Altered Heat-Avoidance Behavior Following Damage to the Extended Architecture of Mexican Jumping Bean Moth Larvae (Cydia saltitans)

Abstract

In response to physical damage, organisms must balance recovery with adaptive responses to other environmental stressors. Understanding how damage and repair influence adaptive responses to high environmental temperatures is of particular interest in light of global climate change. We investigate the impact of damage and subsequent repair on heat-avoidance behaviors in Cydia saltitans larvae using host seeds (Sebastiania pavoniana) as protective structures (together colloquially known as “Mexican jumping beans”). These larvae perform temperature-dependent “jumping” or “rolling” behaviors to escape extreme heat, which are crucial for larval survival in their native arid and hot subtropical dry forests. Due to possible costs of repair and limited energetic resources, we hypothesized that experiencing damage and investing in subsequent repair to a host seed would reduce larval displacement distance from extreme heat when compared to individuals that experienced damage without repairing the host seed, or the undamaged control group. Results suggest that larvae in control conditions exhibited greater displacement from heat compared to those in either damage treatment group. Contrary to predictions, damage and subsequent repair impaired heat avoidance behavior to same extent as damage without investing in repair. This reduced displacement distance in both damage treatment groups may be linked to energy allocation or an adaptive antipredator response. These findings contribute to our understanding of how environmental stressors interact to shape behavioral responses in insects with “extended architecture.” As global temperatures rise, insights into the flexibility of adaptive behaviors are increasingly crucial.

Full text

Vol.: (0123456789)
J Insect Behav
https://doi.org/10.1007/s10905-024-09861-y
RESEARCH
Altered Heat‑Avoidance Behavior Following Damage
totheExtended Architecture ofMexican Jumping Bean
Moth Larvae (Cydia saltitans)
AnnaPurtell· JesseAnderson· RebeccaFerguson· KonradJuskiewicz·
MichaelH.Lee· MeganJ.Lee· LindseySwierk
Received: 18 November 2023 / Revised: 2 August 2024 / Accepted: 19 August 2024
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2024
Abstract In response to physical damage, organ-
isms must balance recovery with adaptive responses
to other environmental stressors. Understanding how
damage and repair influence adaptive responses to
high environmental temperatures is of particular
interest in light of global climate change. We investi-
gate the impact of damage and subsequent repair on
heat-avoidance behaviors in Cydia saltitans larvae
usinghost seeds (Sebastiania pavoniana) as protective
structures (together colloquially known as “Mexican
jumping beans”). These larvae perform temperature-
dependent “jumping” or “rolling” behaviors to escape
extreme heat, which are crucial for larval survival
in their native arid and hot subtropical dry forests.
Due to possible costs of repair and limited energetic
resources, we hypothesized that experiencing damage
and investing insubsequentrepairto a host seed would
reduce larval displacement distance from extreme heat
when compared to individuals that experienceddam-
age without repairing the host seed,or the undamaged
control group. Results suggest that larvae in control
conditions exhibited greater displacement from heat
compared to those in eitherdamage treatmentgroup.
Contrary to predictions, damage and subsequentrepair
impaired heat avoidance behavior to same extent as
damagewithout investing inrepair.This reduced dis-
placement distance in both damagetreatment groups
may be linked to energy allocation or an adaptive
antipredator response. These findings contribute to
our understanding of how environmental stressors
interact to shape behavioral responses in insects with
“extended architecture.” As global temperatures rise,
insights into the flexibility of adaptive behaviors are
increasingly crucial.
Keywords Arthropod· behavioral plasticity·
ecophysiology· energetic trade-off· laspeyresia
solitans· stress response· thermoregulation
Introduction
When animals experience physical damage, such as
injuries from a nonlethal predator encounter, recov-
ery must be balanced with responses to other immi-
nent stressors (reviewed by Archie 2013; Rennolds
and Bely 2023). High environmental temperatures
represent one such stressor that can negatively affect
recovery from physical damage (Denley and Metaxas
Supplementary Information The online version
contains supplementary material available at https:// doi.
org/ 10. 1007/ s10905- 024- 09861-y.
