Mandibular structure, gut contents analysis and feeding
group of orthopteran species collected from different
habitats of Satoyama area within Kanazawa City, Japan
S. Abu ElEla1, W. ElSayed 2 & K. Nakamura 1,3
1,2Graduate School of Natural
Science and Technology, Kanazawa University, KakumaCampus, Kanazawa, 920-1192, Japan
3 Division of Biodiversity, Institute of Nature and
Environmental Technology, Kanazawa University, KakumaCampus, Kanazawa,
920-1192, Japan
Email:1 shosho_ali76@yahoo.com; 2 wael_elsayed88@yahoo.com; 3koji@kenruku.kanazawa-u.ac.jp
Date
of publication (online): 26 May 2010
Date
of publication (print): 26 May 2010
ISSN
0974-7907 (online) | 0974-7893 (print)
Editor: Shinsuki Okawara
Manuscript
details:
Ms # o2346
Received 16 November
2009
Final revised
received 25 February 2010
Finally accepted 08
March 2010
Citation: ElEla, S.A., W. ElSayed & K. Nakamura (2010). Mandibularstructure, gut contents analysis and feeding group of orthopteranspecies collected from different habitats of Satoyamaarea within Kanazawa City, Japan. Journal of Threatened Taxa 2(5): 849-857.
Copyright: © S. Abu Elela, W. Elsayed & K. Nakamura 2010. Creative
Commons Attribution 3.0 Unported License. JoTT allows unrestricted use of this article in any medium
for non-profit purposes, reproduction and distribution by providing adequate
credit to the authors and the source of publication.
Authors
Details: see end of this artilce
Author
contribution: The
study was conducted by SAE and WEunder the supervision of KN. Paper was written by SAE and WE with keen encouragement and
valuable advice from KN.
Acknowledgement: see end
of this article
Abstract: In a survey of orthopteranassemblages from different habitats of Satoyama area,
Kanazawa City, Ishikawa Prefecture, Japan, 50 different species belonging to 10
families representing 17 subfamilies and 27 tribes were recorded. Seven feeding
groups were proposed based on stereo microscopic examination of mandibular morphology and analysis of gut contents. Among
the examined subfamilies, family Tettigonidae proved
to be the most diverse in term of mandible types, with four feeding groups. This was followed by family Acrididae,
which also possessed a variety of mandibularstructures with three feeding groups. Other families contained only
single feeding groups. It was noted that only five species were graminivorous,
all were from the family Acrididae, with mandibles
characterized by very short incisors and relatively wide molar regions. The gut
contents of these five species contained more than 80% monocotyledonous plant
species.
Keywords: Orthoptera, mandibular adaptations, gut contents analysis, feeding
group, Satoyama area
For Images & Tables - - click here
INTRODUCTION
The strong relationship with diet
makes mouthpart morphology (Snodgrass 1935) an important trait for insect
evolutionary biologists (Brues 1939) and systematists (Mulkern 1967). Isley (1944)
was one of the first to study mouthparts in detail and correlate morphological
characteristics with feeding habits. He described three groups of mandibles
according to general structure and characteristic diet: (i)graminivorous (grass-feeding type) with grinding
molars and incisors typically fused into a scythe-like cutting edge, (ii) forbivorous (forb or broadleaf
plant-feeding type) which have a molar region consisting of a depression
surrounded by raised teeth and sharp interlocking incisor teeth, and (iii)
herbivorous (mixed feeding type) that have characteristics of both of the
aforementioned groups.
The original findings on mandlible groups by Isley (1944)
have since proven to be widespread in grasshoppers and other insect taxa. Further
studies have been conducted by many authors in different localities,
significant among them are Snodgrass (1928), Gangwere(1965, 1966), Gangwere et al. (1976) and Patterson
(1984) in North America; Liebermann (1968) and Gangwere& Ronderos (1975) in South America; Williams
(1954), Kaufmann (1965), Gangwere & Morales
(1973) in Europe; Gangwere & Spiller (1995) and Gangwere et al. (1998) in the
Mediterranean islands; Feroz & Chaudhry (1975), Gapud (1968) and
Kang et al. (1999) in Asia; and Chapman (1964) in Africa. A general method for determining the
diet of an insect species begins with an examination of the morphology of the mandibular structure (Isely 1944;Mulkern 1967; Patterson 1984). The morphological characters of the
mandibles, incisor and molar surfaces in particular, are useful in labeling
species as grass- or forb-feeders (Chapman 1964; Bernays & Barbehenn 1987;
Kang et al. 1999). Although most
species with forb feeding mandibles feed on a mixture
of grasses and forbs; determination of the diet of an
insect should be followed by gut contents analysis for more confirmations (ElSayed 2005; ElShazly & ElSayed 2006).
