TITLE: Eyespot peek-a-boo: false eyes improve the survival of
caterpillars in leaf rolls
RUNNING TITLE: Eyespots protect caterpillars in rolled leaves
AUTHOR: *Elizabeth G. Postemaa
a. Department of Entomology and Nematology, Animal Behavior Graduate
Group, University of California, Davis.
KEY WORDS: color, eyespots, predator-prey interactions, leaf roll,
deimatic display, environmental deimatism, lepidoptera
WORD COUNT: 150 in abstract, 4378 in main text
# OF FIGURES, TABLES, AND REFERENCES: 3 figures, 64 references.
STATEMENT OF AUTHORSHIP: EGP conceived the study, collected the data,
performed the analyses, and wrote all parts of the manuscript.
DATA AVAILABILITY STATEMENT: Upon article acceptance, I will upload all
raw data files and R scripts used in this study to Dryad.
*Corresponding Author:
Phone: 734-972-9595, Email: egpostema@ucdavis.edu
Full Address: Elizabeth G. Postema, Department of Entomology and
Nematology, Briggs Hall 380K, 1 Shields Avenue, UC Davis, Davis, CA
95616.
ABSTRACT
Deimatic displays typically involve body parts that can conceal or
reveal visual signals, potentially reducing detectability at a distance
while startling predators up close. Some species may achieve this
“conceal-then-reveal” effect using modified aspects of their
environment (environmental deimatism hypothesis). The larvae of
spicebush swallowtail butterflies (Papilio troilus )
possess large eyespots, and rest in leaf rolls during the day. I tested
the hypothesis that leaf rolls reduce eyespot conspicuousness while
maintaining eyespot effectiveness by comparing avian predation on 659
artificial larvae: eyespotted and non-eyespotted, presented in leaf
rolls or on open leaves. Leaf rolls reduced predation regardless of
color pattern. Eyespots also reduced predation, but only for artificial
larvae in leaf rolls. On open leaves, eyespots neither increased nor
decreased predation. These results suggest that eyespots and leaf rolls
can combine to create a deimatic display – and that this strategy
likely evolved to enhance existing antipredator effects of leaf rolls.
INTRODUCTION
Conspicuous color patterns have well-known advantages in social, sexual,
and antipredator contexts (Prudic et al. 2007; Stuart-Fox &
Moussalli 2008; Aronsson & Gamberale-Stille 2009; Caro & Allen 2017).
However, strong signals may also attract the attention of unwanted
receivers, e.g., predators (Endler 1983; Justin Marshall 2000; Halfwerket al. 2014; de Lira et al. 2018). Even in aposematic
species, high detectability can result in high mortality through the
attraction of naïve, specialist, or otherwise undeterred predators
(Ruxton et al. 2009; Mappes et al. 2014; Fabricant &
Herberstein 2015; Umbers et al. 2015). The inbuilt tradeoffs of
detectability are cited as potential drivers for the evolution of
intermediate aposematic signals (Ruxton et al. 2009),
distance-dependent crypsis (Barnett et al. 2017, 2018), and even
seasonal trends in proportions of aposematic versus cryptic species
(Mappes et al. 2014). Beyond color traits alone, deimatic
displays may allow organisms to resolve detectability tradeoffs
behaviorally (Umbers et al. 2015, 2017; Umbers & Mappes 2015;
Badiane et al. 2018).
Deimatic displays are broadly defined by Umbers and Mappes (2016) as
“momentary, transient, conspicuous” signals that induce “a startle
response” or overload “the senses of an attacking predator, such that
the predator pauses, slows or stops the attack.” Deimatism generally
occurs late in the predation sequence – i.e., when the initial
defense(s) have failed – and may or may not involve honest
advertisements of toxicity and (Umbers et al. 2015, 2019). These
displays often blur lines between traditional categories of antipredator
signalling, combining distinct types of visual defenses (aposematism,
crypsis, masquerade, and/or mimicry) and sometimes additional modalities
(e.g., acoustic, chemical) in a single complex display (Dookie et al.
2017, Badiane et al. 2018, Vidal-García et al. 2020, Whiting et al.
2022, Drinkwater et al. 2022). Deimatic displays thus offer sensory
ecologists a way to study (1) how behavior intersects with morphology to
shape the perception of visual signals, (2) what conditions select for
the evolution of multicomponent and/or multimodal signals, and (3) how
evolutionary tradeoffs can produce and maintain signal diversity (Rowe
1999, Cuthill et al. 2017, Stevens and Ruxton 2018, Postema et al.