A.Purtell· J.Anderson· R.Ferguson· K.Juskiewicz·
M.H.Lee· M.J.Lee· L.Swierk(*)
Department ofBiological Sciences, Binghamton
University, State University ofNew York, Binghamton,
NY13902, USA
e-mail: lindseyns@gmail.com
L.Swierk
Amazon Conservatory forTropical Studies, Iquitos,
Loreto16001, Perú

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2015; Hoffman etal. 2018) and impact various physi-
ological processes across taxa (Gangloff etal. 2016;
Little et al. 2020). Behavioral responses for dealing
with extreme heat in the environment are diverse
and include heat-avoidance behavioral postures (e.g.,
Ward and Seely 1996; Stanton-Jones et al. 2018),
shifts in activity times (e.g., Gilbert and Miles 2019;
Bai etal. 2023), and altered microhabitat choice (e.g.,
Edgerly etal. 2005; Harris etal. 2015). In a changing
climate, identifying how adaptive responses to envi-
ronmental heat are balanced with physiological pro-
cesses like physical repair to damage permits a better
understanding of a species’ resilience (Buchholz etal.
2019).
Species that utilize other organisms or structures
as extensions of their bodies (i.e., “extended
architecture”; Dawkins 1982; Krieger et al. 2020)
often rely heavily on these structures for protection
(e.g., Meyer 1987; Shorthouse and Rohfritsch
1992). When such extended architecture experiences
physical damage, an animal may change its behavior
to mitigate risk through repair or replacement. For
instance, hermit crabs with damaged shells increase
their shell searching time (Gorman etal. 2018), and
galling aphids secrete a sticky fluid to plug holes in
damaged galls (Kurosu etal. 2003; Kutsukake et al.
2009).
Insects respond to high environmental tem-
peratures though diverse mechanisms (reviewed
by González-Tokman et al. 2020). The extended
architecture-bearing larvae of some insect species
can respond to potentially dangerous levels of envi-
ronmental heat by physically moving their protective
structures. This temperature-dependent “jumping”
behavior has been observed in the larvae of gall-
forming wasps (Neuroterus saltatorius; Manier and
Deamer 2014), the leaf-encased caterpillar of the
Southeast Asian moth (Calindoea trifascialis; Hum-
phreys and Darling 2013) and, memorably, in the
Mexican jumping bean moth larvae, Cydia saltitans
(= Laspeyresia solitans) (Heckrotte 1983). Cydia
saltitans is native to the subtropical dry forests in
the mountains of Sinaloa and Sonora, northwestern
Mexico. Adult C. saltitans deposit eggs in the spring
in the inflorescences of a shrub (Sebastiania pavoni-
ana), the seeds of which are invaded by C. saltitans
larvae after hatching. Seeds (ca. 10 to 15mm along
the longest axis) eventually drop to the ground follow-
ing summer rains. C. saltitans larvae remain inside
S. pavoniana seeds for 6 to 8months, feeding on the
inside of the seed until their eventual pupation and
emergence (Hutchins 1956; Heckrotte 1983). These
seed-encased larvae are susceptible to overheating
and desiccation in the high daytime temperatures, and
so C. saltitans larvae use various movements (Herter
1955; West etal. 2012) to “roll” or “jump” its encas-
ing seed away from areas of direct heat or light by
hitting its body against the wall of the seed, generat-
ing movement away from the aversive stimulus (West
et al. 2012). Maximum jumping activity in C. salti-
tans larvae increases with temperature up to 45 °C,
with minimum and maximum active temperatures of
10°C and 45°C, respectively (Heckrotte 1983).