Although often viewed as polyphagous herbivores, most orthopteranspecies, especially grasshoppers, are selective to some degree, exhibiting
specific food preferences (Mulkern 1967). Occasionally, grasshoppers with forb-feeding mandibles regularly feed on grasses or vice
versa (Chapman 1964). Nevertheless, there is some value in assessing mouthpart structure
relative to predicting diet and habitat of the orthopteranspecies, especially for the many rare or non-economic species that are unlikely
to be studied in details. Information concerning the feeding habits and mouthparts of different orthopteran species in Satoyamaarea, Kanazawa City, Ishikawa Prefecture, Japan are fragmentary (Ichikawa et
al. 2006; ElSayed 2010) and there is a shortage of
knowledge concerning the mandibular morphology of
many orthopteran species inhabiting Satoyama. Thus, in this paper the morphological characteristics and structural
adaptations of the mouthparts of 50 different orthopteranspecies co-occurring in Satoyama area and covering
different habitat types were examined and tabulated.
MATERIALS AND METHODS
Study Area: The
survey of orthopteran fauna was conducted among four
sampling sites within Satoyama area of Kanazawa City,Ishiakawa Prefecture, Japan (Image 1). Satoyamacovers an area of ca. 74ha and is located at 150m altitude,
5km southeast from the city center. The area comprises various habitat types ranging from secondary forests
dominated by Konara (Quercus serrata), Abemaki (Q. variabilis), Moso Bamboo (Phyllostachys pubescens) and Japanese Cedar (Cryptomeria japonica) to
grasslands dominated by the Bermuda Grass (Cynodon dactylon) and artificial ecosystems such as ponds, paddy fields
and farmlands.
Collecting: The
entomological sweep net sampling method was used for sampling orthopteran species from various habitats during different
seasons. Sampling was done between 1000 and 1400 hr. Collected specimens were immediately killed and preserved in
70% ethanol in a 1l container secured with a rubber stopper. They were later identified, counted,
sorted and kept in individual labeled glass vials in the laboratory. These vials could be stored in freezer
for a year with no apparent damage to the specimens (Mulkern& Anderson 1959; Brusven & Mulkern 1960; ElSayed 2005).
Orthopteran species were identified following the taxonomic key
offered by Ichikawa et al. (2006), specimens were also
compared with known museum specimens in Kanazawa University for further
confirmation.
Mandibular structure:Mandibles were removed from the specimens by lifting the labrum and pulling out
each mandible separately with forceps. Only young adults were used in order to avoid confusion of mandible type
due to mandible erosion (Chapman 1964; Uvarov1977). This process was replicated
with three individuals from each species. Mandibles were lightly brushed with 80% ethanol and distilled water to
remove adherent sand and debris. After air-drying, each mandible was glued to
the head of a #3 or #2 insect pin, depending on its size, for easier
manipulation. The mandibular structure (with both ventral and dorsal sides)
of 50 species of Orthoptera from 10 families (Acrididae, Eneopteridae, Gryllidae, Mecopodidae, Phaneropteridae, Pyrgomorphidae, Mantidae, Tetrigidae, Tettigoniidae and Trigonididae)
was examined under a stereo fluorescence microscope (Nikon® SMZ800
series) equipped with digital camera and TFT LCD Nikon®monitor. Illumination source was
provided by a double gooseneck Olympus® HLL-301 device. Photographs were taken with the Syncroscopy Auto-Montage system (Kanazawa University,
Laboratory of Biodiversity).
We adopted Isley’s (1944)
description of mandible types and their adaptive functions, with the gut
analysis technique, to divide the mandibles into seven major categories: Forbivorous (F), Herbivorous or Mixed-feeders (H), Graminivorous (G), Scavengers (S), Herbivorous with
observed scavenging behavior (HS), Forbivorouswith scavenging behavior (Fs) and Predators (P). Detailed
explanations of these groups are given hereafter in the methodology.
