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Research Article
Monomorium sahlbergi Emery, 1898 (Formicidae, Hymenoptera): a cryptic globally introduced species
expand article infoPeter Boer, Ana Carolina Loss§|, Frederique Bakker, Kevin Beentjes, Brian L. Fisher§
‡ Naturalis Biodiversity Center, Leiden, Netherlands
§ California Academy of Sciences, San Francisco, United States of America
| National Institute of the Atlantic Forest, Santa Teresa, Brazil
Open Access

Abstract

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.

Keywords

CO1, invasive species, Monomorium dichroum, Monomorium pharaonis

Introduction

Broadening transport networks and rising demand for commodities have led to increases in alien species worldwide (Hulme 2009), including ants (Suarez et al. 2001; Bertelsmeier et al. 2017). In the Netherlands, for example, a relatively large number of non-native ant species are being recorded owing in part to the shipments of plant material imported into the country (Boer and Vierbergen 2008).

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 (Boer et al. 2018). Many of these introduced species are poor colonisers and have not been able to establish and/or spread after arriving (Boer and Vierbergen 2008). The actual number of introduced species is almost certainly greater; some specimens are impossible to identify due to a lack of suitable identification keys and uncertainty about the origin of the ants. Limited identification tools and training increase the chances that species names are ascribed incorrectly, especially in the case of closely related species. In this work we describe an example of one invasive species remaining hidden in the guise of another, more common species. The case concerns two closely related species of the genus Monomorium, of which one, M. pharaonis (Linnaeus, 1758), is considered the most notorious pest ant species in the world (Wetterer 2010). In the Netherlands, M. pharaonis is the first recorded tramp ant species; the oldest specimen is dated 1877 (Boer and Vierbergen 2008).

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 13). Monomorium dichroum was reported as only known from India (type locality) (Imai et al. 1984, Bharti 2015) and China (Guénard and Dunn 2012).

Figure 1. 

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.

Figure 2. 

Monomorium dichroum, syntype from Mumbai, India. Worker, CASENT0908718 A frontal view B lateral view C dorsal habitus.

Figure 3. 

Monomorium sahlbergi, syntype from Jericho, Palestine. Worker, CASENT0904576 A frontal view B lateral view C dorsal habitus.

Materials and methods

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 1) and reported as lengths or indices. All measurements are in millimetres. The numeric characters and abbreviations are defined below.

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

DNA sampling

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 Fisher and Smith (2008). All sequences are available at GenBank and Appendix 1. Phylogenetic analyses also included 20 Monomorium sequences from GenBank and two sequences as outgroup (Huberia striata and Podomyrma sp.), see Appendix 1 for sequence details.

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.

Results

CO1

The phylogenetic tree recovered sequences of M. dichroum and M. sahlbergi in the same clade (Fig. 5), showing low within-clade genetic distance (1.0%). Genetic distance among sequences previously identified as M. dichroum and M. sahlbergi was also low (1.3%). All M. pharaonis sequences clustered together, showing 0.3% within genetic distance and 16.5% genetic distance between this and the M. dichroum + M. sahlbergi clade.

Morphological comparisons

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 Bolton (1987). For a detailed description of M. pharaonis see Heterick (2006). Morphometrically M. sahlbergi is similar to M. pharaonis (Table 1). Compared to the workers of M. pharaonis, 1/4 instead of 2/3 of the first gastral tergite (abdominal segment 4) is light-coloured; the structure of the frontal side of the head is strigulate rather than reticulate; the mesonotal groove is shallower; the pronotum and metanotum are higher than the propodeum in M. pharaonis as opposed to equally high in M. sahlbergi and promesonotal setae are missing on the mesosoma, in M. pharaonis two to six (Figs 14). Note that in Monomorium specimens the setae are quite stiff and break easily, thus reducing utility of this character in some specimens.

Table 1.

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 Bolton 1987
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
Figure 4. 

Monomorium pharaonis from Nampar Macing, Indonesia. Worker, CASENT0171086 A frontal view B lateral view C dorsal habitus.

Figure 5. 

Maximum likelihood phylogeny of Monomorium COI sequences. Blue clade corresponds to M. sahlbergi and green clade to M. pharaonis. Values associated to nodes correspond to bootstrap values.

Taxonomic implications

Monomorium sahlbergi Emery

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.

Distribution

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. 6).

Figure 6. 

