NORTH-WESTERN JOURNAL OF ZOOLOGY 9 (1): 45-50 ©NwjZ, Oradea, Romania, 2013 Article No.: 131102 http://biozoojournals.3x.ro/nwjz/index.html
Wing dimorphism of European mole cricket Gryllotalpa gryllotalpa (L.) (Orthoptera: Gryllotalpidae) in the north-west of Iran
Mohammad Hossein KAZEMI1*, Shabnam JAFARI1, Hosseinali LOTFALIZADEH2 and Mohammad JAFARLOO2
1. Department of Plant Protection, Tabriz branch, Islamic Azad University, Tabriz, Iran. 2. Department of Plant Protection, East-Azarbaijan Research Center for Agriculture & Natural Resources, Tabriz, Iran. *Corresponding author, M.H. Kazemi, E-mail: [email protected]
Received: 24. December 2011 / Accepted: 25. September 2012 / Available online: 27. December 2012 / Printed: June 2013
Abstract. The seasonal study of wing dimorphism in the European mole cricket, Gryllotalpa gryllotalpa (Linnaeus, 1758) (Orthoptera: Gryllotalpidae), was carried out in northwest Iran. Based on present research, the long-winged (LW) morph appeared in early-mid spring when vegetation density is low and the crickets need to fly to search for food. Study of foretibiae showed that the dactyls are elongated and longer than short- winged (SW) morph’s dactyls, and that they are suitable for excavating hard soil in this period. SW adults were observed from May to July and the dactyls are shorter and broader, which are suitable for more tunneling in light soils in the middle of spring.
Key words: European mole cricket, wing dimorphism, long-winged, short-winged, Iran, first report.
Introduction pterous), or totally absent wings (apterous). In addition to differences in wing length, morphs are The European mole cricket, Gryllotalpa gryllotalpa often observed with differences in some other (Linnaeus, 1758), is one of the most important in- morphological, physiological and biological cha- sect pests in turf and field crops of Iran. They are racteristics such as degree of flight muscle deve- burrowing insects and feed on a variety of organ- lopment, duration of nymphal stage, time to first isms in the soil. These insects do not attack plants reproduction, fertility and diapause (Vepsäläinen directly, but by tunneling, extended surface tun- 1978, Harrison 1980). nels, cause significant damage to grass and crops Developing and maintaining the flight appara- of gardens, as they chop off any roots encountered tus carries a cost. For example, macropterous fe- when digging (Weiss & Dickerson 1918, Kazemi et males of the sand cricket, Gryllus firmus (Scudder), al. 2010). have an older reproductive age with shorter life- It was introduced from Europe into the United time fecundities when compared to their short- States about 1913. It has now been reported from winged counterparts (Elizabeth et al. 2011). Impor- Massachusetts, New Jersey, New York, and Penn- tantly, flight capability trades-off occur with re- sylvania (Nickle & Castner 1984). Weiss and productive effort: short-winged females start ovar- Dickerson (1918) determined that the original in- ian growth at an earlier age and often exhibit troduction of this species was in nursery stock greater overall fecundity than their long-winged from Holland and Belgium. It also is widespread counterparts. Long-winged females mainly allo- in the northern European part of Russia, southern cated energy from food to flight muscle develop- Ukraine and the northern Caucasus (Anonymous ment and general maintenance of the body rather 2010). This species in ecological conditions of than to egg production, whereas short-winged fe- north-west of Iran molts eight times during its de- males used it for egg production and longevity velopment. Small nymphs have no wings, but fifth (Zhao et al. 2010, Guerra 2011). The polymorphism instars have small wing pads that will grow in may be determined by genetic differences between later molting. There is only one generation annu- morphs (genetic polymorphism), environmental ally (Kazemi et al. 2010). conditions under which the morphs develop Wing polymorphism is commonly observed in (environmental polyphenism) or by a combination many orders of insects, especially species of of these two (Zera et al. 2007), however, wing Orthoptera, Coleoptera and Hemiptera (Harrison dimorphisms in insects are controlled by a single 1980). The polymorphism consists of discrete locus and polygenes, respectively (Roff & differences in wing length with morphs exhibiting Fairbairn 2007). fully developed (macropterous), reduced (brachy- The relationship of development and repro- 46 M.H. Kazemi et al. duction of flight capable (long-winged) and hind wings never reach to end of abdomen) individuals flightless (short-winged or wingless) morphs of could not fly in the air; thus, soil sampling is the