(236) PROTOCALLIPHORA IN BIRDS' NESTS. (Edward Grey Institute, Oxford.)

Transcription

1 (236) PROTOCALLIPHORA IN BIRDS' NESTS. BV D. f. OWEN. (Edward Grey Institute, Oxford.) INTRODUCTION. DIPTEROUS flies of the genus Protocalliphora belong- to the Calliphoridae, a family in which most species are carrion-feeders. In this genus the larvae are ecto-parasites of nestling birds. The adult flies lay eggs in birds' nests and when the larvae hatch they periodically attach themselves, by means of a suction pad on the first segment, to some part of a nestling and suck its blood. When fully grown the larvae pupate in the bottom of the nest and the flies emerge in about 10 days. At least some species of Protoccdliphora are double-brooded. In the British Isles only one species, P. azurea, occurs. It is widespread, but there are few accounts of its occurrence, probably as few observers critically examine nests once the young have flown. The density of Protocalliphora may vary considerably, for instance in 1952 I examined 41 nests of tits at Wytham near Oxford and found larvae and/or pupae in twenty nests, in numbers ranging from 2 to 70 per nest. In 1953 only one nest out of 85 contained pupae. In 1952 one brood of Great Tits (Parus major) died at the age of twelve days and the nest was found to contain 70 Protocalliphora pupae. However, it was by no means certain that this fly was the cause of death. Apart from this there was no indication that the birds had suffered, the weights just before fledging were as high as those of birds whose nests were not infested. In 1953 at Wytham three Magpies (Pica pica) hatched from a clutch of seven eggs on May 20th: the remaining eggs were infertile. It was noted that the nestlings were not growing as rapidly as those in other nests in the vicinity which had hatched at the same time. On June 4th the smallest of the three young was found dead in the nest. The second bird died on June 7th and an examination of the surface of the stomach of the remaining bird revealed six Protocalliphora larvae firmly attached to the skin and apparently sucking blood. There were clots of blood present and the skin appeared hard and dry. The larvae were removed, but when the nest was visited about an hour later more were attached to the stomach. On June 9th this bird was found dead beneath the nest. The nest was then examined and in the lining of the base were about 250 Protocalliphora larvae. Both parent birds were seen alive after the death of the nestlings, which were fed as frequently as at other nests and on the usual food. Other broods of Magpies in the area were successful, indicating that food was not specially short.

2 VOL. XLVII] PROTOCALLIPHORA IN BIRDS' NESTS. 237 The death of this brood prompted me to search through the literature for further records. The results are summarized in this paper. EUROPEAN RECORDS. There are comparatively few records of the occurrence of Protocalliphora in the nests of British birds, and even fewer instances of the death of one or more of a brood. A list of British host records has been given by Audcent (1942) and by Rothschild and Clay (1952). These and others have been listed in the appendix at the end of this paper. Boyd (1935) has recorded the larvae from nests of the Swallow (Hirundo rustica), and suggests that the death of one or more of the nestlings in a brood might have been due to the presence of this fly. However, availability of food is also a possible factor in such a case. I. J. Ferguson-Lees (in litt.) found that in one year (1951) three nests of the Dunnock (Prunella modularis) were infested with larvae and that the young in two of these nests died. In both Cases the young were well below the average weight for their age at the time of their death. Rothschild and Clay (1952) record 373 larvae in a Magpie's nest where the young survived. Elsewhere in Europe, Lohrl (1949) found that 15 out of 69 nests of the Collared Flycatcher (Muscicapa albicollis) were infested with Protocalliphora, and that young in 9 of these nests died. Other European records have been given by Sperling (1935), Eichler (1936, 1937) and Seguy (1941, 1946). In Britain another fly, Neottiophillutn praeustutn (Neottiophilidae), has similar habits to Protocalliphora, but appears to be much more local. It has been recorded mainly from the nests of Passerines, particularly warblers, thrushes, finches and crows (Rothschild and Clay, 1952). AMERICAN RECORDS. In America there has been considerable interest in the possible effects of Protocalliphora on birds and there are many references in the literature. The life history of the American species has been described by Coutant (1915), but since then the genus has been reviewed by Shannon and Dobroscky (1924), and recently by Hall (1948), who recognises 10 species and places them in the genus Apaulina, thus separating them from the European species, which remain in the genus Protocalliphora. However, all are closely related and apparently show no host specificity, and in this paper they will be referred to as Protocalliphora, irrespective of the species. Most of the records come from bird-ringers, and some of the literature, together with that on other bird parasites, has been summarized by Boyd (1951). One of the earliest references to what must be Protocalliphora is given by Henshaw (1908) who records dipterous larvae from

