Lema (Quasilema) apicalis Lacordaire, 1845

Groll, Elisa Von, 2021, Solving an old dilemma: are the two sympatric species Lema apicalis and L. reticulosa (Coleoptera, Chrysomelidae, Criocerinae) morphotypes of a single species?, Zootaxa 5048 (3), pp. 334-346 : 335-343

Lema (Quasilema) apicalis Lacordaire, 1845

( Figs 1–53 )

Lema apicalis Lacordaire, 1845: 388 ; Blackwelder 1946: 628 (catalogue); Monrós 1951: 468; Guérin 1953: 96 (morphology); Monrós 1960: 134, 214 (biology & distribution); Silva et al. 1968: 429 (biology, host plant); White 1993: 20 (revision); Jolivet 1997:144; Medeiros et al. 1994 (biology); Moura & Grazia 2011: 620 (biology); Santiago-Blay et al. 2012: 334, 336 (biology); Dury et al. 2014: 3 (biology).

Lema reticulosa Clark, 1866: 31 ; Gemminger & Harold 1874: 3259 (distribution); Jacoby & Clavareau 1904: 21 (distribution); Clavareau 1913: 76 (distribution); Blackwelder 1946: 631 (catalogue); Guérin 1953: 96 fig. 139: 108 (morphology); Monrós 1960 (distribution); Bertels 1962: 3 (host plant); Silva et al. 1968: 430 (biology, host plant); White 1987: 106 (distribution); Jolivet 1997: 144; Medeiros et al. 1994 (biology) Moura & Grazia 2011: 620 (biology); Santiago-Blay et al. 2012: 334, 336 (biology); Dury et al. 2014: 3 (biology) new synonym.

