John R. Holsinger

Pattern and process in the biogeography of subterranean amphipods

The comparative data from studies of two ‘superfamily’ groups with large numbers of subterranean taxa, the exclusively freshwater Crangonyctoidea and the predominately marine Hadzioidea, support the hypothesis that distributional patterns and evolutionary processes of stygobiont amphipods are closely linked and that the former can be a useful indicator of the latter. Three major biogeographic patterns are indicated by the distribution of subterranean species in these groups, each apparently reflecting a particular mode of origin: (1) freshwater stygobionts (limnostygobionts) derived from epigean freshwater ancestors through colonizations probably influenced by adaptive shifts, or assisted by stream capture and spring failure; (2) freshwater stygobionts derived from marine/brackish water ancestors by stranding during regression of marine embayments; and (3) marine/brackish water stygobionts (thalassostygobionts) derived from epigean marine/brackish water ancestors through adaptive shifts possibly in concert with fluctuating sea levels.ZusammenfassungVergleichende Untersuchungen zweier Superfamilien, jede mit einer grossen Anzahl unterirdischer Taxa, die ausschiesslich im Süsswasser verbreiteten Crangonyctoidea und die vorwiegend marinen Hadzioidea, stützen die Hypothese, dass Verbreitungsmuster und phylogenetische Prozesse stygobionter Amphipoden eng miteinander verbunden sind, und dass Erstere ein nützlicher Indikator für Letztere sind. Die Verbreitung unterirdischer Arten in dieser Gruppe weist auf drei biogeographische Muster hin, von denen jedes eine bestimmte Herkunft reflecktiert: (1) Süsswasser-Stygobionten (Limnostygobionten) können durch Kolonisation, wahrscheinlich beeinflusst durch Veränderungen in der Anpassung, aus epigäischen Süsswasser-Vorfahren hergeleitet werden, oder unterstützt durch ‘stream capture’ and ‘spring failure’ (Versiegen von Quellen); (2) Süsswasser-Stygobionten stammen von marinen/Brackwasser-Vorfahren ab, welche im Verlauf der marinen Regression ‘gestrandet’ sind: und (3) marine/Brackwasser-Stygobionten (Thalassostygobionten) enstammen epigäischen marinen/Brackwasser-Vorfahren durch Veränderungen in der Anpassung in Zusammenhang mit Wasserstandsänderungen.

TOWARD A PREDICTIVE CAVE BIOGEOGRAPHY: THE GREENBRIER VALLEY AS A CASE STUDY

The theory of island biogeography developed by MacArthur and Wilson (1963, 1967) is playing an increasingly important role in our understanding of habitats other than oceanic islands. MacArthur and Wilson pointed out that many habitats are discontinuous, that the environment for many species consists of habitable patches separated by uninhabitable areas, and that island biogeography theory may be relevant for these situations. But the theory of island biogeography is more than a convenient conceptual framework for considering a certain class of questions: the theory can be directly tested (Simberloff and Wilson, 1969); and in addition, different island-like communities show different patterns that help us better understand the forces that determine the distribution of species (Vuilleumier, 1970; Brown, 1971; Culver, 1970). In this paper we will examine the islandlike patterns of aquatic and terrestrial cave-limited species in the Greenbrier Valley karst area in West Virginia. Caves are limited to limestone in the study area (Davies, 1965), and the exposed limestone which bears caves in the study area has an island-like pattern (Fig. 1). Each continuous area of exposed limestone will itself contain many caves, and each of these caves could be viewed as an island within the continuous region of exposed limestone (Culver, 1970). However, there are good reasons for believing that an analogy between karst areas separated from other

Biodiversity of subterranean amphipod crustaceans: global patterns and zoogeographic implications

Gammaridean amphipod crustaceans are important components of subterranean groundwater communities in many parts of the world. Most subterranean species are stygobionts, which are defined by loss or reduction of eyes and pigment and restriction to hypogean waters. The global subterranean amphipod fauna is composed of about 740 species that are distributed among 36 families and 138 genera; however, 12 families contain about 94% of all hypogean amphipods recorded to date. With respect to number of stygobionts, the four most important families are the Niphargidae, Crangonyctidae, Hadziidae s. lat. (complex), and Bogidiellidae. Many regions of the world contain significant diversities of subterranean amphipods, but the central and southern European-Mediterranean and eastern and southern North American-West Indian regions are clearly superior in taxonomic diversity and species richness. Together these two regions contain about 77% of the worlds subterranean amphipod fauna, and their high diversities are attrib...

