Kartman, L.

Pacific Science

Kartman, L

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Observations on the Haemoproteus of Pigeons in Honolulu, Hawaii

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Observations on the Haemoproteus of Pigeonsin Honolulu, HawaiiL KA,RTMAN1D URING THE PERIOD January to July, 1948,observations were made at different times onthe halteridium parasite of the pigeon, Haemo-proteus columbae Kruse, 1890. Inasmuch asvery little information has been published onthe Haemosporidia of bird s in H awaii, thesenotes are presented with a view toward open-ing anew the question of blood protozoa ofbirds in the Territory, a problem which hasnever been systematically investigated. Fisher(1948) has emphasized the paucity of evidenceregarding these parasites in H awaii.Alicata ( 1939, 1947) indicated that pigeonsin Hawaii are commonly infected with Haemo-proteus columhae, and Bryan ( 1934) showedthat the hippoboscid vector; Pseuflolynchiacanariensis (Macq.) , is generally distributed.N o quantitative data .are given in the abovereports, however. The notes presented in thispaper offer preliminary data on various aspectsof the problem.Pigeons and doves were examined at theHonolulu Zoo. Observations on both juvenileand adult pigeons showed them to be generallyinfested with the fly vector. There was anaverage of 2.0 flies per bird on about 50juvenile 'p igeons examined and an average of1.3 flies per bird on 100 adult pigeons. Of 45. doves examined none was found to harbor thepigeon fly, although the birds were housed inthe vicinity of the pigeon lofts . This observa-tion is in conformity with the remarks of Be-quaert ( 1939) , who indicated that Pseudolyn-1 Department ' of Parasitology, Uni versity of H awaiiAgr icultural Experiment Station . Manuscr ipt receivedJuly 30, 1948.chia canariensis has never been found on a wildhost in N orth America. On the other hand, ithas been taken from at least eight species ofwild Columbidae belonging to' five genera inEurope, Africa, and the Philippines:More consistent infestation was noted onjuvenile pigeons which had attai ned full plum-age. Young bird s between 15 and 25 days ofage had the major infestation with flies where-as younger birds were less consistently infested.Many fly puparia were found in the pige onnests ' and some of these were taken to thelaboratory, placed in test tubes plugged withcotton, and kept at room temperature. Fliesemerged from these pupae at from 15 to 20days after collection. Pupae observed from thetime of deposition by the female fly hatched 'at between 23 and 37 days.Some of the pigeon flies collected at varioustimes were dissected for evidence of infectionwith the pigeon Haem oproteus. Table 1 sum-marizes the data for dissections of 25 flies takenfrom both young and adult pigeons. A total of36 per cent 'of the flies was found to be in-fected; it is interesting to note that of 19 fe-males, 36.8 per cent were infected, and of 6males, 33.3 per cent. Although flies fromseveral juvenile pigeons were not infected,others collected from young birds showed theinfection, indicating that the fly is active inmigrating from adults to young.Blood smears were taken from birds at thezoo to determine . the incidence of infectionwith Haemoproteus columbae in pigeons andto learn whether local doves are naturally in-fected with the pigeon parasite. Alth ough[1 271128 PACIFIC SCIENC~, Vol. III, April, 1949TABLE 1INFECTION OF PSEUDOLYNCHIA CANARIENSIS WITHH AEMOPRO'l'EUS COLUMBAE IN N ATURENUMBER OF INFECTIONSFLIES FLIES FLIES AGE OFDATE DISSECTED INFECTED Salivary INFECTED HOSTMidgut • glandsNumber Number Per cent3-3~8_'_ ' ____ " _'__'_'_" ___" ____' 12 5 5 2 41.7 juveniles andadults3- 31-48_.....~.._... ........._...... 4 0 0 0 0_0 juveniles only5-12-48. ..._.......________.. .___.__ 9 4 4 2 44.4 juvenile s andadultsTotals.....___.___ _.