Trophic Associations of Ants with Aphid Partners and New Distribution Records of some Ants in Pothwar Region of Pakistan
Trophic Associations of Ants with Aphid Partners and New Distribution Records of some Ants in Pothwar Region of Pakistan
Ammara Gull-E-Fareen1, 3, Imran Bodlah1*, Muhammad Tariq Rasheed1, Yasir Niaz2, Muhammad Adnan Bodlah2, Muhammad Asif4 and Nasir M. Khokhar5
1Insect Biodiversity and Conservation Group, Department of Entomology, Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, Pakistan
2Fareed Biodiversity and Conservation Centre, Department of Agricultural Engineering, Khawaja Fareed University of Engineering and Information Technology, Rahim Yar Khan, Punjab, Pakistan
3Department of Environmental Sciences, Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi, Pakistan
4Agricultural Linkages Program (ALP), Pakistan Agricultural Research Council, Islamabad, Pakistan
5Natural Sciences Linkages Programme, Pakistan Science Foundation Islamabad
ABSTRACT
Ants are the economically important and metropolitan insects on earth. They act as soil engineers, scavengers, decomposers, predators, pollinators and herbivores. The mutualistic relationship between ants and aphids is a very common and widespread phenomenon. It has been studied in various parts of the world. In this relationship, aphids provide food to the ants, while in return ants provide them protection from natural enemies. Ants also protect aphids from different diseases. Aphids (serious crop pests) can be divided into myrmecophilous and non- myrmecophilous. The main objective of this study was to determine trophic associations of ants associated with aphids on various host plants in Pothwar. For this purpose, seven ant species were selected, identified as Camponotus compressus (Fabricius, 1787), Formica fusca Linnaeus, 1758, Formica clara Forel, 1886, Lepisiota frauenfeldi (Mayr, 1855), Myrmica aimonissabaudiae Menozzi, 1939, Tapinoma melanocephalum (Fabricius, 1793) and Tetraponera allaborans (Walker, 1859). A lot of surveys were conducted during 2015-17 for the collection of ants associated with aphids on different host plants in different localities of Pothwar region. As a result of surveys, ant-aphid new mutualistic trophic associations were determined like Camponotus compressus with 12, Formica fusca 1, Formica clara 2, Lepisiota frauenfeldi 9, Myrmica aimonissabaudiae 4, Tapinoma melanocephalum 11 and Tetraponera allaborans with 1 new association in various localities of Pothwar on different host plants have been reported. All these associations are recorded for the first time from Pakistan. Trophic associations of studied ants with aphids on different host plants, their world distribution and comments on observed new associations have been given. New distribution records of ant’s species have also been provided.
Article Information
Received 10 May 2019
Revised 23 July 2019
Accepted 01 October 2019
Available online 30 November 2020
Authors’ Contribution
AGF and MTR surveyed, collected and identified aphids and ants. IB planned and compiled the research. YN, NMK and MA wrote the manuscript. MAB helped in aphid species confirmation.
Key words
Mutualism, Ant, Aphid, Distribution, Pakistan
DOI: https://dx.doi.org/10.17582/journal.pjz/20190510120507
* Corresponding author: [email protected]
0030-9923/2021/0001-0101 $ 9.00/0
Copyright 2021 Zoological Society of Pakistan
INTRODUCTION
Ants (Hymenoptera: Formicidae) are the economically important and metropolitan insects on earth. Formicidae is divided into 20 subfamilies (Bolton, 1994; Bolton et al., 2006; Ward, 2007). Ants are good in seed dispersal (Hanzawa et al., 1988). They improve soil aeration (Holldobler and Wilson, 1990). They are known as ecosystem engineers as they are active in underground activities (Folgarait, 1998). They also perform different roles in ecosystem like scavengers, decomposers, predators, pollinators and herbivores. Harvester ants grow fungus in their nest by accumulating leaves and also feed on them (Holldobler and Wilson, 1990). Ants consume honey dew secretions of aphids in symbiotic association (Styrsky and Eubanks, 2007; Jahn and Beardsley, 1996). There is a mutualistic association between ants and aphids (Depa and Węgierek, 2011). In this relationship, aphids provide food to the ants, while in return ants provide them protection from natural enemies (Sudd, 1987; Cushman and Beattie, 1991). Ants also protect aphids from different diseases e.g. Formica podzolica protect aphids, Aphis asclepiadis, from lethal fungal infections (Nielsen et al., 2010). Flatt and Weisser (2000) reported that aphids associated with ants lived longer, had higher rate of reproduction and greater number of progeny (Yoo and Holway, 2011).
