Ecological Entomology (1985) 10,291-298

Host plant toxins and unpalatability of Neacoryphus bicrucis

(Hemiptera: Lygaeidae)

DENSON K. McLAIN and DONALD J. SHURE Department of Biology,

Emory University, Atlanta, Georgia

ABSTRACT. 1. Host plant choice of the seed bug, Neacoryphus

bicrucis Say (Hemiptera, Lygaeidae), was evaluated in four different
Georgia habitats. N . bicrucis utilized only species of Senecio as host
plants at a granite outcrop and at old fields on the coastal plain, in the
piedmont, and in the Blue Ridge Mountains.
2. In laboratory tests N. bicrucis is distasteful to the green anole lizard,
Anolis carolinensis Voight. Only six of ninety field-collected bugs were
eaten in palatability trials while eighty-four of the remaining ninety
attacked bugs were rejected by lizards without apparent harm. How-
ever, the bugs were palatable to Fowler's toads, Bufo woodhousei fowleri
Hinckley, which ate all thirty-six bugs offered to them.
3. N. bicrucis selectively sequesters pyrrolizidine alkaloids from Sene-
cio spp. These may cause the insects' distastefulness to green anoles. In
palatability trials, lizards ate all twenty insects reared on sunflower
seeds, Helianfhus annus, but rejected all twenty reared on Senecio
smallii.

Key words. Alkaloids, Anolis carolinesis, Bufo woodhousei fowleri, host

specialization, insects, Neacoryphus bicrucis, old fields, palatability,
plant-animal interactions, Senecio.

Introduction zidine alkaloids (reviewed in Blum, 1981).

Predators and parasitoids are likely to depress
insect populations (Lawton & Strong, 1981).
Therefore, noxious chemicals sequested from
plants may aid insect defence and even cause
selection for host plant specificity (Rothschild,
1976; Berenbaum, 1981). Numerous studies
document the sequestion from host plants of
toxins including cardiac glycosides and pyrroli-
Correspondeke: Dr D. K. McLain. Department
of Biology, University of Notre Dame, Notre Dame,
IN 46556, U.S.A.
Some species of insects thus exhibit a strong
relationship between host plant choice and
vulnerability to predators (Duffey et af., 1977;
Bowers, 1980, 1981; Brower & Glazier, 1975).
Lygaeids may especially depend upon the
sequestion of plant natural products for their
defence. For example, Scudder & Duffey
(1972) found that species in . twenty-seven
lygaeid genera sequester cardiac glycosides.
The present study examines host plant
choice of the seed bug, Neacoryphus bicrucis
Say (Lygaeidae), in four different habitats in
291
292 Demon K. McLain and Donald .I.
Shure
Georgia. We evaluated the relationship be-
tween palatability to two vertebrate predators
and host plant choice by comparing the re-
sponse of predators to insects reared in the
laboratory on either their natural host plant
seeds or sunflower seeds. The use of two
classes of vertebrate predators, toads and
lizards, permitted us to evaluate whether
generality of repulsiveness to vertebrates can
be inferred from palatability trials involving
only one type of predator.
N . bicruck migrates for long distances across
its large geographic distribution from Brazil to
Canada (Solbreck, 1978). In the southeastern
U.S. it appears to feed preferentially on Sene-
cio spp. or species in related genera (Cacalia
and Erechtites) in the tribe Senecioneae
(Blatchley, 1926; McLain, 1981; Solbreck &
Pehrson, 1979). N.bicruck feeds on a variety
of flowering species elsewhere, exhibiting a
