ISSN 0013-8738, Entomological Review, 2011, Vol. 91, No. 9, pp. 1081–1087. © Pleiades Publishing, Inc., 2011. Original Russian Text © L.Yu. Rusina, 2011, published in Zoologicheskii Zhurnal, 2011, Vol. 90, No. 10, pp. 1197–1203.

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Host Discrimination by Elasmus schmitti (Hymenoptera, Eulophidae) and Latibulus argiolus (Hymenoptera,

Ichneumonidae), Parasitoids of Colonies of Polistes Wasps (Hymenoptera, Vespidae)

L. Yu. Rusina Kherson State University, Kherson, 73000 Ukraine

e-mail: lirusina@yandex.ru

Received March 24, 2011

Abstract—The ability to discriminate parasitized and non-parasitized hosts allows the parasitoids to avoid intras-pecific and often interspecific competition. In 2005–2009, the incidence of mixed infestation of Polistes nimpha (Christ) colonies by parasitoids Elasmus schmitti Ruschka (Hymenoptera, Eulophidae) and Latibulus argiolus (Rossi) (Hymenoptera, Ichneumonidae) was analyzed. In settlements of different types, the frequencies of mixed infestation deviated from the values expected in case of random distribution. The presence or absence of discrimi-nation ability cannot be confirmed unequivocally based on our material. The data obtained are discussed in relation to the biological features of parasitoids.

DOI: 10.1134/S0013873811090016

The study of stimuli affecting the behavior of para-sitoids when they seek and infest their hosts is of both theoretical and practical significance. The numerous observations and experiments allow one to study the seeking mechanisms of parasitoids and their ability to distinguish infested and intact hosts, thus avoiding intraspecific and often even interspecific competition (Salt, 1961; Buleza, 1971, 1996; Viktorov, 1976; Mackauer, 1990; Godfray, 1994; Pedata et al., 2002; Tamò et al., 2006). Viktorov (1976) referred to the ability of parasitoids to distinguish between infested and non-infested hosts as the discrimination ability and considered it to be one of the factors regulating the abundance of insects.

At the interspecific level, the discrimination ability can be estimated directly, by observations and experi-ments, or indirectly, by comparing the observed fre-quencies of host infestation with several species of parasitoids and the expected frequencies in case of random infestation (Godfray, 1994).

In social insects, infestation with several species of parasitoids has never been observed in a single indi-vidual but it may take place at the colony level.

The ability of parasitoids to respond selectively to resocial wasp colonies already infested with a differ-ent species was analyzed by Strassmann (1981). Cases

of mixed infestation of the colonies of Polistes excla-mans Viereck (Hymenoptera, Vespidae) with the para-sitoids Chalcoela iphitalis (Walker) (Lepidoptera, Py-ralidae) and Elasmus polistis Burks (Hymenoptera, Eulophidae) were observed only at the Brackenridge Field Laboratory of the University of Texas at Austin. According to the cited author, the observed frequency of mixed infestation was close to the expected value in case of random distribution. This fact was interpreted as evidence that the two species of parasitoids did not avoid one another (Strassmann, 1981). However, it would be premature to conclude that the two species in question lacked discrimination abilities; since they have different infestation strategies and their interac-tion with the host and with one another may result in a variety of situations, the discrimination ability should be analyzed with reference to the biology of the parasitoids and the history of infestation of a particular host settlement, both in the seasonal and the long-term aspects.

We have addressed this problem by the example of the ectoparasitoids Elasmus schmitti Ruschka (Hyme-noptera, Eulophidae) and Latibulus argiolus (Rossi) (Hymenoptera, Ichneumonidae), infesting polistine wasps in the Palaearctic (Luchetti, 1992; Rusina, 2009).

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MATERIALS AND METHODS

The interspecific interactions in the parasitoids E. schmitti and L. argiolus were studied in 584 nests of Polistes nimpha (Christ) (Hymenoptera, Vespidae) from 21 settlements, collected by myself and kindly provided by my colleagues and students of Kherson and Yekaterinburg universities. The collection locali-ties and sample size are listed in Table 1.