main col- wing polymorphism with endocrine hormones has lection method. Mole crickets that surfaced after flushing the soil and with light traps were collected and counted been investigated (Zera 2003). There is a clear cor- on each sampling day. relation between activity of juvenile hormone (JH) during the last nymphal stadium and subsequent Morphological studies molt to either the long-winged (LW) or short- Morphological data were obtained from measurement of winged (SW) adult (Fairbairn 1994, Fairbairn & pronotum width, length of body, forewings, hind wings, Yadlowski 1997, Roff et al. 1997). Thus far, the pronotum and dactyls of foretibia using cullies (±0.01) on only direct test of the JH wing morph hypothesis both sexes. Two hundreds individuals were examined for these characters. According to Walker and Sivinski (1986), has been undertaken on the cricket, Gryllus rubens the ratios of hind wing (HW) to forewing (FW) length are Scudder (Zera & Denno 1997). Experimental eleva- used to discriminate among wing morphs. Data analyz- tion of JH titer during the last stadium in long- ing was done by t-test, and comparison of adult wing ra- winged-destined G. rubens redirected their devel- tio (HW/FW) in each sex was conducted. opment to the short-winged morph. Endo (2006) reported seasonal wing dimorphism of oriental mole cricket, Gryllotalpa orientalis (Brumeister, Results 1839), in Japan. It was the only report of wing di- morphism in mole crickets. In his study, the short- In ecological conditions Iran, the LW morph ap- winged morph appeared in early spring, and the peared in early-mid of spring when vegetation overwintering nymphs became long-winged density is low and the mole crickets need to fly to adults in summer. search for food and for mates. Habitat stability Considering economical importance of Euro- and quality also affect the fitness of each morph pean mole cricket in Iran, biological and ecological (Roff 1986, Denno et al. 1996). It is reasonable that study of this species is badly needed for making juveniles become SW adults after May (the habitat decision in integrated control of this pest. has good quality in this time of year), with more reproduction that has benefit to brachypterous in- dividuals. Materials and methods As the soil temperature rises in mid-March and April, mole crickets do more tunneling. The Study areas LW adult males in warm evening of late April or The study was done in turf grounds and field crops of May excavate an acoustic (funnel-shaped) cham- Tabriz (N 38º 6', E 46º 26'), Azarshahr (N 37º, E 45º) and ber with an opening to the soil surface for making Miandoab (N 36º, E 46º) in northwest Iran based on ob- servation of the mole crickets’ damage or presence of calling song. signs of tunneling. Mole crickets were sampled four times Females are attracted to the calling aggrega- monthly from mid-March to November in 2009 and 2010. tion, fly over the sound chamber created by the displaying males and then drop to the ground to Collecting access the selected male’s burrow (Hertl et al. Collection was made by two methods: 2001, Howard & Hill 2006, Kazemi et al. 2011). 1) The first method was to collect flying adults with Shortly after mating, oviposition starts. Small ultraviolet fluorescent light traps. The light traps were set for about four hours after sunset. Three light traps were nymphs continue to feed and grow through the set beside the selected areas and trapped mole crickets summer, and they are most destructive in this area were collected the next day. This method is suitable for during late July to August. Brandenburg & Wil- long-winged (LW with hind wings are longer than the liams (2002) believe that, for similar species, the abdomen) individuals. males die after mating and the females die shortly 2) The second method according to Nikouei et al. after oviposition. (2006) was to directly collect adults and nymphs from soil. Mole cricket damage was evaluated using a 0.6 m² frame divided into nine equal, square-shaped sections Morphological studies and damage was rated from zero to nine. The frame was Sex determination placed on the ground and the number of sections which contained mounds or tunnels was counted. Then, 0.6 m² Adults of both morphs have complete wings, and areas were flooded with 8 liters of soapy water. Mole the sexes can be distinguished by forewing vena- crickets that surfaced within the frame after flushing were tion. Forewings of the males have a pair of large collected and counted because short-winged (SW with triangular cells that have been described as harp-
Wing dimorphism of Gryllotalpa gryllotalpa in Iran 47
Table 1. Measurment (in mm) of body parts in male European mole cricket (n=100).