As C. saltitans larvae are soft-bodied and other-
wise vulnerable to predation and desiccation, main-
tenance of the extended architecture of the encas-
ing seed pods is vital to their protection. Published
accounts of predation upon C. saltitans are lacking,
but there is anecdotal evidence from Sinaloa, Mex-
ico, of small mammals gnawing host seeds to con-
sume the C. saltitans larvae inside (pers. comm.,
Amazing Beans© anonymous supplier); some
intact seeds also bear exterior scars suggestive of
rodent teeth. C. saltitans larvae can repair cracks or
holes (Fig. 1A) in their damaged seed by produc-
ing a dense patch of silk (Fig. 1B; Gregory 1971),
which is constructed within hours (see Supplemen-
tary Video 1 for a partial demonstration of this pro-
cess). Although the variables that impact seed pod
choice are not documented in C. saltitans, many gall-
encased insects will primarily select their extended
architecture based on phenology and not necessar-
ily structural integrity (Burstein and Wool 1993);
therefore, repair mechanisms for damaged extended
architecture are likely essential to functionality. In
addition, the seed-encased larvae of C. saltitans
rely on a single, finite food item (the contents of the
seed itself) for up to 8months, consuming the entire
contents and producing virtually no frass (Gregory
1971). As C. saltitans larvae have a strict resource
limit, tradeoffs in their prioritization of energetically
costly activities should be apparent.
This study’s aim is to assess the effects of physi-
cal damage and repair on heat-avoidance behaviors in
C. saltitans larvae. In particular, we investigate how
sequential versus simultaneous timing of two stress-
ors (host seed damage and environmental heat) may
differentially affect larval displacement distances

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away from high temperatures. We predict that C. salti-
tans in host seeds that were damaged one day prior to
heat exposure will be less successful at typical heat-
avoidance behaviors, potentially due to the energetic
costs of seed repair, than will larvae that experienced
those stressors simultaneously (no repair) or larvae in
the control (undamaged) group. We additionally pre-
dict that, due to the survival implications of displace-
ment from extreme heat, C. saltitans will prioritize
heat avoidance over seed repair in the group experi-
encing simultaneous heat and damage; if so, larvae
in the simultaneous stressor group should experience
similar heat avoidance behavior to those in the control
group, despite physical damage.
Methods
Study Organisms
In October 2022, we obtained 200 larval Cydia
saltitans encased in host seeds (hereafter referred
to as “seed complexes”) procured by a commercial
supplier (Amazing Beans©, amazingbeans.com; Lit-
tleton, CO, USA) from Sonora and Sinaloa, Mexico.
Larvae were kept in a windowless laboratory room
at Binghamton University (Binghamton, NY, USA)
in loose-weave cotton bags at 21 °C on a 12:12
light:dark cycle and were misted weekly with water
according to supplier recommendations. Larvae were
acclimated to the laboratory for 15days prior to the
start of trials.
Experimental Setup
Trials were conducted in glass terraria
(51 × 25 × 30.5cm; L x W x H) in the same laboratory
room they were acclimated to prior to trials. The sides
of each terrarium were covered in green opaque paper
to reduce any effect of indirect room lighting on the
larvae. To provide a scale when measuring distance,
0.64 cm square grid paper was taped to the bottom
of the tank. Underneath the tank, temperature zones
were created with a 16W reptile heating pad (Reptile
Heat Mat & Heat Mat Thermostat, Bn-Link, China)
and two ice packs (Hot/Cold Pack, Medvice, China).
Fig. 1 Cydia saltitans larva
(A) at the time of removal
of one full side (the septi-
cidal face) of its host seed
(Sebastiania pavoniana)
and (B) after partial repair.
(C) Experimental treat-
ments included creation of
a much smaller hole in the
flat, septicidal face of the
seed, (D) all of which in the
‘PreviousDamage + Repair
(PDR)’ treatment were
repaired with silk by 20h
following puncture. Photos
by: M.J. Lee

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The heating pad was placed underneath the center of
the tank and the ice packs were placed underneath
both ends of the tank to create a two-way temperature
gradient, with each temperature zone approximately
10cm wide (Fig.2). An infrared thermometer (Laser-
grip 749, Etekcity, China) was used to confirm the
surface temperature of each zone prior to each trial.
