ENDANGERED FRESHWATER INVERTEBRATES David L

ENDANGERED FRESHWATER INVERTEBRATES David L. Strayer Institute of Ecosystem Studies

I. Introduction groundwater Water that occurs in saturated soils and II. Vulnerability of Freshwater Invertebrates geological formations beneath Earth’s surface. III. Pressure of Human Activities IV. Number and Distribution of Endangered Fresh- water Invertebrates V. Protection of Endangered Freshwater Inverte- THE EARTH’S FRESHWATERS CONTAIN A BEWIL- brates DERING DIVERSITY OF INVERTEBRATE LIFE. More than 70,000 species have already been described, and tens of thousands of species remain to be discovered and described by scientists. This diversity is not spread evenly over the surface of the globe, but is concentrated in local ‘‘hot spots,’’ usually geologically GLOSSARY ancient lakes, streams, or groundwaters. These hot spots often contain dozens to hundreds of species of alien species Species that has been moved and estab- freshwater invertebrates that are found nowhere else in lished outside of its native range as a result of human the world. Because freshwaters are such an important activities; also called exotic species, introduced spe- resource for people, and have been used intensively for cies, nonindigenous species. water supply, power, irrigation, ﬁsheries, navigation, aquifer Geological formation that contains and allows waste disposal, and as sites for cities, environmental movement of groundwater. conditions in many of the world’s freshwaters have endangered species Species that is at substantial risk been altered greatly from their original states. Espe- of extinction as a result of human activities. cially where hot spots of diversity coincide with areas endemic species Species that occurs only over a limited of intensive human development, many freshwater geographical range. invertebrates have disappeared from their native habi- eutrophication Process of increasing the produc- tats. Some invertebrate species have already become tivity of an ecosystem by enriching it with nutri- extinct, and thousands of others are in danger of ents. disappearing from the earth. Careful management of

Encyclopedia of Biodiversity, Volume 2 Copyright  2001 by Academic Press. All rights of reproduction in any form reserved. 425 426 ENDANGERED FRESHWATER INVERTEBRATES freshwaters, especially in hot spots of high biological extinction. Table I shows an example of such a system. diversity, is needed to prevent catastrophic extinctions In this article, ‘‘endangered’’ is used loosely to mean a of freshwater invertebrates in the future. species or population that is at substantial risk of be- coming extinct over the next few decades as a result of human activities. I. INTRODUCTION C. Causes of Endangerment A. Freshwater Invertebrates of the World The specific causes of endangerment of freshwater in- Over 70,000 species of freshwater invertebrates have vertebrates are highly varied from case to case. It would been described, representing about 570 families and be impractical (and probably not very illuminating) to 16 phyla. The world’s freshwater invertebrate fauna is discuss all the known cases of endangerment of freshwa- actually much larger than this; probably 10,000– ter invertebrates. Further, because information about 100,000 species await discovery, and new genera and the world’s freshwater invertebrates is still so incom- families are discovered regularly. We are particularly plete, a catalog of known cases of endangerment many ignorant about what lives in groundwaters, what lives be misleading. Instead, the focus here is on the problem outside of Europe and parts of North America, and of endangerment in a more general way, and selected small, soft-bodied invertebrates. Especially widespread case studies are used to illustrate major points. and species-rich groups of freshwater invertebrates in- Endangerment is a product of three factors: the pre- clude insects, crustaceans, mollusks, mites, nematodes, existing vulnerability of a species, the pressure of hu- and rotifers. Invertebrates live in nearly all kinds of man activities, and the sensitivity of the species to spe- freshwater habitats; lakes, rivers, brooks, ephemeral cific human activities (Fig. 1). Thus, a species may ponds, wetlands, caves, alluvial groundwaters, and even become endangered if it already was vulnerable to ex- hot springs each contain a rich and characteristic inver- tinction prior to human involvement, if human activi- tebrate community. Among important freshwater habitats, perhaps only the deepest groundwaters usually lack invertebrates. A typical lake or stream contains a few hundred species of invertebrates representing sev- TABLE I eral dozen families and 8–12 phyla. By comparison with The Nature Conservancy’s System for Ranking the Global the better-known vertebrates, freshwater invertebrates Conservation Status of Species possess a wide range of biological traits. Life spans range GX Presumed Extinct: believed to be extinct throughout its from days to more than a century. Many invertebrates range. Not located despite intensive searches and virtu- reproduce sexually, others reproduce asexually by bud- ally no likelihood that it will be rediscovered. ding or parthenogenesis, and still others change their GH Possibly Extinct: known only from historical occurrences. sexuality or mode of reproduction depending on envi- Still some hope of rediscovery. ronmental conditions. Some invertebrates produce eggs G1 Critically Imperiled: critically imperiled globally because of or other reproductive bodies that remain viable for years extreme rarity or because of some factor(s) making it especially vulnerable to extinction. Typically 5 or fewer oc- to centuries. Freshwater invertebrates include herbi- currences or very few remaining individuals (Ͻ1000). vores, bacteriovores, fungivores, predators, and para- G2 Imperiled: imperiled globally because of extreme rarity or sites, and exhibit a wide range of specialized morpholo- because of some factor(s) making it especially vulnerable gies and behaviors to aid in food gathering. Some even to extinction. Typically 6 to 20 occurrences or few re- use symbiotic algae to photosynthesize! maining individuals (1000 to 3000). G3 Vulnerable: vulnerable globally either because very rare and local throughout its range, found only in a restricted B. What Is ‘‘Endangered’’? range (even if abundant at some locations), or because of other factors making it vulnerable to extinction. Typi- Various terms such as ‘‘endangered,’’ ‘‘threatened,’’ ‘‘im- cally 21 to 100 occurrences or between 3000 and 10,000 periled,’’ and ‘‘at risk’’ have been used to describe species individuals. that are in danger of extinction through human activi- G4 Apparently Secure: uncommon but not rare, and usually ties. Conservation organizations and governments typi- widespread. Possibly cause for long-term concern. Typi- cally more than 100 occurrences globally or more than cally have tried to develop a graded series of carefully 10,000 individuals. defined terms, running from species only remotely G5 Secure: common, typically widespread and abundant. threatened with extinction to those on the verge of ENDANGERED FRESHWATER INVERTEBRATES 427

