Species, Extinct Before We Know Them?

Magazine R177

Essay

Species, extinct before we know them?

Species are going extinct rapidly, while taxonomic catalogues are still before taxonomists could describe incomplete for even the best-known taxa. Intensive fi eldwork is fi nding species them [7]. All of these were island so rare and threatened that some become extinct within years of discovery. species. We are still documenting Recent bird extinctions in Brazil’s coastal forests suggest that some species the impacts of European explorers — may have gone extinct before we knew of their existence. and the rats and cats that came with them — that began centuries ago. We Alexander C. Lees1 watch them go extinct soon thereafter? know about some early extinctions and Stuart L. Pimm2,* If this situation were common, we would from anecdotal evidence, such as also expect to have lost some species eyewitness accounts and drawings. Taxonomists are still describing before taxonomists could name them. They include the inferred extinction new species of birds, mammals and of several species of large Caribbean amphibians, even though these taxa Birds in Atlantic Brazil macaw [8]. Parrots fascinated both have the most complete taxonomic We here consider the Brazil’s the Tupi and early visitors to the New lists. From these groups, we are Atlantic Forest or Mata Atlântica — World and they were valuable items losing species at a rate of hundreds a coastal wet forest. It has the for trade [6]. Martin Waldseemüller’s of extinctions per million species per highest concentration of threatened map of 1507 shows a ‘red parrot’ — year [1]. This is a thousand times faster vertebrates in the Americas [1], due possibly a macaw — just above the than the natural background rate of to its exceptionally high numbers of word ‘America’, famously used here extinction of about 0.1 extinctions small-ranged species coupled with for the fi rst time. Northeast Brazil has per million species per year [1,2]. very high levels of habitat loss. This a similar, albeit less certain example: (Catastrophic events such as that forest once covered 1.2 million km2. multiple travellers reported an all-black at the end of the Cretaceous are Now only ~12% of it remains parrot, but no specimen exists [6]. understood to be exceptional.) This (Figure 1). A quarter of the remaining The 1648 Historia Naturalis Brasiliae comparison raises several questions: forest is found in fragments that are has more compelling evidence for how many recent extinctions might likely to be too small to hold viable historical extinctions [9]. This epic we have overlooked because species populations of most vertebrates [4,5]. eight-volume treatise, a pioneering disappeared before we could discover To answer our questions, we must attempt to catalogue Brazil’s vast them? How fast will extinctions happen understand the timelines of both biodiversity, was the product of in the near future and, in particular, habitat destruction and human efforts fi eldwork by the German and Dutch does habitat destruction precipitate to catalogue the region’s biodiversity. naturalists Georg Marcgrave and Willem extinctions at the rates theory predicts? We fi rst consider the region’s Piso in the then Dutch-controlled New studies from coastal Brazil provide ecological history [6]. Before European Northeast. Most of the bird species some answers to these questions. contact, the native indigenous depicted have been satisfactorily The common, widespread species peoples, the Tupi and Guarani, were identifi ed [10]. An exception is an were discovered long ago. Newly forest dwellers. They hunted mammals illustration and description of what discovered species typically have and birds for food and feathers, and is evidently a curassow of the genus very small geographical ranges and jaguars (Panther onca) for their skins, Crax with a yellow beak. Curassows tend to be very rare within those and they cleared and burned the are large terrestrial birds in four related ranges or located in remote regions forest — actions typical of indigenous genera. They are large and tasty [1]. The same will be true for as-yet forest dwellers in the Amazon today. and, consequently, of 16 species, undiscovered species. So, how fast As Dean [6] put it “one wonders […] the IUCN classifi es 12 as threatened do the ‘very rare’ species succumb to what was the impact upon the [forest] with extinction. Ornithologists have extinction? The IUCN ranks species of the continued extermination of not recorded a species of Crax in the into those that are of Least Concern, thousands of its largest predators.” Northern Mata Atlântica [11]. Thus, then Near Threatened, followed by For the purpose of this essay, we the plate and other paintings from the progressively more severely concentrate on birds. By the end of the same time (Figure 1), and oral threatened species in the categories the 18th century, taxonomists had testimonies from old hunters [11] are Vulnerable, Endangered and Critically described 17% of the approximately unambiguous evidence for either the Endangered [3]. This latter group is of 10,000 bird species known today. historic disappearance of a disjunct special concern. Many species are not Globally, there were 27 bird extinctions population of the similar-looking bare- only naturally rare but occur in places from 1500 to 1800 traced from sub- faced curassow (Crax fasciolata) or an with extreme habitat destruction and fossil bones, skins and a variety of undescribed species. degradation, where they survive, if other sources. The most famous of In the Mata Atlântica, species at all, in remnants of once extensive these is the dodo (Raphus cucullatus). discovery had a slow start: taxonomists habitats. These species are presumed This list continues to grow. The described only 14 of its 215 endemic to go extinct quickly, unless we make recent update of the IUCN Red List birds before 1800 (Figure 2), but extraordinary efforts to save them. has identifi ed 13 more bird species accelerated after 1815 when 111 Might we discover new species only to that went extinct after 1500, but new species were described in two Current Biology Vol 25 No 5 R178