Material examined (n= 138, * = specimen dissected): Brazil. Paraná: 1, Três Barras do Paraná , 19-27.II.1993, A. Bonaldo (238.317); Rio Grande do Sul: 5, [no data provided], T. de Lema (26.044–26.047, 26.060) ; 2, Campo Bom , 25.II.1985, 18.III.1985, C. J. Becker (62.135, 62.273) ; 1, Canela , 22.I.1984, M. Hoffmann col. (61.129) ; 4, ditto except 4.I.1962, 6.I.1962, P.C. Braun (26.048, 26.049, 26.064, 26.063) ; 2, Canguçú, Coxilha do Fogo, I.1998, C. N. Duckett (238.312, 238.313) ; 1, Canoas ( REFAP), 13.XII.1996, L. Moura (238.314) ; 1, Derrubadas, Parque Estadual do Turvo, 31.X.2003, L. Moura (227.992) ; 1, Eldorado do Sul, Faz. São José , 12.XI.1996, L. Moura (163.590) ; 2, 1♂ *, ditto except, 26.I.1999, L. Moura (161.397, 163.591) ; 2, ditto except, A. Bonaldo (161.400, 161.396, 161.478) ; 1♂ *, 1♀ *, Eldorado do Sul, Distrito Parque Eldorado, Parque das Acácias, 26.III.2016, J. Nunes ; 2, Frederico Westphalen, 9.X.2004, L. Massolino & G. Mansur (237.932, 237.933) ; 1, 17.IX.2005, L. Massolino (238.328) ; 1, Gramado, XII.1956, F. Meurer (26.051) ; 8, Gravataí, 11.X.1973, M. H. Galileo (26.052 –26.057, 26.059, 26.065) ; 1, Ijuí, 20.X.2001, M. Daronco (231.899) ; 1, Ijuí, Campus UNIJUÍ, 10.X.2001, F. L. Santos (231.905) ; 1, Maquiné, II.1998, C. N. Duckett (238.330) ; 1, Maquiné, E.E.A. FEPAGRO, 9-11.I.2006, coleta com fogging (237.158) ; 1, Montenegro, 07.VII.1977, H. A. Gastal (22.391) ; 10, ditto except, 20.XII.1977, A. Lise (26.901), 1.XII.1977, A. Lise (25.020, 25.076, 25.078), E. H. Buckup (25.075), V. L. Pitoni (25.077), 15.XII.1977, M. L. Tavares (25.860, 25.861), H. Bischoff (27.164), E. H. Buckup (25.756) ; 5, Passo Fundo (238.305-238.309) ; 1, Porto Alegre, 8.XI.1961, E. Corseuil (238.553) ; 9, ditto except, 5.XII.1963 (238.554-238.558), IX.1953, E. Corseuil (238.559), 26.IV.1961, M. Amago (238.560), 25.XI.1959, P. Godoi (238.561), 27.IX.1985, T. Arigony (62.568) ; 10, Porto Alegre, Jardim Botânico, 29.X.1990, M.A. Santos (124.671), 25.III.1998, L. Moura ( MCNZ 238.302 – 238.304 , 238.319 – 238.321 ), C. Duckett ( MCNZ 238.300 , 238.301 , 238.322 ) ; 3, 1♂ *, 2♀ *, ditto except, 4.X.2013, L. Moura (238.310, 238.311, 238.323–238.226) ; 1♂ *, 3♀ *, ditto except, 29.XII.2015, E. von Groll (238.331–238.334) ; 1♂ *, 1♀ *, ditto except, 2.VI.2016, E. von Groll ( MCNZ 238.546 , 238.547 ) ; 2, Rio Pardo, 5.IX.1961, 6.IX.1961, A. Lise (26.061, 26.062) ; 1, Rolante, 18.XII.1979, J. C. Becker (238.329) ; 5, Rosário do Sul, X.1955, A. C. Duarte ; 1, São Francisco de Assis, Cerro Sul , 29°31’12”S 55°07’35”W, 24.XI.2009, R. Ott & I. Heydrich (237.694) ; 1, São Francisco de Paula, II.1956, L. & E. Buckup (26.050) ; 2, São Francisco de Paula , Inst. Nac. Pinho , 23.I.1959, Pereira et al. (233.655, 233.656) ; 16, 1♀ *, São Francisco de Paula , Passo do Inferno , 4.XI.1996, L. Moura (161.255, 161.257, 161.258, 161.261–161.273) ; ditto except, 1, São Francisco de Paula , Barragem dos Bugres, 2.II.1999, A. Bonaldo (162.610) ; 1, São Francisco de Paula , Faz. 3 Cachoeiras , 3.II.1999, L. Moura (162.919) ; 6, São Francisco de Paula , Boca da Serra , 18-20.IV.2003, L. Moura & I. Heydrich (219.924, 219.925, 219.929, 219.930, 219.931 219.933) ; 1, São Francisco de Paula , Boca da Serra (29°26’38,4”S, 50°37’20”W), 24.I.2009, L. Moura (238.327) ; 1, Triunfo, 15.IX.1977, A. Lise (24.086) ; 1, ditto except, 12.I.989, M. H. Galileo (238.315) ; 8, Triunfo , Copesul , 8.X.1988, M. Hoffmann (216.064), 8.XI.1988, H. A. Gastal (216.066), 21.IX.1989, M. Hoffmann (216.060, 216.062), 24.X.1989, M. A. Marques (216.063), 28.XI.1989, E. H. Buckup (216.059), 11.IX.1992, E. H. Buckup (216.067), 14.II.2008, M. Pasolius (238.316) ; Santa Catarina: 2, Três Barras , 11.VI.1994 (238.318), 12.III.1995 (167.087) .

Redescription. Length 8.0– 10.7 mm, width (humeral region) = 3.0– 4.1 mm; males usually smaller than females, but with considerable overlap. Body oblong ( Figs 1, 3, 5 ), sides parallel, somewhat convex in lateral view ( Figs 2, 4 ). Color varying according to fixation of specimen; live specimens brighter and more vibrant. Head, pronotum, and mouthparts orange, maxillary and labial palpomere and apex of mandible black, scape pale orange, pedicel and antennomeres III–XI black. Scutellum entirely dark blue ( apicalis pattern; Fig. 1 ) or with basal region orange, sometimes extending to central region ( reticulosa and intermediate patterns; Fig. 6 ). Elytra metallic blue, apex with creamy white to yellow triangular mark only ( apicalis pattern: Figs 1, 2 ), or two stripes of the same color as the apex dorsally and laterally ( reticulosa pattern; Figs 3, 4 ), or rarely traces of these stripes, more ( Fig. 5 ) or less marked ( Figs 6, 7 ) (intermediate pattern). Meso- and metaventrie dark blue, except for yellowish mesoventrite and mesanepisterna. Pro- and mesocoxae and trochanters yellowish, metacoxae dark blue. Femora yellow with apex and a dorsal mark black, located posteriorly on the prefemur. Tibiae and tarsi black. Abdomen dark blue; ventrite V with two lateral yellow spots on each side. Leg and ventral pubescence white.