The center zone was set at the highest active tem-
perature for C. saltitans (45°C; actual temperature:
44.3°C ± 0.82 SE), both ends of the tank were set at
C. saltitans’s least active temperature (10 °C; actual
temperature 12.7°C ± 2.0 SE), and the center regions
were at 24.1°C (± 0.4 SE), closely approximating C.
saltitans’s preferred temperature (25 °C; Heckrotte
1983).
Procedure
We randomly assigned 180 seed complexes to three
groups: Previous Damage + Repair (PDR), Current
Damage (CD), and Control. For each seed complex
in the PDR group, we made a single puncture hole
(ca. 2mm in diameter) in the encasing seed using a
standard toothpick (Perfection Round Double-Pointed
Toothpicks, Diamond Brands, U.S.A) at 20h prior to
the temperature trial (Fig.1C). The size of the punc-
ture was conservatively designed to reflect only minor
seed damage that may be experienced in nature, e.g.,
a single puncture hole made by a gnawing rodent. The
puncture hole was made on the flat side of the seed
(i.e., the septicidal face) and was shallowly angled to
avoid the larva itself. Each seed complex in the CD
group was punctured immediately prior to the trial
(15 min before start) using the same equipment and
in the same location. Seed complexes in the Con-
trol group were not punctured. All seed complexes,
including the Control group, were handled at 20h and
at 15min prior to the start of trial to keep handling
effects consistent. After 20 h, all PDR larvae had
visibly covered the hole in their host seed with silk
(Fig.1D).
To begin a trial, five seed complexes from each
treatment group were placed with the rounded face
down along the center line of the high-temperature
section of the terrarium, for a total of 15 seed com-
plexes per trial. We arranged the seed complexes
along the center line in alternating order of treatment
(control, PDR, CD, control, etc.). An iPhone cam-
era (iPhone 12, Apple Inc., Zhenzhou, China) was
placedin a single location on a glass pane across the
center top of the tank facing directly down to photo-
graph starting and ending locations. The trial arena
was left undisturbed for 20min. We used two iden-
tical trial arenas simultaneously during each 20-min
trial period, and trial periods were conducted twice
weekly, resulting in a total of twelve trials over three
Fig. 2 Top-down view of
the experimental arena,
with five thermal gradi-
ent zones each ca. 10cm
in width. The center (red)
represents the high heat
(45°C) zone, set directly
above a heating pad con-
trolled by a thermostat; the
adjacent zones (in white)
wereat room temperature
(25°C); and the zones at
each end (blue) were cooled
to 10°C. Cydia saltitans
seed complexes began trials
in a single line, alternat-
ing treatment groups, in
the center high heat zone.
Distance outward from the
starting line (indicated by
arrows) was measured

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weeks and a total of 60 unique seed complexes per
group (total n = 180 unique seed complexes).
At the conclusion of each trial, the seed complexes
were removed from the trial arena, and we measured
each seed complex’s displacement from the start: the
straight-line distance to the closest point on the center
line, using still images from the camera and the grid
paper lines for scale. We then carefully extracted each
larva from its host seed with a razor blade and twee-
zers and recorded the mass of the larva to the nearest
0.001 g using a microgram scale (Premium Digital
Milligram Scale, Weightman, China). At this time,
alllarvae were confirmed to be alive and undamaged
by the puncture hole (if present) in the seed.
Statistical Analysis
We ran a linear mixed effects model using the lme4
package (Bates et al. 2015) in R (version 4.2.3; R
Core Team 2023) to determine the influence of treat-
ment (PDR, CD, or Control) on displacement dis-
tance, with distance moved as the response, and treat-
ment, trial week, and larval mass as predictors, and
testing group (1–12) as the random effect. Prior to
analysis, distance moved was log(x + 1) transformed
to better meet the assumptions of normality.
