Hypogean Crustacea ecology
The British hypogean Crustacea is impoverished in comparison to that of mainland Europe. It has generally been accepted that this is the result of the last glaciation (known as the Devensian in Britain and the Midlandian in Ireland). At its maximum extent, between 25000 and 15000 years ago it covered most of Ireland, all of Scotland and Wales and north-west England, with permafrost conditions present in the south. It is assumed that the ice would have sterilised the environment beneath it and would have removed sources of food from the surface environment. This theory would suggest that most of the British sygobitic Crustacea populations were established by animals migrating from un-glaciated areas in Europe. The main pattern of distribution of the British species would seem to support this hypothesis, with most records occurring in the southern part of England. It is thought that the cave systems of South Wales were re-colonised by migration from areas such as the Mendip Hills in North Somerset.
However, there are several notable exceptions to this, including Antrobathynella stammeri in the Midland Valley of Scotland and several records of Niphargus aquilex north of the glacial limit. Similarly in Ireland most of the Niphargus irlandicus records are north of the Midlandian glaciation. Current thinking is that the hypogean fauna might have survived in un-frozen groundwater within the tundra (tundral refugia) and in groundwater beneath the ice-sheet (sub-glacial refugia). The recent discovery of two endemic species of hypogean Crustacea in Iceland, Crymostygius thingvallensis and Crangonyx icelandicus (Krisjánsson & Svavarsson, 2007) proves that stygobitic Crustacea can survive beneath ice. It is now thought the populations of South Wales survived beneath the ice in the ancient cave systems there, rather than having become established by re-colonisation at the end of the Devensian. Proudlove et. al. (2003) discuss the geological and geomorphological explanations for the distribution of the British stygobitic Crustacea.
The habitats from which the subterranean Crustacea have been recorded include; the interstitial water in the gravels of rivers and streams (the hyporheic zone); underground aquifers in chalk and other strata; and pools and streams in caves and mines. It is believed that the true habitats of these species are the small channels of deep phreatic water in underground geological strata. Their presence in caves and mines is usually a result of the organisms being washed out of fissures in the rock, into streams and pools following heavy rain. The relatively few individuals seen in caves are not isolated but form part of a larger, unseen population.
The entomologist Frank Howarth has classified the subterranean habitats into three categories, based on size; the microcavernous habitat (>1mm in diameter); the mesocavernous habitat (1 - 200mm in diameter); and the macrocavernous habitat (>200mm in diameter) (Chapman, 1993). Since only the macrocavernous habitat is accessible to cavers one can understand why so little is known about a group of animals in which the major populations dwell beyond the reaches of direct human study.
When washed into caves the local conditions usually determine the fate of hypogean Crustacea. If conditions are favourable and good cover and / or a good food supply are present, then the cave habitat will become a home, as demonstrated by the numerous populations of cavernicolous (cave-dwelling) Crustacea throughout the British Isles. If conditions are unfavourable then the animal can either end up falling prey to other aquatic denizens of the cave (e.g. flatworms) or, if the cave atmosphere is humid enough, it can migrate, either to other pools, larger waterbodies, or back to the mesocavernous habitat. The high moisture content of the air, within many caves, means that the sharp division between the aquatic and terrestrial habitats on the surface are not so clear-cut beneath the ground. Many aquatic organisms in caves have been observed moving over a thin film of water on rocks. A population of the Freshwater Shrimp (Gammarus pulex) has been observed living on a vertical rock face above the stream-way in Manor House Farm Swallet on the Mendips. There was only a thin film of water running down the rock (not even enough to cover the shrimps themselves) and the animals were moving vertically up and down the rock face between small puddles of water, collected on tiny projections. Similarly, during an initial visit to Pridhamsleigh Cavern (near Buckfastleigh, Devon) after heavy rain, many of the cave pools were inhabited by quite large numbers of Niphargus aquilex; whilst a visit ten days later showed most of the same pools to be empty. The ability to move between pools in caves would explain the surprising habitats in which subterranean Crustacea appear, such as water-filled hollows in mud, left by cavers' boots.
