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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:
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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
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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
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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.
ACKNOWLEDGEMENTS
We thank the anonymous referees for their insightful
comments on an earlier draft of this paper, which
have made us re-visit our views and arguments and
attempt to re-focus them, and Nicola von Mende-Loxdale for her editorial suggestions for improving the
manuscript.
© 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 117, 386–398
396
H. D. LOXDALE ET AL.
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