Paul J. Weldon

Natural products from the integument of nonavian reptiles

This review describes the epidermal and glandular chemistry of nonavian reptiles in relation to proposed functions, and includes more than 170 references. The results are presented according to the different reptile taxa.

Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys ( Cebus spp.)

Neotropical monkeys of the genus Cebus anoint themselves by rubbing arthropods and plants against their pelage. A recent study has shown that free-ranging wedge-capped capuchin monkeys (C. olivaceus) in Venezuela self-anoint with a benzoquinone-secreting millipede, an activity by which they are hypothesized to appropriate chemical deterrents of mosquitoes. To evaluate the plausibility of this hypothesis, female yellow fever mosquitoes (Aedes aegypti) were presented with two millipede secretory compounds, 2-methyl-1,4-benzoquinone and 2-methoxy-3-methyl-1,4-benzoquinone, on nylon-reinforced silicone membranes placed over wells filled with human blood, a highly preferred food. Mosquitoes exhibited fewer landings, fed less frequently, and flew more frequently (a possible indication of repellency) in the presence of membranes treated with benzoquinones than with controls. These compounds also elicit self-anointing in captive male and female tufted (C. apella) and white-faced (C. capucinus) capuchin monkeys.

A survey of birds odorous or unpalatable to humans: Possible indications of chemical defense

We solicited information from field and museum ornithologists on the birds that they consider odorous and/or unpalatable in order to identify species that may use chemicals to deter predators. Ninety-two ornithologists from the Americas and Eastern Europe responded to our survey. Eighty genera and 10 families representing 17 orders, primarily Procellariiformes, Falconiformes, Psittaciformes, Cuculiformes, Piciformes, and Passeriformes, were cited as containing malodorous or uniquely odorous birds. Two orders (Opisthocomiformes and Trogoniformes), five families (Procellariidae, Cuculidae, Bucconidae, Picidae, and Furnriidae), and one subfamily (Drepanidinae) were reported to us as either containing many odorous species or consisting primarily of them. Thirty genera and three families representing 13 orders, primarily Passeriformes, were reported to us as unpalatable. The birds cited in our survey and those previously reported as odorous and/or unpalatable are tabulated. Our survey and review point to a number of taxa that may use chemicals to deter predators, although we acknowledge that compounds imparting aversive or unique odors or flavors may arise for a variety of reasons, e.g., as dietary by-products.

