Anopheles (Cellia) ludlowae (Theobald)

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 : 67-68

Anopheles (Cellia) ludlowae (Theobald)

subspecies ludlowae ( Theobald, 1903a) —original combination: Myzomyia ludlowii . Distribution: India, Indonesia, People’s Republic of China, Philippines, Singapore, Sri Lanka, Taiwan, Thailand ( Wilkerson et al. 2021).

subspecies torakala Stoker & Waktoedi Koesoemawinangoen, 1949 —original combination: Anopheles (Myzomyia) ludlowi var. torakala (subspecific status by Harbach & Howard 2007). Distribution: Indonesia (Sulawesi) ( Stoker & Waktoedi Koesoemawinangoen 1949).

Theobald (1903a) described ludlowii (also spelled ludlowi ; emendation to ludlowae by Stone 1957) from a series of six female syntypes from “Luzon, Philippine Islands (Miss Ludlow).” Later authors debated whether ludlowae was a fresh water, blackish water or salt water species. Ludlow (1914) further clarified the type locality: “taken by Dr. Graves in the Province of Abra, Island of Luzon, on the Benguet Road during the construction of that road. The location is definitely inland… there is no sea or blackish water within many miles.”

Nominotypical ludlowae can be recognized in the adult female by the following: Maxillary palpus with three white bands, two apparently at the apices of palpomeres 2 and 3 and third at the apex of palpomere 4 continuing onto palpomere 5; wing with four main dark spots (presector, sector, preapical, apical), with an apical pale spot, an accessory sector pale spot on R 1 (sometimes continuing onto subcosta but not costa), with pale spots and pale fringe at apices of all veins, pale fringe not evident between any of the veins, vein CuA with three dark spots and 1A with two dark spots; legs with distinct speckling, speckles on the hindlegs often extending onto hindtarsomeres 2 and 3, tarsomeres usually banded apically and sometimes basally (specifically described as basal and apical by Theobald 1903a); abdomen without obvious scales; aedeagal leaflets about five or six per side with the longest leaflet somewhat serrate and sinuous ( Russell & Baisas 1936). Characteristics of the larva and pupa of the nominal taxon ludlowae from the Philippines were described by King (1932) and Baisas (1936), respectively, but observations are not available for comparison to subspecies torakala . According to Urbino (1936), the egg of ludlowae does not have floats; the egg of subspecies torakala has not been documented. Subspecies ludlowae is not known as a vector of malarial parasites in the Philippines ( Basio 1971).

Since there are many species with the overall appearance of the adult female of ludlowae , the name was associated with other taxa as a variety or subspecies. There was initial recognition of a “salt water ludlowae ” in the Philippines. King (1932) determined this to be a separate species (currently An. (Cel.) litoralis King, 1932). Bonne-Wepster & Swellengrebel (1953) wrote: “Early writers used the name ludlowi for the common speckled-legged Anopheles species which occurs all over the Sunda Islands, Malaya and the Andamans and which in later years was also found in India, along the coast in brackish and fresh water. Rodenwaldt (1925) noted several important characters in which the species from Indonesia differs from that on the Philippine Islands and described it as ludlowi var. sundaica .” This variety was later elevated to species rank by Christophers (1933). Harrison et al. (1991) reinforced this idea in a rationale for a list of mosquitoes of Thailand and nearby countries: “ Anopheles (Cel.) ludlowae (Theobald) was listed as doubtful and needing further confirmation. Additional confirmation is not necessary. The old records of ‘ ludlowi ’ by Barnes (1923), Barraud and Christophers (1931) and Thurman (1959) were based on misidentified specimens of An. sundaicus (Rodenwaldt) as noted by Scanlon et al. (1968). Anopheles ludlowae is an insular species, not found on mainland Southeast Asia, and should not be included in the Thailand list.”

