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The subgenus Persicargas (Ixodoidea: Argasidae: Argas), 26. Argas (P.) arboreus: Effect of photoperiod on diapause induction and termination
EXPERIMENTAL
PARASITOLOGY
The
40,232-237
( 1976)
Subgenus Persicargas (Ixodoidea: Argasidae: 26. Argus (P.) arboreus: Effect of Photoperiod Diapause Induction and Termination M.
GALJLA Medical Unit
Zoology Number
Department, United Three (NAMRU-3), Arab Republic
(Accepted
for publication
Argus). on
KHALIL
States Naual Medical American Embassy, of Egypt 24 November
Research Cairo,
1975)
KHALIL, G. M. 1976. The subgenus Persicargas (Ixodoidea: Argasidae: Argus). 26. Argus (P.) arboreus: Effect of photoperiod on diapause induction and termination, Experimental Parasitology 40, 232-237. Prefeeding exposure of female Argas (Pemicargas) arboreus to short photoperiod (SP) induces diapause, expressed as oviposition delay for more than 40 days postfeeding. Diapause incidence increases as prefeeding SP exposure periods increase. Postfeeding SP exposure is not essential to maintain diapause. Postfeeding exposure to SP without prefeeding SP exposure does not induce diapause. A 2 week prefeeding exposure to long photoperiod (LP) terminates diapause in two-thirds of the females exposed to LP after feeding. The remaining one-third, which may differ genetically, require a 6 week LP prefeeding exposure to terminate diapause. An 8 week prefeeding exposure to LP is required to terminate diapause in females exposed to SP after feeding. INDEX DESCRIPTORS: Argus (Persicargas) arboreus; Argasidae; Argasid tick; Photoperiod; Diapause; Oviposition.
During the fall-winter facultative dia- diapause induction and termination, respecpause in nature, female Argas (Persicar- tively, in field-collected female A. ( P. ) gas) arboreus Kaiser, Hoogstraal and Kohls arboreus. delay oviposition until spring (Guirgis 1971; MATERIALS AND METHODS Khalil 1974). Field-collected females held Unfed female A. (P.) arboreus (with a under the constant temperatures of 26, 30, 34, or 37 C after feeding did not alter dia- flat body) were collected in July (midsumpause incidence (Khalil and Shanbaky mer) fram trees supporting nests of Bubul1976); thus temperature does not appear to cus i. ibis in the rookery at the Delta Barrage, Qalyubia (‘the type locality of this be a factor controlling diapause termination. Preliminary experiments showed that ex- tick species). posing female A. (P. ) arboreus to a long In the laboratory, LD cycles were conphotoperiod (LP) of LD 16:8 (1ight:dark trolled by two Paragon 7-day timers, each attached to a 4-W cool white fluorescent hours per day) during fall-winter interfered with diapause but a short photope- lamp inside a light-tight container 16 x 18 riod (SP) of LD 9:15 induced diapause. x 22 in. in size. A half-liter jar containing Therefore, we studied the influence of SP saturated NaCl solution in each container and LP before and/or after feeding on provided 75% RH. Both containers were 232 Copyright All rights
0 1976 by Academic Press, Inc. of reproduction in any form reserved.
AND DIAPAUSE IN Argus (P. ) arbmeus
PHOTOPERIOD
placed in an environmental chamber at 26 C ( -tl C). Photophases of 16 and 9 light hr per day represented LP and SP, respectively. Half of the field-collected females were subjected to LP (Stock 1) and the other half to SP (Stock 2) for 10 weeks before beginning the experiments.
233
were moved to the LP container. At weekly intervals, as above, they were fed and divided into two subgroups; one subgroup was returned to LP and the other to SP. Control ticks (30-35 females) from SP Stock 2 were fed at weekly intervals simultaneously with the LP experimental groups. After feeding, the control ticks were maintained in SP. Laboratory hosts in all tests were domestic pigeons. Immediately after feeding, each female was placed in a polyethylene tube with a fed male and observed daily for oviposition. Females ovipositing after more than 40 days were considered to have been in diapause (Khalil 1974). The statistical significance of the data was determined by the test of proportions.
SP Influence on Diapause Induction Ten weeks after collection, 11 groups, each of 60-85 unfed LP Stock 1 females, were moved to the SP container. At weekly intervals, beginnmg on the day of transfer from LP to SP, one group was fed and divided into two subgroups; one subgroup was returned to LP and the other to SP. Control ticks (30-35 females) from LP Stock 1 were fed at weekly intervals simultaneously with experimental groups subjected to SP. After feeding, the control ticks were returned to LP.