3 238 BRITISH BIRDS. [VOL. XLVII. two broods of Bluebirds (Sialia sialis), which eventually died. Plath (1919a, 1919b, 1919c) made some observations on the numbers of Protocalliphora. He examined 63 nests of six species of Passerines and found that 39 were infested with an average of 47 larvae or pupae in each nest. Some mortality of the nestlings was recorded and he observed that many pupae were parasitized by a chalcid, Nasonia brevicornis. Many other records have been given by Johnson {1925, 1927, 1930, 1931, 1932), particularly for Tree Swallows (Iridoprocne bicolor) and Bluebirds. He found that both birds and parasites were double-brooded, and that many more second brood nests were infested than those earlier in the season. Heavy mortality was found among Bluebirds. Exceptionally heavy mortality among nestling Mourning Doves (Zenaidura macroura) was found by Neff (1945). Only in 18 out of 100 nests did the young reach an age suitable for ringing, and the others were said to have died as the result of Protocalliphora infestation. It was found that the nestlings always fell out of the nests just before dying and that the number of larvae in each nest varied between 20 and 86. Some of the larvae were parasitized by chalcids. In a study of the life history of the Bank Swallow (Sand Martin) [Riparia riparia) Stoner (1936) states that during five seasons he handled hundreds of nestlings and found that less than half a dozen were infected by Protocalliphora. However, in a later year he found many infested nests at the same colony, but although some birds seemed considerably distressed by the presence of the larvae, none died. Like other observers, he found that late nests and second broods were more heavily infested than the early ones. This was partly due to an increase in the fly population due to the hatching of a new brood, and partly to the smaller number of nests available later in the year. Lincoln (1931) found Protocalliphora in the nests of the (Barn) Swallow (Hirundo rustica) as well as the Bank Swallow. Some of the larvae were found on the eyelids and in the throat and nostrils of the nestlings. George and Mitchell (1948) found larvae in the nests of the Hermit Thrush {Hylocichla guttata), Chipping Sparrow (Spizella passerina), Song Sparrow (Melospisa melodia), and (American) Redstart (Setophaga ruticilla), usually only three to four larvae in each nest, except in the Redstart where 30 were found. The single bird in this nest eventually died and the cause was thought to have been the larvae of Protocalliphora. Also one brood of Chipping Sparrows were below weight. A more detailed account of Protocalliphora in nests has been given by Mason (1936, 1944). Larvae were found in the nests of several species of Passerines, especially Bluebirds (94 per cent of all nests infected) and Tree Swallows (82 per cent of all nests infected). Some mortality occurred, but it was not always possible to relate the death of a brood to a large number of larvae in the nest. For instance in several nests which held only a few larvae the birds died, yet in one Tree Swallow's nest 430 larvae

4 VOL. XLVII] PROTOCALLIPHORA IN BIRDS' NESTS. 239 were found and the young survived. In order to save some broods, the nests were removed and the parasites destroyed. Hand made nests were then substituted, but after four years it was found that Protocalliphora had increased in the area. Very large numbers of pupae were parasitized by a chalcid, Mormoniella vitripennis*. Other records of Protocalliphora in the nests of Passerines have been given by Arnold (1919), Dobroscky (1925), McAtee (1927, 1929, 1940), Storer (1929), Chapman (1935), Jellison and Philip ( I 933)> Thomas (1936), Guberlet and Hotson (1940) and Pletsch (1948). In one nest of the Mountain Chickadee (Penthestes gambeli) (Thomas, loc. cit.) 100 larvae and pupae were found, but the young survived. There are a number of records of Protocalliphora in the nests of birds of prey, but there is no mention of mortality. In most cases the larvae were found in the ear and nasal cavities (Burtch, 1920; Shannon and Dobroscky, 1924; Sargent, 1938; Hill and Work, 1947 ; and Hill, 1948). OTHER RECORDS. Chisholm (1952) has reviewed the literature on the association of birds and insects in Australia, and has included a short discussion on the dipterous parasite Passeromyia longicornis, which has similar habits to Protocalliphora. This species also appears to be a nest-scavenger, but so far the information is very incomplete. It was first recorded by Gilbert (1919) who found larvae in the nests of the Lyre Bird [Menura superba), White-cheeked Honey-eater (Meliornis serica), White-bearded Honey-eater (M. novae-hollandice) and Tawny-crowned Honey-eater (Glyciphila fulvifrons). The eggs were apparently laid on the nestlings and the larvae took six days to mature. No mortality was recorded, but some of the young were in a bad condition. Hindwood (1930) recorded the same species from the nest of a Goldfinch (Carduelis carduelis) and a Brush Wattle Bird (Anthochcera chrysoptera). In the latter 51 larvae and pupae were found in one nest which contained a single nestling. The larvae were of several different sizes which suggests that more than one fly had laid in the nest. There are other Australian records of fly larvae in the nests of other birds, but the species have not been ascertained. Taylor (1949) found another related species in the nests of 4 species of passerines in South Africa. One brood of Cape Robins (tossypha caffra) died. Other African records have been given by Seguy (1946). THE EFFECT OF PROTOCALLIPHORA ON BIRDS. In some of the references to Protocalliphora in birds' nests the death of one or more of the nestlings has been recorded, in others the nestlings have been found to be underweight or in a bad * This chalcid has been found as a parasite on dipterous pupae in Swallows' nests in Scotland and England (see, antea, vol. xxx, p. no). EDS.

