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Around the world, amphibians are

vanishing, even rom seeminglypristine areas and among

the actors that studies have tied to thedisappearances are disease and climatechange. Because o the climate link, rogs

have become a symbol o extinctionrisk rom global warming, their charmradiating hauntingly rom ront covers omagazines and newspapers rom Natureand Newsweek to The Washington Postand The New York Times, their urgentmessage reaching millions. Awarenesso the rogs plight and its signiicanceincreased in January 2006, when weand a dozen colleagues presentedevidence that climate change is loadingthe dice or disease outbreaks leadingto disappearances o harlequin rogs(the genusAtelopus) across Central

and South America1

. A new study byLips et al.2, however, has challengedthis link, claiming instead that thedramatic losses can be chalked up towhat the authors say is a lone killer:the chytrid ungus Batrachochytriumdendrobatidis. Is there, as one journalistsuggested, a cautionary tale3 hereabout leaving behind the caveatspertaining to scientiic indings whiletheir deinitive elements continue toreverberate? We think not. Resiting theevidence in this scientiic equivalent othe board game Clue4, we deduce that

global warming is a key actor in theextinction crisis.Just as viewers o the 1985 comedy

ilm version o Clue saw dierentendings depending on the theatre theyattended, readers who want to knowwhy harlequin rogs are vanishingind dierent answers depending onthe journal article they peruse. Inthe board game, known as Cluedo inEurope, the cards deining the answerto a murder mystery are kept in a secretcase-ile envelope, and the playerstrying to crack the case move about therooms o a Gothic mansion in search

o clues. The science in the case o themissing harlequin rogs, like this boardgame, involves deductive reasoningand dice rolling. But the scientists usecomputers, o course, to roll the dicetens o thousands o times. Followingsuch an approach, we ound that thedisappearances o harlequin rogs havecome on the heels o unusually warm

years much more oten than chance alonewould dictate1,5. Disagreeing with thisresult, Lips et al. have shown their cards2.

But in this game the stakes are highor everyone. What matters is not whothe winner is, but what the truth is aboutwhy the rogs are vanishing. Globalwarming has long been a suspect in thedisappearances, and it may conspirewith various other culprits, such aslandscape alteration, pollution andthe presence o exotic species5. Thescience, thereore, must go beyond thegame o Clue, in which only a singlekiller is identiied. Around the world,

climate change is stirring up ecologyin diverse ways, ampliying the risko extinction or many plants andanimals, and threatening the integrityo the living systems that are vital tohuman well-being6.

Humanity must decide whether this isa crisis in the here and now, demandingprompt action, or just a nebulousproblem or the uture. Some experts earthat the unvarnished truth will rightenpeople into inaction. We believe thatthe acts, combined with an inspiring

vision o the solutions, can transormwait-and-see attitudes into cries oraction. Journalistic balancing acts suchas talk o a new climate centrism7 areamong the most dangerous games everinvented. I the rogs, who do not give acroak about the let or the right, had a

voice in the matter, they would not singpraise to a alse middle ground.

MULTIPLE SUSPECTS

Does the case o the missing harlequinrogs attest to the urgency o reducinggreenhouse gas concentrations? Sitingthrough the evidence in the case, weconsider existing clues as we search ornew ones. We ollow the game o Cluein spirit, but we go beyond it as well,

visiting several mansions ar rom theAmerican tropics (by secret-passage

travel, o course, to reduce our carbonootprint). As in the game, we also watchthe other players to see where they goand where they do not go.

According to the paradigm putorward by Lips et al. the chytridungus operates alone, invading healthyamphibian communities and causingimmediate die-os, irrespective ochanges in the physical environment.But had they taken account o someclues rom Australia8, they might havequestioned whether this is the wholestory. Frogs in Queensland experiencedincreasing developmental instability,

Beware the lone killerJ. ALAN POUNDS AND LUIS A. COLOMA

Why are harlequin frogs disappearing across the American tropics? A resifting of the evidence

backs up the conclusion that global warming is a key conspirator in the losses.

Onores harlequin frog (Atelopus onorei) of

the Andes mountains in Ecuador is among the

scores ofAtelopusspecies that have vanished in

recent decades1.

L.

A.

COLOMA

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CARTOONBOOK

1949 first edition of Clue.

which is evidence o stress, at least twoyears beore they suered chytrid-relateddeclines. Whats more, the major die-osthere coincided with dramatic regionalwarming that mirrored the global trend.

