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Acarologia
A quarterly journal of acarology, since 1959Publishing on all aspects of the Acari
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HAEMAPHYSALIS PUNCTATA CANESTRINI AND FANZAGO 1877,
A TICK OF PASTURED SEADUNES ON THE ISLAND OF TEXEL
(THE NETHERLANDS)
TICKS DISTRIBUTION
ON HOSTS
DISTRIBUTION DES TIQUES
SUR LES HÔTES
BY A. F. M. GARBEN 1•
2, H. VOS 1 and J. E. M. H. van BRONSWIJK 1
ABSTRACT : Dunesheep are the main hosts for the tick Haemaphysalis punctata on the island of Texel. Ali stages may complete their bloodmeal on these animais. Additional hosts include horses, native mammals (rabbit, ferret) and a number of bird species (especially for the larvae and nymphs). The dependance of this tick on dunesheep appears to originate from the absence of big game on the island and the fact that only sheep are pastured to any extent in the dunes. This also means that only about 3-4 % of the area of the island is infested with this tick.
Ixodes ricinus is present on the island also : adults on sheep, dogs and cats ; nymphs on sheep, rab bits and a few bird species ; larvae on rab bits, mice and birds. This tick is Jess common but occurs on a larger area. lt is not restricted to the dry sheep-grazed dune area, but also present in woods and bushes.
H. punctata is known from a number of other Frisian islands but appears to be absent from the mainland of the Netherlands.
RÉSUMÉ : Les moutons de dunes sont les hôtes primaires des tiques Haemaphysalis punctata de l'île de Texel. Tous les stades peuvent compléter leur repas de sang au détriment de ces animaux. Les hôtes supplémentaires embrassent des chevaux, des mammifères indigènes (comme les lapins; les furets), ainsi qu'un certain nombre d'espèces d'oiseaux (ceci en particulier pour les larves et les nymphes). La dépendance de ces tiques des moutons des dunes semble dériver du fait de l'absence d'animaux de plus grande taille dans l'île, parce qu'on y peut seulement laisser pâturer des moutons à un certain degré dans les dunes. Ce fait-là veut aussi dire que seulement environ 3 à 4 OJo des terrains de l'île sont infectés avec cette tique.
En outre on trouve également à Texel les Ixodes ricinus : les adultes sur les moutons, les chiens et les chats ; les nymphes sur les moutons, les lapins et quelques espèces d'oiseaux seulement; les larves sur les lapins, les souris et quelques oiseaux. Cette tique-là est moins commune mais présente dans un domaine plus étendu. Elle n'est point restreinte à la région sèche des dunes, pâturée par des moutons, mais on la trouve également dans la région des bois et des broussailles.
On rencontre les H. punctata aussi sur quelques autres îles de la Frise, mais ils sem-blent être absents du territoire continental des Pays-Bas. ·
1. Laboratorium voor Minibiologie, Vakgroep Dermatologie, Rijksuniversiteit, Utrecht, The Netherlands. 2. With a grant (nr. 28-398) of the Praeventiefonds, Frankenstraat 3, 's·Gravenhage.
Acarologia, t. XXIII, fasc. 1, 1981.
-20
INTRODUCTION
Recently Haemaphysalis punctata Canestrini and Fanzago has been reported from the island of Texel (UILENBERG et al., 1980). It is quite cornmon on the Frisian islands and was found earlier on Ameland (MOHAMMED, 1976; UILENBERC et al., 1979), Rottum (RITZEMA Bos, 1888), Borkum (preparations in the Oudemans-collection, Leiden), Juist (NUTTÂLL et al., 1915 ; LIEBISCH et al., 1976), Norderney (SCHULZE, 1929 ; LIEBISCH et al., 1976), Amrum (LIEBISCH et al., 1976) and Sylt (SCHULZE, 1929; LIEBISCH et al., 1976). However, only parts of those islands seem to be infested (MOHAMMED, 1?76).
On the mainland of Germany and The Netherlands H. punctata was reported from Holstein, the German part of the Bourtanger moor (SCHULZE, 1929) and the vicinity of the towns of Utrecht and Arnhem (preparations from 1884 and 1897 respectively in the Oudemans-coliections, Leiden).
