Culex (Oculeomyia) annulioris Theobald, 1901

Harbach, Ralph E. & Wilkerson, Richard C., 2023, The insupportable validity of mosquito subspecies (Diptera: Culicidae) and their exclusion from culicid classification, Zootaxa 5303 (1), pp. 1-184 : 103-105

Culex (Oculeomyia) annulioris Theobald

subspecies annulioris Theobald, 1901a —original combination: Culex annulioris . Distribution: Angola, Benin, Burkina Faso, Cameroon, Central African Republic, Côte d’Ivoire, Democratic Republic of the Congo, Ethiopia, Ghana, Guinea, Kenya, Liberia, Madagascar, Malawi, Mali, Nigeria, Republic of the Congo, São Tomé and Príncipe, Senegal, Seychelles, South Africa, South Sudan, Sudan, Tanzania, Uganda, Zimbabwe ( Wilkerson et al. 2021).

subspecies consimilis Newstead, 1907 (in Newstead et al. 1907)—original combination: Culex tigripes var. consimilis (subspecific status by Edwards 1941). Distribution: Cameroon, Democratic Republic of the Congo, Gabon, Ghana, Kenya, Liberia, Mozambique, Nigeria, Sierra Leone, South Sudan ( Lewis 1956, but not Sudan, see Simsaa et al. 2021), Tanzania, Uganda ( Wilkerson et al. 2021).

Culex annulioris was described from a single female collected in Salisbury, Southern Rhodesia (present-day Harare, Zimbabwe), “distinguished by the abdominal ornamentation, which is very marked and peculiar”, “each segment with a triangular basal patch of creamy yellow scales, and with apical lateral patches of yellow scales” ( Theobald 1901a).

Subspecies consimilis , originally proposed as a variety of Lutzia tigripes (de Grandpré & de Charmoy, 1901) and subsequently recognized as a subspecies of annulioris by Edwards (1941), was described from females collected at several localities in the Belgium Congo (present-day Democratic Republic of the Congo). The abdomen of the female was described by Newstead (in Newstead et al. 1907) as having “narrow basal bands; basal segment with two median black apical spots; sixth and seventh segments with two lateral apical pale spots.” As pointed out in a footnote, Edwards (1941) observed that “in the lectotype the slight appearance of banding is merely due to the pale marginal hairs [setae] and not to pale scales.” He also noted that “only small apical lateral spots, if any…” were present on segments VI and VII. Oddly, except for Edwards, there is no mention of a lectotype of consimilis in the catalogs of Stone et al. (1959), Knight & Stone (1977) and Wilkerson et al. (2021); however, Townson (1990) indicated the presence of two syntype females in the British Museum (Natural History) (now the Natural History Museum, London), one from Kasongo, Zaire (present day Democratic Republic of the Congo) and the other one with no locality. As confirmation of the lectotype, Hamon & Ovazza (1956) stated that consimilis was “described from a female from Kasongo, Belgium Congo,” which “differs from the type form by: the absence of basal pale markings on the terga 1–7, the apicolateral pale triangular spots being reduced and not appearing clearly as on segments 6 and 7” (translated from the French).

Edwards (1911b) treated consimilis as a species of Culex , distinct from Cx. annulioris , and recognized Cx. pseudoannulioris Theobald, 1909 , described from three females captured at Obuasi, Gold Coast (present-day Ghana), as its junior synonym. Theobald recognized pseudoannulioris as “A very pronounced, banded proboscis species, coming near C. annulioris, Theobald ”, differing in having the “Abdomen unbanded, deep blackish brown with lateral creamy scales, which to some extent form apical spots above”. In addition to pseudoannulioris, Edwards (1941) recognized Cx. annulioris var. congolensis Evans, 1923 and Cx. bitaeniorhynchus var. mayumbae Galliard, 1931 as synonyms of subspecies consimilis . The former was described from two males collected at Leopoldville, Belgian Congo (present-day Kinshasa, Democratic Republic of the Congo), characterized as having the “ abdomen entirely dark scaled above [sic], the median basal and lateral apical white markings characteristic of annulioris being entirely absent.” The variety mayumbae was based on features of the phallosome of males reared from larvae collected in Tchibanga and Mouila, Gabon.

