The JapanSocietyJapan Society ofMedicalEntomologyof Medical Entomology and Zoology
(Jap･ J, Sanit.Zool,Vol. 32 No,4 p. 301-3081981)
Blaekfiies (Diptera: Simuliidae) in highland streams in Guatemala, with special referenee to the seasonal prevalenee of immature stages and voltinism'
Takao OKAzAwA*' and Hirosi TAKAHAsl"*
** Biolo.oical Institute, Faculty of Science, Hokkaido University, Sapporo, Hokkaido 060. JaPan *'* Ha)'amiya I-40-IO, Nerima-ku, Tokyo l76, JaPan
(Received: June 18, 1981>
Abstract: Immature stages of blackflies were studied in uppermest part of 2 streams in Guatemalan highland, Sierra Madre. In total 5 species, Gigantodax tt'righti., Simulium (Simttlium) tricornis, S. (S.) anduJei and S. (S.) fobbinsi in descending order of abundance, were collected. G, terTi.ohti and S. (E.) sp. svere preclominant and occupied more than 80% of the total specimens collected from each stream, All the 5 species appeared at higher density in the rainy season and the first half of the dry season than in the Iatter half ef the dry season. From thc head width distribution in each month, G, wrighti and S. (E.) sp. were found to be multivoltine species. G. tt]righti had two generations in the rainy season to the first half of the dry season and possibly one generation in the latter half. S. (E,) sp, had 2 generations in the rainy season, and at least one more generation, possibly two, Ln- r.he dry season.
Many studies on seasonal prevalence, ciasis, In the present paper tropical highland growth and ]ife history of blackflies have blackflies in Guatemala were studied on sea- been undertaken (Sommerman et al., 1955; sonal prevalence of immature stages and Davies and Syme, 1958; Ladle and Esmat, voltinism, including a species of the genus Gi- 1973; Hansford, 1978; Wotton, 1978 etc.), gantodax. Gigantodax is one of the phylo- but intensive studies have been restricted to genetically interestin.rr. genera, which is dis- the middle and high latitudes of the northern tributed from the southern end of South
hemisphere. Little has been studied on Meso- America to Mexican highland along the ameriean and Southamerican species except Andes and bevond the Isthmus of Panama. " for the vecter species of human onchocer-
'-g ' STuDY AREA AND IV(ETHoDs
This study was supported by the Ministry Collections were made in streams, of Public Health, Guatemala and Japan 2 the International Cooperation Agenc>' CJICA). Tzojoma and the Sesenta Vueltas in Guate- GJCRCPO-MENSAP Series No.40 malan highland, Sierra Madre, located north ** Present address: Department of Microbielogy, of Lake AtitilEn as shown in Fig, 1. Both 840- Saga Medical College, Nabeshima, Saga streams are small tributaries and rise near Ol, Japan the ridge of the mountains, which has almost ** ,trr e; "}f: i; ma V" if kit : L[L me Jl< if ss glj #va tw S (+ 060 Tr 3,OOOm of altitude. They fiow for about *L Nrti tiic rK :k 10 ec ut 8 fi ) 100 m from the source on the gently inclined -trJfi: iZlesXT+Jit#dilktz#XS (+840-Ol slopes, then run down along the steep slopes iL{ es Tti S& E =- lr Ef ) *** to the with the main rivers. Sam- t･-･-,ts i.･L: (+176 MA'XEkt.eeIg41El-40-iO)301 junctions
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Fig. 1 Topography of study area Arrows indicate the sampling sites, A: the Tzojom5 Stream. B: the SesentaVueltas Stream,
pling sites were chosen in the uppermost, were about 15 and 3 cm, respectively. Month- gently inclined part. The sampling site in ly change of mean maximum and minimum the Tzojoma (A) is close to the highest point temperatures and precipitation in Totonica- of the Central American Road No.1 be- pan are shown in Fig.2. The maximum tween Nahua15 and San Cristobal Tetonica- temperature is almost constant throughout paii, where the departmental border line the year. The minimum temperature is vari- between Solola and Totonicapan lies. The able, being higher in the rainy season than Sesenta Vueltas crosses the National Road in the dry season. The water temperature in No. 1 about 6km from Encuentros to Toto- nicapan. The site is situated at upstream of
the crossing. AItitudes of the sites in the
