［鹿大農学術報告第 68 号, p1–7, 2018］

Do granivorous insects invade fallen acorns of Pasania edulis (Makino) Makino
through exit holes of curculio weevil larvae?

Sone Koichi 1) , Oishi Keita 2) , Hata Kunihiko 1)
1)
2)

Laboratory of Forest Protection, Kagoshima University

The United Graduate School of Agricultural Sciences, Kagoshima University.

Accepted October 1, 2017
Introduction

Pasania edulis (Fagacea) is a dominant tree species in many evergreen broad-leaved forests in southern
Japan and produces many acorns every autumn. However, the establishment of its seedlings is hindered by arange of mortality factors [7, 10]. The curculio weevil, likely Curculio hilgendorfi, is an important mortality
factor that negatively impacts germination and seedling establishment depending on the degree and theposition of cotyledonary damage [9], as reported for other acorn-producing tree species [e.g., 1–6, 8, 11].
In late autumn, the larvae of curculio weevils, having grown in the P. edulis acorn, leave the fallen acorn
through an exit hole they make and overwinter in the ground. These fallen acorns are then exposed to othermortality factors, such as the acorn borer (Coccotrypes graniceps), Tipulidae sp., the Nitidulid beetle(Stelidota multiguttata), and the Bell moth (Cryptaspasma trigonata) [7, 10, 12]. The acorn borer attacks theacorns through a crack at the top of the acorn from which a root or shoot protrudes or makes its own entrance
hole, while the Bell moth uses the exit holes of the weevil larvae or a crack made during germination or byother factors [12]. The exit holes left by the curculio weevil larvae may be by these granivorous insects during
their invasion or may facilitate predation by decomposers such as mites, springtails, and fungi. This may
further lower the germination ratio and seedling establishment.
In 2015, we conducted a field experiment in an evergreen broad-leaved forest in southern Kyushu andexamined whether other granivorous insects and decomposers enter the acorns through the exit holes of
curculio weevil larvae. In April, we buried acorns without any holes (S-acorns), acorns with a hole bored into
them with the same diameter as the exit holes of curculio weevil larvae (H-acorns), and acorns with exit holes
from curculio weevil larvae (W-acorns). In November (the end of the first growing season), we compared thegermination ratio, the condition of cotyledons, and the degree of invasion by the acorn borer and the Bell mothamong the three categories of acorns. We then discussed whether or not the exit holes of the curculio weevil
larvae on P. edulis acorns were subsequently used by other granivorous insects and decomposers.

Sone, Oishi and Hata2Methods

The field study was conducted in an evergreen broad-leaved forest of the Takakuma Experimental Forest ofKagoshima University (TEFKU) (31º31′N, 130º46′E, and 550 m in altitude) in Kagoshima Prefecture,southern Japan. The annual mean temperature and precipitation of this area during the last decade were
14.3 °C and 3,460 mm, respectively. The crown layer of the forest was closed, and P. edulis was the mostdominant species of tree, occupying about 50% of the canopy. Other dominant tree species were Castanopsis
cuspidata, Machilus thunbergii, Neolitsea sericea, Distylium racemosum, Quercus acuta, and Q. salicina. The
understory vegetation was composed of Cleyera japonica, Symplocos lucida, Camellia japonica, and Illicium
anisatum. On the floor, vegetation was poor, and 3–5 cm thick leaf litter had accumulated uniformly throughthe forest.
In October and November 2014, we collected fallen P. edulis acorns, wrapped them in wet paper towels andstored them in a refrigerator (5 °C, dark conditions). In April 2015, we classified these acorns into W-acorns
and S-acorns. We made H-acorns by drilling a hole 2 mm in diameter and 5 mm long in the area about 1/3 fromthe bottom of half of the S-acorns.
On April 9, 2015, we put the 100 S-, W-, and H-acorns in 30×30×10 cm cages,and buried them about 5 cm

