Ixodes ventalloi Gil Collado, 1936
Estrada-Peña, Agustin, Venzal, José M. & Nava, Santiago, 2018, Redescription, molecular features, and neotype deposition of Rhipicephalus pusillus Gil Collado and Ixodes ventalloi Gil Collado (Acari, Ixodidae), Zootaxa 4442 (2), pp. 262-276: 269-274
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|Ixodes ventalloi Gil Collado, 1936|
Ixodes ventalloi Gil Collado, 1936 . Redescription
Male ( Figure 4 A–F View Figure ). Five specimens measured, collected in a burrow of Oryctolagus cuniculus . Idiosoma elongate-oval ( Fig. 4A View Figure ), with broadly rounded posterior margin, widest at level of spiracular plates. Length from scapular apices to posterior idiosomal margin 3.14–3.23 (3.15), breadth 2.22–2.29 (2.25), ratio of idiosomal length/ width: 1.4–1.5 (1.4). Punctations numerous and shallow centrally and more numerous laterally along marginal groove. Scapulae short, bluntly rounded. Lateral carinae absent. Eyes absent. Cervical grooves marked, as two divergent lines. Conscutal setae numerous, long 0.20–0.26 (0.25), white. Male with variable number of rows of conscutal setae at lateral margins of body, with most specimens having two rows. Venter ( Fig. 4B View Figure ). Length and breadth of each ventral plate: pregenital 0.39–0.42 (0.37) x 0.11–0.15 (0.13) (ratio, 2.79–2.85, mean: 2.84), median 1.33–1.41 (1.37) x 1.11–1.15 (1.13) (ratio, 1.20–1.22, mean: 1.20), adanal 0.53–0.58 (0.56) x 0.26–0.28 (0.26) (ratio: 2.15), anal 0.35–0.37 (0.35) x 0.31–0.37 (0.33) (ratio: 1.06). Genital aperture at level of coxae III. Spiracular plate ( Fig. 4C View Figure ) broadly oval, 0.42 long, 0.38 wide (ratio length/width: 1.1) with goblets in four concentric rows and one additional row of punctations around margin of plate.
Gnathosoma dorsally ( Fig. 4D View Figure ), length from palpal apices to posterior margin of basis 0.42–0.52 (0.45). Basis capituli 0.24–0.27 (0.25) long, 0.32–0.39 (0.37) broad, ratio length/width: 0.67, posterior margin essentially straight, external margins diverging anteriorly; cornua present but small, triangular, slightly diverging laterally. Ventral outline of gnathosoma as illustrated ( Fig. 4E View Figure ) with small and laterally projected auriculae and central projection produced posteriorly. Palpi length 0.31–0.34 (0.32), breadth 0.14–0.16 (0.15), ratio length/width of palpi: 2.13. Setae as illustrated, with several long setae on dorsal surface of palpal article II. Hypostome ( Fig. 4F View Figure ) 0.15–0.19 (0.16) long, 0.12–0.14 (0.13) broad (ratio length/width 1.23), with a dental formula of 4/ 4 in most rows, with 6–8 hypostomal teeth, with irregular rows of median very small crenulations to base, lateral denticles larger and more angular than those in internal rows, basal lateral denticles lobate rather than angular.
Legs moderately long. Coxa I ( Fig. 4G View Figure ) with one long internal and one short external spur. Internal spur on coxa I almost straight reaching over as much as half of coxa II. Coxa II with short external and internal spurs. Coxa III with external and internal spur of subequal length. Coxa IV with small external chitinous ridge, not visible in all specimens.
Female ( Fig. 4 View Figure , H–N). Eight specimens measured. Length from scapular apices to posterior idiosomal margin 4.21–4.91 (4.68), breadth 2.94–3.01 (2.97), ratio idiosomal length/width 1.57. Scutum ( Fig. 4H View Figure ) outline broadly rounded, 2.99–3.57 (3.49) long, 2.72–2.99 (2.81) broad, ratio length/width scutum: 1.19–1.23 (1.24). Cervical grooves distinct, appearing as almost parallel or slightly divergent posteriorly integumental depressions, indicated by more dense punctations. Punctations scattered and more abundant, smaller and deeper in periphery of scutum. Setae abundant, very long, same size as other idiosomal setae, randomly distributed, more abundant as longitudinal rows in central portion of scutum, less numerous on lateral regions. Marginal grooves distinct. Alloscutum with abundant long setae. Setae placed on posterior margin of alloscutum are easily seen from ventral view of specimens. Ventral surface as illustrated ( Fig. 4I View Figure ). Genital aperture at level of coxae IV ( Fig. 4I View Figure ). Spiracular plate ( Fig. 4J View Figure ) sub-circular, 0.39 long, 0.40 wide (ratio length/width: 0.92).
