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2012 SOUTHEASTERN NATURALIST 11(1):111–126
Life History Aspects of Exyra semicrocea (Pitcher Plant
Moth) (Lepidoptera: Noctuidae)
Jessica D. Stephens1,* and Debbie R. Folkerts2
Abstract - With as little as 3% of southeastern Coastal Plain pitcher plant bogs remaining,
it is important to understand the life-history aspects of the endemic organisms that
comprise this community. In this study, we elucidate aspects of the life history of Exyra
semicrocea (Pitcher Plant Moth) by incorporating unpublished portions of a thesis from
1978–1979 with recent field and lab observations in 2010. We give morphological descriptions
of both larvae and adults, as well as behavioral descriptions and mortality
measures. In addition, population estimates of E. semicrocea were conducted from east
Texas through North Carolina. Our surveys identified four isolated pitcher plant sites
where E. semicrocea may have been extirpated. This information has important conservation
implications for E. semicrocea and is applicable to other pitcher plant-endemic
Pitcher plant bogs (wet pine savannahs and other habitats dominated by carnivorous
plants) of the southeastern United States Coastal Plain are composed of
a diverse and complex community found nowhere else in the world. This region
contains 29 or more carnivorous plants, with the most conspicuous genus, Sarracenia
(pitcher plants), containing eight or more of these species. Members of
the genus are known to interact with a variety of organisms including bacteria
(Kneitel and Miller 2002, Koopman and Carstens 2011), protozoa (Hegner 1926),
rotifers (Bateman 1987, Bledzki and Ellison 2003, Kneitel and Miller 2003), and
most notably, arthropods (Dahlem and Naczi 2006; Folkerts 1999; Goodnight
1940; Jones 1904, 1907, 1908). Pitcher plant interactions with arthropods as prey
have garnered the most attention (Heard 1998, Wolfe 1981), but it is important
to note that these plants promote a diverse array of interactions with various arthropod
species. These include herbivory, pollination, parasitism, and predation
of primary associates, as well as capture interruption (Folkerts 1999). Some of
these interactions are so specific that many of these arthropods are found only in
pitcher plant bogs.
Pitcher plant moths (Exyra spp.) are the most noticeable of the 17 or more
species of endemic arthropods within pitcher plants (Folkerts 1999, Rymal and
Folkerts 1982) and are among the more studied pitcher plant symbionts because
of damage caused by larval stages on pitchers (Atwater et al. 2006, Moon et al.
2008). These noctuid moths, first described by Gueneé (1852) and later revised by
Grote (1879), consist of three described species: Exyra fax (Grote), E. ridingsii
1Department of Plant Biology, The University of Georgia, Athens, GA 30602. 2331
Funchess Hall, Department of Biological Sciences, Auburn University, Auburn, AL
36849. *Corresponding author - email@example.com.
112 Southeastern Naturalist Vol. 11, No. 1
(Riley), and E. semicrocea (Gueneé). Exyra fax is obligate in Sarracenia purpurea
L. (Purple Pitcher Plant), E. ridingsii is obligate in S. flava L. (Yellow Pitcher
Plant), and E. semicrocea is a generalist on all species of Sarracenia. Initial behavioral
observations on these moths were reported by Jones (1921) and followed
by various reports of range and life-history information (Benjamin 1922, Brower
and Brower 1970, Folkerts and Folkerts 1996), but to date none have provided a
detailed life history of any of the three species.
In this study, we focused on E. semicrocea by presenting information from
the unpublished portions of the thesis of Rymal (1980) regarding (1) larva and
adult morphology/development and (2) mortality factors across all life stages.
Additional data are provided from recent observations made in 2010 on (3) adult
behavior and (4) local abundance across the southeastern Coastal Plain. Together,
with a thorough review of previously published information, we present a robust
account of the biology of E. semicrocea.