Head. Longer than wide, integument smooth and glossy ( Fig. 8 ). Vertex with central fovea between the eyes. Frons with x-shaped groove, with long setae, sparsely distributed, more concentrated on inner superior margin of eyes ( Fig. 8 ). Eyes emarginate, finely faceted, and strongly projecting ( Fig. 8 ). Antennae inserted next to inner margin of the eyes ( Fig. 9 ). Scape and pedicel globose, almost glabrous ( Fig. 8 ); antennomere III slightly shorter than IV, V somewhat longer than VI, and VI and XI subequal; antennomeres III–XI covered with white, short and dense pubescence and with long setae at apex of each segment; apex of antennomere VII with small projecting tubercle ( Fig. 9 ). Gena with length subequal to length of eyes, with pubescence next to inferior margin of the eyes. Clypeus subtriangular, smooth and glossy, with long setae sparsely distributed laterally ( Fig. 8 ). Labrum glossy and sub-rectangular, apical margin slightly emarginate at center; long setae sparsely distributed ( Fig. 10 ). Mandible with three teeth: two anterior prominent and posterior short and thick ( Figs 11, 12 ). Maxillae with galea and lacinia somewhat broad ( Fig. 13 ). Labial palp 3-articulated ( Fig. 14 ).

Thorax. Pronotum laterally constricted, widest in anterior half; angles rounded ( Fig. 15, 16 ). Integument glabrous, smooth and glossy, punctation shallow, restricted to center and lateral areas; central fovea slightly above anterior margin; long setae next to each anterior and posterior angle. Coxal cavities closed ( Fig. 16 ). Profurca long and divergent, distal region dilated and rounded ( Fig. 17 ). Scutellum smooth, somewhat longer than wide, posterior margin rounded ( Fig. 18 ). Mesoventrite with posterior margin sub-rectangular and with sparse pubescence, denser laterally ( Figs 2, 4 , 19 ); mesanepisterna, mesepimeron, and metanepisternum densely pubescent ( Figs 2, 4 , 19 ).

Metendosternite with furcal arms (fa) truncated and divergent; anterior lamina (al) short, projected along the whole furcal arm; anterior tendon (at) inserted at 1/3 of the anterior lamina; ventral lamina (vl) slender; ventral tendon (vt) lobular, at the distal region of the furcal arm ( Fig. 20 ).

Elytra with lateral margins subparallel, surface glabrous, smooth and glossy at basal area and next to suture; other parts of elytra with integument irregularly rugose, usually shiny, but some mounted specimens matt ( Figs 1–5 ). Hind wings fully developed; Subcosta separated from Costa (C), Radius (R) distally enlarged, Radial cell evident; Cubitus (Cu) 1 divided into two evident arms: Cu1a, simple and isolated, and Cu1B; Pos cubital (Pcu) narrow, disappearing after Cub1; first cubital cell (1Cuc) fusiform; J1 sclerotized and short ( Fig. 21 ).

Male. Abdomen. Ventrite I subequal in length to II + III; apical margin of ventrite V rounded. Tergite VIII slightly bilobed at apex.

Genitalia ( Figs 22–24 ). Median lobe elongated and slightly curved in lateral view ( Fig. 24 ); basal region concave, spoon-shaped ( Figs 22–24 ); apical region subacuminate ( Fig. 23 ). Tegmen ( Fig. 22 ) hastate, dorsally flat at apical portion, near center forking into two arms that partially surround median lobe. Internal sac bearing sclerites ( Fig. 24 ).

Female. Genitalia ( Figs 25–32 ). Tergite VII ( Fig. 25 ) slightly sclerotized, apex medially emarginate, pubescent. Tergite VIII rounded ( Fig. 26 ). Sternite VIII emarginate apically, with sparse long setae, apodeme well developed ( Fig. 27 ). Vaginal palpi subquadrangular, sclerotized apically, bearing long setae ( Fig. 28 ). Bursa copulatrix saccular, membranous, and smooth ( Fig. 26 ). Spermatheca sclerotized, anterior region divided into an elongated and cylindrical portion where it is inserted in the spermathecal duct and a coiled portion, which varies independent of elytral pattern ( Figs 25, 26, 29–32 ); distal region divided into rounded base, bearing the spermathecal gland, and projected form, hook-shaped ( Fig. 29 ).