Gnathosoma: Dorsally, length from palpal apices to posterior margin of basis 0.43–0.49 (0.45). Basis capituli dorsally ( Fig. 4K View Figure ) 0.12–0.15 (0.13) broad; ratio gnathosomal length to basis capituli width 3.2–3.5 (3.4). Posterior margin of basis capituli dorsally broadly concave, cornua small. Porose areas irregularly ovoid, anterior margin broadly rounded, posterior margin essentially straight and well delineated, separated by distance slightly larger than breadth of each area. Pores in porose areas irregularly placed. Basis capituli ventrally ( Fig. 4L View Figure ) with posterior margin straight; transverse suture unapparent. Auriculae very large, hook like, internally curved, almost half length of ventral basis capituli. Palpi 0.33–0.39 (0.35) long, 0.05 broad (ratio length/width palpi: 2.33). Hypostome ( Fig. 4M View Figure ) 0.33–0.38 (0.35) long, 0.08 broad, ratio length/width: 4.3. Apex bluntly pointed, corona with few fine denticles, dental formula 3/3 for anterior half, then 2/2 for basal half of hypostome, with 5–11 rows of hypostomal teeth. Medial basal teeth smaller, all denticles sharply pointed.
Legs moderately long, slender, coxae I–IV ( Fig. 4N View Figure ) each with small external spur, that of coxa II longest. Coxa I with long, essentially straight, pointed internal spur, slightly reaching the half of the coxa II. An internal chitinized ring in coxa II. Internal spur or traces of chitinized rings absent on coxae III and IV. Trochanters without spurs.
Nymph ( Figure 5 View Figure , A–F). Eighteen specimens measured. Idiosoma. Dorsally ( Fig. 5A View Figure ) length from scapular apices to posterior idiosomal margin 0.70–0.79 (0.73), width 0.43–0.49 (0.45), ratio length/width 1.62. Scutum broadly pyriform, longer than broad, length 0.57–0.62 (0.59), width 0.54–0.56 (0.55), ratio length/width 1.07; scapulae short, rounded; cervical grooves smooth, widely divergent; lateral carinae slightly visible. Length of median scutal setae: 0.03–0.04 (0.04), length of median alloscutal setae 0.21–0.25 (0.24), length of lateral alloscutal setae 0.12–0.16 (0.14). Alloscutal setae around 5 times longer than median scutal setae. Ventral view as illustrated ( Fig. 5B View Figure ). Anal groove slightly converging posteriorly. Spiracular plates widely rounded, length 0.14–0.17 (0.16), width 0.11–0.12 (0.12), ratio length/width of the spiracular plate: 1.33.
Gnathosoma. Total length (dorsal view) from palpal apices to base of gnathosoma 0.42–0.49 (0.48). Basis capituli triangular ( Fig. 5C View Figure ), width (measured dorsally) 0.29–0.32 (0.31). Ratio gnathosoma length to basis capituli width 1.58. Posterior margin of basis capituli straight; cornua small, narrow, posterolaterally produced, sharply pointed. Lateral margins of base of gnathosoma ventrally convergent from palpal insertions to auriculae ( Fig. 5D View Figure ), then deeply concave, then slightly diverging to posterior margin. Auriculae poorly defined, blunt. Palpi long and internally excavated, combined length 0.33–0.34 (0.33); palpal article I length 0.061; palpal article II length 0.15–0.16 (0.16); palpal article III length 0.13–0.14 (0.13). Combined palpal maximum width 0.15–0.16 (0.15). Article II slightly longer than III. Hypostome ( Fig. 5E View Figure ) length 0.25–0.29 (0.28), width 0.085, (ratio length/width 3.3) with blunt apex; dental formula essentially 3/3 at anterior half of its length, then 2/2 to base, with all denticles sharply pointed.