slight preference for asters (Solbreck, 1978).
Thus, it is interesting to know if this migratory
seed bug sequesters toxins from its host plants
in areas where it specializes on Senecioneae.
This analysis is especially relevant since N . bi-
cruck apparently sequesters cardiac glycosides
from milkweeds in the northern U.S. and
Canada (Scudder 8c Duffy, 1972).
N.bicruck is present in Georgia only in early
spring to early summer (McLain, 1982, 1984a.
b). Laboratory studies indicate that flight activ-
ity for long-range migration’ increases with
declining host plant abundance (Solbreck,
1978). Thus, this species probably migrates from
its Georgia habitats in early summer.
Methods
Host plant choice
Host plant choice was determined at four
field sites. Site A is a granite outcrop, Arabia
Mountain, located 35 km east of Atlanta.
Plants at site A occur in shallow soil-filled
depressions which are separated by exposed
granite. Site B is a 5 ha old field near
Braselton, 70 krn northeast of Atlanta. Sites A
and B are in the piedmont physiographic
province. Site C is a 1 ha old field near
Cordele on the coastal plain approximately 200
km south of Atlanta. Site D is a 1 ha field near
Dillard which is in the Blue Ridge Mountains
approximately 150 km north of Atlanta. The
flowering species composition of these herb-
dominated habitats is described in detail in
McLain (1982).
Each field site contains approximately ten to
thirty species of flowering plants in mid-late
spring when N.bicruck is abundant. Host plant
choice was determined by inspecting for adults
and nymphs on all plants intersected by three
parallel transects located down the long axis of
each field. Host plant choice was determined
at site A in early April 1980-83, at site B in
late April-May 1979-83, at site C in late
April-May 1981, and at site D in June 1979-
82. The relative abundance of host plants was
determined in 1981 as the proportion of 0.25
m2 quadrats located every 2 m along the
transects which contained the host plant spe-
cies. There were 100-150 quadrats sampled
along each transect.
The response of N.bicrucis to plant abund-
ance was determined at site A by counting the
number of bugs and number of host plant
flower heads per 0.25 mz in 1979-81. The area
(m’) of the host plant patch was also recorded.
At site A plant patch boundaries can be
unequivocally determined since large stretches
of barren granite separate different patches.
Differences in the number of seed bugs as a
function of year, patch size and flower head
density were evaluated using a three-way
ANOVA (Sokal & Rohlf, 1981). Four patch
sizes (0.25 mz, 0.25-1.0 m2, 1.0-3.0 mz and
3.0-6.0 mZ)and six flower head densities (0-100,
101-200,201-300, 301300, 401-500, and 501-
600 per 0.25 m2) were recognized in the
analyses.
Palatability
Palatability was first tested with green anole
lizards Anolir carolinensis Voight. This species
has been employed in other studies on insect
palatability .(Sexton, 1964; Sexton et a f . , 1966).
Lizards were obtained from Carolina Biologic-
al Supply Company and maintained on a diet
of crickets and a mixture of field-collected
grasshoppers, flies, plant bugs and snout
beetles for 1 month prior to testing.
Lizards were provided with diet insects twice
per week. Palatability tests were conducted
after the lizards had been starved for 3 days.
Tests were run in 2 5 ~ 2 0 x 4 5cm cages. The
bottom and two sides were of plywood while

