JHR 71: 241-248 (2019) or JOURNAL OF 4 ?ereewed openscess oural
doi: 10.3897/jhr.7 1.36286 SHORT COMMUNICATION ) Hymenoptera

The International Society of Hymenopterists RESEARCH

http://jhr.pensoft.net

Alate gyne of the ant Dolichoderus quadripunctatus (L.)
(Hymenoptera, Formicidae) follows foraging
trail to aphids

Wojciech Czechowski', Gema Trigos-Peral', Istvan Maak', Kari Vepsalainen*

| Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza St 64, 00-679 Warszawa, Poland
2 Organismal and Evolutionary Biology Research Programme, University of Helsinki, PO Box 65, 00014
Helsinki, Finland

Corresponding author: Wojciech Czechowski (wcz@miiz.waw.pl)

Academic editor: Petr Klimes | Received 20 May 2019 | Accepted 26 July 2019 | Published 30 August 2019
Attp://zoobank. org/8 9E633AC-5E30-469F-B1A4-2F78BDEEF047

Citation: Czechowski W, Trigos-Peral G, Maak I, Vepsalainen K (2019) Alate gyne of the ant Dolichoderus quadripunctatus
(L.) (Hymenoptera, Formicidae) follows foraging trail to aphids. Journal of Hymenoptera Research 71: 241-248. https://
doi.org/10.3897/jhr.7 1.36286

Abstract

The first observation of alate gyne of Dolichoderus quadripunctatus (L.) visiting aphids is described. A gyne
walked along a foraging trail to the aphid Panaphis juglandis Goeze colony where it imbibed honeydew
excreted on the leaf by the aphids, after which it returned to the trail. This recurred during two more days,
always a single alate gyne at a time; hence the total number of gynes, one or more, remained open. The
phenomenon, hitherto practically unknown in ants, is presented against the background of the biology of

the species and discussed in the context of specific environmental circumstances and the colony dynamics.

Keywords
Ants, aphids, behavioural plasticity, colony dynamics, gyne foraging, life history, Panaphis juglandis

Introduction

In ants and other social insects, the basic division of tasks is such that workers take
care of the colony tasks, whereas queens reproduce (Hdélldobler and Wilson 1990). The
variation around this basic theme is, however, large, depending on the species and spe-
cific circumstances. For example, workers of many species may produce male offspring
(Bourke 1988). On the other hand queens may forage (see Discussion). Until now,

Copyright Wojciech Czechowski et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

242 Wojciech Czechowski et al. / Journal of Hymenoptera Research 71: 241-248 (2019)

the published records on foraging gynes or queens have been on dealate individuals, in
which plausible explanations are easily found, whereas observations on foraging alates
seem to be lacking.

Here, we report our observations on this previously practically unknown behavy-
iour, foraging of one or more alate ant gynes [though see Discussion on the microgynes
of Manica rubida (Latr.)], and discuss it in a wider context of the biology and life his-
tory of the species in question, Dolichoderus quadripunctatus (L.).

The observations

Observations were made in the area with sparse single-family housing in Brwinédw
(52°08'N, 20°43'E) near Warsaw, Poland. The site of observation was in a garden
growing, among others, a few common walnut trees (Juglans regia L.) next to a de-
tached house with old wooden elements (elevation, pillars, balustrades) (Fig. 1). Nests
of D. quadripunctatus were located in the walnut trees and in the wooden elements of
the building and fences; the ants foraged mainly in the crowns of the trees. Observa-
tions were conducted irregularly in the years 2010-2019, with the most interesting
finding recorded in July 2017.

At the beginning of July 2017, a colony of nymphs of the large walnut aphid Pana-
phis juglandis Goeze appeared on a leaf of a young walnut tree, on its upper surface,
at a height of 1.1 m above the ground. On July 7, the aphids were discovered by D.
quadripunctatus foragers from a nest in a wooden terrace pillar at a height of c. 4.5 m
above the ground (Fig. 1). The ants formed a regular foraging trail from their nest to
the aphids. The intricate trail measured at least 13 m (the ants came out of the crack
of the pillar, but the location of the nest was unknown). ‘The traffic intensity was low:
one to two individuals per minute in each direction. During the day, depending on the
weather, the aphids were accompanied by a few to nearly 30 workers. In the following
days, two smaller P juglandis colonies appeared on other leaves of the same tree. They
were also visited by D. quadripunctatus, although with lower activity.

