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Ukrainian Journal of Ecology
UkrainianJournal of Ecology, 2017, 7(2), 120-123, doi: 10.15421/2017_28
SHORT COMM UNICA TI ON UDC592.18 (470.56)
Parasites, predators and diseases of Lady Beetles (Coleoptera, Coccinellidae) of the Southern Urals and adjacent territories
1Tyumaseva Z.I., 2Guskova E.V.
1 South Ural State Humanitarian Pedagogical University, Lenina 69, Chelyabinsk, RU-454080, Russia 2Altai State University, Lenina 61, Barnaul, RU-656049, Russia E-mail:1 tyumase vazi@mail. r ; 2guskovael@mail. ru
The article gives a review of the Coccinellidae natural enemies (birds, amphibians, insects, mites, fungi, nematodes). Groups of animals that can influence the Coccinellidae population dynamics are identified. The stomachs of frogs Pelophylax ridibundus (Pallas, 1771), Rana temporaria Linnaeus, 1758, Rana arvalis Nilsson, 1842, Rana amurensis Boulenger, 1886, Pelobates fuscus (Laurenti, 1768) have been examined; the occurrence of various Coccinellidae species in the stomachs is evaluated. Key words: Coccinellidae, Coleoptera, Parasites, Population dynamics, Southern Urals.
Introduction
Coccinellidae were among the first to be used in the biological control, and in many cases, due to them, a significant progress was achieved in regulating the number of insect pests of forest, agricultural, ornamental and greenhouse plants (Portchinsky, 1912; Mejer, 1937; Yakhontov, 1950; Dyadechko, 1954; Semyanov, 1974; Yasnosh, 1991; Kuznetsov, 1997; Izhevskiy, 2005; Tyumaseva, 2013). Basically, the Coccinellidae are predators that destroy aphids, scales, parlatorias, thrips, spider mites, leaf-blocks, whiteflies, eggs and larvae of leaf beetles (of first and second ages) and other small arthropods. But their population dynamics is significantly influenced by parasitic insects. A minor role in their destruction is played by predator insects, ticks, simple microorganisms (gregarines, microsporidia), nematodes, insectivorous birds, as well as by fungal diseases. The interest to the study of Coccinellidae has not gone out for several decades yet. Most scientists are interested in questions related to the species composition, environmental issues and their use in the biological and integrated pest control. But entomologists devote insufficient attention to identifying biotic factors that can dramatically reduce the number of these effective predators. The purpose of this study is to identify groups of animals that affect the Coccinellidae population dynamics, and to reveal their species diversity.
Materials and Methods
To identify the parasites infestation of ladybirds, mass collections of beetles, larvae and pupae was carried out. All the collected material was placed into special cages to observe the development and emission of parasites. The infestation by parasitic ichneumons was determined by the dissection of Coccinellidae and growing parasites from them in the laboratory conditions (temperature 25° - 27°C, humidity 70%). The facts of birds and predator insect attacks on Coccinellidae in various phases of their development were established by direct observation in nature and photographing. Nematodes extracted from Coccinellidae were fixed in a special mixture: formalin 40%, acetic acid and water in the ratio of 10:1:89, we also used alcohol 96%, formalin 40%, acetic acid and distilled water in the ratio of 17:6:2:28 (Kiselev, Tyumaseva, 2000).
The total amount of studied material was 6250 adults, 1638 larvae and 820 pupae of Coccinellidae. The material has been collected during 25 years in all the landscape and climatic zones of the Urals, in the Middle Urals and in the zonal and azonal ecosystems of the Middle Ob lowland.