Tzojoma and the Sesenta Vueltas are 2,9eO mmoe and 2,850m, respectively. The site in the c Tzojoma is surrounded by and ,9 grassland -tu00
wheat fields, and the site in the Sesenta -" ,g Vueltas by grassland with low shrubs and g ioe vegetable fields. The stream-bed consists of hard mud. Short hydrophilous grass grow out of water along the margins of the streams,
JFMA MJJASOND The width and depth of the streams in the Month seasen of maximum water discharge were Fig. 2 Mean maximum, minimum tem- about and cm respectively, while the 40 10 in peratures and precipitation during 1954- season of minimum water they the discharge, 1959 at Totonicapan
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the Sesenta Vueltas was constant,, approxi- by Okazawa in November 1977 to October
mately 120C irrespective of time of measure- 1978, and 1 sample by Takahasi in Novem- ment, except March 1979, when it was 160C. ber 1978 to June 1979. All specimens col- The temperature in the Tzojoma fluctuated lected were kept in 70% ethanol, After
between 11 and 170C, with a tendency to- species identification, head widths of all Iar- wards being cooler in January to February vae were measured. and warmer in April to December. The val- ]ey of Tzojema faces southwest and is sur- REsuLTs rounded by grassland, therefore the isola- tion in the afternoon rnay affect the ground The species and number of individuals col- and water temperatures, while the valley of lected are shown in Table 1. In total, 5 the Sesenta Vueltas faces east, resulting in species belonging to 2 genera were collected, rather constant water temperature. In the TzojomE, Simulium (Eusimulium) sp. The rainy season generally begins in May was the most abundant and was followed by and ends in October. Increasecl water dis- Gigantodax ietrighti and Simulium (Simu- charge was observed 1 or 2 months after the lium) tricornis in descending order, while
beginning of the rainy season. The decrease in the Sesenta Vueltas, G. wrighti was the was observed also 1 or 2 months after the most abundant followed by S. (E.) sp,, S. end of the rainy season (Figs,2 and 3). In (S.) tricornis, S. (S.) andu2ei and S. (S.) the later half of the dry season, Ns'ater leveJ 1'obbinsi. G. zvrighti and S. (E.) sp. were was very low, with only a slight trickle of predominant species,' a total of the 2 species water, occupying more than 99% ef the total speci- For inve$tigation of seasonal prevalence, mens collected in the Tzojoma and 81flc in a unit time collection was adopted. Larvae the Sesenta Vueltas, and pupae attached to submerged plant mat- Seasonal prevalence of each species is ter were collected by forceps for ]Omin. shown in Fig.3. G. wrighti was abundant Thoroug.h searching for sirnuliids on each during the period from the rainy season to substrate was made to avoid the bias to larg- the first half of the dry season, but scarce er individuals onlv which are easier to find in the latter half of the dry season. It seems - out and pick up, Once collection was started that there existed 3 peaks in abundance, 2 with a substrate, it continued till all simuliid of them in the rainy season and 1 in the dry Iarvae were completely picked up from the season. However, at the Sesent Vueltas dur- same substrate, then another substrate was ing the rainy season only 1 blunt peak in taken. Samplin.cr was carried out once a July to October was observed. A]l the peaks month. At cach time 2 samples were taken in the Sesenta Vueltas appeared later than
Table 1 Number of blackfly larvae and pupae collected in 2 streams in highland Guatemala during a period ef 1 year, from November 1977 to October 1978 in the Tzojoma Stream and from May 1978 to April 1979 in the Sesenta Vueltas Stream
Tzojomi (A) Sesenta Vueltas Spccies No. of (B) Ne, of
Larvae Pupae %* Larvae Pupae %*
Gigantodax wrighti Vargas, )vlartines and DEaz 945 6ooo172337.0 1,399 IO 66.3 Simulium (Simutium) anduzei Vargas and D{az o O 98 4 4.8 Simuliurn (Sinzulium) J'obbinsi Vargas, Martinez and Diaz o O 89 2 4,3 Sin!ulium (Simuiium) tricornis De Le6n 21,601 O.1 203 O 9.5
15.1100.0 Simulium (Eusimutium) sp. 62.9 309 11
Total 2,S48 100.0 2,09827
' Percentage of number of larvae and pupaeto the totalcollections.