RESULTS
SP Effect on Diapause Induction (Fig. 1) SP before and after feeding. The diapause incidence of females exposed to SP for 1 week ( 6% ) did not differ significantly (P>O.4) from that of females exposed to
LP Influence on Diapause Termination Ten weeks after collection, 11 groups, each of 60-90 unfed SP Stock 2 females
).-.-.. ,
0
WEEKS
FIG. 1. Short long photoperiod;
photoperiod SP-short
2
3
OF EXPOSURE
I
5
6
7
8
T O SHORT PHOTOPERIOD
effect on diapause photoperiod.
induction
in
9
10.
BEFORE
FEEDING
female
Argus
(P.)arboreus.
LP-
234
GALILA
M.
LP before feeding and to SP only after feeding (0% ) . Diapause incidence gradually increased wi’th increased exposure to SP before feeding; diapause was induced in 50% of the population after exposure to SP for 6 weeks and in 90% after 10 weeks. Control groups exposed to LP and fed simultaneously with experiment’al SP groups rarely (212% ) delayed oviposition for more than 40 days. SP before feeding and LP after feeding. Diapause incidence in these groups was not significantly different (P>O.O5->0.9) from the corresponding groups exposed to an equivalent SP period before feeding and to SP after feeding. The diapause incidence curves in both experiments were close in shape and overlapped in many parts. LP Effect on Diapause
Termination
ing (91% ). In both groups, diapause incidence was not significantly different (P> 0.2) from that of the control females maintained under SP and fed simultaneously with these experimental groups (65 and 87%, respectively). Diapause incidence sharply decreased (37% ) after exposure ,to LP for 2 weeks before feeding. No further significant change in incidence occurred after exposure to LP for 3-5 weeks (P> 0.8). Exposure to LP for 6-10 weeks terminated diapause in most or all (87-100% ) ticks. There was no significant change (P >0.05->0.8) in incidence in control groups exposed to SP and fed simultaneously with the experimental groups (64-82s ). LP before feeding and SP after feeding. Diapause incidence after exposure to LP for l-3 weeks was not significantly different (P>O.O5->0.2) from that of the control groups exposed to SP and fed simultaneously with experimental groups. Incidence in females exposed to LP for 4-7 weeks before feeding was at the same level (P> 0.05->0.9) as in those exposed to LP for 2-5 weeks before feeding and also after
(Fig. 2)
LP before and after feeding. About 26% of the females exposed to LP for 1 week terminated diapause. Diapause incidence ( 74% ) was not significantly different ( P> 0.05) from that of females exposed to SP before feeding and to LP only after feed-
,-,
LP
before
and
.--.
LP
before
feedIng
m--.
Co”troi.mal”tolned
KHALIL
oftar
feeding. and
SP after
feedIng
I” sp
0, 0
1
WEEKS
FIG LP-long
2
3
OF EXPOSURE
1
5
6
7
T O LONG PHOTOPERIOD
2. Long photoperiod effect on diapause photoperiod, SP-short photoperiod.
termination
6 BEFORE
in
9
10
FEEDING
female
AT~US
(P.)
arboreus.
PHOTOPERIOD
AND
DIAPAUSE
feeding. Diapause was terminated in most or all (90-100% ) ticks exposed to LP for S-10 weeks only before feeding. Therefore, the diapause termination curves were similar in shape for the group exposed to LP only before feeding and for the groups exposed to LP before and after feeding, except that the former curve was shifted to the right. The curves overl’apped only after S-10 weeks’ exposure to LP.
