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Biological Journal of the Linnean Society, 2016, 117, 386–398. With 1 figure. REVIEW Known knowns and unknowns in biology HUGH D. LOXDALE1*, BELINDA J. DAVIS2,3 and ROBERT A. DAVIS4,5 1 School of Biosciences, Cardiff University, The Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK 2 School of Plant Biology, University of Western Australia, Crawley, Western Australia, 6009, Australia 3 Botanic Gardens and Parks Authority, Fraser Avenue, West Perth, Western Australia, 6005, Australia 4 School of Natural Sciences, Edith Cowan University, 270 Joondalup Drive, Joondalup, Western Australia, 6027, Australia 5 School of Animal Biology, University of Western Australia, Crawley, Western Australia, 6009, Australia Received 7 April 2015; revised 8 July 2015; accepted for publication 12 July 2015 Here we present a knowledge-data framework based on the politico-military statement by Donald Rumsfeld (below) which has, we believe, direct relevance to ecological conservation. Ecological examples of four of the identified categories are provided with discussion of the conservation risks to a species through knowledge or data loss and movement through the categories. We show that so-called known knowns in terms of global biodiversity are not as accurately known as thought, despite 500 years or more of world-wide collecting and recording of eukaryotic species. In addition, as fast as new species, living or fossil, are discovered (unknown unknowns), some of which have revolutionised concepts about the biology of particular taxa, meanwhile, sadly other living species are being extirpated, or are assumed to be so (unknown knowns). These often have a high probability of ultimately being rediscovered, especially if small and/or living in remote, under-sampled regions. Furthermore, we suggest that in some cases it may be possible to predict the existence of known species in new habitats, or the existence of unknown co-evolved animal species (known unknowns). We discuss how technological advances (e.g. molecular markers and DNA sequencing) are inflating current estimates of biodiversity by identifying the existence of cryptic species. We believe the knowledge-data matrix provides another tool for conservation practitioners to focus data collection on bridging knowledge gaps for more effective conservation outcomes. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398. ADDITIONAL KEYWORDS: biodiversity – ecosystems – extant range – predicting species – species decline – species richness. Reports that say that something has not happened are always interesting to me, because as we know, there are known knowns; there are things we know we know. We also know there are known unknowns; that is to say we know there are some things we do not know. But there are also unknown unknowns – the ones we do not know we do not know. And if one looks throughout the history of our country and other free countries, it is the latter category that tend to be the difficult ones. species – extinction – geographical Donald Rumsfeld, then United States Secretary of Defence, in response to a ‘question at a US Department of Defence news briefing in February 2002 about the lack of evidence linking the government of Iraq with the supply of weapons of mass destruction to terrorist groups’ (Rumsfeld, 2002; http://www.defense. gov/transcripts/transcript.aspx?transcriptid=2636). INTRODUCTION *Corresponding author. E-mail: [email protected] 386 Although Donald Rumsfeld was cryptically referring to the lack of evidence linking the government of © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 KNOWN KNOWNS AND UNKNOWNS IN BIOLOGY Understanding Iraq with the supply of weapons of mass destruction to terrorist groups, his statement provides a useful framework for the biological and ecological sciences and ultimately to conservation management. In fact, it is perhaps the category that Rumsfeld failed to mention that is most relevant to biology and ecology, the unknown knowns. The degree of certainty with which we can define and understand a species, community, ecological function or process is highly variable, both spatially and temporally (Fig. 1 and Table 1). The speed at which an unknown biological entity may move from unknown to known is increasing rapidly as technology, especially molecular (DNA) techniques, provides insights into increasingly complex or increasingly finer scale population differentiations. An increasingly holistic approach to the practice of ecology from a species upwards to an entire ecosystem means knowledge gains are made locally or regionally and have applications globally. Our objective is to expand on Rumsfeld’s notion of ‘knowns’ and ‘unknowns’ and thereby present a novel conceptual framework for categorising knowledge under a risk paradigm. To achieve this, we draw on material from diverse fields in biology, which we briefly explore, defining each category as we do so (of the four outlined in Fig. 1 and Table 1), thereby helping prioritise areas of future research of considerable importance for conservation efforts of particular species and perhaps groups of species, e.g. co-evolved ones. Unknown Knowns •Data poor •Unproven hypotheses grounded in data from similar systems/species •Models that have not been ground-truthed Unknown Unknowns •Data poor •Undiscovered and unknown •The new froners of science 387 KNOWN KNOWNS In the proposed framework, known knowns encompass all the organisms currently known to science. The world biodiversity of eukaryotic organisms, including vertebrates, invertebrates and terrestrial plants is thought to be something of the order of 8.7 million species, according to a recent estimate (Mora et al., 2011). This study found that around 2.2 million of these species are marine and concluded that in spite of 250 years of taxonomy, 86% of existing species on earth and around 91% of those in the oceans, still await description. Unsurprisingly, Mora et al. (2011) found that taxonomic knowledge was closely related to higher taxonomic rank, thus higher order groups such as birds are relatively well known compared to fungi. Thus the number of