Legs ( Fig. 5F View Figure ) moderately long. Coxa I with external spur, short and straight, and with wider, sharply pointed, straight internal spur reaching coxa II. Internal spur about twice length of external spur. External spurs of coxae subequal in size, external spur on coxa IV slightly smaller. No spurs on trochanters. Haller’s organ with 6 prehalleral setae plus 6 apparent setae in capsule.
Larva ( Figure 5 View Figure , G–L). All larvae were obtained from eggs laid by two engorged females. Measurements are based on 14 specimens. Because of the very small variability in setal measurements, well below the fourth decimal figure, we refer only to the average of these measurements. Idiosoma. Dorsal surface oval ( Fig. 5G View Figure ). Sensilla sagittiformia (large wax gland) absent. Scutum broadly rounded, clearly wider than long, length 0.52–0.58 (0.56), width 0.41–0.45 (0.44), ratio length/width: 1.23–1.28 (1.27); integument with irregular hexagonal ornamentation, punctations sparse; eyes absent. Scutal setae: 5 pairs (Sc1–Sc5), measuring 0.017, 0.017, 0.017, 0.019, and 0.014, respectively. Alloscutal setae: 12 pairs. Four pairs of central dorsal setae (Cd1: 0.035, Cd2: 0.031, Cd3: 0.04, Cd4: 0.04), 7 pairs of marginal dorsal setae (Md1: 0.09, Md2: 0.092, Md3: 0.091, Md4: 0.053, Md5: 0.053, Md6: 0.039; Md7: 0.032) and 1 pair of supplementary setae (S: 0.046). Ventral surface ( Fig. 5H View Figure ) with 13 pairs of setae plus 1 pair on anal valves, i.e. 3 sternal setae (St1: 0.03, St2: 0.025, St3: 0.027), with St1 located below level of coxae I, St2 below of coxae II and St3 between coxae III, 2 pre-anal pairs (Pa1: 0.031, Pa2: 0.03), 4 premarginal pairs (Pm1: 0.03, Pm2: 0.021, Pm3: 0.026, Pm4: 0.029), and 4 marginal ventral pairs (Mv1: 0.029, Mv2: 0.03, Mv3: 0.025, Mv4: 0.029). Anal groove divergent ( Fig. 5H View Figure ).
Gnathosoma. Basis capituli ( Fig. 6I View Figure ) triangular, with posterior margin essentially straight and cornua absent, length 0.21–0.24 (0.22), width 0.15 (measured dorsally). Ratio length/width 1.4. Palpi length 0.10–0.13 (0.11), width 0.04, ratio length/width: 2.7) not internally excavated, suture between article II and III inconspicuous, Ventral basis ( Fig. 5J View Figure ) with 2 pairs of posthypostomal setae (Ph1–Ph2), distance between Ph1 0.04 and Ph2 0.03; posterior margin of ventral part of gnathosoma sinuous; auriculae long, acute, projected laterally; hypostome ( Fig. 5K View Figure ) total length from apex to Ph1 setae 0.09, width 0.040 (ratio length/width: 2.25), with rounded apex; dental formula 3/3 to mid-length, then 2/2 to base, with all denticles sharply pointed, 9/10 denticles in row I, 9 in row 2 and 6 in row 3. Palpal setae: 7 on genu, i.e. 1 paraxial (Gp1), 2 antiaxial (Ga1–Ga2), 3 dorsal (Gd1–Gd3) and 1 ventral (Gv1); 6 on femur, i.e. 1 paraxial (Fp1), 2 antiaxial (Fa1–Fa2), 1 dorsal (Fd1) and 2 ventral (Fv1–Fv2); 10 on tibiotarsus (Ttt1–Ttt10); trochanter 0.
