Ann. soc. entomol. Fr. (n.s.), 2012, 48 (1–2) : 189-198
ARTICLE
Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in
wetland habitats in western Palaearctic: key and associated
aphid parasitoid guilds
Željko Tomanovi (1), Petr Starý (2), Nickolas G. Kavallieratos (3), Vesna Gagi (1,4), Milan Pleaš (1),
Marina Jankovi (1), Ehsan Rakhshani (5), Aleksandar Ćetkovi (1) & Aneljko Petrovi (1)
(1)
Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
Institute of Entomology, Academy of Sciences of the Czech Republic, Branišovská 31, 37005 České Budějovice, Czech Republic
(3)
Laboratory of Agricultural Entomology, Department of Entomology and Agricultural Zoology, Benaki Phytopathological Institute,
8 Stefanou Delta str., 145 61 Kifissia, Attica, Greece
(4)
Agroecology, University of Göttingen, Grisebachstr. 6, D-37077 Göttingen, Germany
(5)
Department of Plant Protection, College of Agriculture, Zabol University, Zabol, P. O. Box: 998615-538, I. R. Iran
(2)
Abstract. This paper presents over 66 tritrophic parasitoid-aphid-plant associations from wetland
habitats in western Palaearctic, comprising 24 parasitoid species, 24 aphid hosts and over 30 plant
species, based on records from 25 countries. Seven new associations are documented. About half
of the established tritrophic associations (34) were recorded rarely, while 6 associations have been
documented more than 100 times each, based on 4 common and widespread Aphidiinae species. The
majority of recorded parasitoid species (16) are involved in only 1–2 tritrophic associations, 7 species
were recorded in 3–5 associations, and one species (Praon necans) is a member of even 16 different
associations based on wetland habitats. Generally, the most frequently recorded associations are based
on some very common and widespread parasitoids not specific for this class of habitats. On the basis
of distribution, host range and habitat specialization we have divided aphid parasitoid associations
in wetland habitats into three ecological categories. The most specialized group, containing rarely
recorded parasitoid species whose distribution and aphid hosts are strictly associated with wetland
habitats, is potentially highly vulnerable to extinction. The role of aphids associated with wetland
habitats as reservoirs for economically important parasitoid species is discussed and a key for the
identification of aphid parasitoids in wetland habitats is provided.
Résumé. Parasitoïdes aphides (Hymenoptera : Braconidae : Aphidiinae) des milieux humides de
l’Ouest-Paléarctique : clef des parasitoïdes aphides et guildes associées. Cet article présente 66
associations tri-trophiques (Parasitoïdes/Pucerons/ Plantes) des milieux humides de la région OuestPaléarctique. 24 espèces de parasitoïdes, 24 pucerons hôtes et plus de 30 plantes ont été recensés
dans 25 pays différents. 7 associations nouvelles sont rapportées. Environ la moitié des associations
tri-trophiques (34) ont été rarement observées, alors que 6 de ces associations concernant 4 espèces
de parasitoïdes communes et largement répandues ont été constatées plus de 100 fois. La majorité
des espèces de parasitoïdes (16) rencontrées l’ont été sur seulement 1–2 associations tri-trophique, 7
espèces sur 3–5 associations et 1 espèce (Praon necans) s’est trouvé impliqué dans 16 associations.
Globalement, les associations les plus fréquentes concernent des parasitoïdes communs et répandus,
non spécifiques de ce type d’habitat. Sur la base de la distribution, la gamme d’hôtes et la spécialisation
de l’habitat, nous avons divisé les associations pucerons-parasitoïdes des milieux humides en 3
catégories écologiques. Le groupe le plus spécialisé, comprenant des espèces plutôt rares et dont la
distribution ainsi que les pucerons hôtes sont strictement associés aux milieux humides, présentent de
grand risques d’extinction. Le rôle des pucerons associés aux milieux humides en tant que réservoirs
pour des parasitoïdes à impact économique important est discuté. De plus, une clé d’identification des
espèces parasitoïdes de pucerons des milieux humides est proposée.
Keywords: Aphid parasitoids, Tritrophic interactions, Wetlands.
W
etland habitats are naturally occurring in all
climatic/biome zones of western Palaearctic,
from forest tundra in the northernmost Europe and at
E-mail: [email protected], [email protected], [email protected]
com, [email protected], [email protected]
Accepté le 29 septembre 2011
higher altitudes of mountains (e. g. peat bogs), through
diverse temperate to subtropical azonal ecosystems
associated with rivers, lakes/ponds, marshes, etc.
