Nature and Human Society: The Quest for a Sustainable World (1997)
Chapter: Nematodes: Pervading the Earth and Linking All Life
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Nematodes:
Pervading the Earth and Linking All Life
Abundance of Nematodes
The phylum Nematoda (Nemata), known commonly as roundworms, contains the most abundant, common, and genetically diverse multicellular organisms (Lambshead 1993; Platt and Warwick 1983). Usually, these organisms are invisible to all but a few specialized scientists because most are essentially microscopic and transparent. More than 85 years ago, Cobb (1914) eloquently noted that “if all the matter in the universe except the nematodes were swept away, our world would still be dimly recognizable, and if, as disembodied spirits, we could then investigate it, we should find its mountains, hills, vales, rivers, lakes, and oceans represented by a film of nematodes.” “So little do we know of this vast multitude of soil-inhabiting nematodes that the first spadeful of earth we lift is practically certain to contain kinds never seen before”, and 'There exists . . .a greater disproportion between the known and the unknown than exists in almost any other class of organisms.” With respect to Cobb's characterization of our knowledge of nematode diversity, relatively little has changed during the last 85 years. Somewhere between 500,000 and more than 100,000,000 nematode species are believed to exist on Earth (Lambshead 1993), but habitats certain to be richest in new species are mostly unexplored, and fewer than 25,000 species have been described (Andrássy 1992; Platt and Warwick 1983).
Diverse morphological, physiological, and behavioral adaptations allow nematodes to pervade nearly every habitat, but most habitat adaptations cross formal taxonomic boundaries, which arguably include two classes and 18 orders
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(figure 1). Most nematodes are nothing like the vertebrate parasite Ascaris (figure 2J), which represents the phylum in introductory biology texts and laboratory dissections; rather, most are microscopic nonparasites designated microbivorous because they feed on small organisms, such as bacteria, fungi, and algae. A few are parasites of plants, vertebrates, or invertebrates; others browse on plants as herbivores or are predators of small organisms. Most microbivorous nematodes are of unnamed species, but these poorly characterized taxa play an important role in decomposition of organic matter and nutrient cycling in all ecosystems (Freckman 1988; Peterson and Luxton 1982). Nonparasitic nematodes are commonly the most abundant microinvertebrates of terrestrial (Nielsen 1949), marine-estuary sediment (Warwick and Rice 1979), and freshwater ecosystems; they are also taxonomically heterogeneous, transcending 12 orders (figure 1). Seabeds, ranging from the tropics to the Arctic, are the habitats by far richest in nematode species diversity (Boucher 1990; Lambshead 1993). Although 4,000–5,000 marine nematode species have been named and described, full surveys of marine habitats probably will reveal many millions of previously unknown species (Andrássy 1992; Hope and Murphy 1972). The natural histories of these marine nematodes are diverse and sometimes astounding. Consider for example, marine nematodes that are symbiotic with chemotropic sulfur bacteria, a nematode that
Figure 1
Distribution of lifestyles and feeding habits among nematode orders. Classification system
modified from Maggenti (1981) and Chabaud (1974). Validity of order Triplonchida
is discussed in Decraemer (1995).
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Figure 2
Examples of morphological diversity of surface structures of nematodes
(SEM unless noted otherwise).
A.
One of larger plant-parasitic nematodes, Hoplolaimus columbus,
propped on human hair.
B.
Enlargement from figure 2A showing cuticular pattern of transverse
striations, lateral longitudinal lines, and phasmid sensory organ (arrow).
C.
Enlargement of tail end of figure 2A showing position of anus.
D.
En face view of Hoplolaimus columbus; during feeding,
hypodermic-needle-like stylet projects from oral opening and punctures
plant cell for feeding on cytoplasm.
E.
En face view of plant parasitic nematode Belonolaimus longicaudatus;
six minute openings of chemosensory receptors surround oral opening;
sensory receptors, amphid (arrow), occur on each lateral side.
F.
Lacelike surface pattern of new species of microbivorous nematode
Bunonema n. sp.
G.
New species of marine nematode, Epsilonema n. sp.;
arrow indicates position of vulva.
H.
