Biology and Distribution of Palaeolindbergiella simlae (Crawford, 1912) (Hemiptera: Psyllidae) along with its Associations with Ants from Pothwar Region of Pakistan
Biology and Distribution of Palaeolindbergiella simlae (Crawford, 1912) (Hemiptera: Psyllidae) along with its Associations with Ants from Pothwar Region of Pakistan
Imran Bodlah1*, Muhammad Tariq Rasheed1, Muhammad Farooq Nasir1,
Tariq Mahmood2 and Muhammad Asif3
1Insect Biodiversity and Conservation Group, Department of Entomology, Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi
2Department of Environmental Sciences, Pir Mehr Ali Shah Arid Agriculture University, Rawalpindi
3Agricultural Linkages Program (ALP), Pakistan Agricultural Research Council, Islamabad
ABSTRACT
Psyllids (Hemiptera: Psylloidea) are small insects and belong to sucking group of insects. Palaeolindbergiella simlae (Crawford, 1912) belongs to this group and is a serious pest of Bauhinia variegate Linn. The Genus Palaeolindbergiella Heslop-Harrison, 1961 has only 3 species records from the world. Immature stages of this species are 5 which have been described with the help of coloured micro-graphs. Male and female genitalia have been described using line drawings and coloured drawings. Main diagnostic characters, brief description, morphometrics, distribution and illustrations are provided. Biology, trophic associations with 4 ant’s species namely, Camponotus parius, Camponotus compressus, Tapinoma melaocephalum, Lepisiota fraunfeldi have been discussed. Four natural enemies; two species of syrphid flies namely, Allobaccha apicalis (Loew, 1858), Allobaccha sapphirina (Wiedemann, 1830), two species of Coccinellid beetles, Coccinella septempunctata (Coleoptera: Coccinellidae), Menochilus sexmaculatus (Fabricius, 1781) and Chrysoperla carnea (Stephens, 1836) (Chrysopidae: Neuroptera) were found to be the bio-control agents of P. simlae.
Article Information
Received 04 September 2019
Revised 01 November 2020
Accepted 20 November 2020
Available online 09 April 2021
(early access)
Published 24 January 2022
Authors’ Contribution
IB, MTR, MFNand TM designed research and performed experiments.
MA wrote the manuscript.
Key words
Distribution, Immatures, Palaeolindbergiella simlae, Pakistan
DOI: https://dx.doi.org/10.17582/journal.pjz/20190904150911
* Corresponding author: [email protected]
0030-9923/2022/0002-0845 $ 9.00/0
Copyright 2022 Zoological Society of Pakistan
INTRODUCTION
Psyllids or jumping plant-lice (Hemiptera: Sternorrhyncha) are phloem-feeding tiny insects belonging to superfamily Psylloidea and can be further classified into eight families: Aphalaridae, Carsidaridae, Calophy-idae, Homotomidae, Liviidae, Phacopteronidae, Psyllidae and Triozidae according to new classification (Burckhardt and Ouvrard, 2012). These tiny creatures are phytophagous pests being sucking insects resulting in galling making, leaf curling and sooty mould development. On other side they are also considered as vectors of many diseases in various crops like citrus, pear, apple, plum, potato, and tomato (Aubert, 1987; Hodkinson, 2009). They have also been used as bio-control agents of mosquitoes and various alien plant species especially against weeds in various parts of the world like mosquito psyllids in Australia (van Klinken et al., 2003; Donnelly, 2002) and Melaleuca psyllid is being used against its host plant, Melaleuca quiquenervia (Paper bark tree, native to Australia but a serious invasive weed tree in Florida). Both adult and immature (Nymph) of pysllids are phytophagous, nymphs secrete honey dew which is feed by various species of bees, ants and wasps (Mathur, 1975). Psyllid species are most common in forest areas and over 100 species have been recorded as feeding on trees and vegetation growing in forest areas (Mathur, 1975). Up till now, 4000 species have been described throughout the world (Li, 2011) and this number has doubled now according to Burckhardt and Ouvrard (2012) but as far as Pakistan is concerned only a little work has been done on exploration of these entities in Pakistan Bodlah et al. (, , , .
