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Cryptic coloration and choice of escape
microhabitats by grasshoppers (Orthoptera:
Acrididae)
PAULA CABRAL ETEROVICK AND
JOSE EUGfiNIO CORTES FIGUEIRA
Departamto de Biologia Geral, Univerdade Federal de Minas Gerais,
3 0 1 61-970 Minas Gerais, Brasil
JOAO VASCONCELLOS-NET0
I3IE Departamento de <oologia, Universidade Esladual de Campinas,
CP 6109 13083-970 Campinas, ScZo Paulo, B r a d
Received 2 September 1996; acceptedfor publicahin 6 December 1996
Cryptic coloration is found in many Orthoptera, especially in Acrididae, showing a great
variety of forms. In a grasshopper assemblage in southeastern Brazil, preferences for escape
places were detected; grasshoppers tended to escape to backgrounds in which they seem to
be more cryptic. Coloration was measured using the Simpson diversity index, to quantifL
‘aspect diversity’ (diversity of colours and shapes of patches along the insect’s body). A weak
positive correlation was found between grasshoppers’ aspect diversity and diversification in
use of escape places (use of many backgrounds to escape). Grasshoppers with similar colour
patterns tended to use the same structures (leaves, sandy soil, stones) to escape.
0 1997 The Linnean Society of London
ADDITIONAL KEY WORDS:--colour pattern
- habitat selection - escape behaviour.
-
morphological diversity - polymorphism
CONTENTS
Introduction . . . . . . . . . . . . . . . . . . . . . . .
Methods. . . . . . . . . . . . . . . . . . . . . . . .
Study site . . . . . . . . . . . . . . . . . . . . . .
Testing grasshoppers’ preference for escape structures and backgrounds .
Influence of aspect diversity on escape structure and background choice .
Convergence of colour pattern and use of structures . . . . . . .
Results . . . . . . . . . . . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . .
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Correspondence to P. Cabral Eterovick. Email: [email protected]
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0024-4066/ 1997/080485 15 $25.00/0/bj960134
485
0 1997 The Linnean Society of London
486
P. CABRAL ETEROVICK E T A
INTRODUCTION
Cryptic coloration, common in many taxonomic groups of animals (Cott, 1940),
has an important evolutionary meaning for prey species, making their detection
by visually-oriented predators difficult (Tinbergen, 1957; Papageorgis, 1975;
Schultz, 1986). To be considered cryptic, an animal must match some part of its
microhabitat (Endler, 1978). Microhabitat is defined here as background, comprising a portion of the environment with specific colours and composition, e.g.
types of soil and plant cover. Coincidence of an animal colour pattern with the
background pattern can reduce predation, and natural selection by predators can
lead to similarity among forms that use the same background (Vasconcellos-Neto,
1987). On the other hand, in apostatic selection, diversity in prey is maintained
because predators learn to recognize common morphs (or the most common
species) and prey upon them more intensely (Rand, 1967; Vasconcellos-Neto,
1987).
Cryptic beetles can be expected to show their real cryptic potential after detecting
a predator’s presence, when they then choose the most suitable place to avoid
detection (Schultz, 1986). Grasshoppers and other insects which match the same
background can still be very Werent from one another (Rand, 1967). This is
because insects which use the same background can match different portions of it,
which we call here ‘structures’, that is, surfaces with particular colour and texture,
e.g. sandy soil, grass, a leaf or a stone (see Endler, 1978; Sandoval, 1994). Some
insects considered to be specialists can match a given structure in colour as much
as in body shape and position while resting (Endler, 1978). In these cases, an insect’s
colour pattern has become so similar to that of its preferred structure that it is
conspicuous only when on other structures or backgrounds. On the other hand, it
should be expected that cryptic insects using many different structures and backgrounds to escape from predators will have many Werent colours along the body,
thus ensuring that by disrupting the body shape, at least some part of the body
matches each potential escape place.
Orthopterans are well known for their crypsis patterns (e.g. Gill, 1979; Dearn,
1981;Joern & Lawlor, 1981; Schultz, 1981; Sandoval, 1994). Disruptive patterns,
that is, alternating light and dark patches or stripes, probably improve the escape
effect of cryptic coloration, causing the body outline to be less evident (Cott, 1940).