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304 Jap. J, Sanit. Zool. ttttttttt .:[,.,,.."::,.)ctt;S:;,V,k,V..t,{/tl'ttlt wL!lgtt!!ltlll'L'i'il,i".l:[lii'f'1/')'1',l'l't':),C-AT2ejomA 180G;antdaxttttttt L.lyfSS, ±."..,- "i,};].l{'fiil,Slt/IIIil}{':.,lii`l{[I[-Bsesentavueltas 150120906030 l fi
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.S..Pv'S[ tttt.\,.f.Z,l.ft.tt..::S/.s...... oa>Le-oLdinE=zo150$imuliumsp.I;ltl'//{t'lil,l'/II[ll1/,ill'illl://ll'i;/l'l-A .tCt)tt))!tCtt:ttAttt.. ll'/1/Ll'll/1/:1/Il,lttt, "'"t#')'.'.'s\v'sul':'::"=[" /ti･;']...[.lie='C';[l[:ill;'t;1{/llt:, B 120 {/:.",;･.g'llll'I{I･,l'illl･i･l,:i*E:i･.I'1.l/ii'l/1/l/l?l･l･i･ 9060 /lill,I:･1･1/llil}:::.i,li};.i:Ill,ltl' :･l'i//･i',riC;i, :,ls;i}li･ls ll',･l]'I):･:ll,li",jiil･l,l;llli･i.'if't･ii.I･i; {t.'s-':',i}i,}1:El.lIi;',,:l/1:,l.it ttt 30 t]././tt.;..ttlt.ttttt.t. tt..t ''":.;.:l'l::'''.:l'l;lctttttttttt.ttttt'."'.,'s' ''`l'i!:tt.,tCt.'"tt t-ctt'' o' ttttt t imulium enduzei,,,':,.i.'･'･' ...･:･･,. 6030-----s. igtUb!nslbbtnsl'l:;i':'1'･l･lhA,,.'.,.Es.:',.,:. ----･-････-s.'ww,.,:,.i,::,-l,i･i･,:.,Ili;･z'Y'1･i･:･'IL･...?i/1,l.;･,:.i･1,. u',i.-.ir..tMs''...,' ..4 tttttt.l..th.t.lt..---j.,h,. ttt.t.S olsec64=-=:::----･A=.==B tt..tt...,.ttt ..fttt'A ttttttttttttttttttttt tt e tttttttttttti{,Ii･l-,ll,･l･lli#.tYl･1y･I･i･i･:;･,Ii･l,i･..,1'il,l･;,1if.'tt ℃ e2o il;1.;:v;;:;-v,,d{..',' -;i;['1[ff eaLrese,vea g.,6 sl/lllL{'itl{:,;/l,/･://';';ili},il･l-Ei,i:,--'""L-..,i:[iL･:S'lll･･ l:t'':''';'':::;"''"' ---ttf["':' E.12 "le'...･'::･I･l･,,r,.:･;///ll,.I{f,l'.vl..i･l',Itt}f',l----....':.'1: 2 :･};l,;Stl,; -.-'--.t...... -- l:: ts.L s{,a}e".{#.}sltl.-,#l"-V' tttttttttt E:,1.:t..',..l,, wd tttctt)ttt4ttttltttft t-t' oNDJF s3 J77･78MAMJJASONDJFMAMJ ･reMonth
Fig. 3 Seasonal prevalence of 5 sirnuliid species and stream conditions The rainy season is shown by patched area, wd: volume of water discharge, wt: water temperature.