Morphological Differences Among Eyeless Amphipods in the Genus Stygobromus Dwelling in Different Subterranean Habitats

Abstract The amphipod genus Stygobromus occurs in a variety of subterranean habitats in North America, including caves, phreatic (groundwater) lakes, and superficial subterranean habitats (seeps and epikarst). The habitats share the absence of light but differ in other features, such as pore size of the habitat, available food, and degree of seasonality. Measurements of body size, antennal size, and antennal segment number of type specimens were compared for 56 species occurring in the eastern United States. Except for differences in body size, differences among species in the four different habitats were not significant. Body size was related to relative pore size of the habitat, e.g., epikarst, with the smallest spaces, had the smallest species. However, in all habitats, there was one very large species (> 15mm); these enigmatic species apparently occupy a distinct ecological niche, perhaps being more predatory. Differences in relative antennal size showed no significant differences among habitats, and differences in number of antennal segments were marginally significant (P  =  0.06) among habitat types and not in the predicted pattern. Differences among habitats in seasonality and available food seemed to be a minor part of the selective environment; absence of light seemed to be a major part of the selective environment.

What can vicariance biogeographic models tell us about the distributional history of subterranean amphipods

Because of taxonomic diversity, geographic isolation, and other considerations, subterranean groundwater amphipods would appear to make excellent candidates for biogeographic studies. Limted dispersal ability in combination with local endemism makes it likely that vicariance models will generally offer better explanations for present distribution patterns of subterranean amphipods than scenarios based on centers of origin and dispersal. Vicariance biogeography demands a knowledge of both phylogeny and area relationships, which are typically shown on biological area cladograms. To date most biogeographic studies on subterranean amphipods have been limited to cladograms of single taxonomic groups. Although useful in showing possible relationships between areas and nested subsets of taxa, these single taxon studies do not consider covariant patterns among different groups. However, in order to be fully effective, future biogeographic research will have to focus on analyses of congruence between biological area cladograms of amphipod taxa and other subterranean crustacean groups, such as isopods. To date many covariant distributions among groups of subterranean crustaceans have been recognized but not yet analyzed for congruence.

PHYLOGENETIC ANALYSIS OF THE AMPHIPOD FAMILY BOGIDIELLIDAE S. LAT., AND REVISION OF TAXA ABOVE THE SPECIES LEVEL

The increasing number of world-wide discoveries of subterranean amphipods, especially during the last two decades, has led to additions of numerous new taxa in the stygobiont family Bogidiellidae s. lat. To date, the family is composed of 23 genera and 11 subgenera, and approximately 110 described species. However, given the uneven quality of generic and subgeneric diagnoses in the literature, there is considerable confusion regarding the status of some of the taxa at these levels. Even the family itself lacks a clear definition. In order to gain a better knowledge of the phylogeny of this group, a cladistic analysis, employing both PAUP 3.0s and MacClade, was performed on the genera and subgenera currently assigned to the Bogidiellidae s. lat. Supported by the results of this analysis, the taxonomic structure of this group is completely revised above the species level. The revision excludes 5 genera from the family, all remaining subgenera are elevated to generic level. Four taxa are split, resulting in 5 new genera. The family Bogidiellidae now consists of 33 genera. Die wachsende Zahl weltweiter Neuentdeckungen von Grundwasser-Amphipoden, insbesondere wahrend der letzten zwei Jahrzehnte, erweiterte die Stygobiontenfamilie Bogidiellidae s. lat., um zahlreiche neue Taxa. Bis heute sind in der Familie etwa 110 beschriebene Arten in 23 Gattungen und 11 Untergattungen zusammengefasst. Aufgrund der unterschiedlichen Qualitat diagnostischer Beschreibungen herrscht allerdings erhebliche Verwirrung hinsichtlich des taxonomischen Status einiger Gruppen. Sogar die Definition der Familie selbst ist relativ undeutlich. Um neue Einsichten in die Phylogenie der Bogidielliden s. lat., zu erhalten, fuhrten wir eine kladistische Analyse der Gattungen und Untergattungen unter Verwendung der Computerprogramme PAUP 3.0s und MacClade durch. Die Resultate dieser Analyse dienten als hilfreiche Erganzung bei der umfassenden taxonomischen Revision der Gattungen und Untergattungen. Funf Gattungen wurden aus der Familie entfernt und alle Untergattungen zu Gattungen erhoben. Das Aufspalten von vier Taxa resultierte in 5 neuen Gattungen. Die Familie Bogidiellidae besteht somit aus 33 Gattungen.

