Res. Popul. Ecol. (1993)35, 241--250. ~) by the Society of Population Ecology
H O S T P L A N T C O N S P I C U O U S N E S S AND T H E D I S T R I B U T I O N OF EGGS AND L A R V A E IN T H E B U T T E R F L Y , A N T H O C H A R I S
SCOLYMUS ( L E P I D O P T E R A : P I E R I D A E )
Toshiya MASUMOTO,Shintaro NOMAKUCHI*and Kouji SAWADA** Laboratory of Ecology, Department of Biology, Faculty of Science, Kyushu University, 6-10-1, Hakozaki, Higashi-ku, Fukuoka 812, Japan *Department of Biology, College of Liberal Arts, Saga University, 1, Honjo, Saga 840, Japan **Ohori High School, 1-12-1, Ropponmatsu, Chuo-ku, Fukuoka 810, Japan
SUMMARY
We investigated how the distribution pattern of eggs and larval on the host plant, Turritus glabra, was influenced by the oviposition behavior of the pierid butterfly Anthocharis scolymus. Females searched for the host plants visually and they frequently approached taller host plants with sparse surrounding vegetation. After encountering host plants, oviposition behavior of females was independent of host plant characteristics such as height, density, and type of surrounding vegetation. A female laid eggs singly on a host plants. Most females appeared to lay their eggs regardless of the presense of eggs on the host plant. Consequently, egg and larva tended to be abundant on conspicuous host plants as measured by height or relative isolation from other plants. However, overcrowding of eggs on an individual host decreased the survival rate of larvae. KEYWOl~S: Anthocharis scolymus, Turritus glabra, oviposition behavior, egg distribution, host conspicuousness.
INTRODUCTION
Choice of an oviposition site should influence reproductive success of females, especially when the oviposition site is the site of larval growth. Females that lay eggs on appropriate hosts may have high offspring survival, while those that lay eggs on unsuitable hosts may cause reduced survival of their eggs or larvae. In Pieridae, as females search for the host plants visually (Courtney, 1982), conspicuousness of host plants would be influential in a decision of female oviposition. The effects of female behavior on the spatial distribution of the eggs in butterflies has been studied by many authors (e.g., Kobayashi, 1966; Stanton & Cook, 1983; Root & Kareiva, 1984) and the distribution patterns were usually reported to be
242
clumped. Host plants excessively loaded with eggs and larvae may result in severe larval competition for food, occasionally resulting in cannibalism (Courtney and Duggan, 1983).Therefore, female's decision to deposite her eggs on a particular host may also be influenced by the presence of eggs on it. Some butterflies are known to avoid hosts with eggs laid by other females (Shapiro, 1980, 1981; Wiklund and Ahrberg, 1978; Rothschild and Schoonhoven, 1977; Rausher, 1979; Shapiro, 1981). Therefore, both of host plant characteristics and egg load may affect the female oviposition behavior. In the present study, we first examine the behavioral response of ovipositing females ofAnthocharis scolymus to several characteristics of the host plant, Turritus glabra, and to the existence of eggs and larvae. Second, we clarify the distribution pattern of eggs and larvae on the host plant. Third, we analyze the effect of overcrowding and host plant characteristics on the survival of larvae. And finally, we discuss what is the most influential cause of the clumped distribution pattern of eggs and larvae of A. scolymus on the host plants T. glabra.