deep in the soil in TEKFU’s evergreen, broad-leaved forest. These cages were made of 4 mm wire mesh toprevent the buried acorns from being pilfered by granivorous Apodemus mice and predation by large or
medium-sized omnivorous mammals such as the wild boar (Sus scorofa leucomystax), the badger (Meles melesanakuma), and the raccoon dog (Nyctereutes procyonoides viverrinus). We buried one cage each of S- andW-acorns and two cages of H-acorns at intervals of 3–10 m; a total of 100 S-, 100 W-, and 200 H-acorns wereburied. Sone et al. [10] and Nakamura et al. [7] reported that the acorn borer attacked the germinated P. edulis
acorns in the soil, and attacked acorns were observed here and there in the forest, suggesting that the acorn
borer uniformly inhabited the forest and the probability of the buried acorns being attacked by the acorn borer
did not differ with the cages.
On November 2, 2015, we collected the buried acorns and examined them for appearance, the emergence ofshoots and roots, cracks at the top of the acorn, and cracks at parts other than the top (nutshell cracks). In thisstudy, acorns with an emerged root or shoot and root and those with a crack at the top were regarded as
germinated acorns. We dissected each acorn and examined the degree of invasion by the acorn borer or theBell moth and the condition of the cotyledons. The condition of the cotyledons was recorded as being sound,rotten/deteriorated, or absent (acorns were empty because the cotyledons were completely consumed), and anyother alterations were also noted. The cotyledons of some H-acorns had deteriorated around the artificial holeor were rotten in limited sections along the artificial hole. We recorded the condition of these cotyledons assound.

Weevil’s exit holes and acorn borer attack

3Data analysis

We compared the percentages of ungerminated acorns with sound cotyledons in the three categories ofacorns using Fisher’s exact probability test. We conducted Bonferroni’s correction to examine the significanceof the difference between the values of each pair of acorn categories.

Results

In October, we collected a total of 99 S-, 98 W-, and 200 H-acorns and examined their conditions (Table 1).
Of the S-acorns, 34.3% had an emerged root or root and shoot and 10.1% had a crack at the top. Of theW-acorns, 6.1% had an emerged root or root and shoot and 3.1% had a crack at the top. Of the H-acorns,
31.5% had an emerged root or root and shoot and 29.0% had a crack at the top. In addition, the nutshell of6.5% of the H-acorns was cracked vertically (nutshell crack).

Table 1 The percentage of acorns in various conditions
ConditionS-acorns W-acorns
Cracked at the top*
10.1
3.1
Emerged root*
13.1
1.0
Emerged root and shoot*
21.2
5.1
Cracked other than at the top
Unchanged in apperarence**
55.6
90.8
* regarded as germinated** regarded as ungerminatedH-acorns
29.0
8.0
23.5
6.5
33.0

Attacks by the acorn borer were confirmed in 34 (25 germinated and nine ungerminated) S-acorns and 18(13 germinated and 5 ungerminated) H-acorns. The acorn borer had bored into all 25 germinated S-acorns and11 of the 13 H-acorns through a top crack. The acorn borer made its own entrance hole in two H-acorns. Theacorn borer made an entrance hole on five of the nine ungerminated S-acorns and two of the five ungerminatedH-acorns. The acorn borer did not use the artificial holes to enter the acorns (Table 2).

Table 2 the number of S- and H-acorns attacked by the acorn borer throughdifferent sites
Entrance site
S-acorns
H-acorns
Germinated UngerminatedGerminated UngerminatedCrack at the top
250110
Entrance hole made0522by the borer
Artificial hole0000
Others/unknown
0403

Sone, Oishi and Hata

4The Bell moth attacked only the H-acorns (five germinated and five ungerminated acorns). The larvae
entered through the crack at the top of four of the germinated H-acorns and the artificial hole of the othergerminated H-acorn. The larvae entered one of the ungerminated H-acorns through the artificial hole andthrough an undetected path in the other four ungerminated H-acorns (Table 3).

Table 3 The number of H-acorns attacked by
the Bell moth through different sites
Entrance site
Crack at the top
Artificial hole
Others/unknown

Germinated Ungerminated401
104Cotyledons in the acorns attacked by the acorn borer and the Bell moth were completely rotten or absent.
The cotyledons of 21.7% of the ungerminated S-acorns were completely rotten and 78.3% were sound.
Cotyledons were completely rotten and/or absent in 97.8% of the ungerminated W-acorns and only 2.2% weresound. The cotyledon deterioration present in some of the H-acorns had progressed around the artificial hole.
The cotyledons were completely rotten and/or absent in 58.9% of the ungerminated acorns and were sound in
41.1%. The percentage of ungerminated acorns with sound cotyledons varied significantly according to thecategory of the acorns, and the difference in the percentage of ungerminated acorns with sound cotyledons wassignificant for any combination of acorn categories (in all cases, Fisher’s exact probability P < 0.01).