Burrowing as a means of survival in the troglobitic amphipod crustacean crangonyx antennatus packard (crangonyctidae)

The troglobitic amphipod crustacean Crangonyx antennatus occupies mud-bottom pools and small, gravel-bottom streams in caves in the southern Appalachians. One large, mud-bottom pool population in Lee Co., Virginia was observed periodically from 1967 to 1975. Amphipods in this population frequently burrowed into the soft mud substrate, where they were able to survive desiccation during periods when the pool dried up. Animals kept in the laboratory also burrowed and survived desiccation during an experiment which simulated drought conditions similar to those observed in caves. Amphipods collected from both pool and stream habitats burrowed, thereby indicating that stream-adapted populations of this species still retain sufficient flexibility to survive under variable environmental conditions that might be encountered in nature. It is concluded that burrowing provides a means of survival for C. antennatus when it is sometimes exposed to drought conditions in cave pool habitats and also provides protection from potential terrestrial predators under similar conditions. Burrowing also offers amphipods protection from aquatic predators (such as salamander larvae) during normal water levels and possibly allows juveniles a means of escaping cannibalism by adults.

Molecular taxonomy and phylogenetic affinities of two groundwater amphipods, Crangonyx islandicus and Crymostygius thingvallensis, endemic to Iceland.

The amphipod superfamily Crangonyctoidea is distributed exclusively in freshwater habitats worldwide and is characteristic of subterranean habitats. Two members of the family, Crangonyx islandicus and Crymostygius thingvallensis, are endemic to Iceland and were recently discovered in groundwater underneath lava fields. Crangonyx islandicus belongs to a well-known genus with representatives both in North America and in Eurasia. Crymostygius thingvallensis defines a new family, Crymostygidae. Considering the incongruences observed recently between molecular and morphological taxonomy within subterranean species, we aim to assess the taxonomical status of the two species using molecular data. Additionally, the study contributes to the phylogenetic relationships among several crangonyctoidean species and specifically among species from four genera of the family Crangonyctidae. Given the available data we consider how the two Icelandic species could have colonized Iceland, by comparing geographical origin of the species with the phylogeny. Regions of two nuclear (18S and 28S rRNA) and two mitochondrial genes (16S rRNA and COI) for 20 different species of three families of the Crangonyctoidea were sequenced. Four different methods were used to align the RNA gene sequences and phylogenetic trees were constructed using bayesian and maximum likelihood analysis. The Crangonyctidae monophyly is supported. Crangonyx islandicus appeared more closely related to species from the Nearctic region. Crymostygius thingvallensis is clearly divergent from the other species of Crangonyctoidea. Crangonyx and Synurella genera are clearly polyphyletic and showed a geographical association, being split into a Nearctic and a Palearctic group. This research confirms that the studied species of Crangonyctidae share a common ancestor, which was probably widespread in the Northern hemisphere well before the break up of Laurasia. The Icelandic species are of particular interest since Iceland emerged after the separation of Eurasia and North America, is geographically isolated and has repeatedly been covered by glaciers during the Ice Age. The close relation between Crangonyx islandicus and North American species supports the hypothesis of the Trans-Atlantic land bridge between Greenland and Iceland which might have persisted until 6 million years ago. The status of the family Crymostygidae is supported, whereas Crangonyx islandicus might represent a new genus. As commonly observed in subterranean animals, molecular and morphological taxonomy led to different conclusions, probably due to convergent evolution of morphological traits. Our molecular analysis suggests that the family Crangonyctidae needs taxonomic revisions.

Biogeographic and ecological implications of newly discovered populations of the stygobiont isopod crustacean Antrolana lira Bowman (Cirolanidae)

The recent discovery of the stygobiont isopod Antrolana lira Bowman from five new cave localities in the Shenandoah Valley of northwestern Virginia has not only resulted in a significant range extension for this rare species but has also shed new light on its origin and increased our knowledge of its habitat. Prior to 1990, A. lira was known only from two caves on the northeastern end of Cave Hill in Augusta Co., VA. To date A. lira has been found only in bodies of cave water that fluctuate in concert with vertical movements of the local water table, suggesting that this species is confined to open fissures and solution cavities in the phreatic zone. Although it is widely accepted that subterranean freshwater isopods of the predominantly marine family Cirolanidae were derived from marine ancestors by ‘stranding’ during regressions of marine embayments in Late Cretaceous or Tertiary times, until now this theory failed to explain the origin of A. lira. Unlike all other stygobiont cirolanids, the known distr...

Two new species of Pseudoniphargus (Amphipoda), in Bermudian groundwaters"

The genus Pseudoniphargus comprises a number of stygobiont Amphipoda, distributed on both sides of the Atlantic. In Bermuda, groundwaters are inhabited by two species. P. grandimanus and P. carpalis, both new. They occur throughout the entire salinity spectrum, from infrahalne to euhaline, but are most abundant in oligohaline waters. Large adults, but no ovigerous specimens. arc found at greater distance from the sea coast than juveniles, which may indicate that Pseudoniphargus needs anchihaline/marine waters for its reproduction and that juveniles migrate inland to grow up.