Light micrograph of anterior end of new species of marine nematode;
most nematodes are transparent, and oral cavity with tooth is visible;
although this nematode is likely to be microbivorous, presence
of tooth (arrow) might suggest that it can feed as predator; oral cavity
leads to muscular esophagus, which terminates posteriorly (asterisk).
I.
One of pair of chemosensory organs (amphids) on anterior end of
Paradraconema n. sp.
J.
En face view of Ascaris suum, large intestinal parasite of pigs.
Oral opening is surrounded by pronounced papillae (arrow).
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attaches its eggs to itself and guards them until they hatch, and a moderate-size nematode (4 mm long) that lacks a mouth and digestive system but is packed with symbiotic organisms (Bernard 1994). It is impossible to anticipate the richness of lifestyles that will be discovered among such underexplored habitats. Nematodes of soil and freshwater sediment are only somewhat better known; about 6,000 species in these habitats have been named, but the rate of discovery of new species in some habitats suggests that that is only a small fraction of extant species (Andrássy 1992). Although nonparasitic nematodes have great diversity in tropical and temperate soils, they characterize the biota of all soils and are even present in dry Antarctic ones (Freckman and Virginia 1997; Lawton and others 1996; Sohlenius 1980; Yeates 1980).
Many of the most thoroughly studied human parasites, being macroscopic, have been recognized since ancient times (Thorne 1961). However, parasitic taxa of economic importance, such as those of plants and vertebrates, probably include fewer than 5% of all nematode species. Nearly 2,000 species in three orders are herbivores or known to parasitize plants (figure 2A-E); a few hundred principal species are responsible for billions of dollars of crop losses annually (Barker 1994). Even in nonagricultural habitats, the impact of plant parasites can be impressive; pinewood nematodes introduced from North America are capable of killing a large pine tree in Japan in less than six weeks (Mamiya 1983; Rutherford and others 1990). Similarly, roughly 12,000 species in six major orders are known to parasitize vertebrates, but among these, only about 36 are considered to have a direct impact on human health and 300 are of veterinary importance. Most invertebratesmainly insectsalso host nematodes, the associations ranging from phoresis to obligate parasitism. Although hundreds of named nematode species in four orders are known to be associated with insects, they probably represent a small fraction of the existing species, considering insect diversity and nematode specialization on such hosts. It is very likely that this pool of largely unexplored parasites is rich in potential biocontrol agents and management tools for medical, veterinary, and agricultural insect pests.
The inadequately developed state of systematic surveys has been a major limitation in the development of a phylogenetic taxonomic system for phylum Nematoda, but such a framework is fundamental to the predictability and repeatability of all other research on the group. The problem is not unlike assembling a 1,000-piece jigsaw puzzle with 975 missing pieces! Another limitation in developing this taxonomic framework has been the historical fragmentation of nematologists into groups that study vertebrate parasites, invertebrate parasites, herbivore and plant parasites, or free-living forms in such disciplines as agriculture, parasitology, veterinary science, medicine, and ecology. As a consequence, taxonomic classifications often reflect academic specializations, rather than broad-scale nematode phylogenetic relationships. This fragmented approach is like grouping puzzle pieces by their similar shapes; in some cases (as it is with edge pieces) it might be useful; but in most cases, there is little predictive power or congruence with historical relationships. These “discipline-specific taxonomies” are now being tested and for some groups revealed as artificial by robust DNA-based phylogenetic hypotheses (Blaxter and others 1998). Fragmentation by discipline also has resulted
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in overemphasis on parasitic groups of obvious economic importance but with no contextual connection to the grossly understudied nonparasitic groups, which make up the majority of nematodes. Broad-based biotic inventories will transcend these previous boundaries as taxonomists with diverse specializations collaborate to investigate nematode diversity through the application of varied methods.
Most recognized nematode species have been described on the basis of a morphotype that is presumed to be unique. Such species can be synonymized if it is demonstrated that the morphotype either is not unique or representative for the taxon. Andrássy (1992) estimated that 18% of named species of terrestrial and freshwater nonparasitic nematodes are invalid because they are synonyms or because information on the species is inadequate for assessing validity; it is unclear, however, whether this estimate of “invalid species” is generally applicable to the entire phylum. A potential source of error that has been more difficult to assess is the degree to which morphotypic uniqueness is a good estimator for ontologically real species; the integration of molecular data in nematode systematics provides an independent line of evidence to help address this problem (Adams 1998; Szalanski and others 1997; Thomas and others 1997).
