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First published online July 20, 2006
Journal of Experimental Biology 209, 3018-3024 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02335
Diversification of gut morphology in caterpillars is associated with defensive behavior
Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
e-mail: jbgrant{at}nrel.colostate.edu
Accepted 16 May 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: Lepidoptera, digestive tract, anatomy, anti-predator, larva
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Foraging strategy itself is the primary driver of
evolutionary diversification seen in vertebrate
(Van Soest, 1996) and
invertebrate (Dow, 1986)
digestive tracts. Insect gut morphology is exceptionally diverse because of
the multitude of food sources they have exploited over evolutionary time
(Dow, 1986). For example, the
simple, tubular guts of caterpillars typify specialization for rapid passage
and processing of solid plant foods (Dow,
1986). This dietary specialization is thus thought to have
resulted in a lack of gut structure diversity among caterpillars
(Dow, 1986). However, evidence
supporting this hypothesis is lacking.
Modification of insect gut morphology and function is driven by two
important dietary dichotomies: (1) solid/liquid and (2) animal/plant feeding
strategies (Dow, 1986). These
two dichotomies result in four classes of insect feeding habits that may be
used to categorize insect gut structure
(Dow, 1986). In insects, the
gut is essentially a cylinder that connects mouth and anus. It consists of
three physiologically distinct sections (foregut, midgut and hindgut) that
become morphologically modified in response to environmental factors
(Dow, 1986). The foregut is
further modified into three sections: the esophagus, crop and proventriculus,
and the crop's major function is generally considered to be food storage
(Dow, 1986).
Larvae of butterflies and moths are the classic example of solid-plant
feeders (Dow, 1986). Their
guts evolved to rapidly process large quantities of abrasive plant material,
which is thought to have resulted in simple, tubular guts with vestigial
foreguts and expansive midguts (Dow,
1986). Given the apparent dietary homogeneity of this taxon
(Dow, 1986), it is surprising
that little consideration has been afforded to the potential effects of other
behaviors on gut morphology. For example, defensive regurgitation is a common
defensive ploy that effectively deters invertebrate attacks
(Freitas and Oliveira, 1992;
Gentry and Dyer, 2002;
Smedley et al., 1990), and is
a tactic widely used by insects, especially the vulnerable larvae of moths and
butterflies (Fig. 1)
(Bowers, 1993). However, the
extent to which this behavior is used as a primary defensive response among
lepidopteran larvae is unknown (Peterson
et al., 1987), and the degree to which it is associated with
variation in gut morphology has not been explored.
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).
If defense is associated with morphology then caterpillars that primarily rely
on regurgitation for protection would be expected to have a gut morphology
that both reflects these abilities, and differs from that of larvae that rely
on other types of defenses such as spines, glands or hair. I have tested for a
relationship between the behavioral strategy of defensive regurgitation and
specific gut morphology. This defense hypothesis expressly predicts that
primary-regurgitators will possess large crops in which to stockpile defensive
regurgitant, whereas secondary- and non-regurgitators will have smaller crops
as they turn to other weaponry and their reliance on regurgitation
decreases. |
Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Wagner et al., 2001b) and
professional taxonomic advice at Cornell University
(Table A1). Four species
(Utetheisa ornatrix, Limenitis arthemis astyanax, Papilio machaon aliaska,
Callosamia promethea) were donated from laboratory-raised populations of
known species. Utetheisa ornatrix was fed an artificial diet
consisting of pinto beans mixed with its natural diet, the seeds of
Crotalaria spactabilis (Iyengar
et al., 2002). Regurgitation behavior was not expected to be
affected by this laboratory diet as it was similar to the natural diet of
U. ornatrix. Limenitis arthemis astyanax, Papilio machaon aliaska and
Callosamia promethea were fed branches or sprigs of their natural
host plants.
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Behavior
Regurgitation behavior was determined for three replicate mature larvae
(instars IV, V or VI) of 33 species with a pinch assay that simulated
predation. Only mature larvae were used because ontogenetic changes in
defensive behavior often occur at the cutoff between third and fourth instars
(Cornell et al., 1987).
