The diet of entomophagous coccinellids is mainly based on aphids and other food sources such as pollen, nectar, or fungal spores. Knowledge of their foraging behavior on plants infected by powdery mildew and their survival on fungal spores is currently limited. In this study, we investigated the olfactory response of Coccinella septempunctata to odor emission of barley plants infected by powdery mildew and their survival on fungal spores in the presence or absence of aphids. Odors released by powdery-mildew infected plants were more attractive for ladybirds compared to those of uninfected controls. After 3 days, the survival rate of ladybirds feeding only on powdery-mildew spores was less than 50%, while for ladybirds feeding exclusively on Rhopalosiphum padi aphids, the survival rate was close to 90%. After 15 days, the highest survival rate (almost 80%) was observed for ladybirds feeding on plants with both aphids and powdery mildew. Molecular analyses confirmed the presence of fungal spores in ladybird guts when feeding either on powdery mildew or on a mixed diet. Our results provide new insights into foraging behavior of entomophagous coccinellids revealing the potential of powdery mildew to be utilized as important non-essential food in a mixed diet, but also its lethal effect if consumed alone. Keywords Ladybird · Mixed diet · Olfactory response · Fungal spores · Blumeria graminis · Rhopalosiphum padi Introduction far, there is no Coccinellid species for which the complete dietary breadth is entirely known (Weber and Lundgren Coccinellids are a heterogeneous group of insects divided 2009). into three major categories according to their food prefer- Entomophagous coccinellid species regularly consume ences: zoophagous (predating), phytophagous (plant eating), non-prey food such as pollen and nectar (Togni et al. 2016), and mycophagous (fungus eating) (Giorgi et al. 2009). Pred- honeydew and plant parts (Giorgi et al. 2009), and fruits atory ladybirds have evolved from mycophagous ladybirds and fungi (Triltsch 1997). These types of food are an impor- that first were adapted for feeding on sooty molds, but then tant component of diets for many ladybirds as an additional accepted the insects that produce honeydew such as aphids source of energy and often necessary for the development (Leschen 2000). Most predatory ladybirds feed on honey- (Lundgren 2009a). Analyses of gut content have shown that dew-producing insects from the hemipteran suborder Ster- fungal spores can be taken up by, e.g., Coccinella septem- norrhyncha, which they need to complete development. So punctata, and even be more frequently present than prey body parts, especially at low aphid abundance (Triltsch 1999). Putman (1964) suggested that eating on the fungal Handling Editor: Heikki Hokkanen. spores by C. septempunctata happens fully accidentally, but according to Sutherland and Parrella (2009), fungal spores * Velemir Ninkovic can be important seasonal food for ladybirds. The impor- email@example.com tance of the presence of this type of non-prey food in lady- Faculty of Agriculture, University of Belgrade, bird diet and impact on their foraging behavior are poorly Zemun-Belgrade, Serbia understood. Department of Cell and Molecular Biology, Uppsala Entomophagous coccinellids actively utilize olfactory University, Uppsala, Sweden cues associated with the prey odor (Francis et al. 2004), Department of Ecology, Swedish University of Agricultural aphid-infested plants (Ninkovic et al. 2001; Togni et al. Sciences, Box 7044, 750 07 Uppsala, Sweden Vol.:(0123456789) 1 3 686 A. Radonjic et al. 2016), or the combination of both (Jamal and Brown 2001). (Vicia faba). Ladybirds were reared under the same condi- Mycophagous ladybirds showed strong preference to charac- tions as the test-plants. The adults in the experiments were teristic odors released by squash plants infected by powdery 3–4 weeks old. Rhopalosiphum padi used in the experiments mildew showing that such cues can play important roles in were reared on potted oat cv. Belinda under the same grow- ladybird foraging behavior (Tabata et al. 2011). Non-prey ing conditions as infected plants, but in a separate chamber. food sources such as fungi are components of entomopha- gous coccinellid diets, but still we know almost nothing Plants infested by aphids and infected by powdery about how they locate infected plants. Detection and loca- mildew tion of non-essential food such as fungi could be accidental or mediated by odors associated with fungus-infected plants. Barley cv. Annabell was used in the experiments since it had To explore C. septempunctata foraging for powdery mil- been observed to have a high occurrence of ladybirds when dew, we tested their response to the odors from infected and infected with powdery mildew in the field. Ten plants per pot uninfected barley plants using a two-arm olfactometer. We at the two-leaf stage were infested with R. padi (20 aphids also investigated if powdery mildew would constitute an per plant). Seven days after infestation, when the number of appropriate diet for ladybirds and if they eat it as a single aphids per plant was around 100, the plants were used for food or in combination with Rhopalosiphum padi. bioassays. Powdery-mildew infected plants were obtained by infect- ing barley plants at the two-leaf stage by shaking infected Materials and methods plants above healthy plants. Seven days after inoculation, when