COMMUNITY ECOLOGY 9(1): 45-51, 2008 20081585-8553/$20.00 © Akadémiai Kiadó, Budapest DOI: 10.1556/ComEc.9.2008.1.6

Functional response of Chelonus oculator (: ) to temperature, and its consequences to parasitism

M. García-Martín1, M. Gámez2, A. Torres-Ruiz1 and T. Cabello1,3

Department of Applied Biology, Almeria University, Ctra. de Sacramento s/n, 04120-Almeria, Spain

Department of Statistics and Applied Mathematics, Almeria University, Spain ! Corresponding author. Fax: +34-950015476; Phone: +34-950015001, E-mail: [email protected]

Keywords: Biological control, Egg-larval parasitoid, Ephestia kuehniella, Handling time, Lepidoptera, Mathematical models, Spodoptera exigua. Abstract: The parasitization behaviour of Chelonus oculator (F.), egg-larval parasitoid of noctuid lepidopteran species, has been studied under laboratory conditions, using Ephestia kuehniella Zeller as host, at four different temperature levels (10, 20, o 30 and 40±1 C) and five densities of host eggs (50, 100, 150, 200 and 250). A significant effect of temperature and parasitism o o density was observed. At 10 C, there was no parasitism, whilst at 40 C it was very low; presenting adequate values at the two o other temperatures (20 and 30 C). With regard to these facts, the functional responses of this parasitoid species were adjusted and we noted that they display Holling type III. Estimating the handling times from the respective mathematical expressions, o we obtained 10.944 and 15.250 min, at 20 and 30 C, respectively. These values are considerably higher than the respective times obtained by direct observation, 0.597 and 0.560 min for these temperatures (this difference is due to the fact that in the first case, unlike the second one, the time used for the search of the host is also included). The results obtained from the parasitization behaviour of Ch. oculator are discussed, also considering it as a candidate biological control agent against Spdoptera exigua (Hübner), beet armyworm, with a view to its possible use in greenhouse crops in Spain.

Introduction bello et al. 1996). In the case of S. exigua, the parasitoid egg- Spodoptera exigua (Hübner), beet armyworm, is one of larval species that stands out is Chelonus oculator (F.) (Pino the most devastating pest in Spanish greenhouse crops, espe- et al. 2003) which could potentially be a control agent in cially in pepper and water melon (Cabello and Belda 1994, greenhouse crops if increased. We need to point out that the Cabello 2004). The development of biological control meth- functional response offers a good basis to understand the ac- ods against noctuid pests in these crops, with the only excep- tion of entomaphagous agents in biological control pro- tion of Bacillus thuringiensis Beliner, has hardly been com- grammes (Waage and Greathead, 1988; Barlow, 1999), al- pared with that for outdoor crops; as for example, with beit with restrictions as described by Mills and Getz (1996); species of Trichogramma (van Lenteren 2000). To be spe- admitting in addition a biological interpretation of the pa- cific, the allochthonous larval endoparasitoid species Cotesia rameters of the functional response (Cabello et al. 2007). marginiventris (Cresson), has been trialled in greenhouse Thus, when it comes to “classical” biological control, one in- conditions for the control of S. exigua (Messelink 2002, Ur- tends to introduce an allochthonous natural enemy to a new baneja et al. 2002) as well as Baculovirus (SeMNPV) both geographic area, where its prey/host has been previously de- allochthonous (Moscardi 1999, Smits and Vlak 1994), and termined, in order to exert a natural control similar to that autochthonous (Belda et al. 2000). they performed in their area of origin. This operation requires a certain stability of the predator-prey (or parasitoid-host) The lack of commercially available natural enemies for system, which can only be reached with a natural enemy the control of S. exigua, together with the problems of resis- showing type III functional response. The latter is the only tance to insecticides of this pest in our area (Smagghe et al. type considered adaptive depending on the density of the host 2003), constitute a restraining factor for the application of and with good potential for regulating the host population biological control programmes or IPM, in greenhouse crops (Hassell and May 1973, Oaten and Murdoch 1975a,b, (van der Blom 2002), especially in S. exigua (Castañé 2002). Hassell 1978). Contrary to this, in case of inundative biologi- On the other hand, in the outdoor crops of the area, cal control, stability of the system is not important, since our parasitoid and predator species (Cabello 1986, 1988, Cabal- objective then is to get a short-term response, due to the fact lero et al. 1990, Guimaraes et al. 1995, Torres-Villa et al. that the mortality of the prey/host occurs before a generation 2000) as well as entomopathogens (Caballero et al. 1992) are is completed. In this case, in principle, a type I response very abundant and provide very efficient control over the seems to be more adequate, in which there is a linear response pest populations, with elimination rate of 33 and 100% (Ca- between the density of the phytophagous and the mor- bello 1988), which does not happen in greenhouse crops (Ca- tality caused by the entomophagous insect. In this sense, 46 García-Martín et al.