On July 16, an alate D. quadripunctatus gyne appeared at the aphids (Fig. 2). Like
the workers, it licked the honeydew from the leaf surface in the immediate vicinity of
the aphids. It did it less efficiently than the workers, with long breaks, thus spending
much more time on the leaf than the workers. After about 15 minutes, the gyne left
the leaf, following the foraging trail towards the nest. During occasional observations
in the following days, the presence of a single alate gyne among foraging workers was
recorded twice at the same aphid colony. Each time the gyne was seen at the aphids
during sunny warm weather, when the foraging activity of the D. quadripunctatus
workers was highest.

At the end of July, a ladybird (Adalia bipunctata L.) appeared at the aphid colony.
Within three days, without being counteracted by the ants, it ate all the aphids. In the
following days also the other two colonies of P juglandis were consumed, which put an
end to the observations. The lack of defense of the food resources by D. quadripunctatus

Alate gyne of Dolichoderus quadripunctatus (L.) follows foraging trail 243

Figure |. Site of observation; in the foreground, the young walnut with aphids, above (along the stairs),
the black elder bush. The location of the D. guadripunctatus nest is indicated with an arrow. Photo taken
on 16.07.2017 (Tadeusz Berlinski).

Figure 2. Aphids Panaphis juglandis visited by workers and alate gyne of D. quadripunctatus. Photo taken
on 16.07.2017 (Tadeusz Berlinski).

244 Wojciech Czechowski et al. / Journal of Hymenoptera Research 71: 241-248 (2019)

was also revealed by multiple observations of the syrphid fly which, not disturbed by
ants, licked the honeydew in the immediate vicinity of them. Concurrently, elsewhere
in the garden, D. quadripunctatus foragers used experimentally placed baits with
diluted honey, but withdrew on the appearance of Lasius niger (L.) workers.

The foraging trail along which the alate gynes walked to the aphid colony on the
young walnut, led, inter alia, through the trunk and twigs of a black elder (Sambucus
nigra L.) shrub. ‘The critical point of the route was the passage from the elder leaf to
the handrail of the stairs (Fig. 1). When even a slight wind made the leaves touch the
railing intermittently, the ants managed to overcome the gap.

Discussion

Foraging of inseminated dealate young gynes is not uncommon in ants. It is the norm
in a lot of species which found new colonies semi-claustrally (e.g. Fridman and Avital
1983; Johnson 1996; Brown 1999; Brown and Bonhoeffer 2003; Peeters and Molet
2009), although the evolutionarily derived feature, claustral colony founding (where
queens do not leave the nest), is the common mode in extant ants (Hdlldobler and
Wilson 1990). Species with semi-claustral colony founding with foraging dealate
queens are known especially in the tropics and subtropics (e.g. Anderson et al. 2006,
Brown 1999, Johnson 1996, 2002, Lenoir and Dejean 1994). In temperate regions,
the dealate, mated fundatrices (founding queens) of Manica rubida and Myrmica spe-
cies leave their nest to forage still after the first overwintering (Le Masne and Bonavita
1969; Elmes 1982; Lenoir et al. 2010).

In Dolichoderinae, foraging of queens is scarcely documented. It was only recently
documented within the genus 7echnomyrmex Mayr which includes many tramp spe-
cies; ergatoid (worker-like) queens of 7’ vitiensis Mann were foraging outside the nest
with workers (Vaandnen et al. 2018). In the light of this scarceness, the foraging of the
alate Dolichoderus quadripunctatus gyne(s) is peculiar — overall, such foraging of alate
ant gynes seems unusual (or at least unreported) in nature. The mating status and pos-
sible hibernation of the D. guadripunctatus gyne(s) observed by us remain unknown. A
comparable case concerns the poorly known microgyne caste in Manica rubida, whose
status also remains unrecognised. In the colony, the alates seem to fulfil the task of
workers by foraging outside the nests (Lenoir et al. 2010).