Hosts reported from Germany and The Netherlands include cattle, sheep, horses, brown hares, hedgehogs and birds such as the curlew and the long eared owl (NUTTALL et al., 1915 ; SCHULZE, 1929 ; Oudemans-collections, Leiden).
The erratic geographical distribution of H. punctata and its host relationships on the island of Texel are the subject of this article.
MA TERIAL AND METHODS
Sheep have been examined for ticks in two areas on the island of Texel. In June 1978 and May 1979 in the " Mokbaai " and May, June and September 1979 in the " Eierlandse Duinen " (see Fig. lA). These sheep (named dunesheep) only pasture dune vegetation. Sheep were also examined in June 1978 and September 1979 on five localities in the polder behind the dunes (see Fig. 1 B). On the mainland four sheep-herds have been visited in J uly 1978 : " Strabrechtse heide "
(municipality Heeze), " Dwingeloosche heide " (municipality Dwingelo), Haarlerberg (municipality Heliendoorn) and Huurnerveld (municipality Wierden). In each location 15 sheep were inspected. From November 1977 until November 1978 5 sheep were examined for ticks fortnightly in Langbroek, a municipality in the central part of The Netherlands.
Smali mammals were caught alive in many areas on the island of Texel (see Fig. lB) and fortnightly in Langbroek. Peanut butter was used as bait in Longworth's traps.
In May and June 1978 5 breeding grounds of the Herring Gull (Larus argentatus) and the Cornmon Gull (Larus canus) have been visited. In total 102 ducklings of the Herring Gulls and 90 ducklings of the Common Gulls were investigated (Fig. lA '; table 2). Birds were also caught with mist-nets in May and September 1979 in the " Mokbaai " and the " Eierlandse Duinen " on the island of Texel and fortnightly in Langbroek. At the same time a few ducklings of the lapwing (Vanellus vane/lus) and a Curlew (Numenius arquata) were also inspected on the island of Texel.
Other potential hosts such as dogs (3 specimen), cats (2 specimen), rabbits (14 specimen), chickens (5 specimen), horses (2 specimen), cow (1 specimen) and ferret (1 specimen) could be exarriined with the help of the locals (for location see fig. lB).
From the vegetation ticks were sampled by blanket dragging (for location see Fig. lB). The blanket was made of cotton, its sizes were 60 by 90 cm. Usually on each location the blanket was dragged through the vegetation 2 times for 2 minutes. From ali investigated mammals and birds ticks were removed and the hosts released immediately afterwards. Ali larvae and not fully fed nymphal ticks were mounted in Hoyers medium. After clearing they were identified by phasecontrast microscop. Fully fed nymphal and adult ticks were kept in alcohol 70 OJo and identified under a binocular microscope.
A
Den Burg
'
17'1 LU
dunevegetotion of the Wadden
district 1 alter Kolkhoven et al., 19761
~ dunesecticns postured by sheep
* breeding grounds of the Herring Gull
* breeding grounds of the Common Gull
• H. punctoto on sheep
G 1. ricinus on sheep
o sheep without ticks
• ~
0
•
0
• FIG. 1. The island of Texel.
H. punctoto on birds
1. ricinus on birds
birds without ticks
1. ricinus on Wood Mice
Wood Mice without ticks
H. punctato on ether mommols
1. ricinus on ether mommols
ether mommols without ticks
H. punctoto sompled by blonket drogging
1. ricinus sompled by blonket drogging
no ticks sompled by blonket drogging
hypotheticol distribution of H. punctoto
A. Distribution of dunevegetation, sections pastured by dunesheep, and location of the Gull breeding grounds sampled. B. Results of tick investigations.
-22-
RESULTS
Only two tick species were found on the different hosts investigated on the island (table 1 and 2). Supprisingly Ixodes trianguliceps Birula 1895 was absent on the many Woodmice and Root V oies caught.
Adults of H. punctata were round in May and June, the nymphs in May, June and September (only one nymph). The larvae were observed only in September. In case of I. ricinus ali stages were _ p~e~ent in May, June and September.
