred surface food (decaying leaves), with surface populations almost completely avoiding cave food (endogenous bacteria mats). We suggest that (i) food type innovativeness is evolutionary rigid in our system and (ii) the cave food was rather an obstacle against than a trigger of cave colonisation.
... This strategy may be aided by the highly stable climate conditions offered by many deep cave environments, which are likely to help overcome some of the energetic challenges associated with fluctuations in environmental conditions (Tattersall et al. 2012, Stawski et al. 2014. Furthermore, this stability protects freeze-intolerant species against seasonal freezing temperatures experienced at the surface (Novak et al. 2014) and supports specialists adapted to narrow ranges of climate conditions (Peck 1976, Howarth 1980. Some species, however, bridge the subterranean and aboveground environments. ...
Article
Full-text available
Caves and other subterranean features provide unique environments for many species. The importance of cave microclimate is particularly relevant at temperate latitudes where bats make seasonal use of caves for hibernation. White‐nose syndrome (WNS), a fungal disease that has devastated populations of hibernating bats across eastern and central North America, has brought renewed interest in bat hibernation and hibernaculum conditions. A recent review synthesized current understanding of cave climatology, exploring the qualitative relationship between cave and surface climate with implications for hibernaculum suitability. However, a more quantitative understanding of the conditions in which bats hibernate and how they may promote or mediate WNS impacts is required. We compiled subterranean temperatures from caves and mines across the western United States and Canada to (1) quantify the hypothesized relationship between mean annual surface temperature (MAST) and subterranean temperature and how it is influenced by measurable site attributes, and (2) use readily available gridded data to predict and continuously map the range of temperatures that may be available in caves and mines. Our analysis supports qualitative predictions that subterranean winter temperatures are correlated with MAST, that temperatures are warmer and less variable farther from the surface, and that even deep within‐cave temperatures tend to be lower than MAST. Effects of other site attributes (e.g., topography, vegetation, and precipitation) on subterranean temperatures were not detected. We then assessed the plausibility of model‐predicted temperatures using knowledge of winter bat distributions and preferred hibernaculum temperatures. Our model unavoidably simplifies complex subterranean environments and is not intended to explain all variability in subterranean temperatures. Rather, our results offer researchers and managers improved broad‐scale estimates of the geographic distribution of potential hibernaculum conditions compared to reliance on MAST alone. We expect this information to better support range‐scale estimation of winter bat distributions and projection of likely WNS impacts across the west. We suggest that our model predictions should serve as hypotheses to be further tested and refined as additional data become available.
... the dark zone can often be subdivided into subzones based on the physical environment: a "transition zone" where the atmosphere within the passage is subjected to frequent disturbances resulting from weather and diurnal events occurring on the surface; a "deep zone" where the air remains permanently saturated or supersaturated with water vapor; and a "bad air zone" where air exchange with the surface is restricted and decomposition gases can accumulate. the presence and extent of each of these zones is delineated by the size and shape of the entrance(s) and passages (Howarth 1980(Howarth , 1987. ...
Article
Full-text available
We review the diversity of moths, Lepidoptera, known from caves in Hawai'i. Twenty-five spp are listed, of which 6 are alien, 3 are natives accidentally in caves; and 16 natives show morphological or behavioral traits to live in caves.
... Species limited to a subterranean environment are, in contrast to their soil-dwelling relatives, much more susceptible to desiccation due to the loss of most of the physiological mechanisms to control water balance. Since evaporation increases exponentially with rising temperature, subterranean species are considered to be capable of living exclusively within the areas with narrow temperature ranges (Peck, 1976;Howarth, 1980). The RDA analysis applied in this study revealed a general pattern of preferences of particular collembolan species to temperature parameters. ...
Article
Full-text available
A labyrinth of air-filled voids in forested scree slopes represents one of the most common types of terrestrial shallow subterranean habitats in the temperate zone, characterized by relatively strong seasonal fluctuations of temperature and the occurrence of subterranean species of invertebrates. We carried out a year-long study to define the monthly activity dynamics of Collembola communities inhabiting a depth profile (95 cm from the ground surface) of a forested limestone scree in the Western Carpathians, Slovakia. We assessed the response of species sorted into four separate ecological forms, reflecting their affinity to the subterranean environment and to temperature parameters fluctuating over the year. Of the 62 collembolan species identified, 28 were assigned to trogloxenes, 19 to subtroglophiles, 12 to eutroglophiles, and 3 to troglobionts. Fluctuations of activity/numbers during the year were observed in all four ecological forms of Collembola and at all depths. Troglobionts and eutroglophiles, associated predominantly with deeper layers of the scree slope profile, preferred the lower temperature ranges and were typical for the autumn months. Trogloxenes and subtroglophiles were active most of the year near the surface, but specifically during the spring months characterized by higher temperature ranges. The study contributes to the general knowledge of dynamics of invertebrate activity in a forested temperate zone scree slope.
... Caves breathe largely owing to changes in barometric pressure and temperature, and the resulting mass movement of air transfers heat and moisture into and out of a cave depending on the vectors of the pressure differential. Even in the absence of air movement, caves may lose or gain moisture owing to water vapour pressure gradients that cause excessive drying of caves in the temperate winter and at night in the tropics when external temperature falls below cave temperature (the tropical winter effect; Howarth 1980). Recording cave climate is especially difficult in remote areas where changes are frequent (diurnal) and remote (deep into cave in distance or time) or the magnitude of change is great (closer to entrances). ...
Chapter
The chapter anticipates the application of new or emerging methodological, technological and analytical approaches to the discipline of subterranean ecology. It notes the lack of basic biology (natural history) available for subterranean species outside the northern temperate zone and the disparity of knowledge across regions. It highlights the importance of establishing and contributing to open-access regional and global biodiversity data bases including genetic data bases. It examines idiosyncratically selected areas of subterranean ecology that are considered likely to progress partly through the application of these methodologies. It also covers areas of ecology judged to have been neglected in the context of subterranean ecosystems. Included are the general topics of methodological and technological innovations, basic biology (natural history), enumeration and movement, sampling in terrestrial and aquatic systems, diversity and the potential of metagenomics (eDNA), food sources and species interactions, the transition to subterranean life (trogloneogenesis), cave climate and climate change and biofilms and biogeochemistry. It considers the age of subterranean lineages to a proxy for the circumstances that drove the lineage underground and concludes to be alert for the possibility of opportunistic field experiments.