known knowns, and subsequently the potential for their conservation, has a strong link to taxonomic rank. The number of known knowns is also constantly diminishing. With global extinction rates now exceeding long-term background extinction rates by between 100 and 1000 fold (Pimm et al., 1995), a crisis has emerged in that countless species are being lost due to anthropogenic pressures such as habitat loss, pollution, global change and urbanisation before they have been described. The earth is losing biodiversity at an alarming rate and if this continues, future generations of humans may be deprived of ever seeing such iconic animals as tigers, Known Knowns •Data rich •Understanding deep ie. Know abundance, habitat preference, funcon, mechanisc processes Known Unknowns •Data rich •Understanding held back by technological, praccal or methodological pracces. •Previously unknown mechanisc drivers of funcon that alter understanding Data available Figure 1. Matrix of knowledge and understanding. The first identifier for each category refers to the data available (xaxis) on which the knowledge basis is formed, the second (y-axis) to the degree of uncertainty or understanding. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 388 H. D. LOXDALE ET AL. Table 1. Examples of the four known unknown categories I. Known knowns Totals of identified species of Earth Vertebrates 66 178 Invertebrates 1 305 250 (of which around 1 000 000 are insects) Plants 307 674 Others 51 623 Grand total 1 730 725 II. Known unknowns (including estimates) Totals of estimated species of Earth Vertebrates 80 500 Invertebrates 6 755 830 Plants 390 800 Others (not given) Grand total 7 227 130 (References: Chapman, 2009; The World Conservation Union, 2014; see also http://www.currentresults.com/ Environment-Facts/Plants-Animals/estimate-of-worlds-total-number-of-species.php) This category includes inferences made about ‘missing’ organisms from their morphology, both in extant and extinct species (e.g. the beaks of Darwin’s finches and their usage; ears and facial nose leaf apparatus of bats used for echo location of prey before process was fully understood; nasal cavities in the skulls of Hadrosaur dinosaurs probably used for vocalisation; assumed colour of dinosaurs and behaviour of some species as inferred from wound damage to skeletal remains), presence and absence of organisms in apparently similar (sometimes contiguous) habitats, related to ecology and behaviour (e.g. apparent absence of the Nightingale Luscinia megarhynchos (Brehm) from much of southern Bavaria in Germany, even though the habitat appears suitable (H. D. Loxdale, pers. observ.; see also http://www.lfu. bayern.de/natur/artenschutzkartierung/atlasprojekte/doc/05_brutvoegel_nachtigall.pdf). III. Unknown knowns A plethora of animal and plant species have been rediscovered, including in recent years. In addition to the examples given in the main body of the text, other avian and mammalian examples include: Birds Bermuda petrel, Pterodroma cahow Nichols & Mowbray. Considered extinct for 330 years, rediscovered in 1951. New Zealand storm-petrel, Oceanites maorianis Matthews. Lost and found after more than 150 years in 2003 Campbell Island teal, Anas nesiotis (Fleming). Thought to be extinct for more than 100 years but rediscovered on Dent Island, part of the Campbell Island group off the south coast of New Zealand, in 1975. Takahe, Porphyrio mantelli (Owen). None seen in its native New Zealand after 1900, but rediscovered in 1948. Kakapo, Strigops habroptilus G. R. Gray. Effectively extinct by 1974, especially due to cat predation over its native range in New Zealand. Rediscoveries of a small number of birds and breeding programmes on small cat-free islands off the main islands have allowed the species to slowly recover. Jerdon’s babbler, Chrysomma altirostre Collar and Andrew. Lasts seen in its native Myanmar (Burma), part of its Asian range, in 1941, and rediscovered in 2014. Mammals Mountain pygmy possum, Burramys parvus Broom. Known from fossil record since 1895, and later discovered alive at Mount Hotham in Victoria, Australia in 1966. Desert rat-kangaroo, Caloprymnus campestris (Gould). Discovered in central Australia in early 1840s, rediscovered in 1931, then lost and not seen after 1935, thus presumed extinct. . .again! Cuban solenodon, Solenodon cubanus Peters. Thought extinct by the 1970s, but rediscovered in 2003 in the north-east of Cuba. Bahian tree rat, Phyllomys unicolor (Walker). Inhabits the Atlantic rain forest of Brazil. Collected as a single specimen in 1824, rediscovered, also as a single specimen, in 2004 after a year-long search. Machu Picchu arboreal chinchilla rat, Cuscomys oblativa (Eaton). First described from two skulls over 400 years old discovered by Hiram Bingham in 1912 at Machu Picchu in Peru. Rediscovered in 2009 near the original archaeological site. Nb. Fisher & Blomber (2011) conducted a global data set study in which they examined 187 mammalian species apparently extinct since the year 1500, and described how 67 of them (approximately one-third) had subsequently been rediscovered. See also http://www.petermaas.nl/extinct/lists/rediscovered.htm. IV. Unknown unknowns Every year, a few bird and mammal species are discovered new to science, along with other taxa, notably insects, more especially in the tropics. Again concentrating on birds and mammals, recent examples include: © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 KNOWN KNOWNS AND UNKNOWNS IN BIOLOGY 389 Table 1. Continued Birds 2013 Cambodian Tailorbird, Orthotomus chaktomuk Mahood et al. (2013), discovered in 2009. Sierra Madre Ground-Warbler Robsonius thompsoni Hosner et al. (2013), of the Philippine archipelago. 2014 Cryptic treehunter, Cichlocolaptes mazarbarnetti Barnett & Buzzetti (2014), from Brazil. Sulawesi streaked flycatcher, Muscicapa sodhii Harris et al. (2014), from Indonesia. Wakatobi flowerpecker, Dicaeum kuehni Kelly et al. (2014), also from Indonesia. Mammals 2013 Olinguito, Bassaricyon neblina Helgen (2013), a species of the racoon family living in montane forests in Colombia and Ecuador, the first carnivorous mammal to be described in the western hemisphere for 35 years. Lavasoa Dwarf Lemur, Cheirogaleus lavasoensis Thiele et al. (2013), from Madagascar. 