those in the Tzojoma. Seasonal prevalence from May to December, or from the begin- ef S. (E.) sp. was similar to that of G. ning of the rainy season to the month when zvrighti. It was abundant in the rainy season the water discharge decreased, 2 clearly dis- and scarce in the dry season. There were tinguishable successive cohorts were observed
dry 2 clear peaks in the rainy season in both in both streams. In the middle of the streams and 1 peak in the dry season in the season, young larvae of another cohort ap- Tzojoma though it was absent in the Sesenta peared, but this cohort disappeared in the Vueltas. Larval density of both species sud- late dr>r season before maturing in the Se-
denly increased at the beginning of the rainy senta Vueltas. This suggests that G. wrighti season, when the water discharge was still has at Ieast 2 generations, possibly 3 genera- low. Other 3 specie$ show similar patterns, tions per year. The appearance of young that is, a few individuals appeared in the larvae corresponded to the peaks in the sea- beginning of the rainy season, and then the sonal prevalence. The first generation in the density increased at the end of the rainy rainy season appeared without overlapping season, The relatively high density level was with the generation in the dry season. This maintained in the first half of the dry season, generation appeared earlier in the Sesenta Figure 4 shows the size distribution of Vueltas than in the Tzojoma, but the other larval head widths of G. torighti for each generations in the Sesenta Vueltas appeared menth in the 2 streams, During the period, later than in the Tzojoma, In S. (E.) sp.
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40
Gi antodax mptt
40o40May･7s B
June 40
o40o July 40
canyre=v-->--vc----oLoDE=z8040 8040Aug-
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-5 8 11 14 17 20 23 26 29- P -5 8 11 14 17 20 23 26 29- P {40 mits = 1 mm} Width of head capsule
Fig. 4 Frequency distribution ef head-width of Gigantodax wrighti
in 2 streams A: the TzojomE Stream, B: the Sesenta Vueltas Stream, P: pupae.
at least 3 generations could be detected in senta Vueltas, 2 generations were recognized the Tzojoma, although 2 consecutive genera- in the rainy season. The first generatien ap- tions tended to overlap each ether (Fig. 5). peared in the beginning ef the rainy season, Young larvae appcared in each of the 3 May (1979) or June (1978). It is not clear periods, June, August to September and De- when the second one appeared, but the in- cember to April. In the dry season, the creased density of small larvae in August and
density was very Iow, however this species September suggests the existence of another appeared to pass 2 generations. In the Se- generation. In the dry season, larval density
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306 Jap. J. Sanit. Zool.
30
o30oo
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ooo ' 30
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Fig. 5 Frequency distributionof head-width of Simulium (Eusimu- lium) sp. in 2 streams Stream, A: the Tzojoma Stream, B: the Sesenta Vueltas P: pupae.