Morphological radiations are also known in the Acrididae (Cott, 1940) and may be
due to apostatic selection. Grasshoppers are preyed upon by lizards, birds and
mammals (Schultz, 1981; Rocha & Bergallo, 1994; Sandoval, 1994). However, the
effect of selection on the existing morphological variability in Acrididae still needs
rigorous testing (Rand, 1967).
In this study, we investigated three assumptions related to the aspect and spatial
organization of a diversified grasshopper assemblage that occurs in natural montane
fields (‘campos rupestres’) of the Serra do Cipb (Minas Gerais state, Brazil). First,
we tested the existence of preferences for structures or backgrounds as escape space
by Merent forms of grasshoppers. Second, we checked if grasshoppers’ ‘aspect
diversity’ is related to the diversity in structure and/or background use. ‘Aspect
diversity’ was considered here as the diversity of colours and mottling along an
insect’s body. Third, we investigated if grasshoppers using the same structures to
escape were the most similar among the total assemblage.
CHOICE OF ESCAPE MICROHABITATS BY C R m C GRASSHOPPERS
487
METHODS
The study was conducted in a montane field (43”35’32’’W, 19”17’23”S, 1200 m
alt.) in the Serra do Cip6, located in the Serra do EspinhaCo range. The region has
a rich flora, with the following families especially well represented Veloziaceae,
Eriocaulaceae, Cyperaceae, Melastomataceae and various shrubby Asteraceae
(Giulietti et al., 1987). The terrain is hilly, with quartzite elevations, sandy or stony
soil, and small streams and marshes in seepage areas (Sazima & Bokermann, 1977).
The assemblage of acridids studied was located in a field of about 28000m2,
enclosed by quartzite elevations. This field presented a mosaic of sandy soils in
varying shades of grey, and patches of stones and quartz crystals. A herbaceous
stratum consisting primarily of bush grasses and sedges varied throughout the area.
These elements resulted in a mosaic of many backgrounds.
Potential visually-oriented predators of grasshoppers occur at the study site: the
lizards Tmpidum nanuzae and Tmpidulur montunus (T torquatus group), and the birds
Molothm b0nahnsi-s (Icteridae),Cyanocorax cnStutellus (Corvidae), Mimus saturninus (Mimidae), Pobstictus supercilianS (Tyrannidae), Jvystulus chacuru (Bucconidae), Anthus
hlLmyri (Motacilidae), Rhynchotus r u j s c m and Jvothura maculosa (Tinamidae) (M.F.
Vasconcelos, pers. comm.). Tmpidum montanus is known to prey on grasshoppers in
the study site (M.C. Kiefer, pers. comm.). Tyrannids and icterids have been already
cited as grasshopper predators in other sites (Cott, 1940; Schultz, 1981).
5stin.ggrasshoppers’ prejimcefor escape structures and backg/ounds
The acridids sampled in the study site were grouped into morphospecies by
external morphology. Since our predictions are based on camouflage properties,
and colour pattern may vary intraspecifically (Gill, 1979; Dearn, 1981; Sandoval,
1994))each grasshopper with a Merent morphological aspect was considered as a
distinct morphospecies, not considering, for the preference tests, their being polymorphic forms of the same biological species or from different species. Among the
ten morphospecies studied, those numbered 1, 2, 3 and 4 belong to the genus
Rhammatocerus (Gomphocerinae),four others are also Gomphocerinae (Nos. 5, 8, 9
and 10) and two are Leptysminae (Nos. 7 and 8) (Fig. 1).
Observations were made in the dry season, from August to November of 1995,
before the spring rains began. We recorded the structure and background where
adult grasshoppers positioned themselves after jumping when disturbed by our
walking. We used the term ‘escape place’ to refer to both background and structure.
To make the use of statistical tests possible, we included in this study only the 10
morphospecies having at least 10 observations each. Four of these morphospecies
were relatively rare and we observed individuals more than once after successive
jumps. It is important to stress that they always had the possibility of changing the
structure and background used in each observation due to the proximity of all
structures and backgrounds in the habitat mosaic.