Jeschke et al. (2004) point out that a type I functional re- For each temperature at which adequate parasitization sponse is due to two fundamental conditions: a very short values were found, the type of functional response presented manipulation time and a maximal activity state, long enough was determined. First of all, a distinction was made between to reach saturation. This is the case in the majority of the spe- functional response types II and III, estimating the cubic and cies of the genus Trichogramma, which are globally used in quadratic linear parameters in the following equation pest control (van Lenteren 2000, Elzen et al. 2003): they usu- (Juliano 2001): ally follow type I functional response (Cabello 1985, Faria et N exp(PPNPNPN+⋅ +⋅2 +⋅3 ) al. 2000, Mills and Lacan 2004). For all these reasons, the a = 01tt 2 3 t (1) N 1++⋅+⋅+⋅exp(PPNPNPN2 3 ) objective of this study is to establish the functional response t 01tt 2 3 t of this parasitoid and the effects of temperature to complete where Na is the number of parasitized hosts, Nt is egg host its assessment as a potential biological control agent for S. density, Po,P1,P2 and P3 are adjustment parameters. exigua in greenhouses in Spain. Subsequently, the data were adjusted to the equation for parasitoid type III functional response, established by Materials and methods Hassell 1978, according to the following expression:

In all the trials carried out in laboratory conditions, Ch. L F bT⋅⋅ N ⋅ P IO NN=⋅−M1 expG − tt JP (2) oculator mated females were utilised which had emerged at H 2 K NM 1+⋅cNtht +⋅ bT ⋅ N QP from the pupa less than 48 hours before and without previous parasitization experience; as well as eggs less than 24 hours old from the alternative host, Ephestia kuehniella Zeller. In where Na and Nt are as before, T is available time for search- both cases, the specimens came from the populations kept in ing (days), Th is the estimated handling time of the host the Agricultural Entomology Laboratory of the University of (days), Pt is the number of parasitoids, b, c are adjustment Almeria. In the first species, breeding was carried out follow- parameters. ing the methodology of Cabello et al. (2005), and for the sec- All the previous models were adjusted by non-linear re- ond one, the methodology utilised was that of Daumal et al. gression and the Marquardt algorithm (Conway et al. 1970), (1975) and Rodríguez et al. (1988a,b). using the programme GraphPad Prism version 4.00 (Motul- sky and Christopoulos 2003) The trial was factorial, with two treatments: temperature o (at four levels: 10, 20, 30 and 40±1 C) and host density (5 Once the type of functional response had been selected, levels: 50, 100, 150, 200 and 250 E. kuehniella eggs), carry- in order to verify if the functional response curves at 20 and o ing out 10 replications in each treatment. At this point, we 30 C represented the same models or different ones, they anticipate that although it might seem reasonable to make were compared using the extra sum-of-squares F-test with measurements at densities lower than 50, Figure 1 will show the above mentioned GraphPad software (Motulsky and egg number 50 is under the inflexion of the fitted curve, Christopoulos 2003). To discriminate between functional re- which justifies the choice of the corresponding Holling type sponse type II and type III, it is necessary to point out that at of the functional response without further measurements. both temperatures, the linear values found are positive and The containers used for parasitization were filter-paper cyl- the quadratic ones are negative, indicating type III. However, o inders (diameter 9 cm and height 5 cm) that were closed at we must highlight for values at 30 C that these include zero both sides with Petri plastic sheets. A piece of card was in their confidence interval. This needs to be interpreted with placed in each container (3 cm × 3 cm) where the E. caution since, as Juliado (2001) indicates, the parameters are kuehniella eggs were stuck using a brush and water, at each not significantly different if the confidence interval includes of the densities trialled. These were placed in rows and col- zero. umns with 2 mm separation to form the patch. A drop of honey: water mixture (1:1) was also introduced onto a