Foundations for an Integrative Parasitology: Collections, Archives, and Biodiversity Informatics

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Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

2002

Foundations for an Integrative Parasitology: Collections, Archives, and Biodiversity Informatics

Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected]

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Hoberg, Eric P., "Foundations for an Integrative Parasitology: Collections, Archives, and Biodiversity Informatics" (2002). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 662. https://digitalcommons.unl.edu/parasitologyfacpubs/662

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Comp. Parasitol. 69(2), 2002, pp. 124–131

President’s Symposium

Foundations for an Integrative Parasitology: Collections, Archives, and Biodiversity Informatics

ERIC P. H OBERG U.S. National Parasite Collection and Parasite Biology, Epidemiology and Systematics Laboratory, Agricultural Research Service, U.S. Department of Agriculture, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, Maryland 20715, U.S.A. (email: [email protected])

Burgeoning awareness about biodiversity em- ing invertebrate and vertebrate groups. This is phasizes the fundamental importance of museum not a lament, but simply history. Parasitology collections and the contributions of systematists has generally not been a factor in the develop- and taxonomists in documenting the structure ment or programs of most major natural history and history of the biosphere. An essential role museums, and the discipline tended to develop is served by this infrastructure in collecting, pre- along a divergent track, to become dominated paring, analyzing, and disseminating informa- by private or personal collections. Over time, tion about the specimens that represent species, and particularly in the last 25 yr, this dispersed document a range of complex biological asso- infrastructure has contributed to an incremental ciations from symbioses to parasitism, and form erosion by attrition of our systematics knowl- the tapestry and the myriad facets of biodiversity edge and expertise. Further, the tradition of often (e.g., Wilson, 2000). As parasitologists we can closely held, large personal collections has lim- examine how we may contribute to this broader ited the communication, progress, and growth of documentation and understanding of global bio- a cohesive systematics community and has now diversity, and we can articulate and communi- exacerbated the challenge to provide curatorial cate our role as vital participants to a larger services and databasing for an increasing num- community (e.g., Brooks and Hoberg, 2000, ber of significant orphan collections. Only 4 ma- 2001). This becomes increasingly important as jor repositories or specimens-based collections we continue to recognize that the effects of par- of zooparasites now exist in North America, 3 asites on humans, domestic animal food resourc- serving endoparasites, and 1 focusing on arthro- es, and wild biodiversity are a major interna- pod ectoparasites (Lichtenfels, 1994), and a crit- tional concern in this time of dynamic environ- ical mass for research infrastructure diminishes mental change. At the international level para- annually. sites are now viewed as significant components We can recognize that parasitology has made of biodiversity that must be included in plans for seminal contributions to our understanding of survey and inventory, conservation, and other the structure and history of the biosphere (sum- national needs focused on understanding envi- marized in part in Brooks and McLennan, 1993; ronmental integrity and ecosystem function Hoberg, 1997a). Parasitologists can choose to (e.g., Just, 1998; Pe´rez-Ponce de Leoń and Gar- build on the nexus between biodiversity studies cia-Prieto, 2001a, b, and references therein). and parasitology and concurrently construct a Although a core number of museum and in- necessary infrastructure that enhances the im- stitutional collections have been vital for the de- pact of museum collections and affords the ex- velopment of parasitology in North America, in pansion of opportunities for future generations the broader museum community there has been of systematists and taxonomists. Of course, this a relatively limited presence of systematists and is not the only future for parasitology, but 1 sig- taxonomists focusing on parasitic taxa. Addi- nificant cornerstone that emphasizes our classi- tionally, in North America there has not been a cal contributions while building a modern and longstanding tradition for support and develop- cutting edge tool kit for exploration and discov- ment of museum collections, resources, and cu- ery. Parasitology must reaffirm its commitment ratorial positions for parasitology on the scale to systematics; otherwise, the future of parasite evident for programs focusing on many free-liv- systematics will be decided by nonparasitolo-

