NORTH-WESTERN JOURNAL OF ZOOLOGY 14 (2) ©NWJZ, Oradea, Romania, 2018 CORRESPONDENCE - Notes http://biozoojournals.ro/nwjz/index.html
Ant species dispersing the seeds of the bearing seeds of S. colchiciflora (Fig. 1.A) are dispersed by myrmecochorous Sternbergia colchiciflora ants (Pénzes 1934), the identity of seed-dispersing ant spe- cies participating in the process has remained unknown. The (Amaryllidaceae) aim of our study was to assess which ant species are respon-
sible for myrmecochorous seed dispersal in this rare and The evolutionary and ecological importance of myrme- threatened plant species. Our paper provides the first data cochory (ant-mediated seed dispersal in plants) has become on association of this threatened plant species and the elaio- increasingly evident (Lengyel et al. 2009, 2010). Neverthe- some predatory ant species that are engaged/involved in the less, myrmecochory is likely the most understudied of the seed dispersal. main seed dispersal syndromes (Bronstein et al. 2006) and its research is highly challenging (Bologna et al. 2017). In most Thirty localities of Sternbergia colchiciflora (27 in Hungary, three in cases, myrmecochorous seed dispersal of plants was as- Serbia) have been visited in 2017 during the fruiting season (from 25 sumed based on morphological traits: presence of elaiosome, April to 19 May) to detect ant-mediated seed dispersal events. Every a lipid-rich appendage on the seed (Lengyel et al. 2010), ant individual that was observed to carry seeds of S. colchiciflora has rather than on direct observations on seed dispersal events. been collected. The collected material was stored in 50% EtOH in unique vials until determination. All ants have been identified based Consequently, the specificity of this ant-plant interaction on keys by Seifert (1996) and Seifert & Galkowski (2016). We took remains largely unexplored. However, myrmecochory may morphological measurements using an Olympus SZX9 stereomicro- play a significant role in shaping the distribution and sur- scope at a magnification of 100×. vival of plants. Understanding the mechanisms of myrme- cochory is especially important in case of rare and threat- Seed dispersing ants were detected in seven Hungarian lo- ened plant species, because conservation of their population calities. Five ant species (Camponotus piceus, Lasius alienus, is not possible without collateral conservation of ant popula- Lasius bombycina, Lasius fuliginosus and Tapinoma erraticum) tions. were observed to disperse the seeds of S. colchiciflora (Table Sternbergia colchiciflora Waldst. & Kit. (Amaryllidaceae) is a 1.). bulbous geophyte distributed from North Africa through Although fruiting plants were abundant in most localities, Southern Europe and Asia Minor to the Caucasus and ants were observed only on a few plant individuals. How- Ukraine (Pasche & Kerndorff 2002). The species is consid- ever, foraging ants were detected in large numbers on these ered rare or sporadic in many countries within the distribu- highly attractive fruits (Fig. 1.B & C). Ant workers were tion area. It is listed on CITES (Washington Convention) found on 3–7 cm high fruits with ripening, yellowish peri- Appendix II [web1]. carp. Ants removed the seeds from the rifts of ripening fruits Although it has long been known that the elaiosome- and carried them one by one.
Figure 1. Seeds of Sternbergia colchiciflora (A) and its ant dispersers: B – Lasius alienus (Várpalota-Inota). C – Camponotus piceus (Tihany). Photo credits: A–B: A. Molnár V., C – A. Mészáros. Scale bars represent 10 millimetres.
Table 1. Ant-mediated seed dispersal events in Sternbergia colchiciflora in 2017. Observers are indicated by abbreviations of their names (see authors).
