Coccus macarangae Morrison

Gullan, Penny J., Kondo, Takumasa, Fiala, Brigitte & Quek, Swee-Peck, 2018, Taxonomy of coccids (Hemiptera: Coccidae: Coccus L.) associated with Crematogaster ants (Hymenoptera: Formicidae) in the stems of Macaranga plants (Euphorbiaceae) in Southeast Asia, Zootaxa 4521 (1), pp. 1-51 : 22-25

Coccus macarangae Morrison

urn:lsid:zoobank.org:act:30644D80-511B-4645-9BB3-FBFD0D4AC770

( Figs 2A & B , 7 , 8 )

Coccus macarangae Morrison, 1921: 663 .

Type material examined. Holotype: adult female, PENINSULAR MALAYSIA: Selandar forest , in hollow stem

of Macaranga , date not given, coll. I.H. Burkill, Holotype 1(1) ( USNM). Paratypes: same data as holotype, 1(6 first-instar nymphs) ( USNM).

Examined non-type material from original collection. PENINSULAR MALAYSIA: Selandar forest, in hollow stem of Macaranga triloba [now correctly named M. bancana ], date not given, coll. I.H. Burkill, 5-a or 6, two slides also with "1319" in pencil, 3(10) ( BMNH). These three BMNH slides have similar data to the type collection listed above and one slide has the same Burkill collection number as provided by Morrison (1921) in his original description of this species, but they are not type specimens, as explained in the Materials and methods.

Other material examined: BORNEO: Brunei, Batu Apoi Forest Reserve, 4° 33' N, 115° 09' E, ex M. beccariana , M. trachyphylla & Macaranga sp., 3–30 Aug. & 1 Sept. 1995, coll. P.J. Gullan, PJG-B7: 12(8 adult females, 3 third-instar females & 8 first-instar nymphs), PJG-B10: 8(4 adult females, 1 pharate adult female, 1 third-instar female & 14 first-instar nymphs), PJG-B14: 4(4), PJG-B15: 5(5), PJG-B16: 9(9), PJG-B21: 8(8), PJG- B22: 2(2 adult females & 1 third-instar female on slide with C. pseudotumuliferus ), PJG-B23: 1(1) (coll. P.S. Cranston), PJG-B25: 2(2), PJG-B29: 7(7), PJG-B46: 2(1 adult female & 1 third-instar female), PJG-B47: 7(3 adult females, 3 third-instar females & 1 third-instar female pharate in second-instar cuticle), PJG-B50: 1(1), PJG-B52: 3(2 adult females & 4 first-instar nymphs), PJG-B55: 1(1), PJG-B56: 1(1), PJG-B58: 4(3 adult females & 1 thirdinstar female) & PJG-B70: 3(3); Sabah, Crocker Range, Keningau to Ulu Kimanis trail, ~ 5.28° N, ~ 116.05° E, 1100 m, ex M. angulata , 19 Oct. 1999, coll. S.-P. Quek, SPQ.133, DNA voucher 1(1); Sabah, Crocker Range, near Majora, ~ 500 m, ex M. indistincta , 16 Oct. 1999, coll. S.-P. Quek, SPQ.108a, DNA voucher 1(1); Sabah, Crocker Range, Tambunan to Kota Kinabalu Rd, Rafflesia Reserve, 1200 m, M. angulata , 15 Oct. 1999, coll. S.-P. Quek, S.-P. Quek, SPQ.099, DNA voucher 1(1); Sabah, Crocker Range, forest behind Tambunan, 600 m, M. indistincta , 18 Oct. 1999, coll. S.-P. Quek, S.-P. Quek, SPQ.123, DNA voucher 1(1); Sabah, Crocker Range, Tambunan to Trusmadi trail, 1200 m, M. angulata , 23 Oct. 1999, coll. S.-P. Quek, S.-P. Quek, SPQ.156, DNA voucher 1(1); Sabah, Crocker Range, ex M. hullettii , 13 Apr. 2001, coll. B. Fiala, #13 (TK0017), DNA voucher 1(1); Sabah, Luasong, ex M. winkleri , 4 Sept. 2003, coll. B. Fiala, #96, 5(5) (2 ANIC, 3 FRIM); Sabah, Ranau, Langanan [waterfall], ex M. depressa [now correctly named M. angulata ], Feb. 1992, coll. B. Fiala, #23a, 2(2); Sabah, Penangpang [=Penampang), roadside, ex M. bancana , 28 Mar. 2002, coll. B. Fiala, #135 (TK0095), DNA voucher 1(1); Sabah, Poring, ex M. angulata , 25 Mar. 2002, coll. B. Fiala, #110 (TK0100), DNA voucher 1(1); Sabah, Poring, ex M. winkleri , 18 Apr. 2001, coll. B. Fiala, #161 (TK0045), DNA voucher 1(1); Sabah, Poring, ex M.? indistincta , 20 Feb. 1992, B. Fiala, #32a, 2(1 adult female & 1 third-instar female); Sabah, Tawau, road to Madai Caves, ex M. motleyana , 11 Mar. 2002, coll. B. Fiala, #4 (TK0108) & #5 (TK0107), DNA vouchers 2(2); Sabah, Tawau Hills, ex M. kingii [now identified as M. lamellata ] & M. winkleri , 4 & 7 Apr. 2001, coll. B. Fiala, #62 (TK0024) & #96 (TK0032), DNA vouchers 2(2); Sarawak, Lambir, ex M. near kingii [now identified as M. lamellata ], 14 Feb. 1992, B. Fiala, #37a, 2(2) (1 ANIC, 1 FRIM); Sarawak, Lambir, ex M. beccariana, Feb. 1992 , coll. B. Fiala, #51a, 2(2); Sarawak, Lambir, ex M. hullettii , 26 Feb. 1992, coll. B. Fiala, #70a, 3(3); Sarawak, Lambir, ex M. hypoleuca, Feb. 1992 , coll. B. Fiala, #71a, 3(3); Sarawak, 8 km Lambir NP, ex M. lamellata, Dec. 1992 , coll. H.-P. Heckroth, #109, 2(2); Sarawak, Miri, Lambir Nat. Park, ~ 400 m, ex Macaranga sp. [now identified as M. lamellata ], 27 Sept 1993, coll. A. Moog, #93/172, 3(3). PENINSULAR MALAYSIA: Fraser's Hill, ex M. hosei & M. hullettii, Mar. 1993 , coll. H.-P. Heckroth, #274, #281 & #289, 6(6) (4 ANIC, 2 FRIM: #281); Pasoh, ex M. hosei, Mar. 1992 , coll. B. Fiala, #132a & #168a, 3(3); Pasoh, ex M. hypoleuca , 6 Feb. 1992 & Mar. 1992, coll. B. Fiala, #105a: 4(1 adult female & 3 third-instar females) & #193a: 1(1). SUMATRA: Sibolangit, ~ 3° 40' N, ~ 98° 20' E, ex M. bancana , 23 Oct. 1992, coll. U. Maschwitz, sent by B. Fiala, #7a, 2(2).