124 HOBERG—PARASITE COLLECTIONS AND BIODIVERSITY 125 gists. In this context, comments herein will be source for systematic, taxonomic, and diagnostic focused on several areas: 1) resources and infra- ecological and epidemiological research in par- structure for museum collections, with particular asitology has been continuously maintained by focus on the history and dual roles and respon- the USDA for over 100 yr (Lichtenfels et al., sibilities of the Agricultural Research Service 1992; Lichtenfels, 1994; Lichtenfels et al., (ARS) and the U.S. National Parasite Collection 1998). The USNPC has served as a critical re- (USNPC); 2) biodiversity and systematics as es- source for all aspects of parasitology in North sential foundations for research in parasitology America and globally and provides the founda- (e.g., Brooks and Hoberg, 2000); 3) the evolution for all programs within the ARS and else- tion of collections from static repositories to where that deal with the systematics and tax- functional information systems in the realm of onomy of agriculturally and economically sig- biodiversity bioinformatics (e.g., Blackmore, nificant helminthic and protozoan parasites. The 1996; Bisby, 2000; Edwards et al., 2000); and scope and depth of the Collection are unparal- 4) examination of the challenges and opportu- leled in North America. The current holdings are nities facing parasitology in responding to the substantial, and the collection is among the larg- needs of science and society. est in the world (in excess of 100,000 lots, and over 20 million individual specimens; 3,000 ho- THE USNPC: A CENTURY OF SERVICE lotypes, 7,000 type series) and accumulates The ARS of the U.S. Department of Agricul- about 1,000–1,500 new lots of specimens an- ture (USDA) has been the home for mission- nually. A primary role of the USNPC is acqui- oriented and problem-solving research on para- sition, curation, and long-term maintenance of sites and pathogens that directly or indirectly the specimens-based collections, and develop- threaten animal health, food safety, and the en- ment and expansion of the collections database vironment. A core facility within the current lab- as an irreplaceable national archive. The speci- oratory structure is the USNPC located at the men collection is linked to extensive documen- Henry A. Wallace Beltsville Agricultural Re- tation of host occurrence, geographic range, and search Center near Washington, D.C. other core data with which to assess the current Since 1892 the parasitological collections and historical distribution of parasites and path- held by the USDA have been the focus for de- ogens, with a database accessed through the In- velopment of knowledge about the distribution ternet (http://www.anri.barc.usda.gov/pbesl). of parasites, pathogens, and diseases (Lichten- A uniquely federal role is served by the Col- fels et al., 1992, 1998). The evolution of these lection as a center for diagnostics, identification, collections has followed the expansion of re- and dissemination of information. Parasitologists search programs targeted to solve a number of in the ARS and others working in veterinary, emerging problems for agriculture during the medical, and wildlife parasitology have access last century. Concurrently, what is now the to the necessary specimens and database to con- USNPC became the focal point for field-based duct studies on the identification, classification, and empirical research emphasizing survey and and distribution of parasitic helminths and pro- inventory, systematics, biogeography, and ecol- tozoans. The specimens collections, accumulat- ogy among a diverse assemblage of helminth ed over 150 yr, are a historical baseline and re- and protozoan parasites of vertebrates and con- source for biodiversity research globally. The tributed to experimental studies to address the collection is the foundation for proactive pro- biology of an array of economically significant grams, prediction, and prevention with respect parasites. Thus, over the past century, the to parasites and pathogens that pose risks to the USNPC has served an essential and dual role for health of animals, humans, and the environment. science and society in both providing a foun- The USNPC’s vision focuses on these issues: dation of knowledge about the host and geo- ‘‘Serving society through biodiversity discovery graphic distribution of parasites and contributing and exploration, systematics, predictive classifi- to the resolution of a number of real world prob- cations, and interactive information systems for lems facing farm and industrial production of parasites that contribute to identification of new food animals, food safety, and protection of the and emerging threats to animal health, food safe- environment. ty, and the environment.’’ The USNPC, a national and international re- The USNPC serves a diverse and global con- 126 COMPARATIVE PARASITOLOGY, 69(2), JULY 2002 stituency, providing curation and access to spec- can serve as historical or temporal baselines and imens and databases that drive parasitological archives for understanding the influence of en- research. The combined resources of the USNPC vironmental change or human intervention on and its substantial sister-collections, including the distribution of parasites and pathogens. In- the Harold W. Manter Laboratory (University of teractive information systems linking diagnostic Nebraska State Museum), the U.S. National Tick keys with phylogenetic and epidemiological and Collection (Georgia Southern University), the biological information for access on the World Canadian Museum of Nature, and other smaller Wide Web are also central to this concept. In taxonomically focused institutional facilities essence the logical course for growth and rele- (Lichtenfels, 1994), form the primary infrastruc- vancy of parasite collections is in building the ture for systematics, taxonomy, and biodiversity infrastructure for biodiversity bioinformatics, of metazoan and protozoan parasites in North with museum staff serving as ‘‘curators of in- America. In the current environment we have an formation,’’ where a series of interrelated data opportunity to formulate policy and seek syn- frameworks within and among museums collec- ergistic interfaces within this community of sys- tively summarize our base of knowledge in a tematics collections to further a broad goal of synergistic manner (Bisby, 2000; Brooks and contributing to a comprehensive knowledge of Hoberg, 2000, 2001). parasite biodiversity at local, regional, and glob- Biodiversity informatics represents an essen- al scales. tial contribution through formulation of relation- al databases and development of interactive in- COLLECTIONS AS INFORMATION SYSTEMS formation systems that represent the next step in The current view of the USNPC and other managing and disseminating parasitological data collections is that to remain vital and relevant, derived from specimens-based collections. At a we must be in a position to develop our resourc- general level, we can formulate and contribute es as information systems. It is not enough to to a new paradigm of parasite collections as in- simply hold and maintain specimens in a static formation systems by building a world of dis- repository; in this sense size doesn’t matter; tributed databases linking specimens-based col- rather, it is the information contained in unique lections. Parasites thus become a window on the specimens as a representation of a complex bio- world revealing facets of biocomplexity, and sphere that is significant. We have an obligation further, become resources for documenting bio- to maximize the information content of collec- diversity as a general reference system for the tions and to disseminate this information to a dynamics of intricate biological associations. broad-based user community (e.g., Blackmore, 1996). Such an approach is consistent with the THE CHALLENGE FOR PARASITE current mandate of the Convention on Biological SYSTEMATICS Diversity (CBD) and the Global Taxonomy Ini- Systematists are purveyors of basic informa- tiative (GTI), which seek to improve taxonomic tion about species, and it is the systematics com- knowledge and the capacity to meet a country’s munity that collectively creates the foundations needs and support activities for conservation, for biodiversity informatics. Systematists hold sustainable use, and equitable sharing of benefits and codify their special knowledge in the form and knowledge of biodiversity (Creswell, 2000). of species names that represent the physical and Components of a parasitological information ecological characteristics of known organisms, system should include specimens-based biodi- which are the essential elements of genealogical versity inventories, comprehensive species lists, reference systems. Systematics is also the frame- validation of morphological information, sum- work for comparative studies in basic and ap- maries of key phylogenetically diagnostic char- plied biology. In parasitology, systematics re- acters, and total evidence systems incorporating search is the predictive foundation for recogniz- morphological, molecular, and genomic data. ing emergent and invasive species, documenting Development of integrated information systems patterns of distribution for pathogens and dis- linking parasite, host, and geographic (geo-ref- ease, applied epidemiology, and successful in- erenced) data and development of applications tervention either through management or for geographic information systems (GIS) is an- through the use of therapeutic approaches. Fur- other goal. In this context, specimen-based data ther, accurate morphological characterization of HOBERG—PARASITE COLLECTIONS AND BIODIVERSITY 127 parasites and phylogenetic frameworks are crit- particularly among the Platyhelminthes (e.g., ical for the reliability of any capabilities for mo- Brooks et al., 1985; Brooks and McLennan, lecular diagnostics and comparative genomics. 