-r- - -••••-••. •. 25 9 9 4 36.0• In add ition to typical oocysts fount! on th e midgut , it ma y be of interes t to note oocysts found on the hindgut of onefly (see Fig . 3) .5O.'J') 100-1 i'J I ~O. I9'} 200-24') 250·299blood smears cannot indicate the maximum 'rate of infection with H aem oproteus, they area rapid and accurate method of surveying forapprox imate incidence of infection. The smearstaken from pigeons and doves were subjected toGiemsa's stain, usually within 24 hours afterthey were taken , and were then examined. Be-sides recording the positive and negative smears,in every positive smear estimates were made ofthe number of gametocytes infecting red bloodcells. In making this estimation the actual rateof infection in 2,000 or more red cells was firsttabulated and then calculated in terms of game -rocytes per 10,000 red cells. The data for these12Ga mCIOC)" IC'S per10,100ted blood corpusclesFIG_ 1. Intensity of infection with Haemoproteus col-umbae in 10 1 pigeons (based on blood smears ) .observations are shown in Table 2 and Figure 1.In addition to the data shown in the table, 38juvenile pigeons under 30 days of age wereall found negative. Two Chinese doves, Strep-topelia cbinensis, were also negative.It is seen .that the pigeons have a high rateof infection and that this rate is a little overtwo times the rate of infection found in the flyvector. Such an incidence in both definitiveand intermediate hosts indicates an ideal situa-tion for the life cycle of the parasite. It shouldbe noted that most of the birds examined hadmild infections. As' was expected, none of thedoves examined showed an infection with thepigeon parasite.Several experiments .were conducted in anattempt to transmit the H aem oproteus ofpigeons to doves. It has been shown by Huff( 1932 ) that the Haemoproteus of doves couldbe transmitted to domestic pigeons by thepigeon fly. However, the pigeon parasite hasnever been successfully transmitted to doves.Expe rim ent I: ( 1) . On February 20, pigeon flieswere collected from juvenile pigeons and 17 were. placed in a cage with an infected pigeon showing230 garnerocytes per 10,000 red cells.(2). On February 29,10 flies were recovered fromthe pigeon and five were placed on a Chinese dove,Streptop elie cbinensis (Scopoli). This dove had beencaptured on February 2, and blood smears taken onFebruary 2, 15, 22, and 29 were all negative forHaemoproteus of Pigeons-KARTMANTABLE 2INFECTION OF PIGEONS AND DOVES WITH HAEMOPROTEUS COLUMBAE IN NATURE129NUMBER NUMBER PERCENTAGEDATE BIRD EXAMINED POSITIVE POSITIVE1-20-48.... .. ...... .................... .. Pigeon 3 3 100.02-23-48...........:... .......... ......... Pigeon 28 20 71.42-25-48.... ................ .............. Pigeon 4 5 42 93.32-26-48....:............: ...... .......... Pigeon 25 18 72.0:3-30-48. .......... ... ...............:...: Dove " 43 0 0.0Totals (Pigeons only) ........ " 101 83 82.2• Thirty Indi an rin g-neck doves and 13 lace-neck doves.blood parasites. The remaining five flies not placedon the dove were dissected and four were found tohave oocysts on the midgu t. Salivary gland exami-nations were not made.(3 ). Blood smears taken on March 12 and 16were negative and on March 29 the dove was founddead in its cage. Blood smears from the heart andliver were negative for Haemoproteus gam erocytes,(4). Five flies were recovered from the cage con-taining the dead dove and dissections of these showedtwo with both oiicysts and sporozoites, one withoiicysts only, and two with negative rnidguts andsalivary glands.Experim ent II: (l). On May 12, pigeon flies werecollected from juvenile pigeons.' Of three flies dis-sected, one was positive for sporozoites. Fifteen flies. were comminuted with physiological saline in amortar, yielding 1.5 m!' of pooled materia!' . Approxi-mately 0.5 m!' was in jected into the pectoral mu sclesof one ring-neck dove, Stre ptopelia decaocto (Pri-valszky ) , one barred dove, Geopelia striata striata(Linn.) , and one 5-week-old white Leghorn chick.