Parasitology (1975), 70, 195-202
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Observations on the bionomics of Pseudolynchia canariensis (Diptera: Hippoboscidae) THOMAS R. KLEI Department of Biology, Millersville State College, Millersville, Pennsylvania 17551 and DOMINIC L. DEGIUSTI Department of Biology and Department of Comparative Medicine, Wayne State University, Detroit, Michigan 48202 (Received 19 August 1974) SUMMARY
Host suitability, reproduction, effects of temperature on reproduction and pupal development, effects of humidity on pupal development and the effects of photoperoid on puparial deposition, pupal development and adult emergence were studied in a laboratory colony of Pseudolynchia canariensis. Flies were observed to lack strong host specificity. Puparia were produced at regular 24 h intervals by flies maintained at 30 °C, averaging 8-8 puparia per female. Optimum temperature for colony maintenance was observed to range between 26-6 and 30-0 °C. Temperatures of 13 and 37 °C were lethal to pupae. Humidity and photoperiod did not markedly affect pupal development. Puparial deposition and adult emergence occurred only during the photoperiod.
INTRODUCTION
Pseudolynchia canariensis, a puparious dipteran and obligate ectoparasite of the domestic pigeon (Columba livia), is the intermediate host for Haemoproteus columbae. I t has been reared in the laboratory by many workers, primarily for research on H. columbae (Sergent & Sergent, 1907; Adie 1915,1924,1925; Bishopp, 1929; Drake & Jones, 1930; Coatney, 1931; Prouty & Coatney, 1934; Huff, 1932; Kartman, 1949; Levi, 1957; Mohammed, 1958; Schuurmans Stekhoven, Silva, Ines & SanRoman, 1954, 1956, 1957; Herath, 1966; Klei, DeGiusti & Herath, 1968). Although observations on specific aspects of its biology have been reported, data are lacking on the reproductive rate and effects of environmental factors on the life-cycle. A colony of P. canariensis has been maintained in this laboratory for five years to facilitate research on H. columbae. During this period studies were conducted to clarify the bionomics of the fly. Host suitability, reproduction, effects of temperature on reproduction and pupal development, effects of humidity on pupal development and effects of photoperiod on puparial deposition, pupal development and adult emergence were studied. 13
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MATERIALS AND METHODS
Colony maintenance P. canariensis, used to initiate the laboratory colony, were collected from feral pigeons trapped in Detroit, Michigan. In this laboratory the fly has been reared on Japanese quail (Goturnix coturnix japonica), bobwhite quail (Golinus virginianus), domestic pigeons (Columba livia) and mourning doves (Zenaidura macroura carolinensis). The Japanese quail was selected as the most suitable laboratory host. Quail were obtained from Dr T. H. Coleman of Michigan State University. Pigeons and doves were trapped in Detroit, Michigan. Uninfected adult pigeons and squabs used were hatched and raised in the laboratory in a fly-free environment. During the course of experimentation and colony maintenance, various conditions of temperature and humidity were used: 5 and 13 °C at relative humidity (r.h.) 60-70 %; 20, 24 and 37° C at r.h. 50-80 %; 26-6 and 30 °C at r.h. 70-80 %. Unless otherwise stated, 'the insectary' refers to the 30 °C, r.h. 70-80 % condition. All flies were maintained on 12 h photoperiods. Fly-tight breeding cages were used to rear P. canariensis on the various hosts. Cages were constructed so that maintenance procedures were possible with minimum disturbance of bird and fly populations. Details of cage construction have been described elsewhere (Klei, 1971). Throughout this study puparia were collected from the breeding cages, placed in cotton stoppered shell vials (7x2 cm) and placed in the insectary. Flies emerging from the puparia were released into bird cages at 2- to 3-day intervals. Host suitability Birds used in host suitability experiments were adult pigeons with and without previous fly exposure, 6- to 8-week-old squabs without previous fly exposure, Japanese quail with previous fly exposure and adult mourning doves with unknown histories offlyexposure. All birds were examined daily for several days prior to the onset of the experiment to ensure the absence of flies; only birds proven to be free of flies were used. Five male and five female flies, 1-3 days old, were placed on a single bird maintained in an isolation cage kept in the insectary. After a period of 20 days, the total puparial production of flies was recorded and used to determine host suitability. The mean number of puparia was examined statistically by analysis of variance. Reproduction To determine the time necessary for the production of the first puparium and the time interval between subsequent puparial productions, one male and one female fly, 1-3 days old, were placed on an isolated pigeon free of flies. Time intervals between puparial depositions were determined by examining and cleaning the isolation cages at 24 h intervals. The viability of puparia, produced at different times during the life span of the female fly, was also observed. Thirteen pairs of flies were employed in this study. Reproductive characteristics of the laboratory strain of flies were compared with those of the wild strain. Wild flies came from
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puparia produced by flies recovered from wild pigeons. All experiments were conducted in the insectary. Temperature effects Effect of temperature on reproduction was determined by comparing the time necessary for production of the first puparium and the time intervals between subsequent puparial depositions of flies on pigeons in a cold room at 13 °C, compared to pigeons maintained in the insectary. Effect of temperature on pupal development was determined by keeping pupae, collected daily in the insectary, at temperatures of 13, 20, 24, 26-6, 30 and 37 °C until development was complete to adult emergence. Percent emergence and time required to complete development to adult emergence were recorded. Effect of brief exposure to low temperatures on pupal development was determined by subjecting pupae, collected daily in the insectary, to 5 and 13 °C, 5-30 days, and then returning these pupae to the insectary. Percent emergence and time necessary to complete development to adult emergence were recorded. Humidity effect Effect of humidity on pupal development was tested by comparing percent emergence and time necessary to complete development to adult emergence between groups of pupae kept under dry and moist conditions. Chambers for humidity control were constructed by placing 48 x 20 mm shell vials in 78 x 25 mm shell vials. The smaller vials supported aluminium screen disks upon which puparia were placed. A dry environment was maintained by placing drierite below the disk on which the puparia rested and in a 150 mm drying tube inserted in the single hole rubber stopper that sealed the large vial at the open end. A humid environment was maintained by placing water-saturated cotton below the screen on which the puparia rested, and stoppering the large vials with cotton which was moistened daily. Puparia did not come in contact with the water. Vials containing puparia, to which neither desiccant nor water were added, served as controls and were stored at insectary conditions. Twenty-five puparia were tested at each humidity level selected. Photoperiod effect