Legs. Coxa I with 2 triangular spurs; internal longer ( Fig. 5L View Figure ). Coxa II with single external spur, shorter than homologous spur of coxa I. Coxa III with chitinous ridge. Coxa I with 3 setae, 1 anterior (CIa), 1 posterior (CIp) and 1 paraxial (CIpa); coxae II and III each with 2 anterior setae and 1 posterior seta; trochanters without spurs. Tarsus I length 0.21, width 0.07. Setae on tarsus I: group I absent; 4 setae in group II–2 dorsal (dII1, dII2), 1 lateral antiaxial (laII1) and 1 lateral paraxial (lpII1); 4 dorsal in group III (dIII1–4); groups IV and V dorsal setae absent; 2 dorsal in group VI (dVI1–2). Ventral and lateral setae: 4 setae in group I – 2 ventral (VvI1–2); 2 lateral antiaxial (laI1) and lateral paraxial (lpI1); 4 setae in group II – 2 ventral (VvII1–2); 1 lateral antiaxial (laII2) and 1 lateral paraxial (lpII2); 4 setae in group III – 2 ventral (VvIII1–2); 2 lateral antiaxial (laIII1) and lateral paraxial (lpIII1). Haller’s organ with 5 prehalleral setae (phs) plus 3 apparent setae in capsule.
Specimens examined. According to Santos Dias (1985) and Guglielmone et al. (2014) the types of I. ventalloi were deposited in the collection of the Museo de Ciencias Naturales (Barcelona, Spain). However, a search of the type collection in the museum yielded negative results (Gloria Masò, curator of Arthropods Collection, pers. comm.) therefore precluding further comparison with other collections. We therefore proceed to the naming and deposition of a neotype. The neotype specimen is a female, collected in a burrow of Oryctolagus cuniculus in Zuera , 41°88’N, 0.75°W, Zaragoza (Spain) by J.J. Osácar in April, 1991, about 350 km from the original type locality (the host of the original type was also O. cuniculus ). The female neotype is deposited in the U.S. National Tick Collection under the accession number USNMENT00862203. The rest of the specimens of this collection, including 18 females, 12 males, 14 nymphs and 114 larvae (the progeny of one engorged female collected on one rabbit in the same burrow) were used to complete the redescription and the illustrations, and obtain additional measurements. These specimens are deposited in the collection of the Faculty of Veterinary Medicine of Zaragoza (Spain) with the accession number FMV1109. Further specimens, including 2 females and 81 nymphs were obtained from the surroundings of Palermo, 38°11’N, 13.36’E (Sicily, Italy) to check for coherence of the morphological details. These specimens are deposited in the collection of the Faculty of Veterinary Medicine of Zaragoza (Spain) with the accession number FMV1317.
Molecular features. As expected, the 16S rDNA sequence of I. ventalloi from Spain (Genbank accession number: KY231931) are grouped with those of I. ventalloi from Italy ( Fig. 6 View Figure ). The 16S rDNA sequence from Spain is closest to genogroup A from Italy (haplotypes 1 and 2) described by Latrofa et al. (2016). The 16S sequences of Latrofa et al. (2016) available in Genbank (KU178956 - KU178963) are 275-bp in length. For that reason, although we obtained a 16S sequence of 410-bp for I. ventalloi , the alignment used in this phylogenetic analysis consisted of 275 bp fragments. Ixodes ventalloi clustered near other species of the I. ricinus group, but seems to be unrelated to these species and in a different clade, which is in concordance with the morphological features described above.
Hosts and zoogeography. Ixodes ventalloi is a Palearctic species found in southwest Iberian Mediterranean sclerophyllous and mixed forests, northwest Iberian montane forests, and Iberian conifer forests ( Guglielmone et al., 2014). It is found in Northern Africa, the Iberian Peninsula, southern France, Cyprus, southern Italy, Portugal, and Spain ( Chastel et al., 1984; Estrada-Peña et al., 1984; Santos Dias and Santos Reis, 1989; Santos Silva et al., 2011; Ioannou et al., 2009; Mori et al., 2015; Latrofa et al., 2016) and introduced into Germany ( Petney et al., 1996) and the United Kingdom ( Arthur, 1957, as I. festai Tonelli-Rondelli, 1926 ; Jameson and Medlock, 2011). No additional surveys have been carried out in the last two regions to conclude if they have permanent populations in sites outside of the main distribution range. All developmental stages of I. ventalloi have been found on lagomorphs, carnivores and rodents. This species can also be collected on different carnivores such as weasel ( Mustela nivalis ), Iberian lynx (Lynx pardinus), red fox ( Vulpes vulpes ), cats, and Egyptian mongoose ( Herpestes ichneumon ) (Santos Dias & Santos Reis, 1989; Petney et al., 1996; Millán et al., 2007), and on birds such as the red-legged partridge ( Alectoris rufa ) and chukar partridge ( Alectoris chukar ) ( Estrada-Peña et al. 1984; Ioannou et al. 2009). It has also been found on the crested porcupine (Hystrix cristata) ( Mori et al. 2015), hedgehogs ( Erinaceus europaeus ) ( Domínguez, 2014) and humans ( Gilot and Marjolet, 1982). It is however problematic to ascertain the validity of some of these records, because of the diagnostic uncertainty of I. ventalloi , I. ricinus and I. festai ( Gilot and Pérez, 1978) and the impossibility to find and recheck these published records. Ixodes ventalloi could be thus considered a species whose distribution overlaps the original distribution of the European rabbit, including the Iberian Peninsula, southern France and Italy, including the island of Sicily.