In the following, we will discuss this new finding in D. quadripunctatus in the light
of the biology and life history of the species. It is a Euro-West-Siberian xerothermophilic
oligotope of warm bright forests, also found in old orchards, gardens and parks. It is
a dendrobiontic species which forages almost exclusively on trees (mainly in canopies)
and is well adapted to move around the leaves (Seifert 2008). ‘The agility of the species to
move in an unstable environment and ability to find alternative routes (including a few
metres long nylon washing lines) was also evident in our long-standing observations.

The species avoids encounters with heterospecific ants (Torossian 1979; Czechows-
ki et al. 2012; Seifert 2018), although a mere high number of workers may displace

Alate gyne of Dolichoderus quadripunctatus (L.) follows foraging trail 245

other species to the periphery of its foraging area (Stukalyuk 2018). Our own observa-
tions on the non-aggressive behaviour of the D. quadripunctatus workers against the
predatory ladybird beetle which consumed the aphids, and against the honeydew-con-
suming syrphid fly, may be interpreted such that the honeydew source was a relatively
marginal one in the resource spectrum of this ant, which is basically a predatory species
(Seifert 2018). Our D. quadripunctatus gyne(s) and workers were observed only to lick
honeydew from the leaves, not to milk the aphids as it is the norm in true trophobiosis
where the ants in return offer protection to the aphids (Holldobler and Wilson 1990).
Consumption of dropped honeydew without trophobiosis seems to be the usual way of
aphid attendance for D. guadripunctatus (Seifert 2008) as for many other arthropods
which feed on excrements of aphids on the leaves (Ulyshen 2011).

It is noteworthy that Stukalyuk (2018), while working on the supercolony of D.
quadripunctatus, never observed alate gynes on the foraging trails, even though he saw
them outside the nests (pers. comm. to WCz). This indicates that some specific circum-
stances may trigger the visits of D. quadripunctatus alate gynes to extra-nidal food sourc-
es. Here, we suggest two, not mutually excluding, explanations for this seemingly rare
behaviour — remembering that seeming rarity is not synonymous with insignificance.

An evident first reason for the alate gyne(s) to leave the nest and follow worker trails
to aphid colonies is an acute shortage of food in the nest. Indeed, in Poland the spring
of 2017 was late and cool, and the summer generally rainy and unfavourable for insects,
when alate gynes of D. guadripunctatus were observed at the aphids. The supposition
that hunger drives alate gynes to forage is justified in light of the observation of Toros-
sian (1968), who stated that the workers do not display special care for young gynes
gathered together in queenless auxiliary nests from their emerging to mating time.

The impact of evident food shortage on the behaviour of ants, probably caused by
an exceptionally dry summer, was reported by Vepsdlainen and Czechowski (2014).
Myrmica rugulosa Nyl., a submissive species at the bottom of the ant competition hier-
archy, temporarily took over groups of the aphid Stomaphis quercus (L.), which is obli-
gately associated with the highest-level territorial ant species Lasius fuliginosus (Latr.).
This unique intrusion lasted at least two weeks, during which M. rugulosa workers
successfully brought honeydew milked from the S. guercus back to their nest(s). As in
many other rare observations, one chooses the best explanation on indirect evidence.
In this case, because the drought affected severely the herbs which harbour aphids nor-
mally used by M. rugulosa, the ants probably were forced to search for supplementary
food. Here, the successful change of behaviour probably helped the colony to survive
the drought period. As comes to the foraging of the alate gynes of D. guadripunctatus,
the primary benefit was at the individual level.