II. VULNERABILITY OF FRESHWATER INVERTEBRATES A. Small Ranges Many species of freshwater invertebrates had small ranges even before human intervention. Species with small ranges are called narrowly endemic species. For example, half of the 281 North American pearly mussel species were found in only one to three states, even before human intervention. Such species may have had elevated probabilities of extinction through natural ca- FIGURE 1 Diagram illustrating general causes of species endanger- tastrophes, and certainly are especially vulnerable to ment. The three solid lines represent different species, and the dashed human activities (Fig. 2). Small natural ranges often line shows the probability of long-term species survival below which we regard a species as endangered. The arrow shows the point at arise though a small number of understandable pro- which human impacts began. Species 1 and 2 are now endangered, cesses. Because these processes are focused in certain but for different reasons. Species 1 became endangered because it was regions and on species with characteristic biological vulnerable to extinction before human impacts, and was somewhat traits, narrowly endemic species often are clustered to- sensitive to human activities. Species 2 and 3 were not very vulnerable gether into small regions and concentrated in certain to extinction prior to human impacts. Species 2 was either highly sensitive to human activities or lived in an area where human activities taxonomic or ecological groups. were intensive, whereas species 3 was either not very sensitive to human activities or lived in an area where human activities were 1. Causes of Small Ranges weak. A primary cause of small ranges in freshwater invertebrates is the limited dispersal abilities of these animals. All freshwater habitats are islands in a sea of terrestrial ties heavily affect most of the regions or habitats that habitats, and are more or less isolated from other similar it occupies, or if it is especially sensitive to a particular habitats. Although streams are connected into drainage human activity. Conversely, a species is likely to avoid networks, the streams of one drainage network are iso- endangerment only if it evades all three of these condi- lated from those in other drainage networks. The dis- tions. Each of these factors will be discussed in more persal abilities of freshwater invertebrates, and thus the detail. perceived isolation of freshwater habitats, vary widely.

FIGURE 2 Current conservation status of North American pearly mussels (Unionoida) as a function of their native range sizes. Narrowly endemic species were found in one to three states and provinces, moderately endemic species in four to six states and provinces, and widespread species in more than six states and provinces. Conservation status from Williams et al. (1993). 428 ENDANGERED FRESHWATER INVERTEBRATES

For animals like dragonflies, whose long-lived aerial arrival of a competitor, stranded in small refuges, and adults are strong fliers, or ectoproct bryozoans, whose be unable subsequently to disperse out of the refuges. tough resting stages (‘‘statoblasts’’) are readily dispersed This second mechanism may become especially impor- by migratory waterfowl, the separation of freshwaters tant for the freshwater biota if humans cause large probably does not present an important barrier to dis- changes in regional or global climate, especially because persal or gene flow. For other animals, such as fragile habitat alterations and pollution have eliminated many groundwater crustaceans that are poor swimmers, avoid of the natural dispersal corridors between freshwater the light, and lack tough dispersal stages, adjacent habitats. streams or aquifers may be nearly as remote as distant Finally, a species may have a small range because is continents, and even small barriers may prevent migra- requires an unusual habitat, which is itself rare. For tion and gene flow. For instance, the present-day distri- example, the thermosbaenacean crustacean Thermos- bution of microparasellid isopods nearly follows the baena mirabilis was described from ancient Roman pattern of marine beaches from over 20 million years warm baths and is known from only a few thermal ago (Fig. 3), where these species presumably arose and springs in Tunisia. Its small range presumably derives from which they subsequently apparently have been from its unusual habitat requirements as well as its unable to disperse. limited dispersal abilities. The isolation of freshwater habitats may produce small ranges in two ways. First, endemic species with 2. ‘‘Hot Spots’’ of High Endemism small ranges may evolve in place following infrequent Because of processes of speciation, extinction, and dis- crossing of dispersal barriers, resulting in a group of persal do not occur uniformly over the earth, species more or less closely related species whose ranges are richness and endemism vary greatly across the world’s separated by barriers to dispersal. Second, a formerly freshwaters. Some bodies of water contain more than widespread species may be eliminated from most of its 1000 invertebrate species, many of them unique to that former range, for instance by a changing climate or the single body of water. At the other extreme, some bodies

