Trop. Anita. Hlth Prod. (1984) 16, 13-20

D E V E L O P M E N T OF IXODID TICKS UNDER NATURAL CONDITIONS IN N I G E R I A

O. O. DIPEOLU

Department of Veterinary Microbiology and Parasitology, University of Ibadan, Ibadan, Nigeria

SUMMARY

The developmental periods of five tick species were recorded from egg to adult stages under natural conditions. The ticks were Amblyomma variegatum, Boophilus decoloratus, B. geigyi, Hyalomma rufipes and H. truncatum and the natural condition was a grazing field on which "open" site and "shade" were recognised. The investigation took place between April 1980 and March 1981. The hatching patterns of larvae, attachment, engorgement, larvo-nymphal and nympho-adult moulting periods and the survival of larvae and nymphs during different climatic periods of the year were recorded. While the attachment and engorgement periods which were recorded on the animal were relatively constant for each tick species throughout the period of investigation the hatching patterns and moulting periods were influenced by rainfall and temperature. The moulting periods of larvae and nymphs kept in the open as well as the total duration of the life cycle were lower than those of ticks kept in the shade. The survival of larvae and nymphs of all tick species was lowest during the peak of rains and highest during the dry season; the survival was also generally higher among larvae and nymphs kept in the shade than those kept in the open. The results were related to the distribution pattern and seasonal occurrence of some of the tick species in Nigeria.

INTRODUCTION

Most of the reported works on the development of ticks has been conducted in laboratories. Only Branagan (1973) and Dipeolu and Ogunji (1977) observed the development of Rhipicephalus appendiculatus in East Africa and Amblyomma variegatum and Hyalomma rufipes in Nigeria respectively under quasi-natural conditions. During observations on the ovipositional capacity of ixodid ticks maintained under quasi-natural and natural conditions in Nigeria Dipeolu (1983a) showed the effect of direct exposure of ticks to atmospheric conditions and highlighted the importance of shade as a permanent source of supply of tick eggs during all climatic seasons. In this paper the development of A. variegatum, B. decoloratus, B. geigyi, H. rufipes and H. truncatum from the larval to adult stages under natural field conditions is reported.

MATERIALS AND METHODS

The larvae, nymphs and adults used in this experiment were bred directly from ticks collected on slaughter cattle in the Ibadan abattoir. The natural condition was a grazing field within the University campus where two sites--"open site" and "shade"--were recognised. The open site was those parts of the field exposed to the direct sunlight while the shade was a part of the field where close-standing trees created perpetual shade through extensive leaves and branches. Larvae of A. variegatum and Hyalomma spp. and nymphs of Hyalomma were fed on rabbit

13

14 DIPEOLU

ears (Bailey, 1960) while nymphs of all other ticks, hungry adults and all forms of Boophilus were fed on sheep scrota (Ogunji and Dipeolu, 1977). In order to simulate natural conditions as much as possible during tick feeding sheep on which ticks were feeding were left grazing on the experimental field until most of the ticks had engorged and fallen into the bags. Engorged larvae, nymphs and adults were placed individually in plastic containers which had been previously filled up-to 4 cm height with a mixture of fresh sand, soil and grass. Loss of ticks was prevented by accommodating the plastic containers within a specially built open steel container of 30 cm diameter and 6 cm height. A few small perforations were made at the base of each plastic container to facilitate drainage of water on to the steel container after rainfall.

The day in which any tick was placed in the open or shade was regarded as day 0. To obtain the attachment period of any tick stage the bags containing them on the animal were carefully opened between 09.00 and 10.00 h and the ticks which had attached were counted. This was done until all the ticks which would attach had done so. All ticks which had not attached were discarded five days after attached tick counts had yielded the same number. The day the first batch of ticks attached to the day the last batch did so constituted the attachment period. The difficulty posed by the small size of the freshly attached larvae was solved by using a hand lens in counting. The engorgement period is recorded as the interval between the day the last batch of ticks attached to the day the last engorged forms dropped. Moulting period was the number of days it took a stage to moult to the next stage and in this investigation larvo-nymphal and nympho-adult moulting periods were recognised.

