Identification key to the Anopheles mosquitoes of South America (Diptera: Culicidae). III. Male genitalia

Abstract

Background: Accurate identification of the species of Anopheles Meigen, 1818 requires careful examination of all life stages. However, morphological characters, especially those of the females and fourth-instar larvae, show some degree of polymorphism and overlap among members of species complexes, and sometimes even within progenies. Characters of the male genitalia are structural and allow accurate identification of the majority of species, excluding only those in the Albitarsis Complex. In this key, based on the morphology of the male genitalia, traditionally used important characters are exploited together with additional characters that allow robust identification of male Anopheles mosquitoes in South America.

Methods: Morphological characters of the male genitalia of South American species of the genus Anopheles were examined and employed to construct a comprehensive, illustrated identification key. For those species for which specimens were not available, illustrations were based on published illustrations. Photographs of key characters of the genitalia were obtained using a digital Canon Eos T3i attached to a light Diaplan Leitz microscope. The program Helicon Focus was used to build single in-focus images by stacking multiple images of the same structure.

Results: An illustrated key to South American species of Anopheles based on the morphology of the male genitalia is presented, together with a glossary of morphological terms. The male genitalia of type-specimens of previously poorly documented species were also examined and included in the key, e.g. Anopheles (Anopheles) tibiamaculatus (Neiva, 1906) which has a unique quadrangular-shaped aedeagus with an apical opening.

Conclusions: Male genitalia of South American species of Anopheles possess robust characters that can be exploited for accurate species identification. Distortion that can occur during the dissection and mounting process can obstruct accurate identification; this is most evident with inadvertent damage or destruction of unique features and interferes with correctly assigning shapes of the features of the ventral claspette. In some species, the shape, and anatomical details of the aedeagus also need to be examined for species identification. For members of the Myzorhynchella Series, both ventral and dorsal claspettes possess multiple characteristics that are herein used as reliable characters for species identification.

Keywords: Anopheles; Illustrated key; Male genitalia; Morphology; South America.

Fig. 1

Schematic drawing of the male genitalia of An. pseudopunctipennis Theobald, 1901. The proctiger (anal lobe) was removed to permit an unobstructed view of the ventral structures (redrawn after Komp [7])

Fig. 2

Dorsal view of the male genitalia of An. albimanus Wiedemann. Segment IX and the proctiger (anal lobe) were removed to facilitate the observation of structures that occupy the ventral position

Fig. 3

Gonocoxites showing the accessory setae, internal seta and parabasal setae of species of the subgenera Nyssorhynchus (a), Anopheles (b), Stethomyia (c). b and c redrawn after Komp [7]

Fig. 4

Ventral and dorsal lobe claspettes of the male of An. neomaculipalpus Curry, 1931(redrawn after Komp [7])

Fig. 5

Ventral claspette of An. strodei Root, 1926 (redrawn after Faran & Linthicum [10])

Fig. 6

Basal portion of dorsal claspette of species of Anopheles (Nyssorhynchus). a An. braziliensis (Chagas, 1907). b An. argyritarsis Robineau-Desvoidy, 1827 (redrawn after Faran & Linthicum [10])

Fig. 7

Aedeagus of the male genitalia. a Subgenus Anopheles. b Subgenus Nyssorhynchus (redrawn after Komp [7])

Fig. 8

aAn. thomasi Shannon, 1933. b An. antunesi Galvao & Franco do Amaral, 1940

Fig. 9

aAn. kompi Edwards, 1930. b An. thomasi

Fig. 10

An. kompi

Fig. 11

aAn. thomasi. bAn. nimbus (Theobald, 1902)

Fig. 12

aAn. acanthotorynus Komp, 1937 (redrawn after Komp [12]). b, c An. nimbus (c drawn from b)

Fig. 13

aAn. braziliensis. bAn. costai da Fonseca & da Silva Ramos, 1940

Fig. 14

aAn. darlingi Root, 1926. b An. peryassui Dyar & Knab, 1908

Fig. 15

a, bAn. homunculus Komp, 1937. c An. darlingi Root, 1926

Fig. 16

Aedeagus of An. neivai (Lane & Coutinho, 1940) (a) and An. cruzii Dyar & Knab, 1908 (b)

Fig. 17

a Ventral claspette of An. bambusicolus Komp, 1937. b, c An. homunculus (b redrawn after Zavortink [13])

Fig. 18

An. homunculus

Fig. 19

aAn. neivai. bAn. homunculus

Fig. 20

aAn. pholidotus Zavortink, 1973. b An. lepidotus Zavortink, 1973 (redrawn after Zavortink [13])

Fig. 21

a, bAn. homunculus (a redrawn after Zavortink [13]). c An. laneanus Correa & Cerqueira, 1944