Also, important types of wetlands are artificial ones,
like ditches in agricultural landscapes and ornamental
ponds in urban environments. In crop-dominated areas,
due to agricultural intensification and urbanization,
wetland habitats are under great anthropogenic pressure
189
Ž. Tomanovi, P. Starý, N. G. Kavallieratos, V. Gagi, M. Pleaš, M. Jankovi, E. Rakhshani, A. Ćetkovi & A. Petrovi
(Tscharntke et al. 2005). Such habitats now serve as
refugia for many important wild plant and animal
species. In particular, wetland habitats could provide
food, shelter, and overwintering sites for many natural
enemies of pest species, including aphid parasitoids
(Starý 1970). In this context, they could be very
important as reservoirs for aphidiinae parasitoids and
other insects involved in biological control, especially
in lowlands with agroecosystem-dominated landscapes.
Furthermore, wetland habitats are often invaded by
invasive exotic plants and this situation contributes to
the establishment of new aphid/parasitoid associations,
with diverse possible impacts on the surrounding
ecosystems and existing trophic networks.
Aphidiinae parasitoids in wetland habitats of
western Palaearctic are very diverse group, ranging
from some very common, widespread and well-known
taxa, to some highly specific and rarely encountered
ones, for which even the basic taxonomic knowledge is
lacking. Here we present a concise review of available
knowledge about their taxonomy, distribution, guilds
composition and possible threat status. In particular,
we present the established aphid parasitoid tritrophic
associations, and we provide a key for the identification
of aphid parasitoids in wetland habitats.
DISCOVERY stereomicroscope. Several specimens were
gold-coated with a sputter coater and examined using a Jeol
JSM – 6460LV scanning electron microscope. Measurements
in the key were taken using an ocular micrometer. The ratio
measurements were based on slide-mounted specimens. See
Kavallieratos et al. (2001) and Tomić et al. (2005) for more
details about measurements.
Material and methods
Samples of aquatic and semiaquatic plants and their aphidparasitoid associations were collected over 40 years in various
areas of western Palaearctic. Plant samples bearing both live
and mummified aphids were collected. Samples of live aphids
were preserved in 90% ethanol and 75% lactic acid in a ratio
2:1 (Eastop & van Emden 1972) for later identification. The
remaining aphids were maintained in the laboratory until
parasitoid emergence. Mummies, each attached to a small
leaf piece, were placed separately in small plastic boxes with a
circular opening covered with muslin on the lid and put inside
a growth cabinet (22.5 oC, relative humidity 65%, 16L:8D)
(Kavallieratos et al. 2001).
Aphid and aphid parasitoid specimens examined in this study
are deposited in the collection of the Institute of Zoology,
Faculty of Biology, University of Belgrade (Serbia), and the
collection of P. Starý (České Budějovice, Czech Republic). Each
new host plant-aphid-aphid parasitoid record is indicated by
an asterisk in front of the host aphid named in the associations
section. Every published record contains the original reference
in parentheses, but unpublished records for countries contain
full data. Each association which is sampled less than 10 times
throughout the studied area is considered as rare and marked
with (R). Associations sampled between 10 and 100 times are
considered as common, and marked accordingly with (C), and
those recorded more than 100 times are considered as very
common and marked with (V).
The terminology used in this paper regarding the diagnostic
characters of the aphid parasitoid follows Sharkey & Wharton
(1997). Numbers in parentheses in the key indicate uncommon
conditions. External morphology was studied using a ZEISS
Czech Republic: R. nymphaeae on Nymphaea sp. (C) (Starý
2006); Serbia: R. nymphaeae on Alysma plantago-aquatica (R)
(Kavallieratos et al. 2004).
190
Results
Tritrophic associations for western Palaearctic
Aphidius avenae Haliday 1834
Montenegro: *Sitobion sp. on Carex rostrata (R), 20.VII.2004,
Mt. Durmitor-Valovito jezero, 2♀♀1♂.
Aphidius colemani Viereck 1912
Czech Republic: Rhopalosiphum nymphaeae (L. 1761) on
Sagittaria sp. (C) (Starý 2006).
Aphidius ervi Haliday 1834
Czech Republic: Aulacorthum sp. on Malachium aquaticum
(C) (Starý 2006).
Aphidius matricariae Haliday 1834
Aphidius rhopalosiphi De-Stefani Perez 1902
Italy: *R. nymphaeae on A. plantago-aquatica (R), 31.V.1976,
Formigliana–Vercelli; Serbia: *Schizaphis scirpi (Passerini
1874) on Typha latifolia (R), 14.V.2007, 9.VI.2007, Padinska
skela, 52♀♀, 37♂♂.