5 240 BRITISH BIRDS. [VOL. XLVII. condition. Other records refer to larvae in the nest, often in large numbers, without apparent harm to the nestlings. It seems likely that the number of cases in which mortality has been found is exaggerated, as observers are much more.likely to search for a cause when nestlings die than to search every nest they find for parasites. For Protocalliphora to survive in a nest it is necessary for the hosts to remain alive, at least until the larvae are full grown and ready to pupate. Plath (1919b) found that partially grown larvae did not survive if the host was removed. Possibly if the nestlings died just before fledging the fly larvae would be able to live for a time on the bodies of their hosts, but if the larvae caused the death of the birds at an early age, their food supply would soon be exhausted and they would then die. It follows from this that the adult Protocalliphora flies must not lay too many eggs in one nest, as the resulting larvae would use up the food supply too quickly. Presumably the adult flies are in some way able to recognise whether or not the nest has already been visited by one of their own species. One of the causes of early mortality in some broods might be that more than one fly has laid eggs in a nest with the result that there are too many larvae. The eggs of Protocalliphora must be laid at the correct time. First, there must be,a general correlation between the breeding season of the birds and the breeding season of the parasites, but this need not be very precise as the fly does not appear to be in any way host-specific, though as discussed later, there is possibly selection for certain types of nest. It is more important that the adult flies should be able to select nests where the young are of suitable size, for if the young are well grown it is possible that they might fledge before the larvae are ready to pupate. A large number of records of Protocalliphora in birds' nests are for hole-nesting species, or species which build compact nests with a solid base. It has been suggested that the flies select this type of nest as the larvae are less likely to fall out, but it also seems likely, as suggested by Thomas (1936), that in open nests the parasites fall out when about to pupate and so when these are examined after the birds have fledged they appear not to have been parasitized. This was found for the Mourning Dove (Neff, 1945). Many hole-nesters also have longer fledging-periods than open-nesting species and this might give Protocalliphora a greater chance of survival if the larvae were late in hatching. Before it is possible to say whether a brood of birds has died as the result of the presence of Protocalliphora larvae certain other important factors must be known. A large number of larvae or pupae in a nest does not necessarily mean that the birds are suffering to any great extent, for as already shown, many larvae may be present without apparent distress to the birds. It seems that in most cases other factors contribute towards the eventual death of the birds. For instance, one of the parents may have met with