The main host on the island of H. punctata seems to ·be the dunesheep (95 OJo of ali investigated dunesheep were feend infest~d), Thè ticks are present in ample numbers and ali stages may take a bloodmeal on the sheep. The adults and 'lYmphs were mostly found on the head, armpits and groins. Ali dunesheep investigated in September had only larvae in large numbers, specialiy at the upper rim of the hoofs and on the snout. No ticks were found on sheep that didn't pasture dune areas. In fact it appears that the distribution of H. punctata is restricted to sheep pastured dunes (Fig. lB). Other hosts for H. punctata include the horse (ali stages), the rabbit ( only for larvae), the ferret ( only for larvae) and birds (mostly for larvae and nymphs) (see table 1 and 2). Brown hares and hedgehogs, mentioned by earlier investigators as suitable hosts (see above) W!'!re not Sampled. lt is interesting that the larvae of H . punctata did not attack the W oodmice and R.oot Voles present in their habitat (Fig. 2B ; table 1). In addition to birds, man could be important for dispersal of this tick (table 1).
l. ricinus seems to have a larger distribution as compared to H. punctata (Fig. 2B). It is present in dunes, woods and bushes. In addition to the hosts attacked by H. punctata this tick has an affinity for rodents (table 1). Usualiy the density of l. ricinus ticks is less than that of H. punctata as assessed by blanket dragging.
Sheep investigated on the mainland of The Netherlands never bad H. punctata but most were infested with l. ricinus (adults, nymphs and a few larvae). Ali other hosts such as rodents and insectivores (232 specimen) and birds (92 specimen) caught in Langbroek on the mainland of The Netherlands were not infested with H. punctata. Only l. ricinus (larvae and nymphs) and l. trianguliceps (ali stages only on rodents and insectivores) were found .
DISCUSSION
Haemaphysalis punctata is a three-host tick known from steppes and mountainous semidesert and desert regions in Europe, northwestern Africa and southwestern Asia (HOOGSTRAAL, 1973). Apparently this tick prefers a som~~-h~t dry habitat. Although the climate of The .Netherlands is . generally humid, the dunes inhabited by this tick are physiologicaliy dry. Not the whole of the dune area seems to be infested but only those places that are intensively sheep pastured. Ali infested hasts (sheep, birds, rabbits a. o.) were found in this area and only here H. punctata ticks were sampled by blanket dragging. Sorne authors believe that the abundance of birds on the Frisian islands are essential for the survival and distribution of the tick population (LIEBISCH & RAHMAN, 1976 ; MOHAMMED, 1976). We do not think that this is true and would like to formulate the hypothesis that the distribution of H. punctata is limited by the existence of suitable microclimatological conditions and the presence of enough larger mammals as hasts for ali stages of the tick. Since big game does not occur on the island of Texel (WIJNGAARDEN et al., 1971) and cattle or
horses are not regularly pastured in the dunes, sheep are the major host of this tick. In the future we hope to test our hypothesis by accumulation of evidence from other Frisian islands.
-23-
TABLE 1. Mammals as hasts or potential hosts of Haemaphysalis punctata and Ixodes ricin us on Texel (Chiroptera not included) *.
ticks removed ** Name ~f mammal No. sampled H. punctata I. ricin us
No. mammals 1. 9
No. mammals 1. 9 infested
n. 0" infested
n. 0"
Erinaceus europaeus Hedgehog 0 Neomys jodiens Water Shrew 0 Oryctolagus cuniculus Rab bit 14 4 12 0 0 0 2 22 6 0 0 Lepus europaeus Brown Hare 0 Micro/us ratticeps *** Root Vole 12 0 0 0 0 Micro/us minutus Harvest Mouse 0 Apodemus sylvaticus Wood Mouse 75 0 4 7 0 0 0 Ra/lus norvegicus Brown Rat 0 Canis familiaris Dog 3 0 0 0 2 Mustela erminea Stoat 0 Putorius putorius jura Ferret 1 2 0 0 0 0 Felis catus Cat 2 0 2 0 0 0 Equus cabal/us Horse 2 2 Il Il 0 Bos taurus Cow 0 Ovis aries Dune sheep 35 32 27 39 23 20 9 4 3 Ovis aries Polder sheep 58 0 0 Capra hircus Go at 3 0 0 Homo sapiens **** Man 0 0 0
* lncluded are the domestic animais seen on the· island by the authors and the mammals mentioned by Wijngaarden et al., 1971. ln case many ticks were present on sheep only a small number were actually removed and counted.