Results and Discussion
Even though all lady beetles have a bright warning color, and as a rule, in case of danger they emit a toxic yellow liquid with a sharp odor and a bitter taste, it does not save them from birds and other animals, which nevertheless eat "poisonous" lady beetles. On this issue, there are quite contradictory data in the literature. I.A. Portchinsky (1912) assumed that lady beetles are
not eaten by birds; they are not edible for most insectivorous animals due to their noticeable warning body color which emphasizes the toxic properties of these beetles. A.V. Mizer (1970) noted that Coccinellidae, including their mass species, are accidental and rather rare objects of birds feeding. V.I. Taraschuk (1952) observed the eating of some lady beetle species by such birds as: Sturnus vulgaris L. (Sturnidae), Muscicapa striata P. (Muscicapidae), Sylvia atricapilla L. (Sylviidae), Emberiza hortulana L. (Emberizidae), Pica pica L. (Corvidae) and Anthus triviaiis L. (Motacillidae). V.N. Kuznetsov (1973) analyzed the content of 1125 stomachs of 190 bird species taken in various areas of the Primorsky Krai (Russia), and established that lady beetles were found in the stomachs only of some species of birds and in an insignificant amount (0.5-1 % of total number of the examined stomachs of each species). Birds occasionally ate the following lady beetles: Harmonia axyridis (Pallas, 1773), Calvia quatuordecimguttata (Linnaeus, 1758), Coccinella septempunctata Linnaeus, 1758, Cynegetis impunctata, Chilocorus inornatus J. Weise, 1887, Propylea quatuordecimpunctata (Linnaeus, 1758), P. japonica (Thunberg, 1781), Anatis ocellata (Linnaeus, 1758), Henosepilachna vigintioctomaculata(Motszhulsky, 1858). Most often, the Coccinellidae beetles were eaten by: Hirundapus caudacutus Lath. (Apodidae), Sitta europaea L. (Sittidae), Cyanoptila cyanomelana Temm. (Muscicapidae), Picus canusGm. (Picidae), Bonasa bonasia L. (Phasianidae) and Schoenicola brevirostris, Sun. (Megaluridae). The beetles, most often found in the stomachs of birds, were Harmonia axyridis. In localities of mass wintering, these lady beetles are pecked by Picus canusGm. (Picidae) and Sitta europaea L. (Sittidae). According to G.I. Savojskaya (1961), in Southeast Kazakhstan there are few enemies for lady beetles among vertebrates, they are rarely eaten only by Phasianus (Galliformes: Phasianidae), Phylloscopus (Passeriformes: Phylloscopidae), Phrynocephalus(Squamata: Agamida) and Bufonidae (Anura).
A.V. Karpenko, G.A. Timchenko and S.L. Dubickaya (1969) note a case of massive eating of lady beetles by birds on two islands formed after flooding of the Dneprodzerzhinsk Reservoir. In food samples of nestlings Passer montanus L. and Passer domesticus L. there were about 48% lady bugs, in nestlings Ficedula albicollisTem. - up to 38% and in Muscicapa striata Pal. -up to 21 %, while there was normal development of nestlings fed on this diet. The examination of adult birds showed that the number of stomachs with Coccinelidae in Sparrows was 100%, in Muscicapa striata - 70% and in Ficedula albicollis - 33%. We have examined the content of 2315 stomachs of amphibians: Pelophylax ridibundus (Pallas, 1771), Rana temporaria Linnaeus, 1758, Rana arvalis Nilsson, 1842, Rana amurensis Boulenger, 1886, Pelobates fuscus (Laurenti, 1768), extracted in various landscape and climatic zones of the Southern Urals, Trans-Urals and Western Siberia. In the stomachs of frogs Pelophylax ridibundus, Rana temporaria, Rana arvalis,we often found Coccidula rufa (Herbst, 1783), C. scutellata (Herbst, 1783), Anisosticta novemdecimpunctata(Linnaeus, 1758), and Hippodamia tredecimpunctata (Linnaeus, 1758); Hippodamia variegata (Goeze, 1777), and Adalia bipunctata (Linnaeus, 1758) were found more rarely.
In the stomachs of Pelobates fuscus the prevailing lady beetles were H. variegata, Scymnus frontalis (Fabricius, 1787); Propylea quatuordecimpunctata, Psyllobora vigintiduopunctata (Linnaeus, 1758), and Adalia bipunctata (Linnaeus, 1758) were less often. The useful activity of lady beetles is more often prevented by some invertebrates. Our long-term studies have shown that in apple orchards, forest shelter belts and fields of vegetable crops in the Middle Urals, there are quite often attacks of Chrysopidae (Neuroptera) and Syrphidae (Diptera) larvae of older ages on the Coccinellidae eggs laying and larvae of younger ages. The Coccinellidae larvae Coccidula rufa, C. scutellata, Halyzia sedecimguttata (Linnaeus, 1758) are eaten by Carabidae (Coleoptera) and predatory bugs. The adults of lady beetles are eaten by Tettigonia viridissima L. (Orthoptera) and Trichodes apiarius (Coleoptera), which more often attack Bulaea lichatschovii (Hummel, 1827). Anthocoris nemorum L. (Hemiptera: Anthocoridae) is registered as a predator of lady beetle pupae.