6 VOL. XLVII] PROTOCALLIPHORA IN BIRDS* NESTS. 241 an accident or may have deserted the nest. This might mean that the nestlings would get less food and would then stand less chance of recovering from the attacks of Protocalliphora. Also food might be scarce and the parents might be unable to feed the birds frequently enough to satisfy their needs, and the addition of Protocalliphora might cause death whereas had the food supply been better the nestlings would have been able to cope with the parasites. Could food shortage have contributed towards the high mortality of Mourning Doves recorded by Neff (1945)? Yet another possibility is that the brood might have been reduced either by predation or by the failure of some of the eggs to hatch, in which case more larvae would have to feed from each nestling. Possibly this occurred in the case of the (American) Redstart where the brood contained only one nestling which eventually died (George and Mitchell, 1948). Thus it would appear that as Protocalliphora exists mainly on living birds, mortality of the host is exceptional and possibly always linked with other factors. Further data, such as the number of parasites in each nest, the number of nests parasitized in relation to the number not affected, the species parasitized, and any records of the death of the young, particularly if other possible mortality factors are known, might help to solve some of the problems suggested in this paper. Sometimes when Protocalliphora larvae have been carefully examined they have been found to be parasitized in considerable numbers by chalcids. It is possible that these are important in controlling their numbers, but further study is required here. SUMMARY. 1. The habits of Protocalliphora, a genus of flies whose larvae are parasitic on nestling birds, are briefly described. A record is given of a brood of Magpies dying as the result of these parasites. 2. Many American references, some of which refer to the death of broods of birds, are summarized. European and other records are also given. 3. The similarity between the breeding seasons of the birds and those of the parasites is discussed. 4. It is suggested that as the parasites depend on living birds, only exceptionally will their hosts die. In many cases where mortality has been recorded, other factors, such as food shortage, might have been involved. APPENDIX. A LIST OF THE HOSTS OF PROTOCALLIPHORA AZUREA IN BRITAIN. Skylark (Alauda arvensis) Robin (Erithacus rubecula) Swallow (Hirundo rustica) Blackcap (Sylvia atricapilla) House Martin (Delichon urbica) Whitethroat (Sylvia communis) Sand Martin (Riparia riparia) Willow Warbler (Phylloscopus trochilus) Rook (Corvus frugilegus) Dunnock (Prunella modularis) Magpie (Pica pica) Meadow Pipit (Anthus pratensis) Great Tit (Parus major) Pied/White Wagtail (Motacilla alba)

7 242 BRITISH BIRDS. [VOL. XLVII. Blue Tit (Parus cceruleus) Yellow Wagtail (Motacilla flava) Coal Tit (Parus ater) Chaffinch (Fringilla ccelebs) Redstart (Phcenicurus phcenicurus) Yellowhamraer (Emberiza citrinella) Nightingale (Luscinia megarhyncha) House Sparrow (Passer domesticus) Note: It is likely that there are some unpublished records of Protocalliphora from the nests of British birds which would make this list much more complete. It is also probable that a number of records published in certain entomological journals have been missed. The above list is taken mainly from Audcent (1942) and Rothschild and Clay (1952). Other records are unpublished. REFERENCES. AUDCENT, H. (1942). "A preliminary list of the hosts of some British Tachinidae (Dipt.)." Trans. Soc. Brit. Ent,, 8: ARNOLD, W. W. (1919). "Maggot infested birds." Auk, 36: BOYD, A. W. (1935). "A fly parasitic on the Swallow."" Brit. Birds, xxviii: 225. BOYD, E. M. (1951). "The external parasites of birds: a review." Wilson Bull., 63: BURTCH, V. (1920). "Maggots in the ears of nestling Cooper's Hawks (Accipiter cooperi)." Auk, 37: 293. CHAPMAN, L. B. (1935). "Studies of a Tree Sparrow colony." Bird-Banding, (' CHISHOLM, A. H. (1952). "Bird-insect nesting associations in Australia." Ibis, 94: COUTANT, A. F. (1915). "The habits, life history, and structure of a bloodsucking muscid larva (Protocalliphora azurea)." journ. Parasit., 1: (Cited by George and Mitchell, 1948). DOBROSCKY, I. D. (1925). "External parasites of birds and the fauna of bird's nests." Biol. Bull., 48: (Cited by Mason, 1944). EICHLBR, W. (1936). "Die Vogelparasiten Bine Uebersicht fiber die verschiedenen Gruppen 11 Die Vogelblutmaden." Orn. Mschr., 61: ' ( T 937)- "Vogelnester und Vorratsschadlinge." Mitteilungen der Gesellschaft fur Vorratsschutz, 13: GEORGE, J. L. AND MITCHELL, R. T. (1948). "Notes on two species of Calliphoridae (Diptera) parasitizing nestling birds." Auk, 65: GILBERT, P. A. (1919). "A dipterous parasite of nestling birds." Emu, 19: GUBERLET, J. E. AND HOTSON, H. H. (1930). "A maggot attacking young birds, with observations on its history." Murrelet, 21: (Cited by Mason, 1944)- HALL, D. G. (1948). The blowflies of North America. (Cited by George and Mitchell, 1948). HENSHAW, H. W. (1908). "A parasitic fly injurious to our native birds." Auk, 25: HILL, H.M. (1948). "Raptorial hosts of Protocalliphora". Condor, 50: AND WORK, T. H. (1947). Protocalliphora larvae infesting nestling birds of prey." Condor, 49: HINDWOOD, K. A. (1930). "A sub-cutaneous avian parasite." Emu., 30: JELLISON, W X. AND PHILIP, C. B. (1933). "Faunae of the nests of the Magpie and Crow in western Montana." Can. Ent., 65: JOHNSON, C. W. (1925). "Insects that infest birds." Bull. Northeastern Bird- Banding Assn., 1: (1927)- "The infestation of Bluebird's nests by Protocalliphora." Bull. Northeastern Bird-Banding Assn., 3: 1-3. (1930). "Notes on Protocalliphora during the summer of 1930". Bird-Banding, 1: ' (1931). "Nestling birds destroyed by the larvae of Protocalliphora." Boston Soc. Nat. Hist. Bull, 59: (Cited by Mason, 1944).

