1
Motion-triggered defensive display in a Tephritid fly
2
1,3Samuel
Aguilar Argüello, 1Francisco Díaz-Fleischer, 1,2Dinesh Rao
3
4
1Inbioteca
5
Universidad Veracruzana,
6
Av. Culturas Veracruzanas No.101,
7
Col. E. Zapata, CP 91090,
8
Xalapa, Veracruz, México
9
10
3Current
address, Instituto de Ecología, A.C,
11
Apartado Postal 63, CP 91000
12
Xalapa, Veracruz, México
13
14
2Author
for Correspondence; dinrao@gmail.com
15
1
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
ABSTRACT
Interactions between prey and predators are often mediated by signals sent by
the prey. Passive signals such as aposematic colouration, and active signals such as
pursuit deterrence signals are thought to prevent attack from predators. In true
fruit flies (Diptera: Tephritidae), the defensive wing display is called supination, and
studies have shown that supination effectively reduces the chance of being attacked
by salticid predators. In this study, we investigated the proximal causes of
supination in staged interactions in an arena. We asked whether the movement of
the display target influences the likelihood of triggering supination in the Mexican
fruit fly Anastrepha ludens. We tested the effect of motion on fly display in three
different ways using 1. a manually moved dead spider or beetle, 2. live bouts with a
spider and a katydid, and 3. video playback experiments where movement of the
display target was controlled. Our results show that flies are more likely to perform
supination when the display target moves. The identity of the display target did not
influence display propensity suggesting that the supination of flies is a generalized
display behaviour against any possible threat.
32
33
Keywords: supination, jumping spiders, aggressive behaviour, Anastrepha ludens
34
35
2
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
INTRODUCTION
Interactions between prey and predators are often mediated by signals sent by
the prey. These signals can be passive (e.g., aposematic colouration, (Bond 2007)) or
active (e.g., honest signals, (Zahavi and Zahavi, 1997)). In active signalling, there
may also be an element of deception, wherein a prey can send misleading
information to the predator. Prey can also signal to predators to interrupt an attack
(e.g., startle displays, (Ruxton et al. 2004)) or to prevent the launch of an attack (e.g.,
pursuit deterrence, (Caro, 1995)). By signalling the relative difficulty in prey
capture, the prey benefit by thwarting an attack, and the predator can benefit by
conserving energy and redirecting its attack towards a facile prey. Active signalling
to avoid predation has been documented in a taxonomically wide variety of animals
such as tail-wagging in mot mots (Murphy 2006), tail flagging in ground squirrels
(Rundus et al. 2007), inspection behaviour in guppies (Godin and Davis 1995) and
the shimmering behaviour of the Asian hive bee (Tan et al. 2012).
Interactions between jumping spiders (Araneae: Salticidae) and the true fruit
flies (Diptera: Tephritidae) are an example of a system where a prey signals to the
predator and successfully avoids attack. In this system, flies perform a wing display
called supination, where the fly brings the wings forward, perpendicular to the long
axis of the body, while the ventral surface of the wing is turned to face anterior of
the fly such that the costal margin of the wing is dorsal (Headrick and Goeden 1994,
Supplementary Video S1). Supination can be asynchronous or synchronous, i.e., it
can occur with both wings simultaneously or sequentially (Headrick and Goeden
1994). This display is common in both male and female flies and has been observed
during conspecific interactions (Briceno et al. 1999; Headrick and Goeden 1994,
Benelli 2013, 2015, Benelli et al. 2014). Supination has been found effective in
preventing an attack in 4 species of flies against up to 25 species of salticids (Greene
et al. 1987; Hasson 1995; Mather and Roitberg 1987; Rao and Díaz-Fleischer 2012).
The signalling is thought to be deceptive in function, since the flies have bands on
their wings which, when viewed from a certain angle, mimics the leg patterns of the
spiders (Eisner 1985). The display of the flies may mimic the courtship or
aggressive displays of jumping spiders. This hypothesis, termed the predator
mimicry hypothesis because the flies purportedly mimic their predators, has been
invoked to explain the functional significance of these displays (Greene et al. 1987;
Mather and Roitberg 1987). However, there are unresolved questions with respect
to the hypothesis. Firstly, salticids are known to kill other salticids (Jackson 1977),
3
71
72
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
91
and the mere spider-like appearance of a fly is not enough to grant it complete
immunity from attack. However, the spider-like appearance may contribute to
confusion on the part of the spider and thus allow sufficient time for the fly to
escape, akin to evasive mimicry or imperfect mimicry (Ruxton et al. 2004). Secondly,
the display is successful against a range of salticid species, even though salticid
displays are highly species specific (Elias, Land, Mason, and Hoy 2006). Thirdly,
though most true fruit flies have banded wings (Sivinski and Pereira 2005), the
display is seen even in species that are lightly banded. In previous experiments, we
established that the appearance of the bands was not as important as the display
itself in order to prevent an attack (Rao and Díaz-Fleischer 2012).