to April, Davies and Peterson in was very Iow, especially in January by (1966) (1977) as the shapes ef basi- l979, no Iarvae were collected. some characters such mere, ventral plate of male, cercus of female DIscussloN and head spots of larva. Stone (1965) stated is an that S, (E,) aureum in North America species complex. Therefore, we Simtilium (Eusimulium) sp. was treated by unrevised treated here the Guatemalan specimens as Dalmat (1955) and Vargas and Dfaz Najera the S. sp. not as S. aureum. S. (1957) as S. (E.) aureurn (Fries). But (E.) (E.) (E.) related to S, aureum and Guatemalan specimens are rnorphologically sp. is closely (E.) the aureum-group different from S. (E.) aureum redescribed assigned as a member of
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of subgenus Eusimuli･ttm defined by Davies The larvae of S. (E.) sp. appeared all year (1966). round, thou.crh the density of larvae decreased On tl)e vertical distribution of immature in the late drv season. / sta.cr.cs ef blacl{flies in tropical Amcrica, only Dalmat (l955) studied the growth period the work of Dalmat (1955) is available, In of G. aqitamarensis in Guatemala. In his his studs,, he dis,ided the altitude into 7 work, G. aquat7iarensis required 50-63 days it cate.crories. The ]najority of individuals ef for larval development and 5-9 days for G, tvri.ahti, S. (E.) sp, and S, (S.) tricornis pupal devclopn]ent. Judging his rcsults and were collected in the highest and the second our observation that variouslv ' sized larNJae highest categeries, above 1,800 m of altitude, "'ere always present at high density froni though I)e did not show the number of sam- January through September (unpublished, no ples taken from each categor}r. TIie 2 streams data available in rest 3 months trom October under the present study belong to the hi.crhest to December),, G. aquamarensis may be cate.crory of the Dalmat's division. abovc 2,100 multivoltine in Guatemala. G. wrighti was m of pltitude, Thc present authors collected bivo]tine or possibly inultivo]tine in highland thcse S specief;, also in other streams above Guatemala. These su.cr.gest that the species
of the the tropical rc- 2,200m of altitude. G. wrighti and S. (E.) .oenus Gigantodax in sp. were found mainly in the uppermost of gion are not univoltine, but multivoltine. the streanis, some of which dried up in the As the breeding stream of G. aguamarcn- later half of the dry season. No larvae and si's, only one stream, Rio Asruas Amargas, in pupae xvere collected by morc intensive sur- Zunil, Quezaltenango, has been known, vey below 1,o'OO m. From those, these 3 spe- xvhich water discharge is fairJy constant, ap- than through- eies can be called as the highland species. proximate]y more 5 literslsec, Thev tt m.e,v breed in the streams abeve 1.800t out the },･ear. pH is vevy low, being 4.5. m of altitude. Only the ]arvae of G. aquamarensis wcre col-
Difference in the relative abundance of lected in that stream. The larvae appeared each speeieg between the 2 strearns in the successively all >,ear round. On tlie other hand, of present study might be derived from the dif- in the brceding strenms G, ivrighti, ference of water velocity. S. (E.) sp. prefers water dischars,e was seasonally changed. In lower velocity than G. zvrighti. The Sesenta the late dry season larvae of G. tt,righti al- Vueltas is relatively steeper than the TzojomA most disappeared in the uppennost part of
nnd the water velocity in the Sesenta Vueltas the streams. It is sti]I unknewn in what
is higher than that in the T7ojomEl. stage and where the majority of this species Life cyc]es or i,o]tinism of thc species in pass the late dry scason. the present study or taxenomically relatcd ACKNOWLEDGE]IENTS species are knox･s,n very little. S, (E.) aureum is comparable with S. (E.) sp. Rubzow The authors aie grateful to Dr. T. Suzuki, the in Europe, Lewis and Bennett (1959-1964) Teain Leader of the Project on Onchecerciasis Ezenwa and Back and Har- (1973), (1974) Research and Control in Cuatemala, Dr. K. in North America reported the per (1979) Uemoto, Shiga Un:,vcrsity of Medical Scicnce, and cycle ef aureum. these life S.
