Arimoto - MacGowan - Su - 2020 - Lonchaeidae Asociadas A Higo - Japon
Arimoto - MacGowan - Su - 2020 - Lonchaeidae Asociadas A Higo - Japon
Arimoto - MacGowan - Su - 2020 - Lonchaeidae Asociadas A Higo - Japon
A R T I C LE I N FO A B S T R A C T
Keywords: Larvae of the genus Silba Macquart, 1875 were obtained from the syconia of three different species of Ficus
Diptera growing on the southern islands of Japan and Taiwan. Examination of the emerged adults identified four species,
Ficus two of which are described as new to science: Silba erecta MacGowan and Arimoto sp. nov. and Silba thunbergii
Fig wasps MacGowan and Arimoto sp. nov. Of the four species observed, the larvae of S. erecta, Silba ishigaki MacGowan
Lonchaeidae
and Okamoto, 2013 and S. thunbergii feed on the tissue of the fig syconia. Silba inubiwa MacGowan and Okamoto,
Predator
2013 was observed as a predator of three fig wasp species. The biogeographic distribution and biological data
Taxonomy
are provided for each of these fig-associated species.
Introduction on syconium flesh. Data are also provided on the biology and dis-
tribution of two previously described species.
The association of species in the genus Silba Macquart, 1875 with fig
syconia has been known for over a century. Silvestri (1917) provided Materials and methods
the first account when he detailed the life history of Silba adipata
McAlpine, 1956 under the name Lonchaea aristella Becker, 1902 based Field work was conducted on Shikoku and the Ryukyu Islands,
on misidentification. The larvae of this Mediterranean species live in Japan and in Taiwan during 2017 and 2018 to collect Silba larvae
the flesh of Ficus carica L. syconia. More recently, five Silba species closely associated with the fig–fig wasp mutualistic system (Fig. 1).
associated with figs have been described from India (MacGowan et al., Specimens examined were collected by Kôichi Arimoto (KA), Yûji
2012), Japan (MacGowan and Okamoto, 2013), Thailand, and Cam- Matsumoto (YM), Ayako Sasaki (AS), Zhi-Hui Su (ZHS), and members
bodia (MacGowan and Compton, 2018). These Silba species are as- of the laboratory of Taxonomy and Ecology of Forest Plants, National
signed to two groups: in the first, the larvae feed on the flesh of fig Chung Hsing University (TEFP; Po-An Chou, Hiu-Wa Lee, Shin-Hung
syconia, and in the second, the larvae apparently prey on fig wasps Pan, Yu-Chun Yi, and Prof. Hsy-Yu Tzeng). Five to ten syconia in stages
(Okamoto et al., 2012; MacGowan and Compton, 2018). Given the ranging from C (wasp developing) to E (ripe syconia) or F (fallen sy-
approximately 850 species of fig, which comprise the most diverse conia) were examined per male fig tree [terminology after Galil and
group in the family Moracea (Christenhusz et al., 2017), there must still Eisikovitch (1968) and Palmieri et al. (2018)]. When Silba larvae were
be many undescribed Silba species using this microhabitat. Further found in syconia, they were removed and transferred into plastic
study of the taxonomy, behaviour, and feeding habits of these Silba rearing vials. These were kept at room temperature (ca. 25 °C) for about
species should lead to an increased understanding of the biological 2 weeks until adults emerged. Samples of the emerged adults were
diversity and interactions associated with fig–fig wasp mutualism, as preserved in 80% ethanol for morphological examination; the re-
well as the evolution of larval feeding strategies within the genus Silba. mainder were stored in 99.5% ethanol for future molecular analyses.
Therefore, we conducted field work to collect new materials and bio- Leaves of the trees examined were also kept as identification records.
logical information on Silba species in Japan and Taiwan. This paper The syconia from which larvae were removed were preserved in 99.5%
describes two new fig-associated Silba species, the larvae of which feed ethanol and leaves were preserved using the teabag method (Wilkie
⁎
Corresponding author.
E-mail addresses: [email protected] (K. Arimoto), [email protected] (I. MacGowan), [email protected] (Z.-H. Su).
https://doi.org/10.1016/j.aspen.2019.11.007
Received 30 March 2019; Received in revised form 13 November 2019; Accepted 15 November 2019
Available online 05 February 2020
1226-8615/ © 2020 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
K. Arimoto, et al. Journal of Asia-Pacific Entomology 23 (2020) 364–370
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Fig. 2. Male terminalia of Silba erecta sp. nov. A: Epandrium and associated structures, right side, lateral view; B: surstylus, left side, internal view; C: phallus, right
side, lateral view.
more than 0.1 × length of orbital seta; longer setulae on anterior Legs entirely black including ventral row of spicules on fore and hind
margin above lunule. Lunule ground colour black, covered by silver- basal tarsomeres.