We obtained P-values for each predictor using like-
lihood ratio tests of the full model against a reduced
model (Zuur etal. 2010), and we examined pairwise
comparisons using the emmeans package (Lenth
2020). Model fit was assessed by examining the
behavior of residuals and by diagnostic plots of simu-
lated residuals using the DHARMa package (Hartig
2022). Statistical tests were two-tailed, set at an alpha
level at 0.05, and were performed in R.
Results
Treatment significantly impacted seed complex dis-
placement distance (χ2
2 = 54.62, P < 0.001), such
that distance away from the heat stimulus was sig-
nificantly greater in the Control group than in either
the Previous Damage + Repair (PDR; P < 0.001)
or Current Damage (CD; P < 0.001) treatments,
and nearly greater in PDR than in CD (P = 0.066)
(Fig. 3). Trial week also affected displacement dis-
tance (χ2
2 = 12.03, P = 0.002), with distance decreas-
ing with trial week (Week 1 vs. 2, P = 0.704; 1 vs. 3,
P = 0.005; 2 vs. 3, P = 0.026). Larval mass did not
affect displacement distance (χ2
1 = 2.49, P = 0.114).
Discussion
Our findings support the hypothesis that damage to
extended architecture impacts responses to environ-
mental heat in Cydia saltitans larvae. We found that
larvae in the Control group had greater displacement
from the heat source compared to those in the Previ-
ous Damage + Repair (PDR) group and (contrary to
our predictions) the Current Damage (CD) group.
This finding suggests that host seed damage itself,
and not necessarily only the repair, is in some way
costly to C. saltitans larvae. Interestingly, although
larvae in the PDR and CD groups did not significantly
differ in displacement from the heat source, larvae in
Fig. 3 Box plot representation of total displacement dis-
tance away from a high heat zone (45°C) during 20-min tri-
als by Cydia saltitans seed complexes in each treatment group
(Control; CD = Current Damage; PDR = Previous Dam-
age + Repair). Seed complexes in the Control group had sig-
nificantly greater displacement than those in the CD or PDR
groups

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the PDR group did trend towards greater displace-
ment (P = 0.066) than those in the CD group. The
slightly shorter (though non-significant) displace-
ment of the CD group could possibly be explained if
these simultaneously damaged larvae prioritized seed
repair over avoidance of high heat, the opposite of our
expectations.
Given its ecology, heat avoidance behavior regard-
less of seed damage should be adaptive in C. saltitans
larvae, and all treatment groups should equally prefer
to avoid the highest temperatures in the center por-
tion of the arena. When exposed to sunlight or heat,
C. saltitans in natural environments move their host
seeds until they find shade or cracks in the ground;
similar heat avoidance behavior is demonstrated in
the laboratory (Heckrotte 1983). Damage to the C.
saltitans’s host seed alters this typical behavioral
response to heat, and the opportunity to repair the
damage prior to heat exposure did not restore typical
behavior. Following trials, all larvae were removed
from host seeds and were confirmed to be uninjured
by the toothpick insertion (which was shallow and
angled away from the larva), confirming that injury
to the larva itself was not responsible for its reduc-
tion in displacement distance. In addition, all tooth-
pick insertions faced inward and did not cause uneven
or disruptive surfaces on the seed surface that would
impede normal movements. In light of this, we con-
sider alternative explanations for our observations.
Movement in C. saltitans is achieved when a larva,
which is connected to the inside of its host seed by
interior silk threads, walks along the inner walls of
the seed (to produce “rolling” movements) or strikes
the inside wall with its appendages (“jumping”)
(Herter 1955). A possible cause for the shorter dis-
placement distances in damaged groups (PDR and
CD) is the partial disconnection of the larva from the
interior silk that attaches it to its host seed or a change
in normal larval movements or its center of mass due
to the seed damage. The physics of individual jump-
ing movements may also be altered by silk repair.