Specifically, a pinch delivered with No. 5 forceps simulated the mandibular
bite of an ant (Ayre and Hitchon,
1968; Eisner et al.,
1972). Caterpillars were fasted for 6 h prior to the pinch assay
to control for meal size on regurgitation response. As the average meal moves
through a caterpillar's gut in 2.5 h
(Santos et al., 1983), a 6 h
fast was sufficient to ensure that gut content was equalized among test
subjects. The threshold between primary- and secondary-regurgitators was
selected as 2.5 pinches because it was approximately one standard deviation
(s.d.) less than the mean number of pinches required to elicit regurgitation
(mean ± s.d.: 5.5±3.3) and below the lower 99% confidence
interval (CI) of the mean (lower CI=3.9 pinches). This threshold was
associated with discrete defensive behaviors that allowed further distinction
between the two categories, the most prominent being that
primary-regurgitators re-imbibed expelled fluid and directed regurgitant with
accuracy whereas secondary-regurgitators did not. Eight pinches were chosen as
the cut-off for non-regurgitators because it was approximately one standard
deviation above the mean and also above the upper 99% confidence interval of
the mean (upper CI=7.0 pinches). If a caterpillar did not respond by ten
pinches it was classified as a non-regurgitator and no more pinches were
delivered. Generally, if a caterpillar did not respond by seven or eight
pinches, more pinches did not elicit regurgitation. This threshold was also
associated with marked defensive behaviors that allowed further distinction
between the two categories, the most prominent being that non-regurgitators
could seldom be induced to regurgitate whereas secondary-regurgitators would
defensively ooze regurgitant from their oral cavities. These thresholds were
further validated with a hierarchical clustering analysis of the number of
pinches necessary to elicit regurgitation. Quantitative measurement of
regurgitant volume was precluded by other defensive behaviors of caterpillars,
such as thrashing and wriggling to escape.
A lack of well-resolved phylogenies at many lower taxonomic levels among
the Lepidoptera prevents phylogenetically controlled comparative analyses
(Costa and Pierce, 1998).
However, after applying the Runs Test as implemented in Phylogenetic
Independence 2.0 software (Reeve and
Abouheif, 2003), regurgitation behavior was not found to be
phylogenetically autocorrelated (1000 iterations, Cstat=17.48,
P=0.004). Thus, from an evolutionary point of view, these 33 species
represented 33 independent evolutionary events and could be analyzed by
standard multi- and univariate analysis of variance (MANOVA and ANOVA).
Morphology
Gut morphology was measured in three replicate mature larvae (instars IV, V
or VI) of 33 species. Caterpillars were fasted for 6 h prior to dissection and
measurement in order to control for the effect of meal size on crop expansion
and overall gut length. As the average meal moves through a caterpillar's gut
in 2.5 h (Santos et al.,
1983), a 6 h fast was sufficient to ensure gut vacancy.
Caterpillars were killed by freezing at -4°C for 30 min then pinned into a
glass-bottomed magnetic dissecting tray filled with Ringer's solution. The
cuticle was cut from anal plate to head capsule along the dorsal axis and
pinned to the sides to allow for measurement of the gut and its components.
Caterpillars were stretched to their fullest extent to control for differences
in gut elasticity. Because caterpillar guts are tubular and not coiled,
stretching them in this fashion allowed for measurement of maximum gut length.
Total gut length and gut component lengths were measured with calipers to the
nearest 0.1 mm under a 40x dissecting microscope. Caterpillars found to
contain parasitic wasp or fly larvae were excluded from analysis because of
potential behavioral modification resulting from infestation.
To test the association between gut structure and defensive behavior the relationship between relative gut compartment length (crop, midgut and hindgut) and defensive behavior was evaluated using the 33 species behaviorally classified as primary-, secondary- and non-regurgitators by the previously described pinch assay. To control for the effects of body size on gut component length, the proportion of each gut section length relative to total gut length was used in all dissected caterpillars for all statistical analyses.