Clues rom Italy again imply thatthe chytrid is not a lone killer9. Findingsrom Umbria, which Lips et al. also

disregarded, indicate that this unguswas common in rogs, in a previouslyunknown orm that did not cause disease,or at least several years beore it laredup in an epidemic o chytridiomycosis.And when it did, during the 2003 heatwave, a parasitic mesomycetozoeanprotist,Amphibiocystidium ranae , alsowent on the march in the same hostpopulations. This observation agreeswith the evidence that shiting climaticconditions may give an edge to variousrog pathogens5,9.

Likewise, other studies that we

cited in a brie overview5 point toclimate change as an important actor inthe amphibian crisis. Lips et al. however,paid them no heed. For instance, datarom the south o England show thatrising temperatures are degradingtoads body condition, along with theirreproductive success and survivorship10.This inding, which hints at an increasingsusceptibility to disease, has been called asmoking gun11 or the impacts o globalwarming on amphibians.

Is there danger in the air? AsSherlock Holmes said in The Adventure

o the Speckled Band, We have not amoment to lose. Departing the areawhere the toads were studied10, whichlies just north o the chalky Purbeck Hillsin south Dorset, and not ar rom whereClue originated, we head northeastto Cambridge.

Arriving there, we go to the librarythat houses the work o Lips et al. The

study is also reely available online2.But regardless o how one accesses it,beware deception by the seeminglyobvious. Some o the moves in agame o Clue may conound the other

players making them believe, orexample, that a certain card is in thesecret envelope when actually it is not.Even the most intelligent players canbecome conused.

Lips et al. were soon called out12,however, or violating a sacred ruleo deductive logic: avoid circularity.Hypothesizing that the chytrids arrivalspells immediate doom or manyharlequin rogs, the authors used theestimated date o their decline to inerwhen the chytrid arrived at the variousplaces that have been studied. They

envisaged these shock-and-awe arrivalsas a consequence o the microbesintroduction in several places,

ollowed in each case bya wavelike spread, which

they mapped by simplyadding smaller waves untilthe patterns made sense.

The result is an untested,and perhaps untestable,model o pathogen spread,

and only one o variouspossibilities. Contrary to the

authors claims, this colourul montagedemonstrates nothing.

And even i the chytrid is spreadingin a wavelike ashion, what does this tellus? Who can say that such dynamicsare incompatible with the occurrenceo climate-linked epidemics? Indeed,

researchers studying the ebola virus inArica have ound evidence or bothkinds o patterns13. Because a wavelikespread does not necessarily indicate alone killer, Lips et al. may be riding thewave2 to the wrong conclusion.

FALSE ACQUITTAL

As we continue our search in thelibrary, something odd makes itspresence known. And it is not thesmoke o strong Indian cigars thestarting point o an important clue in

The Adventure o the Speckled Band.In this case, the evaluation o ouranalyses by Lips et al. does not smellquite right.

The authors claimed to reute thelink between unusually warm years androg disappearances: by adding randomerror to the data, they said, they wereable to make the patterns go away2. It wasquickly pointed out, however, that thisapproach is invalid12. By adding enougherror to the relevant data, one couldmake some o the most harmul things onEarth appear harmless even the energypolicies o the Bush administration.

Figure 1 Mean difference between the reported date of decline of each harlequin frog species and the lastyear in which it was observed. The three means (AC) are for three different data sets adapted from Table 1

of Lips et al.2; error bars show standard error. Lips et al. claimed that a large time gap (A) revealed a great

deal of sampling error in data representing the last year of observation of the various species. The use of last

observations, however, is appropriate only for species that have disappeared. For this subset of species, the mean

difference is relatively small (B), and it is even smaller after some striking errors in Table 1 are corrected (C).

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Lips et al. added error to dataindicating the year in which each rogspecies was observed or the last time.We had used these data as an indexo the timing o sudden populationdeclines leading to disappearances, andwe ound that large-scale temperaturetended to peak the year beore the

last observation1,5. Lips et al. argued,however, that the declines oten tookplace long beorehand, and they usedthis to justiy their addition o error.Examining, or such cases, data that theypresented in their Table 1, they calculatedan average gap o 11.2 years between theestimated date o decline and the last yearo observation.

