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Portrait of an Insect: Marchalina hellenica Genn. (Sternorrhyncha: Coccina: Margarodidae), important Honeydew Producer in Greece
Apiacta
36, 131-137, 2001
Friederike Erlinghagen
Wilhelm-Raabe-Weg 6, D-30938 Burgwedel, Germany
Email: f.erlinghagen@gmx.de
Abstract
There are described and discussed some morphologic characteristics of the male
and female development stages of Marchalina hellenica Genn. From the morphologic
point of view, there could be differentiated a stage before the oviposition by
the adults. The growing number of rhinaries and the metamorphose of the buccal
apparatus of the mature foundresses coincide with the beginning of the
migration, and the phase of the oviposition. It is possible to suppose
Marchalina hellenica Genn. can be visited by all kinds of ants, that
trophobiotically use all insects that suck the sap of trees.
Keywords Margarodidae, Marchalina
hellenica, honeydew producer, Greece
Introduction
The basis of the forest honey is represented by the honeydew, a secretion with a
high content of sugar, supplied by insects that suck the sap, and excrete the
excess of sugar from their food. The investigations about the insects that are
producing honeydew in Greece were effected above all by Santas (1983). From 1977
to 1981 he realized investigations in all the country. During these, the trees
visited by bees (that is, Pinus spp. and Abies spp.) were examined about the
presence of the sap sucking insects. Santas (1983) supposed that 5 species were
more important to produce forest honey, at the same time mentioning that,
according to the actual level of knowledge, there cannot be made more exact
estimations of the honeydew producers in Greece , on the basis of honey bees.
Marchalina hellenica is mentioned as the most important honeydew producing
insect, from which seems to originate all the pine honey in Greece . This
species is spread all over the eastern area of the Mediterranean Sea . The host
plants are pines: first of all, Pinus halepensis Mill., and, to a smaller
extent, Pinus pinea L., Pinus sylvestris L., and Pinus brutia Ten. Nikolopoulos
(1965) and Santas (1979) wrote about the biology and morphology of Marchalina
hellenica. In the said investigations, the morphologic description was achieved
by means of a stereomagnifying glass. Besides, there are no measurable and clear
values for the male and female stages.
Investigation
area
The Aleppo pine forest lays in the dune region of the western coast of
Peloponnese (southern Greece ), namely in Zacharo, 25 km south of Pirgos.
According to the climatic-geographic criteria, Peloponnese belongs to the
Mediterranean subtropical area, and the west coast – to the vegetation area of
the Mediterranean evergreen deciduous forests, with an evergreen oak subzone
(communion Quercion ilicis). In this area, the Aleppo pine (Pinus halepensis) is
a frequently encountered tree, that prefers the climate of the coastal areas.
Through afforestations, there was obtained a notable extension of the areas
occupied by the same. Thanks to the greater precipitations in the north-western
area of Peloponnese (800-1000 mm of yearly precipitations, as compared to only
600 mm in the north-eastern Peloponnese ), the sandy earth is more richer in
water, so there could also exist a richer herb vegetation.
Material
and method
The area was investigated in February-April, and September-November, 1992.
According to Santas (1983), the honeydew production begins in June, and ends in
the following spring. Honeybees are collecting honeydew only during the period
from August to October, and also, in smaller quantities, in March and April.
Beekeepers have introduced a few years before into that area Marchalina
hellenica, that is suspended to the top of trees pine branches that proceeded
from elsewhere, and on which there were different larvae stages. From there,
Marchalina hellenica has rapidly spread, having a higher reproduction rate, and
nowadays it exists in all the pine forest.
During the year there were noticed and collected different development stages of
the male and female insects, that were to be found on Pinus halepensis. The
biologic material was prepared according to SZELEGIEWICZ method (1978), and was
included in a Berlese mixture. The estimation was made by a Zeiss microscope, at
an 100-400 enlargement. Approximately 200 individuals were classified, and
recorded according to age and development stage.
Results
Morphology
Table 1 includes some morphological data. Females have a heavy and stodgy body,
similar to a sack, and have no wings (Fig. 1)
 Fig. 1 Marchalina hellenica (fundatrices) in maturation, on Pinus halepensis, in spring 1992 |
 Fig. 2 Mature founder (fundatrix), in spring of 1992 (a Berlese preparation) |
The female larvae are very much similar to adults, but in those the stilets and the second maxilla are well developed, while with the maturing founders the buccal apparatus is in retrogression (Fig. 2). Legs and antennae are well developed in all the female and male stages. That is why all the examined stages are able to move freely. Eyes are formed as ocelli. In the sexually mature female stages, the number of the sensory cells on the segments of antenna is growing (see Table 1). Both, the female and the male insects are defending themselves against heat by producing a viscous cover with wax wool.
Table 1 - Morphologic and biologic data about Marchalina hellenica Genn.
SG = antenna segment; 1 = number of
rhinaries on the antenna segments is small and irregular;
2 = number of rhinaries on the antenna segments is growing.
Brushes = buccal appara
Fig. 3a Male larvae stage, in spring of
1992 Fig. 3b An older male larvae stage
(Nikolopoulos 1964)
Development
and life places
Although Marchalina hellenica is bisexual, its reproduction occurs mainly by
parthenogenesis, as males are very rare. Commonly, a generation a year appears.
Eggs are laid naked, and they are wrapped in a viscous cover of wax wool. Before
Pinus halepensis blossoms (March-April), the founders lay eggs in great numbers
on all the pine parts. There are preferred branches, trunks, but many times also
the roots, if they are exposed to the air (Fig. 4 and 5). In these places there
occurs the development of the first (female) larvae stage. All the female larvae
stages are changing the place they are sucking of. On the tree, they are located
in great numbers on the lower part of the branch, or on the part of the trunk
that is opposed to bad weather. In September/October, we noticed under a bit of
bark of about 3 cm² up to 15 L1 larvae, closely grouped together.
