DOI: 10.5281/zenodo.200402

7 (2) • December 2016: 75-82 12th SFSES • 16-19 June 2016, Kopaonik Mt

Reviev Article Received: 31 October 2016 Revised: 12 November 2016 Accepted: 24 November 2016

Plants and in interactions: multitrophic associations

Vladimir Žikić, Marijana Ilić Milošević, Maja Lazarević*, Saša S. Stanković

University of Niš, Faculty of Science and Mathematics, Department of Biology and Ecology, Niš, Serbia * E-mail: [email protected]

Abstract: Žikić, V., Ilić Milošević, M., Lazarević, M., Stanković, S.S.: Plants and insects in interactions: multitrophic associations. Biologica Nyssana, 7 (2), December 2016: 75-82. Studying a biological species, we are very often obliged to examine many other species which are directly or indirectly related to the particular species in order to have broader perspective of its being. Interactions between organisms can be perceived on various levels concerning biological study areas, such as ecology, physiology, morphology etc. In this place, the authors have given some peculiar examples concerning parasitism. This specific interaction is very common in the kingdom, having in mind that about a half of all known organisms are parasitic. The importance of this phenomenon is reflected on many aspects of life, propelling evolution and speciation of each member in the relation. Key words: parasitism, parasitoids, hosts, defending strategies

Apstrakt: Žikić, V., Ilić Milošević, M., Lazarević, M., Stanković, S.S.: Interakcije biljaka i insekata: multitrofičke asocijacije. Biologica Nyssana, 7 (2), Decembar 2016: 75-82. Proučavajući određene biološke vrste često smo primorani da izučavamo i mnoge druge koje su direktno ili indirektno povezane sa njom u cilju šireg sagledavanja njene celokupne biologije. Interakcije između organizama mogu biti proučavane na različitim biološkim nivoima, kao što su ekologija, fiziologija, morfologija itd. U ovom slučaju, autori su prezentovali neobične primere parazitizma. Ova specifična interakcija je veoma česta u životinjskom carstvu, imajući u vidu da skoro polovina poznatih organizama pripada parazitima. Značaj ovog fenomena se ogleda u mnogim aspektima života, podstičući evoluciju i specijaciju svakog člana posmatrane interakcije. Ključne reči: parazitizam, parazitoidi, domaćini, odbrambene strategije

Introduction branches, leaves, flowers, fruits and seed. Even dead plants or their parts can be of use for decomposing The vast majority of plants have evolved along with insects. Other connections between plants and insects insects. A lot of species directly depend on imply symbiosis or mutualism. plants which represent a resource for the whole, or at A specific relationship between plants and least a part of insects’ life cycle. In this trophic most insects is pollination; this particular act can be association plants can offer roots, bulbs, trunks, performed by hymenopterans, butterflies and moths,