2014 Araguaian boto, Inia araguaiaensis Hrbek et al. (2014), a true river dolphin from Brazil. Deraniyagala’s beaked whale, Mesoplodon hotaula Dalebout et al. (2014), a beaked whale from the Pacific region. Black-tailed antechinus, Antechinus arktos Baker et al. (2014), a carnivorous marsupial from Australia. In addition to these extant species, numerous fossilised species are found every year, many totally beyond expectations and which can revolutionise whole areas of knowledge, including about the morphology, ecology, genetics and behaviour of extinct taxa and provide new clues to the evolutionary process. Notable examples include the first Archaeopteryx fossil in the Solnhofen limestone deposits of Bavaria, southern Germany in 1860 or 61. Since then, another ten examples, some more complete than others, have been found, all in Germany. As mentioned in the text, the plethora of feathered dinosaurs discovered in the past 20 years in China has also greatly advanced knowledge on the evolution of birds from their dinosaur ancestors. snow leopards, rhinoceroses to name but a growing few, just as we have already lost the Passenger Pigeon, Ectopistes migratorius (L.) (extinct by 1914), Great Auk, Pinguinus impennis (L.) (extinct by 1844), the Thylacine, Thylacinus cynocephalus (Harris) (extinct by 1936), and Steller’s Sea cow, Hydrodamalis gigas (Zimmermann) (extinct by 1768) (Anderson, 1995; Paddle, 2000; Fuller, 2001). The recently discovered array of so-called cryptic species means that the number of known knowns is also increasing. This is especially evident in insects, a huge group of animals which has been very well studied due to their pest and beneficial status, including using molecular genetic markers (allozymes and DNA). Thus, for example, even the Silverleaf Whitefly, Bemisia tabaci (Gennadius), notorious pest of many cash crops, has now been shown to be, in all probability, a complex of cryptic species (Xu, De Barro & Liu, 2010; Tay et al., 2012), whilst hymenopterous parasitoids are especially rich in cryptic species (e.g. Atanassova et al., 1998) and as noted by Berenbaum (2009), probably a large proportion of recorded species are misidentified and are in reality cryptic species. This includes so-called generalist hymenopterous and dipterous parasitoid species which have been found, using mitochondrial DNA COI (cytochrome oxidase I) sequencing, to be arrays of specialists rather than generalists. In fact the recent introduction and wide- spread use of molecular markers is beginning to question the entire notion of generalism in nature, more especially in insects (Loxdale, Lushai & Harvey, 2011). Some butterflies in Africa, i.e. the African Queen, Danaus chrysippus (L.) sensu lato, are now known from mitochondrial COI studies to be a complex of geographically-genetically isolated semi-species (Smith, 2014). Even in higher vertebrates, cryptic discoveries are ongoing as demonstrated by the recent taxonomic revision of Australo-Pacific kingfishers (Andersen et al., 2015). To date, 11 species had been recognized in Todiramphus Kingfishers (Gill & Donsker, 2015), but increased sampling and the use of mitochondrial DNA to better detect the presence of rapid radiations found strong support for a minimum of 26 species. Evidence was found for extensive range expansion, secondary sympatry and diversification at a rate not observed previously in birds. While this study is not exhaustive, and the authors themselves state that further sampling of difficult-to-reach islands is required for resolution in some parts of the phylogeny, it is a good example of how scientific knowledge is gained incrementally with an increasing accuracy to add to the body of ‘known knowns’. Equally rapid dissemination of these knowledge gains is vital to inform future conservation efforts, policy development, and research questions into similar systems or species. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 390 H. D. LOXDALE ET AL. In terms of known knowns, whatever a species population is exactly, it is a dynamic entity and, depending on the species concerned, can involve resident populations, perhaps showing high habitat fidelity within a local metapopulation structure, for example, the Glanville Fritillary butterfly, Melitaea cinxia (L.), in Europe, vagrant populations that shift according to the seasonal severity/unsuitability of the habitat, such as populations of the European Song Thrush, Turdus philomelos (Brehm), and Robin, Erithacus rubecula (L.), which leave freezing European regions in winter time and head to more temperate climes (e.g. Perez-Tris & Tellerıa, 2002; Tellerıa, Ramirez & Perez-Tris, 2008), to truly migratory species such as Barn Swallows, Hirundo rustica (L.), and House Martins, Delichon urbicum (L.), and in the case of butterflies, Painted Lady butterflies, Vanessa cardui (L.), which always undergo seasonal long distance movements from Africa to northern Europe, in these cases, aerial movements (Stefanescu, Alarcon & Avila, 2007; Stefanescu et al., 2013). Because populations do shift spatially and temporally, it is sometimes difficult to define what, in reality, a native species is exactly and what is invasive, although of course dramatic population changes have been observed in recent historical times. Examples here include the Eurasian Collared Dove, Streptopelia decaocto (Frivaldszky), in Europe and the USA (Fujisaki, Pearlstine & Mazzotti, 2010), and the Speckled Wood butterfly, Pararge aegeria (L.), in the UK (Hill et al., 2002). Such movements can be on a broad front, as in the case of the invasion of the continental European Median wasp, Dolichovespula media Retzius, into the UK in the late 1980s–1990s (Hammond et al., 1989). Alternatively, they may occur by means of stepping-stone changes as with the cynipid Knopper Gall Wasp, Andricus quercuscalicis (Burgsdorf) and its slow progress from its original centre of diversity in the Balkans north-west towards, and finally, into Britain and Ireland (Stone & Sunnucks, 1993). They may occur radially as in the case