Research Article |
Corresponding author: Camiel Doorenweerd ( camiel.doorenweerd@hawaii.edu ) Academic editor: Teresa Vera
© 2020 Camiel Doorenweerd, Arni Ekayanti, Daniel Rubinoff.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Doorenweerd C, Ekayanti A, Rubinoff D (2020) The Dacini fruit fly fauna of Sulawesi fits Lydekker’s line but also supports Wallacea as a biogeographic region (Diptera, Tephritidae). ZooKeys 973: 103-122. https://doi.org/10.3897/zookeys.973.55327
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Although there is scientific consensus on most of the major biogeographic regions in the world, the demarcation of the area connecting Southeast Asia with Australia and Oceania remains debated. Two candidate boundaries potentially explain faunistic diversity patterns in the regions: Lydekker’s and Wallace’s lines. The islands in between both ‘lines’ are jointly termed Wallacea, with Sulawesi as the largest landmass. We surveyed Dacini fruit flies (Tephritidae: Dacinae) in Sulawesi between 2016 and 2019 using traps baited with male lures, resulting in 4,517 collected flies. We identified all specimens to species level, which adds 15 new species records to the island, bringing the total number of Dacini species in Sulawesi to 83. The biogeographic affinity of species in the updated checklist reveals a strong connection with former ‘Sunda’ (41% of species); validating Lydekker’s line, but also a high level of endemism (47% of species), confirming the uniqueness of Wallacea as a biogeographic region. We further describe a new species, Bactrocera (Bactrocera) niogreta Doorenweerd, sp. nov. and discuss the taxonomy of several interesting species.
Bactrocera, biogeography, Dacus, pest, taxonomy, Zeugodacus, zoogeographic
Biogeographic boundaries were initially established to indicate stark and sudden differences between faunas of neighboring areas, as noted by early explorers like Alfred Russel Wallace, and proved fundamental to the understanding of tectonic plate movement (
Map of Sulawesi and neighboring areas showing the four sampling localities with orange spots; the three localities in South Sulawesi were in close proximity to each other. Two typical biogeographical boundaries are indicated with dotted lines: Wallace’s line and Lydekker’s line. Land masses west of Wallace’s line were connected during ice ages as Sunda, east of Lydekker’s line land masses were connected as Sahul. Islands in between the two biogeographical boundaries were never connected by land and are jointly known as Wallacea.
Wallace’s line runs south of the Philippines, east of Borneo and continues south between Bali and Lombok (
Dacini fruit flies (Tephritidae: Dacinae) are a tribe of 938 described exclusively Old World species (e.g.,
We collected Dacini flies using handmade bottle traps. A 3 cm-diameter hole was cut 15 cm from the base of a 500 ml plastic water bottle. Male attractant lures: methyl eugenol 10 g cones (Scentry Biologicals Inc., Billings MT, USA), cue lure 2 g cones (Scentry Biologicals Inc., Billings MT, USA), and zingerone (Sigma-Aldrich, St. Louis MO, USA) were individually suspended by a string inside the bottle, 5 cm from the top. A 100 ml water solution of Fisherbrand Sparkleen detergent (Fisher Scientific, Pittsburgh, PA, USA) poured at the bottom of each bottle trap was used as a killing agent. The traps were then hung from a cacao tree (Theobroma cacao L.) branch at 1.5 m high. Traps were checked every 2–5 days, and trapped flies were transferred to 95% ethanol. Trapping was mainly conducted in Wotu, Kabupaten Luwu Timur, South Sulawesi at sites named “Insitu” [WGS84 N 2.5587 E 120.7935], “MCRC Tarengge” [WGS84 N 2.5547 E 120.8047] and “Arni field” [WGS84 N 2.5587 E 120.7935] (Fig.
