Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N Iberian peninsula)

June 12, 2017 | Author: Joxerra Aihartza | Category: Iberian Peninsula, First record
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Miscel.lania Zooloqica 22.2 (1999)

21

Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N lberian peninsula) E. Imaz, J. R. Aihartza & M. J. Totorika

Imaz, E., Aihartza, J . R. & Totorika, M . J., 1999. Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N lberian peninsula). Misc. Zool., 22.2: 21-30. Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N lberian peninsula).- A study on ectoparasites infesting Chiroptera in Biscay ( N lberian peninsula) was carried out during a distribution survey of bats. 160 potential hosts were examined and 664 ectoparasites were found, collected manually from living bats by means of pointed tweezers. The ectoparasites belonged t o 12 species and 2 subspecies: 5 species and 2 subspecies of Gamasida, 2 species of lxodida and 5 species of Diptera. First records in the study area were obtained for Eyndhovenia euryalis euryalis, Eyndhovenia euryalis oudemansi, Argas vespertilionisand Penicillidia dufouri. Spinturnix plecotina on Rhinolophus ferrumequinum and Rhinolophus euryale and lxodes vespertilionis on Myotis nattereri are reported for the first time in the lberian peninsula; Basilia nattereri is new on Myotis nattereriin Biscay. Associations between parasites and hosts are also reported. Key words: Chiroptera, Gamasida, Ixodida, Diptera, N lberian peninsula. (Rebut: 13 X 98; Acceptació condicional: 2 11 99; Acc. definitiva: 2 1 XII 99) E. Imaz, J. R. Aihartza & M. J. Totorika, Zoologia eta Animali Zelulen Dinamika Saila, Euskal Herriko Unibertsitatea, 644 p. k., E 48080, Bilbo, Espana (Spain).

O 1999 Museu de Zoologia

22

Imaz et al.

Introduction Most papers on bat ectoparasites are descriptive and about most groups little is known about their world-wide distribution and biology and/or ecology. The few studies in the lberian peninsula are fragmentary and the only records on bat ectoparasites in Biscay were assembled during the 50's and 60's by Dr. BALCELLS (1968), some of which were later reexamined by ESTRADA-PErZJA et al. (1988, 1989, 1990, 1991). This paper shows the results of a survey carried out in Biscay. Studied groups belong

to the following families of Arthropoda: Spinturnicidae (Acari, Gamasida), Ixodidae (Acari, Ixodida), Argasidae (Acari, Ixodida) and Nycteribiidae (Diptera). Different taxa found on bats and associations between parasites and hosts are reported. Material and methods During a distribution survey 12 bat species were examined for ectoparasites. Batflies (Diptera) were collected from 160 individuals from July 1994 to June 1995. Mites (Acari,

Table 1, Number of examined bats and number of associated ectoparasites. Ectoparasites: EEE. E. e. euryalis; EEO. E. e. oudemansi; EES. E. e. subspp; SPL. S. plecotína; SMY. S. myotí; SPS. S. Psi; PRH. rhinolophinus; IVE. /. vespertilionis; AVE. A. vespertilionis; NBI. N. biarticulata; NSC. N. schmidii; BNA. 13. nana; BNT. B. nattereri; PDU. P dufouri. Hosts: Rhf. R. ferrumequinum; Rhe. R. euryale; Rhh. R. hipposíderos; Pp. P. pipistrellus; Pn. P. nathussil; Pk. P. kuhlii; Ms. M. screíbersii; Mm. M. myotis; Me. M. emarginatus; Mn. M. natteril; Paur. P. auritus; Paus. P. austriacus. Nb. Number of bats examined; Np. Number of parasites found. Número de murciélagos estudiados y número de ectoparésitos asociados. (Para las abreviaturas ver arriba.)

Ectoparasites Arachnida Gamasida

Insecta Ixodida

Diptera

Hosts

Nb

Np

Rhf

24

65

5

30

3

9

0

0

7

4

0

7

0

0

0

0

Rhe

23

44

14

0

2

1

0

0

0

0

0

24

3•

0

0

0

Rhh

50

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Pp

26

20

4

0

0

0

0

0

0

0

20

0

0

0

0

Pn

1

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Pk

19

11

0

0

0

0

0

0

0

0

11

0

0

0

0

0

Ms

33

273

2

0

0

0

0

251

0

0

0

0

19

0

0

1

Mm

2

34

0

0

0

0

33

0

0

0

0

0

0

0

0

1

Me

5

2

0

0

0

0

0

0

0

0

0

0

0

0

0

2

Mn

4

6

0

0

0

0

0

Q

0

1

0

0

0

3

2

0

EEE EEO EES SPL SMY SPS PRH

IVE AVE NBI NSC BNA BNT PDU

Paur

12

3

0

0

0

3

0

0

0

0

0

0

0

0

0

0

Paus

6

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Total

160

458

21

30

5

13

33 251

7

5

31

31

22

3

2

4

Miscel.lania Zoologica 22.2 (1999)

Garnasida) and ticks (Acari, Ixodida) were sampled i n 135 potential hosts frorn January t o June i n 1995. When more than one b a t was captured a t t h e sarne t i m e they were kept in separate bags. Ectoparasites were collected rnanually frorn living bats by rneans o f pointed tweezers. Consequently, only the most conspicuous parasites on f u r and t h e largest o n t h e patagium were removed. Bats were t h e n released. Sarnples were stored i n ethyl acetate and identified under rnicroscope. Even i f t h e sarnpling rnethod is biased an equal bias f o r al1 t h e species is accepted. Thus, w e calculated associations between parasites and hosts frorn data i n table 1, excluding b a t species o n which n o parasites were found, by rnean o f Pi-square rneasure t o estimate similarity and t h e unweighted pair-group rnethod (UPGNA) f o r clustering (No~usis,1993).

e House; Mt. ~ i h tunnel Ob. Other buildings. Localidades donde se

Localitv T v ~ e

Townshi~

UTM

0056

C

Karrantza

VN68

0243

Ch

Atxondo

WN37

0292

Ch

Lernoiz

WPOO

Results A t o t a l o f 664 ectoparasites were collected, frorn which 12 species and 2 subspecies were identified: 5 species and 2 subspecies o f Gamasida, 2 species o f lxodida and 5 species o f Diptera (table 1). Besides groups studied here, rnany rnacronyssids (Garnasida, Macronyssidae) a n d fleas (Siphonaptera, Ischnopsyllidae) were also collected b u t have n o t been included i n this work. Inforrnation a b o u t each locality is shown i n table 2.

Class Arachnida Order Parasitiforrnes Suborder Garnasida (= Mesostigrnata) Family Spinturnicidae Genus Eyndhovenia Rudnick, 1960 Eyndhovenia euryalis (Canestrini, 1884) A total o f 56 individuals o f this species was collected. Five o f thern could not be identified at subspecies level, d u e t o hard asyrnrnetry on setae distribution and their poor preservation status. Three o f them were collected from one Rhinolophus ferrumequinum (Schreber. 1774) i n cave No 0028, where colonies o f R.

lmaz et al.

ferrumequinum, Rhinolophus euryale Blasius, 1853, Miniopterus schreibersii (Kuhl, 1817) and Myotis emarginatus (E. Geoffroy, 1806) can be found. Two more were found on R. euryale i n roost No 0006; this roost is used by small breeding colonies o f R. ferrumequinum and M. emarginatus, b u t R. euryale is only an occasional visitor. Eyndhovenia euryalis euryalis (Canestrini, 1884) This subspecies is recorded for the first time in Biscay, where 21 individuals were found. R. euryale seems t o be its main host (see table l), even though al1 the individuals carrying this parasite were caught i n t h e same temporary colony, i n cave No 0004, which is also used by R. ferrumequinum, M. schreibersii and M. emarginatus. I t was also collected f r o m R. ferrumequinum in cave No 0028, and f r o m M. schreibersii i n cave No 0031, where this species forms temporary groups. Eyndhovenia euryalis oudemansi (Eyndhoven, 1941) This species is reported on R. ferrumequinum, o n which it was f o u n d i n 30% o f checked individuals. Recorded f o r the first t i m e i n Biscay, where i t shows a high specificity f o r this bat species (table 1). Found in t h e attic o f church No 0266, i n cave No 0028 and i n a small breeding colony i n farm house No0006.

