Research Article |
Corresponding author: Peter Boer ( p.boer@quicknet.nl ) Academic editor: Marek Borowiec
© 2020 Peter Boer, Ana Carolina Loss, Frederique Bakker, Kevin Beentjes, Brian L. Fisher.
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:
Boer P, Loss AC, Bakker F, Beentjes K, Fisher BL (2020) Monomorium sahlbergi Emery, 1898 (Formicidae, Hymenoptera): a cryptic globally introduced species. ZooKeys 979: 87-97. https://doi.org/10.3897/zookeys.979.55342
|
The discovery in the Netherlands in a shipping container of the ant Monomorium sahlbergi Emery, 1898, a species similar to the invasive pharaoh ant M. pharaonis (Linnaeus, 1758), led to a quest to better define the distribution of this species, which was initially obscure due to uncertain specimen identifications. Here it is shown that M. sahlbergi, like M. pharaonis, is found worldwide, almost certainly as a result of introductions. Including quarantine interceptions, this species is recorded from seven global biogeographic regions, but its established outdoor distribution is currently limited to the tropics and subtropics. Monomorium dichroum Forel, 1902 is here presented as a junior synonym of M. sahlbergi syn. nov. based on morphometric and CO1 analyses.
CO1, invasive species, Monomorium dichroum, Monomorium pharaonis
Broadening transport networks and rising demand for commodities have led to increases in alien species worldwide (
A concerted effort is underway to identify ant species introduced into the Netherlands, whether they are established or found during import inspections. Thus far 120 species have been identified (
On 2 June 2014, the pest controller A.J.A. Heetman intercepted ants found in a shipping container at a distribution company in the Netherlands and sent them to the first author. The shipping container, filled with glycine for the food industry, came from a chemical plant in Wuyi, Hengshui, Hebei, China. The intercepted ants appeared similar to the well-known and globally common tramp species M. pharaonis, but differed in their black gaster. While trying to identify the specimens, we came across images of identical specimens on AntWeb (http://www.antweb.org), where they were recorded under the provisional name M. pharaonis_nr (CASENT0173275, CASENT0246074) and M. bicolor complex (CASENT0178876).
Further comparison of our specimens with the images from AntWeb convinced us that the ants discovered in the Hebei shipping container were a previously described species, M. dichroum Forel, 1902 (Figs
Monomorium sahlbergi from Sacramento, USA, imported from Thailand. Worker, CASENT0005783 A frontal view B lateral view C dorsal habitus.
Further exploration of similar species on AntWeb, however, suggested our specimens, and M. dichroum for that matter, were identical to M. sahlbergi Emery, 1898, a little-known species described from Israel. We set out to ascertain the true identity of our specimens and determine whether dichroum and sahlbergi are two distinct species.
Monomorium dichroum, syntype from Mumbai, India. Worker, CASENT0908718 A frontal view B lateral view C dorsal habitus.
Monomorium sahlbergi, syntype from Jericho, Palestine. Worker, CASENT0904576 A frontal view B lateral view C dorsal habitus.
Available descriptions of all Monomorium species occurring in the area between Saudi Arabia in the west and China in the east were consulted. Syntype material of M. dichroum and M. sahlbergi were requested and investigated. Monomorium pharaonis, M. cf. pharaonis, M. nr. pharaonis, and M. bicolor-complex ants identified from the collection of CASC and RMNH were investigated. In total, we examined hundreds of specimens from the Netherlands, France, Germany, Israel, Saudi Arabia, United Arab Emirates, Oman, Yemen, Seychelles, Papua, Nepal, New Zealand, Western Australia, Myanmar, Taiwan, China, Ivory Coast, Cameroon, Madagascar, Indonesia, Panama, Mexico, Trinidad, Netherlands Antilles, and the United States of America.
For morphometrical comparisons, 16 workers of M. pharaonis were examined (all in the collection of Naturalis Biodiversity Center, RMNH). The size and shape characters of these workers were quantified (Table
CI Cephalic Index (CW/CL) ×100.
CL Maximum cephalic length in median line.
CW Maximum cephalic width, across eyes.
EYI Eye Index (maximum eye length / CW) ×100.
Omm Number of ommatidia across the widest diameter of the eye.