Distribution. Lema apicalis is known from southern Brazil, Paraguay, Argentina, and Uruguay ( Blackwelder, 1946; Guérin, 1953, Medeiros et al., 1996) ( Fig. 33 ). Lacordaire (1845) notes L. apicalis in the “surroundings of” Rio de Janeiro (southeast Brazil) ( Fig. 33 ). Blackwelder (1946) mentions the reticulosa pattern in Mexico, which is almost certainly a mistake, as pointed out by White (1987). This record was based on confusion of the Rio Grande River in Mexico with the Rio Grande do Sul in Brazil.

Biology. Eggs, larvae, and adults were most abundant during spring (23 September–21 December), in association with their host plant ( Fig. 34 ). In early September, adults started to emerge, with larger host plants carrying more beetles, and by October, specimens were dense on all host plants. During the following months the population slowly decreased, until autumn (May), when beetles were absent at the field site. However, specimens have been collected in autumn and winter months at other sites (see Material Examined). The apicalis pattern was much more common than the reticulosa pattern, and the intermediate pattern was rarely found.

The only observed hostplant in this study was Vassobia breviflora (Sendtn.) Hunz (Solanaceae) ( Figs 35, 36 ), with distribution in Brazil (São Paulo to Rio Grande do Sul), Bolivia, Paraguay, Argentina and Uruguay ( Hunziker, 1984). According to Bertls (1962), specimens identified as L. reticulosa also fed on Cestrum parqui L’Herit (Solanaceae) , but this may be a mistake: the host plant or beetle could have been misidentified, especially because the reticulosa pattern is found in other Lema species. Vassobia consists of two species in the small subtribe Iochrominae of tribe Physaleae ( Olmstead et al. 2008) . Adults and larvae feed on the entire leaf, except the large central vein, often defoliating the entire plant, which makes it easy to find the beetles. Copulations both ex situ and in situ were often observed ( Figs 37–41 ). All four possible pairings of the two major colour forms occurred: male and female apicalis pattern ( Fig. 37 ), male and female reticulosa pattern ( Fig. 38 ), male reticulosa pattern + female apicalis pattern ( Fig. 39 ), and male apicalis pattern + female reticulosa pattern ( Fig. 40 ). In the field, males and females copulated with more than one individual, regardless of the color pattern and without obvious preference. All the following observations related to copulation were noted for all four pairs above.

Males often competed to mate with females, even in dense populations. Single males used their mandibles to pull the antennae of the mating male off the female. The behavior was often so aggressive that the copulating male stayed connected to the female only by the terminalia. During these attempts, there was audible stridulation but it was not possible to determine which individual was stridulating.

Mate guarding was common. Often it was initiated by refusal of the female to copulate. First, a male climbed on the same female many times in a short period, trying unsuccessfully to connect terminalia. Sometimes it managed to connect the terminalia but briefly, apparently without release of sperm. After a few failed attempts, the male climbed on the female and stayed there for 1–15 minutes, with its body positioned in the opposite direction to the female ( Fig. 41 ). Then the male tried to copulate again, often successfully. If the attempt was again unsuccessful, the male usually went away and tried to copulate with another female; males rarely repeated this behavior with the same female.

Predatory bugs of the genus Podisus Herrich-Schaeffer, 1851 ( Pentatomidae : Asopinae ) were frequently observed feeding on larvae of L. apicalis and this pentatomid was commonly seen on the host plant. An unidentified eulophid wasp was frequently observed parasitising egg masses.

Sometimes, when disturbed, adults ejected a brown liquid from their mouth ( Fig. 42 ). Other observed defense mechanisms were: stridulation, flight, biting, and hiding under the leaves.

Females laid about 200 eggs in a batchon the under surface of leaves ( Fig. 43 ). The egg batch formed a circular mass about 9 mm in diameter and 0.5 mm in height ( Figs 44, 45 ). At first, the eggs were light yellow ( Fig. 43 ), but they became translucent caramel yellow ( Fig. 44 ) due to the change in colour of the sticky paste coating them ( Fig. 45 ). Hatching occurred after five days on average ( Fig. 46 ). Only wasps emerged from parasitized eggs.

First-instar larvae were pale-yellow ( Fig. 46 ), with black head and gray legs; as they developed, they became more yellow-gray.After hatching they instantly formed a large cycloalexic group ( Fig. 47 ). After the second instar, a variety of formations was observed: some of them had many individuals, but others were small, possibly due to the space on the leaf ( Figs 47–50 ). The fourth instar only occured in small groups, but solitary larvae were not observed ( Fig. 51 ).