Long-winged Short-winged Body parts Mean ± SE Min Max Mean ± SE Min Max Length of body 42.7 ± 1.33 35 50 43.00 ± 0.95 38 48 Forewing length 15.7 ± 0.37 14 17 13.50 ± 0.43 12 16 Hind wing length 36.1 ± 0.77* 34 41 22.40 ± 0.73* 19 26 Pronotum length 14.5 ± 0.17 14 15 14.57 ± 0.18 14 15 Pronotum width 11.5 ± 0.17 11 12 11.57 ± 0.18 11 12
* significant difference at α = 5%
Table 2. Measurment (in mm) of body parts of female European mole cricket (n=100).
Long-winged Short-winged Body parts Mean ± SE Min Max Mean ± SE Min Max Length of body 46.90 ± 1.44 41 54 48.50 ± 1.82 38 57 Forewing length 17.60 ± 0.65 14 20 14.60 ± 0.38 13 17 Hind wing length 38.50 ± 0.74* 34 43 24.5 ± 0.85* 22 29 Pronotum length 14.57 ± 0.18 14 15 14.62 ± 0.18 14 15 Pronotum width 11.57 ± 0.18 11 12 11.62 ± 0.18 11 12
* significant difference at α = 5%
shaped. These two cells are the stridulatory area due, in part, to the apparent benefits of flight. This that disappeared in females (Fig. 1). trait allows macropterous organisms to easily co- lonize peripheral areas of their current habitat, Wing morph perhaps, locating to more favorable habitats for Trapped adults are divided into LW and SW survival and reproduction (Gardiner 2009, Hoch- morphs based on forewing and hind wing lengths. kirch & Damerau 2009). Although this is the first The hind wings of LW individuals extend beyond report of morphological dimorphism of G. gryllo- the end of abdomen (flight-capable morph), and talpa, these results need confirmation by molecular females have longer wings (in both pair of wings) study of the two morphs. than males, whereas the hind wings of SW indi- viduals do not cover the abdomen (flightless Foretibia morph) (Fig. 2). Mole crickets spend most of their lives under- The results showed there is not significant dif- ground and their forelegs are the digging type. All ference among the length of body, pronotum and European mole crickets have four dactyls on forewings, but differences of the size of hind wing foretibiae (Nickle & Castner 1984). Both SW and in adults of each morphs are significant (Table 1 & LW morphs have large, powerful strong dactyls 2). Hind wing size of all LW individuals is more on foretibiae that allow for the excavation of com- than 34 mm and the mean ratios of HW/FW in plex burrow systems under ground. At com- both sexes are about 2.23. In SW morph, the length mencement of the period that the adults of each of hind wing is always less than 30 mm and the morph appeared, the morph and size of dactyls mean ratios of HW/FW in both sexes are about are different (Fig. 3). 1.68. According to the literature, this is the first re- LW adults appeared in April that the soil is port of wing dimorphism in European mole not made friable by cultivation; thus, the dactyls cricket. are elongated and longer than SW morph’s dactyls Wing polymorphism is often found in mul- (Fig. 3). This type of dactyls in LW morph facili- tivoltine insects such as many cricket species tates digging the hard soils. However, in SW (Gryllus firmus) (Elizabeth et al. 2011), aphids morph that appeared from May, the dactyls are (Aphis craccivora) (Braendle et al. 2006) and water shorter and broader. This type of dactyls is suit- striders (Gerris lacustris) (Pfenning et al. 2008), able for more tunneling in light soils and mud in whereas in G. gryllotalpa, wing dimorphism is middle of spring. Analysis of the length of dactyls maintained in a univoltine life cycle with two dif- in both morphs showed, although all of dactyls in ferent developmental processes. The independent LW morph are longer than SW morph, but differ- evolution of wings among several animal taxa is ences of the first dactyls are significant (Table 3).