1993; Littlewood and Bray, 2001). Indeed, there In a broader context, parasites are critically im- has been a largely unrecognized revolution in portant as 1) ecological and trophic indicators; parasite systematics, beginning only 25 yr ago 2) historical indicators of phylogeny, ecology, with the publication of the first phylogenetic and biogeography; 3) contemporary and histor- study of any group of parasites by D. R. Brooks ical probes for biodiversity research; and 4) (1977), that has resulted in a deep phylogenetic model systems for exploring a range of theoret- understanding within some taxa. For example, a ical issues in evolutionary biology, and ecosys- cumulative and hierarchical base of knowledge tem and community structure using a compara- about tapeworm phylogeny has blossomed in the tive approach (Brooks and Hoberg, 2000). Sim- 5 yr since the 2nd International Workshop for ply, in the absence of systematics, parasitology, Tapeworm Systematics (Hoberg, Gardner, et al., and biological science in general, could not pro- 1997), which resulted in 1999 in a series of pa- ceed. pers in Systematic Parasitology, Vol. 42. The Although the need for expanding knowledge Workshop and these studies served as a foun- and the inventory of global biodiversity is wide- dation for the development and evaluation of a ly recognized, our abilities to realize this goal series of testable hypotheses for higher level re- are hampered by the ‘‘taxonomic impedi- lationships (Hoberg, Mariaux, et al., 1997; Jus- ment’’—basically a worldwide shortage of crit- tine, 1998; Mariaux, 1998; Caira et al., 1999; ical expertise in systematics (SA 2000, 1994; Olson and Caira, 1999; Caira et al., 2001) that Hoagland, 1996; Brooks and Hoberg, 2000). For have culminated in recent attempts to integrate example, it has been noted that within the USDA molecular and morphological databases and inadequate support of taxonomic and systemat- analyses based on total evidence (e.g., Hoberg, ics expertise has had an adverse impact on mis- Mariaux, et al., 2001; Olson et al., 2001). sion-oriented research linked to biodiversity Through these studies, many of which have ex- (PCAST, 1998). Capabilities for parasite system- tended to the level of resolution among families, atics are not broadly represented among other genera, and species, the tapeworms must now be federal agencies where such would be appropri- considered among the best resolved of any ate, and they do not represent core programs ex- group of organisms, free-living or parasitic. cept at a few academic institutions in North Surprisingly, this basic information on the ge- America. nealogical diversity of the tapeworms and par- Comparative studies using phylogenetic infor- allel data for other parasitic flatworms, based on mation have rapidly expanded in the past de- both morphological and molecular databases, are cade. A growing number of applied research not yet widely represented in the Tree of Life programs in parasitology have recognized this (TOL) (Morell, 1996; Pennisi, 2001). Inclusion and are using phylogenetic information in their in the TOL should offer parasite systematists a studies. Although the taxonomic impediment re- diverse audience for our contributions toward mains apparent, there has been attention to de- understanding the history of life, the universe, velopment of phylogenies for groups that in- and everything. Parasitologists must take the op- clude important helminth parasites of humans portunity to fully engage the broader community and livestock (e.g., for ascaridoid nematodes, and communicate the depth and scope of the Nadler and Hudspeth, 2000; trichostrongyloid phylogenetically driven research programs that nematodes, Hoberg and Lichtenfels, 1994; Gouy¨ emanate from the discipline. Collectively, as we de Bellocq et al., 2001; taeniid tapeworms, Hob- move toward a clearer resolution of relationships erg, Alkire, et al., 2001), and phylogenetic ap- for a diversity of parasitic taxa, we can begin to proaches have figured prominently in recent articulate and evaluate fundamental questions studies of the Apicomplexa (e.g., Barta, 1989; about the structure and history of the biosphere Carreno et al., 1998). (Brooks and McLennan, 1993; Hoberg, 1997a). Despite the challenges of the current environ- Notably, we enter the twenty-first century with ment, systematic parasitology has made