The hatching patterns of eggs maintained in the open and shade were compared. Larvae were separated from unhatched eggs as described by Dipeolu (1983b). This investigation took place from April 1980 to March 1981. Drawing from our experience of tick breeding the breeding programme was scheduled so that larvae, nymphs and adults of all species were available for experimental use during every month. Meteorological data of the University campus was obtained from the climatology unit of the Department of Geography.

RESULTS

Tables I to V show the developmental periods of the experimental ticks during the seasons of the year. The periods of hatching of eggs of all the ticks kept in both shade and open were shortest during the dry season and longest during the peak of rains except those of B. geigyi whose periods were shortest at the peak of rains and longest during the dry season (Table III). Also the periods of hatching were longer in eggs kept in the shade than those in the open except those of B. geigyi where the reverse was observed. There was very minimal fluctuation in the attachment and engorgement periods of larvae and nymphs during all the seasons. Generally the larvo-nymphal and nympho-adult moulting periods were longest for all ticks during the peak of the rains and shortest during the dry season.

Although the results show that development took place throughout the year observations indicated some critical months during which development of some species either ceased or was very slow. Eggs ofA. variegatum and B. geigyi kept in the open failed to hatch in the dry months of December and January and December to February respectively while there was cessation of hatching of eggs of H. truncatum during the high rainfall months of August to October. Larvae and

to

TA

BL

E I

Dur

atio

n of

life

cyc

le in

day

s (l

arva

e-ad

ult)

ofA

mbl

yom

ma

vari

egat

um u

nder

nat

ural

cond

ition

s

Mea

n le

ngth

of

hat

chin

g L

arva

l L

arva

l L

arvo

- N

ymph

al

Nym

phal

N

ymph

o-

of e

ggs

atta

chm

ent

engo

rgem

ent

nym

phal

mou

lt

atta

chm

ent

engo

rgem

ent

adul

t mou

lt

Tot

al

Sea

son

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Dry

sea

son

~ S

hade

10

6

5 4

5 5

19

12

2 2

7 7

18

14

65

50

Op

en

4 4

5 4

5 5

13

9 2

2 7

7 12

10

48

41

B

egin

ning

of

rain

s 2

Sha

de

12

8 6

4 5

5 25

15

2

2 7

7 20

18

77

59

O

pen

5

4 6

4 5

5 18

10

2

2 7

7 16

12

59

44

P

eak

of r

ains

3 S

hade

28

15

8

6 5

5 35

28

2

2 7

7 31

22

11

6 85

O

pen

18

16

8

6 5

5 30

23

2

2 7

7 25

18

95

77

O

O

i Nov

embe

r, D

ecem

ber,

Jan

uary

and

Feb

ruar

y.

2Mar

ch,

Apr

il,

May

, Jun

e.

3 Jul

y, A

ugus

t, S

epte

mbe

r, O

ctob

er.

TA

BL

E II

Dur

atio

n of

life

cyc

le in

day

s (l

arva

e-.a

dult)

of B

ooph

ilus

deco

lora

tus

unde

r nat

ural

cond

ition

s

Mea

n le

ngth

o

f hat

chin

g o

f egg

s L

arva

l L

arva

l L

arvo

- N

ymph

al

Nym

pho-

at

tach

men

t en

gorg

emen

t ny

mph

al m

oult

engo

rgem

ent

adul

t m

oult

T

otal

Seas

on

Max

. M

in.

Ma

x.

Mill

. M

ax.

Min

. M

ax.

Min

. M

ax.

Min

. M

ax.

Min

. M

ax.

Min

.