Among mutualisms, ant-aphid interactions are among the most variable in terms of their outcomes whether or not the ant aphid interaction is beneficial to the aphids often depends upon both the spatial and ecological context. Aphids, the serious insect pests of various crops, fruits, vegetables etc. are myrmecophilous (tended by ants) and non- myrmecophilous (unattended). The great majority of ants taking part in such associations belong to phylogenetically advanced sub-families Dolichoderinae, Formicinae and Myrmicinae (Delabie, 2001). The mutualistic relationship between ants and aphids has been the subject of many studies on various aspects of this phenomenon in various regions of the world. In different regions like Iran, 21 ant species associated with 26 aphid species from 37 host plant species (Mortazavi et al., 2015), 18 ants species associated with 34 species of aphids from Florida (Nielsson et al., 1971), 10 species of ants associated with 24 aphid species from Russia (Addicott, 1979), 23 species of ants associated with 11 aphid species from Oceania (Idechiil et al., 2007), 16 species of ants in association with 19 species of aphids from Ankara Province of Turkey (Özdemir et al., 2008), 17 species of ants associated with aphids in Indonesia (Herwina et al., 2013), 20 species of ants associated with 3 species of aphids in India (Kataria and Kumar, 2013) etc. But as far as Pakistan is concerned, recently a lot of work on both aphids (Bodlah et al., 2013, 2017; Amin et al., 2017a, b; Maryam et al., 2019) and ants (Bodlah et al., 2016, 2017, 2019) has been done but on mutualistic associations are still missing. Recently Bodlah et al. (2017) reported first association of a psyllid, Trioza fletcheri minor crawford, 1912 with two ants species in Pothwar, there is no report on aphids and their mutualistic ants in Pakistan. To fulfill this gap and provide a base for further studies on interactions between aphids and ants, the present study was conducted.
MATERIALS AND METHODS
Ant-aphid collection and preservation
Surveys of Attock, Chakwal, Rawalpindi, Islamabad and Jehlum were conducted for the collection of ants and aphids from different host plants during 2015-17. Ants were collected from aphid infested crop plants, grasses, trees, weeds, ornamentals, fruits, vegetables etc. Only those ant-aphid pairs were collected where we observed ants stroke the aphids with their antennae, stimulating them to release the honeydew. Ants were collected with aspirator and through hand picking, were killed and preserved in 75 % ethanol in small glass vials. Aphids were collected and preserved in 75 % ethanol in small glass vials. Longitude and latitudes of the surveyed areas were determined with the help of GPS device.
Identification of ant-aphid partners
Ants were mounted on triangular cards and pinned. Large ants were preserved by using entomological pins. These specimens were identified by using compound microscope and identification keys by Bingham (1903). Aphids were identified using keys by Blackman and Eastop (1994, 2000). Host plants inhabiting ants and aphids were also collected and identified to develop the mutualistic association among ants, aphids and host plants of aphids. The voucher specimens have been deposited in the Museum collection of Department of Entomology, PMAS-AAUR.
RESULTS AND DISCUSION
Seven different species of ants belonging to seven different genera were associated with different aphid partners on various host plants in different areas of Pothwar region. All associations are new. New distribution records for ants have also been added.
1. Camponotus compressus (Fabricius, 1787)
Aphid partners in association reported during these studies in Pakistan
Black bean aphid (Aphis fabae Scopoli, 1763), Fox glove aphid (Aulacorthum solani Kaltenbach, 1843), Pomegranate Aphid (Aphis punicae Passerini, 1863), Thistle aphid (Brachycaudus cardui Linnaeus, 1758), Woolly Apple Aphid (Eriosoma lanigerum Hausmann, 1802), Mustard Aphid (Lipaphis erysimi Kaltenbach, 1843), Ornate Aphid (Myzus ornatus Laing, 1932), Hemp aphid (Phorodon cannabis Passerini, 1860), Bird cherry-oat aphid (Rhopalosiphum padi Linnaeus, 1758), Wheat aphid (Schizaphis graminum Rondani, 1852), Grain Aphid (Sitobion avenae Fabricius, 1794), Safflower Aphid (Uroleucon carthami Hille Ris Lambers, 1948).
