Impact of Two Attending Ants, Crematogaster subnuda and Camponotus compressus (Hymenoptera: Formicidae), on the Parasitism of Sugarcane Aphid Melanaphis sacchari (Zehnt.)

Zubair Ahmad1, 2, 4, Hamed A. Ghramh1, 2, 3, Khalid Ali Khan1, 2, 3*, Farhat Khan4 and Shujauddin5

1Research Center for Advanced Materials Science (RCAMS), King Khalid University, P.O. Box 9004, Abha 61413, Saudi Arabia

2Unit of Bee Research and Honey Production, Faculty of Science, King Khalid University, P.O. Box 9004, Abha 61413, Saudi Arabia

3Biology Department, Faculty of Science, King Khalid University, P.O. Box 9004, Abha 61413, Saudi Arabia

4Biology Department, Faculty of Sciences and Arts, King Khalid University, Dhahran Al-Janoub, Saudi Arabia.

5Department of Zoology, Aligarh Muslim University, Aligarh-202002, UP, India

ABSTRACT

The mutualistic relation between ants and aphids is considered as one of the best examples of inter-specific mutualism between species that produces net benefits for the participants. In this paper, the interaction between aphid M. sacchari and their attending ants on sugarcane (Saccharum officinerum) was studied. The presence of ants, especially, Crematogaster subnuda Mayr. and Camponotus compressus adversely affects the parasitoid effectiveness of Lysiphlebia mirzai and Aphelinus desantesi. The aphids got 31% and 26.3% parasitism when attended by C. compressus and C. subnuda Mayr., respectively. Further in the presence of these two dominant species the other ants viz., Paratrechina longicornis (Latr) and Tapinoma melanocephalum (F.) are unable to make contact with the aphids and even chased away on their mere appearance in the vicinity of aphid colony. The vague stimuli via the host in C. subnuda Mayr. causes a phenomenal warning to the other members for searching the invader.

Article Information

Received 09 March 2020

Revised 11 May 2020

Accepted 30 May 2020

Available online 21 September 2020

Authors’ Contribution

ZA and SH conceived the idea of the project. ZA and SH carried out the sampling, analysed the data and wrote the manuscript. KAK contributed in final preparation of the manuscript. HAG, KAK and FK provided suggestions and corrections.

Key words

Behavior, Ants, Parasitoids, Aphids, Melanaphis sacchari

DOI: https://dx.doi.org/10.17582/journal.pjz/20200309190337

* Corresponding author: [email protected]

0030-9923/2020/0006-2389 $ 9.00/0

Copyright 2020 Zoological Society of Pakistan

Aphids and ants are the two abundant and highly successful insect groups, which usually share the same habitat and interact with one another, which is one of the classic examples of a mutualistic relationship (Darwin, 1859; Stadler and Dixon, 2005). The interaction of ants and aphids is of economic importance because of their effects on the host plants. The ants get honeydew from the aphids and in return give manifold protection to them (Way, 1963; Völkl et al., 1999; Flatt and Weisser, 2000; Stadler and Dixon, 2005, 2008; Muller et al., 2016). Firstly, they feed upon the honeydew and provide a check on the growth of saprophytic moulds (Way, 1963). The accumulation of honeydew is harmful to the aphids, but its removal indirectly helping the parasitoids too, since the excess of it along with mould retard oviposition (Nielsen et al, 2010; Henry et al., 2015). Secondly, the attending ants regulate the aphid population, protecting sufficient individuals and chaperone them from parasites and predators (Buckley, 1987; Vinson and Scarborough, 1991; Volkl, 1992, 1997; Stechmann et al., 1996; Novgorodova and Ryabinin, 2017). However, ants do not always benefit aphids and their association can be antagonistic (Stadler and Dixon, 1998; Yao et al., 2000). Hence, it is a prerequisite to study and evaluate the economic significance of the specific ant against the parasitoid of its tended aphid species, before an establishment of the parasitoid is made to combat such pests. Notwithstanding of its great economic importance, the detailed studies on the behavior of any specific ant for the parasitoid of its attended aphids are not available except some fragmentary observations mainly focused on one or few pairs of aphid-ant species (Völkl, 1997; Bronstein and Barbosa, 2002; Stadler and Dixon, 2005; Renault et al, 2004; Sadeghi-Namaghi and Amiri-Jami, 2018; Saha et al., 2018; Siddiqui et al., 2019). However, there is a lack of the knowledge of aphid-ant interaction data from Indian subcontinent except for a few scattered studies (Kurl and Misra, 1980; Kataria and Kumar, 2013). The present work includes detailed observations on the behaviour of Crematogaster subnuda Mayr. and Camponotus compressus Fabr. towards the parasitoids and ants of other genera associated with Melanaphis sacchari (Zehnt.) on Saccharum officinarum L.