PI Petiole Index (Maximum width of petiole / maximum width postpetiole) ×100.
PrI Promesonotal Index (Promesonotal width / CW) ×100.
SI Scape Index (Maximum straight line scape length excluding articular condyle / CW) ×100.
The examined specimens in this study are deposited in the following institutions:
CASC California Academy of Sciences, USA
MHNG Museum d’Histoire Naturelle, Geneva, Switzerland
MSNG Museo Civico di Storia Naturale ‘Giacomo Doria’, Genova, Italy
RMNH Naturalis Biodiversity Center, Leiden, the Netherlands (the former Rijksmuseum van Natuurlijke Historie)
TAMU Texas A & M University, Texas, USA
UCDC R.M. Bohart Museum of Entomology, University of California, Davis, USA
NZAC New Zealand Arthropod Collection, D.S.I.R., Auckland, New Zealand
We sequenced 654 base pairs (bp) of mitochondrial cytochrome oxidase I (COI) gene from 39 Monomorium specimens previously identified as M. pharaonis, M. dichroum, or M. sahlbergi. DNA extraction and COI sequencing were performed at University of Guelph (Ontario, Canada) and Naturalis Biodiversity Center (Leiden, the Netherlands), following the protocol described in
Molecular phylogenetic inference. Sequences were aligned using Geneious 11.1.5 (Biomatters Ltd.). The phylogenetic tree was inferred in MEGA7 using maximum likelihood and 100 bootstrap replicates. Nucleotide substitution model selection and genetic p-distance calculation were also performed using MEGA7 (Kumar and Tamura, 2016). The best fit model selected under the corrected Akaike Information Criteria (AICc) was GTR+G+I.
The phylogenetic tree recovered sequences of M. dichroum and M. sahlbergi in the same clade (Fig.
Monomorium dichroum and M. sahlbergi show similar colouration, especially with regard to the infuscate genae and the light spot on the posterior side of the gaster. Morphometrically, these ants are identical. None of the regression analyses of various morphometrical data, such as cephalic width versus cephalic length, scape length, maximum width of postpetiole, width of postpetiole versus width of petioles, comparisons between the cephalic index versus eye index, versus petiole index, versus scape index, and versus promesonotal index, showed any difference. The number of ommatidia across the widest diameter of the eye was the same. Nor could we find any differences in pilosity and pubescence. The surface sculpturing of the head, mesosoma, nodes, and gaster were the same.
Both Monomorium sahlbergi and M. pharaonis belong to the salomonis group, as defined by
Morphometric data of workers of Monomorium dichroum, M. sahlbergi, and M. pharaonis. Arithmetic mean in parentheses.
M. dichroum (n = 48) | M. sahlbergi (n = 32) | M. pharaonis (n = 16) |
M. pharaonis (n = 50) from |
|
CW | 0.41–0.54 (0.44) | 0.40–0.44 (0.42) | 0.41–0.48 (0.44) | 0.40–0.48 |
CL | 0.49–0.66 (0.54) | 0.49–0.54 (0.51) | 0.52–0.59 (0.56) | 0.52–0.60 |
CI | 79–85 (82) | 79–85 (81) | 75–84 (80) | 73–80 |
EYI | 19–24 (21) | 19–26 (22) | 18–20 (19) | 18–21 |
Omm | 7–10 (9) | 7–11 (9) | 7–9 (8) | 5–7 |
PI | 67–86 (74) | 64–73 (69) | 71–82 (78) | – |
SI | 102–110 (103) | 103–110 (106) | 105–117 (109) | 105–117 |
Monomorium pharaonis from Nampar Macing, Indonesia. Worker, CASENT0171086 A frontal view B lateral view C dorsal habitus.
Monomorium sahlbergi Emery, 1898: 131. Syntype worker, ergatoid queen: [Jerico] Jericho, Palestine (J. Sahlberg) (MSNG; worker, unique specimen code CASENT0904576; ergatoid queen, CASENT0904577) [examined].
Monomorium dichroum Forel, 1902: 212. Syntype workers: Poona, India (Wroughton) (BMNH, CASENT0902222) [examined]; Bombay, India (Wroughton) (MHNG, CASENT0908718) [examined] syn. nov.