Material examined
40☿, Rawalpindi: N33֯ 38.929’ E073֯ 04.943’ 1671 ft. elev., 02-12-2015 Triticum aestivum (Wheat), 2☿, N33֯ 38.929’ E073֯ 04.943’ 1645 ft. elev., 01-01-2016 Parthenium hysterophorus (Parthenium weed), Duranta erecta (Golden dewdrop), Bougainvillea spectabilis (Paperflower), Moringa oleifera (Moringa), Cannabis sp. (Hemp); 38☿, Islamabad: N33֯ 40.527’ E073֯ 08.376’ 1762 ft. elev., 03-09-2015 Zea mays (Maize), Triticum aestivum (Wheat), Solanum nigrum (Black nightshade), Spinacia oleracea (Spinach), Parthenium hysterophorus (Parthenium weed), Capsicum annuum (Green Chilly), Abelmoschus esculentus (Okara), Asclepias sp. (Milk weed), Punica granatum (Pomegranate), 3☿, N33֯ 42.558’ E073֯ 01.330’, 1686 ft. elev., 20-11-2015 Bougainvillea spectabilis (Paperflower), Jasminum officinale (Jasmine); 15☿, Murree: N33֯ 59.652’ E073֯ 28.593’ 4980 ft. elev., 28-11-2015 Spinacia oleracea (Spinach), Jasminum officinale (Jasmine), Parthenium hysterophorus (Parthenium weed), Debregsia silicifolia (Siharu); 5☿, N33֯ 55.341’ E073֯ 24.216’ 6302 ft. elev., 09-01-2017 Fragaria ananassa (Strawberry); 2☿, N33֯ 55.016’ E073֯ 23.699’ 6415 ft. elev., 28-11-2015 Carthamus oxycanthus (Wild Safflower), Quercus ilex (Holly oak); 6☿, N33֯ 59.342’ E073֯ 28.573’ 5020 ft. elev., 09-01-2016 Fragaria ananassa (Strawberry), Viola odorata (Sweet violet), Artemisia absinthium (Wormwood), Helianthus annuus (Sunflower), Bischofia javanica (Bishop wood); 14☿, Chakwal: N32֯ 46.160’ E072֯ 42.299’, 2209 ft. elev., 29-09-2015 Eriobotrya japonica (Loquat), Parthenium hysterophorus (Parthenium weed); 10☿, Jhelum: N32֯ 58.118’ E073֯ 41.601’, 859 ft. elev., 15-04-2016 Parthenium hysterophorus (Parthenium weed), Rosa indica (Rose).
Comments on ant-aphid associations
This ant has been reported in association with 5 aphid species namely Aphis craccivora (Kataria and Kumar, 2013; Rakhshan and Ahmad, 2015), Aphis fabae (Kataria and Kumar, 2013), Aphis gossypii (Verghese and Tandon, 1987; Kataria and Kumar, 2013; Lokeshwari et al., 2015), Aphis nerii (Kataria and Kumar, 2013) and Myzus persicae (Kataria and Kumar, 2013) from various parts of the world on different host plants. Here we have added new associations of this species with 12 different aphid partners from Pakistan. Camponotus compressus was found in abundance in association with 12 aphid species on Triticum aestivum (Wheat), Parthenium hysterophorus (Parthenium weed), Duranta erecta (Golden dewdrop), Bougainvillea spectabilis (Paper flower), Moringa oleifera (Moringa) and Cannabis sp. (Hemp) from various localities of district Rawalpindi. On Zea mays (Maize), Triticum aestivum (Wheat), Solanum nigrum (Black night shade), Spinacia oleracea (Spinach), Parthenium hysterophorus (Parthenium weed), Capsicum annuum (Green Chilly), Abelmoschus esculentus (Okara), Asclepias sp. (Milk weed), Punica granatum (Pomegranate), Bougainvillea spectabilis (Paper flower) and Jasminum officinale (Jasmine) from different locations of Islamabad. On Spinacia oleracea (Spinach), Jasminum officinale (Jasmine), Parthenium hysterophorus (Parthenium weed), Debregsia silicifolia (Siharu), Fragaria ananassa (Strawberry), Carthamus oxycanthus (Wild Safflower), Quercus ilex (Holly oak), Viola odorata (Sweet violet), Artemisia absinthium (Wormwood), Helianthus annuus (Sunflower) and Bischofia javanica (Bishop wood) from Murree, Eriobotrya japonica (Loquat) and Parthenium hysterophorus (Parthenium weed) from district Chakwal and Parthenium hysterophorus (Parthenium weed) and Rosa indica (Rose) from areas of district Jhelum. It was found on the tree trunks and barks tending aphids for honey dew secretion. All the collected specimens were identified and found similar to published description of Bingham (1903). Camponotus compressus is reported for the first time in association with any aphid species from Pakistan, so it is reported as new country record.
Comments on distribution of camponotus compressus in Pakistan
Umair et al. (2012) mentioned the distribution of this species only from Islamabad and Rawalpindi. We have added new distribution records in various localities of Pothwar.
2. Formica fusca Linnaeus, 1758
Aphid partners in association reported during these studies in Pakistan
Pine aphid (Cinara orientalis Takahashi, 1925)
Material examined
20☿, (Kuldana) N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 15-04-2017 Pinus wallichiana (Himalayan pine); 10☿, Murree: (Aliote) N33֯ 55.689’ E073֯ 24.957’, 6042 ft. elev., 15-04-2017 Pinus wallichiana (Himalayan pine); 13☿ , (Kuldana) N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 04-05-2017 Pinus wallichiana (Himalayan pine); 15☿, Murree: (Chara Pani) N33֯ 51.013’ E073֯ 19.156’, 3809 ft. elev., 11-11-2016 Pinus wallichiana (Himalayan pine).