Why do the flies display to predators? The display was found to be ineffective
against non-salticid predators such as preying mantids, lizards and assassin bugs
(Greene et al. 1987). The display is also used in aggressive interactions with
conspecifics. Therefore this display may be a reaction to the presence of any
potential aggressor, and not necessarily directed to a specific predator such as a
spider. In this study, we sought to investigate the proximate causes of supination in
the tephritid fly Anastrepha ludens. In particular, we hypothesised that the display is
triggered by the motion of the display-target rather than its identity. If motion is the
proximate trigger for the supination display, then the fly should display regardless
of the source (spider or control) or type of the motion (manually moving objects,
live animals or video playback).
92
93
94
95
96
97
98
99
100
101
102
103
104
105
Methods
In this study we used the large jumping spider, Phidippus audax (Araneae:
Salticidae), which is distributed all across North America (Edwards 2004), and
frequently found in citrus orchards, where it is likely to encounter tephritid fruit
flies. Female spiders (mean body length: 10.93 mm) are bigger than males (mean
body length: 8.39 mm) (Edwards 2004). The abdomen is generally black with a
white spot, though there is some variation in colour in this species (Edwards 2004).
Spiders were collected from an abandoned maize plantation on the outskirts of
Xalapa, Veracruz, Mexico. They were brought to the laboratory of the Inbioteca
campus of the Universidad Veracruzana in Xalapa and housed individually in small
plastic containers (7 cm diameter x 5 cm height). Spiders were fed grasshoppers
weekly and watered every three days. Mass-reared Anastrepha ludens flies were
obtained from the MoscaFrut plant in Metapa de Dominguez, Chiapas. Flies were
4
106
107
108
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125
126
127
128
129
130
131
132
133
134
135
136
137
138
139
acquired as pupae and were allowed to emerge in wooden cages (30 x 30 x 30 cm)
covered in mesh cloth within the laboratory. Flies were fed yeast hydrolysate and
sugar (proportion 1:3) ad libitum. There is sexual dimorphism in Anastrepha ludens
flies since female flies (total body length; mean ± std. dev.: 9.99 ± 0.46 mm) are
larger than male flies (total body length; mean ± std. dev.: 7.40 ± 0.49 mm), and can
be distinguished by the presence of an ovipositor (Tejeda et al. 2014).
Experimental Design
All experiments were carried out in the laboratory under natural light conditions
from 10 am to 4 pm. Flies were chosen randomly from a holding cage for each
experiment and each fly was used only once. Flies were not mated. In all
experiments, flies were introduced into the test arena first and allowed to
acclimatise for 1 min. All experiments were recorded with a Sony HDR-XR260 video
camera from above.
Experiment 1: Manual movement
In this experiment, we tested whether male and female flies (n = 60) would
respond to movement. One spider and one beetle were used for this experiment.
The animals were anaesthetized with CO2 and subsequently frozen. We used a dead
female spider and mounted it with wax on a small circular disc on a wooden
platform. The disc was moved by means of a lever placed at the base of the platform.
The arena consisted of a petri dish (9 cm diameter and 1.3 cm height). As a control,
we used a dead beetle (Calosoma sp.; Coleoptera: Carabidae) of similar size and
colour as the spider. Each interaction trial lasted for 3 min. There were two
treatments: Moving and Still Treatments. For the Moving treatments, the disc was
rapidly rotated when the fly was facing the spider or the beetle. During the Still
treatment, the disc was not moved. The models were rotated only when the fly was
facing it, extending to an angle approximately 45 degrees on either side. We
imported the video clips to an Apple iMac computer and recorded the following
variables: presence or absence of displays, rate of display, bout duration (time from
initiation of interaction to outcome) and proportion of flies that displayed. We
analysed the data with a full factorial Generalized Linear Models, with link functions
according to the distribution of the response variable. The p values of the whole
model correspond to the comparison between the model to the model that contains
only the intercept parameter. Analysis was carried out in JMP v9.