Effect of photoperiod on pupal development was tested by comparing percent emergence and time necessary to complete development using groups of 26 pupae subjected to two different photoperiods. One group was maintained at the normal 12 h photoperiod; the second group was maintained under constant light. Both groups were kept at insectary conditions. Effect of photoperiod on puparial deposition was observed by recording the number of puparia produced during the scotoperiod and two halves of the photoperiod. Fly populations used in these experiments were maintained on Japanese quail in breeding cages kept at a 12-h photoperiod (7.00-19.00). Collections of puparia were made at 7.00, 12.00 and 19.00. The 7.00 collection included puparia produced during the scotoperiod, the 12.00 collection included puparia produced 13-2
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during the first half of the photoperiod, and the 19.00 collection included puparia produced during the second half of the photoperiod. Collections were continued for 5 days. Similar collections were made in continuous light. In addition, 7.00 and 19.00 collections were made during a reversed 12-h photoperiod which extended between 19.00 and 7.00. Theflypopulations were subjected to these reversed conditions of photoperiod for 16 days prior to making the collections. Effect of photoperiod on adult emergence was observed by separating puparia collected from quail cages kept at a 12 h photoperiod, into two groups. One group was exposed to a 12 h photoperiod and the other to continuous light. All pupae were kept in cotton stoppered shell vials in the insectary. After 14 days both groups were checked at 2 h intervals during the 12 h photoperiod and emergence of adult flies recorded. RESULTS
Approximately 47 000 P. canariensis have been reared during the 5 years the fly colony has been maintained on Japanese quail. The majority offlieswere reared on Japanese quail due to this hosts' availability, temperament and ease of maintenance. Flies were also reared on bobwhite quail and domestic pigeons. A statistically significant difference does not exist between the mean number of puparia produced by flies on the various birds used in the host suitability experiments: adult pigeons previously exposed to flies (13-7), adult pigeons not previously exposed to flies (18-3), young pigeons not previously exposed to flies (23-3), Japanese quail previously exposed to flies (16-5) and mourning doves with unknown histories offlyexposure (28-0). The time required for a laboratory strainflyto produce its first puparium after. being placed on a host, ranged from 5 to 10 days with a mean of 6 days. Subsequent puparia were produced every 48 h. Variation of this time interval occurred rarely and irregularly. These deviations were not related to the age of theflies.The number of puparia produced by a singleflyranged from 1 to 28 with a mean of 8.8. If the last puparial deposition can be used as a measure of the life span of the fly, the mean life span under laboratory conditions is 24-2 days with a range of 6-70 days. During the course of this series of experiments, 111 undamaged puparia were collected; 98 % emerged as adults. Emergence from pupae was not influenced by the age of theflythat produced them. Similar observations were made on one pair of P. canariensis wild strain which produced the first puparia 6 days after being placed on a bird. Thirteen puparia were produced in 38 days. Data suggest that domestic and wild strains do not differ in these characteristics. Further experimentation with the wild strain was not possible due to lack of feral flies. Effect of 13 °C on puparial production and longevity of the domestic strain of flies was studied with two pairs of flies that produced 6 and 7 puparia during 45 and 36 days respectively. First puparia were produced at 16 and 7 days after placing the flies on birds. Puparial production at 13 CC was erratic. Flies had a longer average life span at this temperature but produced fewer puparia. Effect of temperature on pupal development was measured by length of time necessary for development and emergence of the adult and percent pupae that
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Table 1. Effect of continuous exposure to selected temperatures on length of development of pupae and emergence of adults
Temp. (°C) 370
30-0 26-6 24-0 20-0 130
85-9 85-0
Average development time (days) 37-0 20-0 22-4 31-4 55-0
0
0
No. of pupae
Per cent emergence
47 50 54 67 20 12
21 960 961
Minimum duration of experiment (days) 60 60 60 60 120 365
Table 2. Effect of 13 °G for varying periods of time on length of pupal development and emergence of adult flies Average
development time
No. days at 13 °C
No. pupae
30 25 20 15 10 5
50 50 50 50 50 50
Emergence 46-0 78-0 96-0 86-0 90-0 920
(days) 48-2 440
39-2 34-4 29-6 24-5
Percent curly wing flies 80 5-0 0-0 0-0 00 0-0
successfully emerged as adults (Table 1). Optimum temperature for development appears to be in the range of 26-6-30-0 °C. Rate of development and emergence varies directly with temperature. Temperatures of 37 and 13 °C proved lethal. Although continuous exposure of pupae to 13 CC is lethal, shorter exposures are not (Table 2). Exposure for 20 days at 13 °C has little effect on emergence, however, exposure beyond 20 days markedly decreases emergence. This experiment also indicates that length of time for development increases with time of exposure at 13 °C. In the fly colony under normal maintenance conditions, 0-2 % of 3692 newly emerged flies had curly, uninflated wings. The occurrence of this lethal characteristic increased when pupae were kept beyond 20 days at 13 °C (Table 2). Exposure of 50 pupae to 5 °C for 10 days was lethal. Adults emerged from only 12 % of 50 pupae kept at 5 °C for 5 days and returned to the insectary (30 °C). The average developmental period for these pupae was 25-7 days. Eighty-eight per cent of pupae maintained in the insectary emerged successfully; 84% emerged under humid and 96% under dry conditions. The number of pupae completing development did not differ significantly (P> 1-0) when compared statistically with the X2 analysis. The average time to successful adult emergence under the conditions of humidity cited was 21-6 days for the group maintained in the insectary, 22-3 days for those maintained under humid and 22-0 days for those under dry conditions. Pupae stored at a 12 h photoperiod and a continuous photoperiod completed development to adults in 20-5 and 20-6 days respectively.