A biogeographic provinces of the Mata Atlântica. Worst affected were the forests in the northeast beyond the São Francisco River in the states of Alagoas, Pernambuco, Paraíba and Rio Grande do Norte. Today, almost half (48%) of the remaining forest cover B there occurs in fragments smaller than 10 ha. Few patches exceed 1,000 ha, while just 3,731 ha are secured as strictly protected areas [4,5]. The pace of discovery and description of new species slowed after 1835: taxonomists described another 46 by the century’s end, then only 16 in the next 60 years (Figure 2). The fate of the 192 species known before 1960 is that one, the Alagoas curassow (Mitu mitu), is extinct in C the wild — it was last seen in the mid-1980s. Five more are Critically Endangered. One of these, the cherry- throated tanager (Nemosia rourei) occurs in just three forest patches and the Stresemann’s bristlefront (Merulaxis stresemanni) is now known from only one. How certain can we be that the three remaining species will survive? Conservation professionals are aware of the ‘Romeo and Juliet’ scenario — giving up on a species when it is not E F D actually lost. The safe thing is never to abandon hope and to continue searching in case one discovers a few survivors. However, the intense interest rare birds generate sets bounds on such optimism. Current Biology No one has reported the glaucous macaw (Anodorhynchus glaucus), Figure 1. Candidate continental avian extinctions from the Atlantic Forest. and purple-winged ground-dove Former limits of the Brazilian Atlantic Forest biome (light blue) with current forest remnants (Claravis geoffroyi) in the wild since (green) and representative missing species. (A) The last known Alagoas Foliage Gleaner 1951 and 2007, respectively. The Philydor novaesi (C. Albano). (B) Purple-winged ground doves Claravis geoffroyi (A.C. Lees © Natural History Museum Tring). (C) ‘Mituporanga’ Crax sp. (photo D. Teixeira painting by kinglet calyptura (Calyptura cristata) Albert Eckhout ca. 1610–1666 from Wikipeda Commons). (D) Glaucous Macaw Anodorhynchus was seen, but not photographed, glaucus (A.C. Lees © Natural History Museum Tring). (E) Kinglet Calyptura Calyptura cristata in 1996 after an absence of over (A.C. Lees © University Museum of Zoology, Cambridge). (F) The type specimen of Rio de 100 years. We have to go back far Janeiro Antwren Myrmotherula fl uminensis, the only evidence that this creature ever existed longer for unambiguous records of (A.C. Lees © Museu Paraense Emílio Goeldi). these species supported by physical evidence in the form of a specimen, decades. The problem is that by then was cheap and Brazil kept slaves until sound-recording or photograph. The this area had been under European 1888, keeping labour costs low. Dean WikiAves [12] database provides infl uence for over three centuries. Most [6] estimates that 18% of the province interesting insights into the species native peoples had been massacred, of Rio de Janeiro was cleared to grow recorded by the recently mobilized enslaved, or died from introduced coffee by 1888. As coffee planters army of Brazilian birdwatchers. diseases. Sugar cane — inevitably supposed that only primary forest was These three species have remained associated with enslaved Africans — suitable, much of the deforestation undocumented by the 20,112 may have consumed 7,500 km2 by was in mountains, areas previously participating bird photographers. That 1850, much of it in the Northeast [6]. spared. Plantations exhausted the soils is a telling comment, given that the Harder to assess were the impacts of after twenty years and more forest was site hosts over one million images gold and diamond mining and land cleared; many of the abandoned farms taken in the fi eld in Brazil, a citizen tenure practices that encouraged became cattle pastures. science milestone worth mentioning, burning then abandonment, resulting Rates of forest loss and degradation which has already produced some in the clearance of large areas. Land varied across the various discrete striking discoveries [13]. Magazine R179

