Coccus secretus 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 : 39-43

Coccus secretus Morrison

urn:lsid:zoobank.org:act:DE21D89F-17C0-4AC6-8EEC-3D8CD663C7A4

( Figs 2F , 13 )

Coccus secretus Morrison, 1921: 662 .

Type material examined. Holotype: adult female, PENINSULAR MALAYSIA: Penang Island, in hollow stems of Macaranga triloba [now correctly named M. bancana ], date not given, coll. I.H. Burkill, ex coll. E.E. Green, 1(2, holotype, clearly marked, and 1 paratype adult female) ( USNM). Paratypes: PENINSULAR MALAYSIA: same slide as holotype, 1(3) ( USNM; a second slide with immature female not seen); SINGAPORE: in hollow stems of Macaranga , date not given, coll. I.H. Burkill, 3(4) ( USNM). Morrison (1921) noted slight morphological differences between the females from these two collections, in the length of the dorsal anal plate setae and the length of the middle spiracular seta, but considered these differences insignificant in terms of even varietal segregation.

Examined non-type material from original collection. SINGAPORE: Selandar [= Selangor] forest, in hollow stem of Macaranga triloba [now correctly named M. bancana ], date not given, coll. I.H. Burkill, 5-b, 1(6) ( BMNH); same data as previous slide except '1318' (instead of 5-b), 1(3) ( BMNH). PENINSULAR MALAYSIA: Penang Island, in hollow stems of M. triloba [now correctly named M. bancana ], coll. I.H. Burkill, 2693, 6(11) ( BMNH). These eight BMNH slides have the same data as the type collection listed above and the last two collections have the same Burkill collection numbers (1318 and 2693) as provided by Morrison (1921). However, none of the specimens are types, as explained in the Materials and methods.