75 BIOLOGICA NYSSANA 7 (2)  December 2016: 75-82 Žikić, V. et al.  Plants and insects in interactions… horned beetles, many flies etc., of which a great roots, petals or flowers, caused by insect or mite number represent very specialized forms as far as activities. Plant tissues show abnormal outgrowths their morphology or behaviour is concerned like tumours in . The most important gall- (B r o n s t e i n et al., 2006). For example, moths from inducing insects are gall wasps, Cynipidae the family Sphingidae are associated with plants (), gall midges Cecidomyiidae whose flowers have deep calyx forming tubes (Diptera), gall aphids Aphididae (Hemiptera) and (F a e g r i & v a n d e r P i j l , 1979; H a b e r & some species from the group of leaf-miner flies, F r a n k i e , 1989). Hovering around the plants these Agromyzidae (Diptera) (e.g., S p e n c e r , 1973; moths suck nectar through a very elongated S t o n e et al., 2002; Y u k a w a & R o h f r i t s c h , proboscis. This type of feeding is not unique in the 2005; F l o a t e , 2010). Galls and cecidia arise after animal world; convergent evolution has appeared females inject cecidogenous fluid, along with egg, in four times in non-related nectar feeders. In mammals, the plant tissue, e.g. Tenthredinidae (Hymenoptera) bats are a very good example, while among birds (K o p e l k e , 1998). Afterwards, parasite larvae force there are hummingbirds, and also two groups of the neighbouring plant cells into gall to start the insects: hoverflies (Diptera: Syrphidae) and hawk division process of meristems. Parasites use the galls moths (K i t c h i n g , 2002). The list of attended as their habitat and shelter; also exploiting the sugars plants is huge, ranging from those with small flowers accumulated in it, they also use the galls as a food with short calyx such as Verbena L., Lantana L., source (L a r s o n & W h i t h a m , 1991). Lobelia L. and Buddleja L., over Petunia Juss. or A very bizarre relationship between plants and Nicotiana L., and furthermore to plants with very insects is found in carnivorous plants such as Drosera large flowers with deep calyx such as various species L., Nepenthes L., Sarracenia L. or Dionaea of Datura L. or Darwin orchid, Angraecum muscipula Ellis that “consume” insects. Leaves of sesquipedale Thouars with a calyx which is 30 cm those mainly bog inhabiting plants form traps, deep. Otherwise, the group of solitary bees usually pitfalls, filled with water and enzymes (Megachilidae), e.g., Eucera longicornis (L.), some (phytotelmata). All kind of traps in carnivorous digger wasps (Crabronidae) and some mining bees plants are supplied with attractive colour, odour and (Andrenidae) specialize in the pollination of various specialized nectary glands. Those glands produce orchids imitating the females; in the first place from sweet smelling nectar to attract and catch insects later the genus Ophrys L. (W i l l m e r , 2011). For many digesting them, using externally excreted enzymes. snapdragon species the only solution of being In this way, plants obtain minerals from insect’s pollinated was to establish an intimate relation with body, since the boggy soil is poor. Once those plants some bumblebees which are capable to open the have to be pollinated, they need insects again. Then, “lips” of the flowers using their strong hind legs (e.g., carnivorous plants suspend all the attractants in their O d e l l et al., 1999). traps, focusing on their flower equipment in order to Myrmecochory is a special kind of ant-plant attract pollinators. This convergent behaviour interaction where ants are engaged in seed dispersal. evolved independently in both dicotyle and For this purpose myrmecochorous plants shaped their monocotyle plant lineages, terrestrial and underwater seeds to carry elaiosomes, various external plants (A l b e r t et al., 1992). appendages rich of nutrients such as lipids, amino acid, or other attractive substances to ants (G i l a d i , Plants, hosts and parasitoids 2006). Some stick insects (Phasmida) have taken advantage of this ant activity by producing seed-like Predators, parasites and parasitoids have an indirect eggs which are carried by ants into their nests where connection with plants via their herbivorous pray or the conditions are favourable for their development host which is essential for their life cycles (P r i c e et (C o m p t o n & W a r e , 1991; S t a n t o n et al., al., 1980; S t o t z et al., 1999). In the case of insect 2015). In Central America there is an example of true parasitoids, the host is usually required during the symbiosis between ants and plants. The acacia ant – larval stage. The plant role in this play is to Pseudomyrmex ferruginea F. Smith, lives in small unintentionally help the host to become less attractive colonies in the base of the horns of the bullhorn or even poisonous for its enemies. The six-spot acacia – Vachellia cornigera (L.) finding a shelter burnet, Zygaena filipendulae L. is capable of there, but at the same time offering protection to its sequestering alkaloids from the food plant Lotus host (J a n z e n , 1967; P i p e r , 2007) as ants attack corniculatus L. In this cases the cyanogenic all approaching animals and plants by stinging them. glucoside linamarin, also lotaustralin are A specific way of insect parasitism takes place biosynthesized in poison thus decreasing predation of in galls. Galls or cecidia are transformations of plant larvae and adults (D a v i s & N a h r s t e d t , 1979; parts (external tissues) such as leaves, branches, Z a g r o b e l n y et al., 2007). This poison protects a