Comments on ant-aphid associations
This species has been recorded to be associated with 57 aphid species from various parts of the world as reviewed by Siddiqui et al. (2019). During our studies, 1 new trophic association of this species with aphid, Cinara orientalis was observed. This association is new country record from Pakistan. This ant species was observed and found in abundance on the pine tree Pinus wallichiana (Himalayan pine) in association with Cinara orientalis. Both the ants and aphids were present in the lenticels of the tree. Aphids were sucking sap from tree trunk and ants were getting honey dew from aphids. All the collected specimens were identified and found similar to the published description of species by Bingham (1903).
Comments on distribution of Formica fusca in Pakistan
Menozzi (1939) reported this species from Karakorum (Province Gilgit-Baltistan). During our surveys, new distribution pattern in Murree (Province Punjab) has been added.
3. Formica clara Forel, 1886
Aphid partners in association reported during these studies in Pakistan
Pine aphids (Cinara confinis (Koch, 1856), (Cinara orientalis (Takahashi, 1925)
Material examined
15☿, Murree: (Kuldana) N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 15-04-2017 Abies pindrow (Pindrow fir); 3☿, (Hill Dhuloo): N33֯ 58.513’ E073֯ 29.703’, 5198 ft. elev., 21-4-2017 Abies pindrow (Pindrow fir); 5☿, (Kuldana): N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 15-04-2017 Pinus wallichiana (Himalayan pine); 20☿, Murree: (Aliote) N33֯ 55.689’ E073֯ 24.957’, 6042 ft. elev., 15-04-2017 Pinus wallichiana (Himalayan pine); 5☿, (Kuldana): N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 04-05-2017 Pinus wallichiana (Himalayan pine); 7☿, Murree (Chara Pani): N33֯ 51.013’ E073֯ 19.156’, 3809 ft. elev., 11-11-2016 Pinus wallichiana (Himalayan pine).
Comments on ant-aphid associations
Siddiqui et al. (2019) mentioned this ant species to be in association with 8 aphid species from the world. During these studies, new associations with 2 aphid species have been added.
Formica clara was found in association with two aphid species namely, Cinara confinis and Cinara orientalis on Abies pindrow (Pindrow fir) and Pinus wallichiana (Himalayan pine) trees. Both aphids and ants were present in the lenticels on the tree trunks. All the collected specimens were identified and found similar to the published species description of Bingham (1903). Formica clara is reported for the first time in association with any aphid species from Pakistan.
Comments on distribution of Formica clara
Seifert and Schultz (2009) mentioned only its distribution in Pakistan but not the exact localities were reported. Here we have added exact localities of its distribution in Pothwar region of Pakistan.
4. Lepisiota frauenfeldi (Mayr, 1855)
Aphid partners in association reported during these studies in Pakistan
Loquat aphid (Aphis eugeniae van der Goot), Giant bark willow aphid (Tuberolachnus salignus (Gmelin, 1776), Wild fig aphid (Greenidea (Greenidea) ficicola (Takahashi, 1921), Greenidea aphid (Greenidea (Trichosiphum) formosana (Maki, 1917), Greenidea aphid (Greenidea (Greenidea) decaspermi Takahashi), Apple aphid (Aphis pomi de Geer), Crepe myrtle aphid (Tinocallis kahawaluokalani (Kirkaldy), Chrysanthemum aphid (Macrosiphoniella sanborni (Gillette), Mint aphid (Ovatus crataegarius), Cotton Aphid (Aphis gossypii Glover, 1877), Black bean aphid (Aphis fabae Scopoli, 1763).
Material examined
10☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-02-2016 Eriobotrya japonica (Loquat); 5☿, Islamabad: N33֯ 39.656’ E073֯ 23.047’, 3327 ft. elev., 19-03-2016 Eriobotrya japonica (Loquat); 4☿, N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 01-03-2016 Eriobotrya japonica (Loquat); 7☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-03-2016 Eriobotrya japonica (Loquat); 4☿, N33 40.527’ E073 08.376’ 1762 ft. elev., 03-03-2016 Eriobotrya japonica (Loquat); 5☿, Rawalpindi: N33 38.929’ E073 04.943’ 1645 ft. elev., 11-03-2016 Salix sp. (Willow); 4☿, Islamabad: N35 40.527’ E072 08.376’ 1763 ft. elev., 13-04-2016; 10☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-03-2016 Salix sp. (Willow); 15☿, Attock: N32֯ 56.655’ E072֯ 51.312’, 1663 ft. elev., 09-03-2016 Salix sp. (Willow); 6☿, Rawalpindi: N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 24-04-2016; Ficus sp. (Fig): 2☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-04-2016 Ficus sp. (Fig); 7☿, Islamabad: N33֯ 43.929’ E073֯02.179’ 3836ft. elev., 17-04-2016 Ficus sp. (Fig); 5☿, Rawalpindi: N33 38.929’ E073 04.943’ 1671 ft. elev., 14-04-2016 Eugenia jambolana (Jaman); 2☿, N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 24-04-2016 Eugenia jambolana (Jaman); 8☿, Murree: N33 55.341’ E073 24.216’ 6302 ft. elev., 09-04-2016 Eugenia jambolana (Jaman); 4☿, Kalar-Kahar: N32֯ 46.138’ E072֯ 42.537’, 2153 ft. elev., 12-04-2016 Eugenia jambolana (Jaman); 6☿, Jhelum: N32 58.119’ E073 41.602’, 859 ft. elev., 15-04-2016 Eugenia jambolana (Jaman); 3☿, Islamabad: N33 40.527’ E073 08.376’ 1762 ft. elev., 23-02-2016 Eugenia jambolana (Jaman); 2☿, Rawalpindi: Ns33 38.929’ E073 04.943’ 1645 ft. elev., 12-03-2016 Psidium guajava (Guava); 12☿, Islamabad: N33 40.527’ E073 08.376’ 1762 ft. elev., 03-04-2016 Psidium guajava (Guava); 5☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-02-2016 Eriobotrya japonica (Loquat); 3☿, Islamabad: N33֯ 39.656’ E073֯ 23.047’, 3327 ft. elev., 19-03-2016 Eriobotrya japonica (Loquat); 2☿, N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 01-03-2016 Eriobotrya japonica (Loquat); 6☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-03-2016 Eriobotrya japonica (Loquat); 3☿, N33 40.527’ E073 08.376’ 1762 ft. elev., 03-03-2016 Eriobotrya japonica (Loquat), 3☿, Rawalpindi: N33֯ 39.655’ E073֯ 23.047’, 3323 ft. elev., 09-03-2016 Malus pumila (Apple); 5☿, Islamabad: (Pir Suhawa) N33֯ 43.929’ E073֯02.179’ 3836ft. elev., 17-3-2016 Malus pumila (Apple); 6☿, Rawalpindi: N33 38.929’ E073 04.943’ 1645 ft. elev., 17-08-2016 Lagerstromia indica (Crepe myrtle); 8☿, Islamabad: N33֯ 43.929’ E073֯02.179’ 3836ft. elev., 27-07-2016 Lagerstromia indica (Crepe myrtle); 5☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-09-2015 Lagerstromia indica (Crepe myrtle); 3☿, Jhelum: N32 58.118’ E073 41.601’, 850 ft. elev., 15-07-2016 Lagerstromia indica (Crepe myrtle), 8☿, Rawalpindi: N32 38.928’ E074 04.943’ 1640 ft. elev., 21-03-2016 Chrysanthemum indicum (Chrysanthemum flower); 5☿, Islamabad: N33 40.527’ E072 08.375’ 1760 ft. elev., 3-04-2016 Chrysanthemum indicum (Chrysanthemum flower); 2☿, Rawalpindi: N34֯ 38.612’ E073֯ 04.470’ 1730 ft. elev., 09-03-2016 Chrysanthemum indicum (Chrysanthemum flower); 9☿, Attock: N32֯ 56.655’ E072֯ 51.312’, 1663 ft. elev., 09-03-2016 Chrysanthemum indicum (Chrysanthemum flower); 4☿, Murree: N33 59.652’ E073 28.593’ 4980 ft. elev., 28-04-2016; 7☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-09-2015 Chrysanthemum indicum (Chrysanthemum flower), 4☿, Murree: N33 55.016’ E073 23.699’ 6415 ft. elev., 28-03-2016 Mentha longifolia (Mint).
Comments on ant-aphid associations
According to Shiran et al. (2013), this species has trophic association with 11 different aphid partners. Siddiqui et al. (2019) mentioned this ant species to be in association with 2 aphids.
In our studies, 9 new ant aphids’ trophic associations have been added. This ant was most abundantly found in association with aphids on a large number of host plant species. It was found associated with 11 aphid species on different plant species including Mentha longifolia (Mint), Chrysanthemum indicum (Chrysanthemum flower), Lagerstromia indica (Crepe myrtle), Malus pumila (Apple), Eriobotrya japonica (Loquat), Psidium guajava (Guava), Eugenia jambolana (Jaman), Ficus sp. (Fig) and Salix sp. (Willow) from different areas of district Rawalpindi, Jhelum, Chakwal, Attock, Murree and Islamabad. It was the most active species found in association with aphids. All the collected specimens were identified and found similar to the published description of species by Bingham (1903). Lepisiota frauenfeldi is reported for the first time in association with any aphid species from Pakistan, so it is added as new country record.
Comments on distribution of Lepisiota fraunfieldi in Pakistan
Umair et al. (2012) recorded this species only from Rawalpindi and Islamabad. New locality records have been added during these studies.
5. Myrmica aimonissabaudiae Menozzi, 1939
Aphid partners in association reported during these studies in Pakistan
Black bean aphid (Aphis fabae Scopoli, 1763), wild rose aphid (Chaetosiphon (Pentatrichopus) glabrum David, Rajasingh and Narayanan, 1971), Pine aphids (Cinara confinis (Koch, 1856), (Cinara orientalis (Takahashi, 1925).