Experiment 2: Live bouts
5
140
141
142
143
144
145
146
147
148
149
150
151
152
153
154
155
156
157
158
159
160
161
162
163
164
165
166
167
168
169
170
171
172
173
174
In this experiment, male (n = 62) and female (n = 58) flies were placed into a
plastic petri dish (14 cm diameter, 2.5 cm height). The petri dish was divided into 2
partitions, separated by an opaque divider. Flies were introduced first into one of
the partitions and the order of introduction (i.e. left or right) was randomised.
Spiders or a control (a katydid) were introduced into the opposite partition
(Supplementary Video S1,2). The katydid was chosen as a control due to its easily
quantifiable sudden movements (pers. obs, Rao. D.). Both animals were allowed to
acclimatize for a minute. Once the trial started, the divider was removed, and the
interaction was filmed from above. The following variables were recorded: presence
or absence of displays, number of displays, presence or absence of movement of the
animals (we considered only movements that involved a change in position, i.e. we
did not include movement of body parts). From the video clips we recorded: bout
duration, the distance at which the fly initiated display (Display Initiation Distance)
and the distance at which the fly escaped or walked away (Flight Initiation
Distance). Distances were measured using the software GraphClick Ver 3.0. We
analysed the data with full factorial Generalized Linear Models, with link functions
according to the distribution of the response variable. The p values of the whole
model correspond to the comparison between the model to the model that contains
only the intercept parameter. Distance data were analysed using a standard least
squares fit model.
We recorded the onset of spider or katydid movement (after approximately 5
seconds of inactivity), fly attention (defined as the moment when the fly detected
the presence of the spider or katydid and moved to face the spider by positioning its
body directly at the animal), display (when the fly finished a display cycle, defined
as from one outstretched wing pose to another outstretched wing pose), end of fly
attention and end of movement. These variables were analysed using the event
recording software JWatcher Ver 1.0 (Blumstein and Daniel, 2007). We performed
an analysis of non-repeating sequences to test whether a given behaviour was more
likely to be followed by another. We computed transitional probabilities for two key
behaviour sequences: movement followed by fly attention, and fly attention
followed by display. To test whether these probabilities were significant, we
obtained the Z-scores (adjusted residuals) of the sequence analysis. These Z-scores
were calculated using a log-linear analysis for data with structural zeros using the
software iLog ver 4.0 (Bakeman and Robinson 1994). Z-scores greater than 1.96 are
considered significant at the 0.05 level (Bakeman and Gottman 1986).
6
175
176
177
178
179
180
181
182
183
184
185
186
187
188
189
190
191
Experiment 3: Video playback
We recorded short clips of spider and katydid movement and configured these
clips to play on an Apple iPod Touch (Supplementary Video S3). As a control we
used a still image of a spider or a katydid. The iPod was integrated into one wall of
an arena (15 x 15 x 7 cm). Male and female flies (n = 60) were introduced into the
arena and the interactions were filmed from above. The trials lasted 3 min. We
recorded the number of displays, bout duration, fly attention (while facing the
screen) and the onset of these behaviours.
Data Analysis
We analysed the data with a full factorial Generalized Linear Models, with link
functions according to the distribution of the response variable (Crawley, 1993;
Agresti, 2007). Count data were analysed using a generalised linear model (GLM)
with Poisson errors, a log-link function and type III significance tests. For binary
data, we used binomial errors and logit-link function and type III significance tests.
The p values of the whole model correspond to the comparison between the whole
model and the model that contains only the intercept parameter. Contrasts were
used to test for differences in levels within variables.
192
193
194
RESULTS
195
Experiment 1: Manual movement
196
197
198
199
200
201
202
203
204
205
206
207
208
Fly display (presence or absence) was significantly triggered by the factors (i.e.,
movement, sex of the fly or the display target) in the model (GLM, binomial
distribution, Logit Link: 2 = 20.32, df = 7, p = 0.005; Fig 1A). Of these factors, sex of
the fly, movement and the interaction between display target and movement were
significant (Table 1). Female flies (probability 0.90) displayed more than male flies
(probability 0.79). Flies were more likely to display to a still beetle (mean
probability of display: 0.85 ± 0.05) than to a moving beetle (mean probability of
display: 0.59 ± 0.14), but this was not seen in the case of the spider (still: 0.66 ±
0.09; moving: 0.63 ± 0.13). Post hoc contrasts revealed that there were significant
differences between movement and still treatments (2 = 6.6, p< 0.001) and no
significant differences between beetle and spider (2 = 2.4, p = 0.12).