76 BIOLOGICA NYSSANA 7 (2)  December 2016: 75-82 Žikić, V. et al.  Plants and insects in interactions… very high percentage of adult moths while larvae still paralyse the host, and they are capable of regulating remain exposed for various parasitoids such as its behaviour and life cycle until they reach maturity various hymenopterans and tachinids (Tachinidae: (D e s n e u x et al., 2009). Usually, parasitoid larva Diptera) (Ž i k i ć et al., 2013). kills the host at the end of its larval stage. An example The great majority of parasitoid insects belong of ectoparasitic koinobionts is an ichneumonid wasp to the Hymenoptera insect order. With some Acrodactyla quadrisculpta (Gravenhorst) which exceptions, they come from the division Parasitica. parasitizes a spider, Tetragnatha montana Simon Parasitoid members of the other division Aculeata, (M i l l e r et al., 2013). The majority of koinobionts are in minority and their kind of parasitism is a little represent endoparasitoids, which develop inside the different (e.g., Chrysididae, Sphecidae, etc.) host body. In some cases, such as the species (W c i s l o et al., 1985; Winterhagen , 2015). Macrocentrus Curtis (Braconidae), the female lays The second important group of parasitoids are only one egg in the host body which undertakes the tachinid flies (Feener & Brown, 1997); also, there are process of polyembryony and ultimately gives some sporadic cases in Coleoptera, Lepidoptera, dozens of individuals which are genetically the same Trichoptera, Neuroptera and Strepsiptera (P i e r c e , (clones) and thus increasing its parasitic capacity 1995; H e r a t y , 2009). A simple association (H o w a r d , 1906; C u s h m a n , 1913; P a r k e r , between a plant (primary food producer), an 1931; Q u i c k e , 2014). Another strategy of herbivorous host (primary food consumer) and a increasing parasitic capacity can be seen in parasitoid (secondary food consumer) is being gregarious parasitoids (e.g., Eulophidae, Encyrtidae, considered through trophic chains; this threesome is Braconidae) where females lay a couple of eggs per usually referred to as a tritrophic association. Higher host, but their offspring is not genetically the same trophic levels with more members include more than and both sexes are developed (Q u i c k e , 2014). one parasitoid species and also hyperparasitoids Multitrophic associations usually include primary food consumer forming a multitrophic hyperparasitoids, the species that parasitize primary association. Parasitoid larvae are carnivorous, parasitoids. However, the hyperparasitism does not feeding outside or inside the host body. Conversely, end here; on the highest level of trophic chains we are adults are free living organisms feeding on flowers talking about hyperparasitoids of the second and the (nectar) or honeydew produced by green aphids. The third level. Clearly, in the trophic chain with a final effect of host-parasitoid interaction is death of maximum number of members in a raw is consisted the host, which makes these organisms very powerful of: 1) primary food producer (plant), 2) primary food biological weapon. Nowadays, several companies consumer (host), 3) secondary food consumer have developed technologies for commercial (primary parasitoid), 4) tertiary food consumer production of a few dozen parasitoid species on (secondary parasitoid = primary hyperparasitoid), 5) artificial nutrient medium. Those species are quaternary food consumer (tertiary parasitoid = applicable both in open fields as well as in secondary hyperparasitoid) and 6) quinary food greenhouses (O l k o w s k i et al., 2003; H a l e & consumer (quaternary parasitoid = tertiary H e n s l e y , 2010). hyperparasitoid). H a r v e y et al. (2009) explained There are various classifications of parasitoids this phenomenon working on the wasp Cotesia based on different criteria concerning their glomerata (L.) (Braconidae) as a primary parasitoid behaviour, life cycle or number of eggs laid per single which is hyperparasitized by Lysibia nana host. On the basis of oviposition location parasitoids Gravenhorst () which is a secondary can be ecto- or endoparasitoids; whether or not parasitoid. Furthermore, the species L. nana was parasitoid larvae alter hosts behaviour they could be hyperparasitized by another ichneumonid wasp Gelis idiobionts or koinobionts accordingly; according to agilis (Fabricius), appearing as a tertiary parasitoid. the number of eggs laid per host there are two cases, Finally, there are some other species from the same solitary (a single egg per host) or gregarious (usually genus, Gelis attack G. agilis. Interspecific parasitism few to more than a hundred eggs laid per host) is considered in more details in S u l l i v a n (1987). (G o d f r a y , 1994). Ectoparasitoids lay their eggs on A kind of parasitism which is known as the host body surface. If the female causes a kleptoparasitism is the interaction where one animal permanent paralysis of the host and parasitoid larvae takes food from another. In parasitoids feed outside the host body, those species represent kleptoparasitism occurs in cuckoo wasps idiobionts (many Ichneumonidae and some (Chrysididae). The cuckoo wasp Omalus Panzer is Braconidae). On the contrary, if the host continues its the parasitoid of the larvae of another hymenopteran life after the larvae have been hatched on its body, family, Crabronidae (Winterhagen , 2015). This those parasitoids are considered as koinobionts. species does not oviposit directly in crabronid larva, Those are parasitoids which only temporarily but in aphids, even though an aphid is many times