Aphidius transcaspicus Telenga 1958
Czech Republic: Hyalopterus pruni (Geoffroy 1762) on
Phragmites australis (V) (Starý 2006); Israel: H. pruni (incl.
Hyalopterus amygdali [E. Blanchard 1840]) on P. australis (V)
(Mackauer & Starý 1967); Italy: H. pruni (incl. H. amygdali)
on P. australis (V) (Mackauer & Starý 1967); Pakistan: H. pruni
(incl. H. amygdali) on P. australis (V) (Mackauer & Starý 1967);
Spain: H. pruni (incl. H. amygdali) on P. australis (V) (Mackauer
& Starý 1967); Iran: H. pruni (incl. H. amygdali) on P. australis
(V) (Starý et al. 2000, Rakhshani et al. 2008); Melanaphis
donacis (Passerini 1862) on Arundo donax (V), 8.X.2009,
Zabol, 11♀♀, 8♂♂; Iraq: H. pruni (incl. H. amygdali) on P.
australis (V) (Mackauer & Starý 1967); M. donacis on A. donax
(V) (Starý & Kaddou 1971); France: M. donacis on A. donax
(V) (Mackauer & Starý 1967); Greece: H. pruni on P. australis
(V) (Kavallieratos et al. 2004); Turkey: H. pruni on P. australis
(V) (Uysal et al. 2004); Uzbekistan: H. pruni on P. australis
(V) (Mackauer & Starý 1967); Turkmenistan: H. pruni on P.
australis (V) (Starý 1965).
Aphid parasitoids in wetland habitats
Aphidius urticae Haliday 1834
Czech Republic: Rhopalomyzus lonicerae (Siebold 1839) on
Phalaris sp. (R) (Starý 2006); S. scirpi on Typha angustifolia (R)
(Starý 2006); Serbia: Aulacorthum solani Kaltenbach 1843 on
Myosoton aquaticum (C) (Kavallieratos et al. 2004); S. scirpi on
T. latifolia (R) (Kavallieratos et al. 2004).
Rhopalosiphum rufulum Richards 1960 on Acorus calamus (R)
(Starý 2006); S. scirpi on T. angustifolia (C) (Starý 2006); S.
scirpi on Typha sp. (C) (Starý 2006); Sweden: H. pruni on P.
australis (V) (Gardenfors 1986).
Ephedrus persicae Froggatt 1904
Binodoxys acalephae (Marshall 1896)
Greece: M. donacis on A. donax (C) (Gardenfors 1986); Iran:
Aphis affinis del Guercio 1911 on Mentha aquatica (C) (Talebi
et al. 2009)
Czech Republic: Aphis nasturtii Kaltenbach 1843 on Caltha
palustris (C) (Starý 2006); Serbia: *Aphis triglochinis Theobald
1926 on Rorippa sylvestris (R), 8.VI.2007, Padinska Skela,
21♀♀11♂♂.
Lipolexis gracilis Förster 1862
Binodoxys angelicae (Haliday 1833)
Czech Republic: Aphis sp. on Malachium aquaticum (C) (Starý
2006); Schizaphis sp. on Typha sp. (C) (Starý 2006).
Diaeretellus palustris Starý 1971
Germany: R. nymphaeae on Sphagnum spp. (R) (Starý 1971).
Diaeretellus macrocarpus Mackauer 1961
Germany: Bacillaphis sp. on Carex sp. (R) (Mackauer 1961);
Thripsaphis sp. on Carex sp. (R) (Mackauer 1961); Sweden:
Iziphya ingegardae Hille Ris Lambers 1952 on Carex sp. (R)
(Mackauer 1961); Montenegro: Thripsaphis verrucosa Gillette
1917 on C. rostrata (R), Carex nigra (R) (Tomanović et al.
2007); Czech Republic: without host data, North Bohemia,
wet meadows (Starý 2006).
Diaeretellus ephippium (Haliday 1833)
England: Decorosiphon corynothrix Börner 1939 on Atricum
undulatum (R), April 1954 Starý 1959; Czech Republic:
unknown aphid on mosses (including Pleurosiphum schreberi)
and Sphagnum spp., Velka Jizerska louka, Jizerske hory range,
Horska Kvilda, Šumava range, South Bohemia (Starý 1959;
Starý 2006).