48 M.H. Kazemi et al.
Figure 1. The forewing of Gryllotalpa gryllotalpa: A. males and B. females. The white arrow indicates harp-shaped cells in male.
Figure 2. The adults of Gryllotalpa gryllotalpa: A. Male SW morph in laterodorsal view, B. Female SW morph in dorsal view, C. Male LW morph in laterodorsal view and D. Female LW morph in dorsal view. The white arrow indicates tips of hind wings.
Figure 3. Dactyls form of foretibia in European mole cricket in northwest Iranian populations: A. LW morph and B. SW morph.
Table 3. The mean length (in mm) of dactyls in fore-tibia of European mole cricket (n=20).
Dactyls of Long-winged Short-winged fore-tibia Mean ± SE Min Max Mean ± SE Min Max 1rst 4.89 ± 0.17* 4.5 5.4 3.51 ±0.27* 3 4 2end 3.52 ± 0.29 3.0 4.0 2.55 ± 0.22 2.1 3.3 3rd 2.59 ± 0.16 2.2 3.0 2.01 ± 0.14 1.7 2.1 4th 2.01 ± 0.17 1.5 2.2 1.66 ± 0.25 1.4 2
* significant difference at α = 5%
Wing dimorphism of Gryllotalpa gryllotalpa in Iran 49
Study of nymphs’ dactyls showed that all of them Elizabeth, G.K., Derek A.R., Daphne, J.F. (2011): The evolutionary genetics of acquisition and allocation in the wing dimorphic are elongated and long (such as LW morph). cricket, Gryllus firmus. Evolution 65(8): 2273–2285. Endo, C. (2006): Seasonal wing dimorphism and life cycle of the mole cricket Gryllotalpa orientalis (Orthoptera: Gryllotalpidae). European Journal of Entomology 103: 743-750. Discussion Fairbairn, D. J. (1994): Wing dimorphism and the migratory syndrome: Correlated traits for migratory tendency in wing This study showed that, in warmer area of north- dimorphic insects. Researches on Population Ecology 36(2): 157- west Iran (such as Miandoab), the overwintering 163. Fairbairn, D.J., Yadlowski, D.E. (1997): Coevolution of traits takes place as either the large nymphs or adults of determining migratory tendency: correlated response of a LW morph, but in cooler conditions (such as critical enzyme, juvenile hormone esterase, to selection on wing Tabriz) the nymphs cannot finish their develop- morphology. Journal of Evolutionary Biology 10(4): 495-513. Gardiner, T. (2009): Macropterism of Roesel’s bushcricket ment into adults before winter and the large Metrioptera roeselii in relation to climate change and landscape nymphs became LW morph in early spring. This structure in eastern England. Journal of Orthoptera Research means that wing dimorphism of G. gryllotalpa in 18(1): 95-102. Guerra, P.A. (2011): Evaluating the life-history trade-off between this area is not linked to the overwintering period. dispersal capability and reproduction in wing dimorphic However, in G. orientalis, at ecological conditions insects: a meta-analysis. Biological Reviews 86(4): 813-835. of Japan, when juveniles reach the last stage dur- Harrison, R.G. (1980): Dispersal polymorphism in insects. Annual Review of Ecology and Systematics 11: 95-118. ing summer, they become SW adults before win- Hertl, P.T., Brandenburg, R.L., Barbercheck, M.E. (2001): Effect of ter. The nymphs that hatch late in the reproduc- soil moisture on ovipositional behavior in the southern mole tive period and can not reach to last molting be- cricket (Orthoptera: Gryllotalpidae). Physiological and Chemical Ecology 30: 466–473. fore winter, have overwinter period at juvenile Hochkirch, A., Damerau, M. (2009): Rapid range expansion of a stages and become LW adults in following