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During the 5 days of 12 h photoperiod, all puparia (78) collected were deposited during the light period with the majority (70%) deposited during the first half. Under conditions of constant light, 75 puparia were collected. These were deposited throughout the 24 h period with no time preference. When the photoperiod was reversed, all (52) puparia were deposited during the light period. Emergence of adults from pupae kept at a 12 h photoperiod occurred only during periods of light with the majority (77 %) emerging during the first half. Pupae kept at a 24 h photoperiod emerged adults throughout the period.
DISCUSSION
Comparisons made on the suitability of various species of birds as laboratory hosts for P. canariensis indicate that the mourning dove is the best host. However, flies reared on all of the birds tested bred successfully and little host specificity was observed. Lack of host specificity in laboratory colonies has also been observed by Coatney (1931), Huff (1932) and Herath (1966). Field studies by Sergent & Sergent (1907), Kartman (1949), Schuurmans Stekhoven et al. (Bequaert, 1952) and Klei & DeGiusti (1974) suggest that young rather than adult pigeons are more suitable hosts for P . canariensis. Lack of exposure to flies may not allow young birds time to become efficient at removing flies. It is also possible that these birds have not developed a physiological resistance or immunity to theflies,if it exists. Resistance of this nature has been demonstrated in sheep to the hippoboscid, Melophagus ovinus (Nelson, 1962a, b; Nelson & Bainsborough, 1963). The critical comparisons made between isolated pigeons of different ages and with different histories of fly exposure suggest that young pigeons not previously exposed to flies might be more suitable hosts than previously exposed adults. However, these results did not differ significantly and further experimentation is necessary to understand this problem in relation to P. canariensis and its pigeon host. Observations on the time interval required for the deposition of the first puparia by P. canariensis (5-10 days) confirm the results of Adie (1915), Schuurmans Stekhoven et al. (Bequaert, 1952) and Herath (1966). The interval between successive puparial production has been reported for many hippoboscids: P . canariensis 2-5-5 days (Coatney, 1931), 3-4 days (Schuurmans Stekhoven et al. (Bequaert 1952)); Ornithomyiafringillina 3 + 1 days (Hill, 1963), 5± 1 days (Bennett, 1961); 0. lagopodis 3-4 days (Hill, 1963); Lynchia americana 4-5 days, Ornithoica vicina 5 + 1 days (Bennett, 1961); Hippobosca variegata 6 days (Schuurmans Stekhoven et al. (Hill, 1963)); Melophagus ovinus 8 days (Swingle, 1913). Many of these observations were not made on single female flies kept under controlled environmental conditions. Daily observations on a number of single female P. canariensis demonstrated the interval between puparial production is 48 h at 30 °C. This rate of reproduction is greater than that previously described for other hippoboscids. Only one pair of first generation wild flies was available for observation. They produced puparia at the same rate as the domestic flies suggesting that reproductive rate has not changed during long periods of laboratory rearing. Our laboratory observations indicate that once puparial production is initiated
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it remains relatively constant throughout the life span of the female fly maintained at 30 °C. Thus, reproductive capacity in P. canariensis appears to be determined by life span. The average reproductively active life span in the laboratory is 24 days. Although these results are pertinent to laboratory studies, inferences from the laboratory to the natural situation must be made with caution because of the lack of information on ecological stresses such as changing microclimate and host availability in the natural environment. Rate of reproduction and pupal development are affected by changes in environmental temperature, as would be expected from results of many studies on other insect species (Bursell, 1964). Optimum temperature conditions for laboratory colony maintenance of P . canariensis range between 26-6 and 30-0 °C. Exposure of pupae to low temperatures suggests that P. canariensis might not survive winter conditions where temperatures drop below 13 °C for prolonged periods. Field studies indicate that fly populations decrease during the winters in Maryland (Jochen, 1962), Argentina (Schuurmans Stekhoven et al. (Bequaert, 1952)) and Michigan (Klei & DeGiusti, 1974). It is probable that seasonal temperature changes in the fly's natural environment are not as marked or rapid as atmospheric temperature changes would indicate. Again, lack of information on the microclimate of the fly in its natural environment does not allow for direct comparison with laboratory results. Puparial deposition and adult emergence occur only during the photoperiod and, to a greater extent, during the first half. Photoperiod had no effect on pupal development and emergence. Photoperiod has been described to affect oviposition and adult emergence in other insects (Beck, 1968); this has not been previously demonstrated in the Hippoboscidae. The observations in this study suggest that vision plays an important role in host location and pupal deposition by P. canariensis.