The beetles are also attacked by ants not allowing them to colonies of aphids. Particularly aggressive are Formica rufa L., F. pratensis Retz.and F. rufibarbis F. Sometimes lady beetles are caught and sucked by Asilidae (Diptera) of the genus Laphria. Spiders, as indicated by N.P. Dyadechko (1954), do not touch lady beetles caught into their webs. However, there were cases of death of lady beetles in spider webs (Savojskaya, 1956) and of a spider Stemonyphantes conspersus(Koch) attacking the adult of Calvia quatuordecimguttata (Linnaeus, 1758) (Lipa, Semyanov, 1967), which is not typical. In the Primorsky krai, numerous cases of various species of spiders attacking larvae and pupae of mass Coccinellidae species were registered (Kuznetsov, 1997). Few parasitoids of entomophagous coccinellids are specialists, some are widely distribut-ed and attack within a subfamily or tribe (Riddick at al., 2009). One of the best understood parasitoids is Dinocampus(Perilitus) coccinellaeSchrank (Hymenoptera: Braconidae), whose host preference, life history, ecology, and behavior have been thoroughly investigated (Ceryngier & Hodek, 1996; Majerus, 1997; Majerus et al., 2000; Okuda & Ceryngier, 2000; Al Abassi et al., 2001; Davis et al., 2006; Firlej et al., 2006; Koyama and Majerus, 2008).
In all the biotopes of the Middle Urals and the Southern Urals, we noted the infection of the Coccinellidae larvae, pupae and adults with various species of Parasitica (Hymenoptera). As our study has shown, Dinocampus coccinellae (Braconidae) parasitizes in the beetles Hippodamia variegata and Coccinella septempunctata. From the second decade of May to the end of the second decade of July, the degree of damage to H. variegata beetles constitutes in average 4%, however in September -October it reaches 20%. From the end of August to October, Dinocampus coccinellae kills over 22% of Coccinella septempunctata adults. Additionally, the parasitoid larvae can overwinter in the host body, and then their flight occurs in spring after wintering. In the second decade of July, mass infection of Coccinella septempunctata pupae with the parasitoid Dinocampus coccinellae reaches 20%, and in the second decade of August, during the pupation of larvae of this species second generation, the degree of pupae infection increases up to 40%. From the third decade of July, Homalotylusplatynaspidis Hof. (Encyrtidae) parasitize in larvae of Platynaspisluteorubra (Goeze, 1777) occurring in meadows. In the second decade of August, it affects up to 10% of the fourth age larvae. Flight of the parasitoid from the dead host pupae is observed. The analysis of publications has shown that Spathius and Dinocampus (Braconidae) affect lady beetles also in other regions (Savojskaya, 1987; Filatova, 1974; Kuznetsov, 1997)
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Larvae and pupae of mass Coccinellidae species are affected by Perllampus, Ganahlia sp., Tetrastichus coccinellae Kurd., Homalotylus flaminiusDalm., Homalotylus eytelweiniiRotz. (Chalcidoidea), as well as by Phalacrotophora fasciata Fald (Diptera: Phoridae) (Dyadechko, 1954; Savojskaya, 1956,1961; Adylov, 1965; Lipa, Semyanov, 1967; Filatova, 1974; Kuznetsov, 1975). And in Southeast Kazakhstan in some years in the second half of the summer Phoridae kill over 30-40 % of the Coccinella septempunctata, Adalia bipunctata and H. variegata population (Savojskaya, 1987). In the Primorskiy krai, Phalacrotophora fasciata Fall. affects from 9,5% to 30% of Harmonia axyridislarvae (Voronin, 1966; Kuznetsov, 1975), and in West Siberia - up to 45% (Filatova, 1974). Degeeria luctuosa Meig. (Diptera: Tachinidae) parasitize in the adults of Adalia decempunctata (Linnaeus, 1758), and Oenopia conglobata(Linnaeus, 1758), (Banks, 1956; Klausnitzer, 1969; Richerson, 1970).
Coccinella quinquepunctata Linnaeus, 1758, and Myrrha octodecimguttata (Linnaeus, 1758), are often affected by Gregarinidae (Sporozoa) and Microsporidia (Protozoa) (Lipa, Semyanov, 1967). Microsporidia affect Malpighian tubes, ovaries, intestines, nervous system of lady beetles. Certain Microsporidia species infect Nosema coccinellae Lipa, N. hippodamia Lipa, N. tracheophila Cole & Briggs. (Richerson, 1970).