The six habitat structures we considered to possess distinct colour and texture in
the field habitat were green leaves, dead (brownish) leaves, light sand, dark grey
sand, brownish stones and quartz crystals. Backgrounds, considered as larger patches
CHOICE OF ESCAPE MICROHABITATS BY CRYF'TIC GRASSHOPPERS
489
of the field habitat, were grouped in nine categories, according to the availability
of structures within them (Fig. 2).
1. Dark sandy soil with an abundant herbaceous cover.
2. Dark sandy soil with sparse grass bushes.
3. Light sandy soil with or without brownish stones and an abundant herbaceous
cover.
4. As 3 but with sparse grass bushes.
5. Mosaic soil of dark and light sand and an abundant herbaceous cover.
6. As 5 but with sparse grass bushes.
7. Soil covered by small quartz crystals (up to 2cm in their longer axis) and
abundant herbaceous cover.
8. As 7 but with sparse grass bushes.
9. Completely covered by a dense herbaceous vegetation.
Structures and backgrounds were quantified in the environment by measuring,
in mm, their extensions in contact with folding rules extended in 30 line transects
1 m long, randomly positioned in the study site. Two measures of structures were
made: one just above the ground and another 10 cm up, to q u a n q their whole
spatial availability, as grasses are used as escape places by grasshoppers, in general,
to nearly this height. Proportion out of whole environment was calculated for each
structure and background type.
Results for use and occurrence of escape places were compared by Chi-square
tests (Fowler & Cohen, 1990). The less common five morphospecies provided
insufficient data to conduct this test; instead, their observed and expected values of
use were compared. Data from morphs of the same grasshopper species (those
numbered 2, 3 and 4) were compared by Kolmogorov-Smirnov tests, which were
adequate to the small sample size (Zar, 1984).
I@uace ofaspect diversity on escape stmctun and background choice
We postulated that grasshoppers with a greater aspect diversity could remain
cryptic in more escape places, using structures and backgrounds with greater
variability. To test this hypothesis, we projected slides showing the morphospecies, and
measured aspect diversity using two perpendicular transects along the grasshoppers'
bodies, all in the same scale (Fig. 3). We measured the length of each body patch
of different colour in the transects, including patches of the same colour when apart
from each other. Endler (1984) measured crypsis of colour pattern of moths against
many backgrounds in a similar way. We calculated two diversity indices, based on
Simpson's Diversity Index, which was chosen because it emphasized larger patches
and more abundant colours. Large patches contribute more to the definition of the
prevalent colour in the insect's body, and the more abundant and prevalent colour
was expected to have an important influence on the cryptic properties of the insect.
An index for patch shape diversity (PJ was given by the formula:
CHOICE OF ESCAPE MICROHABITATS BY CRYF’TIC GRASSHOPPERS
49 1
Figure 3. Transects made through grasshoppers’ bodies to quantify ‘aspect diversity’
Where Pp=number of mm corresponding to each patch length @) divided by
the transects’ total length in mm.
This index gives a measure of mottling (small patches) vs. blotchiness (large
patches or spots). Blotchiness is related to more uniform and less disrupted coloration
patterns, which were expected to keep grasshoppers cryptic in a relatively small
number of structures, which is opposite to mottling. According to Endler (1984) the
shape of blotches on the insect’s body can influence its cryptic potential.
Another index was calculated to measure colour diversity (PJ. For this purpose,
all the patches of each distinct colour had their lengths summed to give a measure
of the abundance of this colour:
Where P,, = sum of lengths of all the patches (mm)of the same colour (co) divided
by the transects’ total length in mm.
The measures of ‘aspect diversity’ (&) was given by the product of ‘Ps’ and ‘Pc’.
&=P, x P,
Two indices were also used to quantify the diversity of escape places preferred,
one to structures (S,) and another to backgrounds (&):
Where P,, =number of observations in which a given morphospecies used structure
‘st’ divided by the total number of observations for this morphospecies.
Where Pb=number of observations in which a given morphospecies used the
background ‘b’ divided by the total number of observations for this morphospecies.
P.CABRAL ETEROVICK ETAL
492
Zona lateralis
Linea media
carina
Barred femur
/ Striped wing
Figure 4. Features and measurements related to crypsis.
