Viewpoint

The Dark Side of TaxonomicSu�ciency (TS)DON MAURERDepartment of Biological Sciences, California State University at Long Beach, Long Beach, California 90840, USA

Benthic invertebrates possess a number of characteristicswhich makes them attractive tools for monitoring pollu-tion. This proposition has been expressed by many for along time. Many indices, coe�cients and analytic ap-proaches have been used to measure the response of ma-rine benthic invertebrates to contaminants. Moreover,benthic invertebrates are frequently used as `bioindica-tors'. Accurate taxonomic analysis must be available forthe use of indicator species to be e�ective (Grant et al.,1995). The Capitella capitata sibling species complex is anexample of how new information emerges about di�erentecophysiological responses of `siblings', and the exclusionof rare species has seriously violated results from generalecological observations and theory, leading to unaccept-able losses of ecological information; the emerging prac-tice of taxononmic su�ciency in monitoring marinebenthic populations exacerbates such concerns. Ó 2000Elsevier Science Ltd. All rights reserved.

Keywords: taxonomic su�ciency; systematics; monitor-ing.

Taxonomic Su�ciency (TS)

Taxonomic su�ciency (TS) involves identifying taxa tothe highest category possible (genus, family, order etc.)without losing statistically signi®cant vigour in assessingpollution impacts. Money accrued from reduced taxo-nomic services often is allocated to other elements of amonitoring program. This is a cost-bene®t exercisewhich has considerable appeal as re¯ected by a numberof recent studies. Another argument for TS maintainsthat there are simply not enough people around who cancon®dently and correctly identify a broad spectrum ofinvertebrates (anonymous reviewer). According to thisview it is more useful, in the long run, to obtain someconsistent information on taxa (e.g., family-level iden-ti®cations and relative abundance) than depend solelyon measures such as biomass or production.

TS also receives additional support when workingwith the meiofauna which are even more di�cult toidentify. Application of TS to harpacticoid copepodsand nematodes makes these groups more useful forpollution assessment by non-specialists than ever before.The practice of TS in those marine habitats which areunder-sampled and poorly known (deep-sea, tropics)also ®nds favour. Regardless of this, the main supportfor TS resides in the economic arguments, but at whatcost? As someone who has collected over 2000 samplesand has helped process (picking, sorting, identifying,counting, weighing) a large number of these, I am awareof the time spent in identifying taxa to the species level.Moreover, I have occasionally participated in specialbenthic studies that have not always enumerated oridenti®ed all individuals and taxa present. While rec-ognizing that opportunities for cost savings in long-termmonitoring deserve consideration, experimentation, andpossible implementation, there are a number of impli-cations associated with TS. These should be consideredand assessed prior to implementing TS as a regularprotocol in monitoring. While saving dollar resourcesthrough TS, we lose currency of another kind. Inthis account I address the `dark side' of taxonomicsu�ciency.

Biodiversity and Taxonomic Illiteracy

Biodiversity is an environmental buzz word for thenineties, and well into the next millennium. Biodiversitygenerally refers to the number of living plants and ani-mals per habitat or the total number of living organismsper ecosystem. Marine biodiversity was featured in abook (Ormond et al., 1997) and Caillet (1997) andothers have described the status of marine biodiversityfor central California. The same is true for otherregions.

Expanding human populations and associated activ-ities have greatly reduced biodiversity. Coincidentalwith this, is dwindling support for training taxono-mists and systematists, and funding for collecting and

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curating the biota. Elliott (1993) decried the low em-phasis of taxonomy in university training in mostcountries. He attributed this to the need or desire tocover the expanding breadth of biological topics duringa biological education, resulting in diminishing classicalskills in taxonomy. Moreover, as retirements occur,faculty positions formerly committed to broad taxo-nomic groups with a classical approach are either notreplaced or are replaced by other sub-disciplines. Be-cause of present funding and award practices, newfaculty positions in taxonomy often require that can-didates use cellular and molecular techniques. Taxon-omy based mainly on morphological di�erentiation isconsidered by many to be an inferior science or noscience at all. This has resulted in a taxonomic inver-sion with the rate of species extinction expanding,and resources and positions for taxonomic specialistsdecreasing.