8 VOL. XLVII.] PROTOCALLIPHORA IN BIRDS' NESTS. 243 (1932)- "Notes on Protocalliphora during the summer of 1931." Bird-Banding, 3: LINCOLN, F. C. (1931). "Protocalliphora infestation of Barn and Bank Swallows." Bird-Banding, 2: LOHRL, H. (1949). "Uber Verluste im Nest kleinerer Hdhlenbriiter durch Fliegenmaden und andere Ursachen. Die Vogelwarte, 2: MASON, E. A. (1936). "Parasitism of bird's nests by Protocalliphora at Groton, Massachusetts." Bird-Banding, 7: (1944). "Parasitism by Protocalliphora and the management of cavity nesting birds." Journ. Wildlife Man., 8: MCATEE, W. L. (1927). "Notes on insect inhabitants of bird houses." Proc. Entom. Soc. Wash., 29 (4): (1929). "Further notes on insect inhabitants of bird houses." Proc. Entom. Soc. Wash., 31 (6): (1940)- "An experiment in songbird management." Auk, 57: NEFF, J. A. (1945). "Maggot infestation of nestling Mourning Doves." Condor, 47: PLATH, E. O. (1919a). Prevalence of Pkormia azurea Fallen in the Puget Sound region." Ann. Ent. Soc. Amer., 12: (Cited by Neff, 1945). ' (1919b). "A muscid larva of the San Francisco Bay region which sucks the blood of nestling birds." Univ. Calif. Publ. Zool., 19: (Cited by Neff, 1945). (1919c). "Parasitism of nestling birds by fly larvae." Condor, 21: PLETSCH, D. D. (1948). "Parasitic dipterous larvae from the nasal cavity of a nestling Magpie." Auk, 65: ROTHSCHILD, M. AND CLAY, T. (1952). Fleas, Flukes and Cuckoos. London. SARGENT, W. P. (1938). "Nest parasitism of hawks." Auk, 55: SEGUY, E. (1941). "Mouches parasites. II. Calliphorines, Sarcophagines, et Rhinophorines de I'Europe occidentale et meridionale." Encly. Ent., 21: (1946). "Notes biologiques et taxonomiques sur les Dipteres." Encyl. Ent., Ser. B., 10: SHANNON, R. C. AND DOBROSCKY, I. D. (1924). "The North American bird parasites of the genus Protocalliphora (Calliphoridae, Diptera)." Journ. Wash. Acad. Set., 14: SPERLING, E. (1935). "Parasiten im Nest von Motacilla c. cinerea." Mitt. orn. Ver. Magdeburg, 9: STONER, D. (1936). "Studies on the Bank Swallow Riparia r. riparia (Linneaus) in the Oneida Lake region." Roosevelt Wild Life Ann., 4: STORER, T. I. (1929). "Protocalliphora in the nest of a Mountain Chickadee". Condor, 31: 227. TAYLOR, J. S. (1949). "Dipterous parasites of nestling birds." Ostrich, 20: 171. THOMAS, E. S. (1936). "Additional records of Protocalliphora." Bird- Banding, 7: [If any of our readers have at any time made detailed records of the infestation of birds' nests by Protocalliphora, Mr. Owen has told us that he would be most grateful if he could see a summary of their observations. The information needed is: (a) the number of nests examined after the birds have fledged; (b) the number of these that contained Protocalliphora larvae and the number that did not; (c) the number of larvae or pupae per nest; and (d) whether there was any evidence that the birds had suffered as a result of the infestation. Those interested should write to Mr. Owen at the Edward Grey Institute, Botanic Garden, Oxford, for further details. EDS.]