Other material examined. BORNEO: Brunei, Batu Apoi Forest Reserve, 4° 33' N, 115° 09' E, Macaranga sp., M. beccariana , M. tanarius [a doubtful identification, since this species is a non-myrmecophyte] & M. trachyphylla , 2–27 Aug. 1995, coll. P.J. Gullan, PJG-B2: 1(1), PJG-B7: 1(1), PJG-B8: 9(9), PJG-B11: 7(7), PJG- B46: 4(3 adult females & 1 third-instar female), PJG-B47: 5(5) & PJG-B50: 1(1); East Kalimantan, ~ 60 km NW of Balikpapan, 0° 06' S, 117° 10' E, 60–200 m, ex M. pearsonii , 15 & 16 Nov. 1992, coll. B. Fiala, #152 & #159a, 4(3 adult females & 1 second-instar female); East Kalimantan, Bukit Bangkirai, 1° 1.497' S, 118° 51.949' E, <100 m, ex M. velutina , 13 Feb. 2005, coll. S.-P. Quek, SPQ.728, DNA voucher 1(1); East Kalimantan, Samarinda to Kota Bangun, 0° 15.735' S, 116° 39.667' E & 0° 17.866' S, 116° 41.446' E, <100 m, ex M. motleyana & M. pearsonii , 11 June 2001, coll. S.-P. Quek, SPQ.324 & SPQ.325, DNA vouchers 2(2); North Kalimantan, Long Ampung, Sungai Anai trail, 1° 42.973' N, 114° 57.344' E, 700 m, ex M.? indistincta , 9 Feb. 2005, coll. S.-P. Quek, SPQ.695a&b, DNA vouchers 2(2); Sabah, Crocker Range, Keningaum to Ulu Kimanis trail, ~ 5.28° N, ~ 116.05° E, 250 m, ex. M. bancana , 19 Oct. 1999, coll. S.-P. Quek, SPQ.142 & SPQ.146, DNA vouchers 2(2); Sabah, Crocker Range, Tambunan to Kota Kinabalu Road, Rafflesia Reserve, 1200 m, ex M. hypoleuca , 15 Oct. 1999, coll. S.-P. Quek, SPQ.100a, DNA voucher 1(1); Sabah, Crocker Range, forest behind Tambunan, 600 m, ex M. hypoleuca & M. motleyana , 18 Oct. 1999, coll. S.-P. Quek, SPQ.116 & SPQ.120, DNA vouchers 2(2); Sabah, Luasong, ex M. indistincta & M. winkleri , 4 Sept. 2003, coll. B. Fiala, #95 & 96, 3(3); Sabah, Poring, logging road, ex M. pearsonii , 10 Mar. 2002, coll. B. Fiala, #2 (TK0102), DNA voucher 1(1); Sabah, Poring, 140 km NE of Kota Kinabalu, ~ 6° N, ~ 116° E, 500 m, ex M. beccariana & M. indistincta , 28 Oct. 1992 & 3 Nov. 1992, coll. B. Fiala, #8 & #34, 3(3); Sabah, Poring, 140 km NE of Kota Kinabalu, ~ 6° N, ~ 116° E, 500 m, ex M. pearsonii , 1 Nov. 1992, coll. B. Fiala, #28a, 4(4) (2 ANIC, 2 FRIM); Sabah, road to Sandakan, ex M. hypoleuca , 16 Feb. 1992, coll. B. Fiala, #12a, 3(3); Sabah, Tawau Hills, ex M. glandibracteolata , 5 Apr. 2001, coll. B. Fiala, #78a (TK0028), DNA voucher 1(1); Sabah, 10 km south of Ranau, ex M. pearsonii , no date, coll. H.-P. Heckroth, #1203, 1(1 with 2 adult females of C. pseudotumuliferus ) ( FRIM); Sabah, 60.5 km south of Ranau, ex M. hypoleuca, 1995 , coll. H.-P. Heckroth, #629, 1(1 on slide with 1 adult female of C. pseudotumuliferus ) ( FRIM); Sarawak, Lambir, ex Macaranga sp. & M. kingii [the latter now named M. umbrosa ], 24 Feb. 1992, coll. B. Fiala, #38a & #39a, 2(2); Sarawak, Lambir, ex M. bancana , M. hullettii & M. trachyphylla, 2003 or 2–4 Aug. 2003, coll. T. Itioka, TI.s32, TI.s38 & TI.s62, DNA vouchers 3(3) ( FDS); Sarawak, 2 km Lambir, ex M. trachyphylla & M. hosei, Dec 1992 . coll. H.-P. Heckroth, #72 & #85, 6(6); Sarawak, 3 km Lambir, ex M. trachyphylla, Dec 1992 . coll. H.-P. Heckroth, #92, 4(4); South Kalimantan, Meratus Mts, Kapayang village, 966 m, ex M. bancana , 17 June 2001, coll. S.-P. Quek, SPQ.334, DNA voucher 1(1). PENINSULAR MALAYSIA: Johor, Mawai camp, ~ 1.871° N, ~ 103.954° E, <100 m, ex M. hypoleuca & M. pruinosa , 5 Sept. 1999, coll. S.-P. Quek, SPQ.023a & SPQ.024, DNA vouchers 2(2); Johor, Sedili, 14 km from Route 3, <100 m, ex M. pruinosa , 5 Dec. 1999, coll. S.-P. Quek, SPQ.180a, DNA voucher 1(1); Pahang, near Kuantan, Pancing Falls, <100 m, ex M. bancana , 15 Sept. 1999, coll. S.-P. Quek, SPQ.059, DNA voucher 1(1); Pasoh, ex M. hosei & M. hypoleuca, Mar. 1992 & 11 Mar. 1992, coll. B. Fiala, #125a, #132a, 168a, 193a & 195a, 13(11 adult female & 2 third-instar females); Fraser's Hill, ex M. hosei, Mar. 1993 , coll. H.-P. Heckroth, #280, 5(5) (2 ANIC, 3 FRIM); Genting, 950 m, ex M. hullettii, Mar. 1993 , coll. H.-P. Heckroth, #212, #213 & 220, 14(14); Gombak, lower logging road, ex M. hosei, Feb. 1992 , coll. H.P. Heckroth, #230, 4(4); Gombak, ex M. hosei, Feb. 1993 , coll. H.-P. Heckroth, #214, #234 & #235, 9(7 adult females & 2 thirdinstar females); Gombak, lower logging road, ex M. triloba [now M. bancana ] & M. hosei, Mar. 1993 , coll. H.P. Heckroth, #209, #268 & #270, 7(7); Johor, Labis Air Panas, ex M. hosei , coll. H.-P. Heckroth, #1069, 1(1 on slide with 3 adult females of C. pseudotumuliferus ) ( FRIM); Sekinchang, ex M. pruinosa, Feb. 1993 , coll. H.-P. Heckroth, #239, 5(3 adult females & 2 third-instar females including one with pharate adult). SINGAPORE: Bukit Timah Forest Reserve, inside stem of Macaranga , 1 Mar. 1994, coll. J.H. Martin, JHM6388, 6(23 adult females, 1 nymphal female & 6 first-instar nymphs) ( BMNH); Bukit Timah, 1° 21' N, 103° 47' E, 100 m, inside stem of Macaranga , 8 Apr. 1989, coll. P.S. Ward, PSW10253, 4(4). SUMATRA: Gunung Leuser area, ~ 3° 50' N, 97° 40' E, ex M. hypoleuca , 31 Oct. 1993, coll. U. Maschwitz, sent by B. Fiala, #12a, 1(1); Ketambe, ~ 3° 50' N, ~ 97° 40' E, ex M. hypoleuca , 30 Oct. 1992, coll. U. Maschwitz, sent by B. Fiala, #1359, 2(2).