Current systematics practice emphasizes that discovery and description of new nematode species requires phylogenetic context for many taxonomic decisions, including reevaluation of previously described species and their relationships. Errors in estimating evolutionary history can have critical implications for over-estimating or underestimating species numbers (Adams 1998). But one advantage of phylogenetic approaches to studying species-level questions is that thorough integrated approaches to gathering character data (for example, structural, molecular, genetic, and developmental data) can promote discovery of new taxa.
Geographic Distribution of Species
A measure of the distribution or degree of localization of nematode species is crucial to developing sampling strategies for estimating worldwide species richness. For example, is species abundance in the North American deserts similar to abundance in African deserts, and to what extent do the same species occur in both habitats? Because lifestyles and feeding habits of nematodes (figure 1) cover the biological spectrum, it is not surprising that species are varied in their patterns of distribution. A high degree of localization might be expected among the majority of nematodes that have low mobility and a life history that lacks a dispersal phase; these are determinants for high speciation rates (Castillo-Fernandez and Lambshead 1990). In some habitats, limited dispersal is by mechanisms that move sediment or soil, including wind or flowing water. Other species are globally distributed, because of a deep evolutionary history predating dispersal of continents (Baldwin 1992; Ferris 1979). In still other cases, nematode distribution is determined by the habitats of organisms with which they are closely associated. Many nematodes are dispersed through phoretic associations with mobile insects or birds, by anthropogenic effects (such as agriculture), or by congruence with a specific host. Such mechanisms determining geographic pattern cannot be separated
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from issues of isolation and speciation. Highly localized species or species restricted to a narrow habitat regime or a single host include a majority of nematodes, and these are most vulnerable to annihilation. The resources to measure the rate at which nematode species, including beneficial ones, are lost to anthropogenic effects are unavailable, but we can expect that the rate of loss is huge.
We have noted arguments that most nematodes are nonparasitic marine species (Lambshead 1993). However, in the marine environment, abundance and perhaps species geographic pattern vary somewhat with concentrations of organic matter, vertical distribution, latitude, and depth (Boucher 1990; Lambshead and others 1995). In deep seabeds and undisturbed soil systems, regardless of overall abundance, individuals of a particular species often are rare (Lambshead 1993; Grassle and Maciolek 1992; Hessler and Sanders 1967). For example, a deep-sea sample yielding 148 nematode species included only 216 individuals (Hope 1987).
Considering terrestrial and freshwater nematodes, Nicholas (1975)citing examples from the orders Dorylaimida, Araeolaimida, and Tylenchidaargued that to a striking degree, particular genera and species occur in all parts of the world and in a variety of habitats, irrespective (within wide limits) of soil's physical and chemical factors, climate, or vegetation. We would add a range of microbivorous Rhabditida, such as Acrobeloides nanus and Panagrolaimus rigidus, which, regardless of limited sampling, are known to have distributions that include all of Europe, Australia, Asia, Africa, and North and South America (Andrássy 1984). Often such wide distribution is difficult to explain. For example, a survey of nematodes in a freshwater lake in the Galápagos, colonized during its recent history of 15,000 years, included 18 species in five orders; 16 of the species were known in other parts of the world (Abebe and Coomans 1995). Thus, mechanisms of dispersal and colonization are not fully understood. In some cases, supposed geographic limits of species are an aberration of inadequate testing. For example, recent sampling in a California desert led to the discovery of microbivorous nematodes, including species previously known only in South Africa. Such geographic limits would be difficult to explain through introductions or biogeography; it is much more likely that more-extensive surveys will demonstrate a broad distribution of these species beyond California and South Africa.