Distribution of Monomorium sahlbergi. White circles represent interceptions; orange circle represents type locality. Details of map locations are given in Appendix 2.

Discussion

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.

Acknowledgements

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).

References

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Appendix 1

Monomorium and outgroups COI sequences information. Asterisks (*) in the final column indicate duplicated haplotypes not included in the phylogeny.

Species Specimen ID number Geographical region GenBank accession number BOLD process ID number
Monomorium aithoderum Australia KJ847507
Australia KJ847472
Australia KJ847473
Monomorium emarginatum USA KR783702
USA MG458955
Monomorium exiguum CASENT0135941-D01 Madagascar MT887664 ASNAU286-09
CASENT0145058-D01 Madagascar MT887665 ASNAU751-09
CASENT0147596-D01 Madagascar MT887669 ASNAU850-09 *
Monomorium fieldi Australia JQ846291
Australia JQ846292
Monomorium floricola CASENT0136664-D01 Comoros GU709847 ASANO792-09
Costa Rica KC418239 ACGAJ207-11
Monomorium minimum USA KX687942
USA KX687943
Monomorium pharaonis Africa KJ847499
Costa Rica KC419188 ACGAJ043-11
Korea KC407745
CASENT0078602-D01 Madagascar GU710435 ASANP639-09
CASENT0120402-D01 Madagascar GU710434 ASANP651-09 *
CASENT0120437-D01 Madagascar GU710437 ASANP653-09 *
CASENT0120835-D01 Madagascar GU710436 ASANP657-09 *
CASENT0122487-D01 Madagascar GU710439 ASANP666-09 *
CASENT0122499-D01 Madagascar GU710438 ASANP667-09 *
CASENT0123480-D01 Madagascar GU710441 ASANP675-09 *
CASENT0125050-D01 Madagascar GU710440 ASANP679-09
CASENT0159459-D01 Seychelles HQ546947 ASAND352-10 *
CASENT0159472-D01 Seychelles HQ546950 ASAND355-10 *
CASENT0160217-D01 Seychelles HQ546997 ASAND421-10 *
CASENT0160424-D01 Seychelles HQ547018 ASAND445-10 *
CASENT0161400-D01 Seychelles HQ547092 ASAND546-10 *
CASENT0162033-D01 Seychelles HQ547099 ASAND557-10
CASENT0162075-D01 Seychelles HQ547102 ASAND560-10
USA JX402725
USA KC617835 DIRTT037-11
Monomorium rothsteini Australia KC572958
Australia KC572978
Monomorium sahlbergi RMNH.5082323 Israel MT943758 MONOM001-20
CASENT0118484-D01 Madagascar MT887671 ASAMY032-07
CASENT0121143-D01 Madagascar GU709866 ASANO669-09
CASENT0122926-D01 Madagascar GU709869 ASANO683-09
CASENT0122935-D01 Madagascar GU709868 ASANO684-09 *
CASENT0122940-D01 Madagascar GU709871 ASANO685-09 *
CASENT0122947-D01 Madagascar GU709870 ASANO686-09
CASENT0122966-D01 Madagascar GU709873 ASANO687-09
CASENT0122991-D01 Madagascar GU709872 ASANO688-09 *
CASENT0124847-D01 Madagascar GU709875 ASANO692-09
CASENT0009847-D01 New Zealand MT887667 ASAMI149-07
CASENT0125184-D01 Reunion MT887663 ASAMY578-07
Monomorium sahlbergi CASENT0125194-D01 Reunion MT887660 ASAMY580-07 *
CASENT0125332-D01 Reunion MT887666 ASAMY588-07
CASENT0125334-D01 Reunion MT887662 ASAMY590-07 *
CASENT0125339-D01 Reunion MT887661 ASAMY591-07 *
RMNH.5082322 Netherlands MT943757 MONOM002-20
CASENT0191347-D01 USA (Hawaii) MT887670 ASANE610-10
CASENT0191348-D01 USA (Hawaii) MT887668 ASANE611-10 *
Monomorium sordidum Australia KC573031
Australia KJ956922
Monomorium stictonotum Australia KJ847503
Monomorium termitobium CASENT0157182-D01 Madagascar JN283174 ASANH122-10
Huberia striata New Zealand FJ824424
Podomyrma sp. Australia DQ353334

Appendix 2

Distribution details of the mapped specimens of Monomorium sahlbergi.

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
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