Diaeretellus heinzei (Mackauer 1959)
Germany: D. corynothrix on mosses (R) (Mackauer 1959);
Czech Republic: without host data, mixed forest undergrowth
(Starý 2006).
Diaeretiella rapae (M´Intosh 1855)
Czech Republic: Myzus sp. on M. aquaticum (C) (Starý 2006);
S. scirpi on T. angustifolia (C) (Starý 2006); Italy: Schizaphis
longicaudata Hille Ris Lambers 1939 on A. donax (C) (Mackauer
& Starý 1967).
Ephedrus plagiator (Nees 1811)
Czech Republic: H. pruni on P. australis (V) (Starý 2006);
Serbia: *S. scirpi on T. latifolia (R), June, 1996, Petnica, 7♀♀
5♂♂.
Lysiphlebus fabarum (Marshall 1896)
Czech Republic: R. nymphaeae on Ranunculus sp. (C) (Starý
2006); Iran: Saltusaphis scirpus Theobald 1915 on Carex sp. (R)
(Starý et al. 2000); A. affinis on M. aquatica (V), 18.IV.2004,
Isfahan, 29♀♀ 18♂♂; Serbia: H. pruni on P. australis (V)
(Kavallieratos et al. 2004); A. affinis on M. aquatica (V)
(Kavallieratos et al. 2004); Greece: A. affinis on M. aquatica
(V) (Kavallieratos et al. 2004).
Praon abjectum (Haliday 1833)
Czech Republic: A. nasturtii on C. palustris (C) (Starý 2006);
Serbia: H. pruni on P. australis (C), 17.VII.2004, Kula, 1♂.
Praon spinosum Mackauer 1959
Germany: Thripsaphis sp. on Carex sp. (R) (Mackauer 1959);
Montenegro: T. verrucosa on C. nigra (R) (Tomanović et al.
2007); Serbia: *Subsaltusaphis picta (Hille Ris Lambers 1939)
on Carex sp. (R), 8.IV.2007, Zasavica, 1♀ 2♂♂.
Praon necans Mackauer 1959
Czech Republic: R. nymphaeae on A. plantago-aquatica (C),
C. palustris (C), Hydrochoeris morsus-ranae (R), Lemna sp. (C),
Menyanthes trifoliata (R), Nuphar sp. (R), Nymphaea sp. (C),
Sagittaria sp. (C), T. angustifolia (C) (Starý 2006); R. rufulum
on A. calamus (R) (Starý 2006); Schizaphis sp. on Typha sp.
(C) (Starý 2006); Germany: R. nymphaeae on A. plantagoaquatica (C) (Boness & Starý 1988); Italy: R. nymphaeae on
A. plantago-aquatica (C) (Mackauer & Starý 1967); Portugal:
R. nymphaeae on Eichhornia crassipes (R) (Mackauer & Stary
1967); France: R. nymphaeae on Sparganium ramosum (R)
(Mackauer & Starý 1967); Serbia: R. nymphaeae on Ranunculus
aquatilis (R) (Kavallieratos et al. 2004); R. nymphaeae on T.
latifolia (C), 14.V.2007, Padinska Skela, 7♀♀ 4♂♂; Hungary:
R. nymphaeae on Trapa natans (R) (Kovacz 2001).
Praon yomenae Takada 1968
France: Staticobium limonii (Contarini 1847) on Limonium
vulgare (R) (Starý et al. 1975).
191
Ž. Tomanovi, P. Starý, N. G. Kavallieratos, V. Gagi, M. Pleaš, M. Jankovi, E. Rakhshani, A. Ćetkovi & A. Petrovi
Figures 1–12
1, Diaeretellus ephippium, wingless ♀; 2, Ephedrus plagiator, forewing ♀; 3, Praon necans, forewing ♀; 4, Praon volucre, forewing ♀; 5, Aphidius transcaspicus,
forewing ♀; 6, Ephedrus persicae, forewing ♀; 7, Ephedrus persicae, dorsal aspect of petiole ♀; 8, Ephedrus plagiator, dorsal aspect of petiole ♀; 9, Praon
spinosum, forewing ♀; 10, Praon spinosum, dorsal aspect of petiole ♀; 11, Praon necans, dorsal aspect of petiole ♀; 12, Praon yomenae, forewing ♀.