Some parasitic nematodes have broad host ranges and are distributed nearly worldwide; an example is the root knot nematode, Meloidogyne incognita, one of the most destructive plant pathogens of agriculture and widespread in relatively undisturbed habitats (Eisenback and Triantaphyllou 1991). Other parasitic nematodes often are highly regionalized by specific requirements of their host and habitat. For example, the citrus pathogenic variant of Radopholus citrophilus, which at one time nearly destroyed the Florida citrus industry, is known only in that region. This nematode's requirement for a habitat of deep sandy soils might limit its distribution (O'Bannon 1977). A closely related species, Radopholus similis, is distributed globally throughout the tropics, whereas most other Radopholus species seem to be restricted to Australia, Asia, or Africa (Huettel and Dickson 1984; O'Bannon 1977; Sher 1968). To some extent, the wide distribution of Radopholus similis might be affected by anthropogenic effects of agriculture, including the spread on infected corms from Asia via propagation of bananas throughout the tropics.
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The cyst nematodes include a group of about six genera and 70 species, many of which have great economic importance to agriculture and diverse patterns of species distribution, determined by host specificity and coevolution, biogeography, and anthropogenic effects (Baldwin 1992; Baldwin and Mundo-Ocampo 1991). For example, the cyst nematode Punctodera chalcoensis is restricted to Mexico and clearly coevolved with its only host, Zea, including Z. mays (cultivated maize) and uncultivated species endemic to Mexico. The potato cyst nematodes, Globodera rostochiensis and G. pallida, were thought to be restricted to potatoes in Europe until the 1950s, when they were discovered on a shipment of potatoes from Peru. Later surveys in South America revealed that the potato cyst nematodes occur on wild plants throughout a region of the Andes, where they probably coevolved with potatoes. It is commonly believed that they were introduced to Europe with potatoes in the 1600s and later throughout many of the potato-growing regions of the world, despite rigorous regulation of shipments (Baldwin and Mundo-Ocampo 1991). Whereas a number of species of Globodera parasitize Solanaceae in the new world, another group of Globodera species seem to have coevolved with Compositae in Europe (Baldwin and Mundo-Ocampo 1991). The distribution of a wide range of cyst species can be traced from particular hosts and regions to biogeographic patterns and more recently movement of these nematodes with soil and roots associated with shipments of agricultural products (Baldwin and Mundo-Ocampo 1991; Ferris 1983, 1985; Stone 1977).
We have noted that distribution of parasites is a function of the distribution of the hosts. One general precept of animal parasitology is the expectation that a host species harbors several parasite species, some of which are probably restricted to that species of host. By extension, many nematologists who study animal parasites are not surprised when a new nematode species is described from a host species that has not been the subject of exhaustive examination. In fact, this generalization is frequently confirmed; most thoroughly investigated vertebrate hosts are likely to yield one or more novel nematode species.
The nematode parasites of domesticated hosts have been intensively studied because of their importance to agriculture. Host-parasite lists (for example, Soulsby 1982) provide some insight into the diversity of nematodes from domesticated hosts and other vertebrates. For example, bovine species have been reported to harbor more than 60 nominal nematode species representing 28 genera; these nematodes include specialists for many “habitats” within the hosts, including the digestive tract, circulatory system, respiratory system, muscles, urogenital system, skin, eyes, and body cavities. Similarly, pigs are reported to serve as hosts for 37 nominal species representing 24 genera, and equids host at least 43 nominal species representing 29 genera. It is unclear how many of the congeners reported from a single vertebrate host species are synonyms. This problem is no doubt more acute for some nematode groups than others, but recent molecular investigations show promise for investigating potential synonymies. For example, a study of nucleotide sequences indicated that three described species of vertebrate parasites (Teladorsagia spp.) had no detectable nucleotide differences in a rapidly evolving region of ribosomal DNA; this result was interpreted as evidence that the previously described morphotypes represented a single species (Stevenson and others
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1996). Similarly, sequence-based results (Newton and others 1998) were consistent with the inference of one species in the case of two nominal (and controversial) taxa of nematode parasites (Cooperia oncophora and C. surnabada) that were previously diagnosed on the basis of structural differences; this molecular finding was also consistent with the results of cross-breeding studies (Isenstein 1971). Conversely, it is unclear how many of the taxa assigned to a single morphological taxon represent cryptic species, but again genetic methods are beginning to shed light on the nature of species complexes in nematodes (Chilton and others 1992; Chilton and others 1995).