of the chrysomelid beetle, the western corn rootworm, Diabrotica v. virgifera Le Conte from its original centre of diversity, also in the Balkans (Ciosi et al., 2008), or lastly, randomly, involving the introduction of a very few individuals, as appears to be the case for the founder finches on the Galapagos Islands (maybe > 30 individuals) (Vincek et al., 1997), and the lupin aphid, Macrosiphum albifrons Essig, into the UK in the early 1980s, possibly as a result of the introduction of a single asexual individual (Carter, Fourt & Bartlett, 1984). When considering the temporal scale of species population invasions, as alluded to with the Knopper Gall Wasp, these can be slow, taking decades or centuries, or relatively swift, occurring over the course of a few days or weeks, depending on the dispersal powers and reproductive capacity of the organism concerned, as well as the suitability of the habitat into which the population invades. Such invaders can be passive, with little apparent ecological effect, or devastating, both in terms of their impact on human affairs, especially agriculture/horticulture/forestry and fisheries of one sort or another, but also in competition with, and sometimes replacing, native taxa or by disease transmission – e.g. native crayfish in Europe, Astacus astacus (L.), in competition with North American species, especially the Signal Crayfish, Pacifastacus leniusculus (Dana) (Holdich & Reeve, 1991). Invaders can be a force for good, or ill, depending on the particular concern and interest, e.g. ecological such as native and endangered Palaearctic White-headed Duck, Oxyura leucocephala (Scopoli) hybridizing with introduced North America Ruddy Duck, Oxyura jamaicensis (Gmelin) (Mu~ noz-Fuentes et al., 2007), or economic as with the invasive prickly pear, Opuntia spp. in Australia controlled by the introduced Cactus moth, Cactoblastis cactorum (Berg) from South America (Marsico et al., 2010). As well as the rise of species, the opposite trend can occur, for example as seen recently in the decline and population retreat of many once common birds in the UK (British Trust for Ornithology, BTO; http://www.bto.org/about-birds/birdtrends/2014/species). It is also relevant to the debate of known knowns to reflect on the fact that whatever the state of the biomes and biodiversity of present day ecosystems, other ecologies, many rich and highly diverse, existed in former times, as first realised by the great English palaeontologist Gideon Mantell (1790–1852) in relation to Mesozoic faunas and floras (Cadbury, 2001). In other words, species populations and their respective ecologies show a clear, longer-term temporal dimension in addition to shorter term dynamic changes, such as seasonal and phenological changes, and what may be present in one epoch largely or completely disappears – for whatever reason/s – in another. In many, if not most cases, we hardly know what these ecologies were for fossilised species, but in the case of terrestrial invertebrates, especially insects, we at least have some reasonable idea of who the central players were and perhaps what some of the habitats they occupied may have been like, especially for organisms trapped in amber, i.e. ~5–130 Mya (Ross, 1998; Grimaldi & Engel, 2005; Penney & Jepson, 2014) (also see Known unknown section below). The published scientific literature plays a central role in relation to the existence and recording of known species. Even when a biological–taxonomic description of a new species is published in a peerreviewed journal, the benchmark of something © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 KNOWN KNOWNS AND UNKNOWNS IN BIOLOGY becoming a known known, knowledge decay may be in action. The pressure to publish rapidly has resulted in the proliferation of incorrect or biased information gleaned from reviews and meta-analyses, rather than the primary literature (Lawrence, 2003; Stewart, 2010). Increasing reliance on review literature can result in citing the review literature as opposed to the primary literature, taking away both the credit of the original author/s and opening the door to knowledge decay. An alarming study by Simkin & Roychowdhury (2003) that quantified the misrepresentation of primary literature tracked typographical errors in the references of an article; they concluded that only approximately 20% of people read the original article. Greenberg (2009) found that distortions in the persuasive use of citations can lead to these becoming unfounded scientific facts. With increasing distance from the original source literature, a proliferation of deviation from the original findings of the study is allowed, and so something that was once a known known can quickly deteriorate to become, in effect, an unknown known. KNOWN UNKNOWNS Many scientific endeavours can be said to have begun as ‘known unknowns’, typically beginning as an untested hypothesis built on the foundation of previous research, or as a theoretical concept. They are species or concepts for which there is a limited amount of knowledge, but resolution on presence, distribution, function, etc. relies on further investigation, e.g. Dmitri Mendeleev’s (1834–1907) prediction of missing chemical elements in the Periodic Table, hitherto unknown elements which were later discovered. In terms of the practical application of scientific knowledge for conservation or land management efforts, a known unknown can be particularly dangerous. Some data are available but not enough for a scientifically robust explanation to be made, leaving the interpretation and application, or at times ignorance, of data open. New technological advances in molecular studies have created a wealth of known unknowns, for example direct DNA sequencing of soil samples has revealed multitudes of fungal species that were previously unknown, unculturable and unnamed (Salvioli & Bonfante, 2013). However, baseline information on distribution, abundance and identity does not provide any insight into the functional role that these fungi play in nutrient scavenging and transfer, ultimately leading to driving woodland community structure (Read, Leake & Perez-Moreno, 2004; Teste