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Visits
by ants
The following ant species are trophobiotically using Marchalina hellenica:
Camponotus athiops (Latr.), Crematogaster schmidti (Mayr.), Pheidole pallidula
(Nyl.), Acantholepis melas (Emery).
Discussions
On the basis of the segments of antenna, there could be differentiated in three
female development stages, namely:
1. nymphs, of the first age (L1, existing in April and September);
2. nymphs, of the second age, or the pre-adult stage (L2, existing in September,
October and April);
3. Sexually immature (existing in February through April), and sexually mature
adults (April).
These results coincide with the investigations of Nikolopoulos (1965) and Santas
(1979).
The founder on the way to maturation has, before the oviposition, a rest period
of 10 to 15 days (Santas 1983). This stage differs of that of the mature
founders. In the present investigation, there could be morphologically
differentiated sexually immature and sexually mature adults. Multiplication of
rhinaries, and the involution of the buccal apparatus do functionally occur
together with the beginning of the migration phase and of the egg laying.
In the investigations of Santas (1979), there are mentioned two larvae stages in
the case of males: a stage of pupa, and a stage of winged adult of Marchalina
hellenica, but nevertheless the description is absent. Within the framework of
Hemipteroidea, there is excluded the presence of a pupa stage. The male larval
stage, detected by the author, as concerns its morphologic characteristics (for
instance, the number of the antenna segments, their size, lack of wing
formation), is different as compared to the stage described by Nikolopoulos
(1964). According to all probabilities, in the case of the biologic material
collected on the western coast of Peloponnese , it is about a younger larvae
stage (7 antenna segments), while Nikolopoulos describes in his work an older
larvae stage (10 antenna segments). Further investigations have to clarify if
both correspond to the larval stages One and Two of Santas (1979), or if there
are, eventually, more male larvae stages. The problem of the phytophagous
relation between the males collected from the leaves of Asphodelus aestivus, and
the aerial or earthly parts of the plant rests further open. The night
precursory to collection, a strong storm up-rooted some pines, so there was the
possibility males to fall to the earth, together with the detached bark, and
then to climb onto the leaves of Asphodelus aestivus.
Marchalina hellenica could probably be visited by all ant species, which on
principle use throphobiotically the insects that are currently sucking the sap
of plants.
Conclusions
The stages that nourish themselves (and so produce honeydew), as well as the
sexually mature adults of Marchalina hellenica could be differentiated. There
are presented and discussed some morphologic characteristics of the male
development stages.
Acknowledgements
I express my thanks to DAAD for financing my stay in Greece. For the support in
the field, my thanks to Mrs Prof. E. Douma-Petridou (University of Patras ,
Greece), Messrs I. Messalas (beekeeper, Patras) and V. Kalogeropoulos
(University of Patras). Special thanks are due to Mr Dr. S. Scheurer ( Berlin ,
Germany ), for his support and help. To Mr B. Seifert (Görlitz , Germany) I
thank for having determined the ant species. To the team of Niedersächsisches
Landesamt für Bienenkunde (Celle , Germany), I thank for their support in many
cases. I also thank Mrs A. Thondorf (UFZ Centre of Environmental research
Leipzig-Halle , Germany), for having done the drawing.
Literature
Erlinghagen F (1995) Zur Morphologie und Biologie von Marchalina hellenica Genn.
(Coccina, Margarodidae), ein wichtiger Honigtauerzeuger in Griechenland. Mitt.
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Erlinghagen F (1995) Beitrag zur Morphologie von Marchalina hellenica Genn.
(Sternorrhyncha: Coccina: Margarodidae). Mitt. Internat. Entomol. Ver. Bd. 20,
Heft ¾, 141-145. Frankfurt a.M.
Erlinghagen F (2001) Portrait of an insect: Marchalina hellenica Genn.
(Sternorrhyncha: Coccina: Margarodidae), important producer of honeydew in
Greece . Apiacta 36, 131-137.
Nikolopoulos Ch (1964) Beschreibung des bisher unbekannten Männchens von
Marchalina hellenica (Gennadius) (Hemiptera, Margarodidae,
Coelostomidiinae). Ecole d’haute etudes agronomiques a Athens, pp. 31 (in
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hellenica (Gennadius) (Hemiptera, Margarodidae, Coelostomidiinae). Ecole
d’hautes etudes agronomiques a Athens, pp. 30 (in Greek).
Santas L.A. (1979) Marchalina hellenica (Gennadius), bedeutendes Insekt für
die Bienenzucht Griechenlands. Apimondia, Athen.
Santas L.A. (1983) Insects producing honeydew exploited by bees in Greece.
Apidologie 14(2), 92-103.
Schmutterer H (1976) Coccina-Schildläuse. In: Stresemann E:
Exkursionsfauna Wirbellose II/2.
Szelegiewicz H (1978) Kluce do ozncaznia owadow Polski, Czesc XVII Pluskwiaki
rownoskrzydle-Homoptera. Zeszt 5a Mszyce – Aphidoidea, Wstep i Lachnidae,
Polskie Towarzystow Entomologiczne 101, pp. 107.
 Fig. 6 Beehives in the investigation area |
 Fig. 7 Aspect with Asphodelus aestivus (Liliaceae) |
 Fig. 8 Romulea bulbocodium (Iridaceae) occurs frequently on thin places in the investigation area, and is an important nectar source for honeybees in the early spring, while Anemone coronoria and Anemone hortensis (Ranunculaceae) are important pollen sources. |
 Fig. 9 Investigation area, western coast of Peloponnese |
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