Planting at Insitu was composed primarily of cacao clones PBC123 and BR25 that were planted 3.5 m apart within a row, with 3.5 m spacing between rows, irregularly shaded by a diversity of fruit trees. This site was the most diversified among the trapping sites, including more than 100 banana (Musa sp.), four large durian tree (Durio sp.), eight rambutan (Nephelium lappaceum L.), six coconut trees (Cocos nucifera L.), as well as some ginger (Alpinia sp.), Luffa (Luffa acutangula L.), papaya (Carica papaya L.), chili peppers (Capsicum sp.) and corns. The cacao trees were not regularly pruned but were treated with an unknown pesticide, and were not artificially irrigated. This farm was surrounded by neighboring cacao farms with a similar diversified composition. In addition, some jackfruit (Artocarpus heterophyllus Lam.), mango (Mangifera indica L.), guava (Psidium guavaja L.), rose apple (Syzygium sp.), as well as breadfruit (Artocarpus altilis (Parkinson) Fosberg) were present around the neighboring farms. The site at MCRC Tarengge represents a 1 ha of cacao trees of clone M01 with a 1.5 × 3 m density, without any other fruit trees within the block. However, several langsat trees (Lansium parasiticum (Osbeck) Sahni & Bennet), banana and a couple of durian trees were present in the neighborhood farms 100 m away from the trapping sites, as well as 20 papaya, 10 rambutan trees (Nephelium lappaceum L.) within 200 m, and several mango trees, jackfruit, guava, and rose apple trees within 400 m radius from the trapping site. No pesticide was applied during our field collection, but both surrounding blocks were regularly treated with pesticides. The site ‘Arni field’ was also mainly composed of cacao trees at lower density (3 × 3 m). Various fruit trees disseminated around the farm, including some banana, rambutans, jackfruit, mangos, guava, and Ambarella (Spondias dulcis L.), with rows of corn (Zea mays L.) and several durian trees within 50 m, as well as jambu putik (Syzygium sp.), rose apple, and breadfruit within 300 m.
In total, the trapping effort at Arni field was approximately four months, five months at MCRC Tarengge, and six and half months at Insitu, spread over different periods during 2016–2019 (Suppl. material
Methods for DNA extraction, PCR primers and conditions, and Sanger sequencing follow those of
We list 83 species of Dacini for Sulawesi (Table
Species | Sulawesi record | Male lure | Insitu | MCRC Tarengge | Arni Field | Manado | Biogeographic affinity |
---|---|---|---|---|---|---|---|
B. abbreviata (Hardy, 1974) | This study | ZN | x | x | Sunda | ||
B. affinibancroftii Drew & Romig, 2013 |
|
ME | Sulawesi endemic | ||||
B. affinidorsalis (Hardy, 1982) |
|
CL | Sunda | ||||
B. albistrigata de Meijere, 1911 |
|
CL | x | x | x | x | Sunda |
B. beckerae (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
B. bifasciata (Hardy, 1982) |
|
CL | Wallacea | ||||
B. bitungiae Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. carambolae Drew & Hancock, 1994 | This study | ME | x | Sunda | |||
B. careofascia Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. commensurata Drew & Romig, 2013 | This study | ME | x | x | x | Sunda | |
B. curvosterna Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. dispar (Hardy, 1982) |
|
– | Sulawesi endemic | ||||
B. dorsalis (Hendel, 1912) |
|
ME | x | x | x | x | Sunda |
B. elongata Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. flavipennis (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
B. flavosterna Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. floresiae Drew & Hancock, 1994 |
|
ME | Sunda | ||||
B. fuscitibia Drew & Hancock, 1994 |
|