... Among the invertebrate groups occurring in caves, ants have been frequently documented in both Brazil (Ferreira, 2000;Dáttilo et al., 2010;Dáttilo et al., 2012, Ferreira, 2019 and in the world (Wilson, 1962;Tinaut & Lopez, 2001;Roncin & Deharveng, 2003;Moulds, 2006;Batucan & Nuñeza, 2013;Figueras & Nuňeza, 2013;Wynne & Voyles, 2013;Dejean et al., 2015;Pape, 2016;Naka & Maruyama, 2018). Some ant species have characteristics that favor life in subterranean environments, especially hypogaeic foraging species, which have a great affinity for underground environments and can easily penetrate into deep zones of some caves (Pape, 2016), where there is a stable moisture-saturated atmosphere (Howarth, 1980;Howarth, 1983). Besides their use of pheromones for navigation, ants have a metapleural gland that secretes antimicrobial substances (Poulsen et al., 2006;Beattie, 2010). ...
Article
Full-text available
Subterranean habitats may be considered limiting for animal colonization, especially for ants, due to permanent darkness and mainly because of oligotrophic conditions. While not as deep as limestone caves, iron ore caves and other subterranean habitats may be more available for colonization because of their shallower depth. We use the richness and composition of ants to assess how differences in habitat structure affect the biodiversity and ecosystem function between cavities and surrounding epigean landscapes. We predicted that the distribution of ants would be different because of the variation in habitat structure and cavity conditions may act as a filter for colonization by ants. A high diversity of ants was found in the 20 sampled cavities (26 species), and most of them were grouped in the generalist trophic guilds. The distribution of ants occurred independently of the type of cavity to which they are associated (caves, impacted caves and mines). Significant differences were observed in ant richness between epigean and cavities habitats, with lower average richness in cavities. The physical attributes of the cavities did not influence richness, mainly because cavity use by ants can usually be explained by their opportunistic habits and generalist lifestyle. Ants can participate directly in the cavities assemblage, playing roles in species composition and trophic functionality, due to the lower use restriction.
... Cave ecosystems typically consist of four environmental zones (Howarth 1980(Howarth , 1983: (1) entrance zone-or light zone, which represents a combination of surface and cave environmental conditions; (2) twilight zone-occurring slightly deeper within the cave and has both diminished light conditions and direct in uence of surface environment; (3) transition zone-aphotic, yet barometric and diurnal shifts may still occur at a signi cantly diminished rate, but the climate is approaching near stable conditions; and, (4) deep zone-complete darkness, high environmental stability, near stable temperature, near water-saturated atmosphere, and low to no air ow (usually in the deepest part of the cave). e deep zone represents the region most conducive to supporting subterranean-adapted animals. ...
Article
Full-text available
We summarize and discuss the 29 known cave-dwelling pseudoscorpion species from China. Four new troglomorphic pseudoscorpion species, Parobisium motianense sp. nov., P. qiangzhuang sp. nov., P. san- louense sp. nov., and P. tiani sp. nov., belonging to the family Neobisiidae, are described based on speci- mens collected in karst caves in Guizhou, China. Detailed diagnosis, descriptions, and illustrations are presented. We also provide recommendations for management of caves where they occur, as well as the cave arthropod communities and the habitats that support them.
... Terminology. The cave environment is typically divided into four environmental zones (refer to Howarth 1980Howarth , 1983: (1) entrance zone-the combination of surface and cave environmental conditions; (2) twilight zone-both diminished light conditions and influence of surface environment; (3) transition zone-aphotic, yet barometric and diurnal shifts are observed at a significantly diminished rate approaching near stable climatic conditions; and, (4) deep zone-complete darkness, high environmental stability, constant temperature, near water-saturated atmosphere, and low to no airflow (usually occurs in the deepest part of the cave). The cave deep zone represents the region most conducive to supporting subterranean-adapted animals. ...
Article
Full-text available
Two new troglomorphic pseudoscorpion species, Parobisium magangensis sp. n. and P. yuantongi sp. n., belonging to the family Neobisiidae, are described based on specimens collected in karst caves from Beijing, China. These are the first troglomorphic pseudoscorpions discovered from caves in northern China. Detailed diagnosis, descriptions, and illustrations are provided. We also offer future research and management recommendations for these two new pseudoscorpion species.
... The presence of such highly troglomorphic Coecobrya in Satun province is unexpected and raises evolutionary questions relative to the climatic drivers of colonisation, diversifica-tion and adaptation. Following the discovery of a rich troglobitic fauna in the lava tube fauna of Hawaii, Howarth (1973) was the first to challenge the view that cave adapted species were absent or exceptional in the tropics and proposed a bioclimatic model to account for this (Howarth 1980). This presence of true troglobites under tropical climate was later confirmed by Deharveng (1987) for Collembola. ...
Article
Full-text available
The most highly troglomorphic Collembola of Southeast Asia, Coecobryasirindhornaesp. n. , is described from a cave in Satun province, Thai Peninsula. It is characterised by its large size, extremely elongated antennae, relatively long legs and furca, reduced macrochaetotaxy, very long and slender claw, pointed tenent hair, four sublobal hairs on outer maxillary lobe, and the absence of eyes and pigmentation. A checklist of Thai Coecobrya species and a key to the troglomorphic species of Thailand are provided. Troglomorphy and conservation of cave habitats in the area are discussed.
... As caves are strongly zonal habitats, this is often a useful approach for dividing the cave into more manageable sampling units. Four principal zones are recognized: two photic (light and twilight) and two aphotic (transition and deep; Howarth, 1980). Howarth & Stone (1990) described a fifth environmental zone, the "bad air" zone, which is beyond, and technically a subdivision of, the deep zone. ...