MATERIALS AND METHODS
The Insect and Study Site Anthocharis scolymus is a pierid butterfly which is commonly distributed in Japan. Adults of this species appear only from early April to early May. Larva feed exclusively on cruciferous plants. Females lay eggs singly on host plants, predominantly near terminal shoot or bud (Saigusa, 1984). Egg color is white immediately after oviposition, turning to orange within 3 days. Hatched larvae ofA. scolymus eat leaves and inflorescences, but they gradually become inflorescence eaters, as they grow larger. Field survey were conducted at a graveyard (area= 70 m • 40 m) located in Fukuoka, Japan from March to June of 1989 and 1990. In this study site, Turritus glabra was the only host plant A. scolymus utilized. The host plant, T. glabra, is dormant through summer to winter and sprouts a shoot late March. Their inflorescence period is from early April to early May. Host Plant, Egg and Larval Census We established a census plot (64 m • 2 m) in the middle of study site and recorded host plant phenology and the number of eggs and larvae present on all host plants. This census was made 11 times during April and June 1990. As the butterflies search for host plants by sight, oviposition behavior may be influenced by the conspicuousness of host plants. The conspicuousness may be affected by several factors including host plant height, density and surrounding vegetation. We measured these parameters as indices of the conspicuousness of each host plant, supposing that isolated and tall host plants without surrounding vegetation
243 were more conspicuous than others. As a measure of surrounding vegetation, we used a scoring method as follows. W h e n host plants were covered with other plants completely, surrounding vegetation was scored as "dense". In contrast, when host plants were not covered by any other plants, it was scored as "sparse". T h e intermediate covering was indicated as "moderate". We used multiple regression analysis for estimating the effect of height, surrounding vegetation and density of host plants on the n u m b e r of eggs and larvae on each host plant. As a measure of density of surronding host plants, the census plot was subdivided into 32 square grids (2 m • 2 m) and the n u m b e r of host plants in each square grid were used. Behavior of Adult Females We followed 16 females in the field for periods of up to 20 minutes and recorded their searching and oviposition behavior. Soon after each focal observation, we recorded characteristics of host plants that butterflies encountered, such as height, surrounding vegetation, surrounding host density within a 1 m radius, n u m b e r of eggs and larvae already present on the host.
RESULTS
Oviposition Behavior of Females We recorded a total of 189 approaches to hosts by 16 females. Sequence of oviposition behaviors, when it was resulted in egg laying, was typically as follows: approaching the host, alighting on the host, bending abdomen to the oviposition site and laying an egg (Fig. 1). From the data recorded during the observation of ovipositing females, we analyzed the females' response to the host plants characteristics. In 47 out of 142 approaches to egg-loaded hosts, females laid an egg. In 14 out of 47 approaches to host without eggs, females laid an egg. T h e height of host plants which females approached tended to be higher than the median height of surrounding conspecific plants within a 1 m radius (Table 1). After females approached host plants, they laid
189(100%)~.I_Approach~
Alighting
Bending~
Fly
Fig. 1. Sequenceof oviposition behavior in A. scolymus.
Egglaying
244 Table 1.
The effect of host plant height on the approaching behavior of females in A. scolymus.
Surrounding vegetation Sparse
Moderate or dense
No. of host plants within 1 m 2~5 6~10
Frequency of approaches to T. glabra taller than median
lower than median
33 28
12 8
Z2
8.89 10.03
11 <
18
6
5.04
Total
84
31
23.51
P
<0.01 <0.01 <0.05 < 0.001
2~5
9
7
0.06
6~10
8
4
0.75
> 0.7 >0.25
11<
11
5
1.56
>0.5
Total
28
16
2.75
> 0.1
their eggs independently of whether or not other eggs and larvae were on the host (G = 0.179, d . f . = l , p > 0 . 5 ) . M e a n height of hosts on which female butterflies deposited their eggs was 38.34 • 2.0 cm ( m e a n + S . E . ) ( N = 6 1 ) . M e a n height of host plants on which female butterflies did not deposit their eggs was 3 8 . 7 8 + 1 . 2 cm ( N = 1 2 8 ) T h e r e was no significant difference between them (t-test d.f. = 187, t = 0 . 1 9 8 , p > 0 . 5 ) . M e a n density of host plants within a l m from the plant which females approached was 7 . 7 8 • ( N = 5 9 ) when females laid their eggs, and was 6.17-/-0.55 ( N = 128) when females did not lay their eggs. T h e r e was no significant difference between them (t-test d . f . = 1 8 7 , t = 1 . 5 7 3 , 0 . 1 < p < 0 . 2 ) . W h e n females laid eggs, the surrounding vegetation density was sparse in 5 cases, moderate in 12 cases and dense in 42 cases. W h e n females did not lay egg, however, vegetation was sparse in 14 cases, moderate in 17 cases and dense in 92 cases. T h e r e was no significant difference between these frequencies (G = 1.427, d.f. = 2, p > 0.4). Distribution of Eggs and Larvae Seasonal changes in the n u m b e r of eggs and larvae in the census plot are shown in Fig. 2. T h e total n u m b e r of eggs and larvae reached a peak on 21 April 1990. Larvae disappeared until the middle of J u n e . T h e distribution of eggs and larvae on the host plants was clumped before May, but became at r a n d o m later (Table 2). T h e n u m b e r of eggs and larvae of A. scolymus on a host plant was analyzed in relation to the conspicuousness of the host. Multiple regression analysis indicated that the n u m b e r of eggs and larvae on a host increased significantly with host height, decreased with density of hosts and decreased w i t h surrounding vegetation (Table 3). Larval Survival No new eggs were found on the host plants after 27 April. We examine the survival rate of larvae on each host plant after April 27 to M a y 8 in relation to the
245
200 0 >
a~
egg
*
1st
--
2nd and 3rd
1= r(/)
01 O)
100
4) qm
0 .Q
E Z
April
May
June
Date Fig. 2.