Relatively little is known about the ecology of the hypogean Crustacea due to their cryptic habitat, with most studies having been carried out on European species. Most of the information below has been taken from Gledhill et. al. (1993).
The recent Groundwater Animals UK project collected a whole suite of groundwater chemical parameters in order to identify any link between preferred water chemistry and the occurrence of stygobitic Crustacea. However, no such link was evident, with void space within the subterranean habitat (i.e is there enough space in which they can live and move) and the degree of surface connectivity (i.e how much surface input is there in terms of food and oxygen etc.) being the main determinands affecting the distribution of hypogean Crustacea (Johns et al. 2015). A study aquarium was also set up in 2010 to 2013, in Joint-Mitnor Cave in the Higher Kiln Quarry (Buckfastleigh, South Devon) in order to study certain aspects of the auto-ecology of Niphargus glenniei and Niphargus aquilex (Knight and Johns, 2015).
Niphargus
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Video of Niphargids captured by Tim Johns of the Environment Agency
The genus Niphargus is known from the Palaearctic region west of the Caspian Sea. It is thought that diversification and specialisation within the genus began in the basins of the Paratethys Sea during the Tertiary Period, from which European fresh waters were subsequently colonised via brackish subterranean waters. This is supported by the fact that the largest number of taxa and those most differentiated morphologically and ecologically are found in the Danubian – Carpathian region and the northern parts of the Balkan Penninsula. There is a reduction in the number of taxa with distance from this area. . However, a recent study into the phylogenetics and phylogeography of Niphargus in north west Europe by McInerney et al. (2014) suggests a very different picture in that Niphargus originated in north-west Europe approximately 88Ma and then underwent a gradual range expansion. When the genus reached south east Europe approximately 25Ma, geomorpholgical and climatic conditions enabled a rapid process of diversification and speciation to occupy many of the new niches, particularly those available in the highly developed karst of the region. Of the over 400 taxa included in Niphargus, only 5% inhabit surface waters, including the bottoms of lakes.
Niphargus species are generally considered to be saprophagous, living on plant and animal detritus, much of which is washed into the subterranean habitat from the surface. However, some are predaceous on other invertebrates, including juvenile niphargids. Niphargus fontanus has been observed preying on Proasellus cavaticus in Welsh caves and niphargids can be captured in traps baited with meat or cheese. Although N aquilex and N. glenniei frequently co-occur in Devon caves, the larger N. aquilex has been shown to be an aggressive predator of the smaller N. glenniei and to also indulge in cannibalism when placed in a restricted space, even with an alternative food source available (Knight and Johns, 2015). Due to the scarcity of food in the underground habitat it is likely that they are opportunistic feeders, eating whatever they encounter. In experiments on the autoecology of Niphargus irlandicus, Arnscheidt et al. (2012) found that specimens in captivity fed on fine detritus and carrion [crab meat and, fish food flakes], exhibited coprophagy but exhibited no evidence of predatory or cannibalistic behaviour. Silt and clay, with its associated bacteria and fungi are also thought to form part of the diet, especially in the European species Niphargus rhenorhodanensis. Research has also highlighted the possibility that some subterranean aquatic organisms are capable of absorbing some of their nutrients directly from solution.