IN
Argus
( P. ) arborem
235
minate diapause. Switching the females to SP ‘after feeding prolonged the LP prefeeding exposure period necessary to terminate diapause to 4 and 8 weeks in twothirds and one-third of the population, respectively. The longer period (2 weeks) needed by ticks exposed to LP only before feeding may be owing to association of diapause termination with a physiological process( es) requiring about 3 to 4 weeks for completion in two-thirds of the popuDISCUSSION lation and about 5 to 6 weeks in the rePhotoperiodic regulation of diapause in maining one-third (oviposition by the nonadult ixodid ticks was reported for Dermadiapause female occurs 1 to 2 weeks after centor marginatus (Belozerov 1963, 1965a, feeding). b; Belozerov and Kvitko 1965; Belozerov A. (P. ) arboreus appears to be a longday species undergoing facultative diaand Lamnova 1967) and D. pictus (Razumova 1965). The present investigation of pause under the influence of SP. Diapause A. (P.) arboreus appears to be the first induction in fall and termination in early study of photoperiod effect on diapause in summer by short and long days, respecan argasid tick. tively, is biologically significant because The results indicate that exposing female herons, the natural hosts of A. (P.) arborookery A. (P.) arboreus to SP before feeding is reus, disperse from the tick-infested essential to induce diapause. Switching SP in late September and return in late March (Guirgis 1971). If tick eggs were laid durfemales to LP after feeding does aot alter ing the fall, emerging larvae would be ,dethe prefeeding SP effect, thus postfeeding exposure to SP is not essential to maintain prived of a food source and die of starvadiapause. The organs affected by SP, i.e. tion (Guirgis 1971). In female A. (P. ) arboreus held outthe nerve ganglion andjor the ovary, are doors in natural fluctuating temperature probably vulnerable to SP effect only when the female is in the unfed state. conditions, diapause termination occurs in Fall daylength in Cairo (30”03’N, 31”15 April-May (Guirgis 1971, Khalil 1974). Diapause is of lower intensity in females E) is longer than the SP (LD 9:16) used (29 in this study. The critical photoperiod in- held at a nearly constant temperature or 30 C) but subjected to normal changes ducing diapause in nature in Cairo remains to be investigated. Decreasing daylength in of subdued dayligh,t, and is terminated fall (September through October) may inspontaneously in November-March (Khalil duce a higher diapause incidence (and/or 1974). “Diapause development” (Andreintensity) than that artificially induced in wartha 1952) or “diapause reactivation” (Belozerov 1968) m,ay proceed faster when this experiment. The effect of decreasing SP on diapause in A. (P. ) arboreus also these females are held under a constant temperature before and after feedmg remains to be investigated. (Khalil and Shanbaky 1976). In this study, two-thirds of the fem,ale Diapause induction in A. (P.) arboreus A. (P.) arboreus population exposed to may be assooiated with synthesis and/or LP for 2 weeks before feeding and also activation of an inhibitor, i.e. a diapause after feeding terminated diapause. The rehormone, for which prefeeding exposure maining one-third, which may be genetito SP is essential. Andrewartha et al. cally different, required at least a 6 weeks’ ( 1974) suggest that a hormone is generally LP exposure period before feeding to ter-
236
GALILA
present in insects with obligate and facultative diapause. If an inhibitor is present in diapause female A. (P.) arboreus, diapausc may be terminated when this inhibitor is slowly degraded after feeding. Exposure to LP before feeding may cause faster inhibitor degradation and permit females to oviposit within 1 to 2 weeks after feeding. However, dia’pause in A. (P. ) arhoreus may be associated with a lack of an activator, e.g., a gonadotropic hormone. In this respect, A. (P. ) arboreus may be similar to the Colorado potato beetle Leptinotarsa decemlineata ( de Wilde and de Boer 1961)) in which diapause is regulated by the titre of the circulating juvenile hormone. Synthesis and/or activation of the speculated hormone in A. ( P. ) arboreus may occur at a slow rate under SP and at a fast rate under LP. As in the adult mosquito Culex pipiens (Spielman 1974) and the alfalfa weevil Hypera postica (Bowers and Blickenstaff 1966), diapause is terminated in female A. (P. ) arboreus by topical application of a juvenile hormone analog [acetaldehyde, 2- (2-ethoxyethoxy ) ethyl p(methylthio) phenyl acetal] (Bassal and Roshdy 1974). A gonadotropic hormone becomes active in the nerve ganglion of nondiapause female A. (P.) arboreus within 3 days after feeding and is released afterwards in the hemolymph (Shanbaky and Khalil 1975). However, we believe that a combined inhibitor and activator lmechanism may regulate diapause in A. (P. ) arboreus. This bifactorial concept of hormonal regulation of diapause (Hinton 1953) seems to function especially in organisms undergoing facultative diapause (Maslennikova 1973). The role of one or more hormones in A. (P.) arboreus diapause regulation is under investigation in this laboratory. These investigations of factors controlling diapause in female A. (P.) arboreus provide background information for studying viral survival and multiplication in diapause and nondiapause ticks and for de-
M.