An overall index for diversity in use of escape places D
(),
product of both indices:
was given by the
D,, = s,X S b
The relation between aspect diversity (&) and diversity in structures and backwas evaluated using Spearman’s correlation (Wilkinson, 1990).
grounds use Pep)
Correlations among patch shape diversity (P,), colour diversity (PJ, structures use
diversity (S,) and backgrounds use diversity ( s b ) were also examined.
Convergence of colour pattern and we of structures
We postulated that grasshoppers with similar colour patterns could use structures
in a similar way. To compare all morphospecies pairs, we considered quantitative
and qualitative features related to colour pattern and cryptic behaviour. They
included body length, the body lengthldepth ratio, presence or absence of the
colours present in the grasshoppers studied (white, light grey, dark grey, black, beige,
brown and green) and presence or absence of stripes and patches commonly found
in grasshoppers (Linea media, Carina media, Lnea scapuhris, striped wing, lateral stripe,
Xona laterah, barred femur and mottled wing; Fig. 4). Similarities between each
CHOICE OF ESCAPE MICROHABITATS BY CRypTlC GRASSHOPPERS
493
TABLE
1. Proportion of structures and backgrounds in the study site (measured in centimeters, with
folding rules on line transects). Substrates are numbered as in Figure 2. In Chi-square tests, degrees
of freedom are 5 for substrates and 8 for backgrounds
Background
types
Total
Availability in
the study site
(Yo)
GL*
DL
Ls
DS
BS
QC
16.3
20.0
6.9
5.2
10.1
25.9
2.3
6.6
6.7
53.3
37.8
62.5
32.6
52.2
27.8
70.3
27.3
89.0
17.9
11.5
7.8
8.7
17.0
12.8
1 .o
22.7
11.0
0.7
1 .8
26.1
54.8
13.4
23.0
27.9
48.6
17.4
27.8
20.3
4.9
3.6
3.8
6.6
0.2
0.3
-
-
100.0
46.4
13.5
11.6
23.3
Availability of each stNcture (“10)
~
-
~
-
1.8
-
2.0
8.4
43.3
-
2.0
3.2
-
~~
* GL =green leaves, DL= dead leaves, LS =light sand, DS =dark grey sand, BS =brown stones, QC =quartz
crystals.
morphospecies pair (S,) were obtained by Colles’ (1967) method, which makes
possible the simultaneous use of quantitative and qualitative variables:
1
s, =-c.c,,
n
Where n =number of variables considered;
Ci, = similarity between morphospecies ‘p’ and ‘q’ considering feature ‘i’
To qualitative variables: Ciw = 1 if ‘p’ and ‘q’ have the same feature ‘i’
Ci, = 0 if ‘p’ and ‘q’ don’t have the same feature ‘i’
To quantitative variables:
Where pi and qi are measures of variable ‘i’ in ‘p’ and ‘q’ and P, and Pmh
measure the total variation of this variable in the grasshopper assemblage.
Similarities in structures use were calculated for each morphospecies pair using
Symmetric Overlap Index ( o j k ) , proposed by Pianka (1973):
Where P, =relative use of structure ‘i’ by morphospecies 2’;
Pik=relative use of structure ‘i’ by morphospecies ‘k’.
We compared Colles’ indices to symmetric overlap indices for all morphospecies
pairs, using Spearman’s rank correlation.
RESULTS
The proportions of structures and backgrounds in the study site are given in
Table 1. Among the 10 morphospecies of Acrididae studied, five showed statistically