Diagnosis and species relationships. A small sized Ixodes . The female is characterized by: elliptical porose areas with irregular disposition of the pores, and relatively superficial and small alloscutal punctations, mainly concentrated in the lateral parts of the scutum; scutal and alloscutal setae long and approximately of similar length; internal spur on coxa I straight and barely reaches over half of coxa II; apparent external spurs on coxae I to IV; marginal groove evident; and dental formula 3/3+2/2. The distinctive feature of the female is the long and curved auriculae, which are absent in every other species of Ixodes reported in the Western Palearctic. The original illustration by Gil Collado (1936), shows the ventral view of an engorged female with a curved internal spur on coxa I, which does not reach coxa II (probably because engorgement of the female distorted the proportions). The male is characterized by its relatively long conscutal setae and the presence of deep and distinct cervical fields, which have a few setae. The nymph is characterized by: presence of a broadly pyriform scutum; lateral carinae slightly apparent; cornua small, almost inapparent; hypostome with blunt apex, presenting dental formula 3/3 at more than half of hypostomal length, then 2/2 to base, all denticles sharply pointed; anal groove slightly converging posteriorly; alloscutal setae abundant, long, and about 6 times longer than those on scutum; and internal spur of coxa I reaching coxa II. The larva has: scutum posteriorly rounded; Md1-Md3 setae the same size as the other setae, which are only slightly longer than scutal setae; cornua present; auriculae long; hypostome with apex clearly rounded with dental formula 3/3 to mid-length, then 2/2 to base; and anal groove clearly divergent. In addition to this unique morphology, the molecular features clearly separate I. ventalloi from the remaining tick species of the I. ricinus group. The morphological features of the specimens collected with the neotype do not differ significantly from the details provided by Latrofa et al. (2016) except in the internal spur of coxa I of the female, which is only slightly curved in all the females examined for this redescription.
Considerable confusion exists regarding the identity of I. ventalloi , I. ricinus (Linnaeus, 1758) , I. festai , the recently described I. inopinatus Estrada-Peña, Nava & Petney, 2016 , I. acuminatus Neumann, 1901 , and I. bivari Santos-Dias, 1990 . Santos Silva et al. (2011) expressed reservation about the validity of the latter species. Few details are known for I. festai . This species was described from engorged females collected from several localities in northern Africa on ground-feeding birds. Most of the confusion arose with the illustrations and short redescription of the species by Colas-Belcour and Rageau (1951). The confusion was reinforced by the descriptions by Hoogstraal (1959) without illustrations, and Arthur (1957, 1958, 1961). The texts and illustrations of these studies refer without question to I. ventalloi . Illustrations of I. festai and I. ventalloi in Cringoli et al. (2005) represent I. ventalloi . The type specimen of I. festai is an engorged female, therefore having distorted body proportions, which lacks many critical structures such as the hypostome and parts of the capitulum. The female of I. festai was separated from I. ventalloi by Gilot and Pérez (1978) based on the shape and relative length of the auriculae, but no clear details are provided for other critical features and no comparison with types was provided. The male of I. festai was briefly described by Pérez (2007) and redescribed by Contini et al. (2011). Both descriptions lack important details. However, from the illustrations in these reports the male shows several details that are similar to the male of I. ventalloi , as redescribed in this study.
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