KHALIL
veloping a model for vector interrelationships.
studies
on virus-
ACKNOWLEDGMENTS From Research Project MF51.524.009-0055, Naval Medical Research and Development Command, Washington, D.C. The opinions and assertions contained herein are the private ones of the author and are not to be construed as official or as reflecting the views of the Department of the Navy or of the naval service at large. This work was assisted by Agreements 03-005-l (now 03-036-N) and 03-016-l between the National Institute of Allergy and Infectious Diseases (N.I.H.) and NAMRU-3. The author is indebted to Dr. Harry Hoogstraal for his supportive interest and critical reading of the manuscript. REFERENCES ANDREWARTHA, H. G. 1952. Diapause in relation to the ecology of insects. Biological Review 27, 50-107. ANUHEWAIITHA, H. G., MIETHKE, P. M., AND WELLS, A. 1974. Induction of diapause in the pupa of Phalaenoides glycinae by a hormone from the suboesophageal ganglion. Journal of Insect Physiology 20, 679-701. BASSAL, T. T. M., AND ROSHDY, M. A. 1974. Argas (Persicargas) arboreus: Juvenile hormone analog termination of diapause and oviposition control. Experimental Parasitology 36, 3439. BELOZEROV, V. N. 1963. Day length as a factor determining oviposition delay in female Dermacentor marginatus Sulz. ( In Russian ). Meditsinskaya Parazitologiya, Moskva 32, 521-526. (In English NAMRU3-T389). BELOZEROV, V. N. 1965a. Diapause in ixodid ticks. (In Russian) Doklady na l&-17. Yezhegodnykh Chteniyakh Pamyati N. A. Kholodkovskogo (April 3, 1963-ApriI3, 1964), p. 1233. BELOZEROV, V. N. 1965b. A developmental stage of Dermacentor marginatus ( Sulz. ) sensitive to photoperiodic effect. (In Russian) Meditsinskaya Parazitologiya, Moskva 34, 52-57. BELOZEROV, V. N. 1968. Photoperiodic control of seasonal development of ixodid ticks. In “Fotoperiodicheskie adaptatsii u nasekomykh i Kleshochey.” ( In Russian. ) Leningradsky Ordena Lenina Gosudarstvennyy Universitet imeno. A. A. Zhdanova, p. 100-128. (In English: NAMRU3-T432 ). BELOZEROV, V. N., AND KVITKO, N.V. 1965. Main features of photoperiodic reaction in the tick Dermacentor marginatus Sulz. ( Ixodidae ). (In Russian ) Zoologicheskiy Zhurnal 44, 363-372. ,- . . ~~ (In English: NAMRUB-T190).
PHOTOPERIOD
AND
DIAPAUSE
BELOZEROV, V. N., AND LAMNOVA, A. I. 1967. Development of winter diapause and response to the day length in Demzacentor maginatus ticks in central Kazakhstan. Meditsinskaya PamzitoZogiya, Moskva 36, 464-l69. (In Russian). BOXERS, W. S., AND BLICKENSTAFF, Hormonal termination of diapause weevil. Science 154, 1673-1674.
C. C. 1966. in the alfalfa
GUIRGIS, S. S. 1971. The subgenus PeTsicaTgas (Ixodoidea, Argaside, Argus). 11. Ecology and seasonal dynamics of A. (P. ) aTboTeus Kaiser, Hoogstraal & Kohls in Egypt. Journal of Medical Entomology 8, 407-414.
HINTON, H. E. 1953.
The and rupture of diapause: ogist 86, 279-291.
initiation, maintenance New theory. Entomol-
KHALIL, G. M. 1974. The subgenus Persicargas (Ixodoidea: Argasidae: Argus). 19. Prehminary studies on diapause in A. (P. ) arboreus Kaiser, Hoogstraal & Kohls. journal of Medical Entomology 11, 363-366. KHALIL, G. M., AND SHANBAKY, N. M. 1976. The subgenus PeTsicargas ( Ixodoidea: Argasidae: Argus). 25. Argus (P.) arboTeus: Effect of tem-
IN
Argus (P.)