Genus Palaeolindbergiella Heslop-Harrison, 1961 was proposed as a subgenus of genus Lindhergiella by Heslop-Harrison (1961). Genus Palaeolindbergiella Heslop-Harrison, 1961 can be recognized by the combination of following characters: Pterostigma of the wing longer and narrower, labium much longer than other member of psyllinae; legs long, well developed and metatarsus with two basal spines (Heslop-Harrison, 1961). According to Ouvrard (2019) 3 species of genus Palaeolindbergiella Heslop-Harrison, 1961 has been reported from the world. Out of these, Palaeolindbergiella primitiva Heslop-Harrison, 1961 is a type species reported from African region (Heslop-Harrison, 1961). Other two namely, P. simlae (Crawford, 1912) and P. thakrei (Mathur, 1973) are reported from India (Crawford, 1912; Mathur, 1973). Palaeolindbergiella simlae (Crawford, 1912) has been classified under the genus Psylla. Currently Burckhardt (2018) revised this species with new combination under genus Palaeolindbergiella. Here we report this species for the first time from Pakistan with the description of immatures and adult, trophic associations with ants and natural enemies.
MATERIALS AND METHODS
Adult psyllid collection and identification:
For collection of adult psyllids, wide range surveys were conducted. Different areas of Rawalpindi and Islamabad were visited during February to May for the collection of Palaeolindbergiella simlae. Adults were collected with the help of nylon made insect collection nets and preserved in small glass vial, and then preserved in 75% ethyl alcohol. Temporary slides of collected specimens were made and identified under the Labomed microscope. Measurements were done by using stage microscope. Adult specimens were micro-graphed under Labomed microscope (CZS6, Labo America, Inc. USA). LEICA MS 5 (Leica Microsystems (Switzerland) Ltd) microscope attached with Amscope 18 megapixel camera (Amscope, China) was used also for microphotography.
Immature stages collection and identification
Immatures stages of psyllid were also collected preserved in 75% ethyl alcohol. They were processed for identification by methods used by Bodlah et al. (2017a). Slide preparation protocal as described by Bodlah et al. (2017b) was used. Permanent slides were prepared and observed under Noif (XSZ-107BN). Stage and ocular meters were used for measurement. Illustrations were processed in Helicon Focus 6 and Adobe Photoshope CS6 (Adobe Inc. USA). Lines drawing of taxonomically important parts were also drawn with the help of ocular grid.
Collection of ants and natural enemies
Those ants were collected which were observed stroking Psyllids immatures with their antennae, stimulating them to release the honeydew on Bauhinia variegata Linn leaves. Ants were collected with aspirator and through hand picking, were killed and preserved in 75 % ethanol in small glass vials. These specimens were identified by using compound microscope and identification keys by Bingham (1903). Adult syrphids, coccinellids and green lacewing were identified by comparing the reference collection of Museum of Department of Entomology, PMAS-AAUR. For confirmation of their role as predators, heavily infested leaves of Bauhinia variegata with the attack of Psyllids were brought to the laboratory and they were reared under laboratory conditions up-till emergence of adults of natural enemies.
Palaeolindbergiella simlae (Crawford, 1912)
First nymphal instar (Fig. 1A)
Body ranges from 0.31 to 0.42 mm. Antennae shorts, two-segmented, with one sensorium, rudiments of wing-pads represented by weak projections bearing one short spatulate seta; abdominal margin with seven pairs of small dagger-shaped setae.
Second nymphal instar (Fig. 1B)
Body ranges from 0.48 to 0.53 mm. Similar to the third instar but with small knob-like wing-pads projecting from the body and bearing single spatulate setae at apex. Antennae 3 segmented with one sensorium on the apical segment. Abdominal margin with three pairs of spatulate and four pairs of dagger-shaped setae.
Third nymphal instar (Fig. 1C)
Body ranges from 0.68 to 0.74 mm. Mostly resembles with resembles the fourth stages excepting antennae 3 segmented having two sensoria on terminal segment.
Fourth nymphal instar (Fig. 1D)
Body ranges from 0.99 to 2.4 mm. This instar is similar to fifth instar excepting following characters: smaller than 5th instar; thoracic and abdomen al sclerites as shown; dorsal derm beset with minute points and ring-based spatulate setae; antennae five-segmented with three sensoria, one on third segment and two simple ring-based setae.