Material examined
11☿, (Kuldana) N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 15-04-2017 Rumex dentatus (Jangli Palak); 4☿, (Aliote) N33֯ 55.689’ E073֯ 24.957’, 6042 ft. elev., 15-03-2017 Rosa brunonii (Himalayan Musk Rose); 3☿, (Osia) N33֯ 55.318’ E073֯ 24.209’, 5027 ft. elev., 25-03-2017 Rosa brunonii (Himalayan Musk Rose); 18☿, Murree: N33֯ 43.255’ E073֯ 02.150’, 4861 ft. elev., 02-03-2016; N33 59.652’ E073 28.593’ 4980 ft. elev., 28-03-2016 Rosa brunonii (Himalayan Musk Rose); 3☿, N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 11-03-2017 Rosa brunonii (Himalayan Musk Rose); 2☿, N33֯ 55.318’ E073֯ 24.209’, 5027 ft. elev., 15-03-2017 Rosa brunonii (Himalayan Musk Rose); 12☿, Murree: (Kuldana) N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 15-04-2017 Abies pindrow (Pindrow Fir); 2☿, (Hill Dhuloo) N33֯ 58.513’ E073֯ 29.703’, 5198 ft. elev., 21-4-2017 Abies pindrow (Pindrow Fir); 2☿, (Kuldana) N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 15-04-2017 Pinus wallichiana (Himalayan Pine); 22☿, Murree: (Aliote) N33֯ 55.689’ E073֯ 24.957’, 6042 ft. elev., 15-04-2017 Pinus wallichiana (Himalayan Pine); 3☿, (Kuldana): N33֯ 55.315’ E073֯ 24.212’, 6324 ft. elev., 04-05-2017 Pinus wallichiana (Himalayan Pine); 7☿, Murree: (Chara Pani) N33֯ 51.013’ E073֯ 19.156’, 3809 ft. elev., 11-11-2016 Pinus wallichiana (Himalayan Pine).
Comments on ant-aphid associations
This species has not been recorded from the world in association with aphids. During our studies 4 novel association of this species were observed for the first time in different localities of Pakistan.
Myrmica aimonissabaudiae was found in association with Aphis fabae, Chaetosiphon (Pentatrichopus) glabrum, Cinara confinis and Cinara orientalis on a number of host plant species including Pinus wallichiana (Himalayan Pine), Abies pindrow (Pindrow Fir), Rosa brunonii (Himalayan Musk Rose) and Rumex dentatus (Jangli Palak) from different areas of Chara Pani, Kuldana, Aliote, Hill Dhuloo and Osia from district Rawalpindi. All the collected specimens were identified and found similar to the published description of Bingham (1903). Myrmica aimonissabaudiae is reported for the first time in association with any aphid species from Pakistan as well as from the whole world, so it is new country as well as new to science association.
Comments on distribution of Myrmica aimonissabaudiae in Pakistan
Menozzi (1939) reported this species only from 2 localities, Karakorum (Gilgit Baltistan Province), Gund (Sindh Province) of Pakistan. Here we reported it for the first time from Pothwar region of Pakistan.
6. Tapinoma melanocephalum (Fabricius, 1793)
Aphid partners in association reported during these studies in Pakistan
Loquat aphid (Aphis eugeniae van der Goot), Giant bark willow aphid (Tuberolachnus salignus (Gmelin, 1776), Wild fig aphid (Greenidea (Greenidea) ficicola Takahashi, 1921, Greenidea aphid (Greenidea (Trichosiphum) formosana (Maki, 1917), Greenidea aphid (Greenidea (Greenidea) decaspermi Takahashi), Apple aphid (Aphis pomi de Geer), Crepe myrtle aphid (Tinocallis kahawaluokalani (Kirkaldy), Chrysanthemum aphid (Macrosiphoniella sanborni (Gillette), Black Bean Aphid (Aphis fabae solanella Theobald, 1914), Cotton Aphid (Aphis gossypii Glover, 1877), Mint aphid (Ovatus crataegarius), Black bean aphid (Aphis fabae Scopoli, 1763).
