By G. J. F. P u g h Department o f Botany, University o f Nottingham
(Received for publication on April 10, 1966)
I ntroduction
It is well established that numerous fungi are carried by birds, and it has long l»en suspected that birds transport plant pathogenic organisms. Tiffany, Gilman and Murphy (1955) examined the fungi which occurred on birds associated with wilted oaks, while Kouyeas and Anastassiadis (1962) showed that magpies, by building nests con taining diseased twigs in healthy trees, can bring about the spread of “ Mai Secco,” a die-back disease of Citrus trees. Fungi pathogenic to animals including man have also been sought on birds. Geese have been examined for Aspergillus fumigatus. causal agent of “ asper gillosis,” by Sladen and Austwick (1957), and geese and gulls have been investigated by Beer (1963). More recently a search has been made for keratinophilic fungi on feathers removed from living birds (Pugh, 1964, 1965), and in nest material (Pugh, 1966 a). Keratinophilic fungi are all potentially pathogenic to man, and include the dermato phytes. Other human pathogens associated with birds have been discussed by Furcolow, Tosh, Larsh, Lynch and Shaw (1961) and by Partridge and Winner (1965).
M a ter ia ls a n d M e t h o d s
The feathers used in this survey were removed directly from the breast and underparts of birds obtained in the Madras area. The feathers were placed in sterile envelopes, on which details about the bird were noted. Some of the birds (the golden plovers and the stints) were obtained from trappers in the Kerambakka region immediately after they were caught. The remainder were sampled in Moore Market, Madras. These birds had been in captivity for some time, possibly one or two days, and were kept in cages while waiting to be sold. This factor may have produced some unknown contamination of the birds. However, the birds were kept in cages with other members of the same species; so although there may have been some cross-contamination between birds of the same species it is less likely that other species
* Birds were identified using “ The book of Indian birds” by Salim Ali, Bombay Natural History Society, J964. Identifications were checked when posdMe by comparison with specimens in the Natural History Section of Madras Museum. would have been affected. Of fifteen Mynas sampled, three (20%) yielded no fungi, so contaminaton could not have been a very impor tant factor. Mynas, parakeets, partridges and quails were sampled from each of several cages, while the crow pheasants and manias were obtained from diiferent cages. In this way it is hoped that the fungal flora obtained from the feathers was representative of the flora on these birds in their natural habitats. In addition to the feathers taken from birds, some unidentifiable feathers were collected at the bird sanctuary at Vedanthangal. In the laboratory, feathers from each bird were placed in a damp chamber consisting of a Petri dish lined with filter-paper which was moistened with sterile water. The large feathers from Vedanthangal were cut up and incubated separately. After incubation at room temperature (about 26° C.) for 3-4 weeks the Petri dishes were exa mined for fungal growth. Fungi able to decompose cellulose were found growing on the filter-paper, and those able to attack keratin and other substances were found on the feathers. Fast-growing fungi which use simple soluble carbohydrates were not able to grow under the conditions used. The birds used in this survey are listed in Table 1. Samples were obtained from eleven species, which are classified in six orders; (i) Galliformes, including partridges, quails and red spurfowl. These birds feed on the ground, mainly on seeds and grain. (ii) Cluradriiformes, including golden plovers and stints, which are waders, feeding on various small animals (insects, snails, crabs) in paddy fields and other wet areas. (iii) Columbiformes: the dove, which is another ground feeder, mainly using seeds and grain. (iv) Psittaciformes: the parakeets, which feed on seeds and fruits amongst the foliage. (v) Cuculiformes: the crow pheasant, which feeds on the ground’ mainly on insects and small animals. (vi) Passeriformes, including the Black drongo. which feeds on insects in flight and on the ground, and also on nectar; the munia, which eats seeds on the ground and on the plant; and the mynas, which are omnivorous, feeding mainly on the ground. The great majority of the birds sampled feed on the ground, and mainly eat seeds and fruits.