60 This scenario recalls the nomadic this new species of treehunter. This passenger pigeon (Ectopistes ornithological detective work ﬁ nished 50 migratorius), the last individual of which in double tragedy. First, Juan died 40 died in captivity 100 years ago. The last tragically young before seeing the purple-winged ground dove may also description published. The species 30 have died in captivity. Several Brazilian now bears his name [19]. Second, 20 bird breeders kept the species up until a recent assessment [20] of the the 1980s but these populations were threatened birds of the forests of the 10 not maintained and died out [16]. north-east failed to ﬁ nd evidence

0 for the continued persistence of this Number of new bird descriptions 1750 1800 1850 1900 1950 2000 New species new treehunter (last seen in 2007), Decade Current Biology In the last few decades, the pace of the Alagoas Foliage-gleaner (Philydor taxonomic accumulation has quickened novaesi; described in 1983, last again as increasing numbers of seen in 2011) or the Pernambuco Figure 2. Decadal fl uctuations in the description of new bird species and their threat ornithologists and birdwatchers have pygmy-owl (Glaucidium mooreorum; status. explored new areas armed with better described in 2002, last seen in 2000). Number of endemic bird species described knowledge of avian vocalisations Conservationists working in north- from the Atlantic Forest biome per decade and molecular analysis toolkits. east Brazil suspect that all three are in the period 1750 to 2014. The number Taxonomists have described 17 species now likely to be extinct, and if any of threatened species (those in the IUCN in the last three decades, three in the individuals do persist their chance of categories Vulnerable, Endangered, Critically Endangered and Extinct in the Wild) is last year (Figure 2). Buzzetti et al. [17] long-term survival is remote. indicated in red. described the São Paulo marsh antwren In sum, recent publications allow (Formicivora paludicola) from wetlands us to consider the patterns of species Given the popularity of bird east of the city of São Paulo. Intensive discovery and ask whether we will photography in Brazil and the fact conservation efforts hope to secure fi nd species before they go extinct or that most of the Mata Atlântica these wetlands from more damage by only afterwards. The simple message and adjoining biomes are readily aggregate extractors, dam builders is that we are constantly adding to accessible, the best guess is that and reclamation. The Red List has not the totals of recently extinct species. the macaw, dove, and calyptura are yet formally evaluated its status, but As predicted from our knowledge now extinct. These extinctions add Buzzetti et al. [17] argue it should be of the effects of habitat destruction, to the increasingly well-documented classed as Critically Endangered. the populations of species the IUCN prediction that extensive habitat loss The Bahian mouse-colored tapaculo deems to be Critically Endangered are causes species extinction [1]. (Scytalopus gonzagai) also made its often too small to be viable. Conservation efforts do save bird debut in 2014 [18]. Tapaculos are Less expected is that we are adding species from extinction, but extinction small, unobtrusive and morphologically new species that, when discovered, can happen before any effective similar grey-brown birds. Novel vocal are so threatened that they survive measures, such as breeding in and molecular analyses allow better for only a few years. That we have captivity, can be implemented. Hunters understanding of species limits across these examples may be by good luck: exterminated the Alagoas currasows in South America. Taxonomists described we will surely have missed many the wild in the 1980s. A few wild-caught 9 of the 41 species of Scytalopus in the others. This renders global estimates birds at the end of the 1970s became last two decades. This latest discovery of extinction rates conservative [1]. the progenitors of a very successful came from the mountains of southern The survival of these global rarities captive breeding program, subject to Bahia. Although the taxon also awaits is dependent on the protection of intensive genetic management with formal evaluation, the authors propose remaining forests, a task no longer plans for future reintroduction [14]. that the species would easily qualify guaranteed amid the current climate The purple-winged ground dove for Endangered status. of downgrading, downsizing and (Figure 1) was not so lucky. The last, The last new species of 2014 was removing protection from existing undocumented report was made in the cryptic treehunter (Cichlocolaptes protected areas in Brazil [21]. 2007. It is one of the region’s three mazarbarnetti). This bird is very similar species reliant on mass-seeding of to the Alagoas foliage-gleaner (Philydor References bamboo [15]. The other two species novaesi; Figure 1), which occupied 1. Pimm, S.L., Jenkins, C.N., Abell, R., are seedeaters of the genus Sporophila the same forests in northeast Brazil. Brooks, T.M., Gittleman, J.L., Joppa, L.N., Raven, P.H., Roberts, C.M., and Sexton, J.O. and the Red List considers them Its discoverer, Juan Mazar Barnett, (2014). The biodiversity of species and their both Vulnerable. Periodic die-offs a brilliant Argentinian ornithologist, rates of extinction, distribution, and protection. of bamboo occur over hundreds of perceived vocal and structural Science 344, 1246752. http://dx.doi. org/10.1126/science.1246752. square kilometres following such differences amongst the few remaining 2. de Vos, J.M., Joppa, L.N., Gittleman, J.L., seeding events. Die-offs would Alagoas foliage-gleaners in their then Stephens, P.R., and Pimm, S.L. (2014). Estimating the normal background rate of not have posed a problem in pre- last two forest fragment redoubts. A species extinction. Conserv. Biol. http://dx.doi. Colombian forest landscapes, where new species was hiding in plain sight. org/10.1111/cobi.12380. birds could disperse long-distances Serendipitously, Juan checked the six 3. IUCN. (2014). The IUCN Red List of Threatened Species. Version 2014.2. http://www. through extensive forests to fi nd Alagoas foliage-gleaner specimens iucnredlist.org. new fl owering bamboo patches. In in the National Museum of Brazil 4. Ranta, P., Blom, T., Niemela, J., Joensuu, E., and Siitonen, M. (1998). The fragmented Atlantic rain today’s fragmented landscape, such and two collected in 1986 turned forest of Brazil: size, shape and distribution of nomadic behaviour is impossible [20]. out to be misidentifi ed specimens of forest fragments. Biodivers. Conserv. 7, 385–403. Current Biology Vol 25 No 5 R180