Life-history and behavior observations were conducted at Packer Bog (1978–
79), Splinter Hill Bog (2010), and Weeks Bay National Estuarine Research Reserve
Site (2010) in Baldwin County, AL (Fig. 1). Historically, Baldwin County
possessed a large and continuous expanse of pitcher plant bog habitat, including
the now pastured Packer Bog, the recently preserved Splinter Hill Bog, and,
most likely, the area now preserved in Weeks Bay National Estuarine Research
Reserve Site (Folkerts 1982). Within the past 100+ years, southern Alabama has
undergone a severe reduction of natural habitat, with remaining bog habitat being
managed by agencies such as Alabama Forever Wild, The Nature Conservancy,
and the National Estuarine Research Reserve System. The bogs in this region are
characterized by deep, poorly drained, and strongly acidic soils found in seep
areas at the bases of slopes and along drainages. The soil is fine, sandy loam on 2
to 5 percent slopes and is very low in natural fertility, with low to medium content
of organic matter. Runoff is slow, and areas that are not ditched are usually saturated
with water from seepage areas (McBride and Burgess 1964). The prominent
pitcher plant species found at each of the three sites was Sarracenia leucophylla
Raf. (White Topped Pitcher Plant), with S. purpurea L. (Purple Pitcher Plant),
S. rubra Walt. (Red Pitcher Plant), and S. psittacina Michx. (Parrot Pitcher Plant)
also occurring at these locations. Surveys of E. semicrocea distribution were
made in 2010 at eighteen sites across the southeastern Coastal Plain (Fig. 2).
Larval and adult morphology/development
Exyra semicrocea larvae were reared from fertilized eggs collected at Packer
Bog in 1978 to 1) determine number of instars and 2) measure head capsule width
of each larval stadium. Larvae (n = 25) were fed cut portions of White Topped
Pitcher Plant leaves in glass petri dishes with moist filter paper at Auburn University.
Daily observations were made to detect ecdysis, and widths of head capsule
2012 J.D. Stephens and D.R. Folkerts 113
were measured on living larvae with an ocular micrometer. The width of the
head capsule has traditionally been used to determine instar stage because head
capsule growth is discrete and occurs with each ecdysis (Harman 1970, Hoxie
and Wellso 1974, Watson and Johnson 1974). The resulting measurements were
used in subsequent field observations to estimate the instar of the larvae. Duration
of developmental stages (i.e., egg, larval instars, pupa) for E. semicrocea
was monitored within tagged pitchers in the field during 1978–79 (n = 72). Adult
lifespans were assessed in 2010 with pupae collected from Splinter Hill Bog, AL
(n = 16), and reared in the lab at Auburn University. Sex of E. semicrocea adults
was determined by detecting the presence of valvae covered by long scales in the
male or the presence of a setose ovipositor in the female. All adults that emerged
in the lab received a nectar substitute of simple sugar water, and information
regarding duration as adult and number of eggs oviposited was recorded.
Figure 1. The three study sites located within Baldwin County, AL where behavioral
observations of Exyra semicrocea were conducted. Due to their close proximity, Packer
Bog and Splinter Hill Bog are represented by one star.
114 Southeastern Naturalist Vol. 11, No. 1
The original description of E. semicrocea was based on drawings and contained
little information about larval morphology (Gueneé 1852). Crumb (1956) briefly
described the larva based on a single preserved specimen. We have expanded this
description and have provided an illustration of the fifth instar (Fig. 3). In addition,
potential morphological adaptations in E. semicrocea adults, which apparently
facilitate walking on downward pointing cellular projections of the pitcher plant
leaf conductive zone, were evaluated using scanning electron microscopy (SEM)
in 1978 and again in 2010. The ability to walk on the interior surfaces of Sarracenia
spp. pitchers is apparently unique to Pitcher Plant Moths (Folkerts 1999).
Therefore, pretarsal characteristics were compared between E. semicrocea and
specimens of two non-pitcher plant-associated noctuids, Helicoverpa zea (Boddie)
(Corn Earworm) and Trichoplusia ni (Hübner) (Cabbage Looper). The latter is a
member of the Plusiinae, the same noctuid subfamily as E. semicrocea.
Adult behavioral observations
Observations of adult flight behavior were made twice a month from June
through September 2010. Ten adults were marked during the day using a florescent
dye powder (Magruder Color Company) and checked the following morning
to assess emergence from leaves (n = 60). Additional adults were located and
their respective pitchers flagged for nighttime observations of flight behavior.
