Preserved biological specimens are increasingly providing source material for research that is moving beyond traditional questions in collections-based studies. Technological advances are facilitating both traditional and nontraditional uses of these shared research resources. For example, advances in analytical chemistry have enabled researchers to obtain data on heavy-metal contaminants and diets from a single feather. Future technological advances will increase nontraditional use of specimens, and two areas of rapid growth at present are in contaminant and stableisotope studies. We address these developments and their implications for bird collections.
Contaminants.—
Retrospective contaminant studies of the 1960s and 1970s premiered a new and important use of specimens. One of the first studies to use bird specimens in contaminant research documented a 10- to 20-fold increase in feather mercury among seed-eaters and raptors after the introduction of alkyl-mercury seed dressings (fungicides) in Europe in the 1940s (Berg et al. 1966). That research led to the banning of those seed treatments, and subsequent retrospective analyses using specimens confirmed the effect of alkyl-mercury fungicides by documenting the decline of mercury concentrations in feathers after the ban (Westermark et al. 1975). Probably the best-known use of museum specimens in retrospective research documented eggshell thinning in raptors following the introduction of DDT in 1947 (Ratcliffe 1967, Hickey and Anderson 1968). These studies and others (see Kiff 2005) contributed to the eventual ban of DDT in many countries.
Researchers have documented high levels of contaminants in the biota of undeveloped regions, citing the global distribution of pollutants as the cause (Arctic Monitoring and Assessment Programme 1998). As global contaminant burdens increase, spatially and temporally distributed biological samples are needed to document changing contaminant levels. Archived avian specimens can document levels of heavy metals, because heavy metals bind to feather keratin at the time of growth (Crewther et al. 1965). Archived specimens were used to document increases in mercury pollution in several avian food webs (Appelquist et al. 1985; Thompson et al. 1992, 1993). Time series of archived seabirds were also used to document increases in feather mercury concentrations in two avian food webs over the past 100 years, which were correlated with anthropogenic inputs (Monteiro and Furness 1997, Thompson et al. 1998).
Although most specimen-based retrospective contaminant analyses have dealt with mercury, all heavy metals can be measured in feathers. Feathers are useful indicators of elemental body burdens at the time of growth, because feathers provide a route for elimination of contaminants (Goede and de Bruin 1984). Contour feathers seem to have the least variation among feather types, allowing comparison among studies (Furness et al. 1986). Despite a general lack of information on toxicity thresholds in feathers (e.g. what concentrations in feathers indicate negative organismal effects), feathers from museum specimens represent a powerful tool for comparing temporal and spatial distributions of heavy metals in the environment.
Birds are useful biomonitors of their environments, and they offer an opportunity to sample at different trophic levels. Contaminant studies generally use tissues and organs not normally preserved by museums. But, with planning, use of birds as biomonitors can be coupled with standard museum processing and preservation to simultaneously achieve very different scientific gains. Enhancing working relationships between museums and contaminants biologists benefits both groups, and this is an important direction of future growth for collections. Increasingly refined analytical abilities will continue to enhance the usefulness of museum specimens for contaminant studies as new techniques reduce the amount of sample required for analyses. Small amounts of muscle tissue now preserved for genetics, for example, may also prove valuable in future contaminants research.
Stable isotopes.—
Stable isotopes are increasingly being used in ecology, population biology, and ecosystem monitoring. Isotopic ratios among many naturally occurring elements vary geographically and are incorporated into local food chains. Different tissues (e.g. feather, bone, liver, kidney, and muscle) have different isotopic turnover rates, and the tissues of archived specimens can be used to provide clues regarding seasonal ecological processes in, for example, migratory birds. Isotope ratios of carbon are often distinct among terrestrial, freshwater, and inshore and pelagic marine food webs, and nitrogen shows predictable trophic enrichment (e.g. Hobson 1999, Kelly 2000). Analyzed in concert, these widely studied isotopes have been used to delineate food webs, infer foraging locations, and document diet shifts. Stable-isotope ratios, like heavy metals, are incorporated into feathers at the time of growth and remain inert, providing a record fixed in time (Mizutani et al. 1990) that enables researchers to monitor long- and short-term changes in ecosystems using avian specimens.