*** Broek & Jansen (1969) also mentioned lv!. ratticeps as hasts for I. ricinus. **** Found running over an investigator one day after a visit to the island of Texel.
TABLE 2. Birds as hasts of Haemaphysalis punctata and Ixodes ricinus on Texel *.
ticks found
Name of bird No. sampled H. punctata I. ricin us
No. birds 1. 9
No. birds 1. 9 infested
n. 0" infested
n. 0"
Gallus domesticus Fowl 0 0 Tadorna tadorna ** Shelduck 2 0 0 Anas platyrhynchos Mallard 0 0 Haematopus ostralegus ** Oystercatcher 0 0 Vanel/us vanel/us ** Lapwing 0 0 Numenius arqua/a ** Curlew 1 0 2 0 1 6 0 0 Larus juscus Lesser Blackbac- 0 0
ked Gull Larus argenta/us** Herring Gull 102 0 0 Larus canus ** Common Gull 90 0 1 0 0 0 Anthus pratensis Meadow Pipit 1 1 2 0 0 0 0 Phylloscopus collybita Chiffchaff 2 0 0 Saxicola rubetra Whinchat 2 0 0 0 0 Phoenicurus phoenicurus Redstart 1 2 0 0 0 0 Turdus meru/a Blackbird 0 0 Passer domesticus House Sparrow 58 8 12 7 0 0 0 0 0 Sturnus vulgaris Star ling 3 0 0
* Only birds that were actually investigated, are included. ** Ducklings.
Even when birds do not limit the distribution of the tick, they are certainly important for dispersal. KAISER & HOOGSTRAAL (1974) saw larvae of H. punctata on a Willow Warbler and a Spotted Flycatcher travelling south through Cyprus. On Texel larvae of H. punctata are present in late summer and in autumn. Especially in this time of the year birds migrate southwards in coastal regions. But although this ticks is transported by birds over long distances no populations of H. punctata could be detected recently on the mainland of Germany (LIEBISCH & RAHMAN, 1976) and The Netherlands (BRONSWIJK et al., 1979 ; MOHAMMED, 1976 ; present in-vestigation).
Between 1880 and 1930 a number of populations -did exist on the mainland of Germany and The Netherlands (NUTTALL et al., 1915 ; SCHULZE, 1929 ; preparations in the Oudemanscollections, Leiden). Presumably agriculture and afforestation destroyed the ecological niches of this tick on the mainland (LIEBISCH & RAHMAN, 1976).
For reasons unknown the host relationships of H. punctata on the island of Texel differ significantly from those reported from Central Europe (NOSEK, 1971). Rodents were not infested with H. punctata on the island of Texel but were important hosts in Central Europe especially fo the larvae and nymphs.
The seasonal distribution of the different stages of H. punctata on Texel is different from those reported from Central Europe (NOSEK, 1971), Great Britain (ARTHUR, 1963) and the nord FriSlan island Amrum (LIEBISCH & RAHMAN, 1976). On Texel (own investigation) and on Ameland (MOHAMMED, 1974; UILENBERG et al., 1979) most adults and nymphs were found in spring and ali larvae in late summer and in autumn. In other European localities adults and nymphs were found in spring and autumn and larvae in summer. Presumably sorne microclimatological factors are responsible for the differences mentioned above.
H. punctata can be a hazard for man and his domestic animais on the Frisian islands. Man may be bitten by the tick, although this seems to occur infrequently. Ticks biting domestic animais
24 )
or man may transmit Babesia major (to cattle), Theileria sp. (to cattle), Babesia moiasi (to sheep), Anaplasma mesaeterum (to sheep), and possible Listeria monocytogenes (to man and sheep) (LIEBISCH & RAHMAN, 1976 ; UILENBERG et al., 1979; UILENBERG et al., 1980; NOSEK, 1971).
ACKNOWLEDGMENTS
We thank the Ministerie van Landbouw en Visserij, Staatsbosbeheer, Haarlem for permitting us to execute the investigations in the nature reserve on Texel and the Directie Faunabeheer, Zoetermeer for permitting us to catch small game. We thank the Ministerie van Cultuur, Recreatie en Maatschappelijk Werk, afdeling Fauna en Flora, Rijswijk for permitting us to catch birds and protected mammals, the fam. KOORN (de Cocksdorp) and Mr. DRIJVER (Den Hoorn) for cooperation on the island of Texel, and Mr. MERKENS for co-operation in Langbroek.