(2) . Blood smears taken from these birds on June8, 17, and J uly 2 were all negative and the experi-ment was terminated.Experim ent III: (1). On May 12 , 10 pigeon flieswere placed on an infected pigeon showing 250 game-tocytes per 10,000 red cells.(2) . On May 22 the flies were removed from thepigeon and placed on a ring-neck dove. Two fliesdissected were found positive for oocysts,(3 ) . Blood smears taken on 'June 17 and July 4were negative. Six flies taken from the dove on July4 showed four positive for sporoz oites.All the doves were examined well within theperiod shown by Adie (1924) to be necessaryfor the appearance of gamerocytes in the peri-pheral ·blood. Even in the case of the dove inExperiment I a period of .30 days intervenedbetween first feeding of the flies and death ofthe bird. Since infected flies were known tobe present in these samples and since the flies .feed on their host every day, it is felt that thedoves had ample opportunity to become .in-fected.The failure to infect these doves and thechicken with the H aemoproteus from thepigeon substantiates the findings of Coatney(1933), who showed that the mourning dove,Z enaidura macroura carolinensis, is not suscep-tible to Haemoproteus colum bae of the pigeon.He ascribes this to the known high degree ofhost specificity among many of the Haemos-poridia and concludes that doves have a highdegree of natural immunity toward the pigeonH aemoproteus.Although earlier in this paper it was indi-cated that the pigeon fly was not taken on dovesin nature, no difficulty was encountered in usingthe doves as hosts of this vector in the labora-tory. Coatney (1933) also found this to betrue in the case of the mourn ing dove.Various workers have indicated that earlystages in the sporogony of Haemoproteus col-umbae are capable of a certain amount of de-velopment in ' bloodsucking insects other thanthe hippoboscid vector. Wenyon (1926: 897)has summarized the reports of Aragao andNemer, who indicated that ookineres wereformed in mites, bedbugs, and various speciesof · culicine mosquitoes. In ·Aedes argenteus(=Aedes aegypti) Noller found that ookinetes130formed quite readily at a temperature of 11°to 12° C. and persisted for at least 6 days.Several exper iments were conducted to testthe developm ental ability of the pigeon Haem o-proteus in local mosquitoes . In all cases themosquitoes were reared from larvae and pupaecollected in the field. Adult females were fedon moist raisins for at least 2 days and werethen kept from both food and water for another2 days before their first blood meal. They wereliberated into a cage 30 inches high, 28 incheswide, and 32 inches deep for feeding on in-fected pigeons. Feathers were plucked fromabout the body of the pigeons to expose the skin'and to allow greater opportunity for engorge-, rnent by the mosquitoes. No difficulty was en-countered in getting a sufficient number ofengorged mosquitoes for the observations de-scribed below, although apparently many of thefemales did not feed on the pigeons. All ex-per.iments were conducted at room temperature,which fluctuated between 62.5° and 83.5° F.during this period.Experiment I: ( 1 ) . On February 5, starved andthirsty females .of Culex quinquefasciatus Say wereliberated into the cage contain ing an infected pigeonPACIFIC SCIENCE, v ei. III, April, 1949with 250 .gamerocytes of Haemoproteus columbae per10,000 red cells. The mosqu itoes were allowed rofeed overn ight and engorged females were collectedrlie next morning, placed in a sma ll cage, and main -tained on moist raisin s. The engorged indi vidualswere presumed to have had one blood meal durin g.the night.