the top and remaining sides were of fibreglass
window screening. A single lizard was placed
in a cage with three newly collected N.bicrucis.
The lizard was allotted 10 min to attack one of
the insects. The trial was concluded if the
lizard swallowed one of the insects. In this case
the insect was considered palatable. Lizards
that attacked and rejected an insect were
placed in another, but identical, cage with
crickets. The N . bicrucis tested was considered
unpalatable only if the lizard ate one of the
crickets. Each lizard was used in only a single
trial.
Palatability tests with lizards were conducted
with field-collected insects from all field sites
(ninety lizards employed) and on insects
reared in the laboratory on the seeds of
sunflower, Helianthus annus L. (twenty lizards
employed) or ragwort seeds, Senecio smallii
Britton (twenty lizards employed). Previous
studies have demonstrated that lygaeids do not
sequester noxious compounds from sunflower
seeds (Duffey et al., 1977).
The palatability of N.bicrucis was also tested
with Fowler's toad, Bufo woodhousei fowleri
Hinckley. Twelve toads were collected from
areas surrounding Lullwater Lake on the cam-
pus of Emory University in suburban Atlanta,
Georgia. Each toad was housed alone in a
25X25X25 cm cage of plywood with a nylon
screen front and top. Each toad was employed
in three trials. Otherwise, the treatment of
toads was exactly like that of lizards.
Sequestration of plant secondary compounds
Host plants were assayed for the presence of
pyrrolizidine alkaloids. Each species or a close-
ly related species is reported to contain these
secondary compounds (Bull et al., 1968; Mat-
tocks, 1972; Levin & York, 1978). The fruiting
parts of five plants of each host species were
collected from field sites A, B and D and
analysed.
Insects from several locations were also
analysed for pyrrolizidine alkaloids. Analyses
of insects (ten individuals per assay) were
delayed for 1 day after collecting. The insects
were kept without food during this period so
that gut contents would not be reflected in the
assays. Insects were obtained at sites B and D
at the peak of Senecio flowering. Insects were
collected from site A on three occasions: (1) a t ,
Unpalatability of Neacoryphus bucrucis, 293
the peak of Senecio flowering, ( 2 ) at the
initiation of flowering when insect abundance
is very low, and (3) during the development of
nymphs when the abundance of adults is very
low. Adults collected at the initiation of
flowering at site A probably represent mig-
rants without prior feeding experience at the
granite outcrop. Insects reared in the labora-
tory on the seeds of either sunflower or
ragwort, Senecio smallii, were tested for the
presence of alkaloids. Eggs were obtained
from females collected at site B.
The colourimetric assay of Mattocks (1971)
was used to screen plants and insects for the
presence of pyrrolizidine. alkaloids. This
method employs a modified Ehrlich's reagent
which produces a red colour if alkaloids are
present. Since it is possible to obtain a positive
result for material not containing alkaloids,
species giving positive results were reanalysed
by thin-layer chromatography. A negative re-
sult with the colourimeter test is conclusive.
The method of Sharma et al. (1965) was
followed for thin-layer chromatography. Tissue
extracts in methanol were applied to a silicagel
G chromatographic plate and developed with a
mixture of chloroform: methanol: ammonia
(85: 14:l). After air drying, the plate was
sprayed with Dragendorff s reagent, which
produces orange spots where alkaloids are
present. Different alkaloids are distinguished
by the distance they migrate on the chromato-
graphic plate. The ratio of the distance an
alkaloid migrates from the point of extract
application divided by the distance the solvent
has run from the point of application yields a
characteristic Rfvalue for each type of alkaloid.
Results
Host plant choice
2V.bicruci.s used only members of the genus
Senecio as host plants at all four field sites
(Table 1). All species of Senecio present at any
field site were utilized as host plants. Other
genera in the tribe Senecioneae were not
present in the habitats examined. Neither the
number of species in the habitat (range ten to
thirty) or the relative abundance of Senecio
(2-74%) influenced host plant choice (Table
1). Eight other species of asters were frequent-
294 Denson K . McLain and Donald J . Shure
TABLE 1. The relative abundance of host Senecio species present at field sites
containing vaned numbers of total plant species, aster species and total number of
plant families. Relative abundance is the proportion of 0.25 m2 transect quadrats
containing Senecio spp.
Site Host plant Relative
species abundance
A Senecio tornentoms 0.51
B S.smallii 0.74
C S.smaNii 0.19
D S.obovotus 0.02
Total
ly present but never utilized. The preference of
N . bicrucis is genus rather than species specific
since different species of Senecio were present
in different habitats (Table 1).
The response of N.6icruci.s to its host plant
species was patch size and resource density-
dependent (Figs. 1 and 2). N . bicrucis adults at
site A were more abundant in large than small
patches of Senecio tomentosus and especially
where the flower head density was high in all
three years, 1979-81 (Fig. 1; P<0.05 for the
effect of year, patch size and flower head
density, three-way ANOVA). The abundance
of nymphs in 1980 and 1981 was also positively
associated with flower head density and patch
size (Fig. 2; Pc0.05for flower head density and
patch size, fi0.05 for year, three-way ANO-
VA). Similar responses were observed at the
other field sites tested (McLain, 1982).
Senecio flowers and then releases its seeds
over a relatively short 6-8 week period in each
habitat. N.bicrucis is not present in any of the
habitats either before or after Senecio comes
into flower. Adults apparently migrate as their
host plants dry up. After the adults migrate
FIG. 1. Abundance of adult N.bicrucis at site A
of flower heads (number per 0.25 m’).
No. species No. asters No. families
11 4 8
30 7 12
10 2 6
16 6 11
45 12 14
nymphs appear on the ground where they
complete their development upon fallen Senecio
seeds. This new generation of adults also
disperses from the field sites upon completion of
development.
Palatability
Insects from all four field sites were highly
distasteful to the green anoles (Table 2). The
proportion of field-collected lygaeids rejected
(84/90)was significantly greater (P<O.OOOl;
t=8.7; 1-test for proportions) than the propor-
tion eaten (6/90).Insects attacked and rejected
by lizards were generally not visibly injured. In
fact, N.bicrucir adults were observed to with-
stand as many as four attacks by different
lizards without apparent harm. The lizards, on
the other hand, were frequently irritated.
Lizards wiped their snout andlor tongue on the
floor of the cage immediately after throwing an
insect aside. These behaviours were not
observed by lizards biting crickets.
Insects reared in the laboratory were un-
palatable if they fed upon Senecio smalfii seeds
as a function of host plant patch size (m’) and density
 Unpalatability of Neacoryphus bicrucis 295