FIGURE 3 Distribution of freshwater microparasellid isopods and Oligocene shorelines (24–37 million years ago). Stippled areas were land during the Oligocene and solid circles show places where freshwater microparasellids have been found. ENDANGERED FRESHWATER INVERTEBRATES 429 of water support fewer than 100 invertebrate species, all of them widely distributed. We might expect sites of high richness and endemism to be habitats of great age, habitats where dispersal is limited, either by geographic isolation or by characteristics of the habitat, or habitats that harbor animal groups that are prone to speciate. Thus, many ancient lakes (Baikal in Siberia, Tanganyika and Malawi in Africa) and river systems (the Tennessee in the United States, the Mekong in Southeast Asia) that have not been recently disturbed by glaciation, marine submergence, or desiccation support unique assemblages of invertebrates. Many aquifers seem to contain a high proportion of endemic species, probably because both the characteristics of aquifers (slow water flow, tortuous passageways within aquifers, and barriers between aquifers) and the characteristics of their inhabitants (e.g., fragile bodies, strong thigmo- taxis) discourage long-range dispersal. Conversely, gla- cial lakes and temporary ponds rarely support locally endemic species. Although we know many hot spots of freshwater invertebrate diversity, it probably is not yet possible to produce a reliable global map that shows all major hot spots. FIGURE 4 Different kinds of animals have different characteristic 3. Species with High Endemism range sizes. The upper panel shows the number of states or provinces Groups of animals vary in their tendency to form new occupied by species of North American dragonflies and pearly mussels. The lower panel shows the number of biogeographic regions species with small ranges. As already suggested, narrow occupied by groundwater and surface-water cyclopoid copepods in dispersal probably allows the development of local spe- Europe. cies, whereas broad dispersal probably provides so much gene flow across populations that speciation is unlikely to occur. Other traits that have been suggested to encourage local speciation include a requirement for 4. Traits of Narrowly Endemic Species outcrossing (as opposed to selfing hermaphroditism or Narrowly endemic species may possess traits (other parthenogenesis), production of large young, live-bear- than small range size) that influence their vulnerability ing (as opposed to egg-laying), and narrow habitat re- to endangerment. For example, the limited dispersal quirements. The importance of each of these (and abilities and specialized habitat requirements of many other) factors is unclear, but it is clear that groups of narrowly endemic species may make them particularly freshwater invertebrates do differ widely in their degree sensitive to and slow to recover from catastrophes, of endemism. whether natural or human-caused. Further, some envi- Figure 4 shows two examples. Dragonflies, most of ronments that contain endemic species may encourage which are strong fliers and easily cross drainage divides, the development of traits that influence species vulnera- are much less likely to have small ranges than pearly bility. Thus, in the food-poor groundwater environ- mussels, which do not readily cross drainage divides. ment, many animals have sparse populations, delayed Even the same group of animals may have dramatically maturity, and low reproductive rates, all of which prob- different degrees of endemism depending on the habi- ably add to their sensitivity to human impacts. tat occupied. Thus, groundwater cyclopoid copepods have very much smaller ranges than their relatives in surface waters. This difference presumably arises B. Sparse Populations because groundwater animals have distinctive behav- Species may be vulnerable to endangerment because iors and especially because dispersal between aqui- their populations are sparse. Because population densi- fers is more difficult than dispersal between lakes or ties of freshwater invertebrates are much less well streams. known than their geographic ranges, relatively little is 430 ENDANGERED FRESHWATER INVERTEBRATES

Box 1 zebra mussel and biotic exchanges through the Rivers in the Southeast United States Tennessee–Tombigbee Waterway, may affect the southeastern freshwater fauna. The U.S. Southeast (extending roughly from the As a result of these massive changes to south- Ohio River south to the coastal plain of Alabama eastern rivers, much of the freshwater invertebrate and Georgia, plus the highlands of Arkansas, Mis- fauna is extinct or imperiled. Among the mol- souri, and Oklahoma) contains ancient river sys- lusks, the only group for which reasonably com- tems with an extraordinarily rich biota. This re- plete data are available, about 60 species and 4 gion was not covered by Pleistocene glaciers, nor genera from the Southeast are now extinct. Liter- was it covered by the sea or desiccated for hun- ally hundreds of additional mollusk species, rep- dreds of millions of years, so river systems like resenting over half of the native fauna, are threat- the Tennessee, Cumberland, and Alabama (and ened or endangered. Hundreds of southeastern their associated aquifers) are very old. The rivers crayfish and aquatic insects are likewise rare or and groundwaters of the Southeast are examples endangered, and additional species of small, of biologically rich ecosystems that have suffered poorly known animals like copepods, isopods, badly from human activities. amphipods, and oligochaetes are doubtlessly ex- The freshwater invertebrate fauna of the South- tinct or at risk of extinction. east contains hundreds of species of mollusks, The southeastern fauna is now receiving some crustaceans, insects, mites, and other animals protection from the U.S. Endangered Species Act (Fig. 7) that are found nowhere else in the world. and parallel state laws. Nevertheless, unless the Dozens of genera and two families of invertebrates continuing damaging effects of human activities [Parvidrilidae (Oligochaeta) and Neoplanorbidae like impoundments are reversed or remediated, (Gastropoda), the latter now probably extinct] it is difficult to be optimistic about the long-term are known only from this region. Many of these prospects for the southeastern freshwater biota. species have small ranges within the Southeast and may have occurred in only one stream. De- Sources: Benz and Collins, 1997; Lydeard and Mayden, 1995. spite a long history of scientific study in the South- east, new species and genera of freshwater invertebrates are discovered regularly in the region. As is the case for many river systems, the streams and rivers of the Southeast have been known about the occurrence of sparse populations of profoundly affected by human activities. Im- freshwater invertebrates. Likewise, relatively little is poundments have been especially damaging to known about the causes of population sparseness, or the invertebrate fauna. All of the large rivers in about how population density per se affects the proba- the region have been extensively impounded for bility of species extinction. Generally, large-bodied ani- flood control, hydroelectric power, and naviga- mals have lower population densities than small-bodied tion, to the point that some of the large rivers animals, and predators have lower population densities have been converted into a continuous series of than their prey, although many exceptions exist to these reservoirs. These reservoir systems differ from generalizations. Further, population densities often are natural rivers in their hydrology, temperature, lower near the edge of a species range than in its center, chemistry, sediments, and so on, and often are and may be lower in unproductive habitats than in unsuitable for the native riverine biota. Other more productive habitats. Thus, we might expect to physical alterations of stream channels, such as find sparse populations especially in large-bodied inver- channelization, dredging, diking, and instream tebrates and in unproductive habitats like deep lakes gravel mining, also have severely damaged the and groundwaters. freshwater biota in parts of this region. Further, as in most developed countries, these river systems have been badly polluted by toxins, nutrients, and sediments from industries, farms, and cities. Coal III. PRESSURE OF HUMAN ACTIVITIES is mined in parts of the Southeast, which brings acid mine drainage and fine sediments into Human activities endanger freshwater invertebrates in streams. Finally, invasive species, particularly the many different ways. Five broad classes of activities ENDANGERED FRESHWATER INVERTEBRATES 431

