Avian Chemical Defense: Toxic Birds Not of a Feather
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Corrections BIOPHYSICS. For the article ‘‘Molecular spectroscopy and dynam- CELL BIOLOGY. For the article ‘‘SEM1, a homologue of the split ics of intrinsically fluorescent proteins: Coral red (dsRed) and hand͞split foot malformation candidate gene Dss1, regulates yellow (Citrine)’’ by Ahmed A. Heikal, Samuel T. Hess, Geoffrey exocytosis and pseudohyphal differentiation in yeast’’ by Jussi S. Baird, Roger Y. Tsien, and Watt W. Webb , which appeared Ja¨ntti,Johanna Lahdenranta, Vesa M. Olkkonen, Hans So¨der- in number 22, October 24, 2000, of Proc. Natl. Acad. Sci. USA lund, and Sirkka Kera¨nen,which appeared in number 3, Feb- (97, 11996–12001), the authors note the following corrections. ruary 2, 1999, of Proc. Natl. Acad. Sci. USA (96, 909–914), the authors note the following correction. In Results under the 1. Eq. 1 on page 11997, line 16 from the top of the left-hand subheading ‘‘SEM1 Is Not Essential for Growth or Invertase column is written as: Secretion,’’ the sentences ‘‘Disruption or deletion of SEM1 did not cause any obvious growth defects at different temperatures 1 1 1 0.5 ͑͒ ϭ ͩ ͪͩ ͪ on synthetic or rich media containing different carbon sources. G ϩ ͞ ϩ ͞2 N 1 D 1 D We conclude that SEM1 is a single-copy gene nonessential for growth,’’ should read ‘‘Disruption or deletion of SEM1 did not m 1 Ϫ ͞ cause any obvious growth defects at different temperatures on ⅐ ͑ Ϫ ϩ r i͒ ͑ Ϫ ͒ 1 fi fie , [1] synthetic or rich media. However, deletion of SEM1 caused poor 1 fi i ϭ 1 growth on rich media when the sole carbon source was glycerol or galactose.’’ but the equation should read: Correction published online before print: Proc. Natl. Acad. Sci. USA, 10.1073͞ pnas.011532098. Text and publication date are at www.pnas.org͞cgi͞doi͞10.1073͞ 1 1 1 0.5 ͑͒ ϭ ͩ ͪͩ ͪ pnas.011532098 G ϩ ͞ ϩ ͞2 N 1 D 1 D m COLLOQUIUM. For the article ‘‘Hair cell recovery in mitotically 1 Ϫ͞ ⅐ ͑ Ϫ ϩ i͒ blocked cultures of the bullfrog saccule’’ by Richard A. Baird, ͑ Ϫ ͒ 1 fi fie , [1] 1 fi i ϭ 1 Miriam D. Burton, David S. Fashena, and Rebecca A. Naeger, which appeared in number 22, October 24, 2000, of Proc. Natl. 2. On page 11998, lines 25 and 27 from the top of the left-hand Acad. Sci. USA (97, 11722–11729), the authors note the following CORRECTIONS column state: corrections. The author and affiliation lines should read: ϭ ϭ Ϯ ⌽ ϭ Ϯ ϫ Ϫ3 † ‡ At kex 514 nm, f1 0.42 0.06 and 1 1.3 0.3 10 , Richard A. Baird* , Miriam D. Burton*, Anna Lysakowski , suggesting that the quantum yield for the reverse photocon- David S. Fashena*, and Rebecca A. Naeger* version is kex dependent. *Fay and Carl Simons Center for Biology of Hearing and Deafness, Central The sentence should read: Institute for the Deaf, 4560 Clayton Road, St. Louis, MO 63110; and ‡Department of Anatomy and Cell Biology, University of Illinois ϭ ϭ Ϯ ⌽ ϭ Ϯ ϫ Ϫ3 At ex 514 nm, f1 0.42 0.06 and 1 1.3 0.3 10 , at Chicago, Chicago, IL 60612 suggesting that the quantum yield for the reverse photocon- Additionally, the acknowledgments should have thanked S. D. version is ex dependent. Price for technical assistance. 3. On page 12000, line 19 from the top of the right-hand column, †To whom reprint requests should be addressed. E-mail: [email protected]. ‘‘( Ϸ 1 ϫ 10Ϫ3⅐kgmϪ1⅐sϪ1)’’ should read ‘‘( Ϸ 1 ϫ 10Ϫ3 kgmϪ1⅐sϪ1),’’ and EVOLUTION. For the article ‘‘Independent adaptation to riverine 4. In Summary on page 12001, line 11 from the top of the habitats allowed survival of ancient cetacean lineages’’ by Insa right-hand column, ‘‘(on 10Ϫ6⅐10Ϫ11-s time scale)’’ should Cassens, Saverio Vicario, Victor G. Waddell, Heather Bal- read ‘‘(on 10Ϫ6–10Ϫ11 s time scale).’’ chowsky, Daniel Van Belle, Wang Ding, Chen Fan, R. S. Lal Mohan, Paulo C. Simo˜es-Lopes, Ricardo Bastida, Axel Meyer, Michael J. Stanhope, and Michel C. Milinkovitch, which ap- COMMENTARY. For the article ‘‘Avian chemical defense: Toxic peared in number 21, October 10, 2000, of Proc. Natl. Acad. Sci. birds not of a feather,’’ by Paul J. Weldon, which appeared in USA (97, 11343–11347), the authors note the following. “We number 24, November 21, 2000, of Proc. Natl. Acad. Sci. USA apologize that acknowledgment to Manuel Garcia Hartmann for (97, 12948–12949), the following corrections should be noted. tissue samples was inadvertently omitted from the published Due to a printer’s error, ‘‘homobatrachotoxinin’’ and ‘‘batra- article.” chotoxinin’’ were incorrectly inserted in place of ‘‘homobatra- Correction published online before print: Proc. Natl. Acad. Sci. USA, 10.1073͞ chotoxin’’ and ‘‘batrachotoxin,’’ respectively. The term ‘‘batra- pnas.011532198. Text and publication date are at www.pnas.org͞cgi͞doi͞10.1073͞ chotoxinin-A’’ was correct in the article. pnas.011532198 PNAS ͉ December 19, 2000 ͉ vol. 97 ͉ no. 26 ͉ 14831 Downloaded by guest on October 