arborew
237
perature on diapause termination. Experimental PaTasitology 39, 431437. MASLENNIKOVA, V. A. 1973. Hormonal control of insect diapause. In (J. LoBue and A. S. Gordon eds. ), “Humoral Control of Growth and Differentiation. Vol. II. Nonvertebrate Neuroendocrinology and Aging,” pp. 3-33, 319. Academic Press, New York and London. RAZUMOVA, I. V. 1965. Seasonal development of diapause in Dermacentor pictus ( Herm. ) and factors stimulating it. (In Russian) Meditsinskaya Parazitologiya, Moskva 34, 46-52. SHANBAKY, N. M., AND KHALIL, G. M. 1975. The subgenus Persicargas (Ixodoidea: Argasidae: Argas). 22. The effect of feeding on hormonal control of egg development in A. (P.) arboreus. Experimental Parasitology 37, 361366. SPIELMAN, A. 1974. Effect of synthetic juvenib hormone on ovarian diapause of Culex pipiens mosquitoes. Journal of Medical Entomology 11, 223-225. WILDE, J. DE, AND BOER, J. A. DE. 1961. Physiology of diapause in the adult Colorado beetle. II. Diapause as a case of pseudo-allatectomy. Journal of Insect Physiology 6, 152-161.
PARASITOLOGY
The
40,232-237
( 1976)
Subgenus Persicargas (Ixodoidea: Argasidae: 26. Argus (P.) arboreus: Effect of Photoperiod Diapause Induction and Termination M.
GALJLA Medical Unit
Zoology Number
Department, United Three (NAMRU-3), Arab Republic
(Accepted
for publication
Argus). on
KHALIL
States Naual Medical American Embassy, of Egypt 24 November
Research Cairo,
1975)
KHALIL, G. M. 1976. The subgenus Persicargas (Ixodoidea: Argasidae: Argus). 26. Argus (P.) arboreus: Effect of photoperiod on diapause induction and termination, Experimental Parasitology 40, 232-237. Prefeeding exposure of female Argas (Pemicargas) arboreus to short photoperiod (SP) induces diapause, expressed as oviposition delay for more than 40 days postfeeding. Diapause incidence increases as prefeeding SP exposure periods increase. Postfeeding SP exposure is not essential to maintain diapause. Postfeeding exposure to SP without prefeeding SP exposure does not induce diapause. A 2 week prefeeding exposure to long photoperiod (LP) terminates diapause in two-thirds of the females exposed to LP after feeding. The remaining one-third, which may differ genetically, require a 6 week LP prefeeding exposure to terminate diapause. An 8 week prefeeding exposure to LP is required to terminate diapause in females exposed to SP after feeding. INDEX DESCRIPTORS: Argus (Persicargas) arboreus; Argasidae; Argasid tick; Photoperiod; Diapause; Oviposition.
During the fall-winter facultative dia- diapause induction and termination, respecpause in nature, female Argas (Persicar- tively, in field-collected female A. ( P. ) gas) arboreus Kaiser, Hoogstraal and Kohls arboreus. delay oviposition until spring (Guirgis 1971; MATERIALS AND METHODS Khalil 1974). Field-collected females held Unfed female A. (P.) arboreus (with a under the constant temperatures of 26, 30, 34, or 37 C after feeding did not alter dia- flat body) were collected in July (midsumpause incidence (Khalil and Shanbaky mer) fram trees supporting nests of Bubul1976); thus temperature does not appear to cus i. ibis in the rookery at the Delta Barrage, Qalyubia (‘the type locality of this be a factor controlling diapause termination. Preliminary experiments showed that ex- tick species). posing female A. (P. ) arboreus to a long In the laboratory, LD cycles were conphotoperiod (LP) of LD 16:8 (1ight:dark trolled by two Paragon 7-day timers, each attached to a 4-W cool white fluorescent hours per day) during fall-winter interfered with diapause but a short photope- lamp inside a light-tight container 16 x 18 riod (SP) of LD 9:15 induced diapause. x 22 in. in size. A half-liter jar containing Therefore, we studied the influence of SP saturated NaCl solution in each container and LP before and/or after feeding on provided 75% RH. Both containers were 232 Copyright All rights
0 1976 by Academic Press, Inc. of reproduction in any form reserved.
AND DIAPAUSE IN Argus (P. ) arbmeus
PHOTOPERIOD
placed in an environmental chamber at 26 C ( -tl C). Photophases of 16 and 9 light hr per day represented LP and SP, respectively. Half of the field-collected females were subjected to LP (Stock 1) and the other half to SP (Stock 2) for 10 weeks before beginning the experiments.