5. Ribeiro, M.C., Metzger, J.P., Martensen, A.C., subject. That experience paved the and Ponzoni, F.J. (2009). The Brazilian Atlantic Q & A Forest: How much is left, and how is the way for a PhD in animal behaviour. remaining forest distributed? Implications for conservation. Biol. Conserv. 142, 1141–1153. As a second generation ethologist 6. Dean, W. (1996). With Broadax and Firebrand: The Destruction of the Brazilian Atlantic Forest. Patrick Bateson did you know the Nobel laureates University of California Press, California. Niko Tinbergen and Konrad Lorenz? 7. Fowlie, M. (2014). News Release: One tenth of bird species fl ying under the conservation As an undergraduate at Cambridge, When I was still an undergraduate, radar. http://www.iucnredlist.org/news/ Patrick Bateson worked on the Ivory I went with three friends to the high one-tenth-of-bird-species-fl ying-under-the- Gull in Spitsbergen and was much Arctic to work on the rare Ivory Gull. conservation-radar. 8. Wiley, J.W., and Kirwan, G.M. (2013). The infl uenced by Niko Tinbergen. After Niko Tinbergen was working on a extinct Macaws of the West Indies with a fi nishing a degree in Zoology, he did a comparative survey of gulls at the time special reference to Cuban Macaw, Ara tricolor. Bull. Brit. Orn. Cl. 133, 125 3–156. PhD on behavioural imprinting under and wanted to come with us. He gave 9 Piso, G., and Marcgrave, G. (1648). Historia Robert Hinde. He spent two years in us a lot of help both in preparing our naturalis Brasiliae auspicio et benefi cio California as a Harkness Fellow with expedition and in writing up what we illustriss. I. Mauritii Com. Nassau illius provinciae et maris summi praefecti adornata. the neuropsychologist Karl Pribram, had discovered later. Sadly a serious Etc.: i–viii, 1–122, (1–2), i–iii, 1–292, (1–2), and then returned to Cambridge ulcer prevented him from joining fi gs.— Amsterdam. 10. Teixeira, D.M. (1990). As fontes do paraiso-um where he stayed until he retired. He us. My initial plan was to work for a ensaio sobre a ornitologia no Brasil Holandês was Director of the Sub-Department doctorate under Niko, but in the end (1624-1654). Rev. Nord. Biol. 7, 1–149. of Animal Behaviour and later became I stayed on in Cambridge to work on 11. Teixeira, D.M. (1986). The avifauna of the northeastern Brazilian Atlantic Forest: a case of Provost of King’s College, Cambridge. behavioural imprinting in birds under mass extinction? Ibis 128, 167–168. He was the Biological Secretary and the supervision of Robert Hinde. 12. WikiAves (2014). Wiki Aves - A Enciclopédia das Aves do Brasil. http://www.wikiaves.com.br/ Vice-President of the Royal Society, As my doctoral research progressed, 13. Lees, A.C., and Martin, R.W. (2014). Exposing and then President of the Zoological I became more and more convinced hidden endemism in a Neotropical forest Society of London. His research has that imprinting shared many features raptor using citizen science. Ibis. http://dx.doi. org/10.1111/ibi.12207. been focused on the development of with perceptual learning and that 14. Sousa, L.M.S.A., Laganaro, N.M., behaviour. He has also been involved in Konrad Lorenz’s claim that imprinting de Camargo, C., Davanço, P.V., de Oliveira, Jr., P.R., Azeredo, R.M., Silveira, L.F., improving the welfare of animals. was a special form of learning was and Francisco, M.R. (2013). Microsatellite wrong. Still a graduate student, I markers for detecting hybrids between the When did you fi rst show interest in described my experiments at an extinct in the wild Alagoas Curassow (Pauxi mitu) and Razor-billed Curassow (P. tuberosa) biology? From a very early age, I told international conference in 1963. (Aves, Galliformes). Conserv. Genet. Resour. 5, anybody who asked that I wanted to Lorenz was sitting in the front row of 181–183. 15. Areta, J.I., and Cockle, K.L. (2012). A be a ‘biologist’ without having any the audience. He became increasingly theoretical framework for understanding clear idea what that might entail. I had angry. At the end of my talk he got the ecology and conservation of bamboo- a very good teacher who gave me, as up and said “I’m going to direct my specialist birds. J. Ornithol. 