et al., 2014). Baseline data on the presence and abundance of a species are a crucial first step, but a lack of data and understanding on seasonal influences, hunting 391 pressures, or ecosystem functional roles can mean conservation and land management practices are ill informed at best. The state of a known unknown can move forward in understanding and become a known known. This has occurred repeatedly through the formulation of hypotheses and experimental testing. To continue with the fungal example above, this scenario has occurred in orchid fungal symbiosis, where we now understand that previously identified fungi of the genus Rhizoctonia form a symbiosis with orchid plants to enable these to obtain nutrition (Burgeff, 1936; Warcup & Talbot, 1980). There is increasing evidence to suggest that this may be a mutualistic relationship (Cameron, Leake & Read, 2006). However, there is an acknowledged uncertainty in the known unknowns category and something may remain in this category indefinitely. For example, a proposed ‘missing link’ in the fossil record may be suspected to exist based on other available fossils either side of the missing evolutionary step, but this fossil may never be recovered and so the hypothesis never tested (see Zhou & Zheng, 2003 for an outline of the discovery of the ‘missing link’ in Ginkgo evolution). The key to precautionary science lies in acknowledging the existence of known unknowns and using them to either guide future research or to guard against the proliferation of assumptions to bridge the knowledge gap. This particular category of known unknowns is, by its very nature, harder to define in a practical sense. Perhaps an example here is the Lulworth Skipper butterfly, Thymelicus action (Rottemburg), known from many areas in Central Europe, Asia Minor and North Africa and first described by the 18th century German entomologist S. A. von Rottemburg in 1775, but which was not discovered in the UK until 1832, at Lulworth Cove in Dorset, hence the English name of this insect (Riley, 2007). Since the species feeds on a widespread host plant, Tor-grass or Heath False Brome, Brachypodium pinnatum (L.) P. Beauv., maybe it was not that unusual to find it in the UK, although the butterfly is very local here, as it is over much of its geographical range, suggesting it to possess special habitat requirements, as well as showing low vagility due to a high degree of behaviourally driven habitat fidelity. Possibly the Lulworth skipper, like the Glanville Fritillary butterfly, confined in the UK to the southern fringe of the Isle of Wight, is an ice age relic species, hanging on at the edge of its range where the climate is most favourable (especially hours of sunshine), and cut off, as was Britain, by the rise of sea level and hence from its former range in mainland Europe. A good case study relating to the difficulties of conservation concerning known unknowns is illustrated © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 392 H. D. LOXDALE ET AL. with regard to the Large Copper butterfly subspecies, Lycaena dispar dispar (Haworth), which finally became extinct in 1864 in its last remaining fenland strong holds of East Anglia, England as a result of the combined effects of habitat loss (with no doubt concomitant inbreeding depression of fragmented remnant populations) and over-exploitation due to overzealous collecting, especially by locals for sale of specimens to butterfly collectors (Thomas & Lewington, 1991; Riley, 2007). An almost identical subspecies, L. dispar batavus (Oberth€ ur) was discovered in the central-eastern Overijsselin fenland region of Holland in 1915 (Riley, 2007) and likely represented what may have been a continuous population before sea level rises separated England from the Continent some 200,000 years ago (Thomas & Lewington, 1991; see also http://news.bbc.co.uk/1/hi/sci/tech/6904675.stm). Re-introduction of L. dispar batavus from Holland to areas of previous known occupation in the UK have subsequently failed. The leading cause of re-introduction failure is thought to be differences in fenland characteristics as a consequence of different management practices between source populations and re-introduction sites (Barnett & Warren, 1995; Strausz et al., 2012). While the existence of the almost identical subspecies of Lycaena dispar batavus was known to occur in very similar habitat, the larvae feeding exclusively on the leaves of the Large Water Dock, Rumex hydrolapathum Hudson, resolution of knowledge required for a successful re-introduction program was not available, including exact knowledge of the genetic, hence chemotype status of the original host plant of the caterpillars of L. d. dispar in England, resulting in the net loss of artificially introduced Lycaena d. batavus specimens and no knowledge gain (cf. Benedek et al., 2015 as an exemplar for the importance of chemotype in insectplant feeding associations). Here the common ‘need for a rapid conservation action’ that surrounds species falling into the known unknown category did not result in a positive conservation outcome. Perhaps on closer inspection of the habitat and habitat requirements of the butterfly, the existence of the Dutch subspecies might have been predicted. Having said that, the ecological/habitat requirement of many butterfly species are still obscure, and it is often difficult to re-introduce populations to areas of previous known occupation, as in the case of the Large Copper, where all UK/Eire re-introductions have ultimately failed, for one or more unknown reason, probably including genetic. The discovery of an apparent subspecies of the Small Mountain Ringlet butterfly, Erebia epiphron (Knoch), in Ireland (possibly subspecies aetheria Esper) was undoubtedly based on knowledge of the butterflies habits and habitat in the highlands of England and Scotland, although the Irish forms is now seemingly extinct (Riley, 2007). However, the discovery of a new species of Wood White butterfly in Ireland in 1988, Leptidea reali Reissinger, mainly from comparative examination of the male genitalia and behavioural/ecological differences between the ‘normal’ Wood