There was a significant effect of the factors on bout duration (GLM, Poisson
distribution, Log link, 2 = 35.73, df = 7, p < 0.0001). Of these factors, movement and
7
209
210
211
212
213
214
215
216
217
218
219
220
221
222
223
224
225
226
227
228
229
230
231
232
233
234
235
236
237
238
239
240
sex of the fly were significant (Table 1). There was also a significant effect of the
interaction between the display target and the sex of the fly, as well as between
movement and display target (Table 1). Female flies displayed for longer against
beetles (Mean ± S.D.; 6.1 ± 3.5 s;) than against spiders (Mean ± S.D.; 4.15 ± 1.08 s),
Male flies displayed for longer against spiders (Mean ± S.D.; 7.01 ± 0.08 s) than
against beetles (Mean ± S.D.; 6.45 ± 2.25 s). However, neither was significant in
post-hoc contrast analysis.
Post-hoc contrast analysis showed that flies displayed for significantly longer to
beetles when there was no movement (Mean ± S.D.; Still: 8.3 ± 0.38 s; Moving: 4.23 ±
0.86s, 2 = 18.50, p< 0.0001), while they displayed for similar durations to spiders
irrespective of movement (Mean ± S.D.; Still: 5.99 ± 1.52 s; Moving: 5.17 ± 2.52s, 2 =
1.97, p = 0.16).
There was no significant effect of the three factors on display rate (GLM, Poisson
distribution, Log link, Χ2= 1.1, df = 7, p = 0.99).
Experiment 2: Live bouts
During live bouts, flies did not significantly differ in their propensity to display
(GLM, binomial distribution, Logit Link: 2 = 2.56, df = 3, p = 0.463); and this pattern
was seen whether the display target was a spider or a katydid or whether the fly
was male or female (Table 2). There was a significant effect of the factors on bout
duration (GLM, Poisson distribution, Identity Link: 2 = 29.01, df = 3, p < 0.0001).
For bout duration, both the display target (Katydids: Mean ± S.D. = 14.14s ± 12.01;
Spiders: Mean ± S.D. = 11.68s ± 8.66) and the sex of the fly (Males: Mean ± S.D. =
14.61s ± 11.79; Females: Mean ± S.D. = 11.27s ± 8.79; Table 2) were significant.
There was no significant effect of display target or sex of the fly on the rate of
display (GLM, poisson distribution, Log Link: 2 = 0.908, df = 3, p = 0.823; Table 2).
Display Initiation Distance (Least squares fit, R2 = 0.06, F 3, 76, p = 0.202) and the
Flight Initiation Distance (Least squares fit, R2 = 0.06, F 3, 76, p = 0.158) were not
significantly different according to whether the flies displayed to a spider or a
katydid.
Flies were significantly more likely to display when the spider or katydid moved.
The relevant transitions of behaviour along with the Z-scores are presented in Fig. 2.
Experiment 3: Video playback
8
241
242
243
244
245
246
247
248
249
250
251
252
253
254
255
256
257
The likelihood of display was influenced by the factors (GLM, binomial
distribution, Logit Link: 2 = 54.71, df = 7, p < 0.0001). Of the three factors, i.e. sex of
the fly, movement or identity of display target, only movement significantly
influenced presence of display (Table 3). Flies were more likely to display to a
moving video clip (Fig. 1B). There was no significant effect of sex of the fly or the
display target or the interactions (Table 3).
Bout duration was significantly influenced by the factors (GLM, Poisson
distribution, Log link, 2 = 359, df = 7, p < 0.0001). Of the factors, both the display
target and movement influenced the length of the bouts (Table 3). All interactions
were significant (Table 3). Post hoc contrasts revealed that there were significant
differences between movement and still treatments (2 = 114.56, p< 0.001). Bouts
by female flies were longer against katydids and spiders when there was movement
(predicted value: 34.27 s). On the other hand, male flies displayed for longer against
katydids when there was movement (predicted value: 31.06 s), but not against
spiders (predicted value: 15.33 s).