REFERENCES
ADIE, H. (1915). The sporogony of Haemoproteus columbae. Indian Journal of Medical Research 2, 671-80. ADIE, H. (1924). The sporogony of Haemoproteus columbae. Bulletin Societe de Pathologie Exotique 17, 605-13. ADIE, H. (1925). Nouvelles recherches sur la sporogonie de Haemoproteus columbae. Institut Pasteur d'Algirie Archives 3, 9-15. BECK, S. D. (1968). Insect Photoperiodism. New York and London: Academic Press. BEQUAERT, J. (1952). The Hippoboscidae or louse flies (Diptera) of mammals and birds. I. Structure, physiology and natural history. Entomologica Americana 32, 1-209 and 33, 211-442 (1953). BENNETT, G. F. (1961). On three species of Hippoboscidae (Diptera) on birds in Ontario. Canadian Journal of Zoology 39, 379-406. BISHOPP, F. C. (1929). The pigeon fly — an important pest of pigeons in the United States. Journal of Economic Entomology 22, 974-80. BUBSELL, E. (1964). Environmental aspects: Temperature. In The Physiology of Insecta, vol. i (ed. M. Rockstein), pp. 283-321. New York and London: Academic Press. COATNEY, G. R. (1931). On the biology of the pigeonflyPseudolynchia maura Bigot (Diptera, Hippoboscidae). Parasitology 23, 525-32. DRAKE, C. J. & JONES, R. M. (1930). The pigeon fly and pigeon malaria in Iowa. Iowa State College Journal of Science 4, 253-61.
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HEBATH, P. R. J . (1966). Colonizing Pseudolynchia canariensis on hosts other than the pigeon Columba livia. M.S. Thesis, Wayne State University. HILL, D. A. (1963). The life history of the British species of Orniihomyia (Diptera: Hippoboscidae). Transactions of the Royal Entomological Society of London 115, 391-407. HXJFP, C. G. (1932). Studies on Haemoproteus of mourning doves. American Journal of Hygiene 16, 618-23. JOCHEN, R. F. (1962). A survey of parasites in a population of pigeons (Columba livia Gmelin) in Henrico County, Virginia. M.S. Thesis, University of Richmond. KABTMAN, L. (1949). Observations on the Haemoproteus of pigeons in Honolulu, Hawaii. Pacific Science 3, 127-32. K L E I , T. R. (1971). Studies on Haemoproteus columbae of the pigeon, Columba livia, and the intermediate host Pseudolynchia canariensis. Ph.D. Dissertation, Wayne State University. KLBI, T. R. & DEGITTSTI, D. L. (1974). Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. (In preparation.) KLEI, T. R., DEGITJSTI, D. L. & HEEATH, P. R. J . (1968). Field and laboratory studies of Haemoproteus columbae and its vector Pseudolynchia canariensis in the pigeon population of Detroit, Michigan. American Zoologist 8, 823. LEVT, W. M. (1957). The Pigeon. Columbia, South Carolina: R. L. Bryan Company. MOHAMMED, A. H. H. (1958). Systematic and Experimental Studies on Protozoa! Blood Parasites of Egyptian Birds, vol. H . Cairo: Cairo University Press. NELSON, W. A. (1962a). Development in sheep of resistance to the ked, Melophagus ovinus (L.). I. Effects of seasonal manipulation of infestations. Experimental Parasitology 12, 41-4. NELSON, W. A. (19626). Development in sheep of resistance to the ked, Melophagus ovinus (L.). II. Effects of adrenocorticotrophic hormone and cortisone. Experimental Parasitology 12, 45-51. NELSON, W. A. & BAINSBOBOTJGH, A. R. (1963). Development in sheep of resistance to the ked, Melophagus ovinus (L.). III. Histopathology of sheep skin as a clue to the nature of resistance. Experimental Parasitology 13, 118-27. PEOTJTY, M. J . & COATNEY, G. R. (1934). Further studies on the biology of Pseudolynchia maura. Parasitology 26, 249-58. ScmrtJRMANS STEKHOVEN, J . H., SILVA, 1.1., INES, ISABEL & SANROMAN, PEDBO. (1954).
Zur Biologie der Tauben Lausfliege. Zeitschrift fur Parasitenkunde 16, 388-406. ScHtruBMANS STEKHOVEN, J . H., SILVA, 1.1., INES, ISABEL & SANROMAN, PEDBO. (1956).
Die Biologie der Tauben Lausfliege Bewegungsphysiologie, Taxismen und Zirkulation des Blutes. Zoologische Jahrbuecher Abteilungfiir Allgemeine Zoologie und Physiologie der Tiere 66, 509-30. SCHUUEMANS STEKHOVEN, J . H., SILVA, 1.1., INES, ISABEL & SANROMAN, PEDBO. (1957).