Two other nominal forms, Cx. annulioris var. gambiensis Theobald, 1903b and Cx. annulioris var. major Edwards, 1935 , are presently considered to be junior synonyms. The former, listed as a synonym of the type form by Edwards (1932a), was described from a single female reared from a larva collected at [Bathurst, renamed Banjul in 1973], Gambia as having the abdomen “like the type, but the triangular basal white spots are very indistinct, but can be detected on each segment by a few white scales”. The variety major , subsequently raised to subspecific rank by Edwards (1941) and synonymized with subspecies consimilis by Hamon & Ovazza (1956), was described from a series of specimens, including the type male, from Nairobi, Kenya, which differed from the type form in being larger and having “abdominal tergites [terga] with distinct basal pale bands which are somewhat widened in the middle; apical lateral pale spots very small or even absent.” Although Edwards (1935) mentioned that the male genitalia of major were not obviously different from those of the typical form, he later ( Edwards 1941) noted that the phallosome differed “slightly from both the typical form and from ssp. consimilis .” Actually, the lateral plate of major is more than slightly different than those of the type form and subspecies consimilis (see below). In addition to the specimens from Nairobi, Edwards also identified specimens of major from localities in the Democratic Republic of the Congo (as the Belgian Congo) and Uganda.

Based on the examination of type material and specimens from Benin (as Dahomey), Cameroon, Côte d’Ivoire, Ethiopia, Kenya, Republic of Upper Volta (as Haute-Volta) and Senegal, Hamon & Ovazza (1956) concluded “that [in] Culex annulioris there are very many variations in colouring which do not correspond at all to variations in the structure of the phallosome, the same structure of the phallosome being able according to the regions to correspond to very dark forms or to very pale forms. The systematic value of the types of C. annulioris and C. annulioris consimilis is therefore almost zero since they are females. For the sake of simplicity, we propose to continue to call C. annulioris sensu stricto the specimens with smooth phallosome [i.e. lateral plate, see below] and C. annulioris var. consimilis those with phallosome bearing numerous and long spicules. Although an almost pure population is generally observed at a given point, there are some forms of passage between the two types of phallosome; given the variations recorded here both in the exterior colouring and in the structure of the phallosome, it does not seem appropriate to continue to regard C. annulioris major as a different variety from C. annulioris consimilis and we propose to treat it as a synonym [translated from the French].”

Cutting to the chase, we find that the conclusions reached by Hamon & Ovazza (1956) are not convincing because they are based on presumed probability that features of the lateral plates of the male genitalia are not correlated with observed differences in the ornamentation of the adult females, principally the absence or presence and development of pale scaling on the abdominal terga. For the most part, neither the quantity nor quality of material available for study was adequate for resolving the taxonomy of the nominal forms. The study of Hamon & Ovazza was based entirely on adult mosquitoes, and characteristics of the immature stages were not considered. Indeed, the larval and pupal stages for all of the nominal forms are unknown, except the type form, which has not been definitely associated with topotypic material. As communicated by Macfie & Ingram (1923), “The larva of this mosquito [ Cx. annulioris ] has been figured by Edwards [1912d] … and included in his key to the larvae of African CULICIDAE ; it is therefore unnecessary for us to do more than mention a few additional characters.” As usual, Edwards only illustrated the head (dorsal view) and abdominal segments VIII and X (lateral view). Macfie & Ingram also provided a description of the pupa, based on a single exuviae, and an illustration of the trumpet. The descriptions were based on specimens found in pools at Accra, Ghana. The authors did not indicate how the specimens were identified to species, but they were presumably associated with reared adults that were identifiable as the type form of Cx. annulioris . Hopkins (1936, 1952) also described and illustrated the head and terminal abdominal segments of the annulioris larva, with notable differences from the illustrations of Edwards (1912d): Antenna slightly curved and slightly more slender distal to seta 1A, with more numerous branches; comb with fewer large spine-like scales; siphon shorter (index about 6.0 as opposed to about 8.4); pecten short, on approximately the basal 0.06 of the siphon (on approximately the basal 0.15 of the siphon illustrated by Edwards).