The rate of display was not significantly influenced by the factors (GLM, Gaussian
distribution, Identity Link: 2 = 1.98, df = 7, p = 0.961; Table 3).
258
259
260
261
262
263
264
265
266
267
268
269
270
271
272
DISCUSSION
In all three experiments, fly displays were triggered by the motion of the display
target, irrespective of the type of motion — manual, live or video playback. Our
results suggest that rather than being a predator-directed display (Greene et al.
1987), supination in A. ludens is a generalized display against any potential threat
and is primarily triggered by motion.
A potential drawback of our methodology lies in the fact that we did not use
multiple examples of the target in experiments 1 and 3. There is the possibility that
the spiders were responding to the target individual in question and not the
movement per se. However, since the treatments are very distinct (i.e. still and
movement), we can consider the response of the fly as representative. Further
studies should incorporate several exemplars in order to resolve this issue.
Of all the display parameters measured, the likelihood to perform display was
influenced by movement across the three experiments. However, other parameters
9
273
274
275
276
277
278
279
280
281
282
283
284
285
286
287
288
289
290
291
292
293
294
295
296
297
298
299
300
301
302
303
304
305
306
such as bout duration and rate of display were also significant. In terms of
interactions between factors, from the manual movement and video playback
experiments, it was apparent that male and female flies do not respond similarly to
the stimulus, which is understandable since they have different needs and
motivations. In A. ludens, there is a lek mating system where courting males guard
non-resource territories and wait for the approach of females. Aggression between
males is more likely at this stage; whereas between females aggression may be more
likely over oviposition locations (Benelli 2015).
From the fly point of view, the display seems to have various functions. The
primary use is against conspecifics in aggressive encounters (Headrick and Goeden
1994). Male flies could use this encounter to evaluate opponents in contests, as seen
in the displays of the stalk-eyed flies (Worthington and Swallow 2010).
Furthermore, the looping side-to-side movement (described in Rao and DíazFleischer 2012) could also serve as a mechanism where the fly integrates sufficient
visual information in order to make a decision regarding the threat level of the
opponent. By observing the target from various angles, the fly could increase the
visual information available to it. It is conceivable that the fly fails to recognise the
jumping spider as a threat until it accumulates sufficient visual input. In the manual
movement experiment, flies displayed even to spiders in the non-moving treatment,
suggesting that movement is not the sole trigger for performing a display, but
perhaps is the dominant component. If we consider that bout duration is a proxy for
time needed to ‘recognize’ the identity of the opponent, flies vary in detection ability
based on the stimulus and the context. These ideas need to be tested further in more
detail.
A multi-stage anti-predator behaviour would help flies to reduce the risk of
predation but also to increase the quality of information with regards to the actual
risk as seen in fiddler crabs Uca vomeris McNeil (Hemmi and Pfeil 2013). When
displaying, flies may collect qualitatively different visual information during
successive stages of their display sequence. Furthermore, since displays are usually
linked to aggression in various species of Tephritidae (Benelli 2015), they may
contain an additional function of deterrence. In this scenario, the trigger for
acquisition of information is the movement of the opposing organism.
In earlier experiments with this species, we established that the deterrence effect
of supination against salticid predators was largely due to the display itself rather
10
307
308
309
310
311
312
313
314
315
316
317
318
319
than the appearance of the wings or the body condition of the fly (Rao and DíazFleischer 2012). This result calls into doubt the predator mimicry hypotheses as an
explanation for the interaction between salticids and tephritid flies. If the aim of the
display is to ‘confuse’ the salticid into misidentifying the fly as another spider, then
the fly by using the same display against various non-salticid predators (Greene et
al. 1987), is hedging its bets that the main predator it will encounter will be
salticids. While there is some evidence that salticids could be one of the main
predators of another tephritid fly, Zonosemata vittigera (Greene et al. 1987), they
are not the only predators of tephritid flies. On the other hand, by mimicking a
salticid, flies could deter attack from potential salticid-averse predators. We suggest
that the supination behaviour primarily arose from intraspecific aggressive
interactions and the deterrence effect on salticids is a side effect of the visual biases
of jumping spiders.
320
321
322
323
324
325
326
327
328
329
ACKNOWLEDGEMENTS
We thank Diana Pérez-Staples, Ajay Narendra and anonymous reviewers for
valuable comments on an earlier version of this manuscript. Thanks to Pablo Nuñez
Berea for help in rearing the spiders and Dina Orozco (Subdirector of Production,
MoscaFrut) for flies. We thank Quiyari Santiago for identifying the beetle. This
project was funded by a Ciencia-Basica CONACyT grant (No. 168746) to DR.