Defensive anointing: extended chemical phenotype and unorthodox ecology

Many animals acquire substances on their integument from heterospecifics through anointing. In active or self-anointing, animals rub against scent sources or they apply them by appendage or mouth. In passive anointing, animals adsorb emitted chemicals. Most investigators suggest that chemicals appropriated via anointing deter predators, ectoparasites, and/or microbial pathogens. Similarly, nesting birds and brood parasites of social insects acquire chemicals from and reside unmolested near or within insect colonies. The acquisition through anointing of chemicals that deter predators, ectoparasites, microbial pathogens, and other offenders, i.e. defensive anointing, constitutes an “extended phenotype”: the genetic machinery by which defensive compounds are synthesized does not reside with the anointing organisms, but the sensory mechanisms and/or behavioral tendencies by which chemicals are appropriated from heterospecifics do. The ecological relationships between anointing organisms and “chemical donors,” and between ”chemical donors” and those responding to chemicals appropriated via anointing, may be unorthodox. Interactions between anointing organisms and chemical donors typically entail abrasive contact with or other damage to the latter. These encounters sometimes are evidenced by telltale marks on chemical donors or by chemicals deposited on the integument of anointing organisms. The organisms furnishing chemicals and those affected by them may not interact, and they may even occupy different habitats, because mobile anointing organisms are the medium by which chemicals are disseminated. Thus, in allelochemical studies where anointing is involved, species can be tested, with ecological legitimacy, using chemicals from organisms they might fail to interact with in nature. Practical implications of anointing stem from its potential importance in conservation and captive management, where consideration is given to the protection that animals derive by accessing topically acquired chemicals from heterospecifics.Summary.Many animals acquire substances on their integument from heterospecificsnthrough anointing. In active or self-anointing, animals rub against scent nsources or they apply them by appendage or mouth. In passive anointing, animalsnadsorb emitted chemicals. Most investigators suggest that chemicals appropriatednvia anointing deter predators, ectoparasites, and/or microbial pathogens. Similarly,nnesting birds and brood parasites of social insects acquire chemicals from and residenunmolested near or within insect colonies. The acquisition through anointing of nchemicals that deter predators, ectoparasites, microbial pathogens, and other noffenders, i.e. defensive anointing, constitutes an “extended phenotype”: the ngenetic machinery by which defensive compounds are synthesized does not reside withnthe anointing organisms, but the sensory mechanisms and/or behavioral tendencies bynwhich chemicals are appropriated from heterospecifics do. The ecological nrelationships between anointing organisms and “chemical donors,” and between n”chemical donors” and those responding to chemicals appropriated via anointing, maynbe unorthodox. Interactions between anointing organisms and chemical donors typicallynentail abrasive contact with or other damage to the latter. These encounters sometimesnare evidenced by telltale marks on chemical donors or by chemicals deposited on the nintegument of anointing organisms. The organisms furnishing chemicals and those naffected by them may not interact, and they may even occupy different habitats, becausenmobile anointing organisms are the medium by which chemicals are disseminated. Thus,nin allelochemical studies where anointing is involved, species can be tested, with necological legitimacy, using chemicals from organisms they might fail to interact withnin nature. Practical implications of anointing stem from its potential importance innconservation and captive management, where consideration is given to the protectionnthat animals derive by accessing topically acquired chemicals from heterospecifics.

Volatile components in dorsal gland secretions of the collared peccary, Tayassu tajacu (Tayassuidae, Mammalia)

Secretions of the dorsal gland of free-ranging adult male and female collared peccaries (Tayassu tajacu) were analyzed by gas chromatography-mass spectrometry. Both sexes contain (2E,6E,10E)-geranylgeraniol; squalene (allE isomer); and the following isomers of springene, a diterpene homolog of β-farnesene: (3E,6E,10E)-α-springene, (3Z,6E,10E)-α-springene, and (6E,10E)-β-springene. A diterpene alcohol and an additional isomer each of squalene and springene also were observed. Straight- and branched-chain esters abound in the secretions of females, but they were not detected in males.

The scent of the reticulated giraffe (Giraffa camelopardalis reticulata)

The giraffe (Giraffa camelopardalis) emits a scent that can be detected by humans over considerable distances. Dichloromethane extracts of hair samples from adult male and female reticulated giraffes (G. c. reticulata) were analysed by gas chromatography–mass spectrometry. Two highly odoriferous compounds, indole and 3-methylindole, identified in these extracts appear to be primarily responsible for the giraffe’s strong scent. Other major compounds identified were octane, benzaldehyde, heptanal, octanal, nonanal, p-cresol, tetradecanoic acid, hexadecanoic acid, and 3,5-androstadien-17-one; the last compound has not previously been identified from a natural source. These compounds may deter microorganisms or ectoparasitic arthropods. Most of these compounds are known to possess bacteriostatic or fungistatic properties against mammalian skin pathogens or other microorganisms. The levels of p-cresol in giraffe hair are sufficient to repel some ticks. uf6d9 2002 Elsevier Science Ltd. All rights reserved.