Fifth nymphal instar (Fig. 1E)
Body ranges from 1.47 mm to 1.55mm. The wing pads large, project well beyond the contour of the body. Eyes prominent. Dorsum with the derm membranous over some parts of the body, and the wing-pads, a pair of
large head plates between the eyes and almost the whole of the posterior half of the abdomen heavily sclerotized. There are several small sclerites on the thorax and narrow sclerotic plates on the abdominal segments. Derm slightly vermiculate and sparsely beset with minute points which are stouter on the abdomen. Abdomen sclerites and apical plate also bear minute fringed processes. Apical abdomen plates show traces of segmentation, and minute points. Body covered with scattered, simple, ring based setae as well as with spatulate ones, both of various lengths; the latter are also present on the apical margin of head, along the margin of wing-pads and abdomen. Margin of apical plate armed with eight dagger-shaped setae. Wing-pads also bear minute clavate setae. Posterior margins of hind wing-pad with three to four spatulate setae. Antennae 0.55 mm long, slender; seven-segmented, bearing simple setae. Four sensoria are present on antennae; one on the 3rd, one on the 5th and two on 7th segment. The 3rd antennal segment has a weak construction at about its middle; the terminal segment imbricate bearing two spines at apex. Legs short and stout, bearing simple setae; without trochanter; with distint tibio-tarsal articulation. Each tarsus with a single golf club seta; claws present. Anal opening set well inside from the apex of abdomen and is surrounded by the outer row of silt-like pores and an inner row of small oval pores.
Identification characters of adult
Coloration
Body brownish generally, having light brown appearance on head, legs and antennae, however antennal segments black from apex-terminal segments. Genae of head black. Forewing hyaline, clavus with black spot apically.
Structure
Body smaller, head width almost equal to thorax, entirely rugulose, slightly deflexed with sparsed pubescent. vertex of head distinctly broader, median suture slightly swollen, having short foveae laterally, triangular lobes present at posterior-middle, frontal part weakly rounded, posterior margin angulate, having swollen post ocellar region, emarginated anteriorly, genal cone 0.2 mm longer, almost equal to the length of vertex, with longer setae, subacute apically, weakly pubescent along with sparsed hairs allover. Eyes prominent, backwardly directed to thorax.
Antennae longer, 10 segmented with robust segments at base, segment 3rd longest than remaining, two unequal setae present on terminal segments. Thorax more or less arched, reticulate, having sparsed and fine pubescent; prothorax smaller, backwardly sloped, dorsum of prescutum broader, anterior margin narrow, angular at lateral and posterior margin; scutum almost equal to prescutum in length, dorsum more broader than other, lateral and posterior margin angular. Legs having minute lines arranged smoothly, having fine and sparsed setae throughout, tibiae of legs having irregular setae apically, small basal spure present at hind femur, both sides having a pair of spine, apex of hind tarsal having a pair of black spine at basal face. Fore wing hyaline, transparent, membranous, having broad pterostigma, vein R smaller than basal, Cu smaller, about more than ½ longer than R, cells of marginal area are sub equal, 2nd cell shorter and narrow than 1st cell, veins having small setae throughout. Hindwing somewhat longer, having few setae at costal margin. Abdomen small, pubescent, long setae present at sternite.
Male genitalia
Male terminalia in profile quit smaller than abdominal part, straight anteriorly, weakly convex, slendrical, dorsum of terminalia somewhat as pear shaped, paramere longer about 0.20 mm, sparsed setae present at outer face, hypandrium with few setae sparsely, outer face of aedagus small than inner face, having spoon like structure apically.
Female genitalia
Female terminalia pubescent, smaller, dorsum longer than ventral, descending at caudal region, eight hairs present at middle of genital, whilst peg like setae present apically, ovipositor acute tip.
Measurements
Body length, male, 1.43mm; female, 1.50; length of forewings, male,1.96mm; female 1.51; width of head with eyes, 1.97mm; Width of vertex between eyes, 0.38; length of antennae, 1.20mm.