P. CABRAL ETEROVICK EIAL.
494
TABLE2. Data for use of structures and backgrounds by the five most common grasshopper
morphospecies. Preferred escape places are printed in boldface. Morphospecies are numbered as in
Figure 1
Morpho
species 2
Morpho
species 4
Morpho
species 5
Morpho
species 7
Morpho
species 8
Structures
obs
exp
obs
exp
obs
exp
obs
exp
obs
exp
Green leaves
Dead leaves
Light sand
Dark sand
Brown stones
Quartz crystals
No. of observations
20
5
8
24
1
4
28.8
8.4
7.2
14.4
1.2
2.0
43
16
32
91
1
8
88.6
25.8
22.2
44.5
3.8
6.1
63
33
5
23
0
3
59.0
17.1
14.7
29.6
2.5
4.1
95
21
0
0
0
0
53.8
15.7
13.5
27.0
2.3
3.7
42
15
30
42
9
7
67.3
19.6
16.8
33.8
2.9
4.6
P
Background
No. of observations
xz
P
191
82.83
<0.01
62
12.53
<0.05
xz
145
36.93
10.0 1
116
127
25.66
<0.01
obs
exp
obs
exp
obs
exp
obs
exp
obs
exp
14
16
1
2
4
10
3
9
5
10.4
12.8
4.4
3.3
6.5
16.6
1.5
4.2
4.3
41
58
1
2
7
55
3
16
9
31.3
38.4
13.3
10.0
19.3
49.7
4.4
12.7
12.9
23
36
2
3
4
23
9
9
18
20.7
25.4
8.8
6.6
12.8
32.9
2.9
8.4
8.5
29
19
0
0
6
26
6
4
26
18.9
23.2
8.0
6.0
11.7
30.0
2.7
7.7
7.8
14
14
4
9
14
92
1
12
0
26.1
32.0
11.0
8.3
16.2
41.4
3.7
10.6
10.7
64
15.85
<0.05
192
41.69
<0.01
127
44.20
<0.01
116
72.17
<0.01
160
92.17
<0.01
obs=tknes each morphospeciesused a structure or background to escape.
exp=tknes each morphospccies would be expected to use a given structure or background to escape due only
to this structure or background proportion in the environment.
sigdicant preferences for certain structures and backgrounds (Table 2). Fewer data
were obtained for the other five, but they also seemed to have preferences (Table
3).
Although some grasshopper forms (Nos. 2, 3 and 4)belong to the same species,
21.26,
they differed in their use of escape space appropriate to the structure (Dmax=
RO.001, df=6, 162 for Nos. 2 and 3; D,=18.61,
RO.001, df=6, 191 for Nos.
2 and 4 and D,=76.13,
RO.001, df=6, 191 for Nos. 3 and 4).Nos. 2 and 3
also differed in their use of backgrounds (D-= 12.18, RO.01, df=9, 64) as did
Nos. 3 and 4 (D,=42.53,
RO.001, df=9, 192). However, Nos. 2 and 4 did not
differ in their use of backgrounds (D-= 7.06, B0.20, df= 9, 64); they differed in
their use of escape space by using distinct structures in the same background. On
the other hand, similarities in escape space use occurred between morphospecies
belonging to different subfamilies (as in morphospecies 1 and 9, see Table 3).
The grasshoppers studied can be grouped by their escape behaviour in those
using the ground (Nos. 1, 2, 3, 4,8 and 9) and those using the grassy vegetation to
escape (Nos. 5, 6 and 7).
Grasshoppers which are grey and have mottled wings tended to use sandy grey
soils. Some of the grasshoppers matched the soil not due to their mottled wings,
but because they were the same size as patches formed by dark and light sand in
CHOICE OF ESCAPE MICROHABITATS BY CRYPTIC GRASSHOPPERS
495
TABLE3.
Data for use of structures and backgrounds by the five least common grasshopper
morphospecies. Preferred escape places are printed in boldface. Morphospecies are numbered as in
Figure 1
Morpho
species I
Structures
Green leaves
Dead leaves
Light sand
Dark sand
Brown stones
Quartz crystals
No. of observations
Background
1
2
3
4
5
6
7
8
9
No. of observations
obs
7
1
3
7
0
.
exp
obs
8.3
7
1
6
2
2.4
2.1
4.2
0.4
0.6
0
Morpho
species 3
Morpho
species 10
obs
exp
obs
exp
ohs
exp
7.4
16
12
0
0
0
0
13
3.8
3.2
6.5
0.6
0.9
3
1
5
7
0
0
7.4
2.2
1.9
3.7
1
5
6
0.3
1
0
7.0
2.0
1.7
3.5
0.3
0.5
0.5
16
18
Morpho
species 9
exp
2.2
1.9
3.7
0.3
0
0
Morpho
species 6
0.5
2
15
16
28
obs
exP
obs
exp
obs
exp
obs
exp
obs
1
5
0
0
1
2.9
2.8
3.4
5
4
4.6
2.0
2.4
0
0
1.2
1
1
2
0.8
0.6
I .8
2
4.7
0.4
1.2
1.2
6
0
0
3
0.9
1.7
4.4
0.4
1.1
1.9
1.5
2.8
7.3
0.6
I .8
1.9
0
1
0
0.9
1
4
0
1
0
8
1.2
3.1
0
1
0
0.3
0.8
0
0
2
13
0
0
0.8
0
-
3.6
1.3
8
1
I
1
18
1.1
17
5.6
0
2
0
2
13
28
12
exp
2.4
3.0
I .o
0.8
1.5
3.9
0.3
1.0
1.0
15
obs = times each rnorphospecies used a structure or background to escape.