Article
Full-text available
Ever-increasing human pressures on cave biodiversity have amplified the need for systematic, repeatable, and intensive surveys of cave-dwelling arthropods to formulate evidence-based management decisions. We examined 110 papers (from 1967 to 2018) to: (i) understand how cave-dwelling invertebrates have been sampled; (ii) provide a summary of techniques most commonly applied and appropriateness of these techniques, and; (iii) make recommendations for sampling design improvement. Of the studies reviewed, over half (56) were biological inventories, 43 ecologically focused, seven were techniques papers, and four were conservation studies. Nearly one-half (48) of the papers applied systematic techniques. Few papers (24) provided enough information to repeat the study; of these, only 11 studies included cave maps. Most studies (56) used two or more techniques for sampling cave-dwelling invertebrates. Ten studies conducted ≥10 site visits per cave. The use of quantitative techniques was applied in 43 of the studies assessed. More than one-third (42) included some level of discussion on management. Future studies should employ a systematic study design, describe their methods in sufficient detail as to be repeatable, and apply multiple techniques and site visits. This level of effort and detail is required to obtain the most complete inventories, facilitate monitoring of sensitive cave arthropod populations, and make informed decisions regarding the management of cave habitats. We also identified naming inconsistencies of sampling techniques and provide recommendations towards standardization.
... Since saturated air is above the equilibrium humidity of bodily fluids, troglobionts must deal with excess water rather than desiccation. In doing so, they have lost many attributes (such as reduction and change in composition of cuticular hydrocarbons and of thinning of the cuticle) that conserve water and have become highly sensitive to desiccation (Howarth 1980;Ahearn and Howarth 1982;Hadley et al. 1981). ...
Chapter
Why certain animals lose features believed essential, like eyes, bodily color, and robustness, to live permanently underground has long intrigued biologists and laymen. Many of these features evolved independently and shared among diverse groups living in caves including both terrestrial and aquatic cavernicoles. The degree of change often correlates with the level of association of the species to caves. This association allowed development of a classification scheme to help understand the evolutionary ecology of cave communities. The refined scheme, called the Schiner-Racovitza system, is based on both morphology and ecology. The categories are troglobionts and stygobionts (animal species that obligately live underground on land or in water, respectively), troglophiles (animals that can live and reproduce in both underground and surface habitats), and trogloxenes (animals that regularly visit caves for food or refuge). Common adaptations to cave life involve morphology, behavior, and physiology. In addition to the conspicuous losses, many compensatory traits have evolved, such as longer appendages, longer and more slender body, more and larger sensory structures, and specialized mouthparts and tarsi. Modified behavioral traits include reduction in circadian rhythm, reduced dispersal ability, slower but nearly continuous activity, and modified mating behavior. Physiological adaptations include low metabolism rate, dietary changes, resistance to starvation, modified water balance mechanisms, tolerance to high CO2 and low O2, and increased longevity. Cave-adapted animals also display greater K-selection with fewer and larger eggs and reduced life cycle.
Technical Report
Relevance analysis and Speleological diagnosis of Fazenda dos Borges Project [in Portuguese]
Article
Full-text available
World experts of different disciplines, from molecular biology to macro-ecology, recognize the value of cave ecosystems as ideal ecological and evolutionary laboratories. Among other subterranean taxa, spiders stand out as intriguing model organisms for their ecological role of top predators, their unique adaptations to the hypogean medium and their sensitivity to anthropogenic disturbance. As the description of the first eyeless spider (Stalita taenaria), an array of papers on subterranean spider biology, ecology and evolution has been published, but a comprehensive review on these topics is still lacking. We provide a general overview of the spider families recorded in hypogean habitats worldwide, we review the different adaptations of hypogean spiders to subterranean life, and we summarize the information gathered so far about their origin, population structure, ecology and conservation status. Finally, we point out the limits of the knowledge we currently have regarding hypogean spiders, aiming to stimulate future research.
Article
Full-text available
Egg attendance is the most common and phylogenetically widespread form of post-ovipositional care among ectotherms. The main benefit of egg attendance is to enhance offspring survival by preventing or attenuating attacks from natural enemies. In arachnids, there are few experimental studies on the benefits of egg attendance, and they pertain to species living in few types of habitats, mainly forests. To understand how the benefits of egg attendance vary in large geographical scales, we need to include species from poorly explored habitats, such as caves. Here, we describe a case of maternal egg attendance in an exclusive cave-dwelling harvestman, Phalangodus briareos. Using a parent removal experiment, we also assessed the benefits of egg attendance. We found that egg attendance improves egg survival because unattended clutches were almost entirely consumed by conspecifics and crickets. When females were maintained on their clutches, egg survival was always high, regardless of female body size. There was a positive effect of clutch size on egg predation, which was higher during nighttime. We suggest that larger clutches emit more chemical cues, attracting more predators in the cave habitat. Finally, we argue that the benefits of egg protection should be higher inside caves when compared to external habitats because food is scarce inside caves and the fauna consists mainly of predators and detritivores.
Article
Full-text available
Two new species of troglomorphic pseudoscorpions of the family Neobisiidae, collected from karst caves in Yunnan, China, are described: Parobisium laevigatum sp. n. and P. muchonggouense sp. n.. A key to the Parobisium species from China is also provided.
Chapter
Full-text available
Almost all orders of Arachnida are represented in caves, except for Solifugae. In some orders (Pseudoscorpiones) there are many troglobitic blind species. Such species are found also among spiders, scorpions, opilions, and others. Further species are prospected in different groups and regions of the World, and the ways in which Arachnida have invaded the caves are discussed here (especially the new discoveries in tropical caves, the subterranean fauna of Hawaii, Galapagos, and unusual caverns such as Movile and Ayalon).
Preprint
Full-text available
Relative humidity (RH) was measured at hourly intervals for approximately one year in two caves at seven stations near Playa del Carmen in Quintana Roo, Mexico. Sistema Muévelo Rico is a 1.1 km long cave with 12 entrances and almost no dark zone. Río Secreto (Tuch) is a large river cave with more than 40 km of passages, and an extensive dark zone. Given the need for cave specialists to adapt to saturated humidity, presumably by cuticular thinning, the major stress of RH would be its deviation from saturation. RH in Río Secreto (Tuch) was invariant at three sites and displayed short deviations from 100% RH at the other four sites. These deviations were concentrated at the end of the nortes and beginning of the rainy season. Three of the sites in Sistema Muévelo Rico showed a similar pattern although the timing of the deviations from 100% RH was somewhat displaced. Four sites in Sistema Muévelo Rico were more variable, and were analyzed using a measure of amount of time of deviation from 100% RH for each 24 hour period. Strong seasonality was evident but, remarkably, periods of constant high humidity were not the same at all sites. In most Sistema Muévelo Rico sites, there was a detectable 24 hour cycle in RH, although it was quite weak in about half of them. For Río Secreto (Tuch) only one site showed any sign of a 24 hour cycle. The troglomorphic fauna was more or less uniformly spread throughout the caves and did not concentrate in any one area or set of RH conditions. Compared to temperature, RH is much more constant, perhaps even more constant than the amount of light.