233
were moved to the LP container. At weekly intervals, as above, they were fed and divided into two subgroups; one subgroup was returned to LP and the other to SP. Control ticks (30-35 females) from SP Stock 2 were fed at weekly intervals simultaneously with the LP experimental groups. After feeding, the control ticks were maintained in SP. Laboratory hosts in all tests were domestic pigeons. Immediately after feeding, each female was placed in a polyethylene tube with a fed male and observed daily for oviposition. Females ovipositing after more than 40 days were considered to have been in diapause (Khalil 1974). The statistical significance of the data was determined by the test of proportions.
SP Influence on Diapause Induction Ten weeks after collection, 11 groups, each of 60-85 unfed LP Stock 1 females, were moved to the SP container. At weekly intervals, beginnmg on the day of transfer from LP to SP, one group was fed and divided into two subgroups; one subgroup was returned to LP and the other to SP. Control ticks (30-35 females) from LP Stock 1 were fed at weekly intervals simultaneously with experimental groups subjected to SP. After feeding, the control ticks were returned to LP.
RESULTS
SP Effect on Diapause Induction (Fig. 1) SP before and after feeding. The diapause incidence of females exposed to SP for 1 week ( 6% ) did not differ significantly (P>O.4) from that of females exposed to
LP Influence on Diapause Termination Ten weeks after collection, 11 groups, each of 60-90 unfed SP Stock 2 females
).-.-.. ,
0
WEEKS
FIG. 1. Short long photoperiod;
photoperiod SP-short
2
3
OF EXPOSURE
I
5
6
7
8
T O SHORT PHOTOPERIOD
effect on diapause photoperiod.
induction
in
9
10.
BEFORE
FEEDING
female
Argus
(P.)arboreus.
LP-
234
GALILA
M.
LP before feeding and to SP only after feeding (0% ) . Diapause incidence gradually increased wi’th increased exposure to SP before feeding; diapause was induced in 50% of the population after exposure to SP for 6 weeks and in 90% after 10 weeks. Control groups exposed to LP and fed simultaneously with experiment’al SP groups rarely (212% ) delayed oviposition for more than 40 days. SP before feeding and LP after feeding. Diapause incidence in these groups was not significantly different (P>O.O5->0.9) from the corresponding groups exposed to an equivalent SP period before feeding and to SP after feeding. The diapause incidence curves in both experiments were close in shape and overlapped in many parts. LP Effect on Diapause
Termination
ing (91% ). In both groups, diapause incidence was not significantly different (P> 0.2) from that of the control females maintained under SP and fed simultaneously with these experimental groups (65 and 87%, respectively). Diapause incidence sharply decreased (37% ) after exposure ,to LP for 2 weeks before feeding. No further significant change in incidence occurred after exposure to LP for 3-5 weeks (P> 0.8). Exposure to LP for 6-10 weeks terminated diapause in most or all (87-100% ) ticks. There was no significant change (P >0.05->0.8) in incidence in control groups exposed to SP and fed simultaneously with the experimental groups (64-82s ). LP before feeding and SP after feeding. Diapause incidence after exposure to LP for l-3 weeks was not significantly different (P>O.O5->0.2) from that of the control groups exposed to SP and fed simultaneously with experimental groups. Incidence in females exposed to LP for 4-7 weeks before feeding was at the same level (P> 0.05->0.9) as in those exposed to LP for 2-5 weeks before feeding and also after
(Fig. 2)
LP before and after feeding. About 26% of the females exposed to LP for 1 week terminated diapause. Diapause incidence ( 74% ) was not significantly different ( P> 0.05) from that of females exposed to SP before feeding and to LP only after feed-
,-,
LP
before
and
.--.
LP
before
feedIng
m--.
Co”troi.mal”tolned
KHALIL
oftar
feeding. and
SP after
feedIng
I” sp
0, 0
1
WEEKS
FIG LP-long
2
3
OF EXPOSURE
1
5
6
7
T O LONG PHOTOPERIOD
2. Long photoperiod effect on diapause photoperiod, SP-short photoperiod.
termination
6 BEFORE
in
9
10
FEEDING
female
AT~US
(P.)
arboreus.
PHOTOPERIOD
AND
DIAPAUSE
feeding. Diapause was terminated in most or all (90-100% ) ticks exposed to LP for S-10 weeks only before feeding. Therefore, the diapause termination curves were similar in shape for the group exposed to LP only before feeding and for the groups exposed to LP before and after feeding, except that the former curve was shifted to the right. The curves overl’apped only after S-10 weeks’ exposure to LP.