exp = times each rnorphospecies would be expected to use a given structure or background to escape due only
to this structure or background proportion in the environment.
the mosaic soil of background 6 (see also Schultz, 1986). Ground-users also have
barred femora and/or dorsal stripes (Linea media, Carina media, striped wings), which
seem to function as disruptive coloration (Cott, 1940) and so allow grasshoppers to
use dark as well as white sand or quartz crystals to avoid detection.
It is also interesting to notice that grasshoppers with small green patches or stripes
(Nos. 1 and 3) used relatively more grass leaves than those with a similar pattern of
patches but no shades of green (Nos. 2 and 4).This reinforces the importance of
coloration in their choice of escape places.
Grasshoppers with a predominance of green or brown and beige colours (Nos.
5 , 6 and 7) often have lateral stripes and used only green or dead grass blades to
escape. The two species of Leptysminae matched grass blades not only in their
colours, but also in the elongated body shape and the positioning of their bodies
and antennae parallel to leaves.
The grasshoppers of morphospecies No. 10 were the only ones that did not follow
any of the tendencies described above. They seem to have another escape strategy:
when they jump to escape, they show a bright red spot on the second pair of wings
and hide it just before settling down.
It is important to stress that during escape many individuals from all morphospecies
when landing on a structure which did not match their colour pattern, walked
immediately to another, better matching substrate. This suggests an active structure
choice.
There was an upper limit to the number of different morphospecies using the
496
P. CABRAL ETEROVICK E T A .
20
40
60
80
100
Aspect diversity (Ad)
Figure 5. Relation between diversity in use of structures and backgrounds and aspect diversity in
acridid morphospecies.
same escape place. Morphospecies using the same structure did not exceed 5
(mean=3.33, s = 1.63). The largest number of users of a background was also 5
(mean = 3.33, s = 1.37).
More ‘aspect diverse’ morphospecies tended to use more structure and background
types, though the correlation between ‘aspect diversity’ (&) and diversity in use of
was not significant at critical value of 0.05 (r,=0.60, -0.10,
escape places Pep)
n = 10) (Fig. 5). No correlation was found among patch shape diversity (P,), colour
diversity (PJ, diversity in use of structures (S,) and diversity in use of backgrounds
(sb)*
Similaritiesamong grasshoppers’ colour pattern (Table 4) were positively correlated
to their convergence in use of structures (Y= 26.4 1 O.42Xy&0.005, n = 45) (Fig.
6). The maximum colour pattern similarity between morphospecies pairs (mean=
0.85, s =0.085) was smaller than the maximum similarity in the use of structures
(mean=0.92, s =0.087).
+
DISCUSSION
The correspondence of an insect’s colour pattern with its background helps it to
avoid detection by visually-orientedpredators (Dearn, 1981;Schultz, 1981;Feltmate,
Williams 8z Montgomerie, 1992). Avoidance of visually-oriented predators can be
the selective factor responsible for the existence and maintenance of polymorphism
in a species, when each form uses a Werent microhabitat (Sandoval, 1994). This
kind of divergence occurred in the polymorphic species of Rhammatocm studied
here.
We found that cryptic grasshoppers using the same structure still differ among
themselves, in spite of being more distinct from morphospecies using other structures.