piece To verify the handling time obtained in the previous ad- justments (T ) with its actual values (T *), a complementary of card (1.5 cm × 1.5 cm) in each container as food for the h h females. Later on, a Ch. oculator mated female was intro- trial was carried out. In this case, the experimental design was also random, with only one factor: temperature, at two duced in each container and left to parasitize for 24 hours. o The remaining environmental conditions were 60-80% rela- levels 20 and 30±1 C and with a total of 10 replicates per tive humidity and 16:8 hours of light:darkness. After the treatment. Glass test tubes (1 cm diameter and 7 cm length) above mentioned 24 hours, the cards with the egg patches were used in this trial as parasitization containers, in each of were deposited in plastic containers (500 ml) with flour and these a card was placed (0.8 cm × 6.0 cm) to which 5 E. o reared at 25 C, until the E. kuehniella or parasitoid adults kueniella eggs had been glued in a single line, with 1 cm. emerged. distance between them. Inside each tube, a Ch. oculator mated female was placed, exposed to each of the tempera- The data obtained for parasitism percentage were sub- tures trialled and observed, under binocular macroscope, to jected to two-way analysis of variance, after log transforma- estimate the handling time. To this end, we measured the total tion; and using minimum difference method, the mean values time spent by an adult parasitoid female for antennating, were compared by SPSS, version 12.0.2 (SPSS 2003). probing, detecting, ovipositing, grooming and resting, for Functional response of Chelonus to temperature 47

Table 1. Percentage of parasitized Ephestia kuehniella eggs by Chelonus oculator females according to host density and tempera- ture, under laboratory conditions (60-80% relative humidity and 16:8 h, L:D).(Values followed by the same letter do not differ sig- nificantly at P = 0.05)

Table 2. Results of logistic regression analyses of the proportion of E. kuehniella eggs parasitized by Chelonus oculator against numbers offered at 20 and 30±1 oC, under laboratory conditions (60-80% R.H. y 16:8 h de L:D).

o each host egg. These are the values included by Hassell tures 20 and 30 C. In Table 2, the linear, quadratic and cubic (1978) in the concept of the manipulation time. The values parameters for the parasitization rate in the logistic adjust- found, after a log transformation, were subjected to a vari- ment are presented, where we obtain type III functional re- ance analysis, with SPSS, version 12.0 (SPSS 2003), and sponse according to Trexler et al. (1988) and Juliano (2001). their mean values were compared with minimum significant The type III functional response equation was adjusted difference. for parasitoids, as shown in Table 3. In Figure 1, these type III functions are plotted together with their confidence limits Results at P = 0.05. The parasitization results of the E. kueniella eggs by Ch. If we compare the two type III equations adjusted for o oculator are shown in Table 1 according to temperature and each temperature (20 and 30 C) by extra sum of squares F density, in laboratory conditions. By ANOVA, highly sig- test, we find that they differ significantly (the null hypothesis nificant effects of temperature (F = 7.54, df = 4, P < 0.01), is rejected, F = 61.83; df = 3/8; P < 0.01). This indicates that host egg density (F = 13.59, df = 1, P < 0.01) and their inter- whilst there is no change in the functional response type, action (F = 7.14, df = 4, P < 0.01) were found. It is possible there is indeed an influence of the parameters due to the ef- to observe that the highest percentage of parasitized eggs was fect of temperature change, which evidently makes them dif- o o o obtained at 20 C; at 30 C the values were significantly ferent. Thus, handling times (Th) estimated at 30 C are 14 o lower at densities equal to or lower than 150 eggs, whilst at times longer than those estimated at 20 C (Table 3); on the higher densities there were no significant differences. The other hand, it has to be indicated that the other parameters (b o values of the two other temperatures trialled, 10 and 40 C and c) are just mathematical adjustment values without a bio- were significantly lower. logical interpretation.