Discussion

Curculio weevil attacks have detrimental effects on the seedling establishment of acorn-producing treespecies [3, 5, 6, 9]. In this study, 44.4%, 9.2%, and 60.5% of the S-, W- and H-acorns were regarded as
germinated and 21.2%, 5.1%, and 23.5%, had emerged shoots and roots, respectively. These results indicate
that, as reported by Sone et al. [9], curculio weevil attacks greatly suppress the seedling establishment of P.
edulis while the artificial holes did not.
After the acorns drop to the ground, insects attack the acorns before and after germination [1, 2, 4–8, 10–12].
Four species of insects have been reported to attack the acorns of P. edulis: the acorn borer, the Tipulidae sp.,the Nitidulid beetle, and the Bell moth [12, 13]. The acorn borer uses the crack at the top of germinated acorns
or makes an entrance hole and the Bell moth larvae attacks through a crack made during germination on thenutshell or a hole made by other insects [12].
In this study, the acorn borer attacked S- and H-acorns and the Bell moth larvae attacked only the H-acorns.
The cotyledons in the acorns attacked by these two insects were completely consumed or absent. These results
suggest that the attacks of these insects have devastating effects on seedling establishment, which is consistentWeevil’s exit holes and acorn borer attack

5with the report by Sone et al. [10] and Nakamura et al. [7] that suggests the attack by the acorn borer is amortality factor.
The acorn borer attacked both germinated and ungerminated acorns. This insect used the crack at the top or
made an entrance hole for its entry, but it did not use the exit holes of the weevil larvae or artificial holes, as
has been reported by Ueda et al. [12]. The Bell moth larvae entered some H-acorns through the artificial holes.
This suggests that although we did not verify the entry of the Bell moth larvae through the exit holes of theweevil larvae, this possibility may remain. However, the ratio of acorns attacked by the Bell moth was very
low in this study. Therefore, in the forest, the exit holes of the curculio weevil larvae may be used for invasion
only by a few granivorous insects on the ground.
The percentage of ungerminated acorns with sound cotyledons was significantly higher in S-acorns than ineither W- or H-acorns. The deterioration of the cotyledons of H-acorns progressed around the artificial hole.
These results show that the fungal and arthropod decomposers invaded the acorns through the exit holes ofweevil larvae. In conclusion, the exit holes of the weevil larvae are not necessarily used by granivorous insects
to invade the acorn on the ground, but may facilitate the deterioration of cotyledons due to the invasion offungal and arthropod decomposers, resulting in the inhibition of germination and seedling establishment.

Acknowledgement

This study was financially supported by a Grant-in-Aid for Scientific Research (No.25660119).

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Weevil’s exit holes and acorn borer attack

7Do granivorous insects invade fallen acorns of Pasania edulis (Makino)through exit holes of curculio weevil larvae?

Sone Koichi 1) † , Oishi Keita 2) and Hata Kunihiko1)
1)
2)

Laboratory of Forest Protection, Kagoshima University

The United Graduate School of Agricultural Sciences, Kagoshima University

Summary

Pasania edulis (Fagacea) is a dominant tree species in evergreen broad-leaved forests in southern Japan.
Predation by insects is harmful to seedling establishment. The larvae of the acorn weevil, likely Curculio
hilgendorfi, feed on the acorns of P. edulis and exit the fallen acorns to overwinter in the ground. The fallenacorns are then invaded by other granivorous insects. To examine whether the exit holes of the weevil larvae
are used for invasion by other insects, we buried the acorns in the ground in April 2015 and compared thegermination ratio, the condition of the cotyledons, and the invasion of the acorn borer, Coccotrypes graniceps,
and the Bell moth, Cryptaspasma trigonata, in acorns in November 2015. The germination ratio wassignificantly higher in acorns without holes (S-acorns) and acorns with artificial holes mimicking the exit holeof weevil larvae (H-acorns) than for acorns with an exit hole (W-acorns). The acorn borer did invade S- andH-acorns, but not through the exit holes or the artificial holes. The Bell moth attacked some H-acorns throughthe artificial holes. The percentage of ungerminated acorns with intact cotyledons was significantly higher inS-acorns than in H- or W-acorns. These results show that the exit holes of the curculio weevil larvae may
contribute only slightly to invasion by other granivorous insects, but may significantly facilitate the invasionof fungal and arthropod decomposers into the fallen acorns.

Key words: Curculio weevil-attacked acorns, Exit holes, Pasania edulis acorns, The acorn borer, The Bell
moth†

: Correspondence to：Koichi Sone (Laboratory of Forest Protection Laboratory, Department of Environmental
Sciences and Technology, Faculty of Agriculture, Kagoshima University）
Phone：099-285-8580, E-mail：sonesun@agri.kagoshima-u.ac.jp