Day/ Quantity of seed Settlement: Locality Observer Ant species (Subfamily) Month carrying ants observed Tihany: Diósi-medows AM 25.04. Camponotus piceus (Leach, 1825) (Formicinae) Numerous workers Pécsely: Klárapuszta AM 25.04. Várpalota-Inota: graveyard AMV 30.04. Lasius alienus Förster, 1850 (Formicinae) Numerous workers Várpalota-Inota: graveyard AMV 02.05. Csór: graveyard AMV 02.05. Tapinoma erraticum (Latreille, 1798) (Dolichoderinae) Single worker Makó: Montág-puszta GB 15.05. Numerous workers Lasius bombycina Seifert & Galkowski, 2016 (Formicinae) Pusztaföldvár: graveyard AMV 13.05. Few workers Battonya: Tompapuszta AICs 19.05. Lasius fuliginosus (Latreille, 1798) (Formicinae) Single worker
266 Correspondence –Notes
Our study provides the first data on ant species that dis- ideal seed dispersal agents, each detected species is domi- perse the seeds of S. colchiciflora. Four out of the five ant spe- nant and abundant in sites with certain bedrock properties. cies observed to remove seeds of S. colchiciflora are known to Because seed maturity may or may not coincide with the disperse elaiosome-bearing seeds of different plants [C. larval biomass peak, other species can also play a role in piceus (Manzaneda et al. 2007, Bas et al. 2009), L. alienus seed dispersal, although probably to a smaller extent. Our (Culver & Beattie 1978, Beattie et al. 1979), Lasius fuliginosus results, however, agree with previous reports that typically (Reifenrath et al. 2012), T. erraticum (Garrido et al. 2002, only one or only a few ant species disperse most of the Manzaneda et al. 2007)]. Seed removal activity of the re- myrmecochorous seeds in any given locality (Rico-Gray et cently described (Seifert & Galkowski 2016) Lasius bombycina al. 2007). Future studies are thus essential before we can is reported here for the first time. fully understand the nature and specificity of ant-mediated Although these omnivorous ant species obviously play a seed dispersal. role in seed dispersal in Sternbergia, we speculate that the in- teractions between S. colchiciflora and these ants are faculta- Acknowledgement. This research was supported by OTKA K108992 tive. Myrmecochory is a mutual interaction between plants Grant. and ant species (Bronstein et al. 2006). Myrmecochorous References plant species increase their dispersal ability by attaching Bas, J.M., Oliveras, J., Gómez, C. (2009): Myrmecochory and short-term seed lipid and protein-rich elaiosomes to the seeds that are attrac- fate in Rhamnus alaternus: Ant species and seed characteristics. Acta tive to ants. Both lipids and proteins are essential sources of Oecologica 35: 380-384. Beattie, A.J., Culver, D.C., Pudlo, R.J. (1979): Interactions between ants and the nutrients for developing ant larvae, hence elaiosomes con- diaspores of some common spring flowering herbs in West Virginia. taining these components in a larger proportion are highly Castanea 44: 177-186. preferred by foraging ant workers at the peak of larval pro- Bologna, A., Toffin, E., Detrain, C., Campo, A. (2017): An automated method for large-scale monitoring of seed dispersal by ants. Scientific Reports 7: 40143. duction, in the spring. After removing the elaiosomes, ants Bronstein, J.L., Alarcon, R., Geber, M. (2006): The evolution of plant–insect drop the seeds, which remain fertile, far from the parental mutualisms. New Phytologist 172: 412-428. plant (e.g. waste disposal area), where the seed can germi- Culver, D.C., Beattie, A.J. (1978): Myrmecochory in Viola: dynamics of seed-ant interactions in some West Virginia species. Journal of Ecology 66: 53-72. nate. The benefits of this interaction are obvious for each Garrido, J.L., Rey, P.J., Cerdá, X., Herrera, C.M. (2002): Geographical variation side. Our observations showed that the presence of elaio- in diaspore traits of an ant – dispersed plant (Helleborus foetidus): are ant somes on the seeds did not attract workers from a distance, community composition and diaspore traits correlated? Journal of Ecology 90: 446-455. because upon the first finding of seeds, ants contacted all Gómez, C., Espadaler, X. (1998): Myrmecochorous dispersal distances: a world parts of the seed equally. Although ants are mass-recruiting survey. Journal of Biogeography 25: 573-580. species, we never observed any recruitment or trail-laying Gorb, S.N., Gorb, E.V. (1999): Effects of ant species composition on seed behaviour towards seeds. Upon contacting seed items, the