Material examined
Islamabad, 2-iii-18, 17♂ and 12♀; Rawalpindi, 23-iv-18, 7♂ and 5♀; Kahuta,14-iii-18, 7♂ and9♀; Sihala, Islamabad, 27-iv-18, 10♂ and 12♀; Ayub National Park, 8-iv-18, 6♂ and 7♀; Rawalpindi, 10-iii-18, 11♂ and 8♀; Morgah Biodiversity Park, 22-iii-18, 8♂ and 12♀; Rawalpindi, 9-iii-18, 5♂ and 10♀; Nawaz Sharif Park, 30-iii-18, 4♂ and 9♀; Rawalpindi, PMAS AAUR, 5-iii-18, 7♂ and 9♀; Shahdra Valley, 20-iv-18, 16♂ and 9♀; Islamabad, F-9 Park, 23-iv-18, 7♂ and 5♀; Islamabad, Kachnar Park, Islamabad, 20-iii-18, 8♂ and 4♀.
Host plant
On young and fresh leaves and inside flower buds of Bauhinia variegata Linn.
Distribution
India (Hodkinson, 1983, 1986): Meghalaya (Lahiri and Biswas, 1990), West Himalaya (Mathurn, 1975) and Pakistan (Current studies as new record from Pothwar region of Pakistan).
Trophic association with ants
Kachnar Park, Islamabad, 20-iii-18, 8♂ and 4♀ (Camponotus compressus, Tapinoma melaocephalum); Islamabad, F-9 Park, 23-iv-18, 7♂ and 5♀ (Lepisiota fraunfeldi, Camponotus compressus); Ayub National Park, 8-iv-18, 6♂ and 7♀ (Camponotus compressus, Tapinoma melaocephalum, Lepisiota fraunfeldi); Rawalpindi, PMAS AAUR, 5-iii-18, 7♂ and 9♀ ( Camponotus parius, Camponotus compressus, Tapinoma melaocephalum, Lepisiota fraunfeldi).
Bio-control agents
Two species of syrphid flies namely, Allobaccha apicalis (Loew, 1858), Allobaccha sapphirina (Wiedemann, 1830), two species of Coccinellid beetles, Coccinella septempunctata (Coleoptera: Coccinellidae), Menochilus sexmaculatus (Fabricius, 1781) and Chrysoperla carnea (Stephens, 1836) (Chrysopidae: Neuroptera) were found to be the bio-control agents of P. simlae.
Biology
This species found to be infesting fresh young buds, leaves and flowers. Leaves became sickly and eventually succumb to the attack. Flowers shriveled and drop to the ground. Leaves and flowers shrivel. Heavy infestation resulted in dwarf and stunted young plants.
DISCUSSION
Specimens collected from Pakistan were compared with published description by Mathur (1973) and found to be similar.
Various aphid species have been reported in association with Camponotus compressus (Mortazavi et al., 2015). Shiran et al. (2013) mentioned Lepisiota fraunfeldi to be in mutualistic associations with various aphid species. Tapinoma melaocephalum have been renowned as to be in association with aphids (Zhang et al., 2012; Mortazavi et al., 2015). Mortazavi et al., 2015 reported Camponotus parius as to be in mutualistic association with aphids. Here we report four species of ants in association with Palaeolindbergiella simlae (Crawford, 1912).
ACKNOWLEDGEMENT
These studies are part of the project (CS-111) funded by Pakistan Agricultural Research Council under (ALP). We are thankful to PARC, Islamabad Pakistan.
Statement of conflict of interest
The authors have declared no conflict of interest.
REFERENCES
Aubert, B., 1987. Trioza erytreae Del-Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two vectors of Citrus Greening Disease: Biological aspects and possible control. Fruits, 42: 149-162.
https://doi.org/10.5962/bhl.title.100740
Bodlah, I., Bodlah, M.A., Jahandad, A., Gull-E-Fareen, A. and Akhter, T., 2017b. Genitalia and new host record of Diaphorina Citri Kuwayama (Hemiptera: Liviidae) from different localities of Rawalpindi and Islamabad. Asian J. Agric. Biol., 5: 47-50.