Each adult was sexed by making an incision into the wall of the pitcher and
carefully using a hand lands to examine the lower abdomen. Leaves containing
individuals were marked prior to dusk and monitored for movement throughout
the night. Sex of individual, time of emergence, duration of flight, number of
pitchers visited, duration inside pitchers, flight distance from original pitcher to
final pitcher, and number of eggs oviposited were recorded. T-tests were conducted
in the R v2.6.2 statistical software environment (R Development Core
Team 2008) to test whether there were differences between sexes regarding time
of emergence and lifespan.
Percentage mortality in egg, larval, and pupal stages was calculated from
tagged samples in Packer Bog in 1978–79 (n = 45, 287, 34 respectively), and
periodic collections of larvae displaying signs of parasitism were brought back to
the lab to rear and identify parasitoids. Dead larvae were also collected in order
to ascertain mortality factors. Additional incidents of predation, parasitism, and
fungal pathogens were recorded from incidental field observations made from
1978 through 2010. Finally, we collected a parasitized E. semicrocea larva and
amplified the mitochondria (mtDNA) cytochrome c oxidase subunit gene (COI).
The subsequent sequence was then compared to extant sequences in the NCBI
database via BLAST (Altschul et al. 1990) in order to make an approximate identifi
cation of the parasitoid.
Surveys of local abundance and possible extirpation across the southeastern
Coastal Plain were prompted by reports of declines in E. semicrocea abundance
2012 J.D. Stephens and D.R. Folkerts 115
(Folkerts and Folkerts 1996). During the summer of 2010, we sampled eighteen
sites from eastern Texas through North Carolina in order to determine
current status of E. semicrocea populations (Fig. 2). Exhaustive searches of
every pitcher were conducted in small bogs to determine Exyra population size,
Figure 2. Shaded region represents historical range of Exyra semicrocea across the
southeastern United States, with hash marks indicating historical range that may no
longer contain bogs. The eighteen sites visited in 2010 are represented by stars. The
three localities west of the Mississippi River are Angelina National Forest (AN),
Big Thicket Nature Preserve (BT), and Kisatchie National Forest (KN). Populations
sampled across the eastern portion of the range are Abita Creek (AC), DeSoto National
Forest (DS), Grand Bay National Estuarine Research Reserve Site/National Wildlife
Refuge (GB), Weeks Bay National Estuarine Research Reserve Site (WB), Splinter
Hill Nature Preserve (SH), Conecuh National Forest (CF), Apalachicola National Estuarine
Research Reserve Site/National Forest (AP), Osceola National Forest (OS),
Okefenokee National Wildlife Preserve (OF), Francis Marion National Forest (FM),
Green Swamp Nature Preserve (GS), Prattville Bog (PT), Centre Bog (CT), Reed
Branch Nature Preserve (RB), and North Carolina Bog (NC).
116 Southeastern Naturalist Vol. 11, No. 1
while populations in larger bogs were estimated by extrapolating from counts in
measured areas. Information regarding life stages and female/male ratio were
recorded for each bog.
Results and Discussion
Development, morphology, and behavior
Egg. Descriptions of egg morphology have been presented previously (Folkerts
and Folkerts 1996, Jones 1921), with both accounts noting the spherical
shape and yellow hue. Eggs were an average diameter of 0.7 mm, with slightly
undulating ridges radiating from a central point, where a micropylar area is
evident. These ridges contain tiny pores that are most likely part of the egg respiratory
mechanism (Wigglesworth 1972). Approximate time spent in the egg life
stage was twelve days (Table 1).
An early report of E. semicrocea indicated that eggs are deposited singly due
to the importance of having one larva per pitcher (Jones 1921). Observations by
Folkerts and Folkerts (1996) indicated that number of eggs oviposited varied
from one to several per pitcher. Results from 2010 support the latter: i.e., females
oviposited anywhere from 1–3 eggs per pitcher. While previous observations
could not ascertain whether eggs were oviposited by multiple females, recent
observations were conducted through close monitoring of female nocturnal behavior.
Therefore, we feel confident that a single female laid multiple eggs in a
single pitcher in 2010.
Larva. Larval development of E. semicrocea spans five instars (determined
from number of ecdyses in 1978–79), with head capsule size ranging between
0.32–1.78 mm (Table 2). Duration of stadia 1–3, stadia 3–4, and stadium 5 during
summer months is roughly twelve, nine, and thirteen days, respectively (Table 1).
Duration increases during colder temperatures when quiescence occurs. Overall,
Table 1. Exyra semicrocea average length of time in life stages.