200
v)
I
%>. 100
z
0

FIG. 2. Abundance of N.bicrucic nymphs at site A as a function of host plant patch size (m') and
density of flower heads (number per 0.25 m').

but not when fed sunflower seeds (Table 2).
Anoles rejected significantly more insects that
had fed on Senecio smallii than insects that had
fed on sunflower seeds v=40; P<O.Ool).
There was no evidence such as snout wiping
behaviour or failure to eat attacked sunflower-
reared insects which indicated that insects
reared on sunflower seeds were unpalatable.
In contrast to the lizards, toads evidently
found the field-collected seed bugs entirely
palatable. All twelve toads ate a seed bug
(36/36 bugs eaten) in all three trials. No bugs
were rejected by toads. There was no be-
havioural indication, such as mouth-wiping,
that the seed bugs were distasteful. Unlike the
lizards which crushed their prey before swal-
lowing, the toads swallowed bugs whole with-
out any obvious chewing.
Toxin sequestration
All of the host Senecio spp. analysed gave
positive results for the presence of pyrrolizi-
dine alkaloids (Table 3). Adult N.bicrucis
collected during peak flowering of Senecio spp.
also gave positive results for the presence of
alkaloids. However, the Rf of the insects and
their host plants did not always match (Table
3). Females collected from habitats with
S.srnallii or Xobovatzu Muhl (sites B, C, D)
possessed alkaloids with Rf values similar to
their host plants. The relative abundance of
these alkaloids in female N.bicrucis did not
always match their relative abundance in Sene-
cio spp. Males at all field sites possessed only a
single alkaloid which in each case had a high
Rf value. Host plants at sites B and D posses-
sed an alkaloid of similarly high Rf value. Male
and female insects at site A contained a high
Rf alkaloid not present in their host plant
species.
Temporal variations occurred in the pre-
sence of alkaloids in insects collected at the
granite outcrop (site A). Adults arriving at the
initiation of S.tomentosus Michaux flowering
lacked detectable quantities of alkaloids. Alka-

TABLE 2. Palatability of field collected and laboratory reared

NeacorvDhlLs bicruck to ereen anoles.
Field site No. No. rejected No. rejected
eaten harmed unharmed
A 1 2 12
B 4 6 43
C 0 2 10
D 1 0 9
Total 6 10 74

Laboratory reared on:

Helianrhus annus 20 0 0
Senecio smallii 0 1 19
296 Demon K . McLain and Donald J . Shure
TABLE 3. R, values of alkaloids present in field collected and laboratory reared N.6icrucis
males and females and host plants, Senecio spp. Relative abundances are indicated by + , + + ,
etc., where more than one alkaloid is present.
Rf values
0.1 0.2 0.3
Field collected
Site A
S. iorneniosus 0.31(+)
N .bicrucis male
female 0.36(+)
Site B
S.srnaNii 0.32(+)
N . bicrucis male
female
Site D
S.obovaius 0.35(+ +) 0.48(+)
N.6icrucis male
female
Laboratory reared
S.smal1ii seeds 0.05( +)
N.bicrucis male
female 0.05( +)
loids were present in adult insects during the
flowering period, but were absent from newly-
moulted adults at the termination of flowering.
Insects reared on sunflower seeds did not
contain alkaloids. However, insects reared in
the laboratory on S.smallii seeds did possess
alkaloids (Table 3). Males possessed only one
alkaloid of high Rfvalue. Females possessed
three alkaloids with Rf values similar to those
of alkaloids in S.smallii seeds.
Discussion
N. bicrucis is distasteful to some but not all of
its potential predators. The distastefulness of
the seed bug to anoles depends upon the
sequestration of toxic or noxious chemicals
from host plants, Senecio spp. Individuals
reared on non-host plant seeds are palatable to
lizards in contrast to the unpaiatability of
insects reared on seeds of their natural host
plants. The impact of plant secondary chemis-
try on the predators of herbivorous insects can
be an important selective factor in the evolu-
tion of host plant choice (Price et al., 1980).
Thus, predation pressure may select for the
observed preference of N. bicrucis for Senecio
spp. Furthermore: the characteristic secondary
chemistry of the genus Senecio (Mattocks,
1972) if not the tribe (Levin & York, 1978)
~
0.4 0.5 0.6 0.7 0.8 0.9
-
0.43(++)
0.81
0.59(+ +) 0.79(+ + +)
0.44(++) 0.83(+ + +)
0.86
0.40(+ +) 0.54( +) 0.78(+ + +)
0.80(+ + +)
0.83
0.40(+) 0.75(++)
0.45(++) 0 87(+++)
0.87
0.50(++) 0.8O(+ + +)
could enable N.bicrucis to feed with impunity
on numerous other species across a wide
geographic area.
The degree to which predation selects for
specialization on Senecio depends upon the
relative risk of predation from predators which
find Senecio spp.-fed bugs distasteful. In this
regard, we have no data on the relative abund-
ance of toads and lizards in the habitats
studied. The most common predators in patch-
es of Senecio spp. are ambush bugs (Phyrnafa
farciafa) and assassin bugs (Sinea diademu).
Neither of these species will attack N.bicriicis
when confined with it in laboratory cages,
although they readily feed on other small
coreids and mirids (McLain, unpublished
observations). Ground-feeding birds may also
be potential predators of N.bicriicis. It is not
known if birds find N.bicritcis unpalatable.
However. birds are highly susceptible to chro-
nic toxicity from pyrrolizidine alkaloids
obtained from dietary Senecio (Cheeke &
Pierson-Goeger, 1983). The present results
certainly suggest that different classes of pre-
dators may perceive prey in entirely different
manners.
N.bicriicis sequesters pyrrolizidine alkaloids
from Senecio spp. Thin-layer chromatography
showed pyrrolizidine alkaloids only in insects
reared on their natural host plants. The se-
questration of pyrrolizidine alkaloids for de-