Fig. 22

aAn. cruzii. bAn. bellator Dyar & Knab, 1906

Fig. 23

aAn. bellator. bAn. laneanus

Fig. 24

aAn. triannulatus. bAn. strodei

Fig. 25

aAn. triannulatus. bAn. guarani Shannon, 1928

Fig. 26

aAn. triannulatus. bAn. halophylus

Fig. 27

aAn. guarani. bAn. albitarsis Lynch Arribálzaga, 1938

Fig. 28

aAn. parvus (Chagas, 1907). b An. antunesi Galvão & Franco do Amaral, 1940

Fig. 29

aAn. atacamensis González & Sallum, 2010. b An. darlingi

Fig. 30

aAn. antunesi. bAn. atacamensis

Fig. 31

aAn. antunesi. bAn. pristinus Nagaki & Sallum, 2010

Fig. 32

aAn. pictipennis (Philippi, 1865). b An. lutzii Cruz, 1901

Fig. 33

aAn. atacamensis. bAn. pictipennis

Fig. 34

a, bAn. lutzii. c, dAn. guarani Shannon, 1928

Fig. 35

a, bAn. darlingi. c, d, eAn. lanei Galvão & Franco do Amaral, 1938

Fig. 36

aAn. lanei. b, cAn. argyritarsis

Fig. 37

aAn. sawyeri Causey, Deane, Deane & Sampaio, 1943. b An. argyritarsis

Fig. 38

aAn. albimanus (redrawn after Faran [9]). b An. marajoara Galvão & Damasceno, 1942

Fig. 39

aAn. albitarsis Lynch Arribálzaga, 1878. b An. marajoara

Fig. 40

a, bAn. braziliensis. c, dAn. marajoara

Fig. 41

aAn. strodei. bAn. nuneztovari Gabaldon, 1940

Fig. 42

a, bAn. benarrochi Gabaldon, Cova-Garcia & Lopez, 1941. c An. rondoni (Neiva & Pinto, 1922). d An. strodei

Fig. 43

a, bAn. rondoni. c, dAn. strodei

Fig. 44

aAn. arthuri Unti, 1941. b An. albertoi Unti, 1941

Fig. 45

aAn. strodei. bAn. albertoi

Fig. 46

aAn. ininii (redrawn after Faran [9]). b An. goeldii Rozeboom & Gabaldon, 1941

Fig. 47

aAn. ininii Senevet & Abonnenc, 1938 (redrawn after Faran [9]). b, c An. nuneztovari

Fig. 48

An. goeldii

Fig. 49

aAn. rangeli Gabaldon, Cova-Garcia & Lopez, 1940. b An. dunhami Causey, 1945

Fig. 50

aAn. dunhami. bAn. galvaoi Causey, Deane & Deane, 1943

Fig. 51

aAn. evansae (Brèthes, 1926). b An. galvaoi

Fig. 52

aAn. aquasalis Curry, 1932 (redrawn after Faran [9]). b An. konderi Galvão & Damasceno, 1942

Fig. 53

a, bAn. galvaoi. c, eAn. oswaldoi (Peryassú, 1922). d, f An. konderi

Fig. 54

aAn. squamifemur Antunes, 1937. b An. pseudotibiamaculatus Galvão & Barretto, 1941

Fig. 55

aAn. pseudotibiamaculatus. bAn. gilesi (Neiva, 1908)

Fig. 56

aAn. pseudotibiamaculatus. bAn. gomezdelatorrei Levi-Castillo, 1955

Fig. 57

aAn. vargasi Gabaldon, Cova-Garcia & Lopez, 1941 (redrawn after Levi-Castillo [15]). b An. gilesi (Neiva, 1908)

Fig. 58

a, bAn. gilesi. c, dAn. oiketorakras Osorno-Mesa, 1947 redrawn after Lane [16]

Fig. 59

aAn. tibiamaculatus Neiva, 1906. b An. costai

Fig. 60

aAn. mediopunctatus (Lutz, 1903). b An. eiseni Coquillett, 1902

Fig. 61

a, bAn. mediopunctatus. cAn. costai. dAn. forattinii Wilkerson & Sallum, 1999

Fig. 62

aAn. costai. bAn. forattinii redrawn after Wilkerson & Sallum [17]

Fig. 63

aAn. mattogrossensis Lutz & Neiva, 191163. b An. peryassui

Fig. 64

a, bAn. vestitipennis Dyar & Knab, 1906 (redrawn after Komp [7]). c An. mattogrossensis Lutz & Neiva, 1911

Fig. 65

aAn. mattogrossensis. b, cAn. eiseni geometricus Correa, 1944

Fig. 66

aAn. peryassui. bAn. calderoni

Fig. 67

a, bAn. peryassui. c, dAn. minor da Costa Lima, 1929

Fig. 68

aAn. anchietai Corrêa & Ramalho, 1968. b An. fluminensis Root, 1927

Fig. 69

aAn. maculipes (Theobald, 1903). b An. anchietai

Fig. 70

aAn. apicimacula Dyar & Knab, 1906. b An. pseudopunctipennis (both redrawn after Komp [7])

Fig. 71

aAn. apicimacula. b, cAn. punctimacula Dyar & Knab, 1906 (both redrawn after Komp [7])

Fig. 72

a, bAn. calderoni Wilkerson, 1991. c, d An. shannoni Davis, 1931 (redrawn after Wilkerson et al. [18])

Fig. 73

aAn. medialis Harbach, 2018 (redrawn after Wilkerson et al. [18]). b An. fluminensis

Fig. 74

aAn. medialis. bAn. fluminensis

Fig. 75

a, bAn. neomaculipalpus (b redrawn from [7], c An. pseudopunctipennis (redrawn after Komp [7])