Bodlah, I., Bodlah, M.A., Rasheed, M.T., Akhter, T., Aihetasham, A. and Yousaf, M., 2017a. New distributional records of psyllid, Trioza fletcheri minor crawford, 1912 and record of its first association with two ants species in Pothwar. Asian J. Agric. Biol., 5: 1-5.
Burckhardt, D. and Ouvrard. D., 2012. A revised classification of the jumping plant-lice (Hemiptera: Psylloidea). Zootaxa, 3509: 1-34. https://doi.org/10.11646/zootaxa.3509.1.1
Burckhardt, D., Sharma, A. and Raman, A., 2018. Checklist and comments on the jumping plant-lice (Hemiptera: Psylloidea) from the Indian subcontinent, Zootaxa, 4457: 1-38. https://doi.org/10.11646/zootaxa.4457.1.1
Crawford, D.L., 1912. Indian Psyllidae. Rec. Indian Mus., 7: 419-435. https://doi.org/10.5962/bhl.part.28242
Donnelly, G.P., 2002. The host range and biology of the mesquite psyllid Heteropsylla texana. BioControl, 47: 363-371. https://doi.org/10.1023/A:1014844108894
Heslop-Harrison G., 1961. Hemiptera (Homoptera): Psyllidae. In: Hanström B. 1961-South African animal life: results of the Lund University Expedition in 1950-1951, 8. Sweden, Almqvist and Wiksell, Stockholm, 511: 487-532.
Hodkinson, I.D., 1983. The psyllids (Homoptera: Psylloidea) of the Austro-Oriental, Pacific and Hawaiian zoogeographical realms: An annotated check list. J. nat. Hist., 17: 341-377. https://doi.org/10.1080/00222938300770251
Hodkinson, I.D., 1986. The psyllids (Homoptera: Psylloidea) of the Oriental zoogeographical region: An annotated checklist. J. nat. Hist., 20: 299-357. https://doi.org/10.1080/00222938600770251
Hodkinson, I.D., 2009. Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): A global synthesis. J. nat. Hist., 43: 65-179. https://doi.org/10.1080/00222930802354167
Lahiri, A. R. And Biswas, S., 1990. Further contribution on the psyllids (Insecta: Homoptera) of Assam and Meghalaya with description of new species. Rec. Zool. Surv. India, 86: 485-492.
Li, F., 2011. Psyllidomorpha of China (Insecta: Hemiptera). Huayu Nature Book Trade Co. Ltd. Beijing, China, pp. 1-2.
Mathur, R.N., 1973. On a collection of Psyllidae (Homoptera) from the Indian subregion with descriptions of three new species. Oriental Insects, 7: 515-526. https://doi.org/10.1080/00305316.1973.10434423
Mathur, R.N., 1975. Psyllidae of the Indian Sub-continent. The Indian Council of Agricultural Research, New Delhi, India, pp. 429.
Mortazavi, Z.S., Sadeghi, M., Aktac, N., Depa, L. and Fekrat, L., 2015. Ants (Hymenoptera: Formicidae) and their aphid partners (Homoptera: Aphididae) in Mashhad region, Razavi Khorasan Province, with new records of aphids and ant species for fauna of Iran. Halteres, 6: 4-12.
Ouvrard, D., 2019. Psyl’list–The World Psylloidea Database [WWW document]. URL http://www.hemiptera-databases.com/psyllist.
Shiran, E., Mossadegh, M.S. and Esfandiari, M., 2013. Mutualistic ants (Hymenoptera: Formicidae) associated with aphids in central and southwestern parts of Iran. J. Crop Protec., 2: 1-12.
Van Klinken, R., Fichera, G. And Cordo, H., 2003. Targeting biological control across diverse landscapes: the release, establishment, and early success of two insects on mesquite (Prosopis spp.) insects in Australian rangelands. BioControl, 26: 8-20. https://doi.org/10.1016/S1049-9644(02)00107-X
Zhang, S., Zhang, Y. and Ma, K., 2012. Disruption of ant-aphid mutualism in canopy enhances the abundance of beetles on the forest floor. PLoS ONE, 7: e35468. https://doi.org/10.1371/journal.pone.0035468
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