Box 2 affinis, seems to be the only potentially damaging Mound Springs of the Great Artesian Basin alien in the springs). Over the past two decades, in Australia the springs of the Great Artesian Basin have come to be recognized as important habitats for conser- Much of the arid interior of eastern Australia is vation, and steps are being taken to limit at least underlain by a large aquifer called the Great Arte- local impacts from grazing and habitat alterations. sian Basin. Freshwater and brackish-water springs Nevertheless, many springs, especially in New occur along the margins of this aquifer in Queens- South Wales, have dried up as a result of ground- land, New South Wales, and South Australia. water extraction, and many have been badly al- These springs range in size from small, moist tered by livestock or people. It seems likely that seeps to large (Ͼ100 liters/sec), flowing springs, Ͼ at least some of the unique invertebrates of the and some of them have built up large ( 10 m Great Artesian Basin have gone extinct, and the high) hills of sand and mineral deposits, and so remaining fauna is at risk of loss. are locally called ‘‘mound springs.’’ Although per- In arid regions around the world, extreme iso- haps connected to one another in the past, when lation of aquatic habitats has promoted speciation the Australian climate was wetter, the springs are and development of endemic invertebrate faunas. now separated from one another by a few meters As in the Great Artesian Basin, water in arid re- to many kilometers of desert, and are not con- gions is a critically important resource that has nected by streams or rivers. been exploited heavily by people. Consequently, Like many springs in arid regions, the springs freshwater invertebrates of arid regions around of the Great Artesian Basin support animals that the world are endangered by forces similar to live nowhere else in the world. Many of these those at work in this basin. species are found in only one or a few neighboring springs. Only the fish and the snails of these Aus- Sources: Knott and Jasinska, 1998; Ponder, 1986, 1995; Pon- der and Clark, 1990; Ponder et al., 1989. tralian springs have received serious study. About 25 species and 3 genera of snails have so far been found to be endemic to the springs (Fig. 8). All of the endemic snails belong to the Hydrobiidae, a widespread family that has produced flocks of endemic species in springs, caves, and groundwa- that are especially important in altering fresh waters ters in the Balkans, the arid Southwest of the and endangering their inhabitants are considered here. United States and Mexico, and elsewhere. Al- though these snails may be very abundant in the Australian springs (Ͼ1,000,000/m2), some species are restricted to one or a few springs, and A. Habitat Destruction and Degradation all are highly vulnerable to human impacts. The Humans have massively altered the physical characteris- endemic fauna is thought to have originated by tics of many freshwaters, usually without consideration speciation in the more or less isolated springs, for consequent effects on the biota. These physical alter- perhaps after a more widespread fauna was ations probably are the chief cause of endangerment of stranded in the springs by an increasingly arid freshwater invertebrates. Dams have been especially Australian climate in the Pleistocene. damaging (e.g., Fig. 5). Above the dam, running-water The chief threat to the spring fauna is from habitats are converted into an artificial pool that is development of wells in the Great Artesian Basin. usually unsuited to the native invertebrate species. Be- Because this is an arid region, there is great de- low the dam, the water temperature and flows of water mand for water for humans and livestock. When and sediment often are so altered that downstream new wells are brought into production, the reaches support a highly artificial biota as well. Finally, groundwater level drops, causing springs to dry the dam itself is a barrier that blocks normal migrations up. Additional threats include the trampling of and movements of the riverine biota. Thus, even a single springs by livestock, which has badly degraded dam may endanger the riverine biota for hundreds of many springs, conversion of springs into pools kilometers, and many river systems are now dismem- by excavation or damming, and introduction of bered by dozens or even hundreds of dams. alien species (so far, the mosquitofish, Gambusia In many rivers and streams, floodplains and other 432 ENDANGERED FRESHWATER INVERTEBRATES

