Systematic collection data in North American invertebrate conservation and monitoring programmes

Authors


P. Z. Goldstein, Division of Insects, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA (fax +312/665 7754; e-mail pgoldstein@fmnh.org).

Summary

  • 1Although likely to yield less copious collections than their tropical counterparts, temperate inventories focused on invertebrates require individuals not only trained to deal with a wide array of taxa but also versed in the techniques used to process and archive specimens.
  • 2Due in part to the prevalence of physically intensive conservation management practices (e.g. prescribed burning) or resource management practices (e.g. selective logging), and in part to a better understanding of temperate invertebrate faunas relative to their tropical counterparts, temperate conservationists bear an inescapable responsibility for monitoring the effects of such practices on species assemblages of conservation concern.
  • 3Counterintuitively, North American conservation programmes, particularly those involving monitoring, run the risk of turning away from concerns for invertebrate assemblages, despite their being relatively well-understood, recognized as powerful conservation tools or indicators, and in some areas the demonstrable majority of the most threatened of animal species.
  • 4Synthesis and applications. To prevent further erosion or underuse of invertebrate monitoring and inventories, there is a recognizable need for professional space in the North American conservation community for parataxonomist-like individuals. These should be trained to deal with both the required field procedures and the standards and practices associated with maintaining systematic voucher and reference collections in natural history museums and herbaria. In particular, the relevance of discovery-orientated biological inventories and collections-based systematic research to the design and implementation of adequate natural areas management and monitoring remains underemphasized and underappreciated by some allegedly science-based conservation programmes.

Introduction

The importance of biosystematic data, in the form of taxonomic revision, phylogenetic analyses and natural history collections, to conservation biology has been well articulated for over a decade. Many published discussions have surrounded the various arenas wherein the kind of understanding that comes from systematics and collection-based research informs conservation decisions. Biological collections and systematic theory form the basis for the identification of species boundaries and management units, the inference of historical distributions, and the arrangement of comparative information garnered from biotic inventories. In regions with hyperdiverse faunas, and for ‘mega-diverse’ groups comprising many invertebrate taxa, numerous challenges confront both scientists and conservation decision-makers. Most broadly, these are (i) the documentation of species-level information and (ii) the interpretation of that information. Although the overwhelming majority of estimated species diversity remains undescribed, some of the most basic standards and practices of retaining specimen-based information do not always realize a key role in bio-inventories undertaken for conservation assessments. Limited expertise coupled with the long process of specimen-based analyses and systematic revisions relative to the immediate need for protecting vast natural areas usually force the conservation decision-making process to proceed with an incomplete understanding of biotic uniqueness and diversity. Even worse, conservation agendas in regions with comparatively well-understood biotas do not always make the most of such understanding even where it exists, particularly with respect to invertebrates.

Basset et al. (2004) describe a number of factors driving the apparent need for parataxonomists as gatherers of primary data in the form of specimens associated with tropical bio-inventory projects: large-scale extinction coupled with our ignorance of the vast majority of invertebrate species engender the pressing need for bio-inventories in the face of limited expertise and inevitable loss of primary habitat. Invertebrate zoologists deal with taxa orders of magnitude more speciose than vertebrate zoologists, and the need for field workers with some measure of taxonomic training as well as the collection, preparation, sorting, rudimentary identification and archiving of specimens is by no means confined to the tropics. The species richness of invertebrate faunas, although generally smaller in temperate than in tropical zones for most taxa, none the less presents a burdensome enough task to overwhelm casual inventorists. The North American invertebrate fauna, for example, has been far better described than that of the neotropics (or most probably any tropical region), but our understanding is far from complete, and our nomenclature far from stable, even for popular groups such as butterflies. As is likely to remain the case, there exist important and understudied North American areas of high diversity and endemism (e.g. the Smoky Mountains, the Ozarks, southern cane brakes), innumerable known but as yet undescribed species (some of which are formally protected under one or more state endangered species acts) and, of course, a predominance of species that cannot readily be identified except by experts. Despite these observations, we have a respectable enough understanding of the distributions, habitat associations and life-history requirements of some North American invertebrate groups to make some informed decisions about relative endangerment, protection, monitoring and even recovery strategies. With this understanding has come legislation, relatively sophisticated in some cases, associated with the conservation of threatened natural areas, species and even populations.