CL/ZN* | Sunda | ||||
B. fuscolobata Drew & Romig, 2013 |
|
CL | x | Sulawesi endemic | |||
B. fuscoptera Drew & Romig, 2013 |
|
ME | Sulawesi endemic | ||||
B. hantanae Tsuruta & White, 2001 | This study | CL | x | Sunda | |||
B. infulata Drew & Hancock, 1994 |
|
ME | Sulawesi endemic | ||||
B. involuta (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
B. latifrons (Hendel, 1915) |
|
– | Sunda | ||||
B. limbifera (Bezzi, 1919) |
|
CL | x | x | x | Sunda | |
B. linduensis Drew & Romig, 2013 |
|
CL | x | Wallacea | |||
B. megaspilus (Hardy, 1982) |
|
CL | x | Sulawesi endemic | |||
B. melastomatos Drew & Hancock, 1994 | This study | CL | x | x | x | Sunda | |
B. moluccensis (Perkins, 1939) |
|
CL/ZN | Sunda | ||||
B. nanoarcuata Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. nationigrotibialis Drew & Romig, 2013 |
|
ME | Sulawesi endemic | ||||
B. neoritsemai Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. niogreta Doorenweerd sp. nov. | This study | ZN | x | Sulawesi endemic | |||
B. ochroma Drew & Romig, 2013 |
|
ME | Sunda | ||||
B. pendleburyi (Perkins, 1938) | This study | ZN | x | x | Sunda | ||
B. penebeckerae Drew & Romig, 2013 |
|
– | Wallacea | ||||
B. penecostalis Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. perkinsi (Drew & Hancock, 1981) | This study | CL | x | Sahul | |||
B. pernigra Ito, 1983 | This study | CL | Sunda | ||||
B. propinqua (Hardy & Adachi, 1954) | This study | CL | x | Sunda | |||
B. pseudobeckerae Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
B. ritsemai (Weyenbergh, 1869) |
|
CL | Sunda | ||||
B. splendida (Perkins, 1938) | This study | ZN* | x | Sunda | |||
B. sulawesiae Drew & Hancock, 1994 |
|
ME | Sulawesi endemic | ||||
B. suliae Drew & Romig, 2013 |
|
ME | Wallacea | ||||
B. syzygii White & Tsuruta, 2001 | This study | ZN | x | x | x | Sunda | |
B. terminifer (Walker, 1860) |
|
– | Sulawesi endemic | ||||
B. trifasciata (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
B. umbrosa (Fabricius, 1805) |
|
ME | x | x | x | x | Sunda; Sahul |
B. usitata Drew & Hancock, 1994 | This study | CL | x | Sunda | |||
B. wuzhishana Li & Wang, 2006 |
|
ME | Sunda | ||||
D. donggaliae Drew & Romig, 2013 |
|
CL | Sulawesi endemic | ||||
D. longicornis (Wiedemann, 1830) | Walker 1860; |
CL | x | Sunda | |||
D. melanopectus Drew & Romig, 2013 |
|
ME | Sulawesi endemic | ||||
D. nanggalae Drew & Hancock, 1998 | Drew and Hancock 1998 | CL | Sulawesi endemic | ||||
D. ortholomatus Hardy, 1982 |
|
– | Sulawesi endemic | ||||
D. pedunculatus (Bezzi, 1919) | This study | ZN* | x | x | Sunda | ||
D. pullus (Hardy, 1982) |
|
ZN* | x | Sulawesi endemic | |||
Z. abnormis (Hardy, 1982) |
|
CL | Sunda | ||||
Z. angustifinis (Hardy, 1982) |
|
CL | x | Sulawesi endemic | |||
Z. apicalis (de Meijere, 1911) |
|
CL | x | Sunda | |||
Z. bogorensis (Hardy, 1983) |
|
CL | Sunda | ||||
Z. buruensis (White, 1999) |
|
CL | Wallacea | ||||
Z. connexus (Hardy, 1982) |
|
– | Sulawesi endemic | ||||
Z. cucurbitae (Coquillett, 1899) |
|
CL | x | x | Sunda | ||
Z. dubiosus (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
Z. emittens (Walker, 1860) | Walker 1860; |
CL | Wallacea | ||||
Z. eurylomatus (Hardy, 1982) |
|
– | Sulawesi endemic | ||||
Z. exornatus (Hering, 1941) |
|
CL | x | Sunda | |||
Z. flavipilosus (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
Z. fulvipes (Perkins, 1938) | Hancock and Drew 2017 | CL | Sunda | ||||
Z. hancocki (Drew & Romig, 2013) |
|
CL | Sulawesi endemic | ||||
Z. heinrichi (Hering, 1941) | Hering 1941 | CL/ZN | Sunda | ||||
Z. melanopsis (Hardy, 1982) |
|
CL | Sulawesi endemic | ||||
Z. neoflavipilosus (Drew & Romig, 2013) |
|
CL | Sulawesi endemic | ||||
