Global diversity of water mites (Acari, Hydrachnidia; Arachnida) in freshwater

Abstract

The Hydrachnidia (water mites) represent the most important group of the Arachnida in fresh water. Over 6,000 species have been described worldwide, representing 57 families, 81 subfamilies and more than 400 genera. The article analyzes extant water mite diversity and biogeography. Data on distribution and species richness of water mites are substantial but still far from complete. Many parts of the world are poorly investigated, Oriental and Afrotropical regions in particular. Moreover, information among different freshwater habitats is unbalanced with springs and interstitial waters disproportionately unrepresented. Therefore, more than 10,000 species could be reasonably expected to occur in inland waters worldwide. Based on available information, the Palaearctic region represents one of the better investigated areas with the highest number of species recorded (1,642 species). More than 1,000 species have been recorded in each of the Neotropical (1,305 species) and Nearctic regions (1,025 species). Known species richness is lower in Afrotropical (787 species) and Australasian (694 species) regions, and lowest in the Oriental region (554 species). The total number of genera is not correlated with species richness and is distinctly higher in the Neotropical (164 genera); genus richness is similar in the Palaearctic, Nearctic and Australasian regions (128–131 genera) and is lower in the Afrotropical and Oriental regions with 110 and 94 genera, respectively. A mean number of about three genera per family occur in the Palaeartic, Nearctic and Oriental while an average of more than four genera characterizes the families of Australasian and Afrotropical regions and more than five genera those of the Neotropical. Australasian fauna is also characterized by the highest percentage of endemic genera (62%), followed by Neotropical (50.6%) and Afrotropical (47.2%) regions. Lower values are recorded for the Palaearctic (26.9%), Oriental (24.4%) and Nearctic (21.4%). The Palaearctic and Nearctic have the highest faunistic similarity, some minor affinities are also evident for the generic diversification of Holarctic and Oriental families. The faunas of Southern Hemisphere bioregions are more distinct and characterized by the presence of ancient Gondwanan clades with a regional diversification particularly evident in the Neotropics and Australasia. This scenario of water mite diversity and distribution reflect the basic vicariance pattern, isolation, phylogenetic diversification, recent climatic vicissitudes and episodes of dispersal between adjacent land masses together with extant ecological factors can be evoked to explain distribution patterns at a global scale.

Introduction

The Hydrachnidia (water mites), also called Hydrachnellae, Hydracarina, Hydrachnida, represent the most important group of the Arachnida in freshwater. Originating from terrestrial ancestors, they have colonized all kinds of freshwater habitats. Water mites are highly diversified both in lotic and lentic habitats, as well as in springs and interstitial waters (Di Sabatino et al., 2000, 2003; Smith et al., 2001). Hydrachnidia belong to the cohort Parasitengona (Actinedida), a group whose species are characterized by a complex life cycle involving a heteromorphic parasitic larva, two pupa-like resting stages (proto- and tritonymph) and free-living predacious deutonymphs and adults. The resting stages provide an adaptation for avoiding unfavourable conditions in unstable environments, and larval parasitism on flying insects confers substantial advantages ensuring dispersal and rapid exploitation of new habitats (Smith et al., 2001).

Water mites are characterized by bright colours and a highly diversified morphology. Plesiotypically, body shape is globular but it may also be flattened dorso-ventrally or laterally, or elongated into a worm-like form (Fig. 1). Length ranges from 0.2 mm up to 10 mm, although most species are between 0.5 and 1.5 mm. As in all Acari, the body of a water mite is divided into two principal units, gnathosoma and idiosoma. The gnathosoma is a complex of trophic and sensory structures composed of a sclerotized capsule (capitulum) and two pairs of appendages (palps and chelicerae). The idiosoma, or body proper, may be soft-skinned or the integumental muscle-attachment sites are transformed to more or less extended sclerotized plates with tendencies to develop complete sclerotization. The idiosoma is also characterized by the presence of series of defensive glands and mechanoreceptive slit organs. The ventral side includes four pairs of sclerotized coxal plates (insertion points for legs and leg muscles), the genital field and the opening of the excretory system. The four pairs of legs of adults are six-segmented and usually bear one pair of terminal claws. Size and chaetotaxy of leg segments are modified in relation to modes of locomotion and reproduction. For more detailed information see Di Sabatino et al. (2000, 2002), Smith et al. (2001) and references therein.