Material examined from non- Macaranga host plants: PENINSULAR MALAYSIA: Selangor, Ulu Gombak, in Lepisanthus tetraphylla ( Sapindaceae ) in association with Crematogaster ants, 28 Mar. 1994, coll. G. Riedel, #94-125.2, 2(2); Selangor, Ulu Gombak, in Pometia pinnata (Sapindaceae) in association with Crematogaster ants, 19 Apr. 1994, coll. G. Riedel, #94-150.2, 5(5); Selangor, Ulu Gombak, ~ 300 m, ex hollow stem of Ryparosa fasciculata (Achariaceae) in association with ants of Cladomyrma ?petalae, 20 Sept. 1993, coll. A. Moog, #93/161, 2(2); Selangor, Ulu Gombak, ex hollow stem of Strychnos vanprukii (Loganiaceae) in association with C.?petalae, 7 Mar. 1993, coll. A. Moog, #93/111, 1(1); Selangor, Ulu Gombak, ~ 300 m, ex hollow stem of S. vanprukii in association with Cladomyrma sp., 12 Jan. 1995, coll. A. Moog, #95/4, 1(1); Perak, road 59, 25 km to Tanah Rata, ex hollow stem of Saraca thaipingensis (Fabaceae) in association with C.?petalae, 13 Mar. 1993, coll. A. Moog, #93/116, 1(1).

Adult female. Unmounted material. “Slightly longer than wide, flat, the center usually slightly elevated, with faint radiating ridges around the margin, dirty pale brown, appearing as if covered with a thin film of dust; ..” ( Morrison 1921: 662). Morrison’s description probably was based on dried specimens and thus differs in body colour from live specimens photographed from two regions in Borneo. Live adult females varied from pale yellowish-white to pale pink or dark pink ( Fig. 2F ), depending on age, with the dorsal wax appearing granular due to being composed of small irregularly shaped pieces, and the marginal stigmatic areas were often distinct due to accumulation of white wax.

Slide-mounted adult female (n=34, including 7 paratypes; Fig. 13 ). Body oval, often broadest posteriorly,

1.2–3.4 mm long, 1.0– 2.7 mm wide.

Dorsum. Derm (dd) membranous and areolated, with very distinct, lightly sclerotised submarginal lines radiating inwards at right angles to margin. Dorsal setae (dset) very short, as long as or slightly longer than width of setal base, each 2.5–10.0 (4–5 µm on paratypes) µm long, tapering to a point, scattered on dorsum. Simple pores (sp) each 1.5–2.0 µm wide, scattered evenly on dorsum. Preopercular pores (pop) circular to oval in shape, very variable in size and number (sometimes absent), if present each 2.5–7.5 µm wide, scarce to numerous, in a group of 2–34 anterior to anal plates. Dorsal microducts (dmic) in areolations each about 2–3 µm wide, appearing bilocular under high magnification. Anal plates (anplt) each almost subcircular with anterolateral margin slightly longer than posterolateral margin and lateral margin rounded, 1.9–2.7 (mostly 2.1–2.4) times longer than wide, often with apex slightly truncate or indented, inner lobes normal, membranous with a tessellated texture, each plate 140–203 µm long, 65–85 µm wide, anterolateral margin 98–150 µm long, posterolateral margin 75–118 (usually 85–100) µm long; each plate with 6–16 dorsal setae, each seta stout and typically ≥ 2 µm wide for most of length and 15–45 (mostly 20–30) µm long with pointed, rounded or expanded apex; setae usually present on posterior two-thirds of each plate. Anal ring (ar) bearing 8 setae [ Morrison (1921: 663) says 6 setae, but the thinner pair are difficult to see], each 70–95 µm long.

Margin. Eyespots present slightly removed from dorsal margin, each 12–25 µm in maximum dimension, often not detected or hard to detect. Marginal setae (mset) sharply spinose, present in 1 row, each 12.5–35.0 (mostly 15– 30) µm long, with 10–21 setae between anterior and posterior stigmatic areas on each side of body. Stigmatic setae (stgset) well developed, almost always numbering 3 (very rarely 2) per cleft, sharply spinose, median setae longest, each 20–48 (mostly 25–35) µm long, lateral setae each 10–33 (mostly 15–25) µm long.