substan- a robust phylogenetic hypothesis, at a minimum tial contributions in resolving the evolutionary to the family level, for all of the Neodermata, relationships among the major parasitic groups, and have begun to accumulate the molecular 128 COMPARATIVE PARASITOLOGY, 69(2), JULY 2002 data necessary to explore a rich and detailed his- toring (Hoberg, 1997b; Hoberg, Kocan, et al., tory for these taxa (see Littlewood and Bray, 2001; Pe´rez-Ponce de Leoń et al., 2000). These 2001). (For a listing of most published phylo- issues again emphasize the importance of col- genetic trees for parasitic helminths, see http:// lections that serve as the foundations for inven- brooksweb.zoo.utoronto.ca/notes.html.) tories of the world’s biota (Blackmore, 1996) and reinforce the significance of the develop- BIODIVERSITY AS A FOUNDATION ment of our specimens-based resources as pri- There is nothing more fundamental than a mary information systems for biodiversity. comprehensive understanding of parasite biodi- At a more fundamental level parasites are the versity, including accurate taxonomy and spe- integrative core of biodiversity survey and in- cies identity, evolutionary relationships, geo- ventory (Hoberg, 1997a). Parasites yield insights graphic distribution, and host associations into the origins and continuity of biota and the (Brooks and Hoberg, 2000). Parasites satisfy the historical, phylogenetic, ecological, biogeo- primary criteria for recognition of priority taxa graphic, and temporal connectivity across and to be included in survey and inventory within within ecosystems (the linkage of macro- and the GTI (Brooks and Hoberg, 2001). These cri- microevolutionary processes, and temporal and teria include 1) taxa that are intrinsically impor- geographic scale). Parasites are critical in de- tant to humans; 2) taxa that are intrinsically im- veloping a synoptic understanding of the history portant to ecosystems that humans want to pre- and structure of the biosphere. Substantial con- serve; 3) taxa that provide efficient means of tributions by parasitological research to biodi- learning something of importance; 4) taxa that versity inventories extend from the accretion of are geographically widespread; and 5) taxa that novel information from the standard surveys es- provide an opportunity for international net- tablished over the past 200 yr to sophisticated working. Parasites are admirably suited for in- research programs for systematics, ecology, bio- clusion in basic survey and inventory of other geography, and evolutionary biology, based on vertebrate and invertebrate taxa and collectively both organismal and molecular approaches provide substantially greater information than (Brooks and Hoberg, 2000). For example, see that derived from the study of free-living organ- the database for the inventory of all eukaryotic isms alone, while causing substantial socioeco- p arasites of 940 species of vertebrates living in nomic impacts on a global scale (Hoberg, 1997a, the Area de Conservacion Guanacaste, Costa b). Rica (http://brooksweb.zoo.utoronto.ca/notes. Incomplete documentation of the biodiversity html), and the developing databases for the Ber- of the global parasite fauna, from the level of ingian Coevolution Project being assembled to species to populations, continues to hamper the examine the complex history of the northern development of relevant control measures, and continents (http://arctos.museum.uaf.edu:8080/ parasites continue to affect science and society projects/0051/index.shtml). significantly. Accurate survey and inventory is critical for recognizing the potential emergence CHALLENGE FOR THE FUTURE: PARASITE of pathogens, and interactions between the par- SYSTEMATICS AND COLLECTIONS IN A asite faunas circulating in domestic and sylvatic CHANGING WORLD hosts and at the interface of agricultural or man- Systematics and our specimens-based collec- aged and wild ecosystems (Hoberg, 1997b; Hob- tions are the foundation of all that has been ac- erg et al., 1999; Brooks and Hoberg, 2000). complished in parasitology and have resolved a Globalization of economies indicates that nar- substantial number of real-world problems in row regional approaches to documentation of di- human and animal health. Comparative phylo- versity for parasites and pathogens are no longer genetic approaches, in their infancy only 20 yr supportable or viable. Translocation and intro- ago, have now become the standard (Brooks and duction of parasites continue as factors deter- Hoberg, 2000). Yet, with this impressive array mining the continental and global distribution of of contributions and tools, and growing interest pathogens and further emphasize the importance in parasitology at all levels of society (e.g., Zim- of systematics and taxonomy in