removal in deciduous forest in eastern Europe. Oikos 84: 110-118. Lengyel, Sz., Gove, A.D., Latimer, A.M., Majer, J.D., Dunn, R.R. (2009): Ants antennation, manipulation and seed retrieval behaviour of sow the seeds of global diversification in flowering plants. PLoS One 4: ants strongly varied depending on the species. e5480. All ant species detected as seed dispersal vectors of S. Lengyel, Sz., Gove, A.D., Latimer, A.M., Majer, J.D., Dunn, R.R. (2010): Convergent evolution of seed dispersal by ants, and phylogeny and colchiciflora, except for Lasius fuliginosus, prefer open, ther- biogeography in flowering plants: a global survey. Perspectives in Plant mophilous habitats, although there are remarkable differ- Ecology, Evolution and Systematics 12: 43-55. ences in their habitat preference within this broad category. Manzaneda, A.J., Rey, P.J., Boulay, R. (2007): Geographic and temporal variation in the ant–seed dispersal assemblage of the perennial herb L. alienus occurs in grasslands, on limestone or dolomite bed- Helleborus foetidus L. (Ranunculaceae). Biological Journal of the Linnean rock, whereas L. bombycina is abundant on loess substrates. Society 92: 135-150. Our results provide some evidence for the phenological Pasche, E., Kerndorff, H. (2002): Die Gattung Sternbergia Waldst. & Kit. (Asparagales, Amaryllidaceae) im Vergleich, unter besonderer matching of seed production/maturation in S. colchiciflora Berücksichtigung der wiederentdeckten Sternbergia schubertii Schenk. Stapfia and the seed dispersal activity of ants. The time period of 80: 395-416. seed maturation (end of April and early May) in S. colchi- Pénzes A. (1934): Termés-ökológiai megfigyelések. Botanikai Közlemények 31: ciflora coincides with the peak of the larval biomass of both 28-35. Reifenrath, K., Becker, C., Poethke, H.J. (2012): Diaspore trait preferences of Lasius alienus and L. bombycina. The nuptial flight of these ant dispersing ants. Journal of Chemical Ecology 38: 1093-1104. species takes place in July to September (Seifert 1992), so in Rico-Gray, V., Oliveira, P.S. (2007): The ecology and evolution of ant-plant next May, their colonies contain rapidly growing sexual lar- interactions. University of Chicago Press, Chicago. Seifert, B. (1992). A taxonomic revision of the Palaearctic members of the ant vae. These species may thus be considered a principal con- subgenus Lasius s.str. (Hymenoptera: Formicidae). Abhandlungen and tributor to seed dispersal in Sternbergia. In contrast, the asso- Berichte des Naturkundemuseums Görlitz 66(5): 1-67. ciation of S. colchiciflora and the arboricular Lasius fuliginosus Seifert, B. (1996): Ameisen, bestimmen, beobachten. Naturbuch Verlag, Berlin. Seifert, B., Galkowski, C. (2016): The Westpalaearctic Lasius paralienus complex might be accidental. This species nests in forests (mostly (Hymenoptera: Formicidae) contains three species. Zootaxa 4132: 44-58. Populus spp.) and its nuptial flight takes place in May, thus, Servigne, P., Detrain, C. (2008): Ant-seed interactions: combined effects of ant mostly pupae or imagos can be found in the nest at the time and plant species on seed removal patterns. Insectes Sociaux 55: 220-230. ***** Web resource: web1 - CITES -
Attila V. MOLNÁR1*, András MÉSZÁROS2, Chalcididae, whose known hosts encompass Lepidop- András István CSATHÓ3, Gábor BALOGH3 tera, Diptera, Hymenoptera, Coleoptera, Neuroptera and and Sándor CSŐSZ4 Strepsiptera, are primary parasitoids, but few species are facultative or obligatory hyperparasitoids (Bouček 1982, Lot- 1. Department of Botany, University of Debrecen, falizadeh et al. 2012, Aydoğdu 2014, Lotfalizadeh & Jafari- H-4032 Debrecen, Egyetem tér 1, Hungary. 2. Balaton-Upland National Park Directorate, Nadushan 2015). In spite of its high economic importance, H-8229, Csopak, Kossuth utca 16, Hungary. Chalcididae is poorly known in the Middle East; only 61 3. Körös-Maros National Park Directorate, species from Iran (Lotfalizadeh et al. 2012, Kazemi & Lotfali- H-5540, Szarvas, Anna-liget 1, Hungary. 4. MTA-ELTE-MTM, Ecology Research Group, zadeh 2014, Tavakoli Roodi et al. 2016), 41 species from Tur- H-1117 Budapest, Pázmány Péter sétány 1/C, Hungary. key, 31 species from Israel and five species from Iraq are *Corresponding author, A.V. Molnár, E-mail: [email protected] known (Noyes 2017). This communication is the second publication of the au-