192
Aphid parasitoids in wetland habitats
Figure 13–24
13, Praon abjectum, dorsal aspect of mesoscutum ♀; 14, Praon volucre, dorsal aspect of mesoscutum ♀; 15, Lysiphlebus fabarum, forewing ♀; 16, Anterolateral
aspect of petiole of Aphidius colemani ♀; 17, Anterolateral aspect of petiole of Aphidius matricariae ♀; 18, Anterolateral aspect of petiole of Aphidius ervi ♀;
19, Aphidius colemani, forewing ♀; 20, Aphidius avenae, antenna ♀; 21, Aphidius transcaspicus, antenna ♀; 22, Aphidius rhopalosiphi, forewing ♀; 23, Aphidius
urticae, forewing ♀; 24, Diaeretellus macrocarpus, forewing ♀.
193
Ž. Tomanovi, P. Starý, N. G. Kavallieratos, V. Gagi, M. Pleaš, M. Jankovi, E. Rakhshani, A. Ćetkovi & A. Petrovi
Praon volucre (Haliday 1833)
Turkey: H. pruni on P. australis (V) (Mackauer & Starý 1967);
Greece: H. pruni on P. australis (V) (Kavallieratos et al. 2004);
Czech Republic: H. pruni on P. australis (V) (Starý 2006,
Starý & Havelka 2008); Estonia: H. pruni on P. australis (V)
(Mackauer & Starý 1967); Finland: H. pruni on P. australis (V)
(Mackauer & Starý 1967); France: H. pruni on P. australis (V)
(Mackauer & Starý 1967); Georgia: H. pruni on P. australis (V)
(Mackauer & Starý 1967); Germany: H. pruni on P. australis
(V) (Mackauer & Starý 1967); Italy: H. pruni on P. australis
(V) (Mackauer & Starý 1967); F.Y.R. Macedonia: H. pruni on
P. australis (V) (Mackauer & Starý 1967); Iraq: M. donacis on
A. donax (C) (Starý & Kaddou 1971); Portugal: H. pruni on P.
australis (V) (Mackauer & Starý 1967); Slovenia: H. pruni on
P. australis (V) (Mackauer & Starý 1967); Ukraine: H. pruni
on P. australis (V) (Mackauer & Starý 1967); Uzbekistan: H.
pruni on P. australis (V) (Starý 1979).
Trioxys auctus (Haliday 1833)
Italy: *R. nymphaeae on A. plantago-aquatica (R), 8.VI.1976,
Formigliana, Vercelli; Serbia: R. nymphaeae on T. latifolia (R)
(Petrović et al. 2009); S. scirpi on T. angustifolia (R) (Petrović
et al. 2009).
Key to females of the Aphidiinae in wetland
habitats of western Palaearctic
1. Wings not developed (Fig.1) (males winged) .............
................................... Diaeretellus ephippium (Haliday)
- Wings normally developed ........................................... 2
2. Forewing RS vein reaching apical margin and close
marginal cell (Figs. 2, 6). Mummy black ...................... 3
- Forewing RS vein not reaching apical margin; marginal
cell open (Figs. 3, 4, 5). Mummy yellow, brown or
white ........................................................................... 4
3. Forewing 3RSa vein shorter than 2RS vein (Fig. 6).
Petiole short, subquadrate (Fig. 7) ...............................
.............................................. Ephedrus persicae Froggatt
- Forewing 3RSa vein longer than 2RS vein (Fig. 2).
Petiole elongated (Fig. 8) ....... Ephedrus plagiator (Nees)
4. Forewing RS + M vein present (Figs. 3, 4). Pupation
under aphid’s empty skin ............................................ 5
- Forewing RS + M vein absent (Fig. 5). Pupation inside
aphid mummy ............................................................. 9
5. Forewing m-cu vein not developed (Figs. 3, 9) ............ 6
- Forewing m-cu vein developed (Fig. 4) ....................... 7
6. Ratio of length to width at the level of the spiracles of
the petiole about 1.4 (Fig. 10). Stigma about 4.5 times
as long as wide (Fig. 9) .......... Praon spinosum Mackauer
- Ratio of length to width at the level of the spiracles of
the petiole 1.0–1.1 (Fig. 11). Stigma about 3.2–3.9
times as long as wide (Fig. 3) ..... Praon necans Mackauer
7. Forewing m-cu vein coloured throughout (Fig. 4). First
flagellomere brown or light brown ............................... 8
- Forewing m-cu vein colourless throughout (Fig. 12).
First flagellomere yellow ............. Praon yomenae Takada
194
8. Antennae 14–15-segmented. Lateral lobes of
mesonotum with hairless areas (Fig. 13) .................
............................................... Praon abjectum (Haliday)
- Antennae 17–18 (19)-segmented. Lateral lobes of
mesonotum densely pubescent (Fig. 14) ......................