sum- wing-dimorphic bush-cricket after the 2003 climatic anomaly. mer (Endo 2006). Endo (2006) believes that is be- Biological Journal of the Linnean Society 97:118–127. Howard, D.R., Hill, P.S.M. (2006): Morphology and calling song cause the overwintering nymphs have a long de- characteristics in Gryllotalpa major (Orthoptera: Gryllotalpidae). velopmental period and grow slowly that leads to Journal of Orthoptera Research 15(1): 53-57. engender LW morph, but SW morph grows quick- Kazemi, M.H., Jafari, S., Lotfalizadeh, H., Jafarloo, M. (2010): Evaluation on morphological characters of European mole ly and can reaches later developmental stages be- cricket, Gryllotalpa gryllotalpa (Orth.: Gryllotalpidae) in the fore winter. Thus, there is a relation between the North-west of Iran. Journal of Agricultural Sciences 14(1): 63-73. overwintering form and wing morphology. [In Persian] Kazemi, M.H., Jafari, S., Lotfalizadeh, H., Jafarloo, M., Vahdani Manaf, N. (2011): Stridulation in European mole cricket, Gryllotalpa gryllotalpa (L.) (Orthoptera: Gryllotalpidae) a North- western population of Iran. Journal of Field Crop Entomology Acknowledgements. We would like to thank Dr. Chihiro 1(1): 1-10. [In Persian] Endo (Department of Zoology, Biological Science, Nickle, D.A., Castner, S.L. (1984): Introduced species of mole Graduate School of Science, Kyoto University, Sakyo, crickets in the United States, Puerto Rico and the Virgin Islands (Orthoptera: Gryllotalpidae). Annals of the Entomological Kyoto 606-8502, Japan) for sending his valuable Society of America 77(4): 450-465. publications and sharing his knowledge about these Nikouei, P., Hatami, B., Khajehali, J., Ebadi, R. (2006): Rating insects with us. We wish to thanks Dr. M. Mofidi (Iranian system to evaluate damage of mole cricket, Gryllotalpa sp. 17th Plant Protection Institute) for identification of specimens. Iranian Plant Protection Congress: 350. [In Persian]. Pfenning, B., Gerstner, S., Poethke, H. J. (2008): Alternative life histories in the waterstrider Gerris lacustris: Time constraint on wing morph and voltinism. Entomologia Experimentalis 129: References 235-242. Roff, D.A. (1986): The evolution of wing dimorphism in insects. Anonymous (2010): Interactive agricultural ecological atlas of Evolution 40: 1009-1020. Russia and neighboring countries. Available from: Roff, D.A., Fiarbairn, D.J. (2007): The evolution and genetics of
50 M.H. Kazemi et al.
Weiss, H.B., Dickerson, E.L. (1918): The European mole cricket endocrinology and evolutionary genetics. Annual Review of Gryllotalpa gryllotalpa, an introduced insect pest. Journal of New Ecology, Evolution, and Systematics 38: 793-817. York Entomological Society 26: 18-23. Zhao, L.Q., Zhu, D.H., Zeng, Y. (2010): Physiological trade-offs Zera, A.J., Denno, R.F. (1997): Physiology and ecology of dispersal between flight muscle and reproductive development in the polymorphism in insects. Annual Review of Entomology 42: wing-dimorphic cricket Velarifictorus ornatus. Entomologia 207-231. Experimentalis et Applicata 135(3): 288-294. Zera, A.J. (2003): The endocrine regulation of wing polymorphism in insects: State of the art, recent surprises, and future directions. Integrative and Comparative Biology 43(5): 607-616. Zera, A.J., Harshman, L.J., Williams, T.D. (2007): Evolutionary endocrinology: The developing synthesis between