Fig. 1
figure1

Scanning electron microphotographs of some water mite genera. (A)—Lebertia (Lebertiidae), ventral view. A widespread genus presents in all bioregions except Australasian. (B)—Feltria (Feltriidae), ventral view. A genus particularly diversified in the Northern Hemisphere, not reported from Afrotropical and Australasian. (C)—Apheviderulix, dorsal view. The only genus of the enigmatic family Apheviderulicidae with distribution limited to South Western Palaearctic and South Western North America. (D)—Harpagopalpus (Harpagopalpidae), frontal view. The few species of this genus are only known from the Afrotropical and Oriental regions. (Photos (A) and (D) are from Gerecke; (B) from collection Carl Bader, Basel; (C) from Gerecke et al. (1999)

Water mites are grouped into eight superfamilies with more than 50 families. Over 420 genera and about 6,000 species are described (Viets, 1987; Smit, in http//www.watermite.org). However, this number likely greatly underestimates global richness of water mites. For example, about 5,500 species are calculated to occur in the Neotropics alone (Goldschmidt, 2002).

Species diversity

The most recent catalogue of water mites (Viets, 1987) included more than 5,000 described species in 50 families and 310 genera. Since then, our knowledge on taxonomy, diversity and distribution has significantly improved. More than 1,000 species have been described and 65 new genera, nine subfamilies (three of which were reinstated) and ten new families (six of which were reinstated) were established (Table 1).

Table 1 New water mite taxa described after 1986 (data from Smit in http//www.watermite.org)

Most of these new species have come from the southern hemisphere. More than 230 species have been added to the list of the Neotropical freshwater fauna with about 140 additional species recorded for South America and 100 for Central America. Australasian is the second region in terms of new species discovered after 1986, with 115 species from Australia, 35 from New Zealand and 34 from western Pacific islands. A considerable number of species were also reported from the still poorly known freshwater fauna of the Eastern Palaearctic with more than 150 species described from China and Russia. More than 100 species were also added to the faunal lists of North America and Europe. At higher taxonomic levels, new families were described from the western Palaearctic, Nearctic, Oriental and Australasian, with Australia and USA being the countries with the highest number of new genera.

These considerations suggest that the actual number of water mite species in the world is large but cannot be readily estimated. A species-accumulation curve calculated for the western Palaearctic, one of the better investigated areas of the world, indicates that the number of new species discovered is still increasing and there is no indication that it is reaching a plateau (Fig. 2).

Fig. 2
figure2

Cumulative numbers of water mite species described from the Western Palaearctic region (data from Gerecke in http//www. watermite.org)

Data on present distribution and species richness of water mites are substantial but still far from complete (Table 2). Many parts of the world, Afrotropical and Oriental regions in particular, are poorly investigated. Moreover, information on distribution and species diversity among different freshwater habitats is unbalanced, with particularly scanty documentation of taxa that dwell in springs or hyporheic-interstitial habitats. Therefore, more than 10,000 species could be reasonably expected to occur in inland waters world-wide.

Table 2 Taxonomic diversity of water mites at global and biogeographic region scales
Fig. 3
figure3

Distribution of freshwater mite (Hydrachnidia) species and genera (SP/GN) per zoogeographic region: PA—Palaearctic; NA—Nearctic; NT—Neotropical; AT—Afrotropical; OL—Oriental; AU—Australasian; PAC—Pacific Oceanic Islands; ANT—Antarctic