thors’ investigation on the Chalcidoidea of Khuzestan prov- ince in South-Western Iran (Moravvej et al. 2016), which ex- On the presence of the subfamily Epitraninae clusively reports a new subfamily for the fauna of Iran, viz. (Hymenoptera: Chalcidoidea, Chalcididae) Epitraninae of the family Chalcididae. in Iran Collecting and preserving methods were introduced in our first contribution (Moravvej et al. 2016). Terminology The family Chalcididae (Hymenoptera: Chalcidoidea) con- follows Bouček (1982). tains five subfamilies (Noyes 2017) only three of which have been reported from Iran (Lotfalizadeh et al. 2012). It contains Systematics 61 species in 16 genera including Chalcidinae with 37.7% of Epitraninae Burks, 1936 species, Dirhininae with 8.2% of species and Haltichellinae Epitraninae includes only the genus Epitranus with 68 nomi- with 54.1% of species (Tavakoli Roodi et al. 2016). nal species (Noyes 2017) which are probably native of the
Old World and were introduced to Nearctic and Neotropical (Fig. 1E); forewing hyaline with strongly reduced pilosity regions (Bouček 1982). The hosts of Epitraninae are also little (Fig. 1G), virtually absent below marginal vein, especially known but records suggest they parasitize lepidopterous not forming any distinct hairline recurrent from stigmal pests associated with stored products such as Tineidae and vein, venation distinct, pigmented, costal cell about 2 times Pyralidae (Bouček 1982). as long as marginal vein. Biology of our examined specimens is unknown in Iran, Genus Epitranus Walker, 1834 but outside it has been recorded from Tinea sp., T. antricola Epitranus clavatus (Fabricius, 1804) (Figs. 1A-G) Meyrick, T. palaechrysis Meyrick and Crypsithyris sp. (Lepi- Chalcis clavata Fabricius, 1804 doptera, Tineidae) (Noyes 2017) thus, its hosts seem to be Epitranus falvescens Walker, 1834 small Lepidoptera, possibly associated with some tropical, Epitranus lacteipennis Cameron, 1883 probably stored products (Bouček 1982). Anacryptus insidiosus Masi, 1917 Geographical distribution: This species has been recorded Anacryptus anpingius Masi, 1933 from Oriental (India, Malaysia Taiwan), Nearctic (USA) and Anacryptus cawnporensis Mani & Dubey, 1973 Neotropical (Brazil, Guyana) regions (Bouček 1982, Noyes 2017); this is a new record of species from Iran. Our finding Material Examined: Iran, Khuzestan province, Ahwaz, of this species from southern part of Iran (Khuzestan) that Chamran University campus, July 2017, Yellow pan trap, S. located between Oriental and Afrotropical regions seems A. Moravvej leg., 1 ♀. Deposited in the Insect Collection of ordinary. Bouček (1982) believes this species is native in the Chamran University, Ahwaz. Old World tropics, possibly in South Asia, but was Diagnostic features: Body mainly reddish (Fig. 1A), with repeatedly introduced to parts of tropical America. some slightly dark parts; thorax with regular punctuations (Fig. 1D), without patches of hairs, interspaces finely granu- Acknowledgements. We would like thank Research Deputy of late or partly obliterated; hind femur with fewer than 15 Shahid Chamran University for financial help and reviewers for the teeth which are relatively broader and less regular than in comments on the manuscript. albipennis and nitens, hind tibia with strong angulate subba- References sal tooth, crenulate under hairs and tarsal sulcus with dis- Aydoğdu, M. (2014): Parasitoid abundance of Archips rosana (Linnaeus, 1758) tinct oblique carina, extending over more than 3/4 up to- (Lepidoptera: Tortricidae) in organic cherry orchards. North-Western Journal of Zoology 10(1): 42-47. wards subbasal tooth (Fig. 1F); hind coxae ventrally with Bouček, Z. (1982): Oriental chalcid wasps of the genus Epitranus. Journal of very coarse but not very dense punctuations (Fig. 1A); pro- Natural History 16: 577-622. podeum dull, with distinct granulate sculpture, also intersti- Kazemi, M.-H., Lotfalizadeh, H. (2014): Hockeria magna Bouček (Hymenoptera: Chalcididae): New record to Iranian chalcidid fauna. North-Western Journal ces on thorax (at least partly) and bottoms of punctures with of Zoology 10 (1): 183-186. distinct reticulation, propodeal areolae very dull with reticu- Lotfalizadeh, H., Ebrahimi, E., Delvare, G. (2012): A contribution to the lation, but thorax and occiput slightly shiny; in female peti- knowledge of family Chalcididae (Hymenoptera: Chalcidoidea) in Iran. ole dorsally flattened and only up to 3 times as long as broad Journal of Entomological Society of Iran 31(2): 67-100.