Article
Full-text available
1. Scientists are renewing their efforts to predict the impact of climate change on biodiversity. Subterranean environments represent ideal systems to study the effect of global change in species with poor dispersal capabilities. 2. We assess the vulnerability to climate change of the subterranean pseudoscorpion Neobisium (Blothrus) vasconicum vasconicum (Nonídez, 1925) (Neobisiidae). 3. Thermal tolerance was measured using two complementary estimates of upper thermal limits: (i) from thermal conditions of the localities in which the species occurs (realised upper thermal limit, RUTL), and (ii) from experimentally determined thermal tolerance data (physiological upper thermal limit, PhUTL). Then, thermal safety margins (TSM) were calculated for all known localities for current and future climatic conditions, using the thermal limits from both approaches. 4. The physiological thermal limit (PhUTL = 17.57 C) was 3.27 C higher than that obtained from the distributional and climate data (i.e., the hottest cave in which the species occurs; RUTL = 14.3 C). Regarding TSM, the future temperature (2070; RCP 8.5) of a half of the caves will be higher than the RUTL and in none of them, it would exceed the average PhUTL. This indicates that the species could have some physiological capacity to cope with warming temperatures in situ. 5. We hypothesize that the most realistic upper thermal limit of the species could be between the RUTL and PhUTL. This study shows that complementary approaches to estimate thermal tolerance could provide more accurate predictions of the capacity to face climate change, not only in subterranean species, but also in poor dispersal species.
Chapter
As factors of distribution of Arachnida are outlined paleogeography and paleodistribution, age of groups, barriers, bridges, ability to overcome them, phoresy, dispersal, climate, orography and many other fundamental concepts.
Chapter
The arachnofauna of various parts of the Earth is analyzed and the particularities, endemics, relicts, and the presumed ways of formation of the fauna are outlined. Also the northern limits of the groups in the Holarctic are indicated, and the connections in the geological time are analyzed.
Article
We synthesized the current knowledge of cave-dwelling millipede diversity from Guangxi Zhuang Autonomous Region (Guangxi), South China Karst, China and described six new millipede species from four caves from the Guilin area, northeastern Guangxi. Fifty-two cave-dwelling millipedes are known for the region consisting of 38 troglobionts and 14 troglophiles. Of the troglobionts, 24 are presently considered single-cave endemics. New species described here include Hyleoglomerisrukouqu sp. nov. and Hyleoglomerisxuxiakei sp. nov. (Family Glomeridae), Hylomusyuani sp. nov. (Family Paradoxosomatidae), Eutrichodesmusjianjia sp. nov. (Family Haplodesmidae), Trichopeltisliangfengdong sp. nov. (Family Cryptodesmidae), and Glyphiulusmaocun sp. nov. (Family Cambalopsidae). Our work also resulted in range expansions of Pacidesmustrifidus Golovatch & Geoffroy, 2014, Blingulussinicus Zhang & Li, 1981 and Glyphiulusmelanoporus Mauriès & Nguyen Duy-Jacquemin, 1997. As with many hypogean animals in Southeast Asia, intensive human activities threaten the persistence of both cave habitats and species. We provide both assessments on the newly described species’ distributions and recommendations for future research and conservation efforts.
Article
Full-text available
Differences between tropical and temperate cave communities are an important topic in the actual biospeleological thinking. Among the most striking differences is the paucity of terrestrial troglobites in tropical caves. This fact may depend on the higher energy input into tropical caves which lessens the selection pressures for energy-economizing troglobite adaptations. Consequently evolutionary rates would be slowed in tropical caves and, in a date group, troglobites would appear later in such caves than in temperate ones with lower energy input. In order to investigate this point the authors studied the degree of adaptation to the cave environment in two species of Mexican Ptomaphagus which, being phylogenetically related, probably descend from the same epigean ancestor. Among these species the first one, P. troglomexicanus Peck, lives in a typical temperate cave (i.e. cold, high altitude cave, with scarce food supply) in the Sierra de Guatemala (Tamaulipas), the other one, P. spelaeus (Bilimek), populates tropical caves (i.e. warm, lowland cave, with rich food supply) in the State of Guerrero. In addition a comparison is made with P. pius Seidlitz, an epigean species from southern Europe. The results show a striking difference between P. troglomexicanus on a side and the other two species. Differences chiefly concern morphological features such as relative antenna length, structural complexity (i.e. the number of sensilla) of the antenna chemioreceptor organs in the 70, 90, 100 segments, degree of reduction of eye, wing and pigmentation and physiological ones such as the length of the life cycle. The possible causes of these differences are discussed. According to the authors these differences appear due to the different selection pressures acting in the two types of caves. In addition a comparison between the “tropical cave” species, P. spelaeus, with the epigean one, P. pius, does not point out the differences that one could expect by the diverse ecology of these species. These observations support the idea that evolutionary rates in cavernicoles are strongly affected by the ecology of the cave, mainly depending on the degree of energy input, and are poorly consistent with the hypothesis that mutations affecting degenerative processes are selectively neutral.
Article
Full-text available
Hamann’s organ in Leptodirus hohenwarti a highly specialized cave Bathysciinae, has been studied under the TEM, SEM and light microscope. This receptor organ located in the 7th, 9th and 10th antennal articles and previously referred to as the “vesicule olfactive” and as the “antennal organ” or “antennal vesicle”, reaches its highest degree of structural complexity in leptodirus. This paper attempts to establish some degree of synonymy among the terms used by earlier authors in describing the various antennal parts and sensilla. Five types of sensilla to be found in the organ are described, namely cribrose-stick sensilla, cribrose-utricular sensilla, star-shaped sensilla, claviform sensilla and branching setae. Comparisons within Bathysciinae species and among the latter and other subfamilies of Catopidae reveal differences in the number of vesicles and in the number and structures of sensilla, these differences appear to depend on i) the degree of phylogenetic relationships among taxa and 2) the degree of specialization to cave environment. The considerable complexity of Hamann’s organ, unrivalled by other insects organs, apart from light receptors, suggests that it has a plurality of functions. Its hygroreceptor role, supported by recent experimental work, is discussed here.