Genus Spinturnix Von Heyden, 1826 Spinturnix plecotina Koch, 1839 This species was collected on Plecotus auritus (Linnaeus, 1758) i n churches No 0243 and 0326, and o n R. ferrumequinum i n church No0266, and from R. euryale in cave No 0004. Horseshoe bats are new hosts i n t h e lberian peninsula.

(genus Myotis) were exarnined, it was only f o u n d occurring on one Myotis myotis (Borkhausen, 1797). Spinturnix psi Kolenati, 1856 A total of 251 individuals were collected, al1 occurring on Miniopterus schreibersii. A l l hosts were caught from t w o ternporary colonies in caves No 0004 and 0031.

Genus Paraperiglischrus Rudnick, 1960 Paraperiglischrus rhinolophinus Koch, 1841 It is recorded f o r t h e first t i m e i n Biscay. Seven specimens were collected, al1 from a single sample o f the 44 R. ferrumequinum host species checked. I t was f o u n d i n an o l d farm house, No0006, where srnall colonies o f R. ferrumequinum and M. emarginatus breed.

Suborder lxodida (= Metastigmata) Family lxodidae Genus lxodes Latreille lxodes (Eschatocephalus) vespertilionis Koch, 1844 This parasite was found occurring on R. ferrumequinum a n d Myotis nattereri (Kuhl, 1817). The latter is recorded for the first time in t h e lberian peninsula. All these records were obtained from hosts caught in underground roosts: caves No0295,0297 and 0028, and mine tunnel No 0055.

Family Argasidae Genus Argas Latreille, 1796 Argas (Carios) vespertilionis (Latreille, 1802)

Spinturnix m y o t i Kolenati, 1856 The m y o t i species group i s conflictive within t h e Spinturnix genera (UCHIKAWA et al., 1994). The species was identified according t o t h e description given b y UCHIKAWAet al. (1994) f o r S. myoti. Although sorne other mouse-eared bats

These parasites w e r e c o l l e c t e d f r o r n Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus k u h l i i (Kuhl, 1819). Hosts were caught b o t h i n roosts and f o r a g i n g sites, localities No 0234, 0288, 0292, 0340 a n d 0336 f o r P. pipistrellus, and No 0090 a n d 0358 f o r P. kuhlii.

Miscel.lania Zoologica 22.2 (1 999)

25

Class lnsecta (= Hexapoda) Order Diptera Farnily Nycteribiidae

caught in caves 0004 and 0051, and the latter in buildings number 0006 and 0071.

Genus Nycteribia Latreille, 1796

Affinities between species

Nycteribia biarticulata Herrnann, 1804

Figure 1 shows t h e affinities between parasite species depending o n host species. A preliminary view enables identification of a large block o f parasites which includes the first seven taxa arranged in the cluster. The first group is forrned by Eyndhovenia euryalis oudemansi and Paraperiglischrus rhinolophinus, w i t h high affinity, followed by Spinturnix plecotina and lxodes vespertilionic. The second group in this big block is formed by Eyndhovenia euryalis euryalis, Nycteribia biarticulata and Eyndhovenia euryalis subspp. Rernaining parasite taxa d o n o t seern t o be so clearly inter-related further than at level o f small groups. Thus, Basilia nana and Basilia nattereri appeared very close. Nycteribia schmidli is also linked t o Spinturnix psi b u t t h e affinity is lower. Finally, Spinturnix m y o t i and Penicillidia dufouri are n o t clearly included i n any group, and Argas vespertilionis appears notably alone. Figure 2 shows association between host species depending o n their parasites. Affinity is low except f o r P. pipistrellus and P. kuhlii. The second group is constituted by R. ferrumequinum, P. auritus and R. euryale, and t h e t h i r d by M. myotis, M. emarginatus and M. schreibersii w i t h lower affinity. Finally, M. nattereri appears alone.

They had been collected occurring on R. ferrumequinum and R. euryale. For the forrner host species, this parasite was found i n 6 roosts, four caves and t w o breeding places in houses, localities No 0006, 0028, 0066, 0272, 0295, and 0297. I t was also collected from R. euryale i n t h r e e caves and one house, No 0004,0006,0056 and 0066. Nycteribia (Listropodia) schmidli Scheiner, 1853 Almost al1 o f thern were collected from M. schreibersi. Three specirnens found occurring o n one R. euryale can n o t be considered as valid data, as this bat was n o t isolated after capture, b u t was i n contact w i t h other Schreiber bats. Thus it can be considered as a casual parasitisrn. M. schreibersii bearing this species were caught i n three temporary roost caves, No 0004, 0028 and 0031. The specimen o f R. euryale was taken i n cave N00066, which is also used as a temporary roost by M. schreibersii.

Genus Basilia Ribeiro, 1903 Basilia nana Theodor & Moscona, 1954 These parasites were collected on M. nattereri i n t w o artificial underground sites, No 0055 and 0073. used as occasional roosts. Basilia nattereri Kolenati, 1857 Collected frorn M. nattereri, this is a new host f o r this batfly i n t h e Biscay locality No 0055.

Genus Penicillidia Kolenati. 1863 Penicillidia d u f o u r i Westwood, 1835 Collected on M. schreibersii, M. myotisand M. emarginatus. The forrner two host species were

Discussion These data confirm t h e presence o f five species and t w o subspecies o f Garnrnasids i n Biscay, o f which one species and one subspecies are recorded for the first time. Arnong thern, Eyndhovenia euryalis is a typical parasite o f horseshoe bats (genus Rhinolophus) i n Europe, i n which three subspecies have been described according t o different rneasurernents f o r different forrns and rnorphological aspects related w i t h t h e idiosoma, dorsal shield, seta, peritrerna, tritosternum, sternal shield, and legs (UCHIKAWA & DUSBABEK, 1978): E. euryalis euryalis, E. euryalis oudemansi, and E. euryalis cornuti. Only the first t w o were found i n this work. Regarding

26

lrnaz et al.

O 5 10 15 Label+---------+----------+--I------.+-----.---+-.---.---

EEO PRH IVE SPL EEE NBI EES

20

+

25

I

AVE

the first, our data agree w i t h previous works (Schreber, 1774), Eptesicus nilssonii (Keyserling stating horseshoe bats are t h e usual host o f et Blasius, 1839), Nyctalus noctula (Schreber, E. euryalis euryalis i n other countries o f Eu1774), Myotis nattereri, Myotis mystacinus rope and t h e lberian peninsula, where it (Kuhl, 1817), Myotis b r a n d t i i (Eversrnann, also occurs o n M. schreibersii (DEUNFF, 1977; 1845) and Myotis daubentonii (Kuhl, 1817) UCHIKAWA & DUSBABEK, 1978; PERIBANEZ-L~PEZ et (DEUNFF,1977; ESTRADA-PENA e t al., 1989; al., 1989). However, E. euryalis oudernansi STANJUKOVICH, 1990). Furthermore, Spinturnix was f o u n d only o n R. ferrurnequinurn. This rnyoti was previously found i n al1 checked also agrees w i t h other authors'data f o r EuMyotis species i n t h e lberian peninsula rope and t h e lberian peninsula (UCHIKAWA& (ESTRADA-PENA et al., 1991). as well as i n genDUSBABEK, 1978; PEREIRA, 1989; ESTRADA-PENA et era Barbastella, Eptesicus, Vespertilio, al., 1991), and it differs considerably frorn Plecotus, Rhinolophus and Pipictrellus i n t h e North African pattern, where E. e. other European areas (DEUNFF,1977; STANJUoudernansi was also reported o n R. mehelyi KOVICH, 1990). Lastly, Spinturnix psi, appears specific for M. schreiberssi, and even indiet al., 1991). a n d R. euryale (ESTRADA-PENA Three species o f genus Spinturnix were v i d u a l ~of R. euryale caught i n t h e same confirmed i n Biscay S. plecotina, S. rnyoti and roosts were free o f it. This agrees w i t h data S. psi, whose presence was unclear f r o m t h e from other authors i n Europe (RUDNICK,1960; bibliography available (ESTRADA-PENA et al., BERON,1971; DEUNFF, 1977; ESTRADA-PENA et al., 1989; ESTRADA-PE~A et al., 1991; CORDERO DEL e t al., 1993), and 1989, 1991; PERIBANEZ-LÓPEZ C A M P I L L al., O ~ ~1994). On the first hand, horsealthough this parasite has been found o n shoe bats are new hosts f o r S. plecotina i n Pipistrellus, Rhinolophus and Myotis bat spet h e lberian peninsula. P. auritus is its rnost cies, these cases were considered occasional usual host i n Europe, although it occurs on contarnination (DEUNFF, 1977). R. ferrurnequinurn, Eptesicus serotinus The last garnrnasid, Paraperiglischrus