Beobachtungen uber die pupale Entwicklung und iiber das Schlupfen von Pseudolynchia canariensis Macquart (Diptera, Pupipara, Tlippohosicid&e). Zoologische Jahrbuecher Abteilung fur Allgemeine Zoologie und Physiologie der Tiere 67, 283-92. SEBGENT, E D . & SEEGENT, E T . (1907). Etudes sur les hematozoaires d'oiseaux. Annales Institut Pasteur 2 1 , 251-80. SWINGLE, L. D. (1913). The eradication of the sheep tick. Bulletin of the Wyoming Agricultural Experiment Station 106, 1-24.
Printed in Great Britain
195
Observations on the bionomics of Pseudolynchia canariensis (Diptera: Hippoboscidae) THOMAS R. KLEI Department of Biology, Millersville State College, Millersville, Pennsylvania 17551 and DOMINIC L. DEGIUSTI Department of Biology and Department of Comparative Medicine, Wayne State University, Detroit, Michigan 48202 (Received 19 August 1974) SUMMARY
Host suitability, reproduction, effects of temperature on reproduction and pupal development, effects of humidity on pupal development and the effects of photoperoid on puparial deposition, pupal development and adult emergence were studied in a laboratory colony of Pseudolynchia canariensis. Flies were observed to lack strong host specificity. Puparia were produced at regular 24 h intervals by flies maintained at 30 °C, averaging 8-8 puparia per female. Optimum temperature for colony maintenance was observed to range between 26-6 and 30-0 °C. Temperatures of 13 and 37 °C were lethal to pupae. Humidity and photoperiod did not markedly affect pupal development. Puparial deposition and adult emergence occurred only during the photoperiod.
INTRODUCTION
Pseudolynchia canariensis, a puparious dipteran and obligate ectoparasite of the domestic pigeon (Columba livia), is the intermediate host for Haemoproteus columbae. I t has been reared in the laboratory by many workers, primarily for research on H. columbae (Sergent & Sergent, 1907; Adie 1915,1924,1925; Bishopp, 1929; Drake & Jones, 1930; Coatney, 1931; Prouty & Coatney, 1934; Huff, 1932; Kartman, 1949; Levi, 1957; Mohammed, 1958; Schuurmans Stekhoven, Silva, Ines & SanRoman, 1954, 1956, 1957; Herath, 1966; Klei, DeGiusti & Herath, 1968). Although observations on specific aspects of its biology have been reported, data are lacking on the reproductive rate and effects of environmental factors on the life-cycle. A colony of P. canariensis has been maintained in this laboratory for five years to facilitate research on H. columbae. During this period studies were conducted to clarify the bionomics of the fly. Host suitability, reproduction, effects of temperature on reproduction and pupal development, effects of humidity on pupal development and effects of photoperiod on puparial deposition, pupal development and adult emergence were studied. 13
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MATERIALS AND METHODS
Colony maintenance P. canariensis, used to initiate the laboratory colony, were collected from feral pigeons trapped in Detroit, Michigan. In this laboratory the fly has been reared on Japanese quail (Goturnix coturnix japonica), bobwhite quail (Golinus virginianus), domestic pigeons (Columba livia) and mourning doves (Zenaidura macroura carolinensis). The Japanese quail was selected as the most suitable laboratory host. Quail were obtained from Dr T. H. Coleman of Michigan State University. Pigeons and doves were trapped in Detroit, Michigan. Uninfected adult pigeons and squabs used were hatched and raised in the laboratory in a fly-free environment. During the course of experimentation and colony maintenance, various conditions of temperature and humidity were used: 5 and 13 °C at relative humidity (r.h.) 60-70 %; 20, 24 and 37° C at r.h. 50-80 %; 26-6 and 30 °C at r.h. 70-80 %. Unless otherwise stated, 'the insectary' refers to the 30 °C, r.h. 70-80 % condition. All flies were maintained on 12 h photoperiods. Fly-tight breeding cages were used to rear P. canariensis on the various hosts. Cages were constructed so that maintenance procedures were possible with minimum disturbance of bird and fly populations. Details of cage construction have been described elsewhere (Klei, 1971). Throughout this study puparia were collected from the breeding cages, placed in cotton stoppered shell vials (7x2 cm) and placed in the insectary. Flies emerging from the puparia were released into bird cages at 2- to 3-day intervals. Host suitability Birds used in host suitability experiments were adult pigeons with and without previous fly exposure, 6- to 8-week-old squabs without previous fly exposure, Japanese quail with previous fly exposure and adult mourning doves with unknown histories offlyexposure. All birds were examined daily for several days prior to the onset of the experiment to ensure the absence of flies; only birds proven to be free of flies were used. Five male and five female flies, 1-3 days old, were placed on a single bird maintained in an isolation cage kept in the insectary. After a period of 20 days, the total puparial production of flies was recorded and used to determine host suitability. The mean number of puparia was examined statistically by analysis of variance. Reproduction To determine the time necessary for the production of the first puparium and the time interval between subsequent puparial productions, one male and one female fly, 1-3 days old, were placed on an isolated pigeon free of flies. Time intervals between puparial depositions were determined by examining and cleaning the isolation cages at 24 h intervals. The viability of puparia, produced at different times during the life span of the female fly, was also observed. Thirteen pairs of flies were employed in this study. Reproductive characteristics of the laboratory strain of flies were compared with those of the wild strain. Wild flies came from