Material examined
8☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-02-2016 Eriobotrya japonica (Loquat); 5☿, Islamabad: N33֯ 39.656’ E073֯ 23.047’, 3327 ft. elev., 19-03-2016 Eriobotrya japonica (Loquat); 2☿, N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 01-03-2016 Eriobotrya japonica (Loquat); 7☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-03-2016 Eriobotrya japonica (Loquat); 3☿, N33 40.527’ E073 08.376’ 1762 ft. elev., 03-03-2016 Eriobotrya japonica (Loquat); 5☿, Rawalpindi: N33 38.929’ E073 04.943’ 1645 ft. elev., 11-03-2016 Salix sp. (Willow); 3☿, Islamabad: N35 40.527’ E072 08.376’ 1763 ft. elev., 13-04-2016; 6☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-03-2016 Salix sp. (Willow); 2☿, Attock: N32֯ 56.655’ E072֯ 51.312’, 1663 ft. elev., 09-03-2016 Salix sp. (Willow). 5☿, Rawalpindi: N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 24-04-2016; Ficus sp. (Fig): 2☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-04-2016 Ficus sp. (Fig); 5☿, Islamabad: N33֯ 43.929’ E073֯02.179’ 3836ft. elev., 17-04-2016 Ficus sp. (Fig); 4☿, Rawalpindi: N33 38.929’ E073 04.943’ 1671 ft. elev., 14-04-2016 Eugenia jambolana (Jaman); 4☿, N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 24-04-2016; Eugenia jambolana (Jaman); 7☿, Murree: N3355.341’ E073 24.216’ 6302 ft. elev., 09-04-2016 Eugenia jambolana (Jaman); 5☿, Kalar-Kahar: N32֯ 46.138’ E072֯ 42.537’, 2153 ft. elev., 12-04-2016 Eugenia jambolana (Jaman); 3☿, Jhelum: N32 58.119’ E073 41.602’, 859 ft. elev., 15-04-2016 Eugenia jambolana (Jaman); 7☿, Islamabad: N33 40.527’ E073 08.376’ 1762 ft. elev., 23-02-2016 Eugenia jambolana (Jaman); 3☿, Rawalpindi: N33 38.929’ E073 04.943’ 1645 ft. elev., 12-03-2016 Psidium guajava (Guava); 6☿, Islamabad: N33 40.527’ E073 08.376’ 1762 ft. elev., 03-04-2016 Psidium guajava (Guava); 2☿, Rawalpindi: N33֯ 38.612’ E073֯ 04.476’ 1733 ft. elev., 09-02-2016 Eriobotrya japonica (Loquat); 8☿, Islamabad: N33֯ 39.656’ E073֯ 23.047’, 3327 ft. elev., 19-03-2016 Eriobotrya japonica (Loquat); 2☿, N33֯ 39.516’ E073֯23.007’, 2153 ft. elev., 01-03-2016 Eriobotrya japonica (Loquat); 4☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-03-2016 Eriobotrya japonica (Loquat); 4☿, N33 40.527’ E073 08.376’ 1762 ft. elev., 03-03-2016 Eriobotrya japonica (Loquat); 5☿, Rawalpindi: N33֯ 39.655’ E073֯ 23.047’, 3323 ft. elev., 09-03-2016 Malus pumila (Apple); 2☿, Islamabad: (Pir Suhawa) N33֯ 43.929’ E073֯02.179’ 3836ft. elev., 17-3-2016 Malus pumila (Apple); 6☿, Rawalpindi: N33 38.929’ E073 04.943’ 1645 ft. elev., 17-08-2016 Lagerstroemia indica (Crepe myrtle); 3☿, Islamabad: N33֯ 43.929’ E073֯02.179’ 3836ft. elev., 27-07-2016 Lagerstroemia indica (Crepe myrtle); 6☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-09-2016 Lagerstroemia indica (Crepe myrtle); 4☿, Jhelum: N32 58.118’ E073 41.601’, 850 ft. elev., 15-07-2016 Lagerstroemia indica (Crepe myrtle), 8☿, Rawalpindi: N32 38.928’ E074 04.943’ 1640 ft. elev., 21-03-2016 Chrysanthemum indicum (Chrysanthemum flower); 2☿, Islamabad: N33 40.527’ E072 08.375’ 1760 ft. elev., 3-04-2016 Chrysanthemum indicum (Chrysanthemum flower); 7☿, Rawalpindi: N34֯ 38.612’ E073֯ 04.470’ 1730 ft. elev., 09-03-2016 Chrysanthemum indicum (Chrysanthemum flower); 10☿, Attock: N32֯ 56.655’ E072֯ 51.312’, 1663 ft. elev., 09-03-2016 Chrysanthemum indicum (Chrysanthemum flower); 5☿, Murree: N33 59.652’ E073 28.593’ 4980 ft. elev., 28-04-2016; 7☿, Chakwal: N32 46.160’ E072 42.299’ 2209 ft. elev., 29-09-2016 Chrysanthemum indicum (Chrysanthemum flower); 3☿, Islamabad: N33 40.527’ E073 08.376’ 1762 ft. elev., 03-09-2016 Solanum nigrum (Black nightshade); 6☿, Rawalpindi: N32 38.928’ E074 04.943’ 1640 ft. elev., 21-05-2016 Cassia fistula (Amaltas); 8☿, Islamabad: N33 40.527’ E073 08.376’ 1762 ft. elev., 03-09-2016 Parthenium hysterophorus (Parthenium weed), Capsicum annuum (Green Chilly), Abelmoschus esculentus (Okara); 3☿, Rawalpindi: N33 38.929’ E073 04.943’ 1671 ft. elev., 02-11-2015 Eriobotrya japonica (Loquat); N33 38.929’ E073 04.943’ 1645 ft. elev., 01-01-2017 Parthenium hysterophorus (Parthenium weed), Duranta erecta (Golden dewdrop); 6☿, Chakwal: N32 46.160’ E072 42.299’, 2209 ft. elev., 29-09-2016 Eriobotrya japonica (Loquat); 10☿, Murree: N33 55.016’ E073 23.699’ 6415 ft. elev., 28-02-2016 Mentha longifolia (Mint).