With regard to the male genitalia, it is disappointing that attention has only been given to the structure of the lateral plate of the phallosome, which, in the case of the nominal taxa considered here, has been referred to inaccurately as the “hypopygium” ( Galliard 1931; Edwards 1935), “mesosome” ( Galliard 1931) and “phallosome” ( Edwards 1941; Hamon & Ovazza 1956). Jupp (1996) correctly referred to it, for the most part, as the “lateral plate of phallosome”. More specifically, distinctions between the nominal forms for which the male genitalia are known (i.e. annulioris , consimilis and major ) have focused on the curved ventrocaudal surface of the inner division of the lateral plate (the “posterior margin of the inner division” of Edwards 1941). In the type form, that surface of the inner division bears numerous very minute spicules (characterized as “smooth” by Hamon & Ovazza 1956) whereas in consimilis and major it bears many semi-recumbent thorn-like projections. However, the lateral plate is a complicated structure that exhibits differences in the shape and development of the dorsocaudal angle and its dorsally projecting recurved teeth, differences which seem to have been overlooked but are readily apparent in the illustrations provided by Galliard (1931), Edwards (1941), Hamon & Ovazza (1956) and Jupp (1996). Although the lateral plates of consimilis and major both have thorn-like projections on the ventrocaudal surface, the contour and development of the surface between the projections and the dorsally projecting teeth is very different, as shown in figures 101f ( major ) and 101g ( consimilis ) of Edwards (1941). As illustrated by Edwards, and also Hamon & Ovazza (1956), in consimilis the region of the plate bearing the thorn-like projects is more or less evenly rounded and a distinct group of small dorsally directed denticles is present at the base of the recurved teeth whereas in major the region bearing the thorn-like processes is more angular and there are no denticles at the base of the recurved teeth. Surprisingly, none of the illustrations of the lateral plates which Hamon & Ovazza illustrated as those of consimilis are similar to the lateral plate of major illustrated by Edwards. We anticipate that other differences in structures of the male genitalia, e.g. the development of the subapical lobe of the gonocoxite and its specialized setae, will be found that further indicate the existence of a number of closely related species.

In addition to overlooking information about larvae and pupae, Hamon & Ovazza (1956) also failed to consider the descriptions and illustrations of structures of the female genitalia of annulioris and consimilis (as separate species) provided by Macfie & Ingram (1922). Differences were noted as follows: In annulioris , the postgenital lobe (their tenth segment) bears four or five small setae on each side of the ventral surface and the posterior margin is emarginate; the spermathecal capsules are “sub-equal, oval; length 99 μ, breadth 68 μ, the chitinised portion of the ducts very short, about 2 μ.” In contrast, the postgenital lobe of consimilis “bears about nine small setae on each side on its ventral aspect” and the posterior margin is not emarginate; the spermathecal capsules are larger, “the middle one measured 137 μ in length by 84 μ in breadth, and the chitinised portion of its duct was about 7 μ long, and in the other two spermathecae the corresponding measurements were 129 μ, 80 μ, and 4μ respectively.” The authors did not mention how the specimens were identified to species or where they were collected, but the observed differences clearly indicate potential specific distinctions.

A look at the collection records for the type form and subspecies consimilis and major reveals that the three forms occur in sympatry throughout central (sub-Saharan) and eastern Africa. It is interesting to note that the type localities of all nominal forms currently regarded as junior synonyms are in countries of central and western Africa, far north of the type locality of annulioris sensu stricto in Zimbabwe. It is particularly interesting to note that the type locality of gambiensis, the sole synonym of the type form, is located more than 6,500 km (by land) from Zimbabwe. Considering the ecological and topographical differences over the very wide distribution of Cx. annulioris sensu lato, it is surprising that Hamon & Ovazza found no correlation of the marked variation in the coloration of the adults with geographical distribution. This is very puzzling because such variation is often suggestive of a species complex.

Whereas Hamon & Ovazza (1956) interpreted Cx. annulioris as an extremely variable species, we believe that the available morphological and distributional data provide evidence of a species complex. In the absence of a comprehensive study of topotypic material, the nominal forms remain poorly and inadequately known, particularly because the immature stages have never been used to help define them—the complete larval and pupal chaetotaxy has not been studied even for the two currently recognized subspecies. As in the case of several species of the Vishnui Subgroup of the subgenus Culex , whose lateral plates are very similar to those of Cx. annulioris and which exhibit marked similarities in the adult stage (see Colless 1957 and Sirivanakarn 1976), we anticipate that larvae of reared specimens collected in the type localities are likely to show that annulioris , consimilis and major are clearly differentiated species.

In addition to morphology, bionomical and molecular data are needed to resolve the composition of the Annulioris Complex. For the time being, we believe it is prudent to recognize the following nominal taxa as separate species of the complex: Culex (Oculeomyia) annulioris Theobald, 1901a , Culex (Oculeomyia) consimilis Newstead, 1907 and Culex (Oculeomyia) major Edwards, 1935 . Culex consimilis and Cx. major need to be added to the list of Culex species recognized in the Encyclopedia of Life. The following nominal forms are provisionally retained as junior synonyms: Cx. annulioris var. gambiensis Theobald, 1903b (synonym of Cx. annulioris Theobald, 1901a ); Cx. pseudoannulioris Theobald, 1909 , Cx. annulioris var. congolensis Evans, 1923 and Cx. bitaeniorhynchus var. mayumbae Galliard, 1931 (synonyms of Cx. consimilis Newstead, 1907 ).