Karaman & Ruffo (1986) recognise three morphological types of niphargid. Species from cave habitats are generally large, with long antennae and a stout Gammarus – like body. Those from phreatic and interstitial habitats are often less than 5mm long, with either a slender and elongated body, often with small non–contiguous coxae, or with a stout body and large contiguous, or partly–overlapping coxal plates. They suggest that body size in phreatic and interstitial habitats is related to differing types of locomotion through different physical media. Some British specimens of Niphargus fontanus seem to follow this pattern, with cave specimens tending to be large and robust and specimens from interstitial habitats, being much smaller and thinner. However, specimens recently collected from wells and boreholes in chalk aquifers have also been found to be large and robust as well, possibly due to the larger fissures present underground in chalk in comparison to aquifers in other strata. Populations of Proasellus cavaticus from the Mendips and from South Wales also exhibit a distinct difference in size (see under species description), although the factors controlling this have not so far been identified. Niphargus kochianus is very rarely recorded from caves in Britain and only recently from the lake in Pen Park Hole, Bristol. These latter specimens do not appear to differ morphologically from those collected from phreatic and interstitial habitats. Similarly, Niphargus aquilex is only common in Devon caves, where again specimens show little difference to those from other habitats. It is thought that the difference in N. fontanus specimens is likely to be an adaptation to habitat rather than being separate cryptic (genetically different but showing the same morphology) species.
The molecular study of McInerney et al. (2014) has recently identified that the endemic species Niphargus glenniei and Niphargus irlandicus are ancient sister species, with no close European relatives. British Niphargus aquilex consist of three cryptic species, two of which are endemic; across Europe Niphargus fontanus consists of four clades, two of which are found in Britain and one of which is endemic; whilst British Niphargus kochianus consist of a distinct endemic clade that has separated from its closet European relatives. Three distinct clades of Niphargus irlandicus were identified by Arnscheidt et al. (2012).
Life cycles in niphargids may be relatively long. Niphargus virei has 13 moults over 3 years to reach sexual maturity and may live for up to 10 years. The numbers of eggs carried by breeding females varies between species but niphargids generally have few eggs. Gledhill & Ladle (1969) studied the life cycle of Niphargus aquilex in exposed gravel beds of the Oberwater, a soft-water stream in the New Forest. N. aquilex was observed to have two generations each year, with mature males and females exceeding 20% of the population. In N. aquilex the number of eggs per female ranges from 1 to 7 (mean 2.9) and are linearly correlated with body length. Small species of Niphargus and surface-dwelling gammarids (4 – 6 mm in length) carry similar numbers of eggs (5 – 7) but the ratio of egg number to body size increases more rapidly in the gammarids. Large mature Niphargus have only half the number of eggs carried by large gammarids of similar size (Ginet, 1960).
Gledhill (1977) carried out a five year study of the population of four species (Niphargus aquilex, N. fontanus, N. kochianus kochianus & Crangonyx subterraneus) of hypogean amphipod in gravels at the head of Waterston watercress beds, which are supplied by relatively hard water from boreholes. N. aquilex and N. fontanus were present throughout the five years, although the latter was scarce at times. N. kochianus kochianus was absent for long periods. N. fontanus, N. kochianus kochianus and Crangonyx subterraneus probably entered the gravel beds through water-filled insterstices in the underlying Upper Chalk via the boreholes tapping the aquifer. Numbers of N. fontanus, Crangonyx and N. kochianus kochianus increased with the flow from the boreholes, whereas numbers of N. aquilex were generally low following a rise in the water level and high during periods of declining water level.
Microniphargus leruthi
The genus Microniphargus is represented by one species Microniphargus leruthi, a tiny (1-2mm) member of the family Niphargidae. Previous to 2006 the species was only known from the Ardennes of Belgium, Luxembourg and the northern Rhine basin in Germany. In 2006 it was discovered in Counties Louth and Cork in Ireland and subsequently in England (2010) and Wales (2011). Survey work since then has found it in caves on the Burren (Co. Clare) and across southern Britain from East Anglia and Kent to South Devon and Pembrokeshire. The species exhibits several morphological features that differentiate it from other genera in the family. These are detailed in the species description section. The comments above on the ecology of the genus Niphargus are also likely to apply to Microniphargus.
Crangonyx subterraneus
The genus Crangonyx is much more widespread than that of Niphargus, being known throughout Eurasia, South and North America and South Africa; suggesting that this genus has been in freshwater for a much longer time, perhaps before the separation of the ancient southern continent of Gondwana from Laurasia (Chapman, 1993). Outside of Britain, Crangonyx subterraneus is known from parts of western and central Europe.