The wasp P. nimpha has the following life cycle. The overwintered fertilized foundresses build a nest during the first decade of May and raise the first gen-eration of workers which emerge in the first half of June. As the colony develops, it switches from rearing workers to raising the sexual individuals (males and future foundresses). The future foundresses of this species appear in August, after mass emergence of the males. The colony disintegrates in late summer and autumn, and the reproductives mate. The males and workers die in autumn, whereas the future foundresses overwinter.

Both parasitoid species have two generations: fe-males of the first generation infest the host colonies from the end of May to mid-June, and those of the second generation, from the second half of July to the beginning of August (Rusina, 2009).

The colonies of P. nimpha in each settlement were subdivided into four classes: (1) colonies with L. argiolus; (2) colonies with E. schmitti; (3) colonies with two species of parasitoids; (4) non-infested colo-nies. Infestation with L. argiolus was recorded by the presence of the cocoons or ovally slanted, pale yellow or pale orange remains of the larval cuticle (Makino, 1983). The presence of E. schmitti was determined by the possession of brown transverse fecal partitions inside individual cell, formed of the parasitoid’s me-conium prior to pupation (Gumovsky et al., 2007).

The history of settlement infestation was described by the mapping method (reflecting the number of me-conia in the cells and the presence of the parasitoids) (Rusina, 2006). Two circumstances were taken into account: first, that at the moment of infestation the parasitoids choose the largest colonies in the settle-ment, and second, that the colonies that get infested earlier in the given season are smaller in size (Rusina, 2009, 2010). The following variants of infestation were distinguished: 1. Parasitoids of the first genera-tion invade the colony before the emergence of work-ers; the nest comprises up to 50 cells at the completion

of its life cycle; the cells with traces of parasitoid ac-tivity are located in the center of the nest. 2. Parasi-toids of the first generation invade the colony after the emergence of workers; the nest consists of 50–120 cells; the cells with parasitoids occur both in the center and in the periphery of the nest. 3. Parasi-toids of the second generation invade the colony while it is raising the reproductive generation; the nest con-sists of 90–220 cells; the cells with parasitoids occur both in the center and in the periphery of the nest.

The relation between colony infestation with one or two species of parasitoids and the total infestation of the settlement was estimated using the Spearman cor-relation test. The settlement infestation (%) was de-termined as the number of colonies infested with any species of parasitoids related to the total number of colonies in the settlement.

For each settlement, the probability of mixed infes-tation (D) was calculated as a product of the probabil-ity of infestation with one parasitoid species (the frac-tion of colonies infested with this parasitoid) and the probability of infestation (the fraction of colonies in-fested) with the other species (Strassmann, 1981).

The theoretical frequencies of each group were cal-culated based on the assumption that infestation of colonies was random (Lakin, 1980).

The results obtained were statistically processed within the Statistica v. 6.0 package (Statsoft Inc, USA 1984–2001).

RESULTS

Analysis of our material showed that in the wasp settlements where mixed infestation was observed, the fraction of colonies containing only L. argiolus was 54.2 [23.5, 64.9] % (the data are presented as the me-dian and quartiles). The colonies infested with E. schmitti were less frequent, comprising only 8.1 [0.0, 14.3] %. The fractions of colonies with mixed infestation and intact ones were 9.1 [3.0, 11.0] and 25.0 [16.0, 36.4] %, respectively. The total rate of settlement infestation with L. argiolus and E. schmitti was 70.3 [42.9, 72.7] and 18.2 [12.5, 30.6] %, respec-tively.

The fraction of colonies infested with only E. schmitti was found to be negatively correlated with that of colonies infested with only L. argiolus (rs = –0.54, n = 21, p < 0.05). The fraction of mixed

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Table 1. The frequency of mixed infestation of Polistes nimpha colonies with the parasitoids Latibulus argiolus and Elasmus schmitti

Frequency of mixed infesta-tion of colonies

Infestation of colonies, %

Nest collection localities Number of nests

% D Latibulus argiolus

Elasmus schmitti

1. Kherson Prov., Golaya Pristan District, Rybal’che, Ukraine, 2005

42 16.7 0 90.5 16.7

2. Crimea, Yalta, Ukraine, 2005 21 28.6 0 95.2 28.6 3. Kherson, Ukraine, 2006 7 28.6 6.1 71.4 42.9 4. Kherson Prov., Belozersky District,