Developmental stage Avg. no. days Range S.D.
Egg 12 6–20 3.9
Larval stadia 1–3 12 7–15 3.2
Larval stadia 3–4 9 7–15 2.5
Larval stadium 5 13 8–21 5.2
Pupa 14 8–20 5.5
Adult 10 7–16 2.8
Table 2. Average measurements of Exyra semicrocea head capsule widths of instars one through
five (n = 10).
Instar Width of head capsule (mm) SD
I 0.32 0.01
II 0.65 0.01
III 0.89 0.07
IV 1.32 0.10
V 1.78 0.21
2012 J.D. Stephens and D.R. Folkerts 117
the eruciform larva ranged from 4 mm in length during the first instar to 30 mm in
length in the fifth instar, with segments having a bright red coloration and white
intersegmental areas (Folkerts and Folkerts 1996, Rymal and Folkerts 1982). The
head capsule of E. semicrocea is ivory with four incomplete and irregular black
bars, and mandibles each possessing five teeth (Fig. 3a). An eversible gland is
present on the ventromeson of the prothorax. Ventral prolegs (Fig. 3b) bear crochets
in a biordinal mesoseries. There are approximately 26 crochets in the two
series on A6, with the shorter series of crochets being bifid (Figs. 3c). The body
is covered with microspinules, which occur in especially dense patches on the
dorsum of A1–A4. The prespiracular group of setae on the prothorax is bisetose.
D1, D2, and SD1 on the meso- and metathorax arise from chalazae. Paired lateral
projections are found on abdominal segments one through four (Fig. 3b), with
length decreasing rearward. These fleshy lateral projections, termed “lappets”
(Jones 1921; Fig. 3b) are covered with microspinules and bear the SD1 seta at
their apex. Lappets are absent in first instar larvae, are relatively narrow and
elongate in instars two and three, and become enlarged in instars four and five.
The ability of E. semicrocea larvae to avoid entrapment in pitcher plants may
be due in part to the function of the lappets (Folkerts 1999, Jones 1921). Larvae,
when disturbed, will often curl their bodies and drop into the pitcher. The projecting
lappets of these larvae prevent them from falling to the lowest, narrowest
portion of the pitcher, which contains long, stiff, downward pointing hairs. Other
important entrapment-avoiding mechanisms of the larva include a dragline of silk
that is often used inside the pitcher to pull the larva up from the pitcher bottom
and also for feeding on the inner leaf surface, which destroys the trapping function
of the leaf.
Damage to the leaves by E. semicrocea has been well documented (Folkerts
1999, Folkerts and Folkerts 1996, Jones 1921, Moon et al. 2008, Rymal and
Figure 3. Exyra semicrocea larva: a) mesal view of the right mandible, b) lateral view of
a fifth instar, and c) ventral view of the crochets of a proleg I.
118 Southeastern Naturalist Vol. 11, No. 1
Folkerts 1982). Typically, a first or second instar cuts a narrow feeding channel
from within a young leaf, which encircles the pitcher and causes wilting
above. The wilted portion of the leaf forms a hardened cap over the mouth of the
pitcher and creates a protective feeding chamber (Folkerts 1999, Jones 1921). In
contrast, feeding on mature pitcher plant leaves does not produce this wilting effect.
Third, fourth, and fifth instar often produce a fine, silken web covering the
opening of an inhabited pitcher (Folkerts 1999). A feeding chamber of this kind
usually has a web ceiling, a floor of frass, which accumulates above the level of
the prey mass, and walls formed by the membranous outer leaf surface, which
remain after the inner leaf layers have been removed by feeding (Folkerts 1999).
The web ceiling was observed to be an effective shelter against water intrusion
during a gentle rain and also excluded potential spider predators (Jones 1921).
It has been suggested that dispersal of larvae only occurs once the entire pitcher
has been consumed because of inherent predation risk (Jones 1921), but Folkerts
(1999) documented multiple migrations between pitchers during development.
Usually movement between pitchers occurs shortly after the first instar hatches,
during second or third instars, in the fifth instar, and finally before pupating. In
most cases, the leaves are not completely consumed. Dispersal of first instar
partly explains why more than one larva is rarely found in a leaf, even though
several eggs may have been present. In a few instances, more than one larva has
been found inhabiting a single pitcher, with webbing or a layer of frass separating
them. This separation was also noticed in individuals reared in the lab in 2010.