2022). Despite a surge of theoretical interest in the past 10 years, the
ecology and evolution of deimatic displays remains poorly understood
relative to other forms of visual defenses (e.g., aposematism, crypsis;
Umbers et al. 2015, 2017, Skelhorn et al. 2016b, Umbers and Mappes
2016). In particular, experimental evidence for the fitness consequences
of deimatic displays is lacking – and, even more so, how these displays
function under natural conditions (but see Umbers et al. 2019).
The caterpillars of swallowtail butterflies (family Papilionidae)
exhibit a wide variety of defensive color strategies (Gaitonde et
al. 2018) and complementary defensive behaviors (Hossie & Sherratt
2012, 2013, 2014; Hossie et al. 2013, 2015). Many species possess
eyespots in the final instars, presumably to deter predators by
mimicking the eyes of more threatening animals (Wagner 2005; Hossie &
Sherratt 2013; De Bona et al. 2015; Skelhorn et al.2016a). Spicebush swallowtail (Papilio troilus ) eyespots are
large compared to other North American species in the same genus, such
as P. eurymedes, glaucus, or rutulus (Wagner 2005).Like other eyespotted Papilio larvae, spicebush swallowtails
inflate their thoraxes in response to agitation (Hossie & Sherratt
2013). This reflex increases the size of the eyespots, and may heighten
the larva’s resemblance to a snake (Hossie & Sherratt 2014). However,
even at rest, P. troilus eyespots may still be conspicuous to
predators unless the larvae are otherwise concealed (Fig. 1a). Unlike
most Papilio species, P. troilus larvae construct shelters
from the leaves of their host plant. They rest in these leaf rolls
during the day (Fig. 1d), emerging at night to feed (Wagner 2005).
Larvae in leaf rolls point their heads up towards the leaf petiole,
generally making their eyespots partially visible at the small opening
at the top of the roll (Wagner 2005; see supplemental table 1).
I hypothesize that the combination of eyespots and leaf rolls inP. troilus larvae creates the same antipredator effect as a
deimatic display. I refer to this potential defensive strategy as
“environmental deimatism”: the use of environmental materials to
create a sudden, startling visual signal that stops or slows predation.
Similar to other deimatic displays, P. troilus eyespots are
concealed at rest, but may become suddenly apparent once a predator
opens or looks into the leaf roll (Fig. 1a,d). This effect would fulfill
the definition of a “momentary, transient signal” that startles a
predator enough to slow or halt its attack (Umbers & Mappes 2016).
Additionally, leaf rolls may offset potential detectability costs of
large, conspicuous eyespots (Hossie et al. 2013, Postema 2022). While
the startling “conceal-then-reveal” effect of eyespots within leaf
rolls has been presumed for both P. troilus larvae and other
lepidopteran species (Wagner 2005; Janzen et al. 2010), this
assumption remains untested. In other arthropod systems, leaf rolls have
been shown to play a role in predator defense (Murakami 1999; Tvardikova
& Novotny 2012) among other functions (Kobayashi et al. 2015;
Romero et al. 2022), but their influence on the perception of
prey color patterns is not well-known. I expect that environmental
deimatism may be a relatively widespread (but not well-characterized)
defensive strategy among shelter-building species – e.g., spiders that
spring out suddenly from leaf rolls (Postema personal
observations ), or other leaf-sheltering caterpillars with conspicuous
markings (Janzen et al. 2010).
To test the environmental deimatism hypothesis, I conducted an
artificial prey experiment using a combination of eyespotted and
non-eyespotted clay caterpillars presented on either open or rolled host
plant leaves (Fig. 1b-e). I predicted an overall protective effect of
leaf rolls, as well as interactions between prey presentation (roll vs.
open leaf) and color (eyespots vs. no eyespots). Specifically, I
expected eyespots to decrease predation on leaf-rolled prey. For prey on
open leaves, I predicted that eyespots would either increase or have no
effect on predation – depending on how well eyespots deter predators
without additional defensive components (Hossie and Sherratt 2013,
Postema 2022). Overall, my primary aims for this experiment were (1) to
conduct a test of the environmental deimatism hypothesis in the field,
and (2) to quantify the potential costs of conspicuous color signals
that lack additional behavioral components.
MATERIALS AND METHODS