To see how the foraging of alate gynes could contribute to the colony dynamics, an
introduction to the social structure of a D. guadripunctatus colony is at place. Typically,
it is monogynous polydomy with one main queenright nest and a few branch nests
inhabited by workers with possible offspring. ‘This structure is caused by the small size
of individual nest spaces which most often can harbour maximally several tens of indi-
viduals; the entire colony usually consists of several hundred, rarely over 1000 adults

246 Wojciech Czechowski et al. / Journal of Hymenoptera Research 71: 241-248 (2019)

(Torossian 1960, 1967a; Seifert 2018). The scattered nest loci of the colony enable the
species the following specific life-history features: (1) males arise only from eggs laid
by workers; (2) worker oviposition is possible only away from the queen; (3) larvae
can develop to gynes only without contact with the queen; (4) insemination of gynes
frequently takes place inside or close to the nest; (5) to initiate a colony, the gyne needs
to be adopted by queenless workers (Torossian 1967b, 1968, 1974; Seifert 2018).
Direct observations on how a gyne is able to find a queenless workforce and start a
colony are lacking. It has been suggested that a group of workers may take the gyne to a
queenless outpost nest (Torossian 1974). We suggest here an additional possibility, where
gynes which visit aphid colonies might serendipitously take a trail back to a queenless
nest and be accepted by its workers. The potential for success of such gyne behaviour
could be highest in large supercolonies — like the one studied by Stukalyuk (2018) —
where foraging trails of a high number of nests merge on a tree trunk, lead up to the
crown, to spread there to a number of food sources (S. Stukalyuk, pers. comm. to WCz).
If our above suggestion has any value in the colony dynamics of D. quadripuncta-
tus, the question remains, why alate gynes seem to be only very occasional visitors at
aphid colonies. One evident reason is that the yearly number of gynes produced by a
colony is low (Torossian 1974) and secondly, that the species is an arboreal ant which
has usually most of its nests high up in the tree crowns, and which only exceptionally
forages in the lower layers of vegetation (Seifert 2018). Simply, observations on what
goes on in the main space of the colonies are needed in order to test our suggestion.

Acknowledgements

We thank the editor Petr KlimeS and two reviewers, whose comments helped to im-
p
prove the article.

References

Anderson KE, Keyl AC, Pollock GB (2006) Mating flight, metrosis, and semi-claustrality in the
seed-harvester ant Pogonomyrmex salinus (Hymenoptera, Formicidae). Insectes Sociaux 53:
92-96. https://doi.org/10.1007/s00040-005-0840-y

Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. The Quorterly
Review of Biology 63: 291-311. https://doi.org/10.1086/415930

Brown MJF (1999) Semi-claustral founding and worker behaviour in gynes of Messor andrei.
Insectes Sociaux 46: 194-195. https://doi.org/10.1007/s000400050133

Brown MJE, Bonhoeffer S (2003) On the evolution of claustral colony founding in ants. Evo-
lutionary Ecology Research 5: 305-313.

Czechowski W, Radchenko A, Czechowska W, Vepsaldinen K (2012) The ants of Poland with
reference to the myrmecofauna of Europe. Fauna Poloniae n.s. 4. Natura optima dux

Foundation, Warszawa.

Alate gyne of Dolichoderus quadripunctatus (L.) follows foraging trail 247

Elmes GW (1982) The phenology of five species of Myrmica (Hym. Formicidae) from South
Dorset, England. Insectes Sociaux 29: 548-559. https://doi.org/10.1007/BF02224224

Fridman S, Avital E (1983) Foraging by queens of Cataglyphis bicolor nigra (Hymenoptera:
Formicidae): an unusual phenomenon among the Formicidae. Israel Journal of Zoology
32: 229-230.

Holldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, MA. https://
doi.org/10.1007/978-3-662-10306-7

Johnson RA (1996) Capital and income breeding and the evolution of colony founding strate-
gies in ants. Insectes Sociaux 53: 316-322. https://doi.org/10.1007/s00040-006-0874-9

Johnson RA (2002) Semi-claustral colony founding in the seed-harvester ant Pogonomyrmex
californicus: a comparative analysis of colony founding strategies. Oecologia 132: 60-67.
https://doi.org/10.1007/s00442-002-0960-2

Le Masne G, Bonavita A (1969) La fondation des sociétés selon un type archaique par une
fourmi appartenant aune sous famille évoluée. Comptes Rendus des Séances de |’Académie
des Sciences, ser. D 269: 2373-2376.