Z. neolipsanus (Drew & Romig, 2013) |
|
CL | Wallacea | ||||
Z. persignatus (Hering, 1941) |
|
CL | x | Wallacea | |||
Z. proprescutellatus (Zhang Che & Gao, 2011) | This study | CL | x | Sunda | |||
Z. synnephes (Hendel, 1913) |
|
CL | Sunda | ||||
Z. tebeduiae (Drew & Romig, 2013) |
|
CL | Sunda | ||||
Z. transversus (Hardy, 1982) |
|
CL | x | Sulawesi endemic | |||
Z. ujungpandangiae (Drew & Romig, 2013) |
|
CL | Sulawesi endemic | ||||
Z. vargus (Hardy, 1982) |
|
CL | Sulawesi endemic |
We report four new male lure records of species attracted to zingerone: Bactrocera splendida (Perkins, 1938), B. fuscitibia Drew & Hancock, 1994 (attracted to both cue lure and zingerone), Dacus pedunculatus (Bezzi, 1919), and D. pullus (Hardy, 1982). Although the three localities “Insitu”, “MCRC Tarengge” and “Arni Field” are geographically within two kilometers of each other, Insitu had a distinctly higher diversity with 28 species, whereas we only collected ten species at MCRC Tarengge, and nine at the Arni Field, with similar collecting efforts. We collected only four species at the “Manado” site, but this is likely due to less trapping days, and possibly because this was a less forested site just 50 m from the coastline. The major, widely distributed, pest species B. albistrigata (de Meijere, 1911) and B. dorsalis (Hendel, 1912) were present at all sites and made up 70.6 % of all specimens collected (Suppl. material
Below, we describe two new species, provide more information on the first records of B. carambolae for Sulawesi, and discuss the presence of B. melastomatos. We also describe the second specimen ever collected of Dacus pullus, and provide morphological and molecular evidence for two species forms of Dacus longicornis.
Male. Labelled: “Indonesia: Sulawesi: South Sulawesi: Insitu. WGS84 -2.5464 120.7921 16–23.i.2019 Zingerone trap. Leg. Jerome Niogret. DNA sample ms09121”. Deposited at the University of Hawaii Insect Museum (UHIM).
Bactrocera (Bactrocera) niogreta sp. nov. is most similar to B. (Tetradacus) brachycera (Bezzi, 1916), which is known from India, Bhutan, and China (
The COI sequence of Bactrocera niogreta is, in our database, most similar to Bactrocera fuscitibia, which can morphologically easily be distinguished by not having a clearly expanded costal band. The EF1-alpha sequences are most similar to B. enochra (Drew, 1972), which is morphologically different in not having a wide costal band, and has a wide red band medially across the scutum and three longitudinal black bands along the abdomen. Both COI and EF1-alpha are diagnostic to identify B. niogreta (See BOLD Dataset DOI: http://doi.org/10.5883/DS-DACSU).
Head
(Fig.
Zingerone.
Unknown.
The species name is an adjective that refers to instigator of the 2016–2019 Dacini surveys in Sulawesi: Jerome Niogret.
the morphology of B. niogreta overall most closely resembles B. (Tetradacus) brachycera, the combination of a short posterior lobe of the surstylus in the male genitalia and a deep concavity on sternum V support placement in subgenus Bactrocera. In the
Dacus longicornis Wiedemann is a widespread Southeast Asian species that is a minor pest: the larvae feed on Luffa, Trichosanthes and some other Cucurbitaceae (
Two forms of Dacus longicornis 8 D. longicornis collected in Bangladesh, Pabna district, 30-ix-3-x-2013 Leg. M. A. Hossain 9 D. longicornis collected in Bangladesh, Maulvi Bazar Rainforest resort, Leg. L. Leblanc & M. A. Hossain 10 specimen ms08424, collected in Sulawesi, with a faint medial postsutural yellow vitta 11 specimen ms08432, collected in Sulawesi 12 specimen ms08428, collected in Sulawesi 13 specimen ms08421, collected in Sulawesi.