Statistical analyses
Midgut data were not transformed because they met the assumptions of
normality (Shapiro-Wilk W-test: midguts, W=0.984,
P=0.90) and equality of variances (Levene's test:
F2,30=2.394, P=0.11). The raw data for crop and
hindgut proportions did not meet the assumptions of normality (Shapiro-Wilk
W-test: crops, W=0.929, P=0.03; hindguts,
W=0.927, P=0.03) and were square root transformed to achieve
a more normal distribution (Shapiro-Wilk W-test: square root (crops),
W=0.950, P=0.14; square root (hindguts), W=0.946,
P=0.10). After transformation, these data also met the assumption of
equality of variances (Levene's test: crops, F2,30=0.0728,
P=0.93; hindguts, F2,30=2.040, P=0.15).
Comparisons of gut proportions among primary-, secondary- and
non-regurgitators were made using MANOVA followed by univariate ANOVA. Because
species to species variation was being tested, the experimental unit was
reduced (i.e. a single response per species was analyzed instead of
statistical replicated measures for each species) by calculating the mean
response for each species (Sall et al.,
2005). Statistical analyses were then performed on these mean
responses. All statistical analyses were performed with JMP® 5.1
software.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Regurgitation defensive strategy clearly differed among the three types of caterpillars. Those in which the initial defense response was regurgitation (primary-regurgitators) behaved very differently than secondary-regurgitators, as measured by both the number of pinches required to elicit the response and the dynamics of the response itself. The initial defensive response of primary-regurgitators was regurgitation directed at the offending forceps, followed by recovery of regurgitant. Regurgitant recovery is expected from caterpillars that regurgitate frequently because of the costs associated with losing gut content nutrients expelled with regurgitant. Primary-regurgitators controlled how regurgitant was discharged and were often noted to produce regurgitant droplets of varying size in response to weaker or stronger pinches. Neither of these behaviors was noted in secondary-regurgitators, in which regurgitation was used secondarily after primary defenses such as flailing, biting or escape attempts failed to deter the simulated predator. Secondary-regurgitators did not produce a distinct droplet, but oozed regurgitant in a non-directed fashion that often resulted in as much regurgitant on the cuticle and substrate as on the forceps. Consistent with a lack of reliance on regurgitation as the primary defensive response, these caterpillars also failed to re-imbibe regurgitant after attack.
The occasional production of regurgitant by non-regurgitators seemed to be more a stress response than an antipredator response. Although not quantified, regurgitant volume appeared to be much less in these animals than in primary- or secondary-regurgitators, and non-regurgitator responses that resulted in regurgitation were often due more to exhaustion than defense. Therefore, it was clear that regurgitation was a primary or secondary defensive tactic in primary- and secondary-regurgitators, but not used as a defense in non-regurgitators. Primary-regurgitators responded by the second or third pinch, secondary-regurgitators responded after four to six pinches, and non-regurgitators required at least eight pinches to elicit regurgitation or did not regurgitate at all (Fig. 2).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Blum, 1992;
Eisner, 1970;
Eisner and Meinwald, 1966).
However, different assemblages of defenses are important for caterpillar
survival (Dyer, 1997) and, as
shown here, regurgitation is not a ubiquitous primary defensive response among
caterpillars. Caterpillars utilize a number of defensive strategies to ward
off several types of enemies (Gentry and
Dyer, 2002), so it is not surprising that defensive regurgitation
is used to varying extents by different species. What was unexpected was the
relationship between gut morphology and reliance on regurgitation as a
defense. Larvae of butterflies and moths for which the primary defensive
response is regurgitation have distinct gut morphology relative to larvae for
which regurgitation is a secondary defensive response or minimally used as a
defense. Previous research on the relationship between lepidopteran gut
structure and function logically focused on the gut's role in digestion, but
overlooked defensive functions such as regurgitation
(Dow, 1986). From a digestive
physiology stance caterpillar guts are expected to be quite similar as a
result of their similar foraging strategies
(Dow, 1986). At a coarse,
taxon-wide scale this proves true, and when broadly compared to other insects
it is reasonable to say that caterpillars possess fairly limited foreguts,
large midguts and small hindguts. However, as shown here, defensive
regurgitation clearly is part of caterpillar gut function and strongly
correlated with gut morphology. Future research in the area of caterpillar gut
function would profit by incorporating both foraging and defense
perspectives.