1, 2021 Commentary Avian chemical defense: Toxic birds not of a feather Paul J. Weldon Conservation and Research Center, Smithsonian Institution, 1500 Remount Road, Front Royal, VA 22630 n 1992, Dumbacher et al. (1) substan- Itially altered prevailing views of avian physiology, biochemistry, and chemical ecology with their report of the potent neurotoxin homobatrachotoxinin in feathers and other tissues of several spe- cies of New Guinean passerine birds of the genus Pitohui. Their discovery was signif- icant not only for suggesting a protective mechanism rarely considered for birds (i.e., chemical defense) but for the nature of the compound they discovered, a struc- turally complex alkaloid that binds Naϩ channels and depolarizes electrogenic membranes. Alkaloids in tetrapods gen- erally had been thought to be confined to amphibians, whose skins have long been acknowledged as arsenals of these biolog- Fig. 1. Hornets (Vespa orientalis) attacking a freshly skinned carcass of a laughing dove (Steptopelia ically active compounds (2). Indeed, be- senegalensis)(Left) while ignoring that of a pied kingfisher (Ceryle rudis). This observation prompted H. B. fore its discovery in Pitohui, homobatra- Cott (4) to undertake an extensive investigation of avian chemical defense. [Reproduced with permission chotoxinin, a member of a family of from ref. 4 (Copyright 1947, The Zoological Society of London).] steroidal alkaloids called batrachotoxinins (BTXs), had been found only in skin se- cretions of Central and South American dichrous), the most toxic of the birds they An additional enigma described by poison-dart frogs (Dendrobatidae) of the examined, is aposematic and may be Dumbacher et al. (3) is the profound genus Phyllobates. In this issue of PNAS, mimicked by the variable pitohui (P. differences observed in the concentra- Dumbacher et al. (3) identify in birds the kirhocephalus) in parts of its range. tions of BTXs among species and popu- three major alkaloids that occur in these This year, Dumbacher et al. (3) docu- lations. Indeed, more comparative data on frogs: homobatrachotoxinin, batracho- ment additional toxic species of New toxin abundances among populations may toxinin, and their synthetic precursor, ba- Guinean birds and additional BTXs, some be needed to ascertain just what the spe- trachotoxinin-A. of which are newly described from nature. cies-typical toxins are and at what levels Birds, in fact, had not escaped notice Newly documented among Pitohui are a they occur. Within the genus Pitohui, P. as bearers of defensive chemicals before series of BTXs, including four novel alka- dichrous and P. kirhocephalus contained Dumbacher et al.’s investigations. While loids. All but one of these compounds, the highest amounts of BTXs, although collecting and skinning birds in Egypt batrachotoxinin-A 3Ј-hydroxypentanoate, some individuals from some populations during 1941, the naturalist H. B. Cott (4) occur in the newly featured toxic bird, the were devoid of toxins. Trace or minor noted that hornets (Vespa orientalis) ar- blue-capped ifrita (Ifrita kowaldi), a mo- amounts of some BTXs were detected in riving on the scene differentially con- notypic species restricted to high montane the crested pitohui (P. cristatus) and the sumed the avian carcasses that he had rainforests (Ͼ1,500 m). black pitohui (P. nigrescens); however, discarded (Fig. 1). Stimulated by this Ifrita, which as adults are approximately these compounds were not observed in the observation, Cott conducted an exten- 35 g, forages around tree trunks and few samples obtained from either the sive series of experiments on the palat- probes for insects in moss and under rusty pitohui (P. ferrugineus) or the white- ability of bird flesh to hornets and do- branches. It overlaps little, if at all, geo- bellied pitohui (P. incertus). Individuals of mesticated cats. In addition, he examined graphically with the much larger (65–100 Ifrita ranged from harboring no detectable the literature and queried field biologists g) species of Pitohui, which are omnivo- to assess the acceptability of various toxins to containing major quantities of all birds for human consumption. The im- rous and occur throughout the vegeta- five of the BTXs that have been detected pression of widespread unpalatability tional column in lower forests down to sea from this species. One of two specimens of that emerged from these studies inspired level. The taxonomic position of Ifrita is the little shrike-thrush (Colluricincla me- Cott to assert that conspicuous plumage problematic, but systematists at least garhyncha, Pachycephalidae) possessed might evolve as an aposematic feature agree that it belongs to a family other than trace amounts of only batrachotoxinin-A; signaling the distastefulness of birds to the Pachycephalidae, which contains Pito- several other pachycephalids contained predators.