Gratitude is expressed to ir. D. KROESKE, dr. G. UILENBERG and dr. A. M. VOÛTE for correcting the manuscript.
LITTERATURE
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BROEK (E.) VAN DEN & JANSEN Jr. (J.), 1969. - Parasites of animais in The Netherlands. Suppl. III : Ecto- and entoparasites of wild mammals. - Bijdr. Dierkunde, 39 : 7-10.
BRONSWIJK (J. E. M. H.) VAN, RIJNTJES (R. H.), ÜARBEN (A. F. M.) & Vos (H.), 1979. - De teken (lxodida) van de Benelux-landen. - Wetensch. Meded. Kon. Ned. Natuurhist. Ver. 131 : 1-36.
HOOGSTRAAL (H.), 1973. - Parasites of endothermal laboratory animais. Ticks. Chap. 14 : pp. 398-424, in Diseases of Laboratory Animais (Flynn, R. J., . ed.). - Univ. Iowa Press, Ames.
KAISER (M. N.) & HOOGSTRAAL (H.), 1974. - Ticks (Ixodoidea) in migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. - Bull. Ent. Res. 64 : 97-110.
KALKHOVEN (J. T. R.), STUMPEL (A. H . P.) & STUMPEL-RIENKS (S. E.), 1976. - Landelijke Milieukartering. Een beeld van de natuur in Nèderland. Rijksinstituut voor Natuurbeheer,. Verhandeling 9, 's-Gravenhage : 141 pp., 5 bijlagen.
LIEBISCH (A.) & RAHMAN (M. S.), 1976. - Zum Vorkommen und zur Okologie einiger human- und vete-
rinarmedizinisch wichtiger Zeckenarten (Ixodidae) in Deutschland. - Zeitschr. Angew. Ent., 82 : 29-37.
LIEBISCH (A.), MELFSEN (J.) & RAHMAN (M. S.), 1976. - Zum Vorkommen der Zecke Haemaphysalis punctata (Cao. et Fanz., 1877) und von Babesia major beim R.ind in Nord-deutschland. - Berl. Münch. Tierartl. Wochenschr. 89 : 477-480.
MOHAMMED (A. N.), 1974. - The seasonal incidence of Ixodid ticks of cattle in northern Nigeria and in The Netherlancts, with particular reference to their role in the transmission of bovine piroplasms. -Ph. D. thesis, Zaria, Nigeria.
MOHAMMED (A. N.), 1976. - The seasonal incidence of Ixodid ticks in the Netherlands. - Tijdschr. Diergeneesk., 101 (8) : 408.412.
NOSEK (J.), 1971. _ The Ecology, Bionomics, and Behaviour of Haemaphysalis (Aboimisalis) punctata tick in Central Europe. _ z. Parasitenk., 37 : 198-210.
NUTTALL (G. H. P.), WARBURTON (C.), COOPER (W. F.) & ROBINSON CL. E.), 1915. _ Ticks : A monograph
25
of the Ixodoidea. Part III. Haemaphysalis. - Univ. Press. Cambridge.
RITZEMA Bos (J.), 1888. - De dierlijke parasieten van de mensch en de huisdieren. - W. E. J. Tjeenk Willink, Zwolle, 262 pp.
SCHULZE (P.), 1929. - Zecken Ixodides. Tierwelt Mitteleuropas, Leipzig.
UILENBERG (G.), VORSTENBOSCH (C. J. A. H. V.) VAN & PERlÉ (N. M .), 1979. - Blood parasites of sheep in the Netherlands. 1. Anaplasma mesaeterum sp. n. (Rickettsiales, Anaplasmataceae). - Vet. Quarterly, 1 (1) : 14-22.
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WIJNGAARDEN (A.) VAN, LAAR (V.) VAN & TROMMEL (M. D. M.), 1971. - De verspreiding van de NederJandse zoogdieren. - Lutra, 13, 1-41, 64 kaarten.
Paru en avri/1982.