 

Materials and methods

The survey of sugarcane fields was conducted every year from July to April (1998-2003) for five years to record the number of different species of ants and their parasitoids associated with aphid M. sacchari in Western Uttar Pradesh. The behaviour of Crematogaster subnuda Mayr. and Camponotus compressus against Paratrechina longicornis (Latr.) and Tapinoma melanocephalum (Fabr.) and parasitoids Lysiphlebia mirzai Shujauddin, and Aphelinus desantesi Hayat was studied in the field. The presence of ants especially Crematogaster subnuda Mayr. and Camponotus compressus and their role on the effectiveness of parasitoids had been established by selecting three plants with healthy aphid populations for parasitoids activity (i) in the presence of Crematogaster subnuda Mayr. (ii) Camponotus compressus and (iii) in the absence of ants. Ten mated females of L. mirzai were released on each plant and after five days 100 aphids were randomly dissected for evaluating % of parasitism in each case and the experiment were repeated three times. The whole experiments were conducted in a screened glasshouse under controlled condition (22 ± 3℃ Tem. 70%-80% R.H.) described by Kennedy and Booth (1954) and El-Ziady (1960). Statistical analyses and significance tests (P <0.05) were performed using STATISTIX, 1998, and the difference among the percentage parasitism of the aphids attended by ants were tested using chi-square test.

 

Results and discussion

The sugarcane aphid M. saccchri is attended by four species of ants, viz. Crematogaster subnuda Mayr., Camponotus compressus, Paratrechina longicornis (Latr.) and Tapinoma melanocephalum (F.). The first two species are found in abundance (66-30%).Throughout, winter Crematogaster subnuda Mayr. is conspicuously in greater number than Camponotus compresus Fabr. With the result that the former does not permit an easy stay of the later in an aphid colony.These two dominant ants do not permit the other two species Paratrechina longicornis (Latr.) and Tapinoma melanecephalum (F.) to develop contact with the aphids so much so that they are chased away on their mere appearance in the vicinity. The ants dislike the parasitoids and markedly decrease their efficiency is supported from the field observations, where % of parasitism of the aphids attended by Crematogaster subnuda Mayr. had been found very low (20%) than unattended as well as the aphids attended by other ants. Similar results were obtained under controlled condition. The aphids in the absence of ants show highest % of parasitism 68.6% (Table I) and the tendency of dispersion might be due to excess of parasitoids activity. These attended by C. compressus got 31% (Table I) parasitism. However, those attended by the Crematogaster subnuda Mayr. are parasitized in the smaller number (26.3%) (Table I).

When Crematogaster subnuda Mayr. is in abundance and predominantly attending the aphids, it may provide heavy protection by building a cover over the rapidly declining populations. Even, at times it is practically impossible to see the aphids under such covers. It had been found that slight disturbance of aphids by foreign invaders or even by artificial means unquiet the attending ants. The members immediately retaliate assuming an aggressive posture by raising their abdomens vertically upwards. The quick and simultaneous alerting of all the members under such circumstances might be due to the release of pheromones by some ants. Similar, behavior has been noticed for an approaching predator or other wasps attracted to the honeydew, although, neither aphids are disturbed nor there is any possibility of simultaneous perception by all of them. However, if an approaching parasitoid or another kind of ant is noticed, it is chased by the single aggressive ant without alerting other members. It indicates that pheromones are only released in the presence of vague stimuli received via host for searching the invaders or concentrating other members to combat with bigger enemies. The disquiet members start a vigorous search for such invaders and if perceived chase and drive them out for quite long distances. Even at times, they directly attack them by their mandibles and may cause fatal injuries.

The parasitoids are also afraid of the ants which are apparent by frequent interruptions in oviposition under the pressure of aggressive ants and they were seen running away from the hosts before completing a succession and generally taking shelter on the reverse side of the leaf. Even sometimes they have left the host after macro contact before stinging though other condition remains quite favorable. On the other hand, under similar conditions, some female parasitoids behave quite differently. They camouflage

 

Table I. Overall percentage parasitism of the aphids attended by ants.