Dry

sea

son

Sha

de

4 2

2 2

3 3

6 6

4 4

8 8

27

Ope

n 3

2 2

2 3

3 6

6 4

4 8

8 26

B

egin

ning

of r

ains

S

hade

5

4 2

2 3

3 6

6 4

4 8

8 28

O

pen

3 3

2 2

3 3

6 6

4 4

8 8

26

Pea

ks o

f rai

ns

Sha

de

15

9 4

2 3

3 8

6 4

4 10

8

44

Ope

n 11

7

4 2

3 3

8 6

4 4

10

8 40

25

25

27

26

32

3O

TA

BL

E II

I

Dur

atio

n of

life

cyc

le in

day

s (la

rvae

--ad

ult)

of B

ooph

ilus

geig

yi u

nder

nat

ural

cond

ition

s

O

Mea

n le

ngth

of

hat

chin

g of

egg

s L

arva

l L

arva

l L

arvo

- N

ymph

al

Nym

pho-

at

tach

men

t en

gorg

emen

t ny

mph

al m

oult

engo

rgem

ent

adul

t m

oult

T

otal

Sea

son

Max

. M

in.

Ma

x.

Min

. M

ax.

Min

. M

ax.

Min

. M

ax.

Min

. M

ax.

Min

. M

ax.

Min

.

Dry

sea

son

Sha

de

19

11

2 2

3 3

5 5

4 4

7 7

40

32

Ope

n 18

18

2

2 3

3 5

5 4

4 7

7 39

39

B

egin

ning

of r

ains

S

hade

11

3

2 2

3 3

5 5

4 4

7 7

32

24

Ope

n 18

5

2 2

3 3

5 5

4 4

7 7

39

26

Pea

k o

f rai

ns

Sha

de

7 7

2 2

3 3

5 5

4 4

7 7

28

28

Ope

n 15

7

2 2

3 3

5 5

4 4

7 7

36

28

TA

BL

E I

V

Dur

atio

n o

f lif

e cyc

le in

day

s (l

arva

e-ad

ulO

ofH

yalo

mm

a ru

fipe

s un

der

natu

ral c

ondi

tions

Mea

n le

ngth

of

hat

chin

g L

arva

l L

arva

l L

arvo

- N

ymph

al

Nym

phal

N

ymph

o-

of e

ggs

atta

chm

ent

engo

rgem

ent

nym

phal

mou

lt

atta

chm

ent

engo

rgem

ent

adul

t mou

lt

Tot

al

Sea

son

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Max

. M

in.

Dry

sea

son

Sha

de

6 3

2 2

10

10

10

6 3

3 7

7 26

10

64

41

O

pen

3

3 2

2 10

10

6

2 3

3 7

7 18

6

49

33

Beg

inni

ng o

f ra

ins

Sha

de

9 5

2 2

10

10

12

6 3

3 7

7 35

18

78

51

O

pen

7

4 2

2 10

10

9

4 3

3 7

7 25

9

63

39

Pea

k of

rai

ns

Sha

de

21

12

6 3

10

10

20

15

3 3

7 78

48

38

11

5 88

O

pen

16

9

6 3

10

10

15

10

3 3

7 7

36

26

93

68

h-I

.<

O

TA

BL

E V

Dur

atio

n o

f lif

e cyc

le in

day

s (l

arva

e-ad

ult)

ofH

yalo

mm

a tr

unca

tum

und

er n

atur

al c

ondi

tions

Mea

n le

ngth

of

hat

chin

g L

arva

l L

arva

l L

arvo

- N

ymph

al

Nym

phal

N

ymph

o-

of e

ggs

atta

chm

ent

engo

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ent

nym

phal

mou

lt

atta

chm

ent

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ent

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lt

Tot

al

Sea

son

Max

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in.

Max

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in.

Max

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Max

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in.

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in.

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in.

Max

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in.

Max

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in.

o

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sea

son

Sha

de

6 3

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15

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3 7

7 21

10

62

38

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pen

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2 8

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2

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15

5 49

30

B

egin

ning

of

rain

s S

hade

11

6

2 2

8 8

18

5 3

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7 42

18

91

49

O

pen

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3

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28

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58

43

123

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en

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18 DIPEOLU

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FIG. i . Survival of larvae and nymphs of A. variegatum under natural conditions.