Miscel.lania Zoologica 22.2 (1999)

Rf Paur Re Mn

rhinolophinus, which was f o u n d only o n R. ferrumequinum during this work, has been reported showing high specificity as a parasite o f other horseshoe bats (DEUNFF, 1977; ESTRADA-PENA et al., 1989; CORDERO DEL CAMPILLO et al., 1994). Some lack o f observations about this species could happen due t o t h e more inexhaustive examination methods o f lateral and w i n g membranes. lndividuals o f this species, mainly females and nymphs, prefer t o be o n t a i l membranes (DEUNFF& BEAUCOURNU, 1981). Among Ixod ida, lxodes (Escha tocephalus) vespertilionis was reported previously occurring o n R. ferrumequinum and P. auritus i n et al., 1989; CORDERO DEL Biscay (ESTRADA-PENA CAMPILLO et al., 1994), where it does n o t seem t o be an abundant species. R. ferrumequinum has been considered its main host in Europe, b u t it has been detected o n several bat species, showing high infestation level in some cases (ARTHUR, 1963; BEAUCOURNU, 1967; HUTSON, 1971; ESTRADA-PENA et al., 1989; CORDERO DEL CAMPILLO e t al., 1994). Although it had also been considered as a " w i n t e r species" (BEAUCOURNU, 1967) only five individuals were collected f r o m February t o June. No lxodes simples Neumann, 1906, was recorded. This parasite is widespread in Central and Eastern

27

I

Europe o n M. schreibersii b u t is rare in t h e lberian peninsula (ARTHUR, 1956; BEAUCOURNU, 1967; ESTRADA-PENA et al., 1991).Argas (Carios) vespertilionis, recorded f o r t h e first time i n Biscay, is a widely distributed species (Europe, Asia a n d Africa), w h i c h prefers pipistrelle bats b u t can occur on al1 bat species except on horseshoe bats (BEAUCOURNU, 1961; CORDERO DEL CAMPILLO e t al., 1994; DUSBABEK & ROSICKY,1976). I t can also occur o n people i n human buildings when n o bat 1933; HOOSTRAAL, host is present (COLAS-BELCOUR, 1956). Concering batflies, t h e occurrence o f Nycteribia biarticulata o n R. ferrumequinum and R. euryale agrees w i t h data f r o m other countries, where this insect was also reported on other horseshoe bats, b u t mainly on these t w o species (THEODOR& MOSCONA,1954; BALCELLS, 1968; KRISTOFIK,1982; ESTRADA-PENA et al., 1991; CORDERO DEL CAMPILLO et al., 1984). In the same way, the high amount o f Nycteribia schmidli found over M. schreibersii agrees w i t h t h e general view t h a t considers this batfly as a typical constituent o f this bat parasite fauna, even i f occasionally small numbers are found on other species (THEODOR & MOSCONA, 1954; KRISTOFIK, 1982; ESTRADA-PENA et al., 1991).

28 The first record of Basilia nana in Biscay and its occurrence on M. nattereri, agrees with previous knowledge about this parasite in the lberian peninsula, where this bat species is its main host. It has also been recorded occurring on Myotis bechsteini (Bechstein's bat), Myotis dasycneme (pond bat), Myotis blythi (lesser mouse-eared bat), Myotis myotis, Myotis emarginatus(Geoffroy's bat), R. ferrumequinum, P auritus as well as on M. schreibersii (THEODOR & MOSCONA, 1954; HUTSON, 1984). BEAUCOURNU (1961) noted M. bechsteini as its main host in Western France. On the other hand, the occurrence of Basilia nattereritogether with B. nana on the same individual of M. nattereri shows an intermediate position between previous northern and southern records. In fact, M. nattereri is a common host of Basilia nattereri in Central Europe where it also infests other small Myotis bats and E. serotinus but on the lberian peninsula this bat is usually parasited by Basilia nana (ESTRADA-PENA et al., 1991). The last species, Penicillidia dufouri, is recorded first on M. emarginatus in the lberian peninsula. It seems to be a nonspecific parasite, since it was previously recorded mainly on M. myotis and M. blythii, but also on other several species such as M. nattereri, Myotis capaccini, R. mehelyi, R. euryale, R. ferrumequinum, E. serotinus and M. schreibersii (FALCOZ, 1923; BALCELLS, 1968; KRISTOFIK, 1982; ESTRADA-PENA et al., 1991; CORDERO DEL CAMPILLO et al., 1994). It is difficult to draw conclusions concerning the affinities between the parasite species and host species shown in figures 1 and 2 as there is an insufficient quantity of data available for many parasite and host species. In figure 1, the large block formed by the first seven taxa is related to parasites of horseshoe bats (genus Rhinolophus), though Spinturnix plecotina is known as parasite on several bat species, and its occurence in this group can be an artifact (DEUNFF, 1977; ESTRADA-PENA et al., 1989; STANJUKOVICH, 1990). The highest affinity between Eyndhovenia euryalis oudemansi and Paraperiglischrus rhinolophinus reflects that they were recorded only on R. ferrumequinum, but only the former has a high specifity for this host, while the latter is a typical parasite of horseshoe bats (DEUNFF, 1977; ESTRADA-PENA et al., 1989; CORDERO DEL CAMPILLO et al., 1994). The same can be argued for Eyndhovenia euryalis

Imaz et al. euryalis and Nycteribia biarticulata, which following our data can be identified as the parasite group of R. euryale, though they are also found also in other rhinolophids in Europe (THEODOR & MOSCONA, 1954; BALCELLS, 1968; DEUNFF, 1977; UCHIKAWA & DUSBABEK, 1978; KRISTOFIK, 1982; CORDERO DEL CAMPILLO et al., 1984; PERIBANEZ-LOPEZ et al., 1989; ESTRADA-PENA et al., 1991). About the remainder, the only consistent group is formed by Nycteribia schmidli and Spinturnix psi, which are considered as the typical parasite fauna of M. schreibersii (THEODOR & MOSCONA, 1954; KRISTOFIK, 1982; ESTRADA-PENA et al., 1991). The higher affinity of Basilia nana and Basilia nattereri is explained by the scarcity of data. Even if they have only been found on M. nattereri during this work, they are known to occur on several bat species in Europe (THEODOR & MOSCONA, 1954; HUTSON, 1984; BEAUCOURNU, 1961). The same occurs with Spinturnix myoti and Penicillidia dufouri, which are not clearly included in any group. And the last case, Argas vespertilionis, which in this work was found only on Pipistrellus, can also be found on other vespertilionids but it shows preference for this bat genus (BEAUCOURNU, 1961; CORDERO DEL CAMPILLO et al., 1994; DUSBABEK & ROSICKY, 1976). About the affinities between host species, the first group formed by P. pipistrellus and P. kuhlii and the high affinity it shows is a consequence of the ixodid Argas vespertilionis, which has a documented preference for this host genus (BEAUCOURNU, 1961; CORDERO DEL CAMPILLO et al., 1994; DUSBABEK & ROSICKY, 1976). The second group includes M. myotis, M. emarginatus and M. schreibersii, but it could be the consequence of data scarcity, specially about the first two bat species. In fact, the parasite species that can explain this grouping in our data is P. dufouri, and many host species have been recorded for it in previous works. Moreover, despite occasional cases, M. schreibersii has an own parasite fauna, including species such as S. psi and N. schmidli. Thus, we can suppose that more data about ectoparasites of M. myotis and M. emarginatus would change this grouping. The third group, formed by R. ferrumequinum, P. auritus and R. euryale, to be more clear, being a consequence of typical parasites of horseshoe bats such as N. biarticulata, E. euryalis euryalis,