Aleksandrovka, Ukraine, 2006 28 7.1 16.1 71.4 32.1

5. Kherson Prov., Berislav District, L’vovo, Ukraine, 2006

25 12 9 68 28

6. Kherson Prov., Ivanovo District, Blagodatnoe, Ukraine, 2006

37 5.4 5.3 70.3 13.5

7. Kherson Prov., Kalanchak District, Novokievka, Ukraine, 2006

8 12.5 0 75 12.5

8. Kherson Prov., Kalanchak District, Razdol’noe, Ukraine, 2006

85 2.4 0 71.8 2.4

9. Odessa Prov., Baltsky District, Chernech’e, Ukraine, 2006

15 6.7 0 60 6.7

10. Kirovograd Prov., Bobrinets, Ukraine, 2006 55 9.1 3.5 72.7 14.5 11. Kherson Prov., Tsyurupinsk District,

Radensk, Ukraine, 2007 11 9.1 6.6 27.3 45.5

12. Kherson Prov., Kalanchak District, Razdol’noe, Ukraine, 2007

20 10 3.3 75 15

13. Nikolaev Prov., Oktyabr’sky District, Kotlyarovo, Ukraine, 2007

24 4.2 4.5 58.3 12.5

14. Kherson Prov., Velikoaleksandrovsky District, Chkalovo, Ukraine, 2007

34 14.7 2.1 38.2 23.5

15. Voronezh Prov., Venevitinovo Research Center, Russia, 2007

58 6.9 0 25.9 6.9

16. Kurgan Prov., Ketovo District, Sychevo, Russia, 2007

14 7.1 4.6 28.6 28.6

17. Kherson Prov., Genich District, Dogmarovka, Ukraine, 2008

11 36.4 0 72.7 36.4

18. Kherson Prov., Tsyurupinsk, Ukraine, 2008 7 28.6 6.1 42.9 71.4 19. Kirovograd Prov., Bobrinsk District,

Charivne, Ukraine, 2008 24 4.2 0 75 4.2

20. Voronezh Prov., Venevitinovo Research Center, Russia, 2008

36 22.2 3.2 61.1 30.6

21. Kherson Prov., Golaya Pristan District, Staraya Zbur’evka, Ukraine, 2009

22 4.5 1.9 18.2 18.2

Note: D is the probability of random mixed infestation.

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infestation was negatively correlated with the number of intact colonies (rs = –0.59, n = 21, p < 0.01).

The observed frequency of mixed infestation of host colonies in two settlements was close to the expected frequency D. This similarity, and also the fact that mixed infestation was observed even in the presence of non-infested colonies (Tables 1, 2), can be regarded as an indirect proof of the random nature of mixed infestation and the absence of interspecific discrimina-tion ability in both L. argiolus and E. schmitti. How-ever, in ten other settlements the observed frequencies of mixed infestation exceeded the expected values of D (Table 1), showing that mixed infestation was not random. One settlement (no. 4; see Table 1) repre-

sented an exception in that the observed frequency of mixed infestation was lower than the expected value. This was the only case in which the parasitoids might have avoided mixed infestation, i.e., revealed discrimination abilities. This settlement (a total of 28 nests) was originally infested with the first genera-tion of L. argiolus, whereas the first generation of E. schmitti appeared there after the emergence of workers (Table 2). Mixed infestation was recorded in two colonies and involved the second generation of the parasitoids.

The settlements (n = 8) in which one of the parasi-toids was found only in the colonies with mixed in-festation had to be excluded from analysis because

Table 2. Temporal parameters of infestation of Polistes nimpha settlements with the parasitoids Latibulus argiolus and Elasmus schmitti

Colony infested by the first parasitoid generation before emergence of workers after emergence of workers

Colony infested by the second parasitoid generation

No. of settle-

ment 1 2 3 1 2 3 1 2 3

Fraction of non-infested

colonies, %

Settlement class I 3 0 0 0 0 1 0 3 0 2 14.3

11 0 0 0 0 3 0 2 1 1 36.4 17 0 0 0 0 0 0 4 0 4 27.3 18 0 0 0 0 2 0 1 1 2 14.3

Settlement class II 1 4 0 0 6 0 1 4 0 5 4.8 2 9 0 0 9 0 1 13 0 6 9.5 4 6 0 0 6 6 0 6 1 2 3.6