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puparia produced by flies recovered from wild pigeons. All experiments were conducted in the insectary. Temperature effects Effect of temperature on reproduction was determined by comparing the time necessary for production of the first puparium and the time intervals between subsequent puparial depositions of flies on pigeons in a cold room at 13 °C, compared to pigeons maintained in the insectary. Effect of temperature on pupal development was determined by keeping pupae, collected daily in the insectary, at temperatures of 13, 20, 24, 26-6, 30 and 37 °C until development was complete to adult emergence. Percent emergence and time required to complete development to adult emergence were recorded. Effect of brief exposure to low temperatures on pupal development was determined by subjecting pupae, collected daily in the insectary, to 5 and 13 °C, 5-30 days, and then returning these pupae to the insectary. Percent emergence and time necessary to complete development to adult emergence were recorded. Humidity effect Effect of humidity on pupal development was tested by comparing percent emergence and time necessary to complete development to adult emergence between groups of pupae kept under dry and moist conditions. Chambers for humidity control were constructed by placing 48 x 20 mm shell vials in 78 x 25 mm shell vials. The smaller vials supported aluminium screen disks upon which puparia were placed. A dry environment was maintained by placing drierite below the disk on which the puparia rested and in a 150 mm drying tube inserted in the single hole rubber stopper that sealed the large vial at the open end. A humid environment was maintained by placing water-saturated cotton below the screen on which the puparia rested, and stoppering the large vials with cotton which was moistened daily. Puparia did not come in contact with the water. Vials containing puparia, to which neither desiccant nor water were added, served as controls and were stored at insectary conditions. Twenty-five puparia were tested at each humidity level selected. Photoperiod effect
Effect of photoperiod on pupal development was tested by comparing percent emergence and time necessary to complete development using groups of 26 pupae subjected to two different photoperiods. One group was maintained at the normal 12 h photoperiod; the second group was maintained under constant light. Both groups were kept at insectary conditions. Effect of photoperiod on puparial deposition was observed by recording the number of puparia produced during the scotoperiod and two halves of the photoperiod. Fly populations used in these experiments were maintained on Japanese quail in breeding cages kept at a 12-h photoperiod (7.00-19.00). Collections of puparia were made at 7.00, 12.00 and 19.00. The 7.00 collection included puparia produced during the scotoperiod, the 12.00 collection included puparia produced 13-2
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THOMAS E. KLEI AND DOMINIC L. DEGIUSTI
during the first half of the photoperiod, and the 19.00 collection included puparia produced during the second half of the photoperiod. Collections were continued for 5 days. Similar collections were made in continuous light. In addition, 7.00 and 19.00 collections were made during a reversed 12-h photoperiod which extended between 19.00 and 7.00. Theflypopulations were subjected to these reversed conditions of photoperiod for 16 days prior to making the collections. Effect of photoperiod on adult emergence was observed by separating puparia collected from quail cages kept at a 12 h photoperiod, into two groups. One group was exposed to a 12 h photoperiod and the other to continuous light. All pupae were kept in cotton stoppered shell vials in the insectary. After 14 days both groups were checked at 2 h intervals during the 12 h photoperiod and emergence of adult flies recorded. RESULTS
Approximately 47 000 P. canariensis have been reared during the 5 years the fly colony has been maintained on Japanese quail. The majority offlieswere reared on Japanese quail due to this hosts' availability, temperament and ease of maintenance. Flies were also reared on bobwhite quail and domestic pigeons. A statistically significant difference does not exist between the mean number of puparia produced by flies on the various birds used in the host suitability experiments: adult pigeons previously exposed to flies (13-7), adult pigeons not previously exposed to flies (18-3), young pigeons not previously exposed to flies (23-3), Japanese quail previously exposed to flies (16-5) and mourning doves with unknown histories offlyexposure (28-0). The time required for a laboratory strainflyto produce its first puparium after. being placed on a host, ranged from 5 to 10 days with a mean of 6 days. Subsequent puparia were produced every 48 h. Variation of this time interval occurred rarely and irregularly. These deviations were not related to the age of theflies.The number of puparia produced by a singleflyranged from 1 to 28 with a mean of 8.8. If the last puparial deposition can be used as a measure of the life span of the fly, the mean life span under laboratory conditions is 24-2 days with a range of 6-70 days. During the course of this series of experiments, 111 undamaged puparia were collected; 98 % emerged as adults. Emergence from pupae was not influenced by the age of theflythat produced them. Similar observations were made on one pair of P. canariensis wild strain which produced the first puparia 6 days after being placed on a bird. Thirteen puparia were produced in 38 days. Data suggest that domestic and wild strains do not differ in these characteristics. Further experimentation with the wild strain was not possible due to lack of feral flies. Effect of 13 °C on puparial production and longevity of the domestic strain of flies was studied with two pairs of flies that produced 6 and 7 puparia during 45 and 36 days respectively. First puparia were produced at 16 and 7 days after placing the flies on birds. Puparial production at 13 CC was erratic. Flies had a longer average life span at this temperature but produced fewer puparia. Effect of temperature on pupal development was measured by length of time necessary for development and emergence of the adult and percent pupae that
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Table 1. Effect of continuous exposure to selected temperatures on length of development of pupae and emergence of adults
Temp. (°C) 370
30-0 26-6 24-0 20-0 130
85-9 85-0
Average development time (days) 37-0 20-0 22-4 31-4 55-0
0
0
No. of pupae
Per cent emergence
47 50 54 67 20 12
21 960 961
Minimum duration of experiment (days) 60 60 60 60 120 365
Table 2. Effect of 13 °G for varying periods of time on length of pupal development and emergence of adult flies Average
development time
No. days at 13 °C
No. pupae
30 25 20 15 10 5
50 50 50 50 50 50
Emergence 46-0 78-0 96-0 86-0 90-0 920
(days) 48-2 440
39-2 34-4 29-6 24-5
Percent curly wing flies 80 5-0 0-0 0-0 00 0-0