Based on its size and locations, it is not surprising thatthe deep-sea is considered an under-sampled habitat.What is surprising is that for even familar nearshorehabitats biodiversity is remarkably undescribed. An in-formal compilation from selected invertebrate taxono-mists revealed that large numbers of common speciesfrom fairly accessible habitats (shallow tropical lagoons,coral reefs, rocky shores) have no formal names (But-man and Carlton, 1995; CBDMS, 1995). Almost one-third of the polychaetes from Georges Bank remainundescribed. Over 50% of the benthic species collectedin the most recent (1977±1989) large-scale surveys of thedeep benthos from the Southern California Bight (SCB)were undescribed taxa (Thompson et al., 1993). Thesesituations prevail in areas surrounded by private andpublic institutions committed to studying the ocean.There are too few taxonomists to handle the task athand, a condition which worsens with each generationand is the result of fewer teachers of taxonomy (Schel-tema, 1996). Our lack of knowledge about soft-bottominvertebrates is due mainly to the paucity of taxonomistsactively working on virtually the entire list of inverte-brate phyla (Caillet, 1997). To paraphrase Sir WinstonChurchill: Never in the annals of biological history haveso few with so little, done so much, for so many. Boero(1996) went so far as to exclaim that taxonomists havebecome endangered species. Accordingly, it is di�cult toreconcile the plaudits of TS practices with the expandingneed to document biodiversity globally. I provide achorus to Feldmann and Manning (1992) who earlierextolled the contradiction between the crisis in system-atic biology and the `Age of Biodiversity'. Pimm andLawton (1998) stated that `...we cannot a�ord the lux-ury of ignoring those most basic of biological skills-taxonomy and the knowledge of which species livewhere'. Elliott (1993) stated that (taxonomic) `problemsare particularly galling in the age of Earth Summitswhich discuss biodiversity...' TS, as presently emergingin monitoring programs, does not advance the need formore and better trained taxonomists.

Disciplinary Disparity

Is the money saved from bargain basement biologymatched with similar economies, and commensuratelywith practices in other marine disciplines? Chemicaloceanographers are now isolating isomeres and cong-eners of organic contaminants. They no longer rely onlitmus paper and Gilbert Chemistry sets to analyse so-lutions at concentrations of parts per billion or trillion.Coastal oceanographers do not use three-arm compassesfor triangulation on land forms, but rely on GPS forprecise navigation. Increased reliance on remote sensing(TOPEX/Poseidon satellite) and development of a va-riety of tools based on acoustic and visual band signals,together with advances in chemical protocols and in-strumentation likewise contrast with minimalist prac-tices in taxonomy. If TS is widely applied as a standardmonitoring practice, the following model emerges: Therewould be serious disparity in competency between bi-ologists studying the living targets of pollution havingless training and rigour than that employed by physicaland chemical oceanographers measuring the agents ofpollution (Carriker, 1976). It costs money to trainphysical and chemical oceanographers, and to conductthe research and development necessary to produce newtechniques and instruments. Accordingly, it will requirea complementary investment in time and money to traina cadre of marine biologists to pursue taxonomic needsand interests to keep apace of their oceanographiccolleagues.

Storage and Retrieval

Carriker (1976) recognized another concern about therole of systematics in assessing pollution e�ects. Accu-rate identi®cation is necessary to unlock the storage andretrieval system of scienti®c information. The speciesname is the doorway to its literary pedigree. Speciesnames make information accessible and useful viapublished aspects of organismic biology. With all duerespect to cladistics, the Linnean system of biologicalnomenclature, internationally applied by biologists sincethe eighteenth century, provides an operational methodof arranging taxa in ways that re¯ect their phylogeneticrelationships. With the advent of large, long-termmonitoring studies, producing 100 000s of biologicaldata bits, new coding systems were developed to adaptthe Linnean system to modern methods of data storageand retrieval. However, when one searches the interna-tional literature for Capitella capitata, one does not typein a code but rather the actual taxon. In fact, emphasison higher taxonomic levels (genus and family, Capitellaand Capitellidae) yield far less discriminating informa-tion from a storage and retrieval system than consider-ing the species level. Moreover, even conventionalstorage and retrieval systems based on Linnean classi-®cation must still deal with the thorny problem

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presented by so-called sibling species hiding under thepatronymic, C. capitata.