Maximum Likelihood trees based on COI (14) and EF1-alpha (15) DNA sequence data for Dacus longicornis, with D. pullescens Munro and D. vertebratus Bezzi as outgroups. Branch support values are rapid bootstrap values and approximate-likelihood ratio test values, scale bar indicates substitutions per site. Full details on the samples can be found in BOLD dataset DOI: http://dx.doi.org/10.5883/DS-DACSU.
We collected more than 300 specimens with a uniform morphotype that are tentatively included in the checklist as B. melastomatos (Table
Maximum Likelihood trees based on COI (20) and EF1-alpha (21) DNA sequence data for Bactrocera melastomatos and allied species, using B. lombokensis Drew & Hancock and B. digressa Radhakrishnan as outgroup. Branch support values are rapid bootstrap values and approximate-likelihood ratio test values, scale bar indicates substitutions per site. Full details on the samples can be found in BOLD dataset DOI: http://dx.doi.org/10.5883/DS-DACSU.
We collected two specimens of Bactrocera carambolae, both at the Insitu locality, which represent the first records for Sulawesi (Figs
The two specimens of Bactrocera carambolae that represent the first records for Sulawesi, photographed in ethanol (wings were removed) 22 dorsal view of specimen ms08439 23 lateral view of specimens ms08439 24 dorsal view of specimen ms10710 25 lateral view of specimen ms10710. Both specimens have the typical rectangular black mark on the lateral sides of the fourth abdominal segment, but lack the black mark on the fore femur, which can further help to distinguish B. carambolae from B. dorsalis.
We record specimen ms09122 as a representative of Dacus pullus (Figs
Sulawesi is a dispersal crossroads for the biotas of Southeast Asia, Australia, and Oceania. The updated species checklist we present here shows that Sulawesi is unique, with many endemic species, but that there are also strong connections with Southeast Asia, at least for the taxa under study. This finding does not support the earlier working hypotheses that posited a closer connection to the Sahul fauna, including Papua (
It has been advocated by some that the categorization of biogeographic regions should follow more quantitative measures (
As a tropical island, Sulawesi has a rich diversity of fruiting plants and, consequently, insects that utilize them. Our surveys were performed in cacao plantations; the only Dacini that is known to feed on cacao is the polyphagous Bactrocera dorsalis (
We would like to thank Suparmi, Wulan, and Jerome Niogret for their contributions in the insect sampling, and Dan Nitta for his help with the molecular lab work. We are grateful to Luc Leblanc for helping with the identifications of the initial samples that were collected, and we thank Norman Barr for bringing CD and Jerome Niogret into contact. We thank the editor and reviewers for helpful comments that improved the manuscript. Funding for this project was provided by the United States Department of Agriculture (USDA) Farm Bill Section 10007 Plant Pest and Disease Management and Disaster Prevention Program in support of suggestion “Genomic approaches to fruit fly exclusion and pathway analysis”: 3.0497-FY17, FY18 and FY19. These funds were managed by the University of Hawaii’s College of Tropical Agriculture and Human Resources. This material was made possible, in part, by a Cooperative Agreement from the United States Department of Agriculture’s Animal and Plant Health Inspection Service (APHIS). It may not necessarily express APHIS’ views. Additional funding was provided by the USDA Cooperative State Research, Education and Extension (CSREES) project HAW00942-H administered by the College of Tropical Agriculture and Human Resources, University of Hawaii.
Table S1
Data type: preadsheet with trapping records
Explanation note: Table including the lot numbers for each trapping event, fly identification, fly counts, lure used and exact locality.