It suggests that apostatic selection has been maintaining morphological diversity
in this grasshopper assemblage, as maximum similarity of appearance among
morphospecies using the same structure does not quite reach the level of similarity
CHOICE OF ESCAPE MICROHABITATS BY CRYPTIC GRASSHOPPERS
497
TABLE
4. Morphospecies characterization according to quantitative and qualitative features and
preferred structures and backgrounds
Morphospecies
Qualitative features
Colours
White
Light grey
Dark grey
Black
Beige
Brown
Green
Othen
Lima mulia
Catina mdia
Linca stapulnris
Striped wing
Lateral stripe
<ow lntcralis
Barred femur
Mottled wing
Quantitative features
Length (mm)
Width (mm)
1
2
3
+*
+
+
+
+
+
+
+
4
5
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
34
8
36
7
32
7
33
6
6
+
+
+
+
+
+
7
8
+
+
+
+
+
+
+
9
+
+
+
+
+
+
+
+
+
23
4
+
+
+
+
+
+
0
+
+
+
+
+
+
+
+
+
+
+
21.5
5
24
5
47
11
+
25
34
2 . 5 3
1
* + =presence of the considered feature.
100
'8P
p
40
30
0
20
0
I
20
I
I
I
40
60
80
Morphological similarity (Spq)
100
Figure 6. Relation between similarity in use of structures and colour pattern similarity in acridid
morphospecies.
in their use of structures. A higher similarity among the grasshoppers could increase
predation levels upon them (see Rand, 1967).
Sandoval (1994) found that grey forms of Z m a cristim have a preference for
grey and brown resting places, and Gill (1979) studied a form of Chorthippus brunneus
498
P. CABRAL ETEROVICK ETAL.
with mottled wings which spent most time on the ground, just like the grey mottled
grasshoppers studied here. It seems that mottled wings perfectly match the sand
texture, causing cryptic coloration to be very efficient. Gill (1979) also described a
morph of Chorthippus brunneus with striped wings that frequently rested on leaves,
and Samdoval (1994) found a preference for green leaves in a green morph of
limema cridnae. In the present study, longitudinal stripes seemed to be associated
with the use of leaf blades, in which the insects rest parallel to the blade so their
stripes align with the margins of the leaves. Cott (1 940) also described this behaviour
for A c d u turrita. The species of Leptysminae studied can be considered specialists
in the use of grass blades, due to their uniform colour, lateral stripes, and resting
behaviour, features that make them remarkably cryptic on grass blades. Morphospecies No. 10, in spite of choosing escape places in which it was not so cryptic,
had another kind of escape behaviour, showing a bright red spot while flying. When
the grasshoppers landed, they hid the spot and became difficultto see. This kind of
display, named flash-colour, is common among grasshoppers (Vasconcellos-Neto,
pers. observ.). It attracts a predator’s attention and then suddenly disappears,
confusing the predator and making prey location difficult (Cott, 1940).
Joern & Lawlor (1981) also defined two guilds of grasshoppers in the southern
United States, based on microhabitat use: those using the ground and those using
the vegetation to escape. They found a maximum of five species in each microhabitat
in Marathon and three in the Sul Ross Mountains, which they related to the
grasshopper guild structure. Organization of an assemblage in escape strategy guilds
can be due to predation pressures in evolutionary time (Ricklefs & O’Rourke, 1975).
We also found a maximum of five grasshoppers using the same escape places. It
may exist an upper limit to the number of grasshopper morphological units which
can use the same escape place in assemblages structured based on cryptic properties.
It would be interesting to look for this limit in grasshopper assemblages from other
different habitats.
Orthoptera species that use the ground as escape space tend to be more widely
distributed in a habitat than those using plant species (Sandoval, 1994). In the
present study, however, the distribution of grasshoppers among backgrounds seemed
to be more related to body coloration than to the structure used. Some grasshoppers
which preferred to use grass blades and have a more variegated colour pattern
(morphospecies No. 5 ) occurred in a greater variety of backgrounds than other less
variegated grasshoppers found on the ground (Nos. 8 and 9) (Fig. 5). The advantage
of aspect diversity may be that the variety of colours and shapes of patches on the
insect’s body makes crypsis possible on a greater variety of backgrounds and
structures. The colour on the insect that matches a part of its background may
disrupt the outline of the body so that predators cannot detect it. Specialists, on the
other hand, must remain associated with the structure to which they are adapted
in order to maintain their cryptic potential. However, specialists, which always rest
on a specific structure, are less likely to be found by generalist predators. Thus, a
trade-off between predation avoidance efficiency and behavioral plasticity may exist
in cryptic grasshoppers.