Feather stable isotopes from archived Atlantic Northern Fulmars (Fulmarus glacialis) documented broad-scale diet shifts during the 20th century, probably attributable to the whaling industry (Thompson et al. 1995). The ability to detect ecosystem-scale shifts in food webs with stable isotopes is also proving useful in ecosystem monitoring. Studies using archived whale baleen suggested long-term changes in oceanic primary productivity in the Bering Sea, one of the world's most important fishing grounds (Schell 2000). This hypothesis is being tested using archived specimens of Bering Sea birds (G. J. Divoky pers. comm.). Similarly, specimenbased isotopic analyses suggest historical dietary changes in federally listed populations of the Marbled Murrelet (Brachyramphus marmoratus), providing insight into possible reasons for their decline (S. Beissinger pers. comm.). This type of research is increasing and highlights the value of historical specimens in documenting change.
Stable isotopes such as deuterium, oxygen, strontium, and sulfur also show regional variation. This variation can be enlisted to address classic questions of population biology (i.e. spatial and temporal distributions) in highly mobile organisms, such as migratory birds. In individuals and populations that move among isotopically distinct regions, multiple stable-isotope analyses have the potential to track organisms throughout their annual cycle, and this is another growing research area (Hobson 1999). Presently, these markers do not provide sufficient resolution to monitor regional movements among habitats or to assess population mixing, and more work is needed to understand links between abiotic and biotic isotopic signatures within the systems (geographic and taxonomic) being studied. However, research on the physiological processes governing stable-isotope ratios in consumer tissues (e.g. Gannes et al. 1997, Pearson et al. 2003), coupled with local environmental studies, will likely enhance our understanding of the relationship between biotic isotopic ratios and the environment and improve the ability to track organism movements.
The proliferation of stable-isotope research has significant implications for specimen use and is an important direction of growth for collections. These studies have shown that specimens are a valuable resource for understanding populations, diets, and changes over time in populations and their environments. This research requires destructive sampling of small pieces of specimens, and such use is certain to increase. This increase should be coupled with expanded participation in building the resource. As Winker (2005) noted, the multidimensional benefits gained through whole-organism sampling suggest that this is the most effective common ground on which to focus such expansion. With planning, this approach would also provide the widest possible array of tissue types for contaminant and stable-isotope studies.
Value of archived specimens.—
Archived specimens provide important baselines for comparison with modern counterparts. This is especially true when attempting to document environmental contamination. Previous retrospective studies in birds highlight the need for, and general lack of, good temporal series. At present, museums generally do not have adequate time series to answer temporal questions with rigor. Unlike genetic samples, some isotopic ratios and contaminant concentrations from the same location can change rapidly and exhibit large variation within and among years. Documenting trends and historical changes at useful geographic scales with statistical power requires continued sampling and proper archiving.
Birds are often sacrificed in food habit, energetic, physiological, population, and pollution studies. Although these studies provide valuable information on avian biology, archiving the specimens can provide important long-term data. We strongly encourage researchers to deposit sacrificed birds into collections and to offset costs to repositories by providing funds for preservation of this resource (see Winker 2005). Archived bioindicators become biomonitors that can be used to establish baselines for future retrospective research.
As museums and new partners continue to build specimen series, it should be recognized that time- and space-saving techniques, such as preparing flat skins, can often be used without compromising the value of the preserved material. Nondestructive sampling (e.g. feather or blood collection) is sometimes used by researchers because it is seen as saving space, time, and money. However, it does not yield the longterm scientific strengths of preserved whole animals and therefore is not supported by most museums. Broad issues of quality control exist in samples that are small in quantity, destined largely for destruction, and unvouchered (Winker et al. 1996, Payne and Sorenson 2003, Smith et al. 2003). For example, using feathers plucked during banding for stable-isotope, contaminant, and genetic research (e.g. Smith et al. 2003) may increase sample sizes for some studies, but sample destruction makes replication problematic. Stable isotopes and contaminants can vary within a single feather and among feather types (Furness et al. 1986, Bearhop et al. 2002, Dauwe et al. 2003); without vouchers, analyses may not be verifiable or repeatable. In short, unvouchered subsamples of birds do not have the high scientific value of the modern museum specimen.
Preserving specimens for retrospective research is clearly important and requires a dynamic vision of how collections will be used in the future. Continued technological advances ensure that specimens will continue to produce answers to unanticipated questions (Suarez and Tsutsui 2004). Birds are important monitors of ecosystem health. New uses for specimens demonstrate an important and growing role for collections in population and ecosystem management. It is important that these “new uses” be documented and publicized to make the scientific community and public aware of the increasing user base and the dynamic role that museums play in conservation and environmental sciences. Public, political, and financial support is necessary if museums are to meet their obligation to anticipate “new uses” and ensure that collections archive material that will meet the needs of future research.