White, L. sinapis (L.) sensu stricto, was totally unexpected (see Riley, 2007 and references therein), although the butterfly is found in other areas of Europe, including Spain, southern France and Italy. Again, perhaps it could have been discovered earlier if these factors had been realised earlier, or even looked for. The different species/sub-specific types of the Wood White form a west-east cline in terms of chromosomal karyotype across Europe (Lukhtanov et al., 2011). Another intriguing aspects of the known unknowns category is that knowing what a habitat looks like in terms of plant morphology/floral diversity, it may be possible to predict what co-evolved animals exist or once existed in the ecosystem, and vice versa. Famous examples include the co-evolved Madagascan orchid flower, Angraecum sesquipedale Thouars, with a long spur filled with nectar and predicted (in 1862; Darwin, 1862) by Charles Robert Darwin (1809–1882) to be pollinated by a sphingid hawk moth (Xanthopan morganii Rothschild & Jordan, as it was eventually shown to be) with a suitably long proboscis (Kritsky, 1991), and the Tambalacoque or Dodo tree, Sideroxylon grandiflorum A. DC of the Island of Mauritius in the Indian Ocean, the seeds of which were apparently swallowed by the Dodo, Raphus cucullatus (L.), allowing subsequent germination of the seeds. With the Dodo’s demise, a concomitant demise of the co-evolved tree occurred such that by 1973 only 13 examples survived, all apparently more than 300 years old (Temple, 1977). However, this number is contested, as indeed is the specific requirement for the Dodo’s role in seed germination (Hershey, 2004), since domesticated turkeys can perform the task perfectly well, hence suggesting the known unknown in this particular case may have included other large bird species. As we go back further in time, it becomes harder to guess what former, essentially unknown ‘fossil’ ecologies were like, and indeed the actual players themselves, rather as is the case in human genealogy. Even so, much information can be gained from the remains of extinct organisms in deducing their morphology, ecologies and sometimes, even behaviour. UNKNOWN KNOWNS This forgotten corner of the Rumsfeld matrix (Fig. 1) refers to a third category, the unknown knowns, those species which we know did once exist, and assume are now extinct for whatever reason, but because of poor data, including observational and © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 KNOWN KNOWNS AND UNKNOWNS IN BIOLOGY poor sampling, cannot prove one way or the other. Data is typically as rudimentary as mere presence/ absence and includes species that were extant in recent historical times but in all probability are now extinct, or may even have been subsequently rediscovered. Untested models and missing links in the fossil record can also be classified as unknown knowns. Classic examples of animals ‘lost’ and then re-found include the Australian marsupial Gilbert’s Potoroo, Potorous gilbertii (Gould), which was rediscovered in 1994 at Two Peoples Bay Nature Reserve, on the south coast of Western Australia after an apparent absence of 125 years (Sinclair, Danks & Wayne, 1997), and the Dibbler, Parantechinus apicalis (Gray), a small predatory marsupial, last seen in 1884 before being rediscovered in 1967 in scrubland at nearby Cheynes Beach, a gap of over 80 years (Morcombe, 1967). Another rediscovery from this area is the dull, skulking but vocal Noisy Scrubbird, Atrichornis clamosus (Gould), rediscovered in the heathland near Albany, Western Australia in 1961, after being declared extinct several times, and having not been seen for many decades (Webster, 1962). A last Australian example is the Night Parrot, Pezoporus occidentalis (Gould). This was thought to be extinct in 1912 but was later found as a road kill in 1990 (Boles, Longmore & Thompson, 1994) and again in 1999 (McDougall et al., 2009) and since then, observed coming to water in the Pilbara region of Western Australia (Davis & Metcalf, 2008) before the discovery and photographs of living birds in Queensland in 2013 along with confirmatory DNA evidence (see http://en.wikipedia.org/wiki/Night_parrot and references therein). All of these examples probably reflect the fact that Australia is a large, sparsely populated landmass, and the fact that these animals were found and then lost, probably reflects inadequate sampling of the habitats concerned. Inadequate sampling of large areas is a global phenomenon as the alleged observation of a living Ivory-billed woodpecker, Campephilus principalis (L.), last recorded alive in 1943 and apparently seen in 2004, illustrates. The forested swamplands of Arkansas in the southern USA where the bird may still survive in remote areas (Fitzpatrick et al., 2005), are vast and the ability to thoroughly and adequately sample such a generally inaccessible area is hence problematic. Other celebrated examples of ‘lost’ and ‘found’ include the Rosy Marsh Moth, Coenophila subrosea (Stephens) in the UK, thought to be extinct by the mid-19th century and not seen again until rediscovered independently in two regions, west Wales and Cumbria, in the late 20th and early 21st centuries, respectively (Skinner, 1984; Jones, 2003). Berlepsch’s 393 Six-Wired Bird of Paradise, Parotia berlepschi Kleinschmidt, named in commemoration of the 19th century German ornithologist, Hans von Berlepsch (1850–1915), was also recently rediscovered, in New Guinea in 2005, after an absence of almost a century (cited in Beehler et al., 2007; see also http://news.bbc.co.uk/1/hi/sci/tech/4688000.stm). Likewise, Nelson’s small-eared shrew, Cryptotis nelsoni (Merriam) of eastern Mexico, first discovered in 1894, was not seen again until 2003 and in the same area as the original discovery, the slopes of the San Martın volcano in Veracruz, Mexico (Cervantes & Guevara, 2010; Guevara & Cervantes, 2014). The whole issue of sampling is crucial in this discussion. Thus to produce, for instance, a species richness curve for terrestrial eukaryotic organisms in any particular area (a graph plotting the number of species found vs. area, time or sampling units; Scheiner et al., 2000) involves