successfully emerged as adults (Table 1). Optimum temperature for development appears to be in the range of 26-6-30-0 °C. Rate of development and emergence varies directly with temperature. Temperatures of 37 and 13 °C proved lethal. Although continuous exposure of pupae to 13 CC is lethal, shorter exposures are not (Table 2). Exposure for 20 days at 13 °C has little effect on emergence, however, exposure beyond 20 days markedly decreases emergence. This experiment also indicates that length of time for development increases with time of exposure at 13 °C. In the fly colony under normal maintenance conditions, 0-2 % of 3692 newly emerged flies had curly, uninflated wings. The occurrence of this lethal characteristic increased when pupae were kept beyond 20 days at 13 °C (Table 2). Exposure of 50 pupae to 5 °C for 10 days was lethal. Adults emerged from only 12 % of 50 pupae kept at 5 °C for 5 days and returned to the insectary (30 °C). The average developmental period for these pupae was 25-7 days. Eighty-eight per cent of pupae maintained in the insectary emerged successfully; 84% emerged under humid and 96% under dry conditions. The number of pupae completing development did not differ significantly (P> 1-0) when compared statistically with the X2 analysis. The average time to successful adult emergence under the conditions of humidity cited was 21-6 days for the group maintained in the insectary, 22-3 days for those maintained under humid and 22-0 days for those under dry conditions. Pupae stored at a 12 h photoperiod and a continuous photoperiod completed development to adults in 20-5 and 20-6 days respectively.
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During the 5 days of 12 h photoperiod, all puparia (78) collected were deposited during the light period with the majority (70%) deposited during the first half. Under conditions of constant light, 75 puparia were collected. These were deposited throughout the 24 h period with no time preference. When the photoperiod was reversed, all (52) puparia were deposited during the light period. Emergence of adults from pupae kept at a 12 h photoperiod occurred only during periods of light with the majority (77 %) emerging during the first half. Pupae kept at a 24 h photoperiod emerged adults throughout the period.
DISCUSSION
Comparisons made on the suitability of various species of birds as laboratory hosts for P. canariensis indicate that the mourning dove is the best host. However, flies reared on all of the birds tested bred successfully and little host specificity was observed. Lack of host specificity in laboratory colonies has also been observed by Coatney (1931), Huff (1932) and Herath (1966). Field studies by Sergent & Sergent (1907), Kartman (1949), Schuurmans Stekhoven et al. (Bequaert, 1952) and Klei & DeGiusti (1974) suggest that young rather than adult pigeons are more suitable hosts for P . canariensis. Lack of exposure to flies may not allow young birds time to become efficient at removing flies. It is also possible that these birds have not developed a physiological resistance or immunity to theflies,if it exists. Resistance of this nature has been demonstrated in sheep to the hippoboscid, Melophagus ovinus (Nelson, 1962a, b; Nelson & Bainsborough, 1963). The critical comparisons made between isolated pigeons of different ages and with different histories of fly exposure suggest that young pigeons not previously exposed to flies might be more suitable hosts than previously exposed adults. However, these results did not differ significantly and further experimentation is necessary to understand this problem in relation to P. canariensis and its pigeon host. Observations on the time interval required for the deposition of the first puparia by P. canariensis (5-10 days) confirm the results of Adie (1915), Schuurmans Stekhoven et al. (Bequaert, 1952) and Herath (1966). The interval between successive puparial production has been reported for many hippoboscids: P . canariensis 2-5-5 days (Coatney, 1931), 3-4 days (Schuurmans Stekhoven et al. (Bequaert 1952)); Ornithomyiafringillina 3 + 1 days (Hill, 1963), 5± 1 days (Bennett, 1961); 0. lagopodis 3-4 days (Hill, 1963); Lynchia americana 4-5 days, Ornithoica vicina 5 + 1 days (Bennett, 1961); Hippobosca variegata 6 days (Schuurmans Stekhoven et al. (Hill, 1963)); Melophagus ovinus 8 days (Swingle, 1913). Many of these observations were not made on single female flies kept under controlled environmental conditions. Daily observations on a number of single female P. canariensis demonstrated the interval between puparial production is 48 h at 30 °C. This rate of reproduction is greater than that previously described for other hippoboscids. Only one pair of first generation wild flies was available for observation. They produced puparia at the same rate as the domestic flies suggesting that reproductive rate has not changed during long periods of laboratory rearing. Our laboratory observations indicate that once puparial production is initiated
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201
it remains relatively constant throughout the life span of the female fly maintained at 30 °C. Thus, reproductive capacity in P. canariensis appears to be determined by life span. The average reproductively active life span in the laboratory is 24 days. Although these results are pertinent to laboratory studies, inferences from the laboratory to the natural situation must be made with caution because of the lack of information on ecological stresses such as changing microclimate and host availability in the natural environment. Rate of reproduction and pupal development are affected by changes in environmental temperature, as would be expected from results of many studies on other insect species (Bursell, 1964). Optimum temperature conditions for laboratory colony maintenance of P . canariensis range between 26-6 and 30-0 °C. Exposure of pupae to low temperatures suggests that P. canariensis might not survive winter conditions where temperatures drop below 13 °C for prolonged periods. Field studies indicate that fly populations decrease during the winters in Maryland (Jochen, 1962), Argentina (Schuurmans Stekhoven et al. (Bequaert, 1952)) and Michigan (Klei & DeGiusti, 1974). It is probable that seasonal temperature changes in the fly's natural environment are not as marked or rapid as atmospheric temperature changes would indicate. Again, lack of information on the microclimate of the fly in its natural environment does not allow for direct comparison with laboratory results. Puparial deposition and adult emergence occur only during the photoperiod and, to a greater extent, during the first half. Photoperiod had no effect on pupal development and emergence. Photoperiod has been described to affect oviposition and adult emergence in other insects (Beck, 1968); this has not been previously demonstrated in the Hippoboscidae. The observations in this study suggest that vision plays an important role in host location and pupal deposition by P. canariensis.
