Sans, Antònia

Traveset, Anna

Biblioteca Digital de les Illes Balears

Insect frugivory in 
Juniperus phoenicea (L.) 
(Cupressaceae) in Cabrera island 
(Balearic Archipelago) 
Anna TRAVESET and Antonia SANS 
SHNB 
@ 
SOCIETAT D'HISTORIA 
NATURAL DE LES 8ALEARS 
Traveset, A. and Sans A. 1994. Insect Irugivory in Juniperus phoenicea (L.) 
(Cupressaceae) in Cabrera island (Balearic Archipelago). BolI. Soco Hist. Nat. 
Ba/ears, 37: 143-150 ISSN 0212-260X. Palma de Mallorca. 
In the present paper, the variation among individuals 01 ,luniperus phoenicea in the 
inciden ce 01 Irugivorous insects is examined in Cabrera island during 1992 and 
1993. The proportion 01 seeds that are damaged is determined, and whether the 
number 01 eones (structures equivalent to the Ileshy Iruits 01 the angiosperms) 
inlested by insects is associated with con e size (diameter) is also examined. A 
great variability in the proportion 01 "Iruits" that are infested is found, representing 
from 3% to 50% of the crap. The larva 01 the frugivoraus insect (a 
micralepidopteran of the family Gelechiidae not yet identified) feeds upon the pulp 
of the fruit and only rarely «3% 01 the cases) damages the seeds. Cone diameter 
does not have any influence on the intensity 01 attack. Larger Iruits do not 
necessarily have more seeds and are not more infested than small Iruits. In 1993, 
Iruit infestation was greater than in 1992 possibly because eones take about two 
years to mature and, thus, those collected in 1993 had been exposed to moth 
infestation lor a longer periodo 
Keywords: Juniperus phoenicea, Cupressaceae, frugivorous insects, Ge/echiidae, 
reproductive /osses, Cabrera, Ba/earic /s/ands. 
FRUGIVORIA D'INSECTES EN JUN/PERUS PHOEN/CEA (L.) (CUPRESSACEAE) 
A L'ILLA DE CABRERA (ARXIPELAG BALEAR). En el present treball s'examina 
la variació entre individus de savina (Juniperus phoenicea) en la incidencia 
d'insectes frugívors (que mengen la polpa i/o lIavors deis fruits) a I'illa de Cabrera 
durant els anys 1992 i 1993. Es determina quina proporció de lIavors són 
atacades, i també es vol coneixer si el nombre de galbuls (estructures equivalents 
als fruits de les angiospermes) atacats pels insectes esta associat amb lIur mida 
(diametre del galbuls). Es troba que hi ha una gran variabilitat en la proporció de 
"fruits" atacats, representant d'un 3% a un 50% de la collita. La larva de I'insecte 
,depredador (unmicrolepidópter de la fam ília 'Gelechiidae que encara no ha pogut 
ésser identificat) menja la palpa que envolta les lIavors, i 5015 en rares ocasions 
(en <3% deis casos) es menja també aquestes. El diametre deis galbuls sembla 
no tenir cap electe sobre la intensitat d'atac. Fruits més grans no ten en 
necessariament més lIavors i tampoc esta n més o menys atacats que fruits petits. 
144 Bo/l. SOCo Hist. Nat. Balears, 37 (1994) 
En 1993, el percentatge d 'atac per insectes jou més elevat que en 1992 
possiblement degut a que els galbuls esta n gairebé dos anys a madurar, i per 
tant, els del 1993 varen estar més temps exposats a I'atac de la falena sobre 
I'arbre. 
Paraules clau: Juniperus phoenicea, Cupressaceae, frugivoria per insectes, 
Gelechiidae, perdues reproductives, Cabrera, lIIes Balears 
Anna TRAVESET and Antonia SANSo Institut d'Estudis Avanc;:ats de les l/les 
Balears, CSIC, Crtra. de Val/demossa, km 7'5, 07071-Palma de Mal/orca. 