Venter. Derm membranous. Ventral setae (vset) slender, longest submedially on posterior abdominal segments, each 17–70 µm long, elsewhere shorter, each 10–18 µm long. Interantennal setae usually numbering 2 pairs, each of a different length, with each seta of each pair either 15–25 µm or 27–50 µm long, more rarely 3 or 4 pairs with each seta 10–35 µm long. Ventral tubular ducts (vtd) present in a broad submarginal band; each duct with outer ductule 12–15 µm long, inner ductule 17–20 µm long, and duct opening about 2 µm wide. Ventral microducts (vmic) each 2–3 µm wide, scattered fairly evenly on venter. Pregenital disc-pores (pgp) each with 4–8 (mostly 7) loculi, each pore 5–8 µm wide. Antennae (ant) usually 6 (rarely 5) segmented, each 108–158 µm long; apical segment 20–33 µm long; fleshy setae present on last 3 segments when 6 segmented, and on last 2 segments when 5 segmented. Clypeolabral shield 180–250 µm long, 163–213 µm wide; labium 80–113 µm long, 100–132 µm wide. Legs very small, with hind trochanter + femur 38–68 µm long; hind tibia + tarsus 43–80 µm long; all tarsal digitules each 15–25 µm long; claw digitules each 13–18 µm long, claws each 10–15 µm long. Spiracles normal: anterior peritremes each 50–88 µm wide; posterior peritremes each 55–90 µm wide. Spiracular pores (spp) each 4– 6 µm wide, with 2–7 (mostly 5) loculi.

Comments. Adult females of C. secretus can be distinguished from all other species of Coccus known from Macaranga by having the combination of (1) short antennae (each <160 µm long and usually with 6 segments); (2) very small legs (e.g., hind trochanter + femur <80 µm long); (3) short dorsal setae (≤ 10 µm long) tapering to a point; (4) a single row of sharply spinose marginal setae, each mostly 15–30 µm long; and (5) robust anal plate setae, each typically ≥ 2 µm wide for most of its length and mostly 20–30 µm long. Adult females of C. secretus are most similar to the adult females of the C. tumuliferus group ( C. caviramicolus , C. pseudotumuliferus and C. tumuliferus ) in having very short dorsal setae but they differ from those females in that their dorsal setae each taper to a point (apex rounded in the other species), their marginal setae are never in 2 rows and never flagellate or fimbriate (sometimes in 2 or even 3 rows and often fimbriate or flagellate in the other species) and their anal plate setae mostly are longer (typically 20–30 µm long) and distinctively broad for their full length (tapering to a point and usually ≤ 20 µm long in the other species). Specimens of C. secretus from non- Macaranga host plants were indistinguishable morphologically from females from Macaranga , although four of the five non- Macaranga females measured had a slightly larger length to width ratio for their anal plates (2.5–2.7) compared with Macaranga females (ratio never greater than 2.4).

The analysis of Quek et al. (2017) using two nuclear genes found C. secretus to be separated from the other Coccus species on Macaranga by the placement of C. hesperidum . This topology also was recovered in one of the two mitochondrial data sets of Ueda et al. (2010). We have not been able to see and verify the identity of the specimen called C. hesperidum that was used in the papers of Ueda et al. (2008, 2010) and Quek et al. (2017), but its proximity to the Macaranga coccids in the nuclear DNA tree of Quek et al. (2017) is consistent with the observation that C. penangensis is close to C. hesperidum based on analysis of two ribosomal genes, one nuclear gene and COI ( Lin et al. 2013). It seems that C. secretus is not closely related to the other specialist Coccus partners of the myrmecophytic Macaranga species. Further analyses including additional genes and a diversity of Coccus species are required to determine the relationships of C. secretus to other Coccus species.

Coccus secretus is a widespread species occurring in both primary and secondary forests of Borneo, Peninsular Malaysia, Singapore and Sumatra ( Heckroth et al. 1998; list of Material examined above). It also has been collected a number of times from inside the hollow stems of non- Macaranga host plants (see list above) even though such plants have been surveyed much less frequently than Macaranga . Heckroth et al. (1998) recorded C. secretus inside the hollow stems of both myrmecophytes and non-myrmecophytes in association with both the obligatory plant-ant genus Cladomyrma and non-specific Crematogaster species. Quek et al. (2017) found that C. secretus in most cases made up a small proportion of the coccid partners of the specialist Crematogaster ants and myrmecophytic Macaranga species. Thus, it is possible that C. secretus is a more facultative or opportunistic partner than the other Coccus species found in the system.

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 13. Adult female of Coccus secretus Morrison. Abbreviations as in Fig. 3.