Article
Full-text available
The scattered literature on the physical speleology and biospeleology of the West Indian island of Jamaica is brought together. As a result of recent field work, a summary of the Jamaican vertebrate and invertebrate caves is given. The invertebrate fauna is known to include some 150 free-living macroscopic species. These are mostly troglophilic scavengers and predators associated with guano accumulations. However, some 25 species, mostly terrestrial and undescribed, are known to be troglobites. This is one of the largest known assemblages of tropical troglobites. Brief descriptions are given for the 54 cave sites which have been biologically studied.
Article
Full-text available
The humidity responses of Bathysciola derosasi and Leptodirus hohenwarti, two species of troglobitic Bathysciinae showing different degrees of adaptation to cave environment, have been studied. Intact and antennectomised subjects were tested using choice-chambers with various combinations of relative humidity alternatives (i.e. 20-100%, 50-100%, 90-100%, 50-90% and, as controls, 100-100%) to investigate the role played by the sense organs situated on the 7th, 9th and 10th antenna segments. The results show that intact-antenna subjects of both species are very sensitive to humidity gradients and that their intensity of reaction varies according to the intensity of stimulus, as previously reported by Argano, Sbordoni and Cobolli Sbordoni (1969). The antennectomy experiments show that receptors situated on the 7th, 9th and 10th antenna segments (Hamann’s organ) are involved in hygroreception. In Leptodirus, insects antennectomised below the 9th segment show a reduced intensity of reaction, while those antennectomised below the 7th segment show no positive response at all. This seems to indicate that receptors in the 9th and 10th antennal segments have additive roles beyond that of the 7th. Further research is needed to ascertain whether the antennal organs of Bathysciinae may have yet further additional sensory roles (e.g. chemioreception) as their complex structure suggests.
Article
Full-text available
Seventy-eight species of free-living invertebrates are known to inhabit caves in Puerto Rico. Of the 52 determined species, 23 are also known from the American mainland, 6 are West Indian, and 23 are endemic to Puerto Rico. Sixteen of the endemics are known from non-cave habitats, while the non-endemic species are usually known associated with caves in other parts of their range. Ninety percent of the total fauna is troglophilic, with only two definitely troglobitic species known. In feeding habits, the fauna is composed of 55 percent guano scavengers, detritivores, and herbivores, and 45 percent predators. Most, if not all the fauna, including the troglobites, probably has a short history of association with Puerto Rican cave habitats dating only since the Pleistocene. The species make-up of the troglophilic component of the community is dynamic and liable to change, even over short time spans, and hence can serve as an experimental system for the study of principals of island zoogeography.
Article
Full-text available
The invertebrate fauna known from within the caves at Jenolan is inventoried and summarised. At least 136 individual taxa have been identified although less than one-half (43%) are assigned to described species, the rest are either undescribed (8%) or have only been identified to genus level (31%) or higher taxa (18%). The collected fauna is dominated by arachnids (47%) and collembolans (24%) followed by insects (15%) and crustaceans (6%) with three or fewer taxa identified in each of the remaining groups comprising molluscs, diplopods, chilopods, annelids, platyhelminths and nematodes. In terms of ecological dependence on caves, 53% of collected taxa comprised typically epigean species with the remainder considered to be habitual cave-dwellers. Eight species (revised from 14 previously) are considered to be obligate hypogean species (terrestrial troglobites or aquatic stygobites) comprising three species of springtail, two spiders, a pseudoscorpion and two aquatic crustaceans. The diversity of troglobite species is fairly typical for karst areas in the eastern highlands of NSW but higher unrecorded diversity of stygobite species is predicted. While the invertebrate cave fauna of Jenolan has received more attention from biologists than any other karst area in NSW, substantial knowledge gaps remain. Research and conservation priorities are: (1) identify existing collections and describe new species, focussing on troglomorphic taxa which are likely to be locally endemic and of conservation significance; (2) targeted field surveys for rare troglomorphic taxa which are under-represented in existing collections; (3) sample for aquatic micro-crustacea and other stygofauna in vadose zone, phreatic zone and interstitial habitats; (4) sample for troglobites in meso-cavern and other cryptic terrestrial habitats.
Article
Full-text available
The Hawaiian Islands offer great potential for evolutionary research. The discovery of specialized cavernicoles among the adaptively radiating fauna adds to that potential. About 50 lava tubes and a few other types of caves on 4 islands have been investigated. Tree roots, both living and dead, are the main energy source in the caves. Some organic material percolates into the cave through cracks associated with the roots. Cave slimes and accidentals also supply some nutrients. Lava tubes form almost exclusively in pahoehoe basalt, usually by the crusting over of lava rivers. However, the formation can be quite complex. Young basalt has numerous avenues such as vesicles, fissures, layers, and smaller tubes which allow some intercave and interlava flow dispersal of cavernicoles. In older flows these avenues are plugged by siltation or blocked or cut by erosion. The Hawaiian Islands are a string of oceanic volcanic islands stretching more than 2500 km across the mid-Pacific. The western islands are old eroded mountains which are now raised coral reefs and shoals. The eight main eastern islands total 16,667 km 2 and are relatively young in geologic age. Ages range from 5+ million years for the island of Kauai to 1 million years for the largest island, Hawaii (Macdonald & Abbott, 1970). The native fauna and flora are composed of those groups which dis-persed across upwards of 4000 km of open ocean or island hopped and became successfully established. Thus the fauna is remarkably disharmonic. The disharmony on oceanic islands has been discussed by Zimmerman (1948) and Gressitt (1971). Zimmerman (1948) estimated that only 250 successful introductions to the Hawaiian Islands have given rise to the entire native insect fauna of more than 5000 species. The aquatic, soil, and cave arthropods of the continents are conspicuously poorly represented because of their inherent lack of dispersal ability. Although the existence of lava tubes in Hawaii has been known for many years, they remained virtually unexplored biologically until my chance discovery of a blind bra-chypterous cixiid and a new endemic cricket in a lava tube on the island of Hawaii in July, 1971 (Howarth 1972). Since that time about 50 different cave systems (Table I) have been at least partially surveyed faunistically, and additional cave-adapted arthro-pods have been found in lava tubes on the islands of Hawaii, Kauai, Maui, and possib-ly Oahu. These are among the first troglobites known from oceanic islands, and open the door to a vast new area of the world biospeleologically.