This suggestion is astonishing rom abiological standpoint. Irrespective o theparadigm that one embraces, the recentcatastrophic declines have oten led torapid disappearances. Species with small

geographic ranges, which are especiallyvulnerable to extinction and accountor a large proportion o the missingharlequin rogs, should thereore beexpected to disappear quickly. So whywould they oten still persist more than adecade ater such a catastrophe?

The answer is that they generallydo not. Lips et al. erred in theircalculations, in part because theyincluded species that, by their owncriteria, have not gone missing. Weexplicitly ocused on disappearances1.Although some o the species that still

survive have indeed declined seriously,one cannot assume that all o thereported declines are equally catastrophicand due to the same causes. And mostsigniicantly, the last year o observationo a species that is still surviving tells uslittle other than when researchers last

visited its habitat.In our original paper1, we repeated

the analysis, adding the species thathad declined severely and had gonemissing or ive years or more but werelater rediscovered in small numbers.Substituting, or these species, the last

year in which each was observed beore itdisappeared temporarily, we again ounda tendency or the disappearances toollow unusually warm years.

The ocus by Lips et al. on a set ospecies that is inappropriate to the taskat hand explains most, but not all, othe erroneous 11.2-year gap (Fig. 1).Another part o this alse discrepancyrelects some large errors in theirTable 1. We have not ully reviewedthe data in this Table . In many cases,their origin is mysterious, even whenthey supposedly came rom our ownpublications. Nevertheless, some o

the errors are striking. For example,Costa Ricas Central Cordillera harlequinrog (Atelopus senex) was seen or the lasttime in 1986, yet Lips et al. claimed thatit was ound as recently as 2004. PerhapsProessor Plum, who in the Clue bookseries was notoriously absent-minded,would have done no better.

So what happens when a player makesa alse accusation? In the present case,this means laying the blame on thechytrid ungus and calling or theacquittal o global warming withoutsound basis. According to the oicialrules o Clue, that player is sidelinedor the rest o the game. But plentyremains to be investigated, and Lipsand colleagues have done some valuabledetective work in the past showing,or example, that the chytrid doesbelong in the line-up wherever rogsgo missing. We would thereore be

willing to waive the rules (but not letthe wave rule) i Lips et al. concede thatthis ungus is not a lone killer and thatclimate change, along with several otherorms o environmental deterioration, isa key actor in many cases.

Published online: 24 April 2008

doi:10.1038/climate.2008.37

References

1. Pounds, J. A. et al.Nature439, 161167 (2006).

2. Lips, K. R., Difendorer, J., Mendelson, J. R. III & Sears, M. W.

PLoS Biol.6, e72 (2008).

3. Revkin, A. C. Dot Earth 24 March 2008;

http://dotearth.blogs.nytimes.com/2008/03/24/vanishing-rogs-climate-and-the-ront-page/

4. Revkin, A. C. New York Times 25 March 2008;

http://www.nytimes.com/2008/03/25/science/25rog.html

5. Pounds, J. A. et al.Nature447, E5E6 (2007).

6. IPCC. Climate Change 2007: Impacts, adaptation, and

vulnerability. Report o Working Group II to the Fourth

Assessment Report o the Intergovernmental Panel on Climate

(Cambridge Univ. Press, 2007);

http://www.ipcc.ch/ipccreports/ar4-wg2.htm

7. Tobis, M. Only In It or the Gold13 November 2007;

http://initorthegold.blogspot.com/2007/11/reply-to-revkin.html

8. Alord, R. A., Bradeld, K. S. & Richards, S. J.

Nature447, E3E4 (2007).

9. Di Rosa, I., Simoncelli, F., Fagotti, A. & Pascolini, R.

Nature447, E4E5 (2007).

10. Reading, C. J. Oecologia151, 125131 (2007).

11. Fisher, M. C.Animal Conserv.

10, 420421 (2007).12. Parmesan, C. & Singer M. C. Responses, PLoS Biol.

28 March 2008; http://biology.plosjournals.org/perlserv/

?request=read-response&doi=10.1371/journal.pbio.0060072

13. Pinzon, J. et al.Am. J. Trop. Med. Hyg.

71, 664674 (2004).

J. Alan Pounds is Resident Scientist atthe Tropical Science Centers MonteverdeCloud Forest Preserve in Costa Rica, andLuis A. Coloma is Proessor o Biology andCurator o Herpetology, Museo de Zoologa,Escuela de Biologa, Pontifcia UniversidadCatlica del Ecuador.e-mail: goldtoad@racsa.co.cr orlcoloma@puce.edu.ec

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