Venom of the slow loris: sequence similarity of prosimian skin gland protein and Fel d 1 cat allergen

Bites inflicted on humans by the slow loris (Nycticebus coucang), a prosimian from Indonesia, are painful and elicit anaphylaxis. Toxins from N. coucang are thought to originate in the brachial organ, a naked, gland-laden area of skin situated on the flexor surface of the arm that is licked during grooming. We isolated a major component of the brachial organ secretions from N. coucang, an approximately 18xa0kDa protein composed of two 70–90 amino-acid chains linked by one or more disulfide bonds. The N-termini of these peptide chains exhibit nearly 70% sequence similarity (37% identity, chain 1; 54% identity, chain 2) with the two chains of Fel d 1, the major allergen from the domestic cat (Felis catus). The extensive sequence similarity between the brachial organ component of N. coucang and the cat allergen suggests that they exhibit immunogenic cross-reactivity. This work clarifies the chemical nature of the brachial organ exudate and suggests a possible mode of action underlying the noxious effects of slow loris bites.

Volatile components in dorsal gland secretions of the white-lipped peccary, Tayassu pecari, from Bolivia

Secretions from the dorsal gland of male and female free-ranging adult white-lipped peccaries (Tayassu pecari) from Bolivia were analyzed by gas chromatography–mass spectrometry. Fifty compounds were identified, some provisionally. Secretions of both sexes contain saturated and unsaturated C5–C18 carboxylic acids as well as isomers of the diterpene springene. The females secretions uniquely possess farnesyl esters of C8 and C10 carboxylic acids, whereas the males secretions uniquely showed two compounds provisionally identified as monounsaturated C16 lactones. Saturated high-molecular-weight esters of C10 carboxylic acids are more abundant in the females secretions than in those of the males. The secretions of both sexes also contain monoalkanoate esters of methylhydroquinone as major components.

Nuisance arthropods, nonhost odors, and vertebrate chemical aposematism

Mosquitoes, ticks, and other ectoparasitic arthropods use chemoreception to avoid vertebrates that are known or presumed to be dangerous or otherwise unprofitable hosts. Nonhosts may belong to a species that is regularly unaccepted or one that includes both accepted and unaccepted individuals. A diverse array of qualities including immunocompetence, vigilant grooming behavior, mechanical inaccessibility, and toxicity have been proposed as the features that render vertebrate chemical emitters unsuitable as hosts for arthropods. In addition to advantages accrued by ectoparasitic arthropods that avoid nonhosts, vertebrates that are not accepted as hosts benefit by evading injurious ectoparasites and the infectious agents they transmit. The conferral of advantages to both chemical receivers (ectoparasitic arthropods) and emitters (unpreferred vertebrates) in these interactions renders nonhost odors aposematic. Chemical aposematism involving ectoparasites selects for vertebrates that emit distinctive odors. In addition, chemical mimicry, where vulnerable organisms benefit when misidentified as nonhosts, may be accommodated by duped ectoparasites.

Composition of the Cloacal Gland Secretion of Tuatara, Sphenodon punctatus

The lipophilic content of the cloacal gland secretion of the tuatara (Sphenodon punctatus) was investigated. GC/EI-MS Analysis of CH2Cl2 extracts of the secretions revealed triacylglycerols as major glandular constituents. Twelve major medium-chain fatty acids were found to be conjugated to glycerol in different combinations, resulting in complex mixtures. These acids were identified by transesterification and subsequent derivatization of natural samples, and their structures were verified by synthesis. The natural glycerides contain predominantly three of the following acids: octanoic (A), (E)- and (Z)-oct-4-enoic (B and C, resp.), (4E,6Z)-octa-4,6-dienoic (tuataric acid; D), (R)-2,6-dimethylheptanoic (E), (R)-2,6-dimethylhept-5-enoic (F), (Z)-dec-4-enoic (G), (4Z,7Z)-deca-4,7-dienoic (H), (R)-3,7-dimethyloct-6-enoic (I), (R)-4,8-dimethylnon-7-enoic (J), (2R,6S)-2,6,10-trimethylundec-9-enoic (K), and (2R,5E)-2,6,10-trimethylundeca-5,9-dienoic acids (L). Several additional acids, occurring in trace amounts only, were tentatively identified by MS. The elucidation of the absolute configuration of the acids was performed by GC on chiral phases. Individual tuatara show specific mixtures of glycerides with up to 100 components. The individual mixtures may permit individual recognition because the bouquets seem to be stable over years.