Species of attending ants	No. of aphids dissected	No. of aphids with parasitism	% Parasitism	X2 Difference
Crematogaster subnuda	1000	263	26.3*	Between A & B = 5.63 (p>0.05) Between A, B, C= 319.93 (p>0.05)
Camponotus compressus	1000	310	31.0*
Absence of ants	600	412	68.6

 

themselves among disturbed aphids by sitting quiet, though, frequently overrun or even occasionally palpated by the disquiet ants. Immediately, after normalization of timid aphids, consequently, settling the aggressive ants, they again resume normal oviposition till other conditions remain favorable. It is quite interesting that a female parasitoid even during its course of oviposition if palpated by the ant is not recognized as intruder unless it gets frightened. The conclusions of Banks (1962), Pontin (1960) and Wichmann (1955) that “ants disregarded the parasites; parasites were not noticed,” a possible explanation for this unique behavior of ants against parasitoids is might be chemical mimicry in which chemical cues on the cuticular surface of some wasps prevent them from being recognized and attacked by mutualistic ants (Völkl, 1992; Völkl and Mackauer, 1993).

The present observations confirm the findings of El-Zaidy and Kennedy (1956), El-Ziady (1960), Völkl and Mackauer (1993), Stechmann et al. (1996), Stadler and Dixon (1999) and Kaneko (2003) that (i) the ants dislike even the nonspecific species, (ii) any foreign invader disturbing the normal life of their attended aphids and (iii) may directly attack them causing fatal injuries with their mandibles are new additions. Some studies on interactions between ants and aphid parasitoids have reported opposing results. Where several studies showed that ant attendance enhanced primary parasitism by some species of aphid parasitoids (Völkl, 1992; Völkl and Stechmann, 1998). A possible reason for this parasitoid preference is that ant tending protects the parasitoid’s offspring against hyperparasitoids and predators (Teegelar et al., 2012; Tegelaar, 2015). Furthermore, wasps developing in ant-attended colonies may benefit from reduced predation, since many predators are attacked and repelled from the aphid colony by tending ants (Banks, 1962; Teegelar et al., 2012; Tegelaar, 2015).

 

Conclusions

The present writers based on field and laboratory studies on the behavior of aforesaid ants conclude that ants dislike any source which disturbs the normal life of their tended aphids and is an important factor controlling the parasitoid effectiveness.

 

Acknowledgements

The authors would like to extend their appreciation to the Research Center for Advanced Materials Science (RCAMS), King Khalid University, Abha, KSA. The second author (ZA) extends his gratitude to the Research Center for Advanced Materials Science (RCAMS), King Khalid University for funding through research program (RCAMS)-04/20.

 

Statement of conflict of interest

The authors have declared no conflict of interest.

 

References

Banks, C.J., 1962. Ann. appl. Biol., 50: 669-679. https://doi.org/10.1111/j.1744-7348.1962.tb06067.x

Bronstein, J.L. and Barbosa, P., 2002. Multitrophic/ multispecies mutualistic, multitrophic level interactions. Cambridge University Press, New York

Buckley, R.C., 1987. Annu. Rev. Ecol. Systm., 18: 111-135. https://doi.org/10.1146/annurev.es.18.110187.000551

Darwin, C., 1859. On the origin of species by means of natural selection. Appleton and Company, New York. pp. 83–85.

El-Ziady, S., 1960. Proc. R. ent. Soc. Lond. (A), 35: 30-38. https://doi.org/10.1111/j.1365-3032.1960.tb00659.x

El-Ziady, S. and Kennedy, J.S., 1956. Proc. R. ent. Soc. Lond., (A), 31: 61-65. https://doi.org/10.1111/j.1365-3032.1956.tb00208.x

Flatt, T. and Weisser, W.W., 2000. Ecology, 81: 3522-3529. https://doi.org/10.1890/0012-9658(2000)081[3522:TEOMAO]2.0.CO;2

Ghosh, D. and S. Chakrabarti 1988. J. Bombay nat. Hist. Soc., 85: 217-218.

Henry, L.M., Maiden, M.C., Ferrari, J. and Godfray, H.C.J., 2015. Ecol. Lett., 18: 516-525. https://doi.org/10.1111/ele.12425

Kennedy, J.S. and Booth, C.O. 1954. Annls appl. Biol., 41: 88-106. https://doi.org/10.1111/j.1744-7348.1954.tb00918.x

Kaneko, S., 2003. Ecol. Res., 18: 199-212. https://doi.org/10.1046/j.1440-1703.2003.00547.x

Kataria, R. and Kumar, D., 2013. Halteres, 4: 25-32.