Overwintering of E. semicrocea occurs as second, third, fourth, or fifth
instars, with feeding ceasing in late November (Folkerts and Folkerts 1996).
Various types of hibernaculae have been observed (Jones 1921). Small larvae are
most often found near the bottom of the pitcher, having burrowed beneath the
accumulation of prey. Large larvae are sometimes buried in frass or cling to dry
pitcher walls, well above the level of frass and prey. Occasionally, chambers have
web ceilings with particles of frass incorporated into the silk.
Pupa. The brown pupa is approximately 11 mm in length (Table 1). Before
pupation, fifth instars disperse to pitchers that are usually undamaged and often
cut a small hole (approximately 2 mm in diameter) in the lower portion of the
pitcher tube (Folkerts 1999). Pupal chambers are located above these holes,
which presumably function to drain excess rainwater. The cocoon varies from a
few strands of supporting silk near the anterior end to a mesh of silken strands
covering the entire pupa (Jones 1921). The simplest type of chamber contains a
pupa, cephalic end up, suspended by silken strands attached to the interior wall
of a pitcher with varying amounts of silk surrounding the pupa. A variant on this
type of chamber is shielded above by a thin sheet of silk and bordered below by
varying amounts of frass and silk (Jones 1921). The least common type of pupation
chamber is found in pitchers with obvious feeding damage. In this case,
the pupa is found beneath the level of frass in a silk-lined chamber only slightly
larger than the pupa itself.
Adult. Adults are approximately 12.5 mm in length with wings folded. The
forewing averages roughly 11 mm in length and has the most variable wing color
2012 J.D. Stephens and D.R. Folkerts 119
patterns of the three Exyra spp. (Folkerts and Folkerts 1996). The common type
has a black distal half of the forewing with a straw basal half and hind wings
completely black or gray in color. Head and prothorax are black, with the remaining
body, including the filiform antennae, being straw (Folkerts 1999, Jones
1921, Rymal and Folkerts 1982; Fig. 4). Two other forms of E. semicrocea with
variations of the forewing pattern were described by Benjamin (1922) and Dyar
(1904), with Benjamin’s aberration validated by McDunnough (1938) when he
listed it as a form. Moths have varying degrees of black mottling on the distal half
of the forewing, which is combined with variation in shading of the hindwing.
However, the variation does not show a geographic pattern, and specimens with
all variations can be found at the same bog (Folkerts 1999).
Regarding avoidance of being trapped in the pitcher plant, Exyra adults
have the apparently unique ability to walk on the interior of pitcher plant leaves
(Folkerts 1999). While it has not been possible to examine the pretarsal position
of a live adult within a pitcher, we can make assumptions about the potential
functions of pretarsi in clinging to pitcher plant surfaces using scanning electron
Figure 4. Exyra semicrocea in copulation. The lower and lighter moth is the male.
120 Southeastern Naturalist Vol. 11, No. 1
micrographs (SEM) and comparative measurements. SEM revealed a difference
in the shape of the pretarsal claws of E. semicrocea when compared to other
noctuids, H. zea and T. ni. Unlike H. zea (Fig. 5a) and T. ni (not pictured), the
metathoracic pretarsi of E. semicrocea (Fig. 5b) have bifid claw tips with arms
of equal length, and claws projecting laterally, causing the empodium and aroliar
pad to extend beyond the claws. This lateral projection of the claws also occurs
in the mesothoracic (not pictured) and prothoracic pretarsi (Fig. 6); the claws of
the prothoracic pretarsus are also bifid, but have thicker bases than in other legs.
In H. zea, the arms of the claw’s bifid tips are of unequal length, and the claw tips
in the T. ni are not bifid. Although it is impossible to conclusively determine the
function of these structures in Exyra, comparative measurements of claws and
leaf projections lead us to believe they are used in placement of the pretarsus on
the leaf surface. Cellular projections of the conductive zone in the White Topped
Pitcher Plant are ≈10 μm wide at the base, tapering to a point, and ≈20 μm apart.
Moth pretarsi have notches in bifid claw tips ≈10 μm wide and a width between
tips of ≈20 μm (measurements were taken at multiple SEM angles not shown).