taking into consideration habitat heterogeneity/complexity, altitude, the behaviour of the animal (in the case of animals) concerned, i.e. whether diurnal or nocturnal, and method of sampling, with quadrats for plants, soil cores for subterranean animals, and perhaps use of Berlese-Tullgren funnels for animals in leaf litter, light traps for flying nocturnal insects, suction traps for both diurnal and nocturnal small flying insects, mist nets for small birds, insects and bats, etc. Unless the right sampling tool/method is employed and adequate sampling is continued for a long enough period, a species may evade detection, perhaps forever. For example, some moths are rarely, if ever, caught in William’s type light traps (which use tungsten light bulbs), but are instead regularly captured in Robinson traps (which use mercury vapour lamps) and vice versa, due to differential moth trap design/operational dynamics and the attractiveness of different electromagnetic spectra to different moth species (e.g. Taylor & Brown, 1972; Fox et al., 2006 [2013] see also Muirhead-Thomson, 1991; Rich & Longcore, 2006; Fayle, Sharp & Majerus, 2007). What separates a species from persisting and eventually being rediscovered and simply becoming extinct is what key changes have transpired and contributed to its decline in the timeframe from being a known known to an unknown known. These changes may be anthropogenically-driven, i.e. in terms of climate change or habitat disturbance, or the more natural erosion of genetic material or resource competition. It is before species reach this tipping point that knowledge is required to effectively prevent decline and eventual extinction. Here acquired knowledge may also prevent the unwitting human-induced extinction of a species thought to no longer exist in an area of impact. It is apparent that unknown knowns are of © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 394 H. D. LOXDALE ET AL. great importance to conservation and are perhaps one of the harder to effectively manage given the lack of available data, linking this category very strongly to sampling effort. UNKNOWN UNKNOWNS The unknown unknowns represent the species (living and fossil) and concepts that are completely novel. By its very nature, this category is often the hardest to convert into one of the other categories in the knowledge-data matrix, lacking either aspect. As such, this category represents a potentially boundless one and may lead to the discovery of new phenomena and hence great leaps forward in our scientific understanding. There are many examples of unknown unknowns found in the fossil record. These include feathered, flying dinosaurs in the late 1990s, early 2000s (e.g. Currie et al., 2004; Turner, Makovicky & Norell, 2007), and recently a giant rodent, Josephoartigasia monesi (Rinderknecht & Blanco), relative of the guinea pig and the size of a bull (estimated 1000 kg) that may have fought its rivals with tusk-like front teeth (Owen, 2008; Rinderknecht & Blanco, 2008). As for living taxa, because so many groups are still inadequately recorded, especially in the biologically rich tropics, then undoubtedly the total fauna is underestimated, probably significantly in the case of insects. With vertebrates, each year brings the discovery of a new mammal species to science (41 in 2009; http:// krisheeter.hubpages.com/hub/How-Many-New-SpeciesHave-Been-Discovered-in-One-Year-Take-a-Guess), sometimes even large ones such as the Saola, Pseudoryx nghetinhensis Dung et al., a species of deer in Vietnam and Laos in the early 1990s (Dung et al., 1993; Schaller & Rabinowitz, 1995), and also quite a few new species of birds, reptiles, amphibians and fishes. As recently as 2005, a totally new extant genera of mammals (Laotian rock rat, Laonastes aenigmamus Jenkins et al.), was discovered in Laos, a so-called ‘Lazarus’ taxon, hitherto only known from extinct examples in the fossil record some 11 Myr old (Jenkins et al., 2004; Dawson et al., 2006). Sometimes the discovery of new species can be truly spectacular, as with the discovery of the Okapi, Okapia johnstoni (Sclater) by Harry Johnston (1858– 1927) in 1901 in the Congo, the long considered extinct Monoplacophora shellfish dredged from a deep trench off the Pacific coast of Central America in 1952 (the extant species of which, e.g. Neopilina galatheae Lemche, have been placed in a Class of their own; Lindberg, 2009) and most famous of all, the discovery of a living Coelacanth, Latimeria chalumnae J. L. B. Smith, thought to have been long extinct for some 80 Myr, off the coast of South Africa in 1939 (Smith, 1956) (the last two mentioned animals could nominally also be included in the ‘unknown knowns’ category in the sense that the taxa were known from the fossil record, but not the actual species discovered alive). All three species may be termed ‘living fossils’. On a species population level, the discovery of a thriving population of the Chequered Skipper butterfly, Carterocephalus palaemon (Pallas) in Scotland in 1939, the species having since become extinct in England in 1976, was an amazing find (Riley, 2007). With plants, the famous Dawn Redwood, Metasequoia glyptostroboides Hu & W. C. Cheng, was only discovered by chance during a botanical survey of the Sichuan and Hubei provinces of China in 1941 and in the fossil record in the same year (Ma, 2003; Ma & Shao, 2003). Following collection of seeds and their wide dissemination by human agency, it is now widely planted in gardens, parks and arboreal collections around the world. These particular examples are interesting because they show that many of the discoveries, fossil and extant, were totally unexpected. In the case of the extant organisms, this may simply be because we do not know the regional faunas and floras well enough (often because the said regions, wherever these are, have not been properly surveyed and explored, even geographically) or because of inadequate (or wrong) sampling, or because our paradigm of how a particular organism should behave and what habitat it should live in, as with the Chequered Skipper example above, is clearly wrong. As a further example of how our