As a consequence of the intense development and resource extraction pressure on native landscapes, and the vagaries of both federal and state endangered species legislation, it has become imperative to document the occurrence of threatened species assemblages as thoroughly and reliably as possible. At the same time, with increased knowledge of threatened species’ requirements comes enhanced responsibility to make the most of that knowledge. A central problem is infrastructural, and parallels the situation among tropical researchers. Many academic scientists rarely have the luxury of focusing on conservation questions, a situation compounded by the fact that many land managers lack the expertise to address invertebrate concerns in management planning and implementation. As such, there is a pressing need for people trained in systematics and taxonomy who may exercise that training in an applied context as well as in academia, where training in systematics has suffered considerably anyway. The challenge thus remains of addressing this dilemma effectively, but in such a way that will not dilute or hamper future systematic and bio-inventory studies. Basset et al. (2004) suggest parataxonomy as a remedy in the form of those who may function full-time in generating and preparing collections for study by experts, thus enabling both the completion of inventories and goals of systematics. To the extent bio-inventories are conducted on a regional basis, this conclusion seems inescapable, but nevertheless demands careful revisitation.

Facing vastly understudied taxonomic groups, particularly invertebrates, the notion and neologism of parataxonomy was erected to bridge the gap between the mountains of raw data in the form of unprepared, unsorted specimens and the peaks of understanding that follow from their arrangement and study. In the last decade there has been an upsurge in the recognition of invertebrates as critical to conservation endeavours in the contexts of inventories, management plans and policies for listing and protecting endangered species. But, ironically, there remains an additional gap in the understanding of that importance among many North American conservation agendas, despite having to deal with less diverse biotas than tropical programmes. It has been my contention that failing to anchor our conservation decisions and monitoring criteria in specimen-based data carries considerable risk and is likely to jeopardize conservation projects in the long run. Following a brief review of the critical importance of proper vouchering, collections, taxonomy and interpretation of systematic data, I argue, first, that despite a less diverse fauna in the raw sense, the effort necessary to train conservationists in the basic techniques of collecting and preparation is no less considerable in the temperates than in the tropics; and secondly, that there exists a growing need for parataxonomist-like professionals in North America (and other regions) paralleling the growing sophistication in our understanding of temperate invertebrate conservation issues. I differ from suggestions that such careers should suffice as ends in themselves, however. I follow a long line of previous authors in arguing that a successful conservation programme will rely fundamentally on systematists and collections-based research, and in urging caution against an overreliance on superficial taxonomy (for key references see Vane-Wright, Humphries & Williams 1991; Nixon & Wheeler 1992; Wheeler 1995; Cracraft 1997; Wheeler & Cracraft 1997; Funk & Richardson 2002).

Scientific collections and vouchering in taxic and threatened species inventories

There is more than enough discussion, if not controversy, on how to interpret species richness and diversity data for the purposes of conservation evaluation to address in this essay. Likewise, the central importance of scientifically sound species delineations to conservation efforts has been ably reviewed elsewhere (Claridge et al. 1997) and I will not belabour that issue here. Suffice it to say that a poor understanding of the relevance of diversity measures and the basis of species circumscriptions can have disastrous consequences for conservation, restoration and reintroduction programmes. The focus of this essay is the retention of that information, whatever its purpose, in a specimen-based form that can be revised and revisited when necessary; in other words, precisely the goals that the practice of phylogenetic systematics is already set up to achieve. Before embarking on a rationale for enhancing the kind of taxonomic expertise necessary to steward and interpret collections-based data, it must first be made clear that biotic inventories are conducted for a variety of purposes and to address a range of questions. That range includes broad primary research in systematics, natural history and biogeography as well as targeted issues of conservation evaluation such as documentation of threatened species assemblages and baseline data for monitoring programmes. The business of conducting inventories of invertebrates, whether for purposes of conservation evaluation or simply the gathering of scientific data, relies fundamentally on the standards and practices of preparation and vouchering, and ultimately on a retrievable database of biological information explicitly tied to specimens, not simply culled from informal sight records or nomenclaturally obsolete lists. Inventories of invertebrates in particular simply cannot be conducted without systematic collections of specimens and people trained to use and study them.

As the repositories for specimens, the actual results of bio-inventories, natural history museums and university collections represent far more than taxonomic libraries and identification guides (Alberch 1993; Mehrhoff 1997): such collections hold primary type specimens that serve as standards and name bearers on which all taxonomic revisions and nomenclatural use rely. Further, and most relevant to conservation endeavours, such institutions are the repositories for historical specimen-based information on rare species occurrences, serving to illuminate historical distributions, identify faunal changes, declines and range contractions (and thereby possible threats to species), document life histories, and provide baseline data for monitoring programmes. Collections often provide the clues to discovering unknown faunas.