Recepció del manuscrit, 27-jun-94. Revisió acceptada, 6-oct-94 
Introduction 
I nsects are potential destroyers of 
large quantities of reproductive struc-
tures in many species of plants (see 
reviews in Crawley, 1989; 1992), and 
have the capacity of limiting plant 
recruitment (Louda, 1982a,b). The in-
sects that feed upon the fruits (either 
on the pulp or the seeds), in particular, 
have received attention for a long time 
and .in different kinds of ecosystems 
(e.g. Janzen 1971, Breedlove .& Ehrlich, 
1972. De Bteven, 1981; Auld, 1986; 
Andersen, 1989; Evans et al., 1989). 
RegardJess ot, orin addition to, 
their demographic efteet on plant 
populatiori dynamics, irisects may al50 
act as selective factors if they diserimi-
nate between plan! phenotypes and 
promote individual variation in r,ep(oduc-
tive losses (Harper, 1977). A particular 
plant attrjbute sueh as fruit erop size 
(e.g. Jordano, 1987; Traveset, 1994), 
numoer of seeds per fruit (e.g., Garfi-
son & Augspurger, 1983; Herr.era, 
1984),or fruif ¡¡¡ize .(e.g., Haré, 1980} 
m.ay be selectéd due 10 the pressure 
exert~d by insects that interact with it 
(fn,lgivorous Jnsects, in this case). 
¡:;ven ~ho\,Jgh junipers ¡;Ire widely 
distributed and are abundant in many 
h.a.bitats, the¡r interactiori with insects 
has been hardly examined. As far as 
we know, there are only two studies 
that examine the effect of insects on 
the reproductive suecess of this group 
of plants (Roques et al. 1984; Fernan-
des and Whitham, 1989). 
In the present paper, we exami-
ne such effect in Juniperus phoenicea 
(L.), a species of juniper commonly 
found in the Balearic Islands. Our 
objectives were the following: 
1) to document the variation among 
individual plants in the incidence of 
insects in the fruits, 
2) to evaluate what proportion of 
seeds are damaged by ¡nseet larvae, 
3) to determine whether fruit infes-
tation is associated with fruit size, and 
4) to know whether the intensity of 
fruit damage by inseetsinereases 
signifieantly from cne year to the next 
sine€! maturing fruits are on the plants 
forabout two years. 
Study site 
The $tuóy wascarried out in the 
island of Cabrera, soutM of Mallorca 
(Balearie lslands), during the autumn of 
1992 and199$. Cabrera island js about 
1130 ha and has a maximum elevation 
of 172 m., The vegetation is mediterra-
neaf) serubland, domiriated by pjstaoia. 
A. Traveset & A. Sans, Inseet frugivory in Juniperus phoenicea in Cabrera 145 
lentiscus, Phillyrea spp., Olea europa ea, 
Juniperus phoenieea, Cistus spp., Ros-
marinus offieinalis and Eriea multiflora. 
Pinus halepensis is very abundant at 
the northeast of the island (see Rita i 
Bibiloni, 1993, for more information on 
the vegetation of the area). 
Mean temperature ranges from 8ºC 
(in January) to 34ºC (in August). Total 
annual precipitation averages 380 mm 
(calculated for the period 1950-1971), 
ranging from 193 to 555 mm. Most 
(43.8%) of such rain falls between 
September and November. A detailed 
description of the climate of Cabrera 
island and surrounding islets can be 
found in Guijarro (1993). 
Study organisms 
Juniperus phoenieea (L.) (Cu-
pressaceae) is a monoecious (functio-
nally subdioecious in most populations, 
according to Jordano, 1991) shrub/small 
tree that can reach up to 8 m in height. 
It is distributed all around the 
Mediterranean Basin, reaching also the 
Canary Islands, and is abundantly found 
in the Balearics (Bonafé, 1979). 