With regard to the data collected, functional response In the actual handling times (T*h), occurring in the com- equations were adjusted only to those obtained at tempera- plementary trial, highly significant effects were observed (P 48 García-Martín et al.

Table 3. Parameters (0.05 confidence limits) and statistical significance for Hassell equation, type III, for numbers of Ephestia o kuehniella eggs parasitized by Chelonus oculator, at two temperature (20 and 30±1 C) and under laboratory conditions (60-80% R.H. and 16:8 h L:D).

Figure 1. Functional response of Chelonus oculator female parasitizing Ephestia kuehniella eggs, at two different temperature levels and under laboratory conditions (60-80% R.H. and 16:8 h L:D). (vertical lines represent standard errors of models, P = 0.05).

o < 0.01) with respect to temperature and to the parasitized that for other gender species it is known that 20 Cisthe host egg (P < 0.05). The mean values were significantly minimum temperature only for the development of Ch. sp. o lower at 30 (0.560 ± 0.142 min) than at 20 C (0.597 ± 0.144 nr. curvimaculatus (Hentz et al. 1998). min). These values were considerably lower than those de- o duced from the adjustment equations: 0.01031 days (= At the maximum temperature trialled (40 C), parasitiza- 14.846 min) and 0.00760 days (= 10.944 min, Table 3). tion and the subsequent development of the parasitoid prog- eny did occur, although with a very low percentage in all den- sities. In this case, unlike in the previous one, the effect was Discussion due to the high mortality caused by this temperature in the o host eggs, since it was observed that their mortality, exclud- At 10 C, the absence of parasitization was not due to the ing parasitism, was higher than 95%. It is known that tem- lack of development of the host, E. kuehniella, whose eggs o peratures from 35 to 40 C cause high mortality in the eggs of are capable of surviving at this temperature (Leopold 1998) this species and in those of the closely related species, E. cau- and of completing their post-embryonic development (Dau- mal et al. 1985). Instead, it was a consequence of the effects tella (Mason and Strait 1998, Navarro et al. 2002). On the of this temperature on the parasitoid, either on the adult level other hand, there are no known data for the maximum tem- or on the development of their progeny. For Ch. oculator, perature that is lethal for the Chelonus species. However, in there are the two previously mentioned effects. Firstly, no the egg parasite species Trichogramma cordubensis Vargas parasitization was observed at this temperature; moreover, in & Cabello and T. pintoi Voegelé there is high mortality in o o o host eggs parasitized at 25 C and transferred at 10 C, the developmental stages at 40 C (Cabello 1985, Cabello and o parasitoid larvae were not capable of completing their devel- Vargas 1989) or even at a slightly lower temperature (37 C) opment (unpublished data). Likewise, we also emphasize as in T. pretiosum Riley (Lopez and Morrison 1980). Functional response of Chelonus to temperature 49