Field cages experiment: Live specimens were kept in wooden cages under natural
environmental conditions and were provided with almost all available plant
species recorded from the field to minimize the hunger-effect. Continual observations of feeding
behavior were made for 3hr in three replicate field cages in each season of the
year. Results from field cages
were compared with those from mandibular morphology
for confirmation concerning feeding group assignments.
Gut contents analysis and feeding groups: Gut contents analysis was performed to compare results
with mandiblular morphological features in an attempt
to deduce the feeding group of each collected orthopteranspecies. Gut analysis technique
was applied according to Mulkern & Anderson
(1959), Ohabuike (1979), Le Gall et al. (1998, 2003) ElSayed (2005), and ElShazly& ElSayed (2006) with slight modifications.
Individuals were dissected and their midgut contents
transferred to clean test tubes. The contents were digested by adding about 3ml of freshly prepared
bleaching agent (1% W/V of sodium hypochlorate and
16.5% W/V of sodium chloride) for a period of 30 minutes (Ohabuike 1979; ElSayed2005). The solution discolored the
chlorophyll and other ingested chitinous parts;
distilled water was added after digestion to stop further bleaching
action. The digested contents were
transferred by pipette to petri dishes for
microscopic examination of fragments, for which estimates were made of the
proportions of different plant species, arthropod parts or other ingested
particles. Characteristic features
of fragments included hair, spines, serration, epidermal characteristics,
orientation of the cells and stomata. Qualitative records were made following ElSayed(2005). The proportions of four
main categories (monocotyledonous plant species, dicotyledonous species, orthopteran or animal parts, and scavenging observations in
caged species) were adopted to classify each orthopteranspecies into one of the proposed seven feeding group. These seven feeding groups are:
1. Herbivorous (H): in which the number of fragments of
dicotyledonous plant is almost equal to the number of fragments of
monocotyledonous species.
2. Herbivorous with scavenging behavior (Hs):
the same as herbivorous group with some scavenging actions were recorded in laboratory caged species.
3. Graminivorous (G): The
number of fragments of monocotyledonous species is more than 75% of the gut
contents.
4. Forbivorous (F): the number
of fragments of dicotyledonous plant species is more than 75% of the gut
contents.
5. Forbivorous with scavenging
behavior (Fs): the same as forbivorousgroup with some scavenging actions were recorded in laboratory
caged species.
6. Scavengers (S): plants species (especially roots or
tubers) and dead orthopteran and/or oligochaetan parts were encountered in almost equal
proportions.
7. Predators (P): all contents of the gut were insect or
other orthopteran body parts with no occurrence of
plant fragments.
Collected orthopteranspecimens were deposited in a catalogued repository in Kanazawa University in
special boxes containing small sachets enclosing naphthalene coated tablets for
further specimen protection against moths and other destructive pests.
RESULTS AND DISCUSSION
The mandibular structures of
50 orthopteran species, belonging to 10 families
representing 17 subfamilies and 27 tribes, collected from different habitats ofSatoyama area were stereomicroscopicallyexamined. Species were sampled
from different habitats including open grasslands, forest margins, ponds and
paddy fields, and belonged to seven major feeding groups, with the results
listed in Table 1. Among the
examined subfamilies, family Tettigonidae proved to
be the most diverse in term of mandible types (four feeding groups). This was followed by family Acrididae which also possessed a
variety of mandibular structures (three feeding
groups). Other families contained only single feeding group (Table 2).
Species from the family Acrididae(Short-horned Grasshoppers) and family Tettigonidae(Long-horned Grasshoppers) can be found in a wide range of habitats, usually in
dense vegetation like open grasslands and around paddy fields or pond
areas. They are quite active in
both walking and flying. It is
interesting to note that species belonging to these subfamilies, with graminivorous type mandibles, were characterized by
extremely slender and elongated bodies and were encountered on the edges of
ponds. This was in accordance with
the findings of other authors (Isley 1944; Squitier & Capinera 2002;
Smith & Capinera 2005). These grasshoppers typically grasp the stems of emergent
grass or grass-like vegetation such as sedges or cattails, blending in almost
perfectly. The Oedipodinaewere split into three mandible types: graminivorous, forbivorous and herbivorous as stated by Capinera (2005). This signifies a more grass-dominated diet. However, these grasshoppers are much more divergent and some
may be completely graminivorous or forbivorous. Most of the species in this subfamily were found on the ground in open
areas on bare soil, rarely on plants or grasses. As a general rule, the Oedipodinaeshow the greatest mandible diversity of among orthopteransubfamilies (Capinera 2005). Isley (1944),Gangwere (1966), and Kang et al. (1999) found a
fairly even distribution of the three mouthpart types
in this group.