330
331
11
332
333
334
TABLES
Table 1: Summary of the statistics for experiment 1 with manual movement.
Significant p values are in bold.
Display
Bout Duration
Display Rate
Χ²
p
Χ²
p
Χ²
p
Display Target
2.26
0.13
0.81
0.37
0.21
0.64
Sex of the fly
6.6
0.01
9.38
0.002
0.2
0.65
Movement
6.56
0.01
16.24
< 0.0001
0.02
0.89
Display Target
* Sex of the fly
0.01
0.91
3.91
0.04
0.001
0.97
Sex of the fly *
Movement
0.09
0.75
2.74
0.09
0.15
0.69
Display Target
* Movement
5.08
0.02
5.21
0.02
0.02
0.86
Display Target
*Sex *
Movement
0.68
0.41
0.01
0.91
0.64
0.42
Variable
335
336
337
Table 2: Summary of the statistics for experiment 2 with live bouts. Significant p
values are in bold.
Display
Variable
Χ²
Bout Duration
p
Display Target
0.46
0.49
Sex of the fly
2.06
0.15
Display Target
* Sex of the fly
1.63
0.99
Χ²
p
8.00
0.0047
15.95 < 0.001
3.58
338
339
340
341
342
343
344
345
346
12
0.058
Display Rate
Χ²
p
0.11
0.74
0.39
0.53
0.57
0.44
347
348
Table 3: Summary of the statistics for experiment 3 with video playback. Significant
p values are in bold.
349
Display
Bout Duration
Χ²
p
Χ²
Display Target
0.36
0.54
40.53
Sex of the fly
1.15
0.28
2.72
Movement
52.94
< 0.001
Display Target
* Sex of the fly
0.12
Sex of the fly *
Movement
Variable
p
Display Rate
Χ²
< 0.0001 0.00008
0.99
0.06
0.79
114.56 < 0.0001
1.19
0.27
0.72
12.05
0.0005
0.02
0.88
0.76
0.38
11.28
0.0008
0.04
0.83
Display Target
* Movement
0.16
0.68
9.33
0.0022
0.12
0.72
Display Target
*Sex *
Movement
0.37
0.54
70.24
< 0.0001
0.34
0.55
350
351
352
353
354
355
356
357
358
359
360
361
362
363
13
0.09
p
364
FIGURES
365
366
367
368
Figure 1A: The numbers of flies displaying were significantly different according to
movement. See Table 1 for details.
369
370
371
Figure 1B: The number of displays of the flies was significantly different according
to movement, but not between the spider and the katydid. See Table 3 for details.
372
373
374
375
Figure 2: Ethograms of fly response to (A) spiders and (B) katydids during live
bouts. Numbers on the arrows represent the transitional probabilities with Z-scores
in parentheses. Negative Z-scores imply that the values are below the mean.
376
377
14
378
379
380
381
382
383
384
Supplementary Material
S1 Video demonstrating the defensive display of the tephritid fly Anastrepha ludens
against a jumping spider Phidippus audax
S2 Video demonstrating the display of the tephritid fly Anastrepha ludens against the
katydid. Note the initiation of the display when the katydid moves.
S3 Video demonstrating the display of the fly against a moving spider on the
playback video screen.
15
385
386
387
388
389
390
391
392
393
394
395
396
397
398
399
400
401
402
403
404
405
406
407
408
409
410
411
412
413
414
415
416
417
418
419
420
421
422
423
424
425
426
REFERENCES
Agresti, A. (2007) An Introduction to Categorical Data Analysis. New Jersey:Wiley–
Interscience.
Bakeman R, Gottman JM (1986) Observing interaction. An introduction to sequential
analysis. Cambridge, UK: Cambridge University Press.
Bakeman R, Robinson BF (1994) Understanding log-linear analysis with ILOG: An
interactive approach. Hillsdale, NJ: Erlbaum.
Benelli G (2013) Aggressive behavior and territoriality in the Olive Fruit Fly,
Bactrocera oleae (Rossi) (Diptera: Tephritidae): Role of residence and time of
day. J Insect Behav 27:145-161
Benelli, G. (2015) Aggression in Tephritidae flies: Where, when, why? Future
directions for research in Integrated Pest Management." Insects 6:38-53.