Lenoir A, Dejean A (1994) Semi-claustral colony foundation in the formicinae ants of the
genus Polyrhachis (Hymenoptera: Formicidae). Insectes Sociaux 41: 225-234. https://doi.
org/10.1007/BF01242293

Lenoir A, Devers S, Marchand P, Bressac C, Savolainen R (2010) Microgynous queens in the
Palearctic ant, Manica rubida: dispersal morphs or social parasites? Journal of Insect Sci-
ence 10: article 17. https://doi.org/10.1673/031.010.1701

Peeters C, Molet M (2009) Colonial reproduction and life histories. In: Lach L, Parr C, Abbott
K (Eds) Ant ecology. Oxford University Press, Oxford, 161-178. https://doi.org/10.1093/
acprof:oso/9780199544639.003.0009

Seifert B (2008) The ants of Central European tree canopies (Hymenoptera: Formicidae) — an
underestimated population? In: Floren A, Schmidl J (Eds) Canopy arthropod research in
Europe Bioform Entomology & Equipment, Nuremberg: 157-173.

Seifert B (2018) The ants of Central and North Europe. lutra Verlags- und Vertriebsgesellschaft,
Tauer.

Stukalyuk S (2018) Supercolony of Dolichoderus quadripunctatus Linnaeus (Hymenoptera, Formi-
cidae). Biology Bulletin Reviews 8: 449-462. https://doi.org/10.1134/S2079086418050092

Torossian C (1960) La biologie de la fourmi Dolichoderus quadripunctatus (Hyménoptére —
Formicoidea — Dolichoderidae). Insectes Sociaux 7: 383-393. https://doi.org/10.1007/
BF02225776

Torossian C (1967a) Recherches sur la biologie et Pethologie de Dolichoderus quadripunctatus
(L.) Hym. Formicoidea Dolichoderidae. I. Etude des populations dans leur milieu naturel.
Insectes Sociaux 14: 105-121. https://doi.org/10.1007/BF02223262

Torossian C (1967b) Role des reines sur le formation et apparition des sexués femelles dans les
sociétés de la fourmi Dolichoderus quadripunctatus (Hym. Form. Dolichoderidae). Compt-
es Rendus de la Sociéte de Biologie 161: 1455-1458.

Torossian C (1968) Recherches sur la biologie et l’éthologie de Dolichoderus quadripunctatus
(L.) (Hym. Form. Dolichoderidae). VIH. Mode de reproduction et cycle biologique des
colonies. Insectes Sociaux 15: 375-387. https://doi.org/10.1007/BF02223634

248 Wojciech Czechowski et al. / Journal of Hymenoptera Research 71: 241-248 (2019)

Torossian C (1974) Polymorphismus und Kastendifferenzierung bei Dolichoderiden. In:
Schmidt GH (Ed.) Sozialpolymorphismus bei Insecten. Wissenschaftliche Verlagsgesells-
chaft MbH, Stuttgart, 862-884.

Torossian C (1979) Importance quantitative des oeufs abortifs d’ouvriéres dans le bilan
trophique de la colonie de la fourmi Dolichoderus quadripunctatus. Insectes Sociaux 26:
295-299. https://doi.org/10.1007/BF02223549

Ulyshen MD (2011) Arthropod vertical stratification in temperate deciduous forests: impli-
cations for conservation-oriented management. Forest Ecology and Management 261:
1479-1489. https://doi.org/10.1016/j.foreco.2011.01.033

Vaananen S, Vepsalainen K, Vepsaldinen V (2018) Technomyrmex vitiensis Mann, 1921 (Hy-
menoptera, Formicidae, Dolichoderinae), a new exotic tramp ant in Finland. Sahlbergia
24.1: 14-19.

Vepsaldinen K, Czechowski W (2014) Against the odds of the ant competition hierarchy: sub-
missive Myrmica rugulosa block access of the dominant Lasius fuliginosus to its aphids.

Insectes Sociaux 61: 89-93. https://doi.org/10.1007/s00040-013-0332-4