Mantidae, on the other hand, were represented by only two tenoderan species (Tenodera angustipennis and T. aridifloia). These
two species were completely predacious in their feeding habit, with mandibles
characterized by sharp incisor points used to pierce and capture prey, and a
long terebral ridge used to kill and slice prey into
pieces. Gut contents analysis
revealed fragments of chitinous arthropod exoskeleton
and other body parts including wings, legs and antennae, confirming their
zoophagous feeding behavior.
It was interesting to note that only five out of the 50
collected orthopteran species were graminivorous, all were from the family Acrididae. The mandibles of
these 5 species were characterized by very short incisors and relatively wide
molar region (Image 2). The
molar area of some individuals of Oxya yezoensis (one of these five species), an example of severe
erosion could be observed (Image 2). It has to be mentioned that, feeding on grasses could be one avenue by
which grasshoppers may avoid toxic chemicals (Bernays& Chapman 1978; ElSayed 2005; ElShazly& ElSayed 2006). In this process, little or no energy, or other resources,
would need to be spent on the detoxification process (Joern1983). During the gut content
analysis of these five graminivorous species silica
particles were recorded in minor amounts. These silica particles could be ingested accidentally during feeding and
accelerate the erosion of the molar area especially in old individuals.
The gut contents of these five species contained more
than 80% monocotyledonous plant species. However, in the graminivorousspecies, Acrida cinerea, small amounts of dicotyledons(less than 12%) were also encountered. Hafez & Ibrahim (1958 a,b),ElSayed (2005) and ElShazly& ElSayed (2006) in their field and laboratory
works on a related acridid, Acrida pellucid,
found that this species may select non-graminousplants for enhancing its reproductive potential since some non-graminous plant species showed a pronounced effect on both
fecundity and development in laboratory rearing and food-choice tests. It could be assumed that Acrida cinerea may utilize some dicotyledonous plant species for
enhancing certain biological and physiological processes. In this study, the acrididspecies with the subfamily Acridinae are typically
considered to be grass-feeders, displaying the classic graminivoroustype mandibles (Isley 1944; Chapman 1964; ElSayed 2005).
Family Gryllidae, with 12 gryllid species, showed mandibles with sharp incisors and
comparatively long knife-shape terebral ridge. These mandibularmorphological modifications could delineate a predacious feeding habit, but the
gut content analysis of these 12 species showed that parts from plant roots,
tubers or even debris (38%) and subterranean arthropod species including
amphipod and isopod species (62%) were collected from different gryllid species. As a consequence, the feeding group of these 12 gryllidspecies could be confined to the scavenging feeding habit.
The seven species of Tetrigidaewere mainly forbivourous (Fm). Their mandibles were
characterized by pointed and sharp incisor points and relatively small molar
region (Image 2). The gut
contents contained only dicotyledonous plan species.
Due to only one representative species from the
subfamilies Eneopteridae, Mecopodidaeand Pyrgomorphidae, determination of the mandibular morphology of these families was limited (Table
1). However, the major mandible type and in turn the feeding group was mostly
confined to the forbivorous type where more
dicotyledonous plants (79%) were consumed in much greater amount than
monocotyledonous species as confirmed by gut contents analysis.
At the family level, it has to be mentioned that the
family Tettigoniidae (12 species) was the most
diverse for mandibular type and feeding group (four
feeding groups). This was followed by family Acrididae(eight species) which harbor three feeding groups
(Table 2). Other families
possessed only a single feeding group irrespective to the number of species
(Table 2). From Table 2, it can be
observed that both family Gryllidae and family Tetrigidae (12 and seven species, respectively) possessed
only one type of mandible and a single feeding group for each family.
Cates (1980) proposed the following criteria to
delineate the degree of diet specialization: (1) monophagy: one or more species within a genus; (2) oligophagy: two or more closely related genera, and (3) polyphagy: two or more plant families. However, none of the orthopteranspecies considered in this study can be considered either monophagyor oligophagy. In all cases, a range of food of plant
and/or animal origin was used, even though some were used infrequently. Thus these orthopteranspecies inhabiting different habitats in Stoyama area
could be considered polyphagous.