fensive functions has been documented for a
grasshopper (Bernays et al., 1977), two species
of arctiid moths (Rothschild et al., 1976; Con-
ner et al., 1981), a danaid butterfly (Bernays ef
al., 1977) and the cinnabar moth (Harbourne,
1981). The pyrrolizidine alkaloids present in
the host plants of the seed bug may be
effective chemicals for insect defence for two
reasons: (1) pyrrolizidine alkaloids are bitter in
taste (McKay, 1979). and (2) they are highly
toxic (Bull et al., 1968; Mattocks, 1972). Bitter
taste could allow predators to assess the
noxious quality of the insect before it is injured
or killed. Unlike lizards, anurans have very poor
sensitivity to bitter taste from a variety of
compounds including alkaloids (Kurihara et al.,
1981). This difference in gustatory discrimina-
tion plus the fact that the toads do not chew
before swallowing as do lizards may account for
the greater palatability of N.bicrucis to toads
than lizards.
The alkaloids present in N.bicrucis differ in
RI value from those present in host plants.
These differences may reflect the conversion of
plant pyrrolizidine alkaloids to their N-oxides
(see Mattocks, 1972). This conversion in-
creases the toxicity of the alkaloids and may
render them more amenable to sequestration
in tissues such as the fat body (Blum, 1981).
The diversity of pyrrolizidine alkaloids in
N.bicriicis is less than that present in plants
(Table 3). The cinnabar moth, Tyria juco-
bueue, which feeds on Seriecio jacubaeur L. is
also selective (Alpin er a / . , 1968). There is a
tendency for insects to be selective in the
retention of non-polar compounds which are
more emetic (Blum, 1981). In general, N.bi-
criicis selectively sequesters the more non-polar
(higher Rf value) alkaloids.
Differences between plant and insect alka-
loids, at site A at least, are not the result of
sequestration of alkaloids from other plants in
other habitats. Adults just arriving at field site
A possessed n o alkaloids. The absence of
alkaloids in these individuals may reflect the
loss of alkaloids during moulting prior to
migration to site A. Loss of toxins during
moulting is observed in other insect species
(Blum, 1981) and is indicated for ff.bicrucis
since freshly moulted adults from site A con-
tained no alkaloids.
Males apparently sequester only one alka-
loid while females sequester several. The sex-
Vnpalatabili~of Neacoryphus bicrucis 297
ual difference may reflect selection on males to
sequester a large quantity of an alkaloid for
use as a pheromone in intersexual communica-
tion. Pyrrolizidine alkaloids are used as phero-
mones by some male lepidopterans (Bernays
ef al., 1977) and flea beetles (Boppre &
Scherer, 1981). In fact, the morphogenesis of
male scent organs as well as the biosynthesis of
pheromones depends on the sequestration of
dietary pyrrolizidine alkaloids in some moths
(Schneider et a[., 1982).
A great majority of the insects attacked in
palatability tests with lizards suffered no appa-
rent harm upon rejection. Other studies have
documented the general survival of distasteful
insects after predatory attempts (Sillen-
Tullberg et al., 1982; reviewed by Wiklund &
Jarvi. 1982). This is important for two reasons.
First, selection in favour of unpalatability as a
defensive strategy only occurs when some
members of the prey population survive after
being attacked (Vermeij, 1982). Second, kin
selection need not be invoked to explain the
evolution of aposematic coloration such as the
red and black markings of N.bicrucis, since
survival reduces selection against rare
aposematic forms during the initial stages of
the evolution of warning coloration (Wiklund
& Jarvi. 1982).
In summary. N. bicrucis specializes on S e w
cio spp. in a variety of habitats and sequesters
chemicals from Seneciu spp. which render it
unpalatable to certain predators.
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Accepted I4 January 1985