Phylogeny and historical processes

Hydrachnidia probably originated during the Mid-Palaeozoic era (400 Mya) from terrestrial Parasitengona-like ancestors, but see also Smith & Cook (1999) for an alternative hypothesis. From plesiotypic unstable and intermittent habitats (temporary pools, seepage areas and small springs) they invaded all kind of freshwater habitats. The only two fossil records from Tertiary deposits refer to larval specimens of highly derivative modern clades (Poinar, 1985). No attempt has been made so far to produce a hypothesis about the age and phylogenetic relationships of the major clades with the support of molecular data. Differentiation of extant superfamilies started from early Mesozoic (240 Mya), Stygothrombioidea, Hydrovolzioidea, Hydrachnoidea, Eylaoidea and Hydryphantoidea are by most authors considered “lower water mites”. Members of these superfamilies share plesiotypic features such as aerial larvae bearing six-segmented legs and parasitism of a wide variety of insect hosts. However, also within these groups, numerous adaptations to particular environmental conditions are realized. Probably from hydryphantoid-like ancestors, the “higher water mites” (Lebertioidea, Hygrobatoidea and Arrenuroidea) evolved and radiated, perhaps in part as a response to the diversification of nematoceran insect hosts. The systematics of higher groups is still in a state of flux. For alternative systems of superfamilial and familial classifications see Tuzovskij (1987), Witte (1991), Harvey (1998) and Panesar (2004).

Present distribution and main areas of endemicity

The currently available information does allow us to present a preliminary scenario on water mite diversity at a global scale (Fig. 3).

Palaearctic

Due to a long tradition of European water mite research and more recent intensive field-work in southern and central Europe, the Western Palaearctic is one of the better investigated areas of the world (Gerecke & Lehmann, 2005—see also Gerecke in http//www.watermite.org). A total of about 1,600 species in 42 families, 40 subfamilies and 131 genera have been documented. More than 1,100 species (114 genera and 40 families) are recorded from the Western Palaearctic, most of them (about 800 species) from countries surrounding the Mediterranean Sea (Di Sabatino & Gerecke, unpublished database). From central Europe a recent list reports 620 species (Gerecke & Lehmann, 2005). Data from the Eastern Palaearctic are more scanty and mostly refer to some Russian territories (Sokolow, 1940; Tuzovskij, 1997) and China (Jin, 1997). Ongoing research and unpublished records suggest that more than 3,000 species are potentially present in this zoogeographic region.

Nearctic

About 1,700 species are estimated to occur in North America, north of Mexico (Smith et al., 2001). So far, 1,025 species have been reported, in 44 families, 69 subfamilies and 131 genera. Over 800 species (100 genera, 35 families) occur in Canada (Smith et al., 1998). Distributional data and check-lists are also available for some Canadian ecoregions (Smith et al., 1998) and North America (Mitchell, 1954; Habeeb, 1967).

Afrotropical

Older data (Viets, 1970; Van Rensburg, 1974) and more recent papers on the distribution of Afrotropical water mites, record about 800 species belonging to 110 genera, 44 subfamilies and 28 families from this region (Gerecke, unpublished). Liberia (180 species), South Africa (160 species) and Cameroon (150 species) are the countries best investigated (Cook, 1966; Viets, 1970; Harrison, 2000). From Madagascar, a country known as particularly rich in species and endemic taxa, only 65 water mite species have been documented so far, with the fauna of springs, running waters and subterranean habitats mostly unknown (Gerecke, 2004). The real diversity is likely to be one order of magnitude higher (Goldschmidt & Gerecke, 2003).

Neotropical

About 1,300 species in over 160 genera, 55 subfamilies and 31 families have been recorded from Central and South America, with large differences in the state of knowledge of different regions and a high percentage of new species discovered also in the better investigated areas (Goldschmidt, 2002; Rosso de Ferradas & Fernandez, 2005). The number of known species ranges from more than 260 from Southern Brazil (Lundblad, 1941, 1942, 1943a, 1943b, 1944), 220 from Southern Mexico (Cook, 1980) and about 180 from Central Chile (Cook, 1988). Conversely, only 5 species are reported from Bolivia and no data exist from Jamaica, Nicaragua or French Guiana.

Oriental

In the Oriental region more than 500 species in 94 genera, 51 subfamilies and 33 families have been found. Our knowledge of the region is far from complete, many areas have hardly been explored (e.g. many Indonesian islands, Southeast Asia, Himalayas, Philippines) but see also Wiles (2004) and references therein. A more detailed documentation exists only from India with 230 species recorded, in 26 families and 61 genera (Cook, 1967).