In conclusion, the relationship between orthopteran mouthparts and food is far from precise. Mulkern(1967) was convinced that only the grossest associations could be made between mandibular structure and diet (i.e., graminivorous,forbivorous, and herbivorous). Occasionally some orthopteran species, in particular grasshoppers with forb-feeding mandibles, regularly feed on grasses or vice
versa (Chapman 1964; Elsayed 2005). Nevertheless,
there is some value in assessing mouthpart structure as predictive of diet and
habitat in orthopteran species, especially for the
many rare or non-economic species that are unlikely to be studied in
detail. Thus, the gut content analysis
together with laboratory observations on feeding behavior were used either as a
confirmation cues for the mandibular structural
adaptations or add to our knowledge some hidden aspects that could not deduced
from the morphological characters of the mandibles if they were treated alone.
REFERENCES
Bernays, E.A. & R.F. Chapman (1978). Plant chemistry and acridoid feeding behavior, pp.99-141. In: Harborne, H.B. (ed.). Biochemical Aspects of Plant and Animal Coevolution:
Annual Proceedings of the Phytochemical Society of
Europe. No.15. Academic Press, New York.
Bernays, E.A. & R. Barbehenn(1987). Nutritional ecology of grass foliage-chewing insects, pp.147-175.In: Slansky, F. & J.G. Rodriguez (eds.). Nutritional Ecology of
Insects, Mites, Spiders, and Related Invertebrates. John Wiley & Sons, New York.
Brues,
C.T. (1939). Food, drink, and
evolution. Science 90:
145-149.
Brusven, M.A. & G.B. Mulkern(1960). The use of
epidermal characteristics for the identification of plants recovered in
fragmentary condition from the crops of grasshoppers. North Dakota Agricultural Experimental Station
Research Reports 3: 11.
Capinera,
J.L. (2005). Relationships between insect pests
and weeds: an evolutionary perspective. Weed Science 53:
892-901
Cates, R.G.
(1980). Feeding pattern of monophagous, oligophagous and polyphagous herbivores: The effect of resource abundance
and plant chemistry. Oecologia 46: 22-31.
Chapman,
R.F. (1964). The structure
and wear of the mandibles in some African grasshoppers. Proceeding of the Zoological Society of London 142: 107-121.
ElSayed,
W.M. (2005). Grasshoppers (Orthoptera: Acrididae)
communities in Abu-Raûwash district (Giza, Egypt). MSc.
Thesis, Cairo University, 169pp.
ElSayed,
W.M. (2010). Diversity
and structure of ground beetles (Coleoptera: Carabidae) assemblages in Satoyama. Ph.D. Thesis, Kanazawa University,
Japan,123pp.
ElShazly, M. & W.M. ElSayed(2006). The
structure and host plant selection of an acrididcommunity on the edge between a desert- and an agro-ecosystem in Egypt. Environmental Informatics
Archives 4: 1-25.
Feroz, M., & M.A. Chaudhry(1975). Studies on mandibles of some grasshoppers of Lahore. Biologia (Lahore) 21:
211-225.
Gangwere,
S.K. (1965). Food selection in the Oediponidae grasshopper Arphia sulphurea . American Midland Naturalist 74:
67-75.
Gangwere,
S.K. (1966). Relationships
between mandibles, feeding behavior and damage inflicted on plants by the
feeding of certain acridids (Orthoptera). Michigan
Entomology 1: 13-16.
Gangwere, S.K. & A. Morales. (1973). Food selection and feeding behaviourin Iberian Orthopteroidea. Anales del Instituto Nacionalde Investigaciones Agrarias. Serie proteccion vegetal. 3: 251-337.
Gangwere,
S.K. & R.A. Ronderos . (1975). A synopsis of food selection in Argentine Acridoidea. Acrida 4: 173-194.
Gangwere , S.K., F.C. Evans & M.L. Nelson (1976). The food habits and Biology of Acrididae in an old-field community in Southeastern
Michigan. Great
Lakes Entomology 9: 83-123.
Gangwere, S.K. & D.O. Spiller (1995). Food selection and feeding behavior in selected Orthoptera sen. lat. of the
Balearic Islands, Spain. Journal of Orthopteran Research 4: 147-160.