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： taxonomy of Davies， L ．（1966） The British 385．
blackHies Diptera ； Simuliidae Trans R Stone A 1965 ： Family Shnuliidae In A （ ）． ． ． ， ． （ ） ， − Entomot ．∫oo ．五 〇 nd ．， 118 ： 413 511 ， catalog of the Diptera of America north of D ， ． and P ， ， Syme 1958 ： Three new Davis， M D （ ） Mexico． Stone，A ．，C ．W ． Sabrosky，W ．W ． Ontario black flieso ［ the Prosimulium Wirth R ． H 。 Foote and ． R．． Coulson eds ． genus ， J （ ）， Diptera こ Simuliidae ． Part II． Ecological ob − こノ S 1）eP Agric ∠【 ‘ 正1andb ： 181 −189 （ ） ． ． ． ． gri ． ， ．， 267 ．
servat 三〇 ns and experiments ： and ； − ．Can ．Entomol．，90 Vargas， L ． A ．Diaz Najera （1957） Simu 744 759． 1idos Mexicanos． Rev ． Inst． Salubr． Enferm ．
； of τ 70 ） ハf6 κ ピ‘o ， 17 ： 143 −399 Ezenwa ， A ．0 ．（1974） Ecology Simuliidae， メ．， Cit）， ． − − − Mermithidae ， and Microsporida in Newfound Wotton ， R S ．（1978 ）： Lifehistory and produc − Iand freshwaters． Can ．∫． Zool ，，52 ： 557 565． tion of blackHies （Diptera ： Simu1 三idae） in
Hansford R ． G ， 1978 ： Life−history and dis− moorland streams in ， （ ） Upper Teesdale Northern − − tribution of Simulium austeni （Diptera ： Simu Eng 艮and ． ∠4rch ． Hydrobiol．，83 ： 232 250． liidae） in relation to phytoplankton 三n 50me southern English r 三vers ． Fresh ω ater Biol．， 8 ： 521 −531 ， 摘 要
Ladle M ． and ： ． ， A ．Esmat （1973＞ R ecords of グ ァ テ マ ラ共 和 国 の 高 原 の ブ ユ と そ の Simuliidae 三 Bere （D ptera ） from the Stream， の お よ び Derset， with details of the life history and 個体数密度 季節変動 化 性 larval of Simulium Eusimulium latiPes ・ growth （ ） グ ァ テ マ ラ共 和 国 の 高地 ， シ エ ラ マ ド レ の 標高 ＿ Meigen ．Entomol．Mon ．Mag ．，8 ： 167 172． 〜 つ 2，800 2， 900rn か ら流 れ 出 る 二 の 川 の 最上 流 で ， Lewis D and G F Bennett 1973 ： The black− ， ． ， ． （ ） ユ ブ 相 ， 幼虫 と 蛹 の 個体数密 度 の 季 節変動 ，お よ び そ − Hies （Diptera： Simuliidae） of insular New の 化 性 を調 べ た ．採集個体数 の 多 い 順 に ，Gigantodax foundland ．1， Distribution and bionomics． Can ， wrighti Simulium Eusimutium sp Simulium ， （ ） り ．Zool ．51 ： 1181− 1187． ノ ， 〈Simulium） tricornis ， s ．（s ．） anduzei s ．（s ．） う一 − ， jo Peterson， B ． V ．（1977 ）： The black flies of Ice binsiの 2属 5 種 が採集 され た ． G ． wrighti と 3．（E ．）
1and （Diptera： Si皿 ul 三idae）． Can ．Entomol リ は に こ sp ． 特 個体数が多 く， の 2 種 の 合計 は それ ぞれ 109 ： 449−472． の 川 の 総採集個体数 の 80％ 以上 を占め た ．採集 され A 1959− 1964 ； Simuliidae Melu − Rubzow ， 1． ．（ ） （ た 5 種 の 個体数密度 は 雨 季 の 始 ま り か ら 乾 季 の 前半 ま sinidae Reg ）， in Die Fliegen Paraearkt， ．， で 高 く， 乾 季 の 後 半 は低 い ．各 月 の 幼虫 の 頭 幅値 の 頻 Lindner E ． ed ． Vol 」 4 ．1−689 ． ， （ 〉， ， pp か ら G wrighti 1 度分 布 ， ． は 雨季 に 2 世代， 乾季 に 世 and − Sommerman ， K ．M ．， R ．1、Sailer C ．0 ．Essel 代 ，計 年 3 世代 ，＆ （E ．）sp ．は 雨季乾季共 に 2世代ず baugh （1955 ）： Biologア of Alaskan black flies つ ，計年 4 世 代経過 す る も の と 考 え ら れ る ． Simuliidae Diptera ． Ecot Monog ． 一 （ ， ） ， ，25 ： 345
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