decomposition of which may reduce concentrations of dissolved oxygen to levels too low to support most species of invertebrates. Other wastes include sub- stances (e.g., mercury used in gold mining, acid precipi- tation from power plants and automobiles) that are directly toxic to freshwater invertebrates. Particularly in industrialized regions, long reaches of streams and rivers have been nearly sterilized of invertebrates as a result of severe, chronic pollution (e.g., Fig. 6). In addition to pollution caused by deliberate waste disposal, pollution may arise from a wide range of human activities in the watershed. Thus, conversion of forests or native grasslands to agricultural fields or development typically greatly increases loadings of sediments, nutrients, and toxins that are washed in from the FIGURE 5 Status of the 91 species of freshwater mussel species that formerly occurred in the Tennessee River (United States), which now altered watershed. These ‘‘non-point-source’’ pollutants consists largely of a series of reservoirs. (From Benz and Collins, are more difficult to track down and control than point 1997.) loadings of pollutants from factories, yet may have equally serious effects on freshwater ecosystems. While pollution has come under partial control in many developed parts of the world, residual pollution from past shallow-water marginal habitats have been destroyed releases and inadvertent spills still damage the freshwa- by dredging, channelization, or filling, or separated ter biota. Spectacular recent examples include a large from the main channel by dikes and levees. Further, spill of pesticides into the River Rhine following a fire humans often simplify shoreline habitats in both lakes at a Sandoz chemical plant, which killed fish and inver- and streams by straightening or filling shorelines and tebrates for hundreds of kilometers, and the overturning removing trees along and in the water. Because marginal of a truck that spilled a rubber accelerant into the Clinch habitats often are important for the feeding and spawn- River, Virginia, which killed most aquatic animals in a ing of the freshwater biota, the loss or isolation of these 10-km reach, including hundreds of endangered mus- habitats may have grave consequences for the native sels. This was the largest ‘‘take’’ of endangered species biota. When water is removed from a river for irrigation in the United States since the Endangered Species Act or held up in a reservoir for hydroelectric generation was passed in 1973. Of course, in many less-developed or flood control, downstream reaches may dry up or parts of the world, water pollution is still poorly con- lose critically important floods. Several of the world’s trolled. major rivers (e.g., the Colorado and the Ganges) no longer flow to the sea during dry periods. Likewise, the drawdown of many of the world’s aquifers from overuse of groundwater presumably has major effects on the groundwater biota, although these effects have scarcely been studied. Finally, mining of underwater deposits (for gravel or gold, for instance) may have devastating effects at the site of mining, as well as far downstream through sediment transport and far upstream though headcutting of the streambed.

B. Pollution Water pollution is another widespread activity that has had severe effects on freshwater invertebrates. Rivers FIGURE 6 Destruction of the freshwater mussel fauna in the Clinton and lakes often have been used for waste disposal. These River, Michigan (United States), in the mid-twentieth century by wastes include sewage and other organic matter, the pollution from the city of Pontiac. ENDANGERED FRESHWATER INVERTEBRATES 433