notions about the ecology and behaviour of living organisms can be quite wrong, the ornithological experiences of Tim Severin and colleagues is illuminating (Severin, 2000). In the late 1990s they went in search of Wallace’s Standard Wing, Semioptera wallacii G. R. Gray on the island of Halmahera, Indonesia, a species of bird of paradise originally discovered by the great naturalist and evolutionist Alfred Russel Wallace (1823–1913) in 1858 (Wallace, 1869). Instead of this rare and endangered bird being found deep within primary forest, as they had expected, it was found living precariously in logged secondary forest near to roads (the author and colleagues did later find a bigger colony of the bird in the interior of the north-west peninsula of Halmahera). Thus we should not impose our aesthetic values or presumptions on species whose adaptability and habitat plasticity may be much greater than we would assume. In the case of extinct animals, the discovery of new fossils can, as with the feathered dinosaurs, completely revise our views on how these long extinct creatures looked and behaved, and give clues to their physiology too, i.e. in this case, warm blooded. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398 KNOWN KNOWNS AND UNKNOWNS IN BIOLOGY Finally, acknowledging our limitations and recognizing that all systems have unknown unknowns should, in terms of ecological and conservation research, lead us to act with caution in the systems we are trying to restore and manage. For example, on Macquarie Island, a remote sub-Antarctic island, 34 km long by 5 km wide some 1500 km south-east of the southern tip of Tasmania, rabbits were introduced in 1878 and by the 1960s, had reached plague proportions and were decimating the endemic vegetation (Bergstrom et al., 2009). Release in 1968 of the European rabbit flea, Spilopsyllus cuniculi (Dale), vector of the Myxoma virus, severely reduced the rabbit population such that 10 years later the vegetation was to a large extent able to recover (Bergstrom et al., 2009). The feral cats of the island had hitherto preferentially predated rabbits but when rabbit numbers dramatically declined, the cats switched to eating seabirds (Bergstrom et al., 2009). A cat eradication programme was thus begun (in 1985) and by the year 2000, they had been completely eliminated (Bergstrom et al., 2009). Thereafter, the effectiveness of the Myxoma virus also declined and with rabbits released from cat predation, their numbers again grew with concomitant devastation of the complex native vegetation communities (Bergstrom et al., 2009). The effects of releasing Myxoma were thought to be known (a simple decline in rabbits allowing seabirds to recover); however, the unknown indirect effects of prey switching were not taken into account due to a lack of knowledge and data. While the employment of adaptive management may have saved seabird populations in the end by removing cats, the greater gain was one of knowledge of the need to manage potential prey switching predators concurrently with invasive prey removal. CONCLUSIONS As far as the actual discovery of living or fossil organisms is concerned, this, like much in life, is open to chance events and, as a consequence, re-interpretation of new facts in the light of new evidence. By such means, the science is pushed forward and our knowledge base grows. Who could have guessed, even as recently as the late 1980s, what amazing fossil dinosaur discoveries would soon be made in the Liaoning Province of north-eastern China, which have led to a golden age of paleontological enlightenment and revision. Perhaps science, like so much of our human culture, being very conservative, treads warily into the future and it takes chance discoveries to wake us up from our lethargy, conceit and orthodoxy. But when new living species are discovered, as 395 with those known knowns already in our sights, we should surely collectively, as the dominant species presently ruling the planet, go to great lengths to preserve such species and their habitats, more especially when one philosophises, as Alfred Russel Wallace did in his famous book The Malay Archipelago (1869; chapter 31), on the vast ages and generations it must have taken for living organisms – in this instance, the King Bird of Paradise, Cicinnurus regius (L.) – to adapt, evolve and persist to the present day and how such a species is very fragile in an ecological sense and hence potentially amenable to extermination at the hands of man. The recent widespread deployment of high resolution molecular markers, including DNA and protein sequencing, has revealed a plethora of morphologically similar-identical cryptic species in many taxa, especially including insects, greatly expanding our views on the extent of current biodiversity in such groups. It is clearly difficult to consider aspects of conservation of the world’s biodiversity, when we have not even got an accurate view of what is actually present in terms of known knowns, let alone the other categories as here described. Because of this, defining these categories, yet realising that they are at the same time fluid, and with leakage into one another, goes some considerable way in giving us more realistic insights, and hence a useful paradigm, on which to plan both current and future conservation strategies. In light of this and in order to put such efforts at species conservation into practice, the knowledge-data framework which we outline in this paper clearly emphasises the importance of identifying knowledge and data gaps in proposed conservation or research programs of particular species, thus prioritising areas in which data collection and research effort should be focussed. Use of the proposed matrix (Fig. 1) also allows practitioners to understand the trajectory a species may take if either knowledge or data are not available or further pursued (i.e. movement of a known known to an unknown known). Recognition of knowledge and data limits allows precautionary and scientifically sound management in light of unknown elements, which is vital to successful conservation efforts. 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