Claw tips may be used in grasping leaf projections. Additional behaviors appear
Figure 5. Scanning electron micrograph of the pretarsus of the adult metathoracic leg of
a) Helicoverpa zea (magnification 500x) and b) Exyra semicrocea (1000x).
Figure 6. Scanning electron micrograph
of the pretarsus of the adult
prothoracic leg of Exyra semicrocea
2012 J.D. Stephens and D.R. Folkerts 121
to be vital in trap avoidance, as E. semicrocea adults always perch in an upright
position within pitchers, and even enter pitchers backward. Moreover, they
copulate at a right angle (Fig. 4), which is in contrast to the end-to-end coupling
typical in noctuids. This copulation position ensures neither moth is oriented with
head downward in the pitcher. It is likely that a combination of morphological
and behavioral traits allow E. semicrocea to avoid entrapment.
Additional behavioral observations of E. semicrocea suggest moths are mostly
stationary and well below the orifice of the pitcher throughout the day. This
is possibly an adaptation to avoid predation. Nighttime observations in 2010 revealed
that moths begin to move prior to dusk, feeding on the extrafloral nectaries
near the orifice of the pitcher before quickly retreating back to their sedentary
position, thus confirming descriptions made by Jones (1921). This feeding behavior
typically occurs one to six times before emergence from the pitcher for flight.
Flight emergence occurred in all florescent dye-marked individuals (n = 60),
as none were found in the original pitcher the following morning. Descriptions
of nightly flight emergence made in 1980 indicated that E. semicrocea females
emerge from pitchers shortly after dusk and fly to nearby pitchers. Males emerge
soon after and fly in search of females within pitchers. Observations made in
2010 supported these inferences and revealed that female moths tend to leave ≈24
minutes after sunset (range of 9–55 min). Females usually fly to nearby pitcher
plants and rarely venture high above the bog. Female flight time was from 2–30
minutes ( x = 13), with an average distance of 16.84 m (n = 12). During this time,
females often visited multiple pitchers ( x = 4), typically staying less than 1 minute
(although three females stayed in visited pitchers for over 30 minutes). Three
out of seven females that were observed in pitchers with males during the day
oviposited 1–3 eggs in those pitchers. Oviposition by females in the lab revealed
a range from 0–93 ( x = 41, n = 5) eggs. These numbers suggest that females have
the ability to lay numerous eggs per pitcher over their average ten-day lifespan as
adults (no difference in male and female lifespan t = -0.9976, df = 14, P = 0.3354;
In contrast to females, males exhibited a more erratic flight pattern and were
therefore harder to observe. The average male emergence time was 3 hours and
32 minutes after sunset, with the earliest emergence being 1 hour and 5 minutes
after sunset. This emergence time is significantly different from females
(t = -8.4349, df =15.477, P < 0.001). Measures of male flight time and distance
were unattainable due to the quickness of males and their tendency to fly several
meters above the bog. Males seen in the field appear to be lighter in color than
females due to a loss of wing scales that likely occurs during flight (Fig. 4). This
observation, when compared to sedentary captive males that retain their dark
coloration in the lab, indicates that males potentially engage in more flight than
females, as is necessary in the search for receptive females. This greater tendency
for flight by males is further supported by a light trap study of E. fax, in which
mainly males were caught, indicating that males of that species also fly more
frequently (Brower and Brower 1970).
122 Southeastern Naturalist Vol. 11, No. 1
Mortality in the egg stage was recorded at 56% in 1978–79 (Table 3). This
rate of mortality is assumed to be the combined results of infertility, predation,
fungal pathogens, and parasitism. Although egg predation was never witnessed,
several small spiders capable of preying upon eggs in pitchers were observed.
Eggs appearing to have been parasitized were distinguished by a silvery black
color and tiny exit hole in the eggshell. The egg parasitoid was never captured
and identified, but is believed to be a hymenopteran. This hypothesis is supported
by previous observations of E. semicrocea egg parasitism by a presumed species
of Chalicidoidea in a bog in North Carolina (Jones 1921).