Australasian

One of the most distinct water mite faunas in the world has evolved in Australasia. About 780 species in 128 genera, 50 subfamilies and 30 families have been found. Australia (24 families, 89 genera, 440 species) and New Zealand (19 families, 52 genera, 143 species) are the best examined countries of the region (Cook, 1983, 1986; Harvey, 1998; Smit, 2005), but our knowledge is still insufficient. New Guinea is very poorly studied, and hardly any data are available from the adjacent islands (e.g. Solomon Islands, Bismarck Archipelago, New Britain).

Oceanic islands/pacific

Only eight families, 13 genera and 27 species are known from Pacific islands (Smit, 2005). Three species are reported from Vanuatu, 12 from Fiji and 14 from the Caroline Islands. Only two species are known from Western Samoa and Hawaii. Water mites are absent from the Galapagos Islands (Gerecke et al., 1996).

Antarctic

No water mites have been reported so far from this region. Their absence is confirmed by recent studies from sub-Antarctic islands (Pugh & Dartnall, 1994; Dartnall, 2005).

Endemism and faunistic similarity at family and subfamily level

A preliminary analysis of the extant differential distribution of families and their generic diversification (Table 3) shows that 19 of the 57 known families (33%) occur in all bioregions, three families (5%) have a near cosmopolitan distribution being absent only from Australasia, 12 (21%) are restricted to two bioregions and 11 are endemic to single regions (Table 4). About 75% of the families occur both in the Palaearctic and Nearctic, 30–33 families (more than 50%) have been documented from Australasian, Oriental and Neotropical regions, and only 27 (47%) are represented in the Afrotropical region.

Table 3 Genera richness of water mite families in each biogeographic region
Table 4 Water mite families and subfamilies endemic to each biogeographic region

The distribution of families shows that the Australasian fauna is particularly distinct (Fig. 4). The Palaearctic and Nearctic (Holarctic realm) have the highest-mutual affinity and are linked, at a low level of similarity, with the Neotropical, Afrotropical and Oriental regions, with the Neotropical distinctly set off from the Afrotropical and Oriental.

Fig. 4
figure4

Dendrogram of faunistic similarity between bioregions based on presence–absence of water mite families (Sørensen index)

An analysis of the regional endemism of water mite taxa (Table 4) shows that four families are endemic to the Australasian region, a further two are exclusive to the Palaearctic, Nearctic and Neotropical, a single family is limited to the Oriental and no endemic families are known from the Afrotropical region. At the subfamily level, the Neotropical region is distinctive with 12 exclusive subfamilies, followed by Palaearctic (4), Nearctic (3) and Australasian (3). A last consideration can be made on the distribution of taxa exclusive for pairs of adjacent biogeographic regions (Fig. 5). Some taxa possibly reflecting an older Laurasian or North-Pangean distribution have their geographical range limited to the Holarctic while two subfamilies are limited to the Palaearctic and Oriental regions. In the Southern Hemisphere, the Neotropical shows a closer affinity with the Nearctic (two families and five subfamilies) than with the Afrotropical region (one subfamily). Two families and two subfamilies have an Afrotropical–Oriental distribution and only a single family and subfamily are exclusive to the Australasian–Oriental regions.

Fig. 5
figure5

Water mite families and subfamilies with distributions actually limited to adjacent biogeographic regions. PA—Palaearctic; NA—Nearctic; NT—Neotropical; ET—Afrotropical; OL—Oriental; AU—Australasian; PAC—Pacific Oceanic Islands; ANT—Antarctic

Endemism and faunistic similarity at generic and species level

When described species are considered, the Palaearctic is the most species-rich region (27% of the known species) followed by Neotropical (22%) and Nearctic (17%). A lower richness is recorded from Australasian and Afrotropical regions (11–13%) followed by the Oriental region with only 9% of described species (Table 5).

Table 5 Species richness of water mite superfamilies in each biogeographic region

The total number of genera (Table 3) is not correlated with species richness and is distinctly higher in the Neotropical (164 genera); genus richness is similar in the Palaearctic, Nearctic and Australasian regions and is lower in Afrotropical and Oriental regions. Moreover, as reported in other groups (Ephemeroptera, this volume), Northern and Southern Hemispheres are characterized by a different mean number of genera per family: about three genera per family occur in the Palaeartic, Nearctic and Oriental regions while an average of more than four genera characterizes the families of Australasian and Afrotropical regions and more than five genera those of the Neotropical.