Miscel.lania Zooloqica 22.2 (1999)

a n d S. plecotina, which i s t h e link between rhinolophids and P. auritus. Finally, t h e seclusion o f M. nattereri must be explained i n t h e same way as f o r t h e other Myotis species, as a consequence o f t h e scarcity o f data, and more information is needed bef o r e a clear view about t h e i r a f f i n i t y patt e r n is obtained.

biarticulata, N. schmidli, Basilia nana, B. nattereri observado por primera vez sobre M. nattereri en Bizkaia, y Penicillidia dufouri primera cita en Bizkaia. También se comenta la afinidad entre especies de parásitos dependiendo de las especies de murciélagos que infestan (fig. 1) y la afinidad entre especies de murciélagos dependiendo de las especies de parásitos que soportan (fig. 2).

Acknowledgements References We would like t o thank E. Bernedo, G. Razkin and R. Agirrebeña f o r their help in the surveys. Special thanks t o J. C. Iturrondobeitia, A. l. Caballero and C. Andrés for their teaching and advice on acarology, and t o Dr. A. M. Hutson and Dr. R. L. C. Pilgrim for their help i n obtaining references.

Resumen Ectoparásitos d e q u i r ó p t e r o s en Bizcaya (N península ibérica) Durante u n estudio de distribución de murciélagos se ha desarrollado un estudio sobre ectoparásitos de quirópteros en Bizkaia (N penísula ibérica). Se han examinado 160 hospedadores potenciales hallándose 664 parásitos. Estos fueron recogidos manualmente sobre murciélagos vivos mediante pinzas afiladas, y conservados en acetato de etilo para su posterior análisis microscópico. Una vez recogidas las muestras los murciélagos fueron puestos nuevamente en libertad. Los ectoparásitos recogidos pertenecen a 12 especies y 2 subespecies (tabla 1) (se han excluido de este trabajo los macronisidos e ischnpsillidos recogidos). Entre los gamásidos se han capturado Eyndhovenia euryalis euryalis y Eyndhovenia euryalis oudemansi, los cuales constituyen primeras citas para el área de estudio, Spinturnixplecotina citado por primera vez sobre Rhinolophus ferrumequinum y Rhinolophus euryale en la península Ibérica, y sobre Plecotus auritus en Bizkaia, S. myoti, S. psi y Paraperiglischrus rhinolophinus. Entre los ixódidos se aporta la primera observación de Argas vespertilionis en Bizkaia, y la primera de lxodes vespertilionis sobre Myotis nattereri en la península Ibérica. Por último, entre los nicterébidos se han recogido Nycteribia

ARTHUR,R., 1956. The lxodes Ticks o f Chiroptera (Ixodoidea, Ixodidae). The Journ a l o f Parasitology, 42: 180-184. - 1963. lxodes vespertilionis C. L.. Koch 1844. British Ticks: 135-144. BALCELLS, E., 1968. Nuevas citas de murciélagos y nicteríbidos del País Vasco-Cantábrico, Bol. R. Soc. Española Hist. Nat. (Biol.), 66: 17-38. BEAUCOURNU, J. C., 1961. Ectoparasites des Chiropteres de L'Ouest de la France. la partie: Ixodoides-Cimicides et Nyctéribiidés. Bulletin de la Société Scientifique de Bretagne, 36: 31 5-338. - 1967. Contribution a la connaissance de la biologie d'lxodes (Eschatocephalus) vespertilionis Koch 1844 e t d'lxodes (Pomerantzevella) simplex Neumann 1906 (Acarina, Ixodoidea), parasites des cuiropteres. Annales d e Spéléologie, 22(3): 545-577. BERON,P., 1971. Sur quelques acariens parasites des mammiferes et des reptiles de France. Bull. Soc. Hist. Nat. de Tolouse, 107 (1-2): 96-102. COLAS-BELCOUR, J., 1933. Contribution a I'étude de la biologie de I'Argas vespertilionis Latr. Bull. Soc. Pathol. exot., 26: 937-940. CORDERO DEL CAMPILLO, M., C A S T A ~L.~ ~&~REGUERA, N, A., 1994. Indice-catálogo de Zooparásitos Ibéricos. Secretariado de Publicaciones de la Universidad de Leon, León. DEUNFF, J., 1977. Observations sur les Spinturnicidae de la région palearctique occidentale (Acarina, Mesostigmata) spécifité, r é p a r t i t i o n e t morphologie. Acarologia, 8(4): 602-617. DEUNFF, J. & BEAUCOURNU, J. C., 1981. Phénologie et variations du dermecos chez quelques especes d e Spinturnicidae (Acarina, Mesostigmata). Annales de Parasitologie, 56(2): 203-224.

I

lmaz e t al.