( 2 ) . Ten females were dissected on February 15.lO on February 17, 5 on February 21, and l O onMarch 10. All of these exami nations showed midgutsnegative for Haemoproteus oocysts.Exp eriment II: ( 1). On April 30, starved andthirsty females of C. quinquefasciatus were liberatedinto a cage with a pigeon showing 175 gametocytes per10,000 red cells. These mosqu itoes were allowed toremain in the cage wi th the pigeon thr ough out theexperiment and some of the engorged individualspresumably had more than one blood meal.( 2) . Fifteen fema les were dissected on May 9, and18 on May 16 with completely negat ive findings.Experi ment III : ( 1 ) . On May 8, 10 starved andth irsty C. quinquefasciatus females were liberated intoa cage with a pigeon showing 250 gametocytes per10,000 red cells.( 2 ) . On May 9, after about 18 hour s, all of thesefemales were dissected with the ' following result s :four females showed no evidence of having taken ablood meal; six females were partially to comp letelyengo rged and stomach smears treated with Giernsa 'sstain showed many garnetocytes of Haemoproteuscolum bae still within red cells and some exoerythro-cytic rou nded macrogarnetocyres. Some extrace llu larFIG. 2. Glo bularforms ofmacrogamerocytes of Haemoproteus columbae .after breakingout of red cells. (A) Sme~r of heparinized blood from infected pigeon. Note that onegametocyte is just breaking away from red cell. (B) Smear from midgut of Aedesalbopictus one hou~ after engo rging on in fected pigeon. (Smears treated ' with Giemsa's .. -. . stain. Phoromicrograph by .Dr. G. .B. Mainl and ; slightly. retouched. )· Haemoproteus of Pigeon s-KARTMANmi crogarnerocyres were noted, but a dil igent searchfailed to show defini te eviden ce of exflagella tio n.All th e round ed gametocytes were morphologicallysim ilar to th ose found in smears made from hepar-inize d pigeon blood ( see Fig. 2 ) . N o oo kinetes wereseen an d most of the garnetocytes were int racellu laran d typi cal halter forms, indicating probable im-maturity.Experiment III also includ ed observa tions on A edesalbopictus (Skuse) . Starved and th irsty fem ales ofthis species were liberated into th e cage on May 8along with the other culicine described above . Twoof these fem ales were dissected 1 hour after feedingon the infected pigeon and stomach smears showeda few rounded macrogarnetocyres . On May 9, abo ut20 hours after bei ng pl aced in the cage ; five engorgedfemales were dissected. Stomach smears' again re-vealed some rounded macrogametocytes. Ten ad di -tion al females were 'dissected on May 15 and 15 morewere exam ined on May 23. All rnidguts were nega-tive for oocysts.As in th e case of Culex quinquefasciatus, thestomach smears of A. albopictus showed a fewrounded rnacrogametocytes, some extracellular mi cro-gametocytes, and many halter forms still with in in-tact red cells. No ookinetes were noted,Experiment IV: An attempt was made to infect thehippoboscid fly ( Oljersie aenescens Thom son }; .whichis normally found on ocean birds. The flies used werecollec ted by employing a juveni le red-footed booby,Sula sula rubripes, as a decoy. About 36 O. aenescenswer e brought to the laboratory on February 28 . Tenwere dissected the next day and were found negativefor evidence of oocysrs on the m idgut. On February29, 20 of these flies were liberated in a cage with aninfected pigeo n show ing 230 garnetocyres of Haemo-protem columbae per 10,000 red cells. Most of the fliesseemed attracted to the lighter side of th e cage andwere not apparen tly interested in the pigeon . Severa l131flies were found dead on each succeeding . day andnone was seen flying about the cage after 7 'days. OnMarch 10 th e pigeon was rem oved from the cageand only one O. aenescens was recovered from it.D issection of th is fly showed fresh blood in the m id-gut , but there was no evidence of oocyst format ion .Experiment V : Four puparia were collected fromthe captive