For many nematodes of vertebrate hosts, the extent to which nominal species are regionalized is often unknown because of the absence of systematic survey data. In addition, assessing geographic distributions of nematode parasites of vertebrates is made more difficult by the fact that nematodes are typically not uniformly distributed among individuals of a host species; instead many hosts remain uninfected while a few individuals harbor many nematodes (overdispersion). Predictably, the nematode parasites of domesticated vertebrates are geographically widespread because of transport of these hosts. Exceptions to that prediction might involve vector-transmitted nematode parasites, inasmuch as hosts could be moved to regions where required vectors are not codistributed. In the case of human-mediated movement of domesticated animals, the effect on their parasites is also evident from studies of nematode population genetic structure. For example, studies of four trichostrongylid nematode species (Ostertagia ostertagi, Haemonchus placei, H. contortus, and Teladorsagia circumcinta) occurring in three domesticated hosts revealed very little genetic differentiation among geographic regions of North America; this suggests that human transport of domesticated hosts has resulted in high nematode gene flow (Blouin and others 1992; Blouin and others 1995). In contrast, the genetic structure of a trichostrongylid nematode of deer (Mazamastrongylus odocoilei) was much more regionalized and showed a pattern of genetic isolation by distance (Blouin and others 1995).
Number of Species Per Habitat.
The vast numbers of nematode species, the diversity of their habitats (from soils and sediments to animals and plants), the paucity of surveys, and the inadequately developed state of nematode taxonomy make a global estimate of nematode species daunting. Nematodes can live in the bark of trees (pinewood nematode); as parasites of bees, lizards, and tomato plants; and even in mushrooms and earthworms. Even the smallest samples of habitat can contain hundreds of nematode species, including many unknown species. For example, Tietjen (1984) found in sampling marine sediments of the Venezuela basin that only two of 196 nematode species had been previously described. Lawton and others (1996) found over 200 nematode species in moist tropical Cameroon soils, but because of the expertise needed and the cost of identifying species, had to leave twice that many undescribed. For these reasons, the number of descriptions of nematode species is still in its infancy, and nematologists and ecologists rely on descriptions of functional groups or become specialists in the identification of particular groups of species.
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Nevertheless, there is some information that we can use with caution to examine global geographic and latitudinal patterns of nematode species diversity (table 1). The few studies in tropical forest soils (Coleman 1970; Hodda and
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Wanless 1994) before Lawton's study did not indicate that the tropics were foci of nematode diversity or abundance, as was found for nematode species associated with plants and animals. Temperate forests had much higher species diversity. Although table 1 shows that the number of species is similar in Indiana agroecosystems and in the Cameroon forest, species were still being identified in the Cameroon when the study ended. The results seem to support Hammond (1992), who suggested that the well-documented floristic richness of areas that are seasonally dry might not be paralleled by the richness of terrestrial invertebrates, fungi, or microorganisms. At the other extreme of diversity are the soils of the Antarctic Dry Valleys (78°S), which have only three endemic speciesperhaps the lowest nematode diversity on Earth (Freckman and Virginia 1997). Surprisingly, agroecosystems, which we think of as being disturbed ecosystems, can have over 100 nematode taxa (Freckman and Ettema 1993; Yeates 1980). Yet we also know that different agronomic practices have different effects on nematode diversity, including the loss of some species. Those examples indicate the need for a more strategic effort in identifying these speciose animals.
The lack of knowledge about the total numbers of nematode species present on even the smallest scalessay, in 10 g of soilmakes estimates of total species in different habitats or even globally a monumental task. There is considerable variability in estimates that have been attempted (table 1), with estimates of total nematode species globally as low as 100,000 (GBA 1995); in contrast, Lambshead and others (1993) estimated the highest number of marine nematode species alone to be 100,000,000.
A fundamental problem encountered in estimating regional or global nematode species diversity is that many of the traditional diversity methods might not be applicable to such a group as poorly described and as varied as nematodes. For the near future, estimates of global nematode biodiversity will remain speculative. Methods often used to estimate species numbers for poorly known but speciose groups do not seem particularly appropriate for nematodes. For example, one traditional method is to extrapolate from reliable available data with ratios that are established for better-known groups, such as birds or vascular plants. For nematodes, reliable data on species numbers on even the smallest scale are available for only a small number of habitats. Furthermore, by definition, groups that are well described can be very different from such poorly described groups, so it cannot be assumed that patterns are similar in both. Other methods, such as relating first principles and processes of ecology to species number (such as body size, food web structures, trophic links, and parasite-host relationships) are similarly compromised because the data behind the relationships are based on groups that are easy to access and might not be representative of nematodes. Methods that base estimates of total species numbers on patterns in the number of species that have already been detected are likely to be uninformative because rates of discovery probably are biased by our interests and resources rather than reflecting a true insight into the ratio of discovered to undiscovered species (Hammond 1992; May 1988, 1998).