Settlement class III 5 2 0 0 4 2 1 8 2 2 16

10 2 1 0 9 0 1 24 2 4 21.8 12 0 0 4 0 0 8 1 2 20 14 1 0 3 1 1 4 1 4 52.9 16 1 0 1 1 0 1 1 1 50 20 0 0 7 2 2 6 1 6 30.6 21 1 0 1 0 0 1 2 1 68.2

Settlement class IV 6 2 0 0 4 1 0 14 1 2 35.1 7 0 0 0 1 0 0 4 0 1 25 8 3 0 0 9 0 0 47 0 2 28.2 9 0 0 0 5 0 0 3 0 1 40

13 1 0 0 2 0 0 10 2 1 33.3 15 2 0 0 6 0 2 3 0 2 74.1 19 5 0 0 8 0 0 4 0 1 25

Notes: 1, colony infested with Latibulus argiolus; 2, colony infested with Elasmus schmitti; 3, mixed infestation.

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the expected frequency was equal to zero in such cases.

Besides the above analysis, we used a somewhat different method in which the settlements were subdi-vided into classes by the degree of infestation with E. schmitti (and a number of other characters) (Table 2). This particular species was selected because the degree of settlement infestation with E. schmitti was found to be correlated with the fraction of colo-nies with mixed infestation (rs = 0.71, n = 21, p < 0.001).

Class I included settlements infested with E. schmitti by 36.4–71.4%. Infestation of colonies with the first generation of parasitoids, if it took place at all, involved only E. schmitti (Table 2). Infestation with both species of parasitoids, including cases of mixed infestation, occurred during the period corre-sponding to their second generation. The intact colo-nies comprised 14.3–36.4%.

As can be seen from Table 3, the incidence of infes-tation with E. schmitti in settlements of this class was significantly greater, and the incidence of infestation with L. argiolus was significantly smaller than the calculated values (“incidence” in this case means the absolute number of cases, used as a measure of their frequency of occurrence – see Lakin, 1980, p. 290).

At the same time, the incidence of colonies infested with two species of parasitoids was greater than the theoretical value, showing that mixed infestation was not random. However, this provides no proof of the presence or absence of the discrimination ability: even when present, this ability cannot be revealed by this method.

Class II included the settlements infested with E. schmitti by 16.7–32.1% and with L. argiolus by 71.4–95.2%; the fraction of non-infested colonies was 3.6–9.5%. The settlements were infested with the first and the second generation of both species of parasi-toids but E. schmitti appeared in the colonies only after emergence of workers. The fraction of colonies with L. argiolus was greater than the expected value, whereas the fraction of intact colonies was smaller; therefore the random nature of mixed infestation may be related to the deficiency of hosts.

Class III was characterized by almost the same frac-tion of colonies with E. schmitti as in class II: 14.5–30.6%. However, the fraction of non-infested colonies in these settlements was greater: 16–68.2%. The set-

tlements were infested with the first and the second generation of both species of parasitoids. The ob-served fractions of different classes of colonies were close to the corresponding expected values. Mixed infestation in such settlements was also random.

Class IV was the largest. Infestation with E. schmitti in settlements of this class was lower than in the pre-ceding classes: 2.4–13.5%, but the fraction of intact colonies was the same as in class III. The colonies were infested with the first and second generations of L. argiolus; the parasitoids usually invade the colonies before emergence of workers. At the same time, E. schmitti was usually represented by the second gen-eration.

The fractions of colonies with mixed infestation and those with E. schmitti were smaller, whereas the frac-tion of intact colonies was larger than the theoretical values. It may be supposed that in these settlements the two species of parasitoids avoided one another; therefore at least one of them had discrimination abil-ity.