DEVELOPMENT OF IXODID TICKS 19

nymphs of ticks moulted during all the seasons and their moulting periods in the open were generally shorter than in the shade except those of Boophilus species which were ascertained on the animal hosts because they are one-host ticks. Generally the duration of the life-cycle was longest during the peak of rains and shortest during the dry season except B. geigyi where the reverse occurred. Similarly the duration of the life cycle during any season was shorter in the open than in the shade except for B. geigyi.

During this investigation 100 larvae and 100 nymphs of the ticks out of those whose moulting periods were being ascertained except Boophilus species were separated out every month through random sampling and the numbers which successfully moulted in the shade and open were recorded. Those which failed to moult were retained for an additional six weeks before they were discarded. Figure I shows the results for A. variegatum which were similar to those of the other ticks. Survival of larvae and nymphs kept in the open and shade was lowest during the peak of rains specially in August and highest during the dry season. The degree of survival was more pronounced in larvae than in nymphs. Generally survival was higher particularly among those kept in the shade.

DISCUSSION

The results of this investigation show the importance of climatic factors in influencing the biology of ticks. The hatching patterns, the various developmental periods and the degree of survival of developmental forms were dependent on climatic factors especially rainfall and temperature. The results of hatching patterns add to the reasons already adduced by Dipeolu (1983b, c) as to why only H. rufipes out of the six Hyalomma spp. found in Nigeria (Dipeolu, 1975a) had established itself in the wet and humid southern Nigeria and as to why B. geigyi had established itself only in the savanna and forest zones (Dipeolu, 1975b) while it is absent in the hot and dry Sahel zone of northern Nigeria. While eggs of H. truncatum would not hatch during the high rainfall months, those of H. rufipes hatched although its density on pastures was low during these periods because of the prolonged hatching period and low survival. On the other hand eggs of B. geigyi kept in the open failed to hatch during the dry months and even those kept in the shade had prolonged hatching duration during these periods.

The data on the moulting periods are an important tool in the prediction of the density of various developmental forms on the pasture in the forest zone of Nigeria in which Ibadan lies. It is apparent from these results that the preponderance of larvae and nymphs on pasture will be highest during the dry season and least during the heavy rains. Since the heavier the rains the less the survival of larvae and nymphs, a year with many months of heavy rains will be characterised by scarcity of these forms on the pasture while a dry year will be characterised by increased density of the forms. The role of shades as major breeding sites throughout the year must also be stressed especially since shades created by tall trees are abundant along the trade cattle routes in Nigeria. The shades serve not only as resting sites for trade cattle during migration but they also serve as shelter against the intense afternoon heat. The author had on several occasions picked engorged ticks in shades along trade cattle routes shortly after cattle had moved away.

The fact that the duration of the developmental periods of the Boophilus species as welt as those of the other tick species (larval and nymphal attachment and engorgement periods) which were recorded on the animals were constant

20 DIPEOLU

throughout the period of investigation shows that ticks are not affected by the environmental climatic factors while they are attached to the host. While this is of advantage to the one-host Boophilus ticks the larvae and nymphs of multiple host ticks were not found to make use of this advantage through prolonged attachment and engorgement during the unfavourable rainy months especially in August.

Accepted for publication December 1982

REFERENCES

Bailey, K. P. (1960). Bulletin of Epizootic Diseases of Africa, 8, 33-46. Branagan, D. (1973). Tropical Animal Health and Production, 5, 153-165. Dipeolu, O. O. (1975a). Bulletin of Animal Health and Production in Africa, 23, 165--172. Dipeolu, O. O. (1975b). Tropical Animal Health and Production, 7, 35-39. Dipeolu, O. O. (1983a). Environmental Entomology (in press). Dipeolu, O. O. (1983b). Insect Science and its Application, 2, 227-231. Dipeolu, O. O. (19830. Veterinary Parasitology, 13, (in press). Dipeolu, O. O. & Ogunji, F, O. (1977). Journal of Pharmacology and Medical Science, 1, 245-248. Ogunji, F. O. & Dipeolu, O. O. (1977). Zeitschrift f~r Parasitenkunde, 51, 285--288.