77 BIOLOGICA NYSSANA 7 (2)  December 2016: 75-82 Žikić, V. et al.  Plants and insects in interactions… smaller than the cuckoo wasp larva. Crabronid secondarily as a result of plant responses that produce females collect the aphids and carry them in a toxins and repellents against pests and also previously made nest to serve as food for their larvae. antibiotics against pathogens. Studying olfactory Accidentally, a crabronid female picks up a physiology and behaviour of a predaceous beetle parasitized aphid with the egg of a cuckoo wasp Thanasimus formicarius (L.) (Coleoptera: Cleridae), which has been laid inside its body. In this way a the authors Z h a n g & S c h l y t e r (2010) showed crabronid wasp brings the parasitoid in its own nest. that the specific chemical substances from other non- Ultimately, when the cuckoo wasp larva emerges target hosts and plants, which are not even a part of from its egg and then from the aphid body, it starts the particular trophic association, can inhibit the looking for food devouring the crabronid larva, and attraction of chemical signals of attacked host/prey. also the collected aphids. In other words, neighbouring target plants resort to Exceptions exist in almost every group of mimicry, thus stopping to smell out, becoming less sibling organisms. Well know example of exception attractive for pests. is panda – being herbivore among the mammal’s The other way of plant communication is order Carnivora. Similarly, among the large groups through soil. They can do that directly by roots, or of Parasitica, there are some exceptions as well; many most often using an “internet” made of fungi. By species of the family Agaonidae (fig wasps) have linking to the fungal network, plants exchange developed a unique mutualistic association with information, nutrients and toxic chemicals with their various Ficus L. trees, and more specifically with neighbours (S o n g et al., 2010). Mutually-beneficial their flowers. The odour released from the fig flowers relationships between plants and fungi, known as (syconium) attracts a fertilized female wasp to enter mycorrhiza can be found in a great majority of plants. the syconium through a tiny opening in the centre. In this way, the wasp is carrying pollen from the flower Host-parasitoid coevolution from which it emerged. However, the main reason of its presence is to lay eggs in fig’s female flowers Under the pressure of parasitoids, hosts develop turning a syconium to a fig fruit (K j e l l b e r g et al., various defending strategies (Kraaijeveld et al., 2005). 1998). A simple type of protection that females use for their offspring is laying eggs in hidden places. For Plant defending strategies and plant example, some Siricidae (Hymenoptera: Symphyta) communications have very long and strong ovipositors with which they drill wood and lay their eggs deep inside it, thus There is a secret language in which plants minimizing the chance of their larvae to be communicate with each other in many ways (e.g., parasitized. Some other species, such as sawflies allelopathy) (B a l u š k a & N i n k o v i ć , 2010). (Hymenoptera: Argidae and Tenthredinidae) saw Modern definition of allelopathy is “chemical plant stems where they will oviposit. In Symphyta interactions that involve toxic allelochemicals and there are also the species causing leaf mines or galls should be distinguished from plant chemical as it was previously explained (H a w k i n s , 1988; communication” (S c h e n k et al., 1999; S c h e n k H e r i n g , 2013). & S e a b l o o m , 2010). A way of emanating The immune system can protect the host evaporative chemical signals via air is the one that is against parasitoids to varying degrees best investigated (V e t & D i c k e , 1992; B r u c e et (Kraaijeveld & G o d f r a y , 1999; C a r t o n et al., 2005). F o w l e r & L a w t o n (1985) found that al., 2008). In a process of encapsulation hosts can the chemicals are a blend of organic molecules such eliminate parasitoids, forming a multi-layered cyst as alcohols, aldehydes, ketones and esters which are made of hemocytes. The hemocytes found in insect’s known as volatile organic compounds (VOCs) also hemolymph are cells with the phagocyte function called kairomones (more recent, semiochemicals). (G o d f r a y , 1994). Recent studies reveal that plants as the lowest trophic Endosybionts are present in many living level, when attacked by herbivores such as aphids, beings, irrespective of whether they are algae, plants, scale insects or caterpillars, emit any substance fungi or animals. These are organisms that live within produced by an individual of one species that benefits the body or cells of other organisms. The most both the producer and the recipient which is of a famous examples of endosymbiosis are nitrogen- different species - synomones which attract natural fixing bacteria associated with legume roots (Franche enemies i.e. parasitoids and predators in order to et al., 2009), single-cell algae living in reef-building defend themselves (V e t & D i c k e , 1992; corals (R o w a n , 1998) and in some Turbellaria T u r l i n g s et al., 1995). This group of authors also (B a r n e a h et al., 2007), or some protists and revealed that the signalling role probably evolved prokaryotes which inhabit the intestine of termites