................................................... Praon volucre (Haliday)
7. Forewing M and m-cu veins united forming M + m-cu
vein, completely developed (Fig. 5) ............................. 9
- Forewing M and m-cu vein only partly developed under
r-m vein (Fig. 15) or absent (Fig. 24) .......................... 15
9. Anterolateral area of petiole costate (Fig. 16) ............... 10
- Anterolateral area of petiole costulate (Fig. 17) or rugose
(Fig. 19) ...................................................................... 12
10. Antennae (16)-17-segmented. Forewing R1 vein clearly
shorter than stigma (stigma 1.6–2.0 times as long as
forewing R1 vein) (Fig. 5) ........................................... 11
- Antennae 15(16)-segmented. Forewing R1 vein
subequal to stigma (stigma 1.1–1.2 times as long as
forewing R1 vein) (Fig. 19) .... Aphidius colemani Viereck
11. Flagellomere 1, 2.5–3.0 times as long as wide at the
middle point (Fig. 20). Body generally dark .............
................................................. Aphidius avenae Haliday
- Flagellomere 1, 3.5–3.6 times as long as wide at the
middle point (Fig. 21). Body generally yellow to light
brown ............................ Aphidius transcaspicus Telenga
12. Anterolateral area of petiole costulate (Fig. 17).
Antennae 14–17-segmented ........................................ 13
- Anterolateral area of petiole rugose (Fig. 18). Antennae
18–19(20)-segmented .................. Aphidius ervi Haliday
13. Antennae 14–15-segmented. Maxillary palpus with
three palpomeres. Labial palpus with two palpomeres
......................................... Aphidius matricariae Haliday
- Antennae 16–17-segmented. Maxillary palpus with
four palpomeres. Labial palpus with three palpomeres
(sometimes second and third palpomeres undivided
and in that case labial palpus has two palpomeres) ....... 14
14. Stigma narrow, 4.00–4.50 times as long as wide
(Fig. 22). Petiole, 3.50–4.00 times as long as wide
........................... Aphidius rhopalosiphi De-Stefani Perez
- Stigma, about 3.50 times as long as wide
(Fig. 23). Petiole, 3.00–3.20 times as long as wide
................................................. Aphidius urticae Haliday
15. Forewing M and m-cu vein only partly developed under
r-m vein (Fig. 15) ......... Lysiphlebus fabarum (Marshall)
- Forewing M and m-cu vein absent (Fig. 24) ................ 16
16. Hypopygium of female without terminal accessory
prongs (Figs. 25, 26) ................................................... 17
- Hypopygium of female with terminal accessory prongs
(Fig. 27) ...................................................................... 21
17. Antennae 13–14-segmented. Forewing r & RS vein
short. Ovipositor sheath wide with gradually narrowing
at the top (Fig. 25) ...................................................... 18
- Antennae 12-segmented. Forewing r & RS vein
almost reach wing margin. Ovipositor sheath narrow,
needle like at the top (Fig. 26) ... Lipolexis gracilis Förster
Aphid parasitoids in wetland habitats
18. Maxillary palpus with four palpomeres. Second
flagellomere with 3–5 longitudinal placodes (Fig. 28)
......................................... Diaeretiella rapae (M´Intosh)
- Maxillary palpus with three palpomeres. Second
flagellomere without or with one longitudinal placodes
(Fig. 29) ...................................................................... 19
19. Distal abscissa of R1 equal or subequal to stigma length
(Fig. 24) ...................................................................... 20
- Distal abscissa of R1 at least for one third shorter than
stigma length (Fig. 30) ....... Diaeretellus palustris Sedlag
20. Antennae moderately thickened. Flagellomere 1, 3.3–
3.4 times as long as wide at the middle point (Fig. 31)
............................... Diaeretellus macrocarpus Mackauer
- Antennae thickened (Fig. 32). Flagellomere 1, 2.5–2.6
times as long as wide at the middle point (Fig. 33) .......
......................................... Diaeretellus heinzei Mackauer
21. Petiole with paired tubercles and with longitudinal
striations in proximal half (Fig. 34) ........................