Sesonal changes in the number of eggs and larvae of A. scolymus in the census plot.
initial number of eggs and larvae, host plant density, surrounding vegetation and plant height. The density of host plants, the surrounding vegetation and plant height did not affect the proprtion of the decrease of larvae. The survival rate of larvae on plants with high density were lower than that of larvae on host plants with low density (Table 4). Factors involved in eggs and larval mortality observed in the field were cannibalism, fighting between larvae, and predation by Mismenops tricuspidatus (spider) and Polistes chinersis (wasp).
Table 2. Seasonal changes in the distribution pattern of eggs and larva on the host plant in 1990. Plants which were dead or less than 3 cm of height were eliminated in the analysis. Coefficient of dispersion were calculated as (s.d.)2/mean no. of eggs and larvae. Date
No. of plants examined
Mean no. of eggs and larva
Coefficient of dispersion
F test
27-March
143
0
0
31-March 3-April 8-April
148 184 195
0 0.16 0.32
0 0.49 1
1.44 3.13
p < 0.01 p<0.01
13-April
201
17-April
211
0.57
1.78
5.56
p<0.01
0.75
2.02
5.44
21-April
p<0.01
216
0.97
2.03
4.25
p<0.01
27-April
206
1.03
1.84
3.29
p < 0.01
8-May
219
0.57
1.04
1.90
p<0.01
19-May 2-Jun
201 158
0.17 0.01
0.46 0.12
1.24 1.14
p<0.05 p > 0.05
S.D.
246 Table 3. The influence of the degree of plant height, density of conspecifics (per 4 m2) and condition of surrounding vegetation on the number of eggs and larvae. We use dummy variables for surrounding vegetation as follow; (zl, z2)=(1, 0) when sparse, (0, 1) when middle and (0, 0) when dense. The linear model is as follow; (the number of eggs and larvae)=~0+~l X(plant height) +/~2 x (density of conspecifics)+/53zx+/~4z2. Date
/~1 (SE)
3-April
0.022*** (0.004) 0.039*** (0.007) 0.049*** (0.009) 0.051"** (0.008) 0.057*** (0.007) 0.051"** (0.006) 0.021"** (0,003) 0.004*
8-April 13-April 17-April 21-April 27-April 8-May 19-May
(0.002) * P<0.05,
** P<0.01,
/~2 (SE)
/~3 (SE)
/~4 (SE)
0.001 0.097 0.171 (O.OO5) ( 0 . 1 1 5 ) (0.087) 0.005 0.512" 0.162 (0.008) (0.22) (0.179) 0.006 1.243"** 0.398 (0.014) (0.368) (0.3i7) --0.015 1.099"* 0.043 (0.014) (0.375) (0.323) --0.039** 0.253 0.341 (0.013) ( 0 . 3 7 3 ) (0.323) --0.045*** 0.076 0.59* (0.013) ( 0 . 3 3 3 ) (0.291) --0.015" 0.25 0.328 ( 0 . 0 0 7 ) ( 0 . 2 0 4 ) (0.188) 0.005 0.014 --0.01
(0.004)
(0. I)
R2
P
N
0.194
<0.001
172
0.152
<0.001
193
0.176
<0.001
201
0.221
<0.001
210
0.315
<0.001
216
0.329
<0.001
206
0.167
<0.001
219
0.047
>0.05
200
(0.093)
*** P<0.001
DiscussioN In this study, we focus attention to the conspicuousness of the host as an i m p o r t a n t factor to u n d e r s t a n d the distribution pattern of eggs and larvae in the field. "Conspicuousness" would be affected at least by 3 parameters: height of the individual plant, density of s u r r o u n d i n g vegetation and density of host plants.