Benelli G, Daane KM, Canale A, Niu C-Y, Messing RH, Vargas, RI (2014) Sexual
communication and related behaviours in Tephritidae: current knowledge
and potential applications for Integrated Pest Management. J Pest Sci 87:385405.
Blumstein DT, Daniel JC (2007) Quantifying behavior the JWatcher way. Sunderland,
MA: Sinauer Associates.
Bond AB (2007) The evolution of color polymorphism: Crypticity, searching images,
and apostatic selection. Ann Rev Ecol Sys 38:489-514
Briceno R, Ramos D, Eberhard W (1999) Aggressive behavior in medflies (Ceratitis
capitata) and its modification by mass rearing (Diptera: Tephritidae). J Kans
Ent Soc 1:17-27
Caro T (1995) Pursuit-deterrence revisited. TREE 10:500-503
Crawley R (1993) GLIM for ecologists. Oxford: Blackwell Scientific Publications.
Edwards GB (2004) Revision of the jumping spiders of the Genus Phidippus
(Araneae: Salticidae). Occ Pap Fla Sta Coll Arth 11: 1-118
Eisner T (1985) A fly that mimics jumping spiders. Psyche 92: 103-104
Elias DO, Land BR, Mason AC, Hoy RR (2006) Measuring and quantifying dynamic
visual signals in jumping spiders. J Comp Physiol A 192:785-797
Godin J, Davis S (1995) Who dares, benefits: Predator approach behaviour in the
Guppy (Poecilia reticulata) deters predator pursuit. Proc Roy Soc B 259:193200.
Greene E, Orsak L, Whitman D (1987) A Tephritid fly mimics the territorial displays
of its jumping spider predators. Science 236:310-312.
Hasson O (1995) A Fly in Spider's Clothing: What size the spider? Proc Roy Soc B
261:223-226.
Headrick DH, Goeden RD (1994) Reproductive behavior of California fruit flies and
the classification and evolution of Tephritidae (Diptera) mating systems. Stud
Dipterol 1:194-252.
Hemmi JH, Pfeil A (2010) A multi-stage anti-predator response increases
information on predation risk. J Exp Biol 213: 1484-1489
16
427
428
429
430
431
432
433
434
435
436
437
438
439
440
441
442
443
444
445
446
447
448
449
450
451
452
Jackson RR (1977) Prey of the jumping spider Phidippus johnsoni (Araneae:
Salticidae). J Arachnol 5:145-149.
Jackson RR, Pollard SD (1996) Predatory behavior of jumping spiders. Ann Rev
Entomol 41:287-308.
Mather MH, Roitberg BD (1987) A sheep in wolf's clothing: Tephritid flies mimic
spider predators. Science 236:308-310.
Rao D, Díaz-Fleischer F (2012) Characterisation of predator-directed displays in
Tephritid flies. Ethology 118:1165-1172.
Rundus A, Owings D, Joshi S, Chinn E, Giannini N (2007) Ground squirrels use an
infrared signal to deter rattlesnake predation. PNAS 104:14372-14376.
Ruxton G, Sherratt TN, Speed MP (2004) Avoiding attack: The evolutionary ecology
of crypsis, warning signs and mimicry. New York: Oxford University Press.
Sivinski J, Pereira R (2005) Do wing markings in fruit flies (Diptera: Tephritidae)
have sexual significance? Fla Entomol 88:321-324.
Spano L, Long SM, Jakob EM (2012) Secondary eyes mediate the response to
looming objects in jumping spiders (Phidippus audax, Salticidae). Biol Lett
8:949-951.
Tan K, Wang Z, Li H, Yang S, Hu Z, et al. (2012) An ‘I see you’ prey–predator signal
between the Asian honeybee, Apis cerana, and the hornet, Vespa velutina.
Anim Behav 83:879-882.
Tejeda MT, Arredondo J, Pérez-Staples DF, Ramos-Morales P, Liedo P, Díaz-Fleischer
F. (2014) Effects of size, sex and teneral resources on the resistance to hydric
stress in the tephritid fruit fly Anastrepha ludens. J Ins Physiol 70: 73-80
Worthington AM, Swallow JG (2010) Gender differences in survival and
antipredatory behavior in stalk-eyed flies. Behav Ecol 21:759-766.
Zahavi A, Zahavi A (1997) The handicap principle. Oxford: Oxford University Press.
453
17