grey pollinosity; face and parafacials lightly grey dusted. Anterior genal Abdomen. Genitalia (Fig. 3). In lateral view epandrium slightly
setulae forming a single row of 5 along mouth margin; basal two setulae higher than long, anteriorly with a semi-circular excavation, numerous
longest and strongest on genae. Antennae entirely black; postpedicel long setulae located ventrally and posteriorly. Cerci rather small, rec-
length to depth ratio 2.5:1; arista with short plumosity, at its greatest tangular in shape, bearing numerous short, stiff setulae (Fig. 3A) In
extent 0.5 × width of postpedicel. ventral aspect large rounded surstyli project beyond shell of the epan-
Thorax. Proepimeron and proepisternum each with 1 seta. Scutum drium, each with a marginal row of setulae. Medial margin of surstyli
sub-shining black, covered with short appressed setulae, which no more with 5–6 lateral creases. Internal view, a pair of setulae present at base
than 0.3 × length of orbital seta. Scutellum on margin with 4 short of cerci (Fig. 3B); prensisetae in a single row of 6 near posterior margin
setulae on right side and 5 short setulae on left side between lateral and of surstyli, gradually becoming longer ventrally; the ventral 2 pre-
apical setae, with a pair of very short setulae between apical setae. nsisetae long and thin, almost 3 × as long as the basal prensiseta.
Anepisternum with a row of 3 anterior and 4 posterior setae, a scat- Pregonites bifurcated, finger–like, with an apical seta. Postgonites large
tering of setulae between these rows no more than 0.5 × length of the and rectangular; medial margin with a row of 5–6 small setulae. Phallus
setae. Katepisternum with 2 setae near dorsal margin; a few setulae relatively small and lightly chitinised, with a pair of small, pointed
lying anterior to these setae otherwise the sclerite almost bare. Wings apical processes and basally a pair of large almost rectangular processes
clear, veins dark brown, wing length 3.5 mm. Calypteres very slightly (Fig. 3C); intromittent organ slender and slightly curved.
greyish with a relatively dense fringe of white setulae. Halteres black. Female. Similar to male apart from the usual sexual differences.
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Fig. 3. Male terminalia of Silba thunbergii sp. nov. A: Epandrium and associated structures, right side, lateral view; B: ditto, ventral view; C: phallus, right side, latral
view.
Aculeus with apical segment spear shaped, dorsally with a pair of basal fig wasps were those of S. inubiwa, whereas the larvae feeding on the
setulae 0.5 × length of apical segment, ventrally with a similar pair syconium tissue belonged to S. thunbergii (see also bionomics of S. in-
setulae near apex; a further much shorter pair setulae located at mid- ubiwa).
point on ventral margin.
Remarks. In several features this species, with 2 setae on the ka-
tepisternum, is a more typical member of the genus Silba but differs in Further data on previously described species associated with figs
the greatly reduced plumosity on the arista. The male terminalia are
also relatively typical of the genus. As is the case in other Silba species Silba inubiwa MacGowan and Okamoto, 2013
the key specific character is the distinctive structure of the phallus
(Fig. 3C). Silba inubiwa MacGowan and Okamoto, 2013: 197 (original de-
Distribution (Fig. 1). JAPAN: Ryukyu Islands (Amami-Ôshima Is.). scription; type locality: Kii-Ôshima Island, Wakayama Prefecture,
Host plant. Ficus thunbergii Maxim. Honshu, Japan).
Bionomics. Eggs of this species were laid between the ostiolar Material examined. Ex. Ficus erecta. JAPAN. Shikoku: 2 males,
bracts of the syconia of Ficus thunbergii (Fig. 4A: arrows). On hatching, Ôshima, Sukumo City, Kôchi Pref., 32.9157° N, 132.6986° E, 19 m, 7 IX
larvae moved inside the syconia (Fig. 4B, C). It was not possible to 2017, KA leg. (J17-695E) [BRH]; 1 female, same place, 32.9155° N,
define the feeding habits of S. thunbergii larvae clearly, as two types of 132.6971° E, 69 m, 7 IX 2017, KA leg. (J17-707 K) [NMS]. Ryukyu.
larvae with different feeding habits were found in the same syconium Kagoshima Pref.: Yakushima Is.: 2 female, Anbô, Yakushima Town,
(Fig. 4C). Many larvae preyed on adult fig wasps inside their galls Kumage District, 30.3164° N, 130.6353° E, 163 m, 19 VII 2018, KA leg.