R esu lts The fungi recorded arc listed alphabetically in Table 1. Of the cellulose decomposers the most frequently recorded fungi were Chaetomium spp. (mostly C.globoxum), followed by Curvularia lunata, which was the predominant species, Aspergillus spp. and Memnoniella S Distribution o f fungi on birds caught near Madras. The figures given
Partridge— Q uail- Spurfowl — Plover- Stint— FraiKoliiua Calidrix pmduerianus Cotnrmx Galloperdix Phwiali) spp. spadUea dominiea temmenciii (?)
AlUrttaria tenuis .. 0 • 3
Atptriillus 1 2 ■ .. 1
BipoUris sp, .. •• .. 2 1 Chidomium bmtrychodet .. .. 1 2 .. 1 1 C. ilatitm ......
C. ^lohosnm .. 3 .. 1
ChryKtporimn spp. .. » ft • « 2 2
Cladoiporium htrlninim ,, • • .• 1 Citnoniyces serratns .. 3 2 ..,.
Cun ularia lunata .. 1 1 .. I • • 5 .. jt ■ 1 .. Menmnnietta echinata 1 2 • • Myrothedum rmdum .. j .. Afyxotrichum «p. ..! 1 i , I .... Papularia sphtcrinptrma .. j .. 1 •• i •• ; 1 Trickoderma viride .. 1 ![ 1 ,. t Sterile hjpha; ., ) Birds with nu fungi .. .. 1 .. C
; 1 Number of fungi .. 0 16 1 » 12 Numtjfr of binis .. 7 j 8 1 7 lU
Average No. of fungi per bird 1-5 1 2-0 1 1-3 0-7 i refer to the number of times each fungus was recorded on each bird
■ 1 ■ Crow Black Dove— Piiisk«et- Myna— Monia— j _ , % of Strefttfelia Pheas«nt — PtiUacula Acriihtkeres Drongo— birds chinttiHs Ctntrapu! spp. tristis Dicrurui with tinensis aJsimiJii fun|u8 I 1 i 1 I ' 6 7.fl ■■ ' I .. 1 8 1 1 17-9
• • .. i I 1 .. 4-6
• • 1 ! 2 1 B 1 ' 1 I 32-8 1 1 S 2 15 1
• t •• •• \ 1 J3 ie-4
• « 1 I l-r. ^ * 1 1i ; i 1 * • ^ 0 1 8.« 1 • • 1 ,, 2 9 ! ! 2C-4
« < 1 ; 2 ! B 13-4 j 1 1 1-6
• • • • ' 1 l.fl
• • .. • • 1 1-0
• • 2 i 3-0 * 1 1 • ♦ : 1 ; i 3 ;I 4-5 , 1 1 « • ! ' 3 ‘ .. 1 9 ,, i
3 3 i 13 22 : 3 5 ' 9B ,, I 2 7 IS 1 2 87 i » 1-5 ]•» 1-5 i 3 2-5 1-4 1 1 1 •• echinata. Aspergillus, most often found on Mynas, and Chaetomium, most often found on parakeets, were each obtained from seven different bird species; Memnoniella was present on six, while Curvularia was found on four, and was especially common on mynas and plovers. The keratin decomposers were represented by Chrysosporium spp., found on five bird species and especially on partridges and quails, and by Ctenomyces serratus, cleistothecia of which were found on partridges, quails and spurfowl. A surprisingly large number of stints (35%) and mynas (20%) yielded no fungi, while the single drongo and the dove had more fungi on them than did the other birds. In general the number of fungi per bird was rather small. There was a basic similarity in the fungal flora recorded on the birds, and this, perhaps, was to be expected as the birds were mostly ground-feeding seed-eaters. In this survey it was not possible to examine the distribution of fungi in relation to different feeding habits. The 18 feathers collected at Vedanthangal had a sparse fungal flora. Fungi were present on seven, of which four were Chrysosporium spp. and the remainder were sterile hyphae. All seven isolates occurred on dark-coloured feathers, while the while and light-coloured feathers showed no fungal growth despite a careful scarch.