The Coccinellidae adults, larvae and pupae are infected with nematodes of the family Mermithidae (Ogloblin, 1913; Telenga, 1948; Dyadechko, 1954; Savojskaya, 1961). In Ukraine, the degree of infection of Chilocorus with nematodes reaches 20% (Dyadechko, 1954). In Kazakhstan, Mermithidae were found in Coccinella septempunctata, Adalia bipunctata and Exochomus quadripustulatus (Linnaeus, 1758) (Savojskaya, 1974). In Tuva, according to Filatova (1974), nematodes of the genus Aphelenchoides (Aphelenchida: Aphelenchoididae) parasite in the adults of Adalia bipunctata and Coccinella magnifica L. Redtenbacher, 1843. In the Southern Urals, Mermissp. (Mermithidae) were found by us in larvae of Coccinella septempunctata and Propylea quatuordecimpunctata.
A large number of red mites of the family Trombiculidae (Acari: Trombidiformes) can be found in August on the abdomens, under the elytra, on the head, thorax and legs of some Coccinellidae of the Middle Urals, more often - in H. variegata and Coccinella septempunctata. Sometimes the number of mites on one specimen is so large that the beetles' activity falls sharply, and they stop feeding. The number of mites on the Coccinellidae body gradually increases, reaching the maximum (from 8 to 10 mites) in the second decade of September. Probably, beetles play a significant role in the migration of mites in natural conditions. In late September - early October, mites are rare.
Field data on the impact of natural fungal pathogens attacking Coccinellidae are limited but suggest that natural infection levels are less than 20% (Ceryngier, 2000; Beyene et al., 2007). Coccinella septempunctata and Coccinella quinquepunctata are affected by fungus BeauveriabassianaVuill. in wintering areas (Lipa, Semyanov, 1967). In South-eastern Kazakhstan, Coccinella septempunctata are killed by fungus Cephalosporium sp. (Savojskaya, 1961), and fungus Monilia lipolytica Harrison. parasites on larvae of Coccinula redimita (J. Weise, 1885), and C. quatuordecimpustulata (Linnaeus, 1758), causing their death. In the Primorsky krai, a mass death of Epilachna beetles from fungal diseases was noted (Ivanova, 1962). Due to observations of V.N. Kuznetsov (1997), in 1971, the infection of Epilachna beetles with fungal microorganisms in Shkotovskiy district was 5.4%, and in 1989, in Khasanskiy district - 6.8%. In addition to Epilachna, fungi affected Coccinella septempunctata, Harmonia axiridis, Calvia quatuordecimguttata and Hippodamia tredecimpunctata. The causative agents of disease were Beauveria tenelle Seim and B. bassiana Vuill. The affection of adults often occurs in August when there are frequent rains, high temperature and air humidity. The beetles killed by these microorganisms are covered with a white coating of the fungus mycelium.
Concluding remarks
Despite the long study of Coccinellidae biology, the role of natural enemies in controlling the population of entomophages is still insufficiently studied. However, we can assume that despite the presence of natural protection mechanisms, the Coccinellidae have a large variety of natural enemies that affect them at different stages of development. Useful activity of lady beetles is mostly prevented by invertebrate animals. The group of insects limiting the Coccinellidae development is dominated by specimens of the order Hymenoptera and Diptera. Unlike phytophages, which have low mobility in comparison with entomophages, Coccinellidae play an important role in the dispersal of such parasites as mites and fungi. This review should contribute to a further comprehensive study of the natural enemies of Coccinellidae.
Acknowledgements
First author was supported by Grant of the FGBOU VO "Mordovian State Pedagogical Institute named after M.E. Evseviev "under the contract for R & D of 14.04.2017 No. 16-449 on the topic "Bioindicational assessment of natural areas of the South Urals using entomofauna".
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Citation:
Tyumaseva, Z.I., Guskova, E.V. (2017). Parasites, predators and diseases of Lady Beetles (Coleoptera, Coccinellidae) of the Southern Urals and adjacent territories. Ukrainian Journal of Ecology, 7{2), 120-123. I Thk work Is licensed under a Creative Commons Attribution 4.0. License