Article
Full-text available
Lava flows of pahoehoe basalt on Kilauea Volcano, Hawaii Island, are colonized by arthropods within months after an eruption and 6 months or more before the first macroscopic plants appear. The barren rock surface is xeric, windy, and subject to high insolation and to daily temperature extremes; however, the numerous cracks and surface irregularities offer refuge for the animals. These animals scavenge on allochthonous windborne (aeolian) organic debris. The most abundant scavenger, as determined by baited trapping, is a remarkable, specialized cricket, Caconemobius fori, which appears to be restricted to these unvegetated lava flows near Kilauea. A native wolf spider, Lycosa sp., also colonizes the very young flows. Few other native or exotic Hawaiian arthropods are able to exploit the rigorous environment. On the nearly continuously active Hawaii volcanoes, new flows cross older flows before the latter can become vegetated. Thus the habitat has been available for colonization possibly as long as Hawaii Island has been subaerial, i.e., approximately 700,000 years.
Article
Full-text available
A remarkable blind troglobitic terrestrial amphipod, Spelaeorchestia koloana, n. g. and n. sp. is described from material collected in lava tubes and a limestone cave on the island of Kauai, Hawaiian Islands. It is allied to a diverse complex of surface species which are endemic to the Hawaiian Islands. Notes on its biology are included. Two tropicopolitan "tramp" species, Talitroides alluaudi Chevreux and T. topitotum Burt, are occasionally found in caves. This is the first record of these 2 introduced species in the Hawaiian Islands. As part of a long-term IBP faunal inventory of caves, lava tubes, and underground caverns of the Hawaiian Islands (Howarth 1973), a number of interesting insects, arachnids, oniscoidean isopods and other terrestrial invertebrates were collected from a lava tube near Koloa, Kauai. Among the presumably troglobitic arthropods were specimens of a moderately large, blind, white amphipod crustacean. These animals were subsequently identified as a very distinctive new taHtrid species, allied to Parorchestia hawaiensis (Dana) previously known from the Hawaiian Islands (Barnard 1955). Distinctive morphological features of this unique sub­ terranean species justify its separate generic recognition, as recently instituted in other Indo-Pacific land amphipods (Bousfield 1971). The species is herewith described as Spelaeorchestia koloana, n. genus, n. sp. FIG. l).
Article
Full-text available
1. The water regime in soil commonly approaches equilibrium of water potential with the insects living there. 2. Even under these conditions, non-equilibrium processes have a significant effect on water movement through the cuticle of soil insects. 3. Measurements of water potential on either side of the cuticle of Costelytra zealandica larvae showed that equilibrium is not reached while the insect is alive. There is an active outward flow of water by thermoosmosis associated with the flow of heat from the insect.
Chapter
Obligatory cavernicoles, or troglobites, have traditionally been of special interest to evolutionary biologists for several reasons. The existence of animal life in caves and other subterranean spaces at first attracted attention because of its novelty; intensive biological exploration of caves began little more than a century ago. Although the discovery and description of the cave faunas of the world is far from complete, especially in the Western Hemisphere, so much descriptive information has been compiled that we can safely assert that, at least in unglaciated, temperate parts of the world, the occurrence of numerous species of troglobites in any major limestone region is a common and highly probable phenomenon.
Article
The temperature and relative humidity preferences and tolerances of two Texas species of cave-adapted millipedes, Cambala speobia (Chamberlin) and Speodesmus bicornourus Causey, were studied. Both species showed gross preferences when tested in gradient chambers for temperatures and relative humidities approximating those of their cave environments. But C. speobia, the less adapted species morphologically, was the more selective of the two species for such conditions. S. bicornourus was far less tolerant of elevated temperatures and reduced relative humidities than was C. speobia. Discussed is a possible reason why a terrestrial troglobite like S. bicornourus would combine intolerance with a lessened ability to perceive those factors to which it is intolerant. Discussed also are the possible causes of the present distribution of Cambala and Speodesmus in the caves of central Texas.
Article
This chapter presents the environmental aspects of humidity on reproduction, the rate of birth, and insect populations. Humidity influences the survival of insects mainly through an effect on their water content. Provided this can be kept within certain limits, exposure to extremely dry or extremely humid conditions may not be harmful. However, it is useful to consider separately the effect of humidity both on the birth and death rates of insects. The effective birth rate of a population may be taken as the rate at which reproducing females are added to it. There are two ways in which this rate may be affected: (1) through effects on the rate at which the progeny is produced and (2) through effects on the rate at which the offspring reaches sexual maturity. The survival of insects depends on their maintaining a balance between the losses and gains of water so that the water content is kept within certain limits. Survival in the field is also affected by humidity in several instances, and circumstantial evidence suggests that death by desiccation may be a common occurrence in many species.
Article
Climate exerts a universal dominant influence on ecology, but processes of karstification have an equally high ecological influence in carbonate rock regions. Development of karst features depends greatly on the degree to which water containing carbon dioxide has been able to move on and through carbonate rocks and to remove some of the rock in solution. Distinctive features of many karst terranes include scarcity of soils, scarcity of surface streams, and rugged topography; less distinctive are the highly permeable and cavernous rocks, especially at the shallow depths. This high permeability gives rise to many practical problems, including (i) scarcity and poor predictability of groundwater supplies, (ii) scarcity of surface streams, (iii) instability of the ground, (iv) leakage of surface reservoirs, and (v) an unreliable waste-disposal environment. Natural karst processes in some carbonate rock regions have caused a greater restriction in the development of biota than man can ever be suspected of causing.