DEVELOPPEMENT DE TIOUES (IXODIDES) DANS LES CONDITIONS NATURELLES DU NIGERIA

R~sum~---On a enregistr~ la dur~e du d~veloppement de l'oeuf au stade adulte de cinq esp~.ces de tiques dans les conditions naturelles. Ces esl~ces ~taient Amblyomma variegatum, Boophilus decoloratus, B. geigyi, Hyalomma rufipes et H. truncatum et les conditions naturelles *talent celles d'une ptiture sur laquelle des sites "d~couvert" et "ombrag~" avaient ~t~ identifi~s. L'~tude s'est d*roul*e d'avril 1980 ~t mars 1981. Les modalit~s d'~closion, de fixation, d'alimentation, les p*riodes de mue larvo-nymphale et nympho-irnaginale et la survie des larves pendant ies diff~rentes p~riodes climatiques de l'ann~e ont ~t* observ~es. Alors que les p~riodes de fixation et de prise alimentaire observ*es sur les animaux ~taient relativement constantes pour les esp~ces de tiques tout au long de la p~riode d'~tude, les modalit*s d'*elosion et les #r iodes de mue ~taient influenc~es par les precipitations et la temp~ature. Les p~riodes de mue des larves et nymphes maintenues ~ d~couvert ainsi que la dur*e totale du cycle de vie ~taient plus faibles que pour les tiques maintenues ~ l'ombre. La survie des larves et nymphes de routes les esp~ces de tiques ~tait plus faible au moment des pluies tes plus intenses et plus ~levC~e en saison s~che. La survie ~tait aussi g*n~ralement plus ~lev~e pour les larves et nymphes gard~es ~ l'ombre que pour celles maintenues ~ d~couvert. Les r~sultats ~taient li~s aux modalit~s de r~partition et I'apparition saisonni/~re de certaines esp~ces de tiques au Nigeria.

DESARROLLO DE GARRAPATAS IXODES BAJO CONDICIONES NATURALES EN NIGERIA

Resumen--Se estudi6 el perfodo de desarrollo bajo condiciones naturales, de cinco especies de garrapatas, desde la eclosi6n hasta el estado adulto. Las garrapatas fueron: Amblyomma variegatum, BoophUus decoloratus. B. geigyi, Hyalomma rufipes and H. truncatum, en un nicho ecol6gico natural compuesto de campos pastoriles abiertos con ireas sombreadas. La investigaci6n se llev6 a cabo de Abril de 1980 a Matzo, 1981. Se tom6 nora del patr6n de eclosiOn de las larvas, adhesi6n, engorde, perfodos de muda y supervivencia de larvo-ninfas y ninfo-adultos, durante los diferentes periodus estacionales. Mientras que los perfodos de adhesifn y engorde con sangre fueron constantes para cada una de las especies estudiadas, los patrones de eclosi6n y muda fueron influenciados por la precipitaciOn pluvial y la temperatura. Los perfodos de muda de larvas y ninfas en campo abierto, lo mismo que la duraci6n del ciclo de vida, fueron mils cortos que los de aquellas que estaban en la sombra. Ida supervivencia de larvas y ninfas de todas las especies estudiadas, fu~ mils bajo durante el pico de lluvias y mayor durante la estaciOn seca; la supervivencia fu~ tambien generalmente mayor en aquellas que estaban en la sombra, durante la estaci6n Iluviosa y seca. Los resuitados se relacionaron con el patr6n de distribuci6n y ocurrencia estacional de algunas de ias especies de garrapatas en Nigeria.