Until a major effort is launched by the scientific community, we will continue to guess at this most abundant and important group of invertebrates. One approach
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that shows promise in estimating nematode species numbers in different habitats, and ultimately globally, is to develop theoretical estimates based on energetics. A model is being developed to estimate the total nematode biomass that can be supported in different habitats, on the basis of the carbon available in those habitats. This information might be used to estimate maximal viable nematode population sizes and species number at each trophic level (Freckman and Moore 1998).
Gaps in Knowledge?
Although nematodes are the most species-rich phylum of metazoa, most of the world's habitats are undersampled, and we can only begin to envision the numbers of species. Worldwide, wherever habitat is destroyed, microscopic nematode species with highly localized distribution are likely to be lost at a high rate with a cost to humankind that includes loss of biological control agents and unique natural compounds. The compounds, largely unexplored, might include anticoagulants, plant-growth regulators, and antimicrobials in bacteria dependent on nematodes (Jarosz 1996). Loss of nematode species also results in loss of opportunities to measure anthropogenic disturbance; the latter has implications for understanding and managing ecosystems. Inadequate knowledge of nematode diversity has led to introduction of destructive nematode species. Most recent surveys are biased toward the regions most accessible to the world's small and shrinking supply of nematode taxonomists, and development of a taxonomic system is biased to parasites that have obvious economic and medical effects. The greatest need is for data from representative habitats that will provide a predictive framework for testing hypotheses of global species diversity and targeting areas of strategic importance for the conservation and use of nematode species. Whereas it would be difficult to identify any region, even Europe or North America, as adequately sampled, the most undersampled habitats, relative to suspected diversity, are deep ocean sediments, wetlands, and tropical nematode-invertebrate associations. Data from expanded nematode surveys in Asia and Africa are particularly needed.
Assessment and conservation of nematode species diversity are confounded by an inadequate taxonomic and phylogenetic framework. The situation is exacerbated by the need for a new generation of nematode taxonomists with broad training in a range of classical and molecular tools in a rigorous phylogenetic context (Barker 1994; Ferris 1994; Hyman and Powers 1991; Systematics Agenda 2000 1994). Taxonomists can broaden their reach by working closely with parataxonomists, specialists trained to work with taxonomists for field collecting, processing material, and routine identifications. Furthermore, substantial financial resources are needed to support research in nematode biodiversity in general and to facilitate greater integration of nematode taxonomists throughout the world via readily accessible and well-supported taxonomic collections and electronic databases.
Number of Trained People Available
There is little argument that the number of persons trained to identify and describe new species of nematodes is woefully inadequate in light of the enormous
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size of the phylum and its largely underexplored state. No group of nematodes is as species-rich as marine forms. Lambshead (1993), predicting 100,000,000 species of marine nematodes, notes that even if there were only 1,000,000 species of nematodes, the task would be overwhelming; if 20 active marine nematode taxonomists worldwide were collectively describing about 200 species per year (an optimistic set of assumptions), it would take 5,000 years to describe the species! Considering broader groups of nematodes, about 30 taxonomists worldwide have the experience necessary to describe species in one or more orders of nonparasitic nematodes, including some marine taxa (SON Systematics Resources Committee 1994). The availability of taxonomists is only slightly greater for more specialized nematodes of economic importance. About 60 taxonomists worldwide work on one or more families of the orders Tylenchida, Dorylaimida, and Triplonchida, which include herbivores and plant parasites (figure 1). Taxonomy is a small portion of the overall responsibilities of these scientists; each might describe one or two species per year. For the six major orders of vertebrate parasites (figure 1), there are about 45 taxonomists worldwide. Species belonging to the four orders that include parasites or associates of other invertebrates (figure 1) have received expanded attention in recent years because of their potential as biological control agents of insect pests; but only about 25 specialists worldwide work on these nematodes. From the perspective of advancing knowledge of nematode biodiversity, more taxonomic emphasis should be placed on understanding nonparasitic taxa, particularly aquatic species.