Primary-regurgitators possess larger crops and smaller midguts than
secondary- and non-regurgitators, results that indicate that regurgitation may
be costly in terms of loss of midgut function. Insect digestion and nutrient
absorption take place almost exclusively in the midgut
(Terra et al., 1996);
therefore a decrease in midgut capacity may result in reduced digestive
function relative to similarly-sized species which have larger midguts.
Further research is necessary to determine if digestive efficiency is
diminished in primary-regurgitators compared to secondary- and
non-regurgitators. Previous research demonstrated another cost of
regurgitation in terms of lost nutrition that resulted in decreased growth
rates (Bowers, 2003).
Primary-regurgitators appear to attempt to compensate for this loss by
re-imbibing regurgitant when possible (this study). Secondary- and
non-regurgitators do not exhibit this behavior, which may indicate that they
are not adapted to regurgitation as a defense as well as are
primary-regurgitators. Nutritional losses may also be minimized in
primary-regurgitators because of their ability to control droplet volume and
direct regurgitant with high accuracy (this study). These abilities were not
observed in secondary- or non-regurgitators, which may make them more
vulnerable to nutritional losses when they are forced to regurgitate. However,
regurgitation remains an important defense in many caterpillars and protects
them against parasitic wasps (Gentry and
Dyer, 2002), ants (Cornelius
and Bernays, 1995; Eisner et
al., 1972; Freitas and
Oliveira, 1992; Peterson et
al., 1987; Smedley et al.,
1993) and spiders (Theodoratus
and Bowers, 1999). Regurgitation is an especially effective
defense when it is combined with sequestered compounds from the larval host
plant (Gentry and Dyer, 2002).
Clearly, there is an important interplay between the costs and benefits of
defensive regurgitation in caterpillars.
Taken together, these results suggest that, for caterpillars, defensive
regurgitation strategy is strongly associated with gut morphology.
Caterpillars that regurgitate as their primary defense have much larger crops
than caterpillars that utilize other defenses. The short foregut of
caterpillars is characteristic of a continuously feeding animal
(Dow, 1986) and inconsistent
with its sole function being one of food storage. Caterpillars appear to have
modified their vestigial crops into defensive weaponry that takes advantage of
the allelochemicals inherent in their plant-based diets. Regurgitation and
even defecation are used defensively by many other insect taxa
(Eisner and Meinwald, 1966),
as well as some birds (Clarke,
1977). Thus, gut modification to enhance defensive regurgitation
ability is potentially a general phenomenon among the Lepidoptera and may
apply more broadly to the Insecta as well as some vertebrate groups.
Furthermore, the feeding of conspecifics and nonconspecifics by regurgitation
(often termed trophallaxis in invertebrates) is a common behavior in many
vertebrate and invertebrate taxa
(Cammaerts, 1996;
Cassill and Tschinkel, 1995;
Janes, 1997;
Mech et al., 1999;
Pal, 2005;
Rauter and Moore, 2002;
Salomon et al., 2005;
Schneider, 2002;
Suarez and Thorne, 2000); a
comparative examination of association of this type of regurgitation and gut
morphology may be profitable. However, trophallaxis has not yet been reported
in caterpillars of any species, perhaps because of a lack of parental care or
kin selection, which appear to be key components in the evolution of
trophallaxis in other invertebrate taxa such as termites, ants and honey bees
(Anduaga and Huerta, 2001;
Brandmayr, 1992;
Sleigh, 2002). Furthermore,
although some species of caterpillars do live in social groups that consist of
genetically related individuals (Costa and
Ross, 1993; Grant,
2005; Porter et al.,
1997), behavioral mechanisms of kin bias such as trophallaxis have
yet to be shown to affect colony structure
(Costa, 1998;
Costa and Ross, 1993;
Costa and Ross, 1994).
Previously, physiologists contended that gut morphology was solely a
function of the influence of diet (Dow,
1986). However, this traditional approach to the organization of
digestive processes in insects has some limitations, despite its general
utility as a classification system (Terra
et al., 1996). A full understanding of gut diversification will be
enhanced by the incorporation of multiple perspectives, including behavioral
ecology and phylogeny, in addition to the traditional approach of research on
diet and digestive processes. The interplay between optimal defensive and
foraging strategies may be an important, but generally overlooked area of
predator-prey interactions.
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Acknowledgments |
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Footnotes |
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