Four larval defense behaviors were observed: (1) fecal shield, (2) cycloalexy, (3) up and down movements of the anterior part of the body, and (4) regurgitation of a dark fluid ( Fig. 49 ). This fluid was released as a drop that the larvae kept holding with their mouth; when the disturbance ended, the fluid was swallowed. The up and down movements occurred before and while the larvae were holding their fluid.

While migrating to the soil for pupation, mature larvae defecated copiously, which caused a change in their color, becoming yellow ( Figs 51, 52 ). After reaching the soil, they went underground and produced isolated white cocoons from an oral foamy substance that solidified into a case ( Fig. 53 ).

Figures

FIGURE 33. Lema (Quasilema) apicalis Lacordaire, 1845 distribution map. Circles represent the material examined and squares, data from literature.

FIGURES 1–14. Lema (Quasilema) apicalis Lacordaire, 1845, apicalis pattern: habitus; 1, dorsal view, 2, lateral view; reticulosa pattern: 3, dorsal view, 4, lateral view; intermediate pattern: 5, dorsal view; intermediate pattern: 6, detail of the scutellum, 7, epipleuron, lateral view; apicalis pattern: 8, head, frontal view; 9, antenna; 10, labrum; mandible: 11, inner view; 12, outer view; 13, maxilla; 14, labium, ventral view (a7, antennomere VII). Scale bars: 1–5 = 1 mm; 6–9 = 0.5 mm, 10–14 = 0.1 mm.

FIGURES 15–21. Lema (Quasilema) apicalis Lacordaire, 1845, apicalis pattern: 15, pronotum; 16, prothorax, ventral view; 17, prothorax, internal view; 18, scutellar plate; 19, meso- and metasternum; 20, metendosternite, dorsal view; 21, hindwing (1J, jugal; 1Cuc, first cubital cell; al, anterior lamina; C, Costa; fa, furcal arm; Pcu, Post cubits; pr, profurca; R, Radius; rc, radial cell; Sc, Subcosta; vl, ventral lamina, vt, ventral tendon). Scale bars: Figs 15–18 = 0.5 mm; Fig. 19 = 1 mm; Fig 20 = 0.2 mm.

FIGURES 22–32. Lema (Quasilema) apicalis Lacordaire, 1845: male, 22, tergite VIII, and genitalia; aedeagus: 23, ventral view, 24, lateral view; female: 25, ventrite VII and genitalia; 26, tergite VIII, and genitalia; 27, sternite VIII; 28, vaginal palpi; 29-31, spermatheca: apicalis pattern: 29, specimen 1, 30, specimen 2, 31, specimen 3; reticulosa pattern: 32. (ap, apodeme; bc, bursa copulatrix; ds, distal part of the spermathecal; i, intestine; gs, spicullum gastrale; ml, median lobe; ov, oviduct; ps, proximal part of the spermathecal capsule; s, spermathecal capsule; s8, sternite VIII; sc, sclerite of the internal sac; sd, spermathecal duct; sg, spermathecal gland; t, tegmen; t7, tergite VII; t8, tergite VIII, v5, ventrite V, vp, vaginal palpi). Scale bars: Figs 22–26 = 0.5 mm; Figs 27, 28 = 0.2 mm; Figs 29–32 = 0.1 mm.

FIGURES 34–42. 34, Lema (Quasilema) apicalis Lacordaire, 1845 on the host plant; Vassobia breviflora (Sendtn.) Hunz.: 35, adult plant, fully mature; 36, flower; 37–40, Lema apicalis, copule; 37, male and female apicalis pattern; 38, male and female reticulosa pattern; 39, male reticulosa pattern and female apicalis pattern; 40, male apicalis pattern and female reticulosa pattern; 41, mate guarding; 42, defense behavior (regurgitation).

FIGURES 43–53. Lema (Quasilema) apicalis Lacordaire, 1845: 43, development of immature stages on Vassobia breviflora (Sendtn.) Hunz (leaf with underside facing up); eggs: 44, one day; 45, five days, immediately pre-hatching; 46, larvae hatching from eggs; 47–50, larval feeding; 51, larvae, last instar, before defecating; 52, larval last instar, defecation and migration to soil; 53, pupae. Arrow indicates regurgitation.