Problem-Solving and Approaches for Greater Awareness
Increasing public value of ecology and the environmental sciences presents nematologists with opportunities to respond to a public receptive to understanding food webs, nutrient cycling, regulation of microbial populations, natural history, and biogeography. Bernard (1994) suggests that ocean-dwelling nematodes, because of their remarkable structural and biological variation, are potential magnets for programs that illustrate their natural history. Research on the nematode model Caenorhabditis elegans has already been featured in PBS programs on genetics, reproduction, and developmental biology. Internet sites, such as the Tree of Life Project (D.R. Madison and W.P. Madison; http://phylogeny.arizona.edu/tree/phylogeny.html), should not be underestimated in their effect on increasing public awareness of nematodes. The cost associated with such increased public awareness is that nematologists must be willing to set aside other responsibilities to accept outreach opportunities.
Understanding of nematode biodiversity will advance most efficiently when there is a global program harnessing the world's nematology expertise for coordinated sampling and database development; the first step in such a program will be to develop a sampling strategy designed to yield maximal information on global diversity with minimal expenditure of time and human and economic resources. Because nematodes are so pervasive and integrated with all of life, a global sampling program must be integrated with appropriate complementary
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expertise, including soils, marine biology, entomology, botany, and vertebrate zoology.
Development of the taxonomic infrastructure in nematology requires a commitment to programs for strengthening taxonomic expertise; these include international programs for training new taxonomists and support for systematic museum collections. Specimen-based collections provide basic tools for taxonomic work as repositories of preserved specimens, preserved DNA, and supporting databases and Web sites to aid inventory and access for specialists. Among the most promising new approaches for taxonomists are molecular tools refined to increase the efficiency and accuracy of surveys through databases that link morphological and molecular species diagnostics (NSF Workshop on Systematics and Inventory of Soil Nematodes, http://www.nrel.colostate.edu/soil/home.html) (Szanlanski and others 1997; Thomas and others 1997). Surveys and species identification are inseparable from the task of reconstructing a phylogenetic framework for nematodes (Adams 1998), but the tools for developing such a framework are more powerful and promising than ever before (Blaxter and others 1998).
The sciences that support advances in our understanding of nematode biodiversity are at an important crossroads. Nematology's base of classical taxonomistswith their wealth of information on nematode structure, diagnoses, and natural historyhas been seriously eroded over the last 15 years. Although molecular systematists are applying modern approaches that offer much promise to advance the discipline, the most fruitful outcomes will come from collaborative efforts of classically trained nematologists, molecular systematists, and other scientists who can apply novel tools that enhance our ability to address complex problems in biodiversity. There is a very narrow window of opportunity to train the next generation of nematode biosystematists schooled in both classical and new approaches, given that many universities have hired scientists who use reductionist approaches in preference to those who use the entire organism as the unit of study. With the reduction and dispersion of the remaining expertise, training of broad-based nematode biosystematists is more expensive because it often requires on-site work at several laboratories. Given our lack of data on the full extent of nematode diversity, it is not practical to estimate how many additional scientists are required to develop a thorough understanding of the phylum. But doubling the number of nematode biosystematists during the next two decades seems to be a conservative and necessary first step. Clearly, more emphasis should be placed on taxa that are not of direct economic importance, such as nonparasitic soil and aquatic species.
Those scientific imperatives cannot be accomplished without addressing some serious practical considerations. What agencies will provide the funding for this important research? How will the current pecking order among scientists be altered so that organismal biologists are considered to be as essential to university research programs as scientists who study fundamental processes at the molecular level? Documents like this cannot serve science if such practical problems remain unresolved or if scientists themselves do not adopt a more panoramic perspective of biology and, in the process, see fit to set priorities in research support for groups of organisms that are poorly understood and rapidly disappearing.
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Acknowledgments
We acknowledge support of National Science Foundation grants PEET 97-12355, DEB-93-18249, OPP 91-20123, and DEB 96-26813 and the help of Gina Adams. This work is a contribution to OPP 92-11773, the MCM LTER.
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