Summary and Conclusion

In future practices of marine monitoring, TS will ex-acerbate some of the issues presented here. Although notby design, TS results in a rationale to delay commitmentto training a cadre of taxonomists to handle the prob-lems of the new millennium, is inconsistent with chal-lenges facing biologists as they hasten to deal with thereduction of global diversity, and facilitates compro-mising the quality of taxonomic services. Cailliet (1997)encouraged more studies on the basic taxonomy ofmarine organisms prior to managing them e�ectively. Intheir summary and prospectus for future research in theSCB Thompson et al. (1993) identi®ed the virtual ab-sence of training as a problem reducing entry of youngscientists to the ®eld of systematic zoology.

For economic and other reasons TS will continue tobe employed in marine monitoring. I hope this trend willnot coincidentally preclude a revitalized commitment todevelop a new group of taxonomically trained marinebiologists. My experience with students mirrors that ofEllis (1988). Initial sorting of macrobenthos to highercategories (phylum, class, order) is not demanding. Ellis(1988) described how ®nal term undergraduates per-formed speci®c identi®cations with a high degree ofaccuracy within well-de®ned and well-known taxonomicgroups, assuming some degree of quality control by anexperienced supervisor. However, consistent and accu-rate identi®cation of taxa to species requires consider-able training, and years of experience (Carriker, 1976;Snelgrove and Grassle, 1995). The care and nurturing oftaxonomic specialists is a necessary step to resolve thisproblem. This process will require a reallocation offunding priorities to move students through advanceddegree programs in preparation for their professionalcareers.

In the United States funding is made available fortraining marine engineers and scientists to develop newtechniques and instrumentation for ocean science (Ro-yer, 1999). A major deterrant facing young biologistsinterested in pursuing a career in taxonomy or syste-matics is the poor prospect of employment (Carriker ±pers. comm.). This problem represents a real barrierdiscouraging entry to the ®eld. An anonymous reviewerof this paper pointed out that as vital as the funding fortraining is, training becomes dead-ended unless there arejob opportunities for the trained. While integratingcellular and molecular techniques in their training, thereshould be no compromise with mastering conventionalpractices in taxonomy based on morphology, ecologyand behaviour. Scheltema (1996) cited an encouraginginitiative in the United States (NSF ± Partnership forEnhancing Expertise in Taxonomy). Cailliet (1997) citeda number of workshops and initiatives to address thisproblem and outlined (pers. comm.) plans for creation

of an International Marine Biodiversity Institute(IMBI); itsÕ mission statement includes a strong com-mitment for training in taxonomy of marine organisms.While preparing this account, I received an e-mail fromDr. Jack Pearce via Dr. David Dow describing a newprogram by the British Natural History Museum. TheMuseum has established an Identi®cation Quali®cation(IdQ) scheme with the aim of improving standards inenvironmental work in the United Kingdom by award-ing certi®cates of competence in animal and plantidenti®cation to biologists and ecologists. The need forquality control in the ®eld of ecological consultancy waswidely recognized and IdQ addresses biological identi-®cation skills.

A regional initiative actively responding to thisproblem involves the Southern California Association ofMarine Invertebrate Taxonomists (SCAMIT). SCAMITconsists of marine scientists from industry, academia,and public agencies who work daily with marine inver-tebrates. They conduct regular meetings exchangingspecimens from their respective study areas, collectivelyexamining them under microscopes, and resolving tax-onomic problems and usage within the SCB. In addi-tion, they prepare taxonomic keys, conduct workshopswith invited specialists, and communicate results ofmeetings, workshops and taxonomic usage in a regularnewsletter. SCAMIT is a constructive alternative to TS,and would be a complementary e�ort to the identi®ca-tion centres recommended by Ellis (1986) and the IdQ.

An important outcome of the US Marine MineralsManagement Service (MMS) Outer Continental Shelf(OCS) Program has been the preparation of severaltaxonomic guides for the Northern Gulf of Mexico anda series of taxonomic atlasÕ on the benthic fauna of theSanta Barbara Channel. The Santa Barbara series hasbeen extremely useful for teaching classes on marineorganisms in California. I encourage MMS to continueproducing these valuable taxonomic guides as still an-other way to mitigate taxonomic illiteracy.