The infestation of settlements with E. schmitti and L. argiolus is related to the peculiarities of colony development, in particular, with the timing of a parasi-toid invasion. For example, infestation of settlements with E. schmitti is positively correlated with the num-ber of colonies infested with the first generation of this parasitoid and negatively correlated with the same parameter for L. argiolus (rs = 0.67, p < 0.001 and rs = –0.51, p < 0.05, respectively). In a similar way, infestation of settlements with L. argiolus is positively correlated with the number of colonies infested with both the first and second generation of this species (rs = 0.45, p < 0.05 and rs = 0.55, p < 0.01) and nega-tively correlated with the number of colonies infested with the first generation of E. schmitti (rs = –0.57, p < 0.01).

Judging by the maps of colonies with mixed infesta-tion, E. schmitti infested the colonies already contain-ing L. argiolus, rather than vice versa.

Thus, the incidence of mixed infestation differed from the values expected in case of random dis-tribution, in two out of four classes of settlements (Table 3). This phenomenon was observed at both low and high rates of infestation with E. schmitti.

DISCUSSION The situation observed in most settlements is incon-

sistent with the hypothesis that the two species of

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parasitoids avoid one another during infestation of the host colony. It is more likely to support the opposite assumption: in many cases mixed infestation occurs more frequently than it could be expected in case of random distribution, i.e., some “attraction” is ob-served. This phenomenon may result from the fact that both species prefer host colonies with specific parame-ters, for example, larger ones (Rusina, 2010). The interspecific competition should be reduced in such colonies due to abundant trophic resources. Processing of the entire body of data has shown the fraction of mixed infestations to increase with the rate of settle-ment infestation with E. schmitti. However, high rates of settlement infestation with E. schmitti are rarely observed, which may be related to the activity of its hyperparasitoid, Bariscapus elasmi Demolin (Hymen-optera, Eulophidae). The method used in this research does not allow us to estimate the degree of infestation of E. schmitti with the secondary parasitoid; however, some indirect data indicate that the low abundance of E. schmitti is primarily determined by its hyperparasi-toid (Rusina, 2009).

In general, all the situations of non-random mixed infestation involve infestation of colonies with the first generation of parasitoids.

The discrimination ability may be absent in E. schmitti but present in L. argiolus. Such difference may be related to the different competitive abilities of these two species in case of mixed infestation. In par-

ticular, E. schmitti is a pro-ovigenic (the newly hatched adults contain mature eggs and often produce offspring in the same host nest) and gregarious (one female lays several eggs on the host larva) parasitoid. The other species, L. argiolus, is a synovigenic parasi-toid (the new-generation adult requires additional feeding for the eggs to mature) and infests the host larva with a single egg. In these circumstances, the discrimination ability should be adaptive for L. ar-giolus. However, special experiments are needed to confirm the presence or absence of discrimination ability in these species. It is possible that the very con-cept of discrimination ability as applied to parasitoids of social insects should be reconsidered and emended.

ACKNOWLEDGMENTS The author is very grateful to A.V. Lopatin (Vo-

ronezh State University), A.V. Fateryga (Taurida Na-tional University), and students of Kherson and Yekaterinburg State Universities T.V. Vasilenko, Ya.V. Norchenko, I.A. Pekanova, E.Yu. Petrovskaya, and V.V. Shlapachenko, for their help in collecting the wasp nests. Sincere thanks are due to G.M. Dlussky for valuable comments on the manuscript.

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Table 3. Comparison of the observed (1) and theoretical (2) distribution of the infested and intact colonies of Polistes nim-pha by the classes of settlements

Class of colonies Colonies

with Latibulus argiolus Colonies

with Elasmus schmittiColonies with Latibulus

argiolus and Elasmus schmitti Non-infested

colonies Class

of settlement 1 2 1 2 1 2 1 2

N

I 10 18.5 8 2.47 9 3.8 9 11.3 36 χ2 3.90* 12.42*** 7.30** 0.46 II 63 46.7 7 6.2 15 9.5 6 28.5 91 χ2 5.65* 0.09 3.18 17.78*** III 90 105.8 20 14.1 25 21.5 71 64.6 206 χ2 2.37 2.46 0.56 0.64 IV 137 128.9 5 17.2 12 26.2 97 78.7 251 χ2 0.05 8.65** 7.71** 4.28* Number of colonies

300 40 61 183 584

Notes: The statistically significant values are shown in bold. * p < 0.05, ** p < 0.01, *** p < 0.001. N is the number of colonies.

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