Material examined from non- Macaranga host plants: BORNEO: Sabah, Ranau, Poring Hot Springs, ~ 700 m, in domatium of Myrmeconauclea sp. ( Rubiaceae ), 24 Mar. 1995, coll. A. Moog, #95/149, 1(1). PENINSULAR MALAYSIA: Selangor, Ulu Gombak, ex hollow stem of Ryparosa fasciculata (Achariaceae) in association with Cladomyrma ?petalae, 20 Sept. 1993, coll. A. Moog, #93/161, 4(4); Selangor, Ulu Gombak, ex hollow stem of Strychnos vanprukii (Loganiaceae) in association with C.?petalae, 7 Mar. 1993, coll. A. Moog, #93/111, 2(2); Selangor, Ulu Gombak, in Lepisanthus tetraphylla ( Sapindaceae ) in association with Crematogaster ants, 28 Mar. 1994, coll. G. Riedel, #94-125.2, 1(1); Selangor, Ulu Gombak, in Saraca thaipingensis (Fabaceae) in association with Crematogaster ants, 25 Apr. 1994, coll. G. Riedel, #94-160.2, 3(3).

Adult female. Unmounted material. “Short oval, pale reddish brown, darker in middle, flat, with faint radiating ridges near margin; dorsal surface appearing naked, possibly with a very thin film of secretion; ..” ( Morrison 1921: 663). Morrison’s description of probably dried adult females from Singapore agrees fairly well with live specimens photographed in Borneo ( Fig. 2A & B ). Adult females from M. winkleri in Sabah ( Fig. 2A ) were orange-brown with some whitish waxy dorsal secretion and ridges radiating inwards from the margin. The amount of dorsal waxy secretion appears to increase as females age but the body margin remains largely devoid of wax, as shown by a mature female from M. beccariana in Brunei ( Fig. 2B ).

Slide-mounted adult female (n=18, including holotype and 4 of Burkill's specimens from Selandar forest; Fig. 7 ). Body oval to elongate oval, body often truncated anteriorly on head, 2.0– 4.4 mm long, 1.3–3.1 mm wide.