Larval mortality is difficult to ascertain, as disappearance of larvae from tagged
pitchers was often due to dispersal to nearby pitchers. Therefore, a disappearance
rate was calculated at 60% and observed mortality at 15% (Table 3). Predation
of dispersing larvae was observed on multiple occasions between 1978 and 2010
by spiders (i.e., Peucetia viridans (Hentz) [Green Lynx Spider], Strotarchus
piscatoria (Hentz) [Bent-leaf Spider], and Phidippus audax (Hentz) [Common
Jumping Spider]) and Solenopsis invicta Buren (Formicidae; Red Imported Fire
Ant). Fire ants and S. piscatoria have also been seen preying on E. semicrocea
larvae within pitchers. Additional mortality of E. semicrocea larvae within pitchers
was due to an unidentified tachinid parasitoid, a braconid parasitoid, and the
fungal pathogen Nomuraea rileyi (Farlow) (Moniliaceae). The fungal pathogen
attacks larvae of all instars and was most commonly seen in late fall. The tachinid
parasitoid emerges as a larva from the fifth instar and was most commonly seen
during the overwintering period. The braconid parasitoid was collected as a pupa
from a third instar in 1978. In addition to predation and parasitism, larvae have
been witnessed to drown in pitchers after severe storms.
The pupal stage incurred 29% mortality, primarily the result of spider predation
(Table 3). For example, Bent-leaf Spiders preyed upon 50% of the tagged
pupae during a one-week period in 1978. In addition, a hymenopteran parasitoid
mitochondrial cytochrome oxidase subunit I (COI) sequence (97% match with
Diadegma semiclausum (Hellén) [Ichneumonidae] within the NCBI database)
was discovered in one pupal sample from a study in 2010 (data not shown).
Table 3. Mortality factors for Exyra semicrocea in Sarracenia leucophylla in Baldwin County, AL.
Lifestage n Mortality Mortality factors Noted predators and parasites
Egg 45 56% Infertility, fungal pathogen, Unknown
Larval 287 75%* Dispersal, fungal pathogens, Bent-leaf Spider, Green Lynx
predation Spider, Jumping Spiders, Red
Imported Fire Ants, Fungus,
Pupa 34 29% Parasitism, predation Bent-leaf Spider
Adult N/A N/A Dispersal, predation Lycosids, Odonates, Green Lynx
*60% missing, 15% observed mortality.
2012 J.D. Stephens and D.R. Folkerts 123
Percent mortality in the adult stage was not estimated, as adults could not be
tracked in the field. However, a variety of predation events have been witnessed
in incidental field observations. Exyra semicrocea does not fly during the daytime
unless disturbed from the pitcher. When this occurs, dragonflies have been observed
to be diurnal predators. Nocturnal predators are generally bats and spiders.
For example, predation of a female moth in flight by a wolf spider was observed
during the 2010 observations. It has also been noted on several occasions that
dead adult Exyra semicrocea were present and still in the upright position within
the pitcher, with no apparent cause of death.
Numbers, life stages, and sex ratios varied substantially across all sampled
sites (Table 4), which is typical for a multivoltine insect. Individuals were not
found at four localities (i.e., CT, PT, RB, NC; see Fig. 2 for abbreviations),
although E. semicrocea had been previously recorded at those sites (D.R. Folkerts,
pers. observ.; M. Hodges, The Nature Conservancy, Atlanta, GA, pers.
comm.). These sites are home to small, isolated pitcher plant bogs composed
of one or two federally endangered pitcher plants (i.e., S. oreophila (Kearney)
Wherry [Green Pitcher Plant], S. rubra ssp. alabamensis (F.W. & R.B. Case)
Schnell [Alabama Pitcher Plant]; USDA NRCS 2009). An exhaustive search
of all pitchers at AC, AN, OS, OF, FM, and GS bogs revealed low abundance,
potentially due to limited, patchy habitat. For example, bog habitat in OF,
OS, and FM was mostly found along roadsides, with patches of interior bog
at OF and FM; AN has recently undergone bog restoration. On the other hand,
Table 4. Numbers of E. semicrocea at eighteen sites (see Fig. 2 for site localities and corresponding
names) surveyed during May–June 2010.