.................................................. Trioxys auctus (Haliday)
- Petiole with two paired (primary and secondary)
tubercles and without longitudinal striations in
proximal half (Fig. 35) ............................................... 22
22. Distance between primary and secondary tubercles
shorter than width at spiracles (Fig. 35). Petiole and last
tergites dark brown. Ovipositor sheath sub-quadrate at
base (Fig. 36) ................. Binodoxys acalephae (Marshall)
- Distance between primary and secondary tubercles
longer than width at spiracles (Fig. 37). Petiole dark
brown to yellow. Last tergites yellow. Ovipositor sheath
rounded at base (Fig. 38) .. Binodoxys angelicae (Haliday)
Discussion
We documented over 66 tritrophic parasitoidaphid-plant associations from diverse wetland habitats
of western Palaearctic, comprising 24 parasitoid species, 24 aphid hosts and over 30 plant species, based
on records from 25 countries. Seven tritrophic associations of parasitoid species associated with aphids in
wetland habitats are new for science. About half of the
established tritrophic associations (34) are recorded
rarely, i.e. less than 10 times each, and as many as 16
parasitoid species are involved in them; some of these
species are themselves quite rarely encountered, while
others are relatively common, principally found on
hosts from other habitat types. The remaining associations were recorded considerably more frequently, and
6 associations have been documented more than 100
times each (based on 4 common and widespread aphidiinae species: Aphidius transcaspicus, Ephedrus plagiator, Lysiphlebus fabarum, Praon volucre).
The majority of the listed parasitoid species (16) are
involved in only 1–2 tritrophic associations, 7 species
are recorded in 3–5 associations, and one species (Praon
necans) is a member of even 16 different associations
based on wetland habitats. Only 6 parasitoid species
are involved in both rare and common/very common
association category. Generally, there is no obvious
difference between rare and common parasitoid
species with respect to the number of established
associations, i.e., even the widespread and relatively
polyphagous species are mainly represented with
small number of trophic relationships within wetland
habitats. Conversely, only some of the very common
and widespread parasitoids are involved in the most
frequently recorded associations. Therefore, the
dominant component of the aphid parasitoid trophic
networks in the western Palaearctic wetlands, as
observed at this coarse geographical scale, are mainly
the species not specific for this class of habitats; the
only exception is P. necans, which is a strictly wetland
species, involved in by far the largest number of
tritrophic associations (16), of which almost half are
moderately frequent and widespread.
Insect parasitoids operate at a high trophic level and
tend to be highly specialized (LaSalle & Gauld 1993).
According to Shaw and Hochberg (2001) these characteristics make them vulnerable. Therefore, given the
general trends of wetlands degradation, it is of interest
to consider the possible risks for the aphid parasitoid
trophic networks in this class of habitats. On the basis
of distribution, host range and host habitat specialization, three broad categories of aphid/parasitoids associations in wetland habitats can be recognized. The
first category comprises the associations of parasitoid
species whose distribution and aphid hosts are restricted to wetland habitats: Diaeretellus palustris, D.
macrocarpus, D. heinzei, D. ephippium, Praon necans, P.
spinosum and Trioxys auctus (the latter sometimes also
parasitizes R. padi in cereal crops – see Starý 1981).
Most of these species are relatively rarely sampled (van
Achterberg 2004; Tomanović et al. 2007), and for
some of them (Diaeretellus palustris, D. macrocarpus,
D. heinzei, D. ephippium), the listed records comprise
almost all the available data. Mainly due to the paucity
of occurrence, some of them can be regarded as taxonomically unresolved (Tomanović et al. 2006, 2007),
and accordingly, the knowledge of their idioecology is
completely lacking (Tomanović et al. 2007). Because
of their restricted host specialization, tightly associated
with endangered habitat types, these parasitoid species may be regarded as vulnerable to extinction. As
mentioned above, only one member of this host/habitat specialist group is a relatively common, widespread
and frequently encountered species (P. necans).
The second category is based on widely distributed
parasitoid species, with respect to both host and habitat type, but whose hosts in wetland habitats are only
the strictly wetland aphid species. We classified here
Aphidius colemani/ Rhopalosiphum nymphaeae, Aphidius
transcaspicus/ Melanaphis donacis, Aphidius matricariae/
195
Ž. Tomanovi, P. Starý, N. G. Kavallieratos, V. Gagi, M. Pleaš, M. Jankovi, E. Rakhshani, A. Ćetkovi & A. Petrovi
R. nymphaeae, Aphidius rhopalosiphi/ R. nymphaeae,
Aphidius urticae/ Schizaphis scirpi, Binodoxys angelicae/
Schizaphis sp., Diaeretiella rapae/ S. scirpi, Schizaphis
longicaudata, Ephedrus persicae/ A. affinis, Melanaphis
donacis, E. plagiator/ S. scirpi, Lysiphlebus fabarum/ R.