lesions were visible, the plants were exploited for Powdery mildew experiments. Plants treated with both aphids and powdery mildew were An isolate of powdery mildew, Blumeria graminis f. sp. obtained by releasing 20 aphids per plant on plants that were hordei (Bgh), was obtained from Lantmännen SW Seed AB, infected by powdery mildew the day before. Seven days Svalöv, Sweden. For propagation of powdery mildew, the later, the plants were used in bioassays. Each pot with ten highly susceptible barley cultivar (cv.) Steffi was used. Plants plants (treated or control) was placed in a Plexiglas cylinder were grown in a greenhouse and maintained at 18–22 °C (Ø 6.8 cm, height 32.8 cm, thickness 2 mm) and the top of with a light regime of L16:D8. Ten plants per pot (Ø 12 cm, the cylinder was sealed with a square of powdery-mildew height 9 cm) were grown in potting soil (Special Hasselfors proof cloth and tightened with a rubber band. garden, Hasselfors, Sweden). Barley plants infected 7 days earlier with B. graminis were used to inoculate 10-day-old plants (second leaf start to develop) with B. graminis by Olfactometer bioassay shaking infested plants above healthy plants. Infected plants were covered with Plexiglas cylinders (Ø 10 cm, height Olfactory responses of ladybird adults were measured using a two-way airflow olfactometer consisting of two stimulus 32.8 cm, thickness 2 mm) closed on the top by a square of felt and a rubber band. Plants were incubated in a climate zones (arms) directly opposite of each other, with a central neutral zone separating them (Ninkovic et al. 2001). Air was chamber at 18–22 °C with a light regime of L16:D8 and relative humidity 70% for 5–7 days, until new sporulating drawn from the center of the olfactometer using a vacuum pump, establishing discrete air currents in the side arms. lesions of powdery mildew formed on the leaves. Airflow in the olfactometer was set to 180 ml/min, measured with a flow meter at the arm inlets. Each arm of the olfac- Insects tometer was connected to a cage containing the plants. Three different arrangements were set up (1) barley infested by Seven-spotted ladybird, Coccinella septempunctata, adults were collected from natural habitats close to Uppsala, Swe- R. padi in one cage versus healthy barley plants in another cage, (2) barley infected by powdery mildew versus healthy den (59°47′00.0″N, 17°39′00.0″E) and reared through at least five generations before they were used in experiments. barley plants, and (3) barley infected by powdery mildew versus barley infested by R. padi. A single ladybird, ran- Ladybirds were reared in cages (40 × 40 × 80 cm). They fed on mixed diet consisting of bird cherry-oat aphid (Rhopa- domly chosen without sex determination, was introduced into the olfactometer and after an adaptation period of losiphum padi), green peach aphid (Myzus persicae), pea aphid (Acyrthosiphon pisum), and pollen of flowering white 10 min, its position was recorded every 2 min over a 20-min period. The number of tested individuals per combination mustard (Sinapis alba). Aphids were reared on specific host plants; R. padi on barley (Hordeum vulgare), M. persicae varied from 21 to 23. Ladybirds remaining immobile for longer than 10 min were discarded. Each ladybird was tested on rape seed (Brassica napus), and A. pisum on broad bean 1 3 The phytopathogen powdery mildew affects food-searching behavior and survival of Coccinella… 687 only once. After each tested individual, the olfactometer was Results cleaned using 70% ethanol. Ladybird olfactory responses Test of ladybird survival Odors released from stressed plants (powdery-mildew The effect of diets on ladybird survival was investigated in infected or aphid infested) influenced the olfactory four different treatments: (1) plants infected with powdery responses of C. septempunctata (Fig. 1). The odors of mildew, (2) plants infested with R. padi, (3) plants both powdery-mildew infected plants evoked a positive behav- infected with powdery mildew and infested with R. padi, ioral response by ladybirds compared to the odor of unin- and (4) control plants without aphids or powdery mildew. fected controls (Wilcoxon test: Z = 2.663, P = 0.0077, After 7 days of treatment, one ladybird was introduced in n = 21; Fig. 1a). The odor of R. padi infested plants also each cylinder. Ladybirds had access to water through a cot- evoked a positive behavioral response by ladybirds com- ton wool plug connected to the water in a small container pared to the odors released from non-infested plants (Wil- placed near the plant. Every third day, we recorded alive or coxon test: Z = 2.84, P = 0.0045, n = 23; Fig. 1b). There dead ladybirds during an experimental period of 15 days. was no difference in ladybird olfactory responses when Dead ladybirds were collected at each observation and put they had a choice between the odor of powdery-mildew in − 20 °C. Ladybirds still alive at day 15 were also put in infected and aphid-infested barley plants (Wilcoxon test: − 20 °C. All ladybirds were kept there until DNA analysis Z = 0.243, P = 0.807, n = 22; Fig. 1c). of gut content. DNA extraction and PCR Ladybird survival Isolated guts were placed in Eppendorf tubes, flash frozen The overall test comparing all four treatments showed with liquid nitrogen, and homogenized with a sterile pestle. that the ladybird survival rate was strongly dependent Total DNA was extracted by a Qiacube automated extraction