(Fig. 4C: white arrow), whereas others fed on syconium tissue (Fig. 4C: (J18-614B) [1 female: NMS; 1 female: BRH]; Amami-Ôshima Is.: 1
black arrow) in C to D phase. We believe that the larvae preying on the female, Agina, Setouchi Town, Ôshima District, 28.1610° N, 129.3228°
E, 133 m, 13 IV 2018, KA, YM, AS & ZHS leg. (J18-120A) [NMS]; 1
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Fig. 4. Silba spp. and Wiebeia fig wasps from the syconium of Ficus thunbergii, Amami-Ôshima Island, the Ryukyu Islands, Japan (J18-127B). A: Fly eggs between
ostiolar bracts of the syconium; B: hatched or unhatched fly eggs (arrows: unhatched egg); C: fly larvae feeding on fig wasp or syconium tissue (white arrow:
predation of an adult female fig wasp inside a fig gall; black arrow: feeding on syconium tissue); D: adult male fig wasps predated by fly larvae (arrows: abdomen
from which internal organs were lost).
female, Nishikomi, Setouchi Town, Ôshima District, 28.2382° N, 3 females: BRH]. Chiayi County: 2 males, 1 female, along Dadungshan
129.1604° E, 54 m, 13 IV 2018, same collectors as the former (J18-133) Walkway, Meishan Township, 23.5022° N, 120.7137° E, 1,678 m, 4 IX
[NSMT]; 2 males, Amami City, 28.3003° N, 129.4724° E, 159 m, 14 IV 2018, KA, AS, ZHS & TEFP leg. (TW18-277A) [1 male, 1 female: NMS; 1
2018, same collectors as the former (J18-151A) [NMS]. Okinawa male: BRH]. Ex. Ficus thunbergii. JAPAN. Kagoshima Pref.:
Pref.: Okinawa-jima Is.: 1 male, 1 female, near Mt. Terukubi, Yakushima Is.: 2 males, 3 females, Miyanoura, Yakushima Town,
Kunigami Village, Kunigami District, 26.7614° N, 128.2574° E, 358 m, Kumage District, 30.4127° N, 130.5659° E, 30 m, 20 VII 2018, KA leg.
2 VII 2018, KA leg. (OK18-1E) [NMS]; Tokashiki-jima Is.: 2 females, (J17-647 J) [2 males, 2 females: NMS; 1 female: BRH].
Tokashiki, Tokashiki Village, Shimajiri District, 26.2044° N, 127.3549° Distribution. JAPAN: Honshu (Wakayama Pref.), Shikoku (Kôchi
E, 169 m, 5 V 2018, KA leg. (J18-441I) [1 female: NMS; 1 female: BRH]; Pref.), Ryukyu Islands (Yakushima Is., Amami-Ôshima Is., Okinawa-
Kume-jima Is.: 1 male, Zenda, Kume-jima Town, Shimajiri District, jima Is., Tokashiki-jima Is., Kume-jima Is., Ishigaki-jima Is.). TAIWAN:
26.3206° N, 126.8039° E, 46 m, 25 IV 2018, KA leg. (J18-216C) [NMS]. Taoyuan City, Yilan County, Chiayi County.
TAIWAN. Taoyuan City: 3 males, 4 females, along Northern Cross- New records from the all islands, except for Honshu and Ishigaki-
County Highway, Hualing Village, Fuxing District, 24.6515° N, jima Island (Fig. 1). This species is widely distributed from mainland
121.4177° E, 1,289 m, 27 VIII 2018, KA, AS, ZHS & TEFP leg. (TW18- Japan to Taiwan and from 30 to 1700 m in altitude.
29A) [2 males, 2 females: NMS; 1 male, 2 female: BRH]; 1 male, 3 Host plant. Ficus erecta Thunb. var. erecta (MacGowan and
females, same tree as the former (TW18-29B) [1 male: NMS; 3 females: Okamoto, 2013) and Ficus thunbergii Maxim. (new record).
BRH]; 2 males, same tree as the former (TW18-29C) [1 male: NMS; 1 Bionomics. Females were often observed flying around, alighting
male: BRH]; 2 males, 2 females, same tree as the former (TW18-29D) [2 on, and walking on syconia of F. erecta (Fig. 5A). On finding the en-
males: NMS; 2 females: BRH]; 3 females, same tree as the former trance to the syconia (ostiole) in the C phase (Fig. 5B), oviposition took
(TW18-29F) [1 female: NMS; 2 females: BRH]; 1 male, along Northern place in the ostiolar bracts (Fig. 5C). On hatching, the larvae moved to
Cross-County Highway, Shuanyuan, Fuxing District, 24.6446° N, the interior of the syconia (Fig. 5D: black arrows). The oviposition
121.4442° E, 1,094 m, 27 VIII 2018, KA, AS, ZHS & TEFP leg. (TW18- behaviours observed were generally similar to those noted for Silba
32A) [1 male: NMS;]; 4 male, 3 females, same tree as the former adipata (Katsoyannos, 1983). It took approximately 10 days for adults
(TW18-32D) [1 male, 2 females: NMS; 3 males, 1 female: BRH]; 1 male, to emerge after pupation.