Harbach & Howard (2007) noted that subspecies torakala was first published in 1938 in Dutch but neither they nor we have been able to obtain a copy of the publication. Therefore: “it is not known whether or not the name was originally introduced in 1938” or at what rank/status. Subspecies torakala is recognized as an important vector of human malarial parasites ( van Hell 1952; Basio 1971). A brief description, with illustrations of the maxillary palpus of both sexes, a wing and a hindleg, was later published in English by Stoker & Waktoedi Koesoemawinangoen (1949) as a variety of ludlowi . The type locality, discussed by Kitzmiller (1982), is in South Sulawesi Province. No type specimens are known. Stoker & Waktoedi Koesoemawinangoen briefly described and illustrated, not only torakala , but also Anopheles (Myzomyia) ludlowi (sensu Walch & Soesilo 1929) and Anopheles (Myzomyia) ludlowi “ typicus ” (= sensu Theobald 1903a, i.e. the nominotypical form). The descriptions are brief and do not provide a differential diagnosis or an explanation about specimens or literature examined, but we surmise the following: torakala does not have an accessory sector pale spot on the subcosta and the accessory sector pale spot on vein R 1 is not demarcated by the additional dark mark between it and the sector pale spot (“ typicus ” has a distinct accessory sector pale spot on the subcosta and R 1, with three pale spots on R 1 below the sector dark); torakala does not have a pale fringe spot between CuA and 1A (“ typicus ” has a continuous pale fringe spot from CuA to 1A); in torakala it is difficult to interpret but it appears that vein R 3 does not end in a pale fringe spot (“ typicus ” has a continuous pale fringe spot between the ends of veins R 3 and R 4+5); torakala has CuA with two dark spots (“ typicus ” has CuA with three dark spots); torakala has three dark spots on the subcosta (“ typicus ” with two dark spots on the subcosta). In addition, judging from the illustrations, we do not see significant differences in banding on the maxillary palpi or the speckling of the legs.

From the above, a likely significant character is the pale fringe between CuA and 1A, the presence of which is used in keys to distinguish Indonesian ludlowae from torakala , which does not have the spot. In contradiction, this fringe spot is not present on the wing of Philippine ludlowae (sensu stricto). Lee et al. (1987) did not distinguish between ludlowae and ludlowae var. torakala in the Australasian Region and combined them in their key, in which they state that there is usually a pale fringe spot between CuA and 1A. Since only the nominotypical form has been characterized in all life stages, no certain comparisons can be made with Indonesian forms, except for one character of the male genitalia. Bonne-Wepster & Swellengrebel (1953) compared the aedeagal leaflets of Philippine ludlowae with the aedeagal leaflets of males from Sulawesi (the Celebes). Their figure 51 shows that the leaflets of Celebes specimens are long and numerous whereas the leaflets of Philippine specimens, as discussed above, have only five or six leaflets on each side, with the longest sinuous or S-shaped.

In summary, because of commonly shared characters in this group of species, we think that the concept of ludlowae from the Philippines has been mixed and confused with what probably is a species complex in Sulawesi, and elsewhere in Indonesia. How to adequately characterize torakala is not possible without further study, especially utilizing molecular methods. Because of noted differences in the transmission of malarial parasites, the presence of pale fringe between CuA and 1A in torakala and differences in the form of aedeagal leaflets, we think these are probably separate species, and therefore elevate torakala to species status: Anopheles (Cellia) torakala Stoker & Waktoedi Koesoemawinangoen, 1949 . Anopheles torakala is currently listed as a species in the Encyclopedia of Life.

Three names (formosaensis, hatorii , cabrerai) are currently in synonymy with ludlowae / torakala . Since those nominal species do not occur in the geographical range of An. torakala , we believe all three are synonyms of An. ludlowae . Anopheles ludlowii var. formosaensis Koidzumi, 1917 was preoccupied and replaced by An. hatorii Koidzumi, 1920 , as explained by Yamada (1925): “ Koidzumi (1917) pointed out, however, the Formosan form differs slightly from ludlowii and placed the former as a variety of the latter, giving it a name, Anopheles ludlowii var. formosensis . After that, Koidzumi (1920) leaned to separate the Formosan form specifically from ludlowii and gave it provisionally another name A. hatorii nov. sp. (?) replacing formosensis preoccupied. But the provisional name was lately made valid by the author (1924). It was, however, placed again as a synonym of ludlowii by Christophers (1924).” Anopheles (Cellia) ludlowae ssp. cabrerai Cagampang-Ramos & Darsie, 1969 (in Darsie & Cagampang-Ramos 1969) was described in comparison with ludlowae as having three dark spots on vein 1A instead of two. The authors ( Darsie & Cagampang-Ramos 1977) later determined that this single character was variable and recognized cabrerai as a synonym of ludlowae .