PEREIRA, A., 1989. Contribución al estudio de DUDBEBAK, F. & ROSICKY, B., 1976. Argasid ticks ectoparásitos de micromamíferos de la (Argasidae, Ixodoidea) o f Czechoslovakia. Comunidad Autónoma gallega: Acaros del Acta Sc. Nat. Brno, 1O(7): 1-43. ESTRADA-PENA, A., SANCHEZ-ACEDO, C., PERIBANEZ- suborden Mesostigmata y de la familia L ~ P E M. Z , A., BALCELLS-ROCAMORA, E. & SERRATrombiculidae; Insectos del Orden SiphoCoeo, J., 1988. Nuevos datos relativos a la naptera. Tesis doctoral, Universidad de Sandistribución de los lxodoidea de España. tiago de Compostela. III. Garrapatas de Quirópteros. Rev. Iber. PER~BANEZ-L~PEZ, M. A., ~ÁNCHEZ-ACEDO, C. & ESTRADA-PENA, A., 1989. Estudio morfológico Parasitol., 48(2): 203-204. ESTRADA-PENA, A., PERIBANEZ-L~PEZ, M. A., SANCHEZde los ácaros de la familia Spinturnicidae ACEDO, C., BALCELLS-ROCAMORA, E. & SERRA-COBOS, (Acarina, Gamasida) del Norte y Levante J., 1989. Distribution and faunal composiK Parasitol., 49(4): 357-373. español. R ~ Ibér. t i o n in North and Northeast o f Spain o f PERlBÁÑtZ-L~PEZ,M. A., ESTRADA-PENA, A., some mites and ticks parasitic on Chiroptera SANCIIEZ-ACEDO, C. & SERRA-COBO, J., 1993. (Spinturnicidae, Macronyssidae, Ixodidae, Acarofauna parasita d e l murciélago troglodita, Miniopterus schreibersi (Kuhl, and Argasidae). Acarologia, 30(4): 345-353. ESTRADA-PENA, A., leAÑ~z,C. & TRUIILLO, D., 1990. 1819). Distribucion estaciona1 d e las Nuevas citas de ácaros parásitos de especies mas representativas. Doñana, Acta Quirópteros en la Península Ibérica, Norte Vertebrata, 20(1): 73-81. RUDNICK, A., 1960. A revision o f mites of the de África e Islas de la Macaronesia. Rev. Iber. Parasitol., 50(1-2): 91-94. family Spinturnicidae. Univ. o f California Press.: 157-282. ESTRADA-PENA, A., BALCELLS, E. & SERRA-COBO, J., 1991. Los artropodos ectoparásitos de STANIUKOVICH, M. K., 1990. The gamasid mites murciélagos en España. In: Los Murciélagos and argasid ticks o f bats from Pribaltica de España y Portugal: 253-279 (J. Benzal and Leningrad district. Parasitología, & O. de Paz, Eds.). Ed. ICONA, Madrid. 24(3): 193-200. FALCOZ, L., 1923. Pupipara (Diptera).Archives A., 1954. On bat paraTHEODOR, O. & MOSCONA, de Zoologie Expérimentale e t Générale, sites in Palestine. l. Nycteribiidae,Streblidae, 61(4): 36 & 521-552. Hemiptera, Siphonaptera. Parasitology, 44: HOOGSTRAAL, H., 1956. African Ixodoidea. 1. 157-245. Ticks o f t h e Sudan. Dep. Med. Zool. U. S. UCHIKAWA, K. & DUSBABEK, F., 1978. Studies On mesostigmatid mites parasitic on mammals Naval Med. Res. Unit 3, Cairo. and birds in Japan. VIII: Bat mites o f t h e HUTSON, A. M., 1971. Ectoparasites o f British bats. Mammal review, lO(6): 143-150. genus Eyndhovenia, Rudnick, 1960, w i t h - 1984. Keds, Flat-Flies and Bat-Flies. Diptera, redescription o f Eyndhovenia euryalis euryalis (Canestrini, 1884). Bull. Natn. Sci. Hippoboscidae and Nycteribiidae. In: HandMus., Ser. A. (Zool.), 4(4): 245-261. books for the ldentification o f British Insects, UCHIKAWA, K., MENG-YU ZHANG,O'CONNOR, B. M. Vol. 10, Part 7. Ed. M. G. Fitton, London. J., 1982. Finds o f flies o f t h e family & KLOMPEN, H., 1994. Contribution t o t h e KRISTOFIK, Nycteribiidae (Diptera) on the territory o f taxonomy o f genus Spinturnix (Acari: Slovakia. Biológia (Bratislava), 37: 191-197. Spiniturnicidae), with the erection o f a new genus, Emballonuria. Folia Parasitologica, NORUSIS, M. J., 1993. SPSS for Windows. Professional Statistics Release 6.0. Chicago, Illinois. 41: 283-304.



Deskripsi

Miscel.lania Zooloqica 22.2 (1999)

21

Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N lberian peninsula) E. Imaz, J. R. Aihartza & M. J. Totorika

Imaz, E., Aihartza, J . R. & Totorika, M . J., 1999. Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N lberian peninsula). Misc. Zool., 22.2: 21-30. Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N lberian peninsula).- A study on ectoparasites infesting Chiroptera in Biscay ( N lberian peninsula) was carried out during a distribution survey of bats. 160 potential hosts were examined and 664 ectoparasites were found, collected manually from living bats by means of pointed tweezers. The ectoparasites belonged t o 12 species and 2 subspecies: 5 species and 2 subspecies of Gamasida, 2 species of lxodida and 5 species of Diptera. First records in the study area were obtained for Eyndhovenia euryalis euryalis, Eyndhovenia euryalis oudemansi, Argas vespertilionisand Penicillidia dufouri. Spinturnix plecotina on Rhinolophus ferrumequinum and Rhinolophus euryale and lxodes vespertilionis on Myotis nattereri are reported for the first time in the lberian peninsula; Basilia nattereri is new on Myotis nattereriin Biscay. Associations between parasites and hosts are also reported. Key words: Chiroptera, Gamasida, Ixodida, Diptera, N lberian peninsula. (Rebut: 13 X 98; Acceptació condicional: 2 11 99; Acc. definitiva: 2 1 XII 99) E. Imaz, J. R. Aihartza & M. J. Totorika, Zoologia eta Animali Zelulen Dinamika Saila, Euskal Herriko Unibertsitatea, 644 p. k., E 48080, Bilbo, Espana (Spain).

O 1999 Museu de Zoologia

22

Imaz et al.

Introduction Most papers on bat ectoparasites are descriptive and about most groups little is known about their world-wide distribution and biology and/or ecology. The few studies in the lberian peninsula are fragmentary and the only records on bat ectoparasites in Biscay were assembled during the 50's and 60's by Dr. BALCELLS (1968), some of which were later reexamined by ESTRADA-PErZJA et al. (1988, 1989, 1990, 1991). This paper shows the results of a survey carried out in Biscay. Studied groups belong

to the following families of Arthropoda: Spinturnicidae (Acari, Gamasida), Ixodidae (Acari, Ixodida), Argasidae (Acari, Ixodida) and Nycteribiidae (Diptera). Different taxa found on bats and associations between parasites and hosts are reported. Material and methods During a distribution survey 12 bat species were examined for ectoparasites. Batflies (Diptera) were collected from 160 individuals from July 1994 to June 1995. Mites (Acari,

Table 1, Number of examined bats and number of associated ectoparasites. Ectoparasites: EEE. E. e. euryalis; EEO. E. e. oudemansi; EES. E. e. subspp; SPL. S. plecotína; SMY. S. myotí; SPS. S. Psi; PRH. rhinolophinus; IVE. /. vespertilionis; AVE. A. vespertilionis; NBI. N. biarticulata; NSC. N. schmidii; BNA. 13. nana; BNT. B. nattereri; PDU. P dufouri. Hosts: Rhf. R. ferrumequinum; Rhe. R. euryale; Rhh. R. hipposíderos; Pp. P. pipistrellus; Pn. P. nathussil; Pk. P. kuhlii; Ms. M. screíbersii; Mm. M. myotis; Me. M. emarginatus; Mn. M. natteril; Paur. P. auritus; Paus. P. austriacus. Nb. Number of bats examined; Np. Number of parasites found. Número de murciélagos estudiados y número de ectoparésitos asociados. (Para las abreviaturas ver arriba.)

Ectoparasites Arachnida Gamasida

Insecta Ixodida

Diptera

Hosts

Nb

Np

Rhf

24

65

5

30

3

9

0

0

7

4

0

7

0

0

0

0

Rhe

23

44

14

0

2

1

0

0

0

0

0

24

3•

0

0

0

Rhh

50

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Pp

26

20

4

0

0

0

0

0

0

0

20

0

0

0

0

Pn

1

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Pk

19

11

0

0

0

0

0

0

0

0

11

0

0

0

0

0

Ms

33

273

2

0

0

0

0

251

0

0

0

0

19

0

0

1

Mm

2

34

0

0

0

0

33

0

0

0

0

0

0

0

0

1

Me

5

2

0

0

0

0

0

0

0

0

0

0

0

0

0

2

Mn

4

6

0

0

0

0

0

Q

0

1

0

0

0

3

2

0

EEE EEO EES SPL SMY SPS PRH

IVE AVE NBI NSC BNA BNT PDU

Paur

12

3

0

0

0

3

0

0

0

0

0

0

0

0

0

0

Paus

6

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Total

160

458

21

30

5

13

33 251

7

5

31

31

22

3

2

4

Miscel.lania Zoologica 22.2 (1999)

Garnasida) and ticks (Acari, Ixodida) were sampled i n 135 potential hosts frorn January t o June i n 1995. When more than one b a t was captured a t t h e sarne t i m e they were kept in separate bags. Ectoparasites were collected rnanually frorn living bats by rneans o f pointed tweezers. Consequently, only the most conspicuous parasites on f u r and t h e largest o n t h e patagium were removed. Bats were t h e n released. Sarnples were stored i n ethyl acetate and identified under rnicroscope. Even i f t h e sarnpling rnethod is biased an equal bias f o r al1 t h e species is accepted. Thus, w e calculated associations between parasites and hosts frorn data i n table 1, excluding b a t species o n which n o parasites were found, by rnean o f Pi-square rneasure t o estimate similarity and t h e unweighted pair-group rnethod (UPGNA) f o r clustering (No~usis,1993).

e House; Mt. ~ i h tunnel Ob. Other buildings. Localidades donde se

Localitv T v ~ e

Townshi~

UTM

0056

C

Karrantza

VN68

0243

Ch

Atxondo

WN37

0292

Ch

Lernoiz

WPOO

Results A t o t a l o f 664 ectoparasites were collected, frorn which 12 species and 2 subspecies were identified: 5 species and 2 subspecies o f Gamasida, 2 species o f lxodida and 5 species o f Diptera (table 1). Besides groups studied here, rnany rnacronyssids (Garnasida, Macronyssidae) a n d fleas (Siphonaptera, Ischnopsyllidae) were also collected b u t have n o t been included i n this work. Inforrnation a b o u t each locality is shown i n table 2.