Comments on ant-aphid associations
This ant species has been recorded in association with 4 aphid species namely, Aphis gossypii, Hysteroneura setariae, Myzus persicae and Pentalonia nigronervosa as reviewed by Siddiqui et al. (2019). Here we added 11 new trophic associations of this ant with different aphids on different host plants. Tapinoma melanocephalum was most abundantly found in association with aphids on a large number of host plants. It was found associated with 12 aphids species on Mentha longifolia (Mint), Parthenium hysterophorus (Parthenium weed), Duranta erecta (Golden dewdrop), Capsicum annuum (Green Chilly), Abelmoschus esculentus (Okara), Cassia fistula (Amaltas), Solanum nigrum (Black nightshade), Chrysanthemum indicum (Chrysanthemum flower), Lagerstroemia indica (Crepe myrtle), Malus pumila (Apple), Eriobotrya japonica (Loquat), Psidium guajava (Guava), Eugenia jambolana (Jaman), Ficus sp. (Fig) and Salix sp. (Willow), from different locations of District Rawalpindi, Islamabad, Attock, Jhelum and Chakwal. All the collected specimens were identified and found similar to the species description of Bingham (1903). Tapinoma melanocephalum is reported for the first time in association with any aphid species from Pakistan, so it is added to the country’s fauna as new record.
Comments on distribution of Tapinoma melanocephalum in Pakistan
Wetterer (2009) recorded this ant from Karachi (Sindh Province) of Pakistan. During our studies
new distribution records have been added from various localities of Pothwar (Punjab Province). This species is reported for the first time in Punjab.
7. Tetraponera allaborans (Walker, 1859)
Aphid partners in association reported during these studies in Pakistan
Willow aphid (Chaitophorus sp.)
Material examined
8☿, Rawalpindi (Neela Sand): N33֯ 54.762’E072֯ 28.237’ 993 ft, 1846 ft. elev., 13-04-2016 Salix sp. (Willow); 5☿, Rawalpindi (Neela Sand): N33֯ 54.762’E072֯ 28.237’ 993 ft, 1846 ft. elev., 3-05-2016 Salix sp. (Willow plant); 15☿, Rawalpindi (Neela Sand): N33֯ 54.762’E072֯ 28.237’ 993 ft, 1846 ft. elev., 13-04-2017 Salix sp. (Willow plant); 5☿, Rawalpindi (Neela Sand): N33֯ 54.762’E072֯ 28.237’ 993 ft, 1846 ft. elev., 23-05-2017 Salix sp. (Willow plant).
Comments on ant-aphid associations
This species has been reported in new association with aphid for the first time in the world. Previously it was not reported with any association with aphids. Tetraponera allaborans was found associated with Willow aphid (Chaitophorus sp.) on Salix sp. (Willow plant) from Neela Sand area of district Rawalpindi. This ant along with aphid was present on the branches of willow plant. Ants were collecting honey dew from aphids. All the collected specimens were identified and found similar to the description of Bingham (1903). Tetraponera allaborans is reported for the first time in association with any aphid species from Pakistan, so it is added as new country record.
DISCUSSION
Mutualistic association of ants and aphids has been a topic of interest by various ecologists and taxonomists of the world in the history and recent years. Mutualism is a fundamental element in aphid-ant communities, found within various aphid-ant groups and formulates the species richness, abundance and distribution (Styrsky and Eubanks, 2007). Understanding of the aphid-ant associations generally provides patterns of aphid-ant species complexes in different ecological zones. There is a need of more studies related with taxonomy and ecology for better understanding of aphid-ant associations (Siddiqui et al., 2019).
Camponotus compressus with 12, Formica fusca with 1, Formica clara with 2, Lepisiota frauenfeldi with 9, Myrmica aimonissabaudiae with 4, Tapinoma melanocephalum with 11 and Tetraponera allaborans with 1 new associations on various host plants have been reported for the first time from Pakistan. Prior to our studies, only faunal work on aphids and ants separately has been done. These studies will provide baseline for further studies on patterns of ant-aphid mutualistic associations in various ecological zones of Pakistan leading towards their interactions with other communities of ecosystem. New distribution of studied ant species have been added in Punjab province, previously recorded from other provinces.
ACKNOWLEDGMENTS
We are grateful to Pakistan Science foundation for funding under the project PSF/NSLP/P-UAAR (313) for these findings.
Statement to conflict of interest
The authors declare there is no conflict of interest.
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