Site n surveyed (ha) (#/per ha) # larvae # pupae # adults F:M ratio
AN* 3 0.25 12 3 0 0 n/a
BT 30 0.15 300 13 3 14 3:4
KN* 32 0.25 128 0 0 32 1:1
AC* 30 3.00 9 21 0 9 2:7
DS 30 2.00 16 28 0 2 1:1
GB 30 2.75 11 0 0 30 1:2
WB 54 1.21 44 15 1 38 11:8
SH 27 1.11 24 9 1 17 7:10
CF 29 0.74 39 28 0 1 1:0
CT* 0 0.10 0 0 0 0 n/a
PT* 0 0.08 0 0 0 0 n/a
AP 30 0.52 60 0 0 30 1:2
OS* 5 0.04 125 5 0 0 n/a
OF* 22 0.36 61 19 3 0 n/a
RB* 0 0.18 0 0 0 0 n/a
FM* 18 0.16 113 11 5 2 1:1
GS* 17 2.75 6 17 0 0 n/a
NC* 0 0.28 0 0 0 0 n/a
*Indicates sites that were exhaustively searched.
124 Southeastern Naturalist Vol. 11, No. 1
other bog habitats, such as AC, were large but had not been burned recently, and
therefore, pitcher plants were less dense. The low population numbers of E. semicrocea
at GS and FM may be influenced by competition with a sister species,
E. ridingsii. Exyra ridingsii only inhabits the Yellow Pitcher Plant, which extends
from Alabama into North Carolina. The abundance of E. ridingsii appears
to shift with increase in latitude, from being rare to absent in the southernmost
portion of Yellow Pitcher Plant range to replacing E. semicrocea in leaves of
Yellow Pitcher Plant in the northern portion of the range (J.D. Stephens, pers.
observ.). While this observation may not be the case year-round, this potentially
competitive interaction (exclusion) of E. semicrocea from Yellow Pitcher Plant
was also noted in another population in South Carolina in the early 1900s (Jones
1921). The abundance of E. ridingsii throughout its range, as well as effects on
E. semicrocea, has not been studied.
The lack of E. semicrocea at four sites surveyed, low abundance at other sites,
and loss of bog habitat (e.g., Packer Bog and the peninsula of Florida) is of serious
concern, especially with estimates predicting that perhaps 3% of original
bog habitat remains due to fire restriction, urbanization, forestry, and agriculture
(Folkerts 1982, Folkerts and Folkerts 1993). This decline in bog habitat has
resulted in fragmentation of once continuous bog habitat (Folkerts 1982). Current
management practices to preserve these fragments often involve prescribed
burns conducted during the dormant season (i.e., winter burns). While these fires
are beneficial to the plants, they may have negative effects on members of the
arthropod community that are not adapted to winter burns. For example, E. semicrocea
populations overwinter as larvae, are unable to disperse, and are likely
to be severely damaged by winter burns (death of larvae in even a light burn has
been observed). When prescribed burns involve the entire bog area, as is often
the case in small and isolated fragments, no insects survive to repopulate those
areas after the burn. Therefore, more research to address winter fire effects on
the pitcher plant community is warranted, especially given the great diversity of
endemics and associates inhabiting pitcher plant bogs. Maintaining and restoring
pitcher plant bogs in the southeast is vital to preserving these communities for
We would like to thank R.L. Godwin, N. Hall, C.R. Holt, S.R. Santos, and M.C. Wooten
for comments and suggestions that greatly improved this manuscript as well as R.L.
Godwin, C. Stephen, and R. Hoskins for invaluable field assistance. We would also like
to thank R.L. Brown, B.G. Scholtens, and D.L. Wagner for reviewing this manuscript
and D.L. Wagner for taking the time to provide additional larval characteristics. We are
extremely grateful to the following agencies for facilitating logistics associated with this
study: Alabama Forever Wild, NERRS/NOAA (Matt Chasse, Alison Krepp, Scott Phipps,
and Angela and Will Underwood), The Nature Conservancy (Adrienne Bell, NC; Malcolm
Hodges, GA; Sara Over, NC; Megan Sutton, NC; Keith Tassin, AL), US Forest Service,
and US National Park Service (Brian Lockwood). We thank the late George W. Folkerts
2012 J.D. Stephens and D.R. Folkerts 125
for the inspiration behind this study and for the initial introduction to this species. Parts
of this research were conducted under an award from the Estuarine Reserves Division,
Office of Ocean and Coastal Resource Management, National Ocean Service, National
Oceanic and Atmospheric Administration (Award # NA10NOS4200038) and a Grant-In
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