Dorsum. Derm (dd) membranous, areolated and with faint submarginal wrinkle lines radiating inwards at right angles to margin. Dorsal setae (dset) mostly sharply spinose, occasionally with a few setae with open divided apices, each 15–40 (mostly 25–35) µm long, scattered on dorsum. Simple pores (sp) each 2.0– 2.5 µm wide, scattered evenly on dorsum. Preopercular pores (pop) each 5–11 µm wide, present in a group of 20–50 anterior to anal plates. Dorsal microducts (dmic) in areolations each about 2–3 µm wide, appearing bilocular under high magnification. Anal plates (anplt) each triangular, anterolateral margin subequal to posterolateral margin (ratio 0.9–1.2) and posterolateral or both margins usually slightly convex, length of each plate 1.4–1.9 times width, inner lobes swollen, with a tessellated texture, each plate 130–145 µm long, 80–103 µm wide, anterolateral margin 85– 120 µm long, postero-lateral margin 85–115 µm long; each plate with 3–4 dorsal setae, each 20–40 mm long. Anal ring (ar) bearing 10 setae [ Morrison (1921: 664) said apparently 8 setae, but these setae are difficult to see], each 100–135 µm long.

Margin. Eyespots present slightly removed from dorsal margin, each 17–23 µm in maximum dimension, often not detected or hard to detect. Marginal setae (mset) fimbriate to sharply spinose, present in 1 row, each seta 10–30 µm long, with 7–30 (mostly 12–24) setae between anterior and posterior stigmatic areas on each side of body. Stigmatic setae (stgset) well developed, numbering 3, lanceolate to tapered spinose with rounded apices, much thicker than marginal setae, bases often swollen, median setae longest, each 18–43 µm long, lateral setae each 7–25 (mostly 12–20) µm long.

Venter. Derm membranous. Ventral setae (vset) slender, with most posterior prevulvar pair longest (each seta 50–70 µm long), elsewhere shorter, each 7–35 µm long. Interantennal setae numbering 2 pairs, each seta ≤ 20 µm long. Ventral tubular ducts (vtd) present in a broad submarginal band; each duct with outer ductule 16–19 µm long, inner ductule 13–20 µm long, and duct opening about 2 µm wide. Ventral microducts (vmic) each about 2 µm wide, scattered fairly evenly on venter. Pregenital disc-pores (pgp) each with 5–10 (mostly 7 and 8) loculi, and each pore 6–7 µm wide. Antennae (ant) 7–8 (mostly 8) segmented, each 200–275 µm long; fleshy setae present on last 3 segments. Clypeolabral shield 240–290 µm long, 180–230 µm wide; labium 80–100 µm long, 135–155 µm wide. Legs with hind trochanter + femur 113–145 µm long; hind tibia + tarsus 120–163 µm long; all tarsal digitules each 25–37 µm long; claw digitules each 17–25 µm long, claws each 20–25 µm long. Spiracles normal: anterior peritremes each 60–93 µm wide; posterior peritremes each 65–100 µm wide. Spiracular pores (spp) each 4–5 µm wide, with 3–5 (mostly 5) loculi, with an occasional pore with 6 or more loculi.

Comments. Adult females of C. macarangae can be distinguished from all other species of Coccus known from Macaranga by having the combination of (i) sharply spinose dorsal setae each mostly 25–30 µm long but a few can be up to 40 µm long; (ii) marginal setae in a single row, with each seta 10–30 µm long with apex fimbriate to sharply spinose; and (iii) anal plates each with 3 or 4 setae, each mostly 20–30 (rarely up to 40) µm long. Adult females of C. macarangae are most similar to the adult females of C. circularis in having fewer than 10 setae on each anal plate and many marginal setae that are apically fimbriate or bifurcate, but differ from C. circularis in that the dorsal setae are sparser, generally longer (up to 40 µm long) and less slender and the preopercular pores are more numerous (20–50) and usually larger (5–11 µm wide) in C. macarangae (dorsal setae 15–30 µm long with flagellate apices and preopercular pores scarce (≤10) and 5–6 µm wide in C. circularis ).

Coccus macarangae was poorly represented in the molecular phylogeny of Quek et al. (2017), although it appears to be a common and widespread species that is found inside the hollow stems of Macaranga species belonging to each of the three myrmecophytic sections of the genus. It also occurs in the hollow stems of several other myrmecophytic genera, namely Lepisanthus, Myrmeconauclea , Ryparosa , Saraca and Strychnos , each belonging to a different plant family (refer to 'Material examined' list above). Adult female coccids from these different hosts showed no consistent differences from females collected from the hollow stems of Macaranga . Morphological variation in the number and size of the preopercular pores was noted among Macaranga -associated adult females of C. macarangae . The length of the dorsal setae also sometimes varied, with a few females having slightly shorter (15–20 µm) and others slightly longer (often 30–40 µm) setae than the typical length of 25–30 µm. One female from Tawau Hills in Sabah collected from M. winkleri (DNA voucher TK0032, coll. B. Fiala, #96) is unusual in having 6-segmented antennae and few pregenital disc pores near the vulva but was confirmed as C. macarangae based on 12S sequences (T. Kondo & L.G. Cook, unpublished data).