All PDR larvae were observed to repair their seeds
prior to trials, and yet they still did not demonstrate
significantly greater displacement distances than the
CD larvae, which were not offered repair time. It is
possible that the PDR larvae were able to complete
exterior, but not interior, silk repair before the tri-
als. However, given that all larvae from all treat-
ments were still observed to be capable of performing
typical movement behaviors (rolling and jumping),
these movements were clearly still possible despite
the seed damage, suggesting that the interior silk did
not sustain incapacitating damage. Essentially, larvae
from the three treatments differed in their displace-
ment distances, butnot in their fundamental abilities
to perform these behaviors.
Intact C. saltitans seed complexes are able to travel
10 to 25 cm in only two minutes to reach preferred
temperatures (Gregory 1971). Given that our trials
were ten times this duration(20min), C. saltitans lar-
vae had ample time to move to their preferred temper-
atures if the damage itself did not hinder movement.
An energetic perspective may therefore help explain
reduced displacement distances by larvae in the dam-
aged seed complexes. Energy budgeting strategies in
C. saltitans are unknown but, in other larval insects,
silk production can be energetically expensive (e.g.,
Berenbaum etal. 1993), and so C. saltitans in dam-
aged host seeds may divert resources from muscle
movements to silk production, either before (PDR) or
during (CD) the trials. That said, in other insects, the
cost of silk production is minimal (e.g., only 1.5% of
the energy budget in larval Malacosoma americanum;
Ruggiero and Merchant 1986). Given this variability
in silk costs, an examination of the energy budget of
C. saltitans, particularly given a larva’s restriction to
a single food item, is a topic of future study.
It is alternatively possible that lack of move-
ment by larvae in damaged seed complexes may
serve an antipredator function. If predators (mam-
malian or otherwise) of C. saltitans larvae selec-
tively target the more conspicuous moving beans,
then lack of movement and decreased conspicu-
ity following damage to the protective host seed
would likely be adaptive. In support of this, we
note that shaking C. saltitans seed complexes tem-
porarily stops their movements (Heckrotte 1983),
which could be explained if a shaking motion cor-
responds to predator disturbance in natureand sub-
sequent lack of larvalmovement reduces detection
by predators. Future work comparing the relative
conspicuity of moving and non-moving seed com-
plexes would help to identify if lack of movement
in damaged seeds could be an antipredator adapta-
tion. We also note that the highest temperature used
in our study (45°C) is notlethal to C. saltitans lar-
vae within at least 60min (Heckrotte 1983), which
may explain the lack of urgent displacement from

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the high-temperature zone in some seed complexes
during the 20-min trials (Fig. 4); we predict that
increased time spent at 45°C would result in more
seedcomplexes demonstrating greater displacement.
These data add to our greater understanding of how
multiple environmental stressors influence behavioral
responses in a model insect using “extended archi-
tecture”. We demonstrated that physical damage to
protective extended architecture alters larval response
to environmental heat. These behavioral responses
following host seed damage may represent either a
constraint or an adaptation in C. saltitans. As climate
change continues to intensify ambient temperatures,
our understanding of how animals can respond and
adapt to multiple stressors, particularly though flex-
ible behavioral responses, is increasingly crucial.
Acknowledgements The research adheres to the ASAB/
ABS Guidelines for the Use of Animals in Research, the legal
requirements of the U.S.A., and all institutional guidelines of
Binghamton University, State University of New York. We
thank A. Martin for advice in designing a heating gradient and
J. Talavera for laboratory support.
Author Contributions Anna Purtell and Lindsey Swierk
wrote the main manuscript text and prepared figures. Anna
Purtell, Jesse Anderson, Rebecca Ferguson, Konrad Juskie-
wicz, Michael H. Lee, Megan J. Lee, and Lindsey Swierk con-
tributed to experimental design and execution and reviewed the
manuscript.
Funding This research was supported by the Department of
Biological Sciences, Binghamton University.
Data Availability Data to accompany this paper are depos-
ited in the Open Repository at Binghamton (ORB) and are
freely accessible (https:// orb. bingh amton. edu/ bio_ fac/ 26).
Declarations
Conflict of Interest The authors declare no competing inter-
ests.
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group (Control; CD = Cur-
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