The program for the Cape Cod Bay Census con-ducted at the Marine Biological Laboratory, WoodsHole, Massachusetts in the late sixties through theeighties, could be re-established for a ®ve year period.Under the aegis of Dr. Melbourne Carriker that pro-gram trained and provided experience for a number ofthe marine taxonomists in the United States who pres-ently or shortly face retirement. Coupling cellular andmolecular techniques with classical approaches wouldmake such a program more acceptable to academic in-stitutions. In her acceptance speech of ASLOÕs LifetimeAchievement Award, Dr. Ruth Patrick stated: `For ex-ample, they (some consulting ®rms) will only identifyorganisms to the family or genus level. Anyone workingin this ®eld, be it terrestrial or in the water, knows that itis the species or subspecies that indicates the presence ofpollution'. Let the response to the `dark side' of taxo-nomic su�ciency provide the `force' to address theseproblems.

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Several people have been very helpful and sup-portive in preparing this account. I am pleased torecognize my colleague Dr. Don Reish who reviewed adraft and provided a number of suggestions and ad-ditional references. Dr. Melbourne Carriker also re-viewed a draft lending his extensive experience andinterest in the topic. Dr. Gregory Cailliet providedsome documents about a number of initiatives con-cerning problems of biodiversity, here and abroad. Dr.Jack Pearce and three anonymous reviewers providedthoughtful comments and suggestions to balance myobvious bias.

Boero, F. (1996) Episodic events: their relevance to ecology andevolution. Marine Ecology 17, 237±250.

Butman, C. A. and Carlton, J. T. (1995) Marine biological diversi-ty:some important issues, opportunities and critical needs. In USNational Report to International Union of Geodesy 1991±1994, ed.R. Pielke.

Cailliet, G. M. (1997) What do we really know about marinebiodiversity in central California? In California and the WorldOceanÕ97. Proceedings of Conference, American Association of CivilEngineers, San Diego, California, pp. 487±506.

Carriker, M. (1976) The crucial role of systematics in assessingpollution e�ects on the biological utilization of estuaries. InEstuarine Pollution Control Assessment. Proceedings of Conference,pp. 487±506. USEPA O�ce of Water Planning and Standards.

Committee on Biological Diversity in Marine Systems (CBDMS)(1995) Understanding marine biodiversity: a research agenda forthe nation. In Ocean Studeies Board, National Research Council,pp. 1±114. National Academy Press, Washington, DC.

Elliott, M. (1993) The quality of macrobiological data. MarinePollution Bulletin 26, 2±3.

Ellis, D. V. (1986) Identi®cation centres. Marine Pollution Bulletin 17,479±480.

Ellis, D. V. (1988) Quality control of biological surveys. MarinePollution Bulletin 19, 506±512.

Feldmann, R. M. and Manning, R. B. (1992) Crisis in systematicbiology in the `Age of Biodiversity'. Journal of Paleontology 66,157±158.

Grant, J., Hatcher, A., Scott, D. B., Pocklington, P., Schafer, C. T. andWinters, G. V. (1995) A multidisciplinary approach to evaluatingimpacts of shell®sh aquaculture on benthic communities. Estuaries18, 124±144.

Ormond, R. F. G., Gage, J. D. and Angel, M. V. (eds.) (1997) MarineBiodiversity: Patterns and Processes, pp. 1±350. Cambridge Uni-versity Press, Cambridge, MA.

Pimm, S. L. and Lawton, J. H. (1998) Planning for biodiversity.Science 279, 2068±2069.

Royer, T. (1999) Exciting, unsettling changes in store for physicaloceanography. EOS 80: 394±395.

Scheltema, R. S. (1996) Describing diversity: Too many new species,too few taxonomists. Oceanus 39, 16±18.

Snelgrove, P. V. R. and Grassle, J. F. (1995) The deep sea: desert andrainforest: debunking the desert analogy. Oceanus 38, 25±29.

Thompson, B., Dixon, J., Schroeter, S. and Reish, D. J. (1993) BenthicInvertebrates. In Ecology of the Southern California Bight:A Synthesis and Interpretation, eds. M. D. Dailey, D. J. Reish andJ. W. Anderson, pp. 1±926. University of California Press, Berkeley,CA.

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