4 females, along Northern Cross-County Highway, Shuanyuan, Fuxing The larvae of S. inubiwa prey on fig wasps (Okamoto et al., 2012;
District, 24.6448° N, 121.4443° E, 1,101 m, 27 VIII 2018, KA, AS, ZHS MacGowan and Okamoto, 2013), as do those of Silba ischnopoda
& TEFP leg. (TW18-33A) [1 male, 1 female: NMS; 3 females: BRH]. MacGowan and Compton, 2018 (MacGowan and Compton, 2018).
Yilan County: 7 males, 9 females, along Northern Cross-County Okamoto et al. (2012) reported that larvae of Silba sp. (=Silba inubiwa)
Highway, Sidauban, Datong Township, 24.6309° N, 121.4826° E, fed on adult female Blastophaga nipponica Grandi, 1922 on syconia of F.
1,224 m, 27 VIII 2018, KA, AS, ZHS & TEFP leg. (TW18-39A) [1 male, 3 erecta. The Silba larvae in the syconia of F. thunbergii were observed
females: NMS; 2 males, 6 females: BRH]; 2 males, 2 females, same data preying on both adult female and adult male fig wasps (Fig. 4C: white
as the former, (TW18-40A) [1 male, 1 female: NMS; 1 male, 1 female: arrow). The larvae fed mainly on the internal organs within the abdo-
BRH]; 1 female, same tree as the former (TW18-40B) [BRH]; 4 males, 3 mens of male wasps, entering from the ventral aspect (Fig. 4D: arrows).
females, same tree as the former, (TW18-40C) [2 males: NMS; 2 males, The fig wasp species associated with F. erecta in Taiwan was
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Fig. 6. Puparium of Silba ishigaki MacGowan and Okamoto, 2013 (TW18-262A). A: Normal empty puparium from which an adult fly emerged; B: empty puparium
due to predation by the larva of a staphylinid beetle (arrow: hole opened by the larva to enter the puparium).
previously thought to be B. nipponica (Chen and Chou, 1997). However, former (TW18-262C) [NMS].
subsequent analysis of sequence data suggested that the Taiwanese Distribution. JAPAN: Ryukyu Islands (Ishigaki-jima Is.). TAIWAN:
population of B. nipponica and two other fig wasp species (Blastophaga Chiayi County.
taiwanensis Chen and Chou, 1997 and Blastophaga tannoensis Chen and New record from Taiwan (Fig. 1).
Chou, 1997) represent a single panmictic population and are distinct Host plant. Ficus variegata Bl. and Ficus benguetensis Merr.
from the Japanese population of B. nipponica (Wachi et al., 2016). These Bionomics. Larvae were collected from fallen syconia of F. var-
Taiwanese species have not yet been revised taxonomically. The Tai- iegata, which contained no fig wasps. Adults emerged during the period
wanese fig wasps from F. erecta must differ from B. nipponica and be 14–17. IX. 2018. Beetle larvae of the family Staphylinidae attacked
assigned to B. taiwanensis based on the nomenclature. Otherwise, the fig several pupae, making entry holes to predate the pupae (Fig. 6). They
wasp species associated with F. thunbergii is considered to be an un- left the puparium after consuming the contents (Fig. 6B).
described species of Wiebesia Bouček, 1988 (Yokoyama and Iwatsuki, MacGowan and Okamoto (2013) found larvae of S. ishigaki in sy-
1998). In conclusion, the larvae of S. inubiwa are currently believed to conia of F. variegata, which contained no fig wasps, in the B (receptacle)
prey on three fig wasp species: B. nipponica, B. taiwanensis, and Wiebesia phase and suggested that the larvae fed on the tissue of fresh syconia.
sp. (also see the bionomics of Silba thunbergii). We assumed that syconia damaged by larvae feeding in the B phase had
fallen to the ground without ripening, and that the larvae kept feeding
on the syconia tissue regardless of status of the syconia.
Silba ishigaki MacGowan and Okamoto, 2013
Silba ishigaki MacGowan and Okamoto, 2013: 198 (original de- Declaration of Competing Interest
scription; type locality: Ishigaki-jima Island, Ryukyu Islands, Japan).
Material examined. 4 males, 5 females, along Neishan Road, Fanlu The authors declare that they have no known competing financial
Township, Chiayi County, Taiwan, 23.3640° N, 120.6115° E, 546 m, 3 interests or personal relationships that could have appeared to influ-
IX 2018, KA, AS, ZHS & TEFP leg., ex. Ficus variegata (TW18-262A) [3 ence the work reported in this paper.
males, 3 females: NMS; 1 male, 2 females: BRH]; 1 male, 1 female, same
tree as the former (TW18-262B) [NMS]; 3 males, same tree as the
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