Box 3 endemic invertebrate fauna that may yet be pre- Lake Baikal, Russia served through careful management. Lake Baikal, part of a rift system in southeastern Sources: Kozhov, 1963; Kozhova and Izmest’eva, 1998; Mar- tens et al., 1994. Siberia, is the oldest (Ͼ25 million years old) and deepest (Ͼ1600 m deep) lake in the world, and covers 31,500 km2. It is the only great rift lake that is oxygenated to its bottom, allowing coloni- zation of the entire lake by a wide range of inverte- C. Direct Harvest brates. So far, more than 1400 species of inverte- Some freshwater invertebrates are harvested for human brates have been found in the lake, about 60% of use, which may contribute to their endangerment. which live nowhere else in the world. Many gen- Freshwater mussels have been fished for their shells, era and four families of invertebrates [Lubomir- pearls, and meat since prehistoric times. Especially in skiidae (Porifera), Baicalarciidae (Turbellaria), the nineteenth and twentieth centuries, harvest rates Baicaliidae (Gastropoda), Benedictiidae (Gastro- became so high that many populations were locally poda)] are endemic to Baikal. Probably the most depleted in Europe and North America. For example, remarkable group of endemic species in Baikal is over 13 million kg of shells from living unionids were Ͼ the huge flock (46 genera and 250 species) of taken from Illinois streams and rivers in a single year endemic gammarid amphipod crustaceans (Fig. during peak harvests. Another heavily harvested fresh- 9). These amphipods, which constitute more than water invertebrate is the medicinal leech Hirudo medici- one-third of all gammarid species in the world, nalis, which was collected in large numbers in Europe have diversified into a wide range of morphologies when blood-letting was widely practiced in the eigh- and behaviors and occupy a range of ecological teenth and nineteenth centuries. As a result of this niches, including planktonic and benthic herbi- collecting and widespread pollution and habitat de- vores, detritivores, predators, and semiparasites struction, this animal is now threatened. Harvests of on sponges. New species of invertebrates are Australian crayfish from the wild are now hundreds of found regularly in Baikal, so it is clear that the tons per year and have contributed to the endangerment true diversity in the lake is even higher than these of some species. Other invertebrates are collected for figures imply. A distinctive feature of the Baikal bait or the pet trade, which may contribute to local fauna is that, though nearshore areas contain a depletion of populations. Invertebrates sometimes are mixture of endemic and widespread species, the protected by harvest regulations (e.g., closed seasons, open water and abyssal sediments are inhabited size regulations, bag limits), but such regulations may chiefly by Baikalian endemics. be inadequately conceived and poorly enforced. Fortu- In many ancient lakes (e.g., Victoria in Africa, nately, for economic reasons, harvests usually (but not Biwa in Japan, Lanao in the Philippines), pollu- always) concentrate on common species rather than tion, habitat destruction, overfishing, and intro- rare ones. ductions of alien species have extinguished many endemic species. Baikal has been protected by its remoteness and vast size, and its fauna has so far D. Alien Species been relatively unaffected by human activities. Humans often move species outside of their native Nevertheless, industrial and domestic waste and ranges. Such introductions may be deliberate, such as siltation arising from deforestation of the catch- the stocking of trout throughout much of the temperate ment have polluted nearshore areas. Although world, or inadvertent, such as the widespread move- lakewide water quality seems not to have suffered ment of species in ships’ ballast water. Whatever the yet, pollution is a concern in Baikal because the cause, these alien species often have strong ecological long residence time of water in the lake means impacts, and sometimes are responsible for the endan- that contaminants entering Baikal may remain in germent of freshwater invertebrates. A spectacular ex- the lake for a very long time. In addition, alien ample is the loss of native unionid mussel populations species (e.g., including several fish and the aquatic throughout much of northeastern North America as a plant Elodea canadensis) have the potential to af- result of competition with the introduced zebra mussel fect the nearshore fauna. Lake Baikal is a remark- (Dreissena polymorpha). It is projected that the zebra able example of an ancient lake with a richly mussel will be the final blow that will drive several 434 ENDANGERED FRESHWATER INVERTEBRATES species of unionids into global extinction. Alien species which includes 1151 species of freshwater invertebrates may also serve as important predators of freshwater (Table II). Although an enormous amount of work by invertebrates, as in the case of the brown trout (Salmo experts went into compiling the IUCN list, it is clearly trutta), which when introduced to Tasmania apparently incomplete. The list is dominated by large, conspicuous, preyed on and reduced the range of the unusual and and attractive animals (mollusks, decapods, dragonflies, endemic anaspidacean crustacean Anaspides tasmaniae. and damselflies). There is no reason to believe that Because the effects of alien species tend to be cumulative smaller and less conspicuous animals are less endan- and difficult to reverse, this is a difficult and growing gered, but there is simply insufficient information on problem in invertebrate conservation. the status and trends of their populations to identify many endangered species. Likewise, almost 80% of IUCN-listed species are from North and Central America, Australia, or Europe, which probably reflects E. Global Climate Change the geographical distribution of conservation biologists Humans have changed the chemistry of the earth’s at- as much as the actual distribution of endangered fresh- mosphere so much that significant changes in global water invertebrates. Another way to assess global en- climate are expected in the twenty-first century. At this point, it is difficult to make precise predictions about how these changes will affect specific bodies of freshwa- TABLE II ter. In many bodies of water the changes may be varied Numbers of Species of Freshwater Invertebrates and large, involving such diverse characteristics as tem- Included on the 1996 IUCN Red List of perature, hydrology, water level, rising sea level, strati- Threatened Animals, by Taxonomic Group fication, the nature and severity of disturbances, in- and Continent creases in damaging ultraviolet light, water chemistry, Turbellaria (flatworms) 1 riparian vegetation, and food quality. In regions where Hirudinoidea (leeches) 1 freshwater becomes scarcer while human demands for Gastropoda (snails, limpets) 375 water continue to grow, human destruction and degra- Bivalvia (clams, mussels) 192 dation of freshwater habitats probably will become Amphipoda (scuds) 73 more severe. Even though we cannot yet specify the Syncarida (anaspidaceans, bathynellaceans) 4 details of global climate change, it is almost certain that Cladocera (water fleas) 8 this change will endanger or extinguish many freshwa- Anostraca (fairy shrimps) 24 ter invertebrate species. A rapid, large change in climate Conchostraca (clam shrimps) 4 will make habitats unsuitable for some of their native Notostraca (tadpole shrimps) 1 species. To survive, such a species will have to disperse Copepoda (copepods) 78 to a body of water with suitable ecological conditions. Decapoda (crayfish, crabs, prawns) 169 As we have seen, though, the dispersal rates of many Isopoda (sow bugs) 34 freshwater invertebrates are slow, almost surely too Ostracoda (seed shrimps) 9 slow to keep up with the pace of climate change that Ephemeroptera (mayflies) 3 current models predict. Further, human modifications Plecoptera (stoneflies) 3 to waterways (e.g., impoundments) probably have made Odonata (dragonflies, damselflies) 143 long-distance dispersal more difficult. Coleoptera (beetles) 22 Trichoptera (caddisflies) 3 Diptera (true flies) 4 IV. NUMBER AND DISTRIBUTION North and Central America 601 South America 21 OF ENDANGERED Africa 143 FRESHWATER INVERTEBRATES Europe 147 Asia 62 How many of the world’s freshwater invertebrates are Australia 163 endangered, and where do they live? The most compre- Oceanic islands 14 hensive list of endangered animals available is the IUCN Total 1151 Red List (compiled by the World Conservation Union), ENDANGERED FRESHWATER INVERTEBRATES 435 dangerment of freshwater invertebrates is to examine These environments typically support highly endemic where damaging human activities coincide with areas invertebrate faunas that are probably very sensitive to of high endemism (Table III). Areas where freshwater human impacts. Throughout much of the world, hu- invertebrates are especially likely to be endangered in- mans living in arid and semiarid regions are pumping clude river systems throughout much of the unglaciated water out of aquifers faster than it can be replenished, world, groundwaters and springs in arid and semiarid resulting in large, rapid drops in the water table, which regions, and many industrialized areas. in turn dries up springs and aquifers. We know that Except in or near areas covered by Pleistocene ice, desert spring communities are endangered (see Box 2 recently emerged from the sea, or desiccated, river sys- on Australian springs), and it is possible that aridland tems often support species that are endemic to that aquifers are experiencing large but unseen losses in bio- drainage basin. Most river systems have been very diversity. highly modified through impoundment and other phys- In addition to these current threats to freshwater ical modifications, water withdrawals, and pollution. invertebrates, we can expect increasing problems in any Thus, we could project that most old river systems regions of rapid human population growth or economic probably contain endemic invertebrates, and that many development (e.g., China and Southeast Asia) from the of these invertebrates probably are endangered as a wide range of impacts that typically accompany human result of human activities (see Box 1 on the U.S. South- populations. Further, any rapid changes in climate east, for example). Only species that are good dispersers probably will cause endangerment and extinction of and thus live in many drainage basins or are habitat freshwater invertebrates. These climate changes are pro- generalists and thus occur in nonriverine environments jected to be most severe in middle to high latitudes. are likely to escape endangerment. Human impacts on Because of glaciation, endemism of freshwater inverte- rivers are almost global, and even river systems that brates is higher in midlatitudes than at high latitudes, have not yet been heavily impounded and modified so impacts of climate change may be most severe at (e.g., some basins in Southeast Asia and central Africa) midlatitudes, especially where the freshwater fauna and are facing impoundment and other large modifications environments already have been damaged by human in the coming decades. activities. Again, the poorly dispersing species will A second area where we might expect to find many probably be most severely affected. endangered invertebrates are groundwaters and springs As to the question of how many freshwater inverte- in arid and semiarid regions (e.g., northern Africa, the brates actually are endangered (or extinct) globally, American Great Plains and Southwest, and Australia). there is no certain answer at present. Only for a few