D isc u ssio n [n a survey of ccllulolytic and keratinophilic fungi on birds in Britain, Pugh (1965) found that Penicillium spp. occurred on the widest range of birds, and were the most frequently encountered fungi. Oidiodendron spp. were almost as widespread in occurrence although they were much less common than Penicillium. Arthroderma curreyi, Chaetomium spp., Chrysosporium spp. and Cladosporium lierbarum were all fairly often recorded. This distribution is markedly different from the present results, in which Chaetomium spp. were widespread and most frequently isolated. C. globosum, however, was the most common species of this genus in both areas. Aspergillus spp., Chryso sporium spp., Curvularia lunata and Memnoniella echinata were all fairly abundantly represented on Indian birds. Aspergillus spp., occurring on almost 18% of the Indian birds, was much more abundant than in Britain, where it was found on 12% of the birds. There was no dominant species of Aspergillus in the Indian results, whereas in Britain, A.fumigatus was the most frequently recorded species. Curvularia and Memnoniella were not found on the British birds, while Chryso sporium was almost equally represented, being present on 19-4% of the Indian birds, and 20% of those in Britain. The suggestion (Pugh, 1965) that because the fungi recorded in Britain are cosmopolitan there may well be quantitative differences on birds from other parts of the world appears to have been justified. More important, however, are the large qualitative differences which have now been established. Much more work will have to be carried out before it can be known if these quantitative and qualitative dif ferences in mycoflora can be used to plot possible migration paths, as has been done by Ash, HopeJones and Melville (1961) using the pollen masses found on the beaks and head feathers of migrating birds. The main migrants examined, the golden plovers and stints, yielded a flora essentially similar to that found on indigenous birds, except that a large percentage of stints had no fungi on their feathers. Presumably migrants would have to be sampled before they had become contaminated by the local flora at their destination, as fungal propagules generally arc not as sticky as pollen masses. The numbers of fungi found on the birds were relatively smaller than in Britain. There, the average number of isolates per bird was 2-3 (1093 isolates on 470 birds) compared with an average of 1-4 on the Indian birds (96 isolates on 67 birds). This may reflect the very dry state of the vegetation in January, 1966, when sporulation of fungi would probably be much less than on wet material. A corres ponding investigation on birds caught during the monsoon could well produce a different balance between the fungi recorded, especially if hyaline-spored forms were then able to grow and sporulate. Such forms were much less frequently found than were the dark-spored fungi which are more resistant to desiccation and strong light. Tn Britain, the majority of fungi recorded were members of the Xerosporae, and the same pattern appears here. These dry, wind- dispersed spores would also tend to be more prevalent in very dry areas, and it would be interesting to sec if members of the Gloiosporae, with water-dispersed, slimy spores also became more abundant during monsoon conditions. When the cellulolytic fungi found on the birds are compared with those found in soils from the same area (Pugh, 1966 A) Chaetomium and Curvularia are seen to form a larger percentage of the total fungi on birds than in the soil, and Memnoniella was recorded only on birds. Fungi which were relatively more abundant in the soil included Alter- naria, Aspergillus, fusarium, Humlcola, Myrothecium, Penicillium and Thielavia. These differences may reflect in part the habits of the birds, but also may be indicative of the normal distribution of the fungi, i.e., on the surface litter rather than in the soil or vice versa: for example, it may be significant that there were seven isolates of Chaetomium on the seven parakeets sampled, as these birds normally feed in the foliage rather than on the ground: similarly Memnoniella w&s found on a range of ground feeding birds, but was not recorded in the soils which were sampled. No fungi known to be pathogenic to man were found during this survey. However, the keratinophilic fungi were represented by Chrysosporium spp., found on five different bird species, and Cteno- myces serratus. Cleistothecia of this heterothallic sjwies were found on partridges, quails and spurfowl. Of the sixteen birds in this Order which were sampled, eight (50%) yielded Chrysosporium, and six (35%) ^ield^ Ctenomyces. The only previous record of Ctenomyces on a bird was also on a partridge (Pugh, 1965). Just as Arthroderma curreyi seems to have an affinity for birds of the genus Turdus, so Ctenomyces appears to be associated with members of the Galliformes. It is not known whether or not A', curreyi or C. serratus grow actively on the birds. Their presence on these birds and not on others with the same general habitat and similar feeding habits would suggest some selective association. Pugh (1965) has pointed out that circumstantial evidence suggests that humidity conditions on the bird’s surface approach a level suitable for fungal growth, as bird lice, in vitro, grow at relative humidities close to the lower limit for fungal growth. It has been found that some of the non-blood-sucking lice have fun^l spores present in their crops, along with feather debris. The active life of ccrtain of these lice is confined to birds, so if hyphal fragments were to be found in their crops, this would be indirect evidence of the growth of fungi on the bird.