ACKNOWLEDGEMENTS
We are grateful to W.W. Benson, G.W. Fernandes, M.A. Marine, R.P. Martins
and D. Yanega who kindly read the manuscript and gave helpful suggestions. We
also thank D. Yanega for revision of the English.
CHOICE OF ESCAPE MICROHABITATS BY CRYPTIC GRASSHOPPERS
499
REFERENCES
Colles DH. 1967. An examination of certain concepts in phenetic taxonomy. systematic <oology 16:
6-2 7.
Cott HB. 1940. Adaptive coloration in animals. London: Methuen.
DearnJM. 1981. Latitudinal cline in a color pattern polymorphism in the Australian grasshopper
Phaularridium uittutum. Hmdi& 47: 1 1 1-1 19.
Endler JA. 1978. A predator view of animal color patterns. Euohtionaly Biology 11: 319-364.
Endler JA. 1984. Progressive background in moths, and a quantitative measure of crypsis. Biological
Journal ofthe Lintuan So&& 22: 187-231.
Feltmate BW, Williams DD, Montgomerie A. 1992. Relationship between diurnal activity
patterns, cryptic coloration, and subsequent avoidance of predaceous fish by perlid stoneflies.
Canadian Journal of F k h s and Aquatic Sciences 49: 263Ck2634.
Fowler J, Cohen L. 1990. Practical stutktisforjeld biology. Philadelphia: Open University Press.
Gill PD. 1979. Color-pattern variation in relation to habitat in the grasshopper Chorthippus brunneur
(Thurnberg). Ecological Entomology 4: 249-257.
Giulietti AM, Menezes NL, PiraniJR, Meguro MyWanderley MGL. 1987. Flora da Serra do
Cip6, Minas Gerais: caracterizaq2o e lista de espkcies. Bobtim Botcinico, Uniuersidade de Sao Paulo 9:
1-151.
Joern A, Lawlor LR. 1981. Guild structure in grasshopper assemblages based on food and microhabitat
resources. Oikos 37: 93-104.
Papageorgis C. 1975. Mimicry in Neotropical butterflies. American Scientist 63: 522-532.
Pianka ER. 1973. The structure of lizard communities. Annual Review ofEcology and Syslematics 4:
53-74.
Rand AS. 1967. Predator-prey interactions and the evolution of aspect diversity. A& do Simpdsio sobre
a Biob Ama&ica 5: 73-83.
Ricklefs RE, O'Rourke K. 1975. Aspect diversity in moths: a temperate-tropical comparison.
Evolution 29: 3 13-324.
Rocha CF, Bergallo HG. 1994. I: torqualm (Collared Lizard) diet. Herpetological Revieu, 25: 69.
Sandoval C. 1994. Differential visual predation on morphs of limema &tinae (Phasmatodeae:
Timemidae) and its consequences for host range. BiologicalJournal ofthe Linnean So&& 52: 341-356.
Sazima I, Bokermann WCA. 1977. Anfibios da Serra do Cip6, Minas Gerais, Brasil. 3: ObservaqBes
sobre a biologia de Hyla aluamgai Bok. (Anura, Hylidae). Re&tu Brm'kira de Biologia 37: 41 3 4 1 7.
Schultz JC. 1981. Adaptive changes in antipredator behavior of a grasshopper during development.
Euolution 35: 175-1 79.
Schultz JC. 1986. Role of structural colors in predator avoidance by tiger beetles of the genus Cicindela
(Coleoptera: Cicindelidae). Bulbtin ofthe ESA (Fall):142-146.
Tinbergen N. 1957. Defense by color. Scimtjfic American 197: 49-55.
Vasconcellos-Net0 J. 1987. GenCtica ecobgica de C h b o r p h a cribaria F. 1775 Cassidinae, Chrysomelidae. PhD. Thesis, Universidade Estadual de Campinas, Silo Pado, Brazil.
Willtinson L. 1990. SYSTAE 2% g s h f o r stutistics. Evanston, I L Systat Inc.
Zar JH. 1984. Biostutistical anahh. Englewood Cliffs, New Jersey: Prentice-Hall.