providing a pre- mer, 2000), our future does not seem assured. dictive framework for identification, documen- The parasitology community, often at the in- tation, and subsequent surveillance and moni- stitutional level, has undervalued museum col- HOBERG—PARASITE COLLECTIONS AND BIODIVERSITY 129 lections, although collections are increasingly this emphasizes the urgent need for scientists, important in the context of burgeoning programs societies, and institutions to seek mandates for for biodiversity survey and inventory and hold support of basic systematics, for support of mu- irreplaceable baseline and archival knowledge of seums, and for initiation of processes that will the biosphere. It appears to be a general as- strengthen and build new avenues for the dis- sumption that these resources will simply con- semination and application of information on- tinue to exist and provide essential services in line. Concurrently systematists must embrace a the absence of any community-level support or transition from being collectors of specimens to support from the stakeholders who are depen- functioning as curators of information, particu- dent on this fragile foundation. However, con- larly information that is broadly relevant to sci- sider the significance of the USNPC in context. ence and society (Brooks and Hoberg, 2000). For the ARS and American agriculture, the col- Parasite taxonomists must strive for a cultural lection makes possible a multifaceted research change and recognize the need to present a program contributing to our understanding of the stronger case to those who use systematics in- diversity and significance of helminth and pro- formation but do not understand the intrinsic tozoan parasites and pathogens in ruminants, significance of the information on which they equines, and wildlife species. For the United are dependent. A duality is evident—at once a States and North America, the collection and challenge for all of parasitology to participate other dispersed museum and institutional re- and at once an opportunity to build a cooperative sources make parasitological research possible. and synergistic framework for promoting contri- Concurrent with diminishing resources for butions to a larger infrastructure for global bio- collections is the realization that the value of diversity. Parasitology can reestablish and main- systematics has been overlooked especially in tain relevancy in a dynamic world. parasitology. Except perhaps in the context of a limited number of National Science Foundation ACKNOWLEDGMENTS (NSF) Partnerships for Enhancing Expertise in My career in systematics has been the con- Taxonomy (PEET), projects that support system- sequence of working with powerful and insight- atics of the Eucestoda, Nematoda, and Apicom- ful mentors, particularly Robert Rausch and plexa, the number of systematists continues to Gerald Schmidt, whose seminal studies provided decrease, making training opportunities rare in a remarkable view of the world. Our current ma- North America. Thus, the current trend for in- jor collections were developed and expanded clusion of parasites in projects supported by the through the vision of J. Ralph Lichtenfels at the Division of Environmental Biology through the U.S. National Parasite Collection and Mary Biotic Survey and Inventory Program (BS&I) of Hanson Pritchard at the Harold W. Manter Lab- the NSF is highly laudable and is indicative of oratory. Ideas presented in this paper were artic- recognition of parasites and parasitism as com- ulated over the past several years during collab- ponents of biocomplexity. Despite this recogni- orations with Daniel Brooks at the University of tion by a broader community, neither the BS&I Toronto and Douglas Causey at the Museum of nor PEET have been drivers of the cultural Comparative Zoology, Harvard University. I change that is clearly necessary in the academic also appreciate the insights gained from conver- sector. As has been noted by Brooks and Hoberg sations with Gerardo Pe´rez-Ponce de Leoń and (2001), saving biodiversity and promoting hu- Virginia Leoń-Regagnon at the Instituto de Hel- man socio-economic development is a complex mintologia, Universidad Nacional Autonoma de problem requiring networks of people and of re- Mexico, Mexico City. Additionally, my col- search programs. Networks require common lan- leagues at the USNPC, Benjamin Rosenthal and guage and discourse, as well as collaborative de- J. Ralph Lichtenfels, and Kurt Galbreath con- velopment of theory and research capacity. Fully tributed to the development of this paper. trained modern systematists are the masters of a LITERATURE CITED language powerful enough to facilitate such necessary discourse. Barta, J. R. 1989. 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