Remarkably few data are available about actual conditions between the skin and the covering feathers on birds. It is impoitant that the bird surface microhabitat should be fully investigated, especially as it represents a field where ornithologists, parasitologists and myco logists could profitably co-operate.
S um m a ry
Feathers have been obtained from birds caught in the Madias area, and incubated in moist chambers. Chaetomium spp., Curvu- laria lunata. Aspergillus spp. and Memnonietla echinata were the most frequently found cellulolytic species. Chrysosporium spp. and Cteno myces serratus, the only keratinophilic fungi recorded, appear to have an affinity for partridges and quails. The fungi recorded have been compared with those found in soils collected near Madras, and with those recorded on birds sampled in Britain.
A cknowledgements
I would like to express my deep appreciation to Professor T. S. Sadasivan for his most generous help and hospitality; to the British Council for financial assistance: to the Univetsity of Madras for its hospitality; and to the University of Nottingham for granting leave of absence. Thanks are also due to Mr. Moses for his help in obtaining the birds, and to Mr. V. Arjuna Rao for technical assistance.
R eferences
A sh , 1. S., H o pe-Jones, P. a n d M elville, R. 1961. The contamination of birds with pollen and other substances. Br. Birds 54 : 93-100. Bee«, J. V. 1963. The incidence of Aspergillus fumigatus in the throats of wild ^$e and ^Us. Sabouraudia 2 : 238-47, F u r c o l o w , M. L., T o sh , F. E,, L a rs h , H. W.. L v n c h , H. J. a n d S h aw , G. 1961. T he emerging pattern of urban Histoplasmosis. New Eiigl. J. Med. 264: 1226-30.
K o uyeas, V. AND A nastassiauis, B. 1962. Dissemination of Druterophoma tracheiphila by (he common magpie (Pica pica l„). Annls. Inst, phvtopalh. Benaki N.S., 4 ; 52-55. '
Pa r tr id g e, B. M. a n d W in n er , H. 1. 1965. Cryptucoccus neoformans in bird droppings in London. Lancet: 1060-61. Pugh, G. J. F. 1964. Dispersal of Arthroderma curreyi by birds, and its role in the soil. Sahourmdia 3: 275-78. 1965. Cellulolytic and keratinophilic fungi recorded on birds. Ibid. 4 : 85-91. ------, 1966 a. Associations between birds’ nests, their pH, and kcratinophilic fungi. Ibid. 5: 49-53. 1966 6. Cellulose decomposing fungi isolated from soils near Madras. /. Indian hot. Soc. 45 : 232-41.
T iffa n y , L. H., G ilm a n , J. C. and Murfhv, D. R. 1955. Fungi from birds asso ciated with wilted oaks in Iowa. Iowa St. Coll. J. Sci. 29; 659-706.