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HEBATH, P. R. J . (1966). Colonizing Pseudolynchia canariensis on hosts other than the pigeon Columba livia. M.S. Thesis, Wayne State University. HILL, D. A. (1963). The life history of the British species of Orniihomyia (Diptera: Hippoboscidae). Transactions of the Royal Entomological Society of London 115, 391-407. HXJFP, C. G. (1932). Studies on Haemoproteus of mourning doves. American Journal of Hygiene 16, 618-23. JOCHEN, R. F. (1962). A survey of parasites in a population of pigeons (Columba livia Gmelin) in Henrico County, Virginia. M.S. Thesis, University of Richmond. KABTMAN, L. (1949). Observations on the Haemoproteus of pigeons in Honolulu, Hawaii. Pacific Science 3, 127-32. K L E I , T. R. (1971). Studies on Haemoproteus columbae of the pigeon, Columba livia, and the intermediate host Pseudolynchia canariensis. Ph.D. Dissertation, Wayne State University. KLBI, T. R. & DEGITTSTI, D. L. (1974). Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. (In preparation.) KLEI, T. R., DEGITJSTI, D. L. & HEEATH, P. R. J . (1968). Field and laboratory studies of Haemoproteus columbae and its vector Pseudolynchia canariensis in the pigeon population of Detroit, Michigan. American Zoologist 8, 823. LEVT, W. M. (1957). The Pigeon. Columbia, South Carolina: R. L. Bryan Company. MOHAMMED, A. H. H. (1958). Systematic and Experimental Studies on Protozoa! Blood Parasites of Egyptian Birds, vol. H . Cairo: Cairo University Press. NELSON, W. A. (1962a). Development in sheep of resistance to the ked, Melophagus ovinus (L.). I. Effects of seasonal manipulation of infestations. Experimental Parasitology 12, 41-4. NELSON, W. A. (19626). Development in sheep of resistance to the ked, Melophagus ovinus (L.). II. Effects of adrenocorticotrophic hormone and cortisone. Experimental Parasitology 12, 45-51. NELSON, W. A. & BAINSBOBOTJGH, A. R. (1963). Development in sheep of resistance to the ked, Melophagus ovinus (L.). III. Histopathology of sheep skin as a clue to the nature of resistance. Experimental Parasitology 13, 118-27. PEOTJTY, M. J . & COATNEY, G. R. (1934). Further studies on the biology of Pseudolynchia maura. Parasitology 26, 249-58. ScmrtJRMANS STEKHOVEN, J . H., SILVA, 1.1., INES, ISABEL & SANROMAN, PEDBO. (1954).
Zur Biologie der Tauben Lausfliege. Zeitschrift fur Parasitenkunde 16, 388-406. ScHtruBMANS STEKHOVEN, J . H., SILVA, 1.1., INES, ISABEL & SANROMAN, PEDBO. (1956).
Die Biologie der Tauben Lausfliege Bewegungsphysiologie, Taxismen und Zirkulation des Blutes. Zoologische Jahrbuecher Abteilungfiir Allgemeine Zoologie und Physiologie der Tiere 66, 509-30. SCHUUEMANS STEKHOVEN, J . H., SILVA, 1.1., INES, ISABEL & SANROMAN, PEDBO. (1957).
Beobachtungen uber die pupale Entwicklung und iiber das Schlupfen von Pseudolynchia canariensis Macquart (Diptera, Pupipara, Tlippohosicid&e). Zoologische Jahrbuecher Abteilung fur Allgemeine Zoologie und Physiologie der Tiere 67, 283-92. SEBGENT, E D . & SEEGENT, E T . (1907). Etudes sur les hematozoaires d'oiseaux. Annales Institut Pasteur 2 1 , 251-80. SWINGLE, L. D. (1913). The eradication of the sheep tick. Bulletin of the Wyoming Agricultural Experiment Station 106, 1-24.
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