TABLE III Expected Global Patterns of Endangerment of Freshwater Invertebrates as a Function of Human Activities

Activity Geographic distribution Groups of animals affected

Impoundment Global, especially North America, China, India, and arid Many, especially migratory species or those that de- regions pend on flooding or turbid water Physical alterations Global, especially highly developed regions Many, especially those that depend on marginal (diking, channel- habitats (shallows, floodplains) ization, shoreline modification) Water withdrawal Global in arid and semiarid regions Many, perhaps especially species living in groundwaters and springs Toxic pollution Global, especially industrialized regions Most species Eutrophication Global, especially densely populated or farmed regions Species of lake profundal sediments or plant beds Harvest Locally important throughout the world Bivalves, decapods, sometimes others Alien species Global in surface waters, perhaps rare in groundwaters Many Climate changes Global, especially in high latitudes Many, perhaps especially species that disperse poorly 436 ENDANGERED FRESHWATER INVERTEBRATES

FIGURE 7 Some endemic freshwater invertebrates from the U.S. Southeast. Clockwise from upper left (with length in parentheses): the flatworm Sphalloplana holsingeri (14 mm), the snails Io fluviatilis (73 mm), Gyrotoma alabamensis* (25 mm), and Amphigyra alabamensis* (2 mm wide), female (50 mm wide) and male (38 mm wide) of the pearly mussel Epioblasma lewisii,* the copepod Rheocyclops carolinianus (0.4 mm), the isopod Antrolana lira (20 mm), and the stonefly Beloneuria georgiana (22 mm). Species marked with an asterisk are thought to be extinct. [From Bowman, T. E. (1964). Antrolana lira, a new genus and species of troglobitic cirolanid isopod from Madison Cave, Virginia. Int J Speleol 1, 229–244; Burch, J. B. (1975). Freshwater Unionacean Clams (Mollusca: Pelecypoda) of North America. Malacological Publications, Hamburg, Michigan; Burch, J. B. (1989). North American Freshwater Snails. Malacological Publications, Hamburg, Michigan; Kenk, R. (1977). Freshwater triclads (Turbellaria) of North America. IX. The genus Sphalloplana. Smithsonian Contributions to Zoology 246, 1–38; Reid, J. W., et al. (1999). Rheocyclops, a new genus of copepods from the southeastern and central United States (Copepoda: Cyclopoida: Cyclopidae). J. Crustacean Biol. 19, 384–396; Stewart, K. W., and B. P. Stark (artist Jean A. Stanger). (1988). Nymphs of North American Stonefly Genera (Plecoptera), Thomas Say Foundation Vol. 12, Entomological Society of America. All figures are reprinted with permission.] ENDANGERED FRESHWATER INVERTEBRATES 437

FIGURE 8 Endemic hydrobiid snails (Jardinella spp.) from springs in Australia’s Great Artesian Basin. Shells are 1.5–3.5 mm high. (From Ponder and Clark, 1990, with permission.)