Class Arachnida Order Parasitiforrnes Suborder Garnasida (= Mesostigrnata) Family Spinturnicidae Genus Eyndhovenia Rudnick, 1960 Eyndhovenia euryalis (Canestrini, 1884) A total o f 56 individuals o f this species was collected. Five o f thern could not be identified at subspecies level, d u e t o hard asyrnrnetry on setae distribution and their poor preservation status. Three o f them were collected from one Rhinolophus ferrumequinum (Schreber. 1774) i n cave No 0028, where colonies o f R.

lmaz et al.

ferrumequinum, Rhinolophus euryale Blasius, 1853, Miniopterus schreibersii (Kuhl, 1817) and Myotis emarginatus (E. Geoffroy, 1806) can be found. Two more were found on R. euryale i n roost No 0006; this roost is used by small breeding colonies o f R. ferrumequinum and M. emarginatus, b u t R. euryale is only an occasional visitor. Eyndhovenia euryalis euryalis (Canestrini, 1884) This subspecies is recorded for the first time in Biscay, where 21 individuals were found. R. euryale seems t o be its main host (see table l), even though al1 the individuals carrying this parasite were caught i n t h e same temporary colony, i n cave No 0004, which is also used by R. ferrumequinum, M. schreibersii and M. emarginatus. I t was also collected f r o m R. ferrumequinum in cave No 0028, and f r o m M. schreibersii i n cave No 0031, where this species forms temporary groups. Eyndhovenia euryalis oudemansi (Eyndhoven, 1941) This species is reported on R. ferrumequinum, o n which it was f o u n d i n 30% o f checked individuals. Recorded f o r the first t i m e i n Biscay, where i t shows a high specificity f o r this bat species (table 1). Found in t h e attic o f church No 0266, i n cave No 0028 and i n a small breeding colony i n farm house No0006.

Genus Spinturnix Von Heyden, 1826 Spinturnix plecotina Koch, 1839 This species was collected on Plecotus auritus (Linnaeus, 1758) i n churches No 0243 and 0326, and o n R. ferrumequinum i n church No0266, and from R. euryale in cave No 0004. Horseshoe bats are new hosts i n t h e lberian peninsula.

(genus Myotis) were exarnined, it was only f o u n d occurring on one Myotis myotis (Borkhausen, 1797). Spinturnix psi Kolenati, 1856 A total of 251 individuals were collected, al1 occurring on Miniopterus schreibersii. A l l hosts were caught from t w o ternporary colonies in caves No 0004 and 0031.

Genus Paraperiglischrus Rudnick, 1960 Paraperiglischrus rhinolophinus Koch, 1841 It is recorded f o r t h e first t i m e i n Biscay. Seven specimens were collected, al1 from a single sample o f the 44 R. ferrumequinum host species checked. I t was f o u n d i n an o l d farm house, No0006, where srnall colonies o f R. ferrumequinum and M. emarginatus breed.

Suborder lxodida (= Metastigmata) Family lxodidae Genus lxodes Latreille lxodes (Eschatocephalus) vespertilionis Koch, 1844 This parasite was found occurring on R. ferrumequinum a n d Myotis nattereri (Kuhl, 1817). The latter is recorded for the first time in t h e lberian peninsula. All these records were obtained from hosts caught in underground roosts: caves No0295,0297 and 0028, and mine tunnel No 0055.

Family Argasidae Genus Argas Latreille, 1796 Argas (Carios) vespertilionis (Latreille, 1802)

Spinturnix m y o t i Kolenati, 1856 The m y o t i species group i s conflictive within t h e Spinturnix genera (UCHIKAWA et al., 1994). The species was identified according t o t h e description given b y UCHIKAWAet al. (1994) f o r S. myoti. Although sorne other mouse-eared bats

These parasites w e r e c o l l e c t e d f r o r n Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus k u h l i i (Kuhl, 1819). Hosts were caught b o t h i n roosts and f o r a g i n g sites, localities No 0234, 0288, 0292, 0340 a n d 0336 f o r P. pipistrellus, and No 0090 a n d 0358 f o r P. kuhlii.

Miscel.lania Zoologica 22.2 (1 999)

25

Class lnsecta (= Hexapoda) Order Diptera Farnily Nycteribiidae

caught in caves 0004 and 0051, and the latter in buildings number 0006 and 0071.

Genus Nycteribia Latreille, 1796

Affinities between species

Nycteribia biarticulata Herrnann, 1804

Figure 1 shows t h e affinities between parasite species depending o n host species. A preliminary view enables identification of a large block o f parasites which includes the first seven taxa arranged in the cluster. The first group is forrned by Eyndhovenia euryalis oudemansi and Paraperiglischrus rhinolophinus, w i t h high affinity, followed by Spinturnix plecotina and lxodes vespertilionic. The second group in this big block is formed by Eyndhovenia euryalis euryalis, Nycteribia biarticulata and Eyndhovenia euryalis subspp. Rernaining parasite taxa d o n o t seern t o be so clearly inter-related further than at level o f small groups. Thus, Basilia nana and Basilia nattereri appeared very close. Nycteribia schmidli is also linked t o Spinturnix psi b u t t h e affinity is lower. Finally, Spinturnix m y o t i and Penicillidia dufouri are n o t clearly included i n any group, and Argas vespertilionis appears notably alone. Figure 2 shows association between host species depending o n their parasites. Affinity is low except f o r P. pipistrellus and P. kuhlii. The second group is constituted by R. ferrumequinum, P. auritus and R. euryale, and t h e t h i r d by M. myotis, M. emarginatus and M. schreibersii w i t h lower affinity. Finally, M. nattereri appears alone.

They had been collected occurring on R. ferrumequinum and R. euryale. For the forrner host species, this parasite was found i n 6 roosts, four caves and t w o breeding places in houses, localities No 0006, 0028, 0066, 0272, 0295, and 0297. I t was also collected from R. euryale i n t h r e e caves and one house, No 0004,0006,0056 and 0066. Nycteribia (Listropodia) schmidli Scheiner, 1853 Almost al1 o f thern were collected from M. schreibersi. Three specirnens found occurring o n one R. euryale can n o t be considered as valid data, as this bat was n o t isolated after capture, b u t was i n contact w i t h other Schreiber bats. Thus it can be considered as a casual parasitisrn. M. schreibersii bearing this species were caught i n three temporary roost caves, No 0004, 0028 and 0031. The specimen o f R. euryale was taken i n cave N00066, which is also used as a temporary roost by M. schreibersii.

Genus Basilia Ribeiro, 1903 Basilia nana Theodor & Moscona, 1954 These parasites were collected on M. nattereri i n t w o artificial underground sites, No 0055 and 0073. used as occasional roosts. Basilia nattereri Kolenati, 1857 Collected frorn M. nattereri, this is a new host f o r this batfly i n t h e Biscay locality No 0055.