As such, proper specimen vouchering is central to conservation and monitoring strategies from both scientific and legislative perspectives. Taxonomic revision, the discovery of cryptic species and the invasion of exotic species may each confound casual monitoring protocols. Of particular concern are cases where putative targets for monitoring are not determined to species, but simply lumped into higher taxa; worse still are cases where specimens are discarded or improperly or irretrievably vouchered. Insufficient as these practices are, they are not uncommon in active conservation programmes. I believe this is because there exist few generalized frameworks for incorporating collections-based work, neo-parataxonomy if you will, to the ongoing business of most professional conservation programmes. The scientific incentive for non-profit conservation organizations to adhere to the standards and practices that form the ongoing focus of groups such as the Entomology Collections Network remains largely unrecognized.

Strangely, we seem to face the counterintuitive situation in which the most extensive and available collection-based data are underutilized in regions that do not even support the highest species diversity. An important question is whether the comparatively thorough degree to which the North American biota has been described has enabled a complacency of sorts whereby the importance of proper collecting is poorly understood as a scientific standard among recent generations of conservationists. This complacency is evident both in how we view the taxonomic stability of North American insects, for example butterflies, and in the decoupling of species-based information from the evaluation of conservation management and monitoring success. In North America the recent proliferation of anti-collecting movements within such spheres of popular entomology as butterfly watching, and even within the ranks of conservationists, has raised a dangerous spectre: the dissemination of distributional information of rare species without vouchered specimens or photographs. As inventories of rare insect species are being undertaken with increasing frequency, it becomes imperative that such efforts consist of more than sight records, which are notoriously prone to error and exaggeration. In some cases, the dissemination of rare species occurrence data for which no proof exists in the form of a voucher specimen deposited in a scientific collection may lead to erroneous conclusions of a species’ or population's vigour (Goldstein 2001). This is particularly so for cryptic species that cannot be identified without careful dissection. Notably, this phenomenon is not necessarily less of a problem for vertebrate biologists, particularly molecular systematists who, proscribed from collecting in heavily restricted regions, are often confronted with a choice between using a voucher tissue consisting of a feather, fur or scat sample versus using nothing at all.

From a legal standpoint, specimen vouchers of threatened species may be the only concrete proof that these species exist in threatened natural areas when the fate of such areas lies in the judiciary system. One may point to numerous cases where the documentation of threatened species occurrences was challenged, and at least as many where the results of inadequate inventories, such as those conducted by hired consultants at the wrong time of the year to observed threatened species, were used to assert that those species did not in fact exist at the sites in question. A professional system of checks and balances is sorely needed in the North American conservation community, and the reliable retrieval of collection-based data occupies a mission-critical role to the enabling of that system.

Complacency with respect to the role of species monitoring in North America may also be evident in a variety of paradigms that, if misapplied, rely on abstractions such as ecosystem health, ecosystem processes, biological integrity, etc., to the exclusion of species-based information (Goldstein 1999). Such was an early criticism of ecosystem management in the broad sense, as it lent itself to sore misapplication. In their review of the genesis of parataxonomy and specifically its role in invertebrate programmes, Basset et al. (2004) allude to at least one early controversy surrounding its implementation in tropical invertebrate inventories, specifically the concern of systematists that parataxonomy would serve as a shill for the adoption of ‘taxonomic minimalism’ promoted by Beattie & Oliver (1994) and other authors. This latter argumentation is to be distinguished sharply from that of Basset et al. (2004). Indeed, as one who believes that biodiversity cannot be understood (or prioritized for conservation purposes) in the absence of systematics (Goldstein 1997), I and others (Brower 1995) expressed wariness that parataxonomy in the broad sense would replace a deeper understanding of organismal diversity if its development were not met with parallel efforts to boost professional training in the systematics of diverse groups. To state the issue in what is perhaps an oversimplified way, the characterization of native biodiversity for conservation purposes in terms of raw species numbers without systematic context runs the risk of overlooking unique, if species-poor, assemblages of organisms in favour of diverse assemblages composed of common, widespread or even exotic species. Of equal concern was the idea that the relevance of systematics to regionally geared bio-inventories would be overlooked by focusing exclusively on ecological questions surrounding species diversity and richness (Wheeler & Cracraft 1997). In North America, following the spread of various ecosystem management paradigms, the 1990s witnessed a movement away from detailed conservation focus on species assemblages paralleling a desire to avoid too-narrowly focused single species management. Ironically, bureaucratic and programmatic agendas appear to have perpetuated this shift by relying on ecological abstractions such as ecosystem health, biological integrity and processes to the exclusion of useful species-specific information (Goldstein 1999).