Kurl, S.P. and Misra, S.D., 1980. J. environ. Res., 1: 1-6.

Muller, K.E. and Wagenious, S., 2016. Ecol. Ent., 41: 51-60. https://doi.org/10.1111/een.12257

Nielsen, C., Agrawal, A.A. and Hajek, A.E., 2010. Biol. Lett., 6: 205-208. https://doi.org/10.1098/rsbl.2009.0743

Novgorodova, T.A. and Ryabinin, A.S., 2017. Arthropod Plant Interact.

Pontin, A.J., 1960. Ent. Mon. Mag., London, 95: 154-155.

Renault, C.K., Buffa, L.M. and Delfino, M.A., 2004. Ecol. Res., 20: 71-74. https://doi.org/10.1007/s11284-004-0015-8

Sadeghi-Namaghi, H. and Amiri-Jami, A., 2018. Entomol. Sci., 21: 406-411. https://doi.org/10.1111/ens.12319

Saha, S., Das, T. and Raychaudhuri, D., 2018. W. News Nat. Sc., 20: 62-77.

Siddiqui, J.A., Li, J., Zou, X., Bodlah, I. and Huang, X., 2019. Appl. Ecol. env. Res., 17: 5471-5524.

Stadler, B., and Dixon, A.F. 1998. J. Anim. Ecol., 67: 454–459. https://doi.org/10.1046/j.1365-2656.1998.00209.x

Stalder, B. and Dixon, A.F., 1999. Ecol. Ent., 24: 363-369. https://doi.org/10.1046/j.1365-2311.1999.00195.x

Stadler, B. and Dixon, A.F., 2005. Annu. Rev. Ecol. Evol. Syst., 36: 345-372. https://doi.org/10.1146/annurev.ecolsys.36.091704.175531

Stadler, B. and Dixon A.F., 2008. Mutualism: Ants and their insect partners. Cambridge University Press, New York. https://doi.org/10.1017/CBO9780511542176

Stary, P., 1966. Aphid parasites of Czechoslovakia. Academia Prague, pp. 242. https://doi.org/10.1007/978-94-017-5223-7

Stary, P., 1970. Ser. Ent., 6: 643.

Stechmann, D.H., Völkl, W. and Stary, 1996. J. appl. Ent., 120:119-123. https://doi.org/10.1111/j.1439-0418.1996.tb01576.x

Tegelaar, K., 2015. Dynamics of the aphid-ant mutualism. (Dissertation). Stockholm University, Stockholm.

Tegelaar, K., Hagman, M., Glinwood, R., Pettersson, J. and Leimar, O., 2012. Oikos, 121: 61–66. https://doi.org/10.1111/j.1600-0706.2011.19387.x

Ullyett, G.C., 1932. Sci. Bull. U.S. Afr. Dept. Agric. Pretoria, 178: 28.

Vinson, S.B., and Scarborough, T.A., 1991. Ann. Ent. Soc. Am., 84: 158-164. https://doi.org/10.1093/aesa/84.2.158

Völkl, W., 1992. J. Anim. Ecol., 61: 273-281. https://doi.org/10.2307/5320

Völkl, W., 1997. Ecol. Stud., 130: 225-240. https://doi.org/10.1007/978-3-642-60725-7_13

Völkl, W. and Mackauer, M., 1993. J. Insect Behav., 6: 301-312. https://doi.org/10.1007/BF01048111

Völkl, W. and Stechmann D.H., 1998. J. appl. Ent., 122: 201-206. https://doi.org/10.1111/j.1439-0418.1998.tb01484.x

Völkl, W., Woodring J., Fischer M., Lorenz M.W. and Hoffmann K.H. 1999. Oecologia, 118: 483-491. https://doi.org/10.1007/s004420050751

Way, M.J., 1963. Annu. Rev. Ent., 8: 307-344. https://doi.org/10.1146/annurev.en.08.010163.001515

Wellenstein, G., 1957. Teil 1. Zang. Ent., 41: 368-384. https://doi.org/10.1002/sce.37304104254

Wichmann, H.E., 1955. Z. angew. Ent., 37: 507-510. https://doi.org/10.1111/j.1439-0418.1955.tb00805.x

Yao, I., Shibao, H. and Akimoto, S.I., 2000. Oikos, 89: 3–10. https://doi.org/10.1034/j.1600-0706.2000.890101.x