Genus Penicillidia Kolenati. 1863 Penicillidia d u f o u r i Westwood, 1835 Collected on M. schreibersii, M. myotisand M. emarginatus. The forrner two host species were

Discussion These data confirm t h e presence o f five species and t w o subspecies o f Garnrnasids i n Biscay, o f which one species and one subspecies are recorded for the first time. Arnong thern, Eyndhovenia euryalis is a typical parasite o f horseshoe bats (genus Rhinolophus) i n Europe, i n which three subspecies have been described according t o different rneasurernents f o r different forrns and rnorphological aspects related w i t h t h e idiosoma, dorsal shield, seta, peritrerna, tritosternum, sternal shield, and legs (UCHIKAWA & DUSBABEK, 1978): E. euryalis euryalis, E. euryalis oudemansi, and E. euryalis cornuti. Only the first t w o were found i n this work. Regarding

26

lrnaz et al.

O 5 10 15 Label+---------+----------+--I------.+-----.---+-.---.---

EEO PRH IVE SPL EEE NBI EES

20

+

25

I

AVE

the first, our data agree w i t h previous works (Schreber, 1774), Eptesicus nilssonii (Keyserling stating horseshoe bats are t h e usual host o f et Blasius, 1839), Nyctalus noctula (Schreber, E. euryalis euryalis i n other countries o f Eu1774), Myotis nattereri, Myotis mystacinus rope and t h e lberian peninsula, where it (Kuhl, 1817), Myotis b r a n d t i i (Eversrnann, also occurs o n M. schreibersii (DEUNFF, 1977; 1845) and Myotis daubentonii (Kuhl, 1817) UCHIKAWA & DUSBABEK, 1978; PERIBANEZ-L~PEZ et (DEUNFF,1977; ESTRADA-PENA e t al., 1989; al., 1989). However, E. euryalis oudernansi STANJUKOVICH, 1990). Furthermore, Spinturnix was f o u n d only o n R. ferrurnequinurn. This rnyoti was previously found i n al1 checked also agrees w i t h other authors'data f o r EuMyotis species i n t h e lberian peninsula rope and t h e lberian peninsula (UCHIKAWA& (ESTRADA-PENA et al., 1991). as well as i n genDUSBABEK, 1978; PEREIRA, 1989; ESTRADA-PENA et era Barbastella, Eptesicus, Vespertilio, al., 1991), and it differs considerably frorn Plecotus, Rhinolophus and Pipictrellus i n t h e North African pattern, where E. e. other European areas (DEUNFF,1977; STANJUoudernansi was also reported o n R. mehelyi KOVICH, 1990). Lastly, Spinturnix psi, appears specific for M. schreiberssi, and even indiet al., 1991). a n d R. euryale (ESTRADA-PENA Three species o f genus Spinturnix were v i d u a l ~of R. euryale caught i n t h e same confirmed i n Biscay S. plecotina, S. rnyoti and roosts were free o f it. This agrees w i t h data S. psi, whose presence was unclear f r o m t h e from other authors i n Europe (RUDNICK,1960; bibliography available (ESTRADA-PENA et al., BERON,1971; DEUNFF, 1977; ESTRADA-PENA et al., 1989; ESTRADA-PE~A et al., 1991; CORDERO DEL e t al., 1993), and 1989, 1991; PERIBANEZ-LÓPEZ C A M P I L L al., O ~ ~1994). On the first hand, horsealthough this parasite has been found o n shoe bats are new hosts f o r S. plecotina i n Pipistrellus, Rhinolophus and Myotis bat spet h e lberian peninsula. P. auritus is its rnost cies, these cases were considered occasional usual host i n Europe, although it occurs on contarnination (DEUNFF, 1977). R. ferrurnequinurn, Eptesicus serotinus The last garnrnasid, Paraperiglischrus

Miscel.lania Zoologica 22.2 (1999)

Rf Paur Re Mn

rhinolophinus, which was f o u n d only o n R. ferrumequinum during this work, has been reported showing high specificity as a parasite o f other horseshoe bats (DEUNFF, 1977; ESTRADA-PENA et al., 1989; CORDERO DEL CAMPILLO et al., 1994). Some lack o f observations about this species could happen due t o t h e more inexhaustive examination methods o f lateral and w i n g membranes. lndividuals o f this species, mainly females and nymphs, prefer t o be o n t a i l membranes (DEUNFF& BEAUCOURNU, 1981). Among Ixod ida, lxodes (Escha tocephalus) vespertilionis was reported previously occurring o n R. ferrumequinum and P. auritus i n et al., 1989; CORDERO DEL Biscay (ESTRADA-PENA CAMPILLO et al., 1994), where it does n o t seem t o be an abundant species. R. ferrumequinum has been considered its main host in Europe, b u t it has been detected o n several bat species, showing high infestation level in some cases (ARTHUR, 1963; BEAUCOURNU, 1967; HUTSON, 1971; ESTRADA-PENA et al., 1989; CORDERO DEL CAMPILLO e t al., 1994). Although it had also been considered as a " w i n t e r species" (BEAUCOURNU, 1967) only five individuals were collected f r o m February t o June. No lxodes simples Neumann, 1906, was recorded. This parasite is widespread in Central and Eastern

27

I

Europe o n M. schreibersii b u t is rare in t h e lberian peninsula (ARTHUR, 1956; BEAUCOURNU, 1967; ESTRADA-PENA et al., 1991).Argas (Carios) vespertilionis, recorded f o r t h e first time i n Biscay, is a widely distributed species (Europe, Asia a n d Africa), w h i c h prefers pipistrelle bats b u t can occur on al1 bat species except on horseshoe bats (BEAUCOURNU, 1961; CORDERO DEL CAMPILLO e t al., 1994; DUSBABEK & ROSICKY,1976). I t can also occur o n people i n human buildings when n o bat 1933; HOOSTRAAL, host is present (COLAS-BELCOUR, 1956). Concering batflies, t h e occurrence o f Nycteribia biarticulata o n R. ferrumequinum and R. euryale agrees w i t h data f r o m other countries, where this insect was also reported on other horseshoe bats, b u t mainly on these t w o species (THEODOR& MOSCONA,1954; BALCELLS, 1968; KRISTOFIK,1982; ESTRADA-PENA et al., 1991; CORDERO DEL CAMPILLO et al., 1984). In the same way, the high amount o f Nycteribia schmidli found over M. schreibersii agrees w i t h t h e general view t h a t considers this batfly as a typical constituent o f this bat parasite fauna, even i f occasionally small numbers are found on other species (THEODOR & MOSCONA, 1954; KRISTOFIK, 1982; ESTRADA-PENA et al., 1991).

28 The first record of Basilia nana in Biscay and its occurrence on M. nattereri, agrees with previous knowledge about this parasite in the lberian peninsula, where this bat species is its main host. It has also been recorded occurring on Myotis bechsteini (Bechstein's bat), Myotis dasycneme (pond bat), Myotis blythi (lesser mouse-eared bat), Myotis myotis, Myotis emarginatus(Geoffroy's bat), R. ferrumequinum, P auritus as well as on M. schreibersii (THEODOR & MOSCONA, 1954; HUTSON, 1984). BEAUCOURNU (1961) noted M. bechsteini as its main host in Western France. On the other hand, the occurrence of Basilia nattereritogether with B. nana on the same individual of M. nattereri shows an intermediate position between previous northern and southern records. In fact, M. nattereri is a common host of Basilia nattereri in Central Europe where it also infests other small Myotis bats and E. serotinus but on the lberian peninsula this bat is usually parasited by Basilia nana (ESTRADA-PENA et al., 1991). The last species, Penicillidia dufouri, is recorded first on M. emarginatus in the lberian peninsula. It seems to be a nonspecific parasite, since it was previously recorded mainly on M. myotis and M. blythii, but also on other several species such as M. nattereri, Myotis capaccini, R. mehelyi, R. euryale, R. ferrumequinum, E. serotinus and M. schreibersii (FALCOZ, 1923; BALCELLS, 1968; KRISTOFIK, 1982; ESTRADA-PENA et al., 1991; CORDERO DEL CAMPILLO et al., 1994). It is difficult to draw conclusions concerning the affinities between the parasite species and host species shown in figures 1 and 2 as there is an insufficient quantity of data available for many parasite and host species. In figure 1, the large block formed by the first seven taxa is related to parasites of horseshoe bats (genus Rhinolophus), though Spinturnix plecotina is known as parasite on several bat species, and its occurence in this group can be an artifact (DEUNFF, 1977; ESTRADA-PENA et al., 1989; STANJUKOVICH, 1990). The highest affinity between Eyndhovenia euryalis oudemansi and Paraperiglischrus rhinolophinus reflects that they were recorded only on R. ferrumequinum, but only the former has a high specifity for this host, while the latter is a typical parasite of horseshoe bats (DEUNFF, 1977; ESTRADA-PENA et al., 1989; CORDERO DEL CAMPILLO et al., 1994). The same can be argued for Eyndhovenia euryalis