IN
Argus
( P. ) arborem
235
minate diapause. Switching the females to SP ‘after feeding prolonged the LP prefeeding exposure period necessary to terminate diapause to 4 and 8 weeks in twothirds and one-third of the population, respectively. The longer period (2 weeks) needed by ticks exposed to LP only before feeding may be owing to association of diapause termination with a physiological process( es) requiring about 3 to 4 weeks for completion in two-thirds of the popuDISCUSSION lation and about 5 to 6 weeks in the rePhotoperiodic regulation of diapause in maining one-third (oviposition by the nonadult ixodid ticks was reported for Dermadiapause female occurs 1 to 2 weeks after centor marginatus (Belozerov 1963, 1965a, feeding). b; Belozerov and Kvitko 1965; Belozerov A. (P. ) arboreus appears to be a longday species undergoing facultative diaand Lamnova 1967) and D. pictus (Razumova 1965). The present investigation of pause under the influence of SP. Diapause A. (P.) arboreus appears to be the first induction in fall and termination in early study of photoperiod effect on diapause in summer by short and long days, respecan argasid tick. tively, is biologically significant because The results indicate that exposing female herons, the natural hosts of A. (P.) arborookery A. (P.) arboreus to SP before feeding is reus, disperse from the tick-infested essential to induce diapause. Switching SP in late September and return in late March (Guirgis 1971). If tick eggs were laid durfemales to LP after feeding does aot alter ing the fall, emerging larvae would be ,dethe prefeeding SP effect, thus postfeeding exposure to SP is not essential to maintain prived of a food source and die of starvadiapause. The organs affected by SP, i.e. tion (Guirgis 1971). In female A. (P. ) arboreus held outthe nerve ganglion andjor the ovary, are doors in natural fluctuating temperature probably vulnerable to SP effect only when the female is in the unfed state. conditions, diapause termination occurs in Fall daylength in Cairo (30”03’N, 31”15 April-May (Guirgis 1971, Khalil 1974). Diapause is of lower intensity in females E) is longer than the SP (LD 9:16) used (29 in this study. The critical photoperiod in- held at a nearly constant temperature or 30 C) but subjected to normal changes ducing diapause in nature in Cairo remains to be investigated. Decreasing daylength in of subdued dayligh,t, and is terminated fall (September through October) may inspontaneously in November-March (Khalil duce a higher diapause incidence (and/or 1974). “Diapause development” (Andreintensity) than that artificially induced in wartha 1952) or “diapause reactivation” (Belozerov 1968) m,ay proceed faster when this experiment. The effect of decreasing SP on diapause in A. (P. ) arboreus also these females are held under a constant temperature before and after feedmg remains to be investigated. (Khalil and Shanbaky 1976). In this study, two-thirds of the fem,ale Diapause induction in A. (P.) arboreus A. (P.) arboreus population exposed to may be assooiated with synthesis and/or LP for 2 weeks before feeding and also activation of an inhibitor, i.e. a diapause after feeding terminated diapause. The rehormone, for which prefeeding exposure maining one-third, which may be genetito SP is essential. Andrewartha et al. cally different, required at least a 6 weeks’ ( 1974) suggest that a hormone is generally LP exposure period before feeding to ter-
236
GALILA
present in insects with obligate and facultative diapause. If an inhibitor is present in diapause female A. (P.) arboreus, diapausc may be terminated when this inhibitor is slowly degraded after feeding. Exposure to LP before feeding may cause faster inhibitor degradation and permit females to oviposit within 1 to 2 weeks after feeding. However, dia’pause in A. (P. ) arhoreus may be associated with a lack of an activator, e.g., a gonadotropic hormone. In this respect, A. (P. ) arboreus may be similar to the Colorado potato beetle Leptinotarsa decemlineata ( de Wilde and de Boer 1961)) in which diapause is regulated by the titre of the circulating juvenile hormone. Synthesis and/or activation of the speculated hormone in A. ( P. ) arboreus may occur at a slow rate under SP and at a fast rate under LP. As in the adult mosquito Culex pipiens (Spielman 1974) and the alfalfa weevil Hypera postica (Bowers and Blickenstaff 1966), diapause is terminated in female A. (P. ) arboreus by topical application of a juvenile hormone analog [acetaldehyde, 2- (2-ethoxyethoxy ) ethyl p(methylthio) phenyl acetal] (Bassal and Roshdy 1974). A gonadotropic hormone becomes active in the nerve ganglion of nondiapause female A. (P.) arboreus within 3 days after feeding and is released afterwards in the hemolymph (Shanbaky and Khalil 1975). However, we believe that a combined inhibitor and activator lmechanism may regulate diapause in A. (P. ) arboreus. This bifactorial concept of hormonal regulation of diapause (Hinton 1953) seems to function especially in organisms undergoing facultative diapause (Maslennikova 1973). The role of one or more hormones in A. (P.) arboreus diapause regulation is under investigation in this laboratory. These investigations of factors controlling diapause in female A. (P.) arboreus provide background information for studying viral survival and multiplication in diapause and nondiapause ticks and for de-
M.