Following the taxonomic nomenclature 
used by Palau (1976), the species most 
commonly found in the island of Cabre-
ra, and the one studied here, is J. 
phoenicea varo turbinata (Guss.) Parl. 
The female strobili (fleshy eones or 
"fruits" or "berries", hereafter) are 
functionally analogous to angiosperm 
fleshy fruits. The strobili are dark-red 
when ripe and measure 8-14 mm in 
diameter; they reach full size about a 
year after pollination, and mature during 
the following year (Roques et al. 1984). 
Important seed dispersers of jUnipers 
are birds of the genus Turdus (see 
Jordano, 1993), although carnivores 
might also act as major dispersers in 
some regions. In the island of Cabrera, 
although Turdus appear to be the main 
fruit consumers of this plant (Traveset, 
pers.obs.), the fruits are also eaten by 
genets (Genetta genetta) and by an 
endemic lizard, Podareis lilfordi 
(Lacertidae), which pass the seeds 
intact through their intestines (Traveset, 
1993). 
The berries are attacked by 
different species of insects which 
oviposit on them at different times of 
cone development, and have different 
life cycles. Roques et al. (1984) found 
four species of lepidopterans, one 
coleopteran and one himenopteran 
infesting the fruits in France and in 
Corsica Island. In the island of Cabrera, 
we have found only one species of 
microlepidopteran that belongs to the 
family Gelechiidae (but is not yet 
identified) the larva of which appears to 
infest the fruit during the first year of 
cone development, remaining inside it 
until the following one. AII insect exit 
holes appear on the berries collected in 
1993. In only one ocassion we found 
an exit hole in 1992 which suggests 
that there might be another species of 
insect, with a different life cycle, 
attacking the fruits of this plant. 
Methods 
On September 19, 1992, a total 
of 30 fruits were randomly collected 
from each of 10 haphazardly chosen 
individuals scattered in Cabrera island. 
The eones were placed in paper bags 
and taken to the laboratory to be 
dissected. For each dissected fruit, we 
146 BolI. SOCo Hist. Nat. Balears, 37 (1994) 
recorded: (1) fruit diameter, (2) the 
number of seeds in it, (3) whether it 
was infested by larvae and (4) how 
many seeds had been damaged. 
On September 24 of 1993, we 
collected 50 fruits from each of other 
10 individuals chosen haphazardly from 
the areas where we had collected in 
1992. We could not use the same indi-
vidual plants because most of the labels 
placed were damaged by sheep that 
graze freely in the island. The variables 
recorded for each dissected fruit were 
the same as in 1992, except for fruit 
diameter. 
The data were analyzed performing 
an analysis of variance, using the 
proportion of fruits damaged per plant 
as the dependent variable and plant as 
the main effect. The proportions were 
normalized using the angular 
transformation before the analysis. Also, 
a correlation analysis was executed in 
order to find associations between fruit 
size, number of seeds and fruit 
i nfestation. 
Results 
Table 1 shows the incidence of 
insect larvae in the fruits of J. 
phoenicea. There was a great variation 
among plants, the proportion of eones 
infested ranging from 3.3% to 50%. In 
1993, the proportion of fruits attacked 
was significantly greater than in 1992 
(F1.18=8A6, P<0.01) and also varied 
from 3.3% to 48%. 
The moth larvae were observed to 
feed upon the pulp of the fruit, and only 
occasionally (2.75 % of the cases) had 
damaged the seeds (usually only one 
seed per cone). Fruit infestation was 
not associated with fruit diameter in 
1992 (Figure 1). The number of seeds 
per fruit did not appear to be correlated 
with fruit diameter either (r=0.02, 
P»0.05, n=300). This implies that even 
if fruit infestation was related to fruit 
size and larvae were preying upon the 
seeds, they would not be killing more 
seeds when infesting larger fruits. Fruit 
diameter differed significantly among 
plants (F9290=32.9, P=0.0001), being on 
average 10A ± 6A mm and ranging 
from 9.2 to 11.6 mm. The mean 
number of seeds per fruit was 6A ± 1.0 
(s.d.) and also differed significantly 
among plants (F9,290=27.3, P=0.0001, in 
1992, and F 9.489=32.6, P=0.0001 in 
1993). 