Gangwere,
S.K., J.C. Mc kinney, M.A. Ernemann& R.G. Bland (1998). Food
selection and feeding behavior in selected Acridoidea(Insecta: Orthoptera) of
the Canary Islands, Spain. Journal of Orthopteran Research 7: 1-21.
Gapud,
V.P. (1968). The external
morphology of the head and mouthparts of some Philippine Orthoptera. Philippine
Entomology 1: 11-32.
Hafez, M. & M.M. Ibrahim (1958a). Ecological and biological studies on Acrida pellucida Klug in Egypt. Bulletin of the Society of Entomology of Egypt XIII: 163-183.
Hafez, M. & M.M. Ibrahim (1958b). Studies on the egg and nymphal stages of Acrida pellucida Klug in Egypt. Bulletin of the Society of Entomology of Egypt XIII: 183-198.
Ichikawa,
A., Y. Kano, Y. Kawai, M. Kawai, O. Tominago & T.Murai (2006). Orthoptera of the Japanese
Archipelago in Color. 2ndeds., 687pp. (In Japanese).
Isley,
F.B. (1944). Correlation
between mandibular morphology and food specificity in
grasshoppers. Annals of Entomological Society of America 37: 47-67.
Joern,
A. (1983). Host
Plant Utilization by Grasshoppers (Orthoptera: Acrididae) from a SandhillsPrairie. Journal Range Management36: 793-797.
Kang, L., Y.Gan & S.L. Li (1999). The structural adaptation of
mandibles and food specificity in grasshoppers on Inner Mongolian grasslands. Journal of Orthopteran Research8: 257-269.
Kaufmann, T.
(1965). Biological
studies on some Bavarian Acridoidea (Orthoptera), with special reference to their feeding
habits. Annals of
Entomological Society of America58: 791-801.
Le Gall, P.,
E. Mingouolo & G. Bani(1998). Diets of Zonocerus variegates (L.)
(Orthoptera: Acrididae) in
Cassava fields in Congo. Journal of Applied Entomology122, 9-13.
Le Gall, P.,
Z. Djihou, G. Tchenga &
C.J. Lomer (2003). Diet of Zonocerus variegatus (Linné, 1758) (Orthoptera: Acrididae) in cassava field in Bénin. Journal of Applied
Entomology 127(7): 435-440.
Liebermann,
J. (1968). The mandibles of
grasshoppers of the subfamily Chilacridinae. Revista de Investigaciones Agropecuarias, serie 5 (Patalogía Vegetal) (Buenos
Aires), (5): 53-62 5: 53-62. (In
Spanish)
Mulkern,
G.B. (1967). Food selection
by grasshoppers. Annual Review of Entomology12: 59-78.
Mulkern, G.B. & J.F. Anderson (1959). A technique for studying to the food
habits and preferences of grasshoppers. Journal of Economic Entomology 52: 342.
Ohabuik,
J.E. (1979). Grass availability and food
preference of the African migratory locust, Locusta migratoria migratoriodes (R. and
F.). Zeitschrift für Angewandte Entomologie 88: 354-363.
Patterson,
B.D. (1984). Correlation
between mandibular morphology and specific diet of
some desert grassland Acrididae (Orthoptera). American Midland Naturalist 111: 296-303.
Smith, T.R. & J.L. Capinera (2005). Host preferences and habitat
associations of some Florida grasshoppers (Orthoptera:Acrididae). Environmental Entomology 34:
210-224.
Snodgrass,
R.E. (1928). Morphology and evolution of the insect head and its appendages. Smithsonian
Miscellaneous Collection 81:
1-158.
Snodgrass,
R.E. (1935). Principles of Insect
Morphology. McGraw-Hill. New York, 667pp.
Squitier, J.M. & J.L. Capinera(2002). Habitat associations of Florida
grasshoppers (Orthoptera: Acrididae). Florida Entomologist85: 235-244.
Uvarov,
B. (1977). Grasshoppers and Locusts. A
Handbook of General Acridology, Vol. 2, Cambridge,
United Kingdom, 613pp.
Williams, L.H. (1954). The feeding habits and food preferences of Acridinae and the factors which determine
them. Transaction of the Royal
Entomological Society of London 105:
423-454.