nymphaeae, L. gracilis/ S. scirpi and Praon yomenae/
Staticobium limonii associations. All these parasitoids
have relatively small populations in wetland habitats,
compared to the broad distribution of the other populations (Mackauer & Starý 1967). According to Unruh and Messing (1993) the small size of some iso-
lated populations can lead to reduced gene exchange
and can disrupt their genetic variability. In such cases
various environmental changes can cause their local
extinction. Some of these species are considered to be
represented by specialized wetland-aphid biotypes. In
certain cases, status of such biotypes is taxonomically
unresolved. Based on the COI mitochondrial gene, Kos
et al. (2011) found that haplotype of A. rhopalosiphi associated with R. nymphaeae/ T. latifolia showed genetic
isolation from other A. rhopalosiphi haplotypes.
Figures 25–33
25, Diaeretiella rapae, lateral aspect of ovipositor sheath; 26, Lipolexis gracilis, lateral aspect of ovipositor sheath; 27, Trioxys auctus, lateral aspect of last sternite
prong ♀; 28, Diaeretiella rapae, flagellomere 1 and 2 ♀; 29, Diaeretellus palustris, flagellomere 1 and 2 ♀; 30, Diaeretellus palustris, forewing ♀; 31, Diaeretellus
macrocarpus, flagellomeres 1 and 2 ♀; 32, Diaeretellus heinzei, antennae ♀; 33, Diaeretellus heinzei, flagellomeres 1 and 2 ♀.
196
Aphid parasitoids in wetland habitats
Finally, the third category comprises the associations
of widely distributed parasitoid species, whose aphid
hosts in wetlands are not particularly characteristic
only for these habitat types: Aphidius avenae, A. ervi,
A. transcaspicus, A. urticae, Binodoxys acalephae, B.
angelicae, Diaeretiella rapae, Ephedrus plagiator, Praon
abjectum, P. volucre.
Some of these wetland-based associations could
be of great importance for the agroecosystems maintenance, as reservoirs of aphid parasitoids relevant for
biological control of cereals and other crops. For example, Phragmites australis represents rather powerful
reservoir of Hyalopterus pruni attacked by Praon volucre and, less effectively, by Ephedrus plagiator in cooler
areas (at higher altitudes and latitudes) and Aphidius
transcaspicus in the southern warmer areas.
Aphids such as Rhopalosiphum nymphaeae,
Melanaphis donacis, Schizaphis scirpi, and Schizaphis
longicaudata are important alternative hosts for some
beneficial parasitoid species, and represent large
potential for biocontrol, since they do not attack any
cultivated plant (Kavallieratos et al. 2004; Starý 2006).
For example, R. nymphaeae is a reservoir for even
five parasitoids (Aphidius colemani, A. matricariae, A.
rhopalosiphi, Lysiphlebus fabarum and Trioxys auctus),
Schizaphis aphids are for the three (Lipolexis gracilis,
Ephedrus plagiator and Diaeretiella rapae), and M.
donacis is reservoir for the two (Aphidius transcaspicus
and Praon volucre). All these parasitoid species are well
known as effective natural enemies of some major
aphid pests in agroecosystems (Kavallieratos et al. 2004;
Tomanović et al. 2003, 2009), so the maintenance of
their presence in the neighboring wetland systems
may have significant effect on the control of pest
populations.
Further taxonomical and ecological investigation
of the composition and structure of aphid and aphid
parasitoid communities in wetland habitats are needed
to provide the knowledge necessary for the evaluation
of their pest/biocontrol potential, and also for the
conservation of this specific fauna.
Acknowledgments. We would like to thank Olivera PetrovićObradović (Faculty of Agriculture, University of Belgrade) for
aphid identification and Vladimir Žikić (Faculty of Sciences,
University of Niš) for technical assistance. This research was
partially supported by the Grant 043001 (The Ministry of
Science and Technological Development of the Republic of
Serbia) and the Entomology Institute project AV0Z50070508
(Academy of Sciences of the Czech Republic).
Figures 34–38
34, Trioxys auctus, dorsal aspect of petiole ♀; 35, Binodoxys acalephae, dorsal aspect of petiole ♀; 36, Binodoxys acalephae, lateral aspect of last sternite prong and
ovipositor sheath ♀; 37, Binodoxys angelicae, dorsal aspect of petiole ♀; 38, Binodoxys angelicae, lateral aspect of last sternite prong and ovipositor sheath ♀.
197
Ž. Tomanovi, P. Starý, N. G. Kavallieratos, V. Gagi, M. Pleaš, M. Jankovi, E. Rakhshani, A. Ćetkovi & A. Petrovi
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