Little is known of the ecology of Crangonyx subterraneus but it is likely to be an opportunistic omnivore like Niphargus species. The epigean Crangonyx pseudogracilis (a species introduced to Britain from North America in the 1930s and now widespread) appears to be herbivorous, grazing on algae and living and decomposing plant materials.
Proasellus cavaticus
The Asellidae, the largest family of freshwater isopods, occur in both epigean and hypogean waters in North America and Eurasia. Proasellus cavaticus is known throughout north and west Europe as well as England and Wales.
Relatively little is known of its ecology in Britain, although there have been several European studies. These indicate that the life cycle is longer than in epigean isopods, with laboratory specimens living up to 11 years, with long intervals between moults to sexual maturity. Jefferson & Chapman (1979) whilst studying cave fauna in Ogof Ffynnon Dhu, South Wales, observed Proasellus as being exceptionally sedentary, possibly an adaptation to conserve energy in an energy-scarce environment. Males do not enter into a prolonged precopulatory amplexus with females, as in the epigean British species Asellus aquaticus and Proasellus meridianus. The largest ovigerous P. cavaticus females (approx. 8.5mm in length) carry approximately 55 eggs, half the mean (approx. 110) for A. aquaticus and P.meridianus females of similar body length. The eggs of all three species appear to be similar in size. Egg / embryo development is much longer in P. cavaticus, 70 to 80 days at 11°C, compared to 30 days in Asellus aquaticus.
In Britain epigean Asellus are omnivorous, although they are generally regarded as detrivores. They feed on some living plants and algae (especially filamentous diatoms) but mostly eat decomposing plant material and the associated flora of fungi and bacteria. Jefferson & Chapman (1979) and subsequent observations have found Proasellus cavaticus in Ogof Ffynnon Ddu and other Welsh caves to commonly occur in thin films of water on brown-stained flowstone. Specimens frequently have dark matter in their guts and have likely been grazing the brown sediment, which has been found to contain Chlamydo-bacteria and other micro-organisms (Chapman, 1993).
Antrobathynella stammeri / Bathynella natans
The bathynellids are recorded mainly from temperate regions, although some are known from tropical areas. With the exception of two species in Lake Baikal, all members of the Bathynellacea are stygobonts and confined to freshwater, except for two species of Hexabathynella which will also tolerate brackish water. With the exception of several Australian species, they are mostly tiny animals, about 1mm long, with a thin, elongated body shape adapted to interstitial and phreatic habitats. It is generally accepted that they originated in marine waters and penetrated subterranean continental freshwaters.
Little is known of bathynellid biology. They are believed to feed on detritus, bacteria and fungi and their locomotion consists of a combination of swimming and crawling. Post embryological development is abbreviated, with only two phases, a larval (parazoeal) phase and a juvenile (bathynellid) phase, supporting the idea that they evolved by neoteny. The developmental period for German specimens of Antrobathynella stammeri averages 9 months.
It is now generally accepted that only Antrobathynella stammeri occurs in the British Isles. Earlier specimens were recorded as Bathynella natans, although these have since been thought to have been incorrectly identified Antrobathynella stammeri. Gledhill & Gledhill (1984), Gledhill et. al. (1993) and Proudlove et. al. (2003) discuss the occurrence of Bathynella natans and Antrobathynella stammeri in Britain and concluded that only the latter is likely to be present. Proudlove and Gledhill (Proudlove et. al., 2003) attempted to examine early specimens held by the British Natural History Museum and the Marine Biological Association. Many of the specimens were either missing, or they were unwilling to dissect what valuable museum material remained in order to confirm identification. Specimens from a Welsh cave submitted for genetic analysis in the study of Camacho et al. (2017) were all shown to be Antrobathynella stammeri.