Imaz et al. euryalis and Nycteribia biarticulata, which following our data can be identified as the parasite group of R. euryale, though they are also found also in other rhinolophids in Europe (THEODOR & MOSCONA, 1954; BALCELLS, 1968; DEUNFF, 1977; UCHIKAWA & DUSBABEK, 1978; KRISTOFIK, 1982; CORDERO DEL CAMPILLO et al., 1984; PERIBANEZ-LOPEZ et al., 1989; ESTRADA-PENA et al., 1991). About the remainder, the only consistent group is formed by Nycteribia schmidli and Spinturnix psi, which are considered as the typical parasite fauna of M. schreibersii (THEODOR & MOSCONA, 1954; KRISTOFIK, 1982; ESTRADA-PENA et al., 1991). The higher affinity of Basilia nana and Basilia nattereri is explained by the scarcity of data. Even if they have only been found on M. nattereri during this work, they are known to occur on several bat species in Europe (THEODOR & MOSCONA, 1954; HUTSON, 1984; BEAUCOURNU, 1961). The same occurs with Spinturnix myoti and Penicillidia dufouri, which are not clearly included in any group. And the last case, Argas vespertilionis, which in this work was found only on Pipistrellus, can also be found on other vespertilionids but it shows preference for this bat genus (BEAUCOURNU, 1961; CORDERO DEL CAMPILLO et al., 1994; DUSBABEK & ROSICKY, 1976). About the affinities between host species, the first group formed by P. pipistrellus and P. kuhlii and the high affinity it shows is a consequence of the ixodid Argas vespertilionis, which has a documented preference for this host genus (BEAUCOURNU, 1961; CORDERO DEL CAMPILLO et al., 1994; DUSBABEK & ROSICKY, 1976). The second group includes M. myotis, M. emarginatus and M. schreibersii, but it could be the consequence of data scarcity, specially about the first two bat species. In fact, the parasite species that can explain this grouping in our data is P. dufouri, and many host species have been recorded for it in previous works. Moreover, despite occasional cases, M. schreibersii has an own parasite fauna, including species such as S. psi and N. schmidli. Thus, we can suppose that more data about ectoparasites of M. myotis and M. emarginatus would change this grouping. The third group, formed by R. ferrumequinum, P. auritus and R. euryale, to be more clear, being a consequence of typical parasites of horseshoe bats such as N. biarticulata, E. euryalis euryalis,

Miscel.lania Zooloqica 22.2 (1999)

a n d S. plecotina, which i s t h e link between rhinolophids and P. auritus. Finally, t h e seclusion o f M. nattereri must be explained i n t h e same way as f o r t h e other Myotis species, as a consequence o f t h e scarcity o f data, and more information is needed bef o r e a clear view about t h e i r a f f i n i t y patt e r n is obtained.

biarticulata, N. schmidli, Basilia nana, B. nattereri observado por primera vez sobre M. nattereri en Bizkaia, y Penicillidia dufouri primera cita en Bizkaia. También se comenta la afinidad entre especies de parásitos dependiendo de las especies de murciélagos que infestan (fig. 1) y la afinidad entre especies de murciélagos dependiendo de las especies de parásitos que soportan (fig. 2).

Acknowledgements References We would like t o thank E. Bernedo, G. Razkin and R. Agirrebeña f o r their help in the surveys. Special thanks t o J. C. Iturrondobeitia, A. l. Caballero and C. Andrés for their teaching and advice on acarology, and t o Dr. A. M. Hutson and Dr. R. L. C. Pilgrim for their help i n obtaining references.

Resumen Ectoparásitos d e q u i r ó p t e r o s en Bizcaya (N península ibérica) Durante u n estudio de distribución de murciélagos se ha desarrollado un estudio sobre ectoparásitos de quirópteros en Bizkaia (N penísula ibérica). Se han examinado 160 hospedadores potenciales hallándose 664 parásitos. Estos fueron recogidos manualmente sobre murciélagos vivos mediante pinzas afiladas, y conservados en acetato de etilo para su posterior análisis microscópico. Una vez recogidas las muestras los murciélagos fueron puestos nuevamente en libertad. Los ectoparásitos recogidos pertenecen a 12 especies y 2 subespecies (tabla 1) (se han excluido de este trabajo los macronisidos e ischnpsillidos recogidos). Entre los gamásidos se han capturado Eyndhovenia euryalis euryalis y Eyndhovenia euryalis oudemansi, los cuales constituyen primeras citas para el área de estudio, Spinturnixplecotina citado por primera vez sobre Rhinolophus ferrumequinum y Rhinolophus euryale en la península Ibérica, y sobre Plecotus auritus en Bizkaia, S. myoti, S. psi y Paraperiglischrus rhinolophinus. Entre los ixódidos se aporta la primera observación de Argas vespertilionis en Bizkaia, y la primera de lxodes vespertilionis sobre Myotis nattereri en la península Ibérica. Por último, entre los nicterébidos se han recogido Nycteribia

ARTHUR,R., 1956. The lxodes Ticks o f Chiroptera (Ixodoidea, Ixodidae). The Journ a l o f Parasitology, 42: 180-184. - 1963. lxodes vespertilionis C. L.. Koch 1844. British Ticks: 135-144. BALCELLS, E., 1968. Nuevas citas de murciélagos y nicteríbidos del País Vasco-Cantábrico, Bol. R. Soc. Española Hist. Nat. (Biol.), 66: 17-38. BEAUCOURNU, J. C., 1961. Ectoparasites des Chiropteres de L'Ouest de la France. la partie: Ixodoides-Cimicides et Nyctéribiidés. Bulletin de la Société Scientifique de Bretagne, 36: 31 5-338. - 1967. Contribution a la connaissance de la biologie d'lxodes (Eschatocephalus) vespertilionis Koch 1844 e t d'lxodes (Pomerantzevella) simplex Neumann 1906 (Acarina, Ixodoidea), parasites des cuiropteres. Annales d e Spéléologie, 22(3): 545-577. BERON,P., 1971. Sur quelques acariens parasites des mammiferes et des reptiles de France. Bull. Soc. Hist. Nat. de Tolouse, 107 (1-2): 96-102. COLAS-BELCOUR, J., 1933. Contribution a I'étude de la biologie de I'Argas vespertilionis Latr. Bull. Soc. Pathol. exot., 26: 937-940. CORDERO DEL CAMPILLO, M., C A S T A ~L.~ ~&~REGUERA, N, A., 1994. Indice-catálogo de Zooparásitos Ibéricos. Secretariado de Publicaciones de la Universidad de Leon, León. DEUNFF, J., 1977. Observations sur les Spinturnicidae de la région palearctique occidentale (Acarina, Mesostigmata) spécifité, r é p a r t i t i o n e t morphologie. Acarologia, 8(4): 602-617. DEUNFF, J. & BEAUCOURNU, J. C., 1981. Phénologie et variations du dermecos chez quelques especes d e Spinturnicidae (Acarina, Mesostigmata). Annales de Parasitologie, 56(2): 203-224.

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