78 BIOLOGICA NYSSANA 7 (2)  December 2016: 75-82 Žikić, V. et al.  Plants and insects in interactions…

(O h k u m a , 2008) and other wood-consuming that many details are concealed or maybe beyond our insects. There are also bacterial endosymbionts that reach, the accumulated knowledge and permanent protect host insects, e.g., aphids against parasitoids. investigation of this topic has provided us with many Bacteria from the genus Buchnera overproduce benefits. The most useful is pest management and tryptophan (plasmid borne enzyme) and other amino using biocontrol agents to combat pest insects. This acids that minimize the exposure of aphids to has some serious repercussions in healthier food parasitoids (R o u h b a k h s h et al., 1997). production and sustainable agriculture. Hamiltonella defensa is a species of bacteria, that “Let it be borne in mind how infinitely lives as an endosymbiont of aphids (most studied is complex and close-fitting are the mutual relations of the pea aphid – Acyrthosiphon pisum Harris) all organic beings to each other and to their physical providing its host protection against parasitoids. conditions of life” (D a r w i n , 1872). Mechanism of protection implies that H. defensa is Acknowledgements. We would like to thank to the infected with temperate bacteriophages called th Acyrthosiphon pisum secondary endosymbionts organisation board of the 12 Symposium on the Flora of South-eastern Serbia and Neighbouring Regions, (APSEs) (v a n d e r W i l k et al., 1999; Kopaonik Mt. Review of English language was done by V o r b u r g e r , 2014). Those bacteriophages encode Antonis Mylonopoulos, Komotiní, Greece. We also thank different toxin genes killing the parasitoid eggs or to Dr. Andjeljko Petrović for the selection of references to larvae thus protecting the aphid host (D e g n a n & write this manuscript. The authors participate in the project M o r a n , 2008). Endosymbiotic male-killing of the Ministry of Education, Science and Technological bacteria from the genera Wolbachia and Rickettsia Development of the Republic of Serbia, grant no. eliminate only the male sex in parasitoid embryos III43001.This study is partly supported by EU project defined by genetics. It is not yet clear why males are BIOCOMES (FP7-KBBE-2013-7). more sensitive to Wolbachia; it might be due to the fact that they have only one X chromosome or References because they lack the whole garniture of chromosomes (haploids) (e.g., H u r s t & J i g g i n s , Albert, V.A., Williams, S.E., Chase, M.W. 1992: 2000; K o n d o et al., 2002; B e l s h a w & Carnivorous plants: phylogeny and structural Q u i c k e , 2003; W e r r e n at al., 2008). evolution. American Association for the Parasitoids also have evolved a variety of Advancement of Science, 257 (5076): 1491-1495. strategies to overcome host immune responses, but Baluška, F., Ninković, V. 2010: Plant on the other hand they developed strategies to defend communication from an ecological perspective. themselves against hyperparasitoids. 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