Compared to the presence–absence of families, a quantitative analysis of the richness of genera among families (Fig. 6) leads to slightly different results. The regions are here grouped into two clusters, the first including again the Palaearctic and Nearctic, but linked at low level of similarity with the Oriental; the second is formed by Neotropical and Afrotropical–Australasian regions.

Fig. 6
figure6

Dendrogram of faunistic similarity between bioregions based on generic richness of water mite families (Bray-Curtis index)

This pattern seems mainly determined by the generic diversification of some cosmopolitan families (Fig. 7). The Holarctic and Oriental regions are characterized by the diversification of hydryphantids and the Oriental furthermore by the massive presence of anisitsiellid genera. On the other hand, Hygrobatidae, Limnesiidae and Aturidae are more diversified in the Neotropics, Afrotropical and Australasian regions with the Neotropical being unique because of the extreme diversification of Limnesiidae.

Fig. 7
figure7

Generic diversity of some cosmopolitan water mite families in each bioregion

The percentages of endemic genera (Table 6) follow the same pattern described above for the generic diversification of the most cosmopolitan families, with regions of the Southern Hemisphere having a high degree of endemism with about 50% of the genera exclusive for each area. Also in this case, Australasia is distinctive with 62% of the genera known only from this region. Conversely, in the Palaearctic, Nearctic and Oriental regions the percentages of endemic genera are markedly lower (between 21 and 27%).

Table 6 Numbers of endemic water mite families, subfamilies, genera and percentage of endemic genera in each biogeographic region

At species level, the Nearctic is characterized by the dominance of lentic adapted species of the genera Arrenurus, Unionicola and Piona, which represent about 30% of the North American water mite fauna; also remarkable is the diversification of the lotic-adapted genera Feltria (37 species) and Aturus (49 species). The Palaearctic fauna is mostly dominated by lotic species of the genera Atractides, Lebertia and Sperchon (more than 25% of the whole fauna) and by lentic-adapted species of the genera Hydrachna, Piona and Eylais. In the Neotropical, species of the genera Koenikea, Limnesia, Corticacarus and Torrenticola represent about 40% of the Neotropical mite fauna. The Afrotropical water mite fauna is mostly represented by species of the genera Arrenurus, Neumania, Hygrobates, Torrenticola and Monatractides (more than 40% of the whole fauna). The Oriental region is characterized by a relatively large number of Monatractides, Torrenticola and Atractides species, while the genus Lebertia is little represented. Almost 30% of the Australasian fauna is represented by species of endemic (Procorticacarus) and Gondwanan genera (Australiobates, Aspidiobates), and by species of the more widespread genera Limnesia, Axonopsella, Koenikea and Frontipoda. The latter two genera have the highest-species richness in the austral part of the world. A number of near-cosmopolitan genera are absent in the Australasian region i.e. Lebertia, Atractides and Torrenticola.

Global distribution patterns

From the data presented above we can conclude that the extant distribution of water mites is in good agreement with the basic vicariance pattern proposed by Smith & Cook (1999). A differential distribution of water mite fauna had been established before the break-up of Pangea with a distinction between Northern and Southern Pangean clades. After the separation, Laurasia and Gondwanaland were both characterized by the presence of a distinct temperate and tropical fauna.

In Laurasia a prevalent temperate fauna evolved and diversified from the original stock with tropical clades mainly confined to the southern part of the supercontinent. These elements may have persisted until today as localized endemism in non-glaciated areas of both North America and southern Eurasia (possible extant representatives could be the family Apheviderulicidae and the genera Javalbia, Utaxatax and Momonisia). Palaearctic and Nearctic endemics are mainly localized in Eastern Eurasia and Western North America which represented the western and eastern borders of Laurasia. Areas of particular interest with endemic species and genera are also localized in southwestern North America and in the Mediterranean area in southern Europe.