First-instar nymph. Slide-mounted material (n=10, all from Brunei, Borneo; Fig. 8 ). Body oval to elongate oval, body often truncated anteriorly on head, 370–460 µm long, 205–280 µm wide.

Dorsum. Derm membranous. Dorsal setae (dset) extremely difficult to see and appearing absent except under x100 objective under oil; each seta very short, at most 1 µm long, in perhaps 4 pairs submedially on thorax and first abdominal segment. One pair of minute simple pores (sp) present on head, but difficult to see except with x100 objective under oil. Preopercular pores and dorsal microducts absent. Anal plates each elongate triangular, 42–58 µm long, 20–33 µm wide, anterolateral margin 25–40 µm long, posterolateral margin 27–40 µm long; each plate with 2 dorsal setae each 10–12 µm long, positioned one each side of long apical seta, 110–124 µm long, plus 1 short inner margin seta. Anal ring (ar) 17–20 µm wide, bearing 6 setae, each 48–62 µm long.

Margin. Eyespots present as pigmented spots on margin, each 9–12 µm in maximum dimension. Marginal setae (mset) flagellate and with distinct bend at about half-length, each seta 10–15 µm long, present in 1 row, with always 2 setae between anterior and posterior stigmatic areas on each side of body, 12 (rarely 13) on head between anterior stigmatic areas and 8 on each side of abdomen with most posterior seta always straight. Stigmatic setae (stgset) numbering 3 in each cleft, thicker than marginal setae, median seta longest, 13–20 µm long, and spinose with rounded apex, lateral setae very small and rounded at apices, each 2–5 µm long.

Venter. Derm membranous. Ventral setae (vcs) as follows: short setae, each 2–3 µm long, present in a marginal and a submarginal longitudinal row of 7 setae on each side of abdomen, with 3 pairs of longer setae (called prevulvar setae on adult female), each 20–35 µm, submedially on posterior abdominal segments; a few setae similar to those on margin of abdomen present marginally on each side of mesothorax and metathorax; 1 pair of ventral cephalic setae (vcs), each 2–4 µm long, situated near apex of head; 1 pair of interantennal setae, each about 30 µm long, between bases of antennae. Ventral tubular ducts absent. Ventral microducts (vmic) each about ~ 1 µm µm wide, very few, present submarginally around body, between each pair of setae on abdomen, 2 located submarginally between anterior and posterior stigmatic areas, and 1 present between base of antenna and body margin, on each side. Abdominal disc-pores absent. Antennae 6 segmented, each 95–112 µm long; fleshy setae present on last 3 segments. Clypeolabral shield 65–90 µm long; labium 25–30 µm long, with 2 pairs of apical setae. Legs normal; hind trochanter + femur 50–62 µm long; hind tibia + tarsus 53–65 µm long; tarsal digitules each 15– 27 µm long, one of each pair slightly thicker than other, each with a small knobbed apex; claw digitules each 10–14 µm long, both knobbed, one thicker than other; claws each 10–14 µm long, with small denticle present (only easily visible with x100 objective). Spiracles normal: peritremes each 4–6 µm wide. Spiracular pores (spp) each ~ 2 µm wide, with 4 loculi; spiracular furrows each with 3 or 4 pores in a line.

Figures

FIGURE 2. Live coccids and ants inside the cut stems of Macaranga plants: A, C. macarangae Morrison, in M. winkleri, Luasong, Sabah, Borneo (E. Linsenmair, 2003 BF #96); B, C. macarangae, in M. beccariana, Temburong, Brunei, Borneo (P.J. Gullan, PJG-B16); C, C. penangensis Morrison, in M. glandibracteolata, Poring, Sabah, Borneo (B. Fiala, 2003 BF #2); D, C. penangensis, in Macaranga sp., Temburong, Brunei, Borneo (P.J. Gullan, PJG-B31); E, C. pseudotumuliferus Gullan & Kondo sp. n., in M. pearsonii, Tawau, Sabah, Borneo (B. Fiala, 2003 BF #64); F, C. secretus Morrison, in M. indistincta, Tawau, Sabah, Borneo (B. Fiala, 2003 #95). All photographs taken by the collector specified in parentheses.

FIGURE 7. Adult female of Coccus macarangae Morrison. Abbreviations as in Fig. 3.

FIGURE 8. First-instar nymph of Coccus macarangae Morrison. Abbreviations for enlargements: ar—anal ring; dset—dorsal seta; mset—marginal setae; sp—simple pore; spp—spiracular pore; stgset—stigmatic setae; vcs—ventral cephalic seta; vmicventral microduct; vset—ventral seta.