Article
Ptomaphagus lincolnensis and Ptomaphagus manzano, small-eyed, flightless, high elevation forest litter species from New Mexican mountains, are discribed as new. Their relation to cave species is possible. High elevation spruce-fir forest of New Mexico harbor a suite of terrestrial litter arthropods "preadapted" for cave colonization. That cave faunas in the southwest (west of the Edwards Plateau of Texas) are comparatively lacking in troglobites (obligate cavernicoles) must thus be due to environmental dryness, and not to a lack of ancestral species with cave colonizing potential and ability.
Article
An environmental chamber which maintains any desired temperature between 10°C and the avg daily ambient temperature (±1°C) is easily made in the field or laboratory by insulating a water bath and using a sunken container of ice as a heat sink. The test cages are partially submerged near the water surface.
Article
World-wide troglobite (obligate cavernicole) distribution patterns are reviewed. The troglobite faunas of the Edwards Plateau of Texas and the Sierra de El Abra of Mexico are compared and related to the world-wide distributions. Striking differences exist between temperate and tropical cave communities. Temperate caves contain far more troglobites than tropical caves. Terrestrial troglobites in particular are uncommon in tropical caves; most tropical troglobites are aquatic. Several suggestions are offered in explanation of these disparities. The paucity of tropical troglobites is possibly a reflection of the higher energy input into tropical caves which lessens the selection pressures for energy-economizing troglobite adaptations. Consequently, evolutionary rates are slowed, and troglobites appear later in tropical caves than in temperate caves of lower energy input. Abundance of terrestrial troglobites in temperate caves has resulted largely from the effects of Pleistocene glaciation which removed surface faunas leaving populations in protective cave environments to evolve in geographical isolation. The absence of these effects in tropical areas and the nature of the tropical climate permit continuing gene exchange between cave and surface populations preventing speciation. Most tropical troglobites are aquatic since aquatic populations may be geograhically isolated in caves by means ineffective in the isolation of terrestrial populations.
Article
Studies were made on the preference responses and tolerances of the troglobitic carabid beetle Rhadine subterranea to light, temperature, and relative humidity. The beetles are weakly photonegative and appear to have a strong preference for atmospheres of low saturation deficit. Both these responses seem to be orthokineses. They have a strongly developed temperature sense, and their temperature preferendum shifts seasonally. This response seems to be a klinotaxis. They are neither strongly stenothermal nor stenohygrobic. The preference responses, especially that of temperature, are probably mechanisms tending to restrict the beetles to their habitat. The tolerance data suggest that the epigeum could, at times, be used as a dispersal route.
Book
The following values have no corresponding Zotero field: ID - 156
Article
The role of carbonic acid as a soil cation leaching agent was found to decrease as annual temperature decreased among four sites ranging from tropical rainforest to subalpine and northern forest. Carbonic acid dissociation was suppressed by low pH in the subalpine and northern soil solutions, and the presence of organic acids is suspected in these solutions. The presence of the bicarbonate anion has a major impact on yearly cation transport through a soil. It is hypothesized that the reduced bicarbonate concentrations at low pH in the subalpine and northern sites reduces nutrient loss from the rooting zone. The roles of sulfate and chloride in the anion component of soil solutions are also discussed with reference to sources of SOâ and sea salt and the cycling of S and Cl.
Article
The biology and ecology of U. coprophila was studied in mite cultures in the laboratory and from analyses of samples taken from a heap of bat guano in a small cave chamber. The guano heap was formed over many years of cyclical roosting in the chamber by several thousand bent-winged bats, whose faeces and urine form the source of energy for the permanent community of organisms in the heap. U, coprophila is a major component of this guano community because of its exceedingly high numbers (up to 33.7 x l0*6 per square metre). Freshly defaecated bat guano was collected from the cave and used as a substrate for laboratory cultures of mites. The mites feed and mature on fungi. There are five stages in the life cycle: eggs, larvae, protonymphs, deutonymphs, and adults of both sexes. No phoretic nymphs were found. The mean duration in days of each of these stages was determined at 14,20, and 24°C. There was a positive linear relationship between temperature and the rate of development of larvae and protonymphs. Age-specific fertility and mortality were determined. Laboratory experiments supported the hypothesis that a regular supply of fresh bat guano was necessary for continuous growth and reproduction of U. coprophila. When fresh dung was not available, females ceased laying eggs and growth of the immature stages ceased. Nymphs and adults became quiescent. Annual changes in the cave population of mites and their vertical distribution in the guano heap were determined from quantitative samples of bat guano collected at regular intervals from August 1966 to July 1970. A sieve-sampling method for guano deposits is described; mites were extracted by a modified Tullgren funnel. Mites feed primarily in the surface layers of guano and move into the heap to moult. Sex ratios were found to be significantly biased towards males at most times of the year. Several generations were produced each year. These overlapped and became indistinguishable. A graphical method was used to determine instar-specific mortality of the mites. Recruitment to the population occurred when bats were present in the chamber and fresh dung was being deposited. When bats were not present, the fresh guano was used up rapidly and growth and reproduction of the mite population ceased. It is suggested that the mite population progresses through an annual cycle of four phases keyed with the annual roosting cycle of the bats and that limitation of the mite numbers is by a complex interaction between fly larvae, food, and temperature of the guano until an absolute shortage of food occurs and mites become quiescent.
Article
At several occasions red coloured caridean shrimps have been reported from tropical land-locked saltwater pools. These pools are situated at some distance from the sea, but, because the level of the water rises and falls with the tides, must have subterranean connections with the sea. The shrimps belong to species that so far have not been found outside this special type of habitat, although some have a rather extensive geographical distribution. Apart from the peculiar habitat in which they are found and apart from their red coloration, there is very little that these species have in common. The 11 species so far found exclusively in these pools belong to 9 different genera and to 5 different families (see also Holthuis, 1963; Chace & Manning, 1972). It is suggested now to use the term "anchialine" (from the Greek anchialos, near the sea) to indicate this type of habitat, rather than to have to define it each time as "pools with no surface connection with the sea, containing salt or brackish water, which fluctuates with the tides". Recently, I received unusually interesting caridean material taken from several of such anchialine pools in the Indo-West Pacific region. This material was provided by various persons. In November 1971 and again in March 1972 Dr. Ch. Lewinsohn, Zoology Department, Tel-Aviv University, Tel-Aviv, Israel, and Dr. F. D. Por, Zoology Department, Hebrew University, Jerusalem, Israel, submitted to me a number of shrimps collected in a saltwater pool near the southern tip of Sinai Peninsula near Ras Muhammad. This material contained a new species of Periclimenes and a new genus and species of Hippolytidae. To my great surprise, the latter new genus and species of Hippolytidae was also represented in Pacific material from Maui Island (Hawaiian Archipelago) and Funafuti (Ellice Islands)
Article
1.1. Eleodes armata exhibited greater water loss than Cryptoglossa verrucosa at all temperatures and humidities.2.2. At low temperatures and humidities, water lost through transpiration predomated; at higher temperatures and humidities, a greater percentage was lost via quinone secretions.3.3. No uptake of atmospheric moisture was observed for either species, C. verrucosa exhibited a reduction in water loss with increased dehydration.4.4. The presence of intact elytra reduced water loss in E. armata.5.5. Resistance to desiccation in the two species was correlated with observations of their seasonal abundance and activities.