T h e individual
host m a y be m o r e conspicuous when it is taller, the s u r r o u n d i n g vegetation was sparser and host density was lower as shown by C o u r t n e y (1982) and Ives (1978). K o b a y a s h i (1960) showed that the clumped egg distribution ofP. rapae on cabbage was affected b y the n u m b e r of eggs laid in an oviposition bout, even though visiting frequency of butterflies to each plant was at r a n d o m .
In contrast, females of A.
scolyrnus lay eggs singly on each host plant. T h e y tend to a p p r o a c h taller host plants than lower ones, especially when the s u r r o u n d i n g vegetation was sparse.
This is
probably because s u r r o u n d i n g vegetation reduced the conspicuousness of host plants to females. Local spots where m a n y host plants grew m a y have attracted m o r e females than others, however, eggs would be diluted to several hosts.
As a result, the
n u m b e r of eggs laid on each plant became small, as predicted by a stochastic model (Jones, 1977). After females approached host plants, they deposited their eggs independently of the plant characteristics. These indicate that the conspicuous hosts frequently receive the female's visits resulting in frequent ovipositions by m a n y females. T h u s the
247
e-.,
o
v
II
248 clumped distribution patterns of eggs and larvae on host plants was suggested to be caused by the host plant characteristics in relation to conspicuousness. Analyzing larval disappearance rate from 27 April to 8 M a y , we found that it was not influenced by any of host plant characters such as plant height, surrounding vegetation or host plant density. host plant.
O n l y i m p o r t a n t factor was the larval density on each
Although we could not quantify the mortality factors, intraspecific fights
a m o n g larvae and/or cannibalism were observed frequently, suggesting to be an i m o r p t a n t cause of the reduced survival at high density, like related species Anthocharis
cardamines (Courtney, 1981; C o u r t n e y and D u g g a n , 1983).
Therefore, it appears to be advantageous for females to assess egg load on the host plant which they approached for oviposition. Several studies have reported that butterflies, whose larvae eat inflorescence or small hosts, show an egg-load assessment (Anthocharis sara by Shapiro 1980, Anthocharis cardamines by Wildund and A h r b e r g 1978, and Battus philenor by R a u s h e r 1979). In these species, females tended to avoid oviposition on host plants with conspecific eggs. In A. scolymus, however, we could not detect a n y effect of egg load assessment on the spatial distribution of eggs despite that the larvae are inflorescent eaters.
Minkenberg
et al (1992) suggested that the decision m a k i n g by females whether to oviposit or not on each host plant should be influenced not only by the egg load assessment but also by the n u m b e r of m a t u r e eggs that females held.
T h e y hypothsized that females with a
large n u m b e r of eggs should maximize the host plant encounter rate, while females with smaller n u m b e r of eggs should maximize the larval survival.
A s s u m i n g that
younger A. scolymus females oviposit in higher rate than older ones, like other Pieridae butterflies (ex, Suzuki, 1978, K i m u r a and T s u b a k i 1986), most of eggs might be laid by y o u n g females regardless of egg load on conspicuous host plants.