An example from North America may serve to illustrate the acute need for more widespread taxonomic expertise in temperate conservation and monitoring programmes. In the United States, Massachusetts and Florida are typically considered to have the strongest environmental legislation. Massachusetts currently lists more than 100 species of invertebrates as protected under the Massachusetts Endangered Species Act (MESA). But most of the listed invertebrates are difficult to inventory and identify without expert training. Despite a growing understanding of threatened invertebrates in Massachusetts, recent years have witnessed an ironic retreat from more in-depth inventory work in some areas in favour of what can only be considered a return to notions of single species management. In fact, areas that now support the highest concentrations of regionally rare and legally protected terrestrial animals in the region are threatened by conversion to anthropogenic landscapes in the name of ecological restoration. Some conservation programmes appear to have been driven by agendas at odds with available scientific data. In one case, there has been a public proposal to convert conservation lands to anthropogenic landscapes in order to accommodate the introduction of non-native prairie chickens. This notion was promoted as a ‘reintroduction’ of a non-native animal, a replacement of sorts for the extinct heath hen, to serve as an umbrella species whose persistence would signal the stability of native, extant regional rarities (Cokinos 2000). But none of the considerable research conducted on prairie chickens, heath hens or the sandplain grasslands, which may support prairie chickens but had little to do with appropriate heath hen habitat, supports this assertion, or indeed the assertion that such habitats were ever native in the first place (Motzkin & Foster 2002). In such cases, it appears that a reluctance to utilize available entomological expertise (in sharp contrast to the taxonomic impediment usually blamed for overlooking invertebrates) has obstructed efficient monitoring of threatened invertebrates, and enabled a ‘prairie envy’ of sorts in natural areas better served otherwise. As in the case of the early suggestions of taxonomic minimalism, taxonomic neglect is here being addressed with taxonomic abandonment and scientific ignorance.

Basset et al. (2004) do quite astutely point out that the monitoring of would-be ‘umbrella species’, ‘flagship species’, ‘keystone species’ or other alleged indicators or surrogates has not necessarily proven valuable in protecting whole assemblages. It is equally noteworthy that the usage of parataxonomy, if we are to judge by the content of Basset et al.'s (2004) paper, no longer necessarily connotes a dilution of the systematic endeavour. I would add that parataxonomists are undeniably useful in completing inventories (whatever their purpose). So long as it is recognized that bio-inventory data are comparable only to a point and that rough determinations made by parataxonomists should not form the crux of conservation priority decisions, these individuals play an important role in bio-inventories. Whether parataxonomy should be viewed as a fruitful field of study in and of itself remains open to question, as does the efficacy of regional all-taxon biotic inventories (ATBI) vs. a more global, taxon-based approach to cataloguing the Earth's biodiversity (Wheeler & Cracraft 1997; Goldstein 1997).

Basset et al. (2004) do not confine their comments to the utility of parataxonomists in completing inventories. Although such bio-inventory work appears to have comprised their primary professional purview to date, parataxonomists have also been involved in ecological experiments ( Novotny et al. 1999). The relevance of understanding invertebrate assemblages to conservation planning is highlighted here by contrasting those few areas in North America that support relatively well-characterized faunas with tropical areas only now undergoing bio-inventories for the first time. In many areas of North America, particularly the eastern sandplains and mid-western prairies, the parallel developments in understanding threatened invertebrate species and management techniques (prescribed burning, for example), has set the stage for a relatively advanced (if as yet unanswered) series of questions concerning the effects of particular management practices on suites of threatened species (Swengel 2001). Indeed, the possible impacts of certain management practices, particularly prescribed burning, on invertebrate populations has been highly controversial (Swengel 1996, 1998; Swengel & Swengel 2001; Panzer 2002). However, it is questionable whether the kind of active management undertaken by temperate land managers will be necessary or effective in more ecologically complex ecosystems such as tropical rain forests, and to the extent that this is the case, regular monitoring of invertebrate assemblages for the express purpose of evaluating management techniques in such areas may never be as crucial, feasible or indeed relevant a component of conservation planning. Herein lies the central arena in which parataxonomists or individuals with comparable training are likely to be used differently in temperate vs. tropical regions: as conductors of monitoring programmes vs. as enablers of basic scientific description. The distinction here is not an oversimplified characterization of ecosystems that are static vs. those more dynamic, as dynamic systems exist and provide management challenges in both temperate and tropical regions. Rather, I emphasize the distinction between temperate areas undergoing active or heavy wildlife management in the face of available relevant invertebrate data, and more pristine, unexplored tropical natural areas not necessarily undergoing such active management and where invertebrate data are much more limited. Clearly this distinction is irrelevant wherever actively managed or heavily harvested diverse tropical areas come to the fore. Here the distinction to be made is between tropical parataxonomists devoted to discovery and documentation, and tropical taxonomists devoted to monitoring. While practically these are not necessarily mutually exclusive, conceptually the distinction is useful.