KHALIL
veloping a model for vector interrelationships.
studies
on virus-
ACKNOWLEDGMENTS From Research Project MF51.524.009-0055, Naval Medical Research and Development Command, Washington, D.C. The opinions and assertions contained herein are the private ones of the author and are not to be construed as official or as reflecting the views of the Department of the Navy or of the naval service at large. This work was assisted by Agreements 03-005-l (now 03-036-N) and 03-016-l between the National Institute of Allergy and Infectious Diseases (N.I.H.) and NAMRU-3. The author is indebted to Dr. Harry Hoogstraal for his supportive interest and critical reading of the manuscript. REFERENCES ANDREWARTHA, H. G. 1952. Diapause in relation to the ecology of insects. Biological Review 27, 50-107. ANUHEWAIITHA, H. G., MIETHKE, P. M., AND WELLS, A. 1974. Induction of diapause in the pupa of Phalaenoides glycinae by a hormone from the suboesophageal ganglion. Journal of Insect Physiology 20, 679-701. BASSAL, T. T. M., AND ROSHDY, M. A. 1974. Argas (Persicargas) arboreus: Juvenile hormone analog termination of diapause and oviposition control. Experimental Parasitology 36, 3439. BELOZEROV, V. N. 1963. Day length as a factor determining oviposition delay in female Dermacentor marginatus Sulz. ( In Russian ). Meditsinskaya Parazitologiya, Moskva 32, 521-526. (In English NAMRU3-T389). BELOZEROV, V. N. 1965a. Diapause in ixodid ticks. (In Russian) Doklady na l&-17. Yezhegodnykh Chteniyakh Pamyati N. A. Kholodkovskogo (April 3, 1963-ApriI3, 1964), p. 1233. BELOZEROV, V. N. 1965b. A developmental stage of Dermacentor marginatus ( Sulz. ) sensitive to photoperiodic effect. (In Russian) Meditsinskaya Parazitologiya, Moskva 34, 52-57. BELOZEROV, V. N. 1968. Photoperiodic control of seasonal development of ixodid ticks. In “Fotoperiodicheskie adaptatsii u nasekomykh i Kleshochey.” ( In Russian. ) Leningradsky Ordena Lenina Gosudarstvennyy Universitet imeno. A. A. Zhdanova, p. 100-128. (In English: NAMRU3-T432 ). BELOZEROV, V. N., AND KVITKO, N.V. 1965. Main features of photoperiodic reaction in the tick Dermacentor marginatus Sulz. ( Ixodidae ). (In Russian ) Zoologicheskiy Zhurnal 44, 363-372. ,- . . ~~ (In English: NAMRUB-T190).
PHOTOPERIOD
AND
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BELOZEROV, V. N., AND LAMNOVA, A. I. 1967. Development of winter diapause and response to the day length in Demzacentor maginatus ticks in central Kazakhstan. Meditsinskaya PamzitoZogiya, Moskva 36, 464-l69. (In Russian). BOXERS, W. S., AND BLICKENSTAFF, Hormonal termination of diapause weevil. Science 154, 1673-1674.
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KHALIL, G. M. 1974. The subgenus Persicargas (Ixodoidea: Argasidae: Argus). 19. Prehminary studies on diapause in A. (P. ) arboreus Kaiser, Hoogstraal & Kohls. journal of Medical Entomology 11, 363-366. KHALIL, G. M., AND SHANBAKY, N. M. 1976. The subgenus PeTsicargas ( Ixodoidea: Argasidae: Argus). 25. Argus (P.) arboTeus: Effect of tem-
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