In the Southern Hemisphere the situation is more complex. Gondwanaland was subjected to multiple fragmentation and extensive migration (drifting) of continental blocks. India separated first and moved largely northward experiencing dramatic climatic change. Most of the original fauna disappeared and only a few Gondwanan elements persist today (Teratothyadidae, Harpagopalpidae). The extant Oriental fauna is mostly dominated by immigrant Southern Palaearctic elements and by some Australasian taxa.

The water mite fauna of currently southern bioregions is mainly derived from ancient tropical Gondwanan clades. The long-term isolation and phylogenetic diversification of most of these clades in Australia and New Zealand could explain the distinctive fauna of Australasian. Remnants of older temperate elements could have persisted at high elevation or high latitude in South America, Australia and New Zealand.

The separation of the Oriental and the Australasian regions has always been of great interest to science. Many boundary lines have been proposed between these two faunal regions (for a review see Simpson, 1977 and Cox, 2001). When one considers the water mite fauna, Lydekker’s Line (Lydekker, 1896) seems to match most closely the boundary of the Australasian fauna. Lydekker’s Line corresponds with the edge of the continental shelf of New Guinea and Australia. East of this line a typical Australasian fauna is found, with characteristic genera including Australiobates and Procorticacarus. Sulawesi has a predominantly Asian fauna, with member of the family Torrenticolidae dominating. Moreover, species of Atractides, a genus absent from Australasia, have been reported from Sulawesi. No records have been published from the intermediate area between Sulawesi and Australia.

In the Pacific, species of islands north of the Equator are of Asian origin, while those south of the Equator are of Australasian origin. Only one endemic genus is known i.e. Fijilimnesia from Fiji. Two Aspidiobates species, a genus with a Gondwanan distribution, are found on Vanuatu, which has never been a part of Gondwana. The number of species decreases from west to east, and from Western Samoa eastward streams are devoid of water mites (Smit, 2005).

The fauna of South America also conserves a typical mixture of tropical and temperate elements. The recent establishment of the Central American land bridge did not alter the original composition of the fauna except for the northernmost part and the Caribbean area. Conversely, a number of taxa migrated northward and invaded North America (Smith & Cook, 1999; Smith et al., 2001).

These considerations suggest that the actual scenario of water mite diversity and distribution reflect essentially the basic vicariance pattern. Isolation, phylogenetic diversification, recent climatic vicissitudes and episodes of dispersal between adjacent land masses together with extant ecological factors can be evoked to explain distribution patterns at a global scale.

Human related issues

Water mites represent a robust component of aquatic communities in terms of both abundance and species richness. Their high specialization to particular microhabitats and the strength of biotic interactions as predators (deutonymphs and adults) and parasites (larvae) are important features not shared by other components of macroinvertebrate communities. Perhaps because of this specificity and interconnectedness, they reflect natural changes and human induced modifications of freshwater communities (see Di Sabatino et al., 2000, 2002 and references therein). Water mites are mostly absent from springs, running waters, ponds and lakes whose natural sediment structure has been destroyed and/or water quality reduced by organic waste waters, heavy metals or other poisonous compounds. Moreover, due to the high number of taxa specialized for life in spring habitats (Di Sabatino et al., 2003) or in the upper part of the interstitial zone, their study offers an important but seldom exploited tool for understanding and monitoring human impacts in groundwaters (Boulton et al., 2003) and groundwater–surfacewater interactions.

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Acknowledgements

We wish to thank H. Proctor (Alberta, Canada) and three anonymous reviewers for their helpful comments on an earlier draft of this article. ADS wish to thank P. Vignini (L’Aquila, Italy) for her valuable help during the preparation of the manuscript. ADS and BC were in part financially supported by the Italian MIUR (ex 60%).

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Correspondence to Antonio Di Sabatino.

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Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens

Freshwater Animal Diversity Assessment

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Di Sabatino, A., Smit, H., Gerecke, R. et al. Global diversity of water mites (Acari, Hydrachnidia; Arachnida) in freshwater. Hydrobiologia 595, 303–315 (2008). https://doi.org/10.1007/s10750-007-9025-1

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Keywords

  • Biodiversity
  • Biogeography
  • Freshwaters
  • Global assessment
  • Water mites
  • Hydrachnidia