Discussion 
A broad inter-individual variation in 
fruit infestation by moths was observed 
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FRUIT DIAMETER (mm) 
Fig. 1. Relation between fruit size and 
number of fruits damaged by insects, N=10 
plants. Data from 1992. 
Fig. 1. Relació entre mida del fruit i nombre 
de fruits danyats per I'insecte. N=10 plantes. 
Dades del 1992. 
A. Traveset & A. Sans, Insect frugivory in Juniperus phoenicea in Cabrera 147 
in J. phoenicea, representing from 3% 
to 50% of the crop. A great variance in 
the levels of attack (6.7% - 83.9%) was 
also reported by Roques et al. (1984) 
from some French populations. Either 
factors intrinsic to the plant (plant size, 
fecundity, etc.) or extrinsic to it (position 
of the individual in the habitat, etc.) 
may be responsible for such variance, 
as it has been found in other species 
(e.g., Roitberg & Prokopy, 1982; 
Courtney & Manzur, 1985; Jordano, 
1987; Traveset, 1994). In the present 
system, fruit size did not appear to be 
associated with the number of infested 
eones, and thus, it is an intrinsic factor 
that does not influence insect attack. 
This is possibly because the adult moth 
begins ovipositing when the eones are 
still developing (at least most of them 
are). so it has no much opportunity to 
choose among fruit sizes. 
As also reported by Roques et al. 
(1984), the number of seeds damaged 
by insect larvae is very low. These 
authors found that only two of the five 
species of insect frugivores of J. 
phoenicea had a direct influence 
reducing the number of viable seeds. In 
the present study, we observed that the 
larvae feed upon the soft, fibrous pulp, 
and only rarely (in <3% of the infested 
fruits) damage the seeds, which 
probably have a too hard seed coat for 
them. 
The number of attacked fruits was 
greater in 1993 than in 1992. This 
suggests that the moth keeps 
ovipositing even when fruits have begun 
maturing. However, the possibility exists 
that some larvae present in the eones 
dissected in 1992 were still too small to 
be detected and thus were missed 
when recording fruit infestation. 
Even though insects did not seem 
to represent a great loss in the 
reproductive success of J. phoenicea 
because of the low proportion of seeds 
damaged, they may be more important 
reducing the potential number of viable 
seeds dispersed since fruits that have 
been damaged and bear exit holes rot 
soon and are not attractive to birds 
(Traveset, pers. obs.). Such fruits 
usually remain on the branches for a 
long time without ever being dispersed. 
Year Fruits dissected 
per plant 
Plants % Fruits infested 
X ± S.O. C.V. 
1992 30 10 13.3 ± 14.1 106.0 
1993 50 10 29.2 ± 13.1 44.9 
Table 1. Infestation by moths of J. phoenícea fruits in Cabrera island during the two years 
of the study. (C.V.: coefficient of variation). 
Taula 1. Atac deIs fruíts de J. phoenicea pel mícrolepídopter a l'íl/a de Cabrera durant els 
dos anys d'estudí. (C. V.: coefícíent de varíacíó). 
148 BolI. 50c. Hist. Nat. Ba/ears, 37 (1994) 
Acknowledgements 
We are grateful to ICONA, and 
especially to the people working at Parc 
Nacional de Cabrera, for their logistic 
support and kind attendance in the 
island. We also want to thank Jaime 
Bartolomé for his help dissecting fruits 
in 1992. This paper is framed within 
project PB91-0055 financed by oGICYT. 
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Insect frugivory in Juniperus phoeniceae (L.) (Cupressaceae) in Cabrera Island (Balearic Archipelago)

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