Article
Observations and collections of the fauna of the Dark Cave of Batu Caves at Kuala Lumpur, Malaysia, were made between May 1959 and January 1961. The caverns have an extensive invertebrate population, many species of which remain unidentified. Twenty-three species of vertebrates were observed, the most abundant being Eonycteris spelaea and Hipposideros diadema. The collections included 151 identified species of 94 families of invertebrates . Coprophagous mites of several species and Diptera were the most abundant arthropods. Populations and species make-up varied from the entrance to the rear of the caverns. Most species developed maximum populations where light and
Article
Ptinellodes Matthews 1872, and its polymorphic type species lecontei (Gemminger and Harold) 1868 from the southeastern United States are redescribed and the following 4 polymorphic species are newly described: suteri n. sp. (southeastern United States), similis n. sp. (Jamaica), malkini n. sp. (Nicaragua), and heterosternus n. sp. (Bolivia and Brazil). Ptinellodes and several other genera in the family exhibit a characteristic kind of polymorphism. Two strongly differentiated morphs occur in each sex, a normal morph with normal eyes, wings, and body pigmentation, and a vestigial morph, in which the eyes, wings and other structures are reduced or absent. The vestigial morph is by far the more abundant (ca. 90% or more of all individuals). Typically, each species of polymorphic Ptiliidae is represented by all 4 phenotypes (males and females of both morphs), although the degree of regression in particular vestigial characters varies according to species. The morphs occur together at the same time and place, but in very unequal numbers. Sex and morph data are presented for all the specimens (ca. 1100) of the 5 species of Ptinellodes in the study. The characters involved in the polymorphism, the relative proportions of the different phenotypes, and the taxonomic, geographic, and ecological distribution of the polymorphism in the family are reviewed. Other topics discussed are the possible mechanisms controlling the expression of the morphs, the proportion of phenotypes in relation to habitat, sex ratios, and the possible adaptive significance or selective advantage of the polymorphism. Ptiliidae are the smallest beetles in the vast order Coleoptera, and it can be assumed that availability of space and materials for essential structures is a limiting condition in such minute forms. Among the various explanations that have been proposed to account for loss or reduction of structure (regressive evolution), the principle of material compensation, as a means of conserving developmental energy and space in favor of reproductive effort, is considered to account best for the selective advantage and high incidence of polymorphism in the Ptiliidae, as well as for the great numerical preponderance of the vestigial morph in all the polymorphic species. Parthenogenesis, like polymorphism, also has an exceptionally high incidence in the Ptiliidae. Only one egg is accomodated and matured in the abdomen at a time, and a low fecundity is postulated. Thelytokous parthenogenesis (production of females from unfertilized eggs) in this family has been previously interpreted as an adaptation that enhances fecundity (because no eggs need to be “wasted” on males). I hypothesize that the 2 phenomena, polymorphism and parthenogenesis, represent adaptations or solutions to the limiting factors resulting from evolution to small size in the Ptiliidae. If the hypothesis has validity, there should be a higher incidence of both phenomena in the smallest members of various lineages of arthropods in which evolution to small size has occurred.
Article
A review is given of the adaptations of arthropods to life on land. The terrestrial Arthropoda are divided ecologically into two main groups. The first of these includes woodlice, centipedes, miilipedes and their allies which lose water rapidly in dry air and consequently are restricted to damp, dark habitats which they leave only at night when the temperature falls and the relative humidity of the air rises. The second group includes most insects and Arachnida: these are comparatively independent of moist surroundings because their integument possesses an impervious layer of wax which prevents desiccation.
Article
Late instar larvae starved at 53% r.h. maintained constant haemolymph osmotic pressure (O.P.) for 12 days with only a small rise from 353 to 363 mOsm at day 17 when haemolymph volume was nearly zero. Total body water was also nearly constant for the first 12 days and then dropped from 62 to 58·5%. At low r.h. for 7 days, starved larvae lost more water than those at high r.h., but haemolymph O.P. ranged from 351 to 363 mOsm, and total body water remained nearly constant. Measured values were lower than expected from actual water losses, requiring that solutes be removed from the blood. Larvae starved at 53% r.h. for 7 days and then given distilled water took in 60 per cent of the starved weight and increased haemolymph water volume by 55 per cent. O.P. dropped only to 326 mOsm as against the expected 210 mOsm. More solute was mobilized than had been apparently sequestered during starvation. Thus body fluids are closely regulated despite wide internal and external changes.
Article
UPTAKE of water vapour from subsaturated atmospheres has been demonstrated in a variety of terrestrial insects and mites but no previous effort to identify the site and mechanism has been completely conclusive. The tracheal system, the rectum and the general body surface have variously been proposed in specific studies.
Article
1.1. The desert cockroach Arenivaga sp. was compared with Periplaneta americana as regards certain physiological responses to light dehydration, but no significant differences were found.2.2. In both species dehydration caused a reduction in haemolymph water as well as in general tissue water, but no conclusive evidence was found to indicate significant movement of water from haemolymph to tissues.3.3. The haemolymph osmotic pressure increased during dehydration, but was subject to strong osmoregulation.4.4. Removal of chloride ions from the haemolymph appears to contribute to such regulation.
Article
Limestone caves provide unique natural laboratories for studying biological and geological processes.