Ol jersi« aene scens described above. Atroom temperature two of th ese hatched in from 52to 53 days, but the others failed to emerge. The twoflies were pl aced on an infected pigeon on April 24,and both immediately ran underneath the fea thers.On ' May 4 these .two flies were taken from the bir dand dissected with negative findings.SUMMARY1. Observations have been made on the halteri-dium parasite of the pigeon, H aem oproteuscolumbae Kruse , 1890, in pige ons from loftsat the Honolulu Zoo.2. The hippoboscid vector, Pseudolynchia can-ariensis (Macq.) , was found to be presentat an average rate of 2.0 per bird on about50 juvenile pigeons and 1.3 per bird on 100adult pigeons. Of 45 doves examin ed, noneharbored this fly.3. Of a total of 25 P. canariensis dissected, 9 or36.0 per cent were found to be natur ally in-fected with the pigeon Haemoproteus.4. Of 101 adult pige ons examined by the bloodsmear technique , 83 or 82.2 per cent werepositive for Haemoproteus columbae. Of 43doves examined, none was found infectedwith the pigeon parasite or any oth er bloodprotozoan.FIG. 3. Left: Oocyst of Haemop roteus coln mbae on midgut of Pseudolynchia canariensis. Approx.950 x . Right: Oocysrs of H. columbae on hindgut of P. canariensis. Approx. 44 0 X .1325. Attempts to transmit the pigeon H aemo-protett s to three species of doves and toayoung chicken, either by means of the flyvector or by inoculation of macerated flies,proved negative.6. Ookinetes and oocysts failed to develop inCulex qttinqttefasciattts Say, Aedes albopicttts(Skuse) , and Olfersia aenescens Thomsonwhen these species were allowed to feed oninfected pigeons. O. aenescens did not feedreadily on pigeons. Smears of the stomachcontents of engorged female mosquitoes ofboth species showed mainly halter forms inred cells and some rounded macrogameto-cytes, Some extracellular microgametocyteswere also noted but definite evidence of ex-flagellation was not found .Ackn owledgments: Thanks are due the fol-lowing persons for their aid in these experi -ments: Paul Breese, Di rector of the HonoluluZoo, for generously allowing complete freedomin observations and examinations of pigeonsand other birds; Jane Y. C. Yuen for her aid intaking blood smears and for laboratory help;-Dr. D. D. Bonnet, Territorial Board of Health,for supplies of larval and pupal Culex qttinqtte-fasciattts; Dr. Frank Richardson, Assistant Pro-fessor of Zoology, Uni versity of Hawaii, forhelp in collecting hippoboscid flies from oceanPACIFIC SCIENCE, Vol. III , April , 1949birds ; and Dr. J. Bequaert, Harvard Museumof Comparative Zoology, for identifying theOlfersia aenescens. Appreciation is also due theUniversity of Hawaii Agricultural ExperimentStation for the use of certain of its facilities.REFERENCESADIE, H. A. 1924. The sporogony of Haemo -proteas columbee. Soc. Path. Exot., Bal.17(7): 605- 613.ALICATA, J. E. 1939. Poultry parasites. HawaiiA gr. Expt. Sta. Rpt. 1938: 79-82 .--- 1947. Parasites and parasitic diseasesof domestic animals in the Hawaiian Islands.Pacific Sci. 1 (2) : 69-84.BEQUAERT, J. 1939. Hippoboscid flies fromNorth American doves. Science 89 (2308):-267- 268. -BRYAN, E. H., JR. 1934. A review of the Ha-waiian Diptera, with descriptions of -newspecies. H awaii. Ent. Soc., Proc. 8(3): 399-468.COA'fNEY, G. R; 1933. Relapse and associatedphenomena in the Haemoproteus infection ofthe pigeon. Amer. JOM. Hyg. 18(1 ): 133-160.FISHER, H. I. 1948. The question of avian in-troductions in Hawaii. Pacific Sci. 2 (1 ) : 59-64.HUFF, C. G. 1932. Studies on H aemoproteasof mourning doves. Amer. JOM. Hyg. 16('2):618-62 3.W ENYON, C. M. 1926. Protozoology. Vol. II.ix + 784 pp, 128 figs. Bailliere, Tindall andCox, London.

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Observations on the Haemoproteus of Pigeons in Honolulu, Hawaii

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