All records of M. sahlbergi originate from desert-like, urban, industrial, and military areas ranging from sea level to an elevation of 1800 m. It is not clear from our research what the original geographic region of M. sahlbergi was. Based on the distribution of other species in the salomonis group, the native distribution would include specimens from the Indomalaya region (Nepal, India, Thailand). Our data came from the following main geographic regions: Palearctic (China, Israel, Netherlands (interception)), Australian (New Zealand, from likely interceptions), Nearctic (USA, in part interceptions), Neotropical (Panama, Galapagos), Afrotropical (Reunion, Madagascar) and Oceania (Hawaii) (Fig.
The global distribution of Monomorium sahlbergi suggests a history of introductions. Although the native distribution requires further evaluation, specimen records from disturbed habitats suggest that, like the introduction in the Netherlands, this species has already been introduced to other regions. Some distribution records suggest that M. sahlbergi could indeed be a successful invasive species, and is already successfully established in areas such as disturbed areas on the islands of the Galapagos (Ecuador) and urban areas in Texas, USA, Panama-City, Hawaii, Madagascar, and Reunion.
It is easy to confuse M. sahlbergi with the well-known pharaoh ant M. pharaonis, because the former also lives near or in human settlements and looks very similar to M. pharaonis. Therefore, we suspect that M. sahlbergi has more than once been misidentified as M. pharaonis, a view supported by the misidentifications encountered in this study. These findings suggest that M. sahlbergi is likely more common than we realise.
Without the rich photographic archive and specimen data of AntWeb, this study would not have been possible. We would like to thank all collectors and curators for their assistance, especially A.J.A. Heetman, for initiating this research by providing the specimens from the Netherlands. We thank G. Kapp (The Steinhardt Museum of Natural History, Tel Aviv) for providing us with a sample of M. sahlbergi from Israel, and Alex Wild for his information about M. sahlbergi from Panama. This work was partly supported by US National Science Foundation grant DEB-1655076. ACL was supported by Conselho Nacional Científico e Tecnológico (CNPq, Brazil; grant numbers 306772/2019-1 and 300737/2020-3).
Monomorium and outgroups COI sequences information. Asterisks (*) in the final column indicate duplicated haplotypes not included in the phylogeny.
Map ID number | Locality | Country | Latitude | Longitude |
---|---|---|---|---|
1 | Maui | USA | 20.63 | -156.1 |
2 | Kawaihae | USA | 20.04 | -155.8 |
3 | Elk Grove | USA | 38.41 | -121.3 |
4 | El Paso | USA | 31.76 | -106.4 |
5 | College Station | USA | 30.63 | -96.33 |
6 | Panama City | Panama | 8.98 | -79.52 |
7 | Galapagos | Ecuador | -0.59 | -90.32 |
8 | Rijen | Netherlands | 51.59 | 4.92 |
9 | Jericho | Israel | 31.86 | 35.46 |
10 | Riyadh | Saudi Arabia | 24.71 | 46.68 |
11 | Um-al-Quwain | UAE | 25.52 | 55.71 |
12 | Wadi Maidaq | UAE | 25.35 | 56.09 |
13 | Muscat | Oman | 23.59 | 58.41 |
14 | Socotra | Yemen | 12.46 | 53.82 |
15 | Mumbai | India | 19.08 | 72.88 |
16 | Pune | India | 18.4 | 73.85 |
17 | Belgaum | India | 15.85 | 74.5 |
18 | Coonoor | India | 11.35 | 76.8 |
19 | Odisha | India | 20.95 | 85.1 |
20 | Hetauda | Nepal | 27.44 | 85 |
21 | Fujian | China | 26.48 | 117.92 |
22 | Mahajanga | Madagascar | -15.69 | 46.33 |
23 | Toamasina | Madagascar | -18.14 | 49.4 |
24 | Toliara | Madagascar | -23.35 | 43.69 |
25 | Grotte des Premiers Français | Reunion | -21.02 | 55.26 |
26 | Le Port | Reunion | -20.94 | 55.3 |
27 | Napier Port | New Zealand | -39.48 | 176.91 |
28 | Port Nelson | New Zealand | -41.26 | 173.28 |