The parataxonomist's future

Unfortunately, the sheer volume of specimen material typical of bio-inventory yields, particularly invertebrate-focused projects, necessitates far more post-collection laboratory work than might typically be imagined by non-specialists, and the need for some measure of training in collecting, preparing, sorting, rudimentary identification and maintenance of specimens is by no means confined to the tropics. In particular, the panoply of collecting and preparation techniques unique to each group of organisms is no less daunting than in the tropics regardless of the taxic richness of the inventory's yield. Each group carries unique needs both at the point of collection and in the course of long-term collection maintenance, and it is perhaps the preparation, curation and maintenance of such collections that represents the greatest potential training gap for would-be parataxonomists, however one defines the term.

Thus, regardless of the estimated reduction in species diversity and sample volume compared with tropical endeavours, bench time per specimen still presents a serious obstacle for temperate studies. It is no coincidence that few rapid assessment programmes target invertebrates, and that relatively few tropical bio-inventories target microlepidoptera or other preparation-intensive insect groups despite their diversity (but for counterexamples involving butterflies see Kremen 1994). As is always the case for specimen-related research, the question remains of who will do this work, regardless of whether it is conducted in an infrastructure-rich context of developed academic settings or in a developing tropical country.

The paradigm of parataxonomy, up to and including its explication by Basset et al. (2004), may be viewed as an extension of more traditional concepts of field assistantship in that it is viewed as a longer-term profession in and of itself, one requiring more detailed natural history training than a guide or porter, and one devoted to inventory- and monitoring-related tasks generally held to be outside the purview of primary researchers in systematics. It should be emphasized that these are not small tasks, and it is difficult to envision someone willing to devote the time and training hours necessary to become an expert without wanting to develop their skills further, whether as a community ecologist, systematist or conservationist. The more the role of the parataxonomist is expanded, the greater the possibility that he or she will (and should) wish to develop his or her skills beyond an assistance-capacity role. One of the issues raised by Janzen (1993) is whether it really behoves developing nations to whisk away their young scientists to training programmes in developed countries, possibly never to return. Conversely, it may not behove such individuals to impose a professional ceiling above which a parataxonomist may not rise. The central question from the parataxonomist's perspective is whether he or she simultaneously boosts inventory efficiency, facilitates the interpretation of data, perpetuates expertise through training and being trained, and retains some measure of professional stability. If this characterization is accurate, I observe that it strongly reflects the goals of many life-long naturalists.

The role of the parataxonomist, defined in the sense of Basset et al. (2004) as someone who works at the side of the systematist in an essentially technical capacity, must be seen as critical to extensive inventories regardless of their taxic depth. But at the root of any such endeavour lies the necessity of maintaining well-referenced collections that can aid future monitoring efforts in the event expertise does indeed become scarce. The building and maintenance of such collections, whether they are to be retained as synoptic collections to aid future researchers or as a primary scientific resource, adds a layer of training and expertise necessary to the parataxonomist, who must now double as ‘paracurator.’ Indeed, this has certainly been the case in the most developed bio-inventory/parataxonomy programmes, such as INBio, although realistically this notion must be viewed as a luxury in most tropical situations. Regardless, one cannot overemphasize the importance of proper techniques of development, vouchering, preparation, documentation and maintenance of systematics collections, be they developed as local reference collections, as collections intended for deposition and research at public institutions, or as benchmarks for conservation monitoring.

In short, the human resource challenges facing both tropical and temperate bio-inventory and conservation agendas are complex, and must be addressed in ways that comprehend regional, scientific and sociological landscapes.

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