o o At the other two temperature levels (20 and 30 C), Ch. cur at the other temperature, 30 C, (14.690 min). For this oculator presents a type III functional response that coin- reason, in functional response studies it would be appropriate cides with that of Ch. blackburni Cameron (Ballal and Ku- to calculate both times for a better understanding of the be- mar 1991, García-Martín et al. 2005); but is different from haviour of the species. that presented by Ch. texanus Cresson, which is type II (Ul- However, the above statement does not explain that fe- liett 1949, Holling 1959, Hassell 1978). It is necessary to o males with greater activity at 30 C have a higher estimated point out that other braconid species also present a type III time (Th*). This may be influenced by the decision of the response (Montoya et al. 2000, Rakhshani et al. 2004) and adult entomophagous parasitoid (or predator) to abandon the this is relatively important in other hymenopteran species as patch (Hassell 1978), which in the case of the parasitoid is well (Jones et al. 2003, Wang et al. 2006, Chen et al. 2006, fundamentally determined by the rate of encounter with pre- Wang and Ferro 1998; Reay-Jones et al. 2006). With regard viously parasitized eggs (van Alphen and Jarvis 1997). In Ch. to these discrepancies, we have to point out that in various o oculator, values of the number of eggs parasitized at 30 C entomophagous species (predators and parasitoids) their were presented, up to a density of 200, below these values at functional response can change from type II to type III when o 20 C (Fig. 1) which can representative this tendency; only they are offered non-natural or inadequate prey or hosts (van with higher densities was the value higher, probably due to Alphen and Jervis 1997). This is not considered to be the rea- o the fact that at 20 C, as females use more time to search, satu- son for the different types of curves among Chelonus species, ration will be reached, when no more time for the search is since in all cases alternative, non-natural hosts were used (E. available (T = 1 day). Therefore, patch residence time is a kuehniella for Ch. texanus and Ch. oculator and Phthori- value that should be taken into account in functional response maea operculella (Zeller) for Ch. blackburni); therefore, the studies in laboratory conditions, since it can mask the results obtained differences should be due to the biological charac- obtained. teristics of each species. According to the results obtained for type III functional The form of functional response type III curves pre- response concerning Ch. oculator, this species is a good can- sented by Ch. oculator, is generally attributed to an increase didate for biological control programmes against beet army- in the parasitization rate with an increase in the host density, worm in greenhouse crops, due to two facts. 1) As mentioned up to an inflection point, from which level it decreases above, there are no natural enemies in greenhouses, which (Hassell 1978). Thus, temperature seems to affect the density o could permit us to simulate what happens in ‘classical’ bio- ranges which trigger this behaviour. At 20 C, Ch. oculator logical control. 2) By inoculative releases, we can proceed in reaches inflection point with around 100 host eggs, whereas o such a way that they act in the long run, regulating the sub- at 20 C, this occurs with the highest densities (200 and 250 sequent pest generations occurring during the crop cycle. All eggs, Table 1). this is based on the fact that this type of response, as men- On the other hand, the handling time estimated in the tioned above, is the only one considered adaptive depending functional response equations (Th) was 1.4 times lower at 20 on the density of the host and with good potential for regu- o than at 30 C (Table 3). In other entomophagous species, lating the host population. However, the differences between longer times have been discovered when temperature in- laboratory and field studies as stated by Mills and Getz creases (Flinn and Hangstrum 2002, Menon et al. 2002). (1996), as well as the results found in the present study, sug- Conversely, the actual handling times (Th*) obtained through gest that the control agent potential should be corroborated direct observation, were almost 1.1 times lower at 30 than at by studies carried out in a greenhouse. o 20 C; in this case similar results have been found in other Acknowledgements: This work has been financed by the species (De Clercq et al. 2000, Schenk and Bacher 2002). European Union, Fifth Framework, Life Quality Programme, The latter result, in which adult Ch. oculator females pre- project: Development of an environmentally-friendly protec- sent a shorter action time at a higher temperature is logical. tion for sweet pepper and strawberry (ref.: QLK5-CT-2001- 70484). Finally, the authors are grateful to the anonymous This can be due to the fact that parasitization behaviour is a referees for their valuable comments. complex phenomenon which includes various events, as has been pointed out by several authors (van Alphen and Jarvis 1997, Powell and Poppy 2001, Wang and Messing 2003). In References each of these events, as in the activity of any adult insect, temperature has a marked influence (Goldsworthy and Joyce Ballal, C.R. and Kumar, P. 1991. Response of Chelonus blackburni 2001), affecting its physiological activity rate. (Hym.: Braconidae) to different ages and densities of potato tu- ber moth eggs. BioControl 36: 513-518. The discrepancy between actual and estimated time may Barlow, N.D. 1999. Model in biological control: a field guide. In: be due, to the fact that the latter includes both handling time, Hawkins, B.A. (ed.), Theoretical Approaches to Biological until the parasitoid (or predator) has left the host (or prey) and Control. 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