In fact,
N o m a k u c h i et al. (unpublished) observed that older females tended to avoid oviposition on hosts loaded with eggs, while y o u n g females are not so discriminate as old ones in the same population. It should be solved in future how a female change o v i p o s i t i o n behavior from non-discriminative to discriminative in her life both in theoretically and emprically. ACKNOWLEDGMENTS; We thank Y. Ono and M. Murai for giving advice and encouragement. We are indebted to R. C. Titus for reading the manuscript and making many helpful suggestions. Thanks are also due to N. Suzuki, N. Takebayashi, L. Riggs and T. Sunahara for assistance in improving the manuscript. This paper owes much to the helpful comments of members of the Laboratory of Ecology, Department of Biology, Faculty of Science, Kyushu University. This study was partly supported by a Japan Ministry of Education Science and Culture Grant-in-Aid for Scientific Research on Priority Area (#319), Project "Symbiotic Biosphere: An Ecological Interaction Network Promoting the Coexistence of Many Species".
249
REFERENCES
Courtney, S. P. (1981)
Coevolution of pierid butterflies and their cruciferous foodplants III Anthocharis
cardamines (L.) Survival, development and oviposition on different hostplants Oecologia 51: 91-96. Courtney, S. P. (1982)
Coevolution of pierid butterflies and their cruciferous foodplants IV. Crucifer
apparency and Anthocharis cardamines (L.) Oviposition.
Oecologia52: 258-265.
Courtney, S. P. and A. E. Duggan (1983) The population biology of the orange tip butterfly Anthocharis cardamines in Britain. Ecol. Entomol. 8: 271-281. Ives, P. M. (1978)
How discriminating are cabbage butterflies? Aust. J. Ecol. 3: 261-276.
Jones, R. E. (1977)
Movement patterns and egg distribution in cabbage butterflies. J. Anim. Ecol. 46:
195-212. Kimura, K. and Y. Tsubaki (1986)
Oviposition schedule of the small white butterfly, Pieris melete
M~n~tris (Lepidoptara: Pieridae). Appl. Ent. Zool. 21: 28-32. Kobayashi, S. (1960)
Studies on the distribution pattern of the eggs of the common cabbage butterfly,
Pieris rapae cruciovora in a cabbage farm and the factors affecting its concintraring trend. Jap. J. Ecol. 10: 154-160. (in Japanease with English summary) Kobayashi, S. (1966)
Process generating the distribution pattern of the eggs of the common cabbage
butterfly Pieris rapae crucivora. Res. Popul. Ecol. 7: 109-117. Minkenberg, O. P . J . M . ,
M. Tatar and J. A. Rossenheim (1992)
variability in insect foraging and oviposition behavior. Rausher, M. D. (1979)
Egg recognition: its advantage to a butterfly. Anim. Behav. 27: 1034-1040.
Root, R. B. and P. M. Kareiva (1984) ecological consequences and environment. Saigusa, T. (1984)
Egg load as a major source of
OIKOS 65: 134-142.
The search for resources by cabbage butterflies (Pieris rapae):
adaptive significance of marcovian movements in a patchy
Ecology 65: 147-165. Oviposited position on a foodplant, Rorippa indica (L.), in Anthocharis scolymus
(BUTLER) (Pieridae, Pierinae). Shapiro, A. M. (1980)
Tyo to Ga. 35: 91-92. (in Japanese)
Egg-load assessment and carryover diapause in Anthocharis (Pieridae). J. of the
Lepidopterists ' Society 34:307-315. Shapiro, A. M. (1981)
The pierid red-egg syndrome. Am. Nat. 117: 276-294.
Stanton, M. L. and R. E. Cook (1983) of Colias butterflies. Suzuki, Y. (1978)
Source of intraspecific variation in the hostplant seeking behavior
Oecologia. 60: 365-370.
Adult longevity and reproductive potential of the small cabbage white, Pieris rapae
crucivora Boisduval (Lepidoptara: Pieridae). App. Ent. Zool. 13: 312-313. Wiklund, C. and C. Ahrberg (1978) Host plants nectar source plants, and habitat selection of males and females ofAnthocharis cardamines (Lepidoptera).
OIKOS 31: 169-183.
250
r ~ Turritus glabra J = 9
f,:.
~ ~,tJ!~9
~ ~ -- "./7~t g" 9 Z 5 ? g . ~ , ~
5 U~"C~ , 70 9
l{~.