153, 163–170. 16. Silveira, L.F., and Straube, F.C. (2008). Aves a fi ve year old, a love of natural history. remarks not to you, but to Robert ameaçadas de extinção no Brasil. p.379–666. But another reason was that I had a Hinde”. In: A.B.M., Machado, G.M. Drummond, and A.P. Paglia (eds.). Livro Vermelo da Fauna Brasileira kinsman who was an eminent biologist: Subsequently I was asked to give Ameaçada de Extinção. Ministério do Meio William Bateson, who, as one of the a plenary lecture at the Ethology Ambiente/Fundação Biodiversitas, Brasília. champions of Gregor Mendel, coined conference in 1967. Konrad Lorenz 17. Buzzetti, D.R.C., Belmonte-Lopes, R., Reinert, B.L., Silveira, L.F., and Bornschein, M.R. (2013). the term ‘genetics’. He was a cousin of was in the chair and was studiously A new species of Formicivora Swainson, 1824 my grandfather and had died 12 years polite. Although my relations with him (Thamnophilidae) from the state of Sao Paulo, Brazil. Rev. Bras. Ornitol. 21, 269–291. before I was born, but the family was never fully recovered after my talk four 18. Maurício, G.N., Belmonte-Lopes, R., evidently very proud of him and often years before, it was obvious to me Pacheco, J.F., Silveira, L.F., Whitney, B.M., referred to him. that he was a man of enormous charm and Bornschein, M.R. (2014). Taxonomy of “Mouse-colored Tapaculos”(II): An endangered In my teens, I spent several and charisma. It is hard to believe that new species from the montane Atlantic Forest holidays at a bird observatory on the ethology would have achieved what it of southern Bahia, Brazil (Passeriformes: Rhinocryptidae: Scytalopus). Auk 131, 643–659. Northumberland coast which launched did without Konrad Lorenz or indeed 19. Barnett, J.M., and Buzzetti, D.R.C. (2014). A my interest in ornithology. I was told Niko Tinbergen, who exerted a strong new species of Cichlocolaptes Reichenbach that I could go on to do something infl uence on me throughout my career. 1853 (Furnariidae), the ‘gritador-do-nordeste’, an undescribed trace of the fading bird life of called a P H D involving the study of Nevertheless, the subject was moving northeastern Brazil. Rev. Bras. Ornitol. 22, 75–94. birds in depth. I had little idea of what into a much more rigorous phase than 20. Periera, G.A., Dantas, S.M., Silveira, L.F., Roda, S.A., Albano, C., Sonntag, F.A., Leal, S., that meant at that time, but it sounded in its early days. Many of the classical Periquito, M.C., Malacco, G.B., and Lees, A.C. like heaven and I set my heart on doing examples that fi gured so strongly in the (2014). Status of the globally threatened forest research on birds. fi rst text books on animal behaviour birds of northeast Brazil. Pap. Avul. Zool. 54, 177–194. When interviewed for an would not pass editorial scrutiny in the 21. Bernard, E., Penna, L., and Araújo, E. (2014). undergraduate place at Cambridge, 21st century. Lorenz used to say: “If I Downgrading, downsizing, degazettement, and reclassifi cation of protected areas in Brazil. I was told briskly that birds only have one good example, I don’t give Conserv. Biol. 28, 939–950. took up two weeks in the second a fi g for statistics”. Small samples, year. However, I was admitted, read non-independence of measurements 1 Museu Paraense Emílio Goeldi, CP 399, Natural Sciences and in my third year (when measurements were made), Av. Perimetral, 1901, Terra Firme, 66077-530 I specialized in Zoology. Finally I was naïve or improper use of statistics Belém, Pará, Brazil. 2Nicholas School of the Environment, Duke University, Durham, doing what I wanted to do since I was (when statistics were used), lack of North Carolina 27708, USA. a child. It was wonderful to be able to adequate controls (when experiments *E-mail: [email protected] think critically and creatively about the were carried out), not conducting Current Biology Correction