conspicuous and well-studied invertebrates (e.g., listed as a protected species may not provide enough unionoid mussels, odonates) are the IUCN estimates help to endangered invertebrates. In many countries, likely to be an accurate reflection of actual endanger- resources for managing endangered species are insuffi- ments. A reasonable guess might be that 3000–10,000 cient, and attention naturally goes to the larger, more of the world’s freshwater invertebrate species are extinct charismatic species. In a recent year in the United States, or endangered as a result of human activities. half of all money spent on endangered species was directed to just seven species, all of them vertebrates. As a result, so little money and attention may be spent on invertebrates that plans for recovery of invertebrate V. PROTECTION OF ENDANGERED species often are general and not pursued aggressively. FRESHWATER INVERTEBRATES Third, current approaches to species protection may be inadequate to protect species over the long term. Often, Although freshwater invertebrates are protected by in- legal protection focuses on trying to prevent further ternational, national, and local regulations, this protec- losses from the remaining small populations of an en- tion often is inadequate, for several reasons. First, lists dangered species, without adequate attention to remov- of protected species usually underlist invertebrates and ing the threats that endangered the species in the first include only the largest, most conspicuous species. For place. Consequently, legal protection may slow the rate instance, in the United States, only 111 domestic species at which an invertebrate species approaches extinction of freshwater invertebrates are protected under the En- without reversing its downward trajectory. dangered Species Act (compared with 318 species of How might we more effectively reduce extinction vertebrates), all but 25 of them mollusks. Thus, many rates of freshwater invertebrates? First, we need to de- species of endangered freshwater invertebrates, espe- vise ways to protect species without formally listing cially small and inconspicuous animals, are not being them. Human activities will endanger or extinguish protected by existing regulations. Second, simply being many species of freshwater invertebrates before we ever FIGURE 9 Endemic gammarid amphipods from Lake Baikal, showing some of the wide diversity of body forms. Body lengths are 1.5–6 mm. [From Salemaa, H., and R. Kamaltynov. (1994). The chromosome number of endemic Amphipoda and Isopoda—An evolutionary paradox in the ancient lakes Ohrid and Baikal. Arch. Hydrobiol. Ergeb. Limnol. 44, 247–256, with permission.] ENDANGERED FRESHWATER INVERTEBRATES 439 gather enough information on their status to satisfy Despite these problems, it may be necessary to con- requirements for legal listing, and before we have front the problem of species reestablishments, espe- enough information on their biology to develop effec- cially if climate change in the twenty-first century is tive species-specific plans to protect them. One way to substantial. Clearly, we will need much better informa- do this is to take advantage of the fact that many species tion on how fast species are able to disperse in response of endemic freshwater invertebrates co-occur in hot to a changing climate (to identify which species, if any, spots by protecting such hot spots from the most dam- will perish without intervention), practical information aging of human activities (e.g., dams, excessive water on how to establish populations of freshwater inverte- withdrawals, toxic pollution). Such a program of hot brates, and reliable models to predict whether the spe- spot protection will require better identification, recog- cies we move will have undesirable effects in their nition, and protection of hot spots. Nonetheless, it may new homes. require less research and provide more effective protection to the world’s freshwater invertebrates than ex- See Also the Following Articles isting species-based programs. Of course, not all endangered species occur in hot spots, so species-based ENDANGERED MARINE INVERTEBRATES • ENDANGERED • • research and protection will necessarily have to accom- TERRESTRIAL INVERTEBRATES ENDEMISM EUTROPHICATION/OLIGOTROPHICATION • HOTSPOTS • pany any program of hot spot protection. Further, con- INTRODUCED SPECIES • INVERTEBRATES, FRESHWATER, servation biologists and policymakers need to be more OVERVIEW • LAKE AND POND ECOSYSTEMS aggressive in identifying and removing threats that endanger species rather than just trying to protect the few Bibliography populations that have somehow escaped threats. This will require creative thinking about how to preserve Benz, G. W., and D. E. Collins (eds.). (1997). Aquatic Fauna in Peril: or restore essential features of habitat without making The Southeastern Perspective, Southeast Aquatic Research Institute Special Publication 1. Lenz Design and Communications, Deca- unrealistic demands on humans. tur, Georgia. A second class of possible solutions could be focused Knott, B., and E. J. Jasinska. (1998). Mound springs of Australia. In on alleviating the dispersal limitations that are so acute Studies in Crenobiology: The Biology of Springs and Springbrooks for many freshwater invertebrates by actively establish- (L. Botosaneanu, ed.), pp. 23–28. Backhuys, Leiden, Netherlands. ing new populations of endangered species. This class Kozhov, M. M. (1963). Lake Baikal and Its Life. Dr. W. Junk, The Hague. of solutions is motivated by two main concerns. First, Kozhova, O. M., and L. R. Izmest’eva (eds.). (1998). Lake Baikal. simple protection of existing populations of endangered Evolution and Biodiversity. Backhuys, Leiden, Netherlands. species may fail to assure long-term survival because Lydeard, C., and R. L. Mayden. (1995). A diverse and endangered natural or human-caused catastrophes (e.g., the Sandoz aquatic ecosystem of the Southeast United States. Conservation spill) or normal population fluctuations ultimately may Biol. 9, 800–805. Martens, K. B., Goddeeris, and G. Coulter (eds.). (1994). Speciation drive many isolated populations into extinction. Sec- in ancient lakes. In Advances in Limnology, Vol. 44. E. Schweitzer- ond, it seems likely that global climate change may bart’sche Verlagsbuchhandlung, Stuttgart. occur faster than the abilities of some freshwater inver- New, T. R. (1995). An Introduction to Invertebrate Conservation Biol- tebrates to disperse into suitable habitats. To preserve ogy. Oxford University Press, Oxford, United Kingdom. species under these conditions it may be necessary to Ponder, W. F. (1986). Mound springs of the Great Artesian Basin. In Limnology in Australia (P. De Deckker and W. D. Williams, deliberately establish populations of endangered species eds.), pp. 403–420. CSIRO, East Melbourne, Australia. in new locations where suitable habitat exists. Several Ponder, W. F. (1995). Mound spring snails of the Australian Great serious problems attend this approach. First, we cur- Artesian Basin. In The Conservation Biology of Molluscs (E. A. Kay, rently cannot reliably identify ‘‘suitable habitat’’ for most ed.), pp. 13–18, Occasional Paper of the IUCN Species Survival freshwater invertebrates. Second, we do not have good Commission 9. IUCN, Gland, Switzerland. Ponder, W. F., and G. A. Clark. (1990). A radiation of hydrobiid snails protocols for reintroductions for most species. Third, in threatened artesian springs in western Queensland. Records of species introduced outside their native ranges may have the Australian Museum 42, 301–363. unpredictable and undesirable effects on ecosystems Ponder, W. F., R. Herschler, and B. Jenkins. (1989). An endemic and other species. Finally, many biologists feel that it radiation of hydrobiid snails from artesian springs in northern is unethical to introduce species outside of their known South Australia: Their taxonomy, physiology, distribution and anatomy. Malacologia 31, 1–140. historical ranges (of course, for many invertebrate spe- Williams, J. D., M. L. Warren, K. S. Cummings, J. L. Harris, and cies, the known historical range is much smaller than R. J. Neves. (1993). Conservation status of the freshwater mussels the actual and unknowable historical range). of the United States. Fisheries 18(9), 6–22.