The fate of natural history museums in the face of good intentions

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A recent opinion advocating for a reorientation of natural history museums to hold ‘compassionate collections’ that minimize harm to wildlife (Byrne 2023) begs commentary. Such collections are defined by four premises, only the first of which (avoiding the killing of organisms to obtain specimens) is controversial. The remaining three principles promote optimization of the maintenance and study of existing collections, whilst fostering a more inclusive community (Byrne 2023), which museum curators already strive to do. In our opinion, because the fundamental functioning of natural history museums would be impacted by this doctrine, its promotion and potential consequences should therefore elicit an in-depth evaluation by museum scientists. We hope to demonstrate here that compassionate collections would not fulfil the urgent exigencies of scientifically assessing biotic diversity, which is vital to our understanding of ecosystems and evolution. Neither could they stimulate anything other than a more superficial connection to the complex and intricate realities of the natural world than presently exists. Rather, if endorsed, such a dogmatic vision would result in a progressive and dramatic loss of knowledge, with an inevitable concomitant threat to the future of biotic studies. As humans, we commend compassion as a quality that enables us to appreciate humans and nature more fully. However, as museum taxonomists we believe that compassionate collections as described in Byrne (2023) hold the power to fundamentally influence epistemology. The compassionate collection vision forms part of a recent spate of opinion pieces promoting alternative and often iconoclastic approaches in museum science (e.g. Minteer et al. 2014, Guedes et al. 2023). Because we welcome discussion relating to the evolution of museum science, such as that which Byrne’s (2023) proposal has stimulated, a response to it is required in order to present a wholly divergent perspective. We agree that natural history museums are places of wonder that induce powerful emotions in visitors. That awe only intensifies with contemplation of the enormous scientific value of their specimen collections and the great responsibility and effort spent to conserve them for posterity. Biologists try to understand how life functions at molecular and cellular levels, in addition to at the scale of ecosystems. While tremendous progress has been achieved in understanding life functions and mechanisms at a microscopic level, knowledge of ecosystems lags far behind (Kim and Byrne 2006). The difficulty is due primarily to the fact that the basic units of ecosystems are species, along with their functional traits. Because knowledge of species diversity forms the foundation of study of the living environment (Wilson 2000), the assessment of species (i.e. the forms of life that evolved on our planet) should be considered a priority. However, it is sobering to observe the discrepancy between the bewildering species richness on our planet and the dwindling number of researchers seeking to discover, name and study it (Engel et al. 2021). To date, only a small proportion of extant species diversity has been recognized and described (Mora et al. 2011). Estimates of the total number of species are inconsistent, ranging from millions to billions (e.g. Erwin 1982, Costello et al. 2012, Dijkstra 2016, Sinniger et al. 2016, Larsen et al. 2017, Stork 2018, Louca et al. 2019). However, it appears that at best only 20% of extant animals have been hitherto described (Chapman 2009), with biological information lacking entirely for many of them. Because invertebrates alone constitute about 97% of the animal kingdom, they therefore exemplify the enormous gaps in our knowledge (Zhang and Shear 2007). Although some of the as-yet-unnamed species have already been collected and are preserved in museum collections awaiting formal description, the majority have yet to be sampled, whilst their threatened habitats continue to shrink around them. In the field, taxonomists regularly find undescribed species whenever, for example, they enter a tropical or subtropical forest, examine deep-sea samples, or seek intestinal parasites in other animals (our personal observations, Appeltans et al. 2012, Scholz and Choudhury 2014). Hence, describing species diversity on Earth is arguably one the most challenging tasks confronting biologists, with increasing urgency in the face of ever diminishing and declining biotopes. Species are concepts—we are faced with contemplating no fewer than 32 of them (Zachos 2016). Notwithstanding, all species descriptions are necessarily based upon specimens, with each species being distinguished according to the idiosyncratic criteria of individual taxonomists, influenced by pre-existing knowledge and available technology at a given time. Because no two specimens can be identical, each species exhibits variation that is usually incompletely known. Robustly assessing the limits of variation within a species requires the study of numerous specimens, a task that is only achievable using natural history collections. Therefore, assessment of biodiversity relies on museum collections and faces theoretical and practical problems. A second major issue derives from the innumerable characters that each specimen exhibits. Only some of these are conspicuous, and relatively few are selected to discriminate individual species. Historical data, based on fewer recognized species and outdated technology, frequently become obsolete. Consequently, taxonomists spend a large part of their time unravelling, verifying, and updating previously published information, a tedious but crucial task based on study of important voucher specimens held in collections. Because science, by definition, requires continuous hypothesis testing and revision as new information becomes available, there is no reason to believe that vouchers will lose their ‘raison d’être’. Collections in natural history museums are and will remain prerequisites for sound biodiversity studies (Lister 2011, Miller et al. 2020), and they represent much more than solely archives of hitherto described and studied life forms. They document the changing distribution of species across space and time and are essential as falsifiable vouchers when published data appear dubious and in need of scrutiny. Physical vouchers of collected species are, and arguably will remain, key to gaining deeper insights into our understanding of the natural world for generations to come (Ruane and Austin 2017, Schmidt et al. 2019, Raxworthy and Smith 2021, Warnett et al. 2021). The recommendation of replacing preserved specimens by photographs and tissue samples (Byrne 2023), which could avoid killing wildlife and which are easier to store, is not new (Minteer et al. 2014). Accepting this suggestion would limit knowledge of species to a minute fraction of the most obvious characters, impede recognition of similar syntopic species, and render information much less verifiable and falsifiable, thereby shifting taxonomy away from the realm of science (Ceríaco et al. 2016). Furthermore, in many cases meaningful photography of the informative anatomical structures of living animals is impractical or impossible and would relegate important biological fields, such as parasitology, to the sidelines. But even proposing photography of living animals as an alternative is a moot point because most animals are very small species of invertebrates that simply could not realistically be found and sampled alive in the field, let alone be kept alive long enough to enable compassionate collection, including the requisite viable release into the wild. For example, many insect species are known only from specimens collected with necessarily lethal traps (Malaise traps, flight-interception traps, etc.). Another parochial assertion is the proposal that DNA samples can replace entire specimens. The encrypted information in genomes

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