Species, extinct before we know them?

Alexander C. Lees and Stuart L. Pimm* *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2015.03.001

(Current Biology 25, R177–R180; March 2, 2015) Due to a production error, the legends for Figure 1 panels B and C in this Essay were reversed, as were the legends for Figure 1 panels D and E. The ﬁgure and its correct legends are shown here. The journal apologizes for the error.

E F D

Current Biology

Figure 1. Candidate Continental Avian Extinctions from the Atlantic Forest Former limits of the Brazilian Atlantic Forest biome (light blue) with current forest remnants (green) and representative missing species. (A) The last known Alagoas foliage-gleaner Philydor novaesi (C. Albano). (B) ‘‘Mituporanga’’ Crax sp. (D. Teixeira photo of Albert Eckhout painting ca. 1610–1666; Wikimedia Commons). (C) Purple-winged ground doves Claravis geoffroyi (A.C. Lees ª Natural History Museum Tring). (D) Kinglet calyptura Calyptura cristata (A.C. Lees ª University Museum of Zoology, Cambridge). (E) Glaucous macaw Anodorhynchus glaucus (A.C. Lees ª Natural History Museum Tring). (F) The type specimen of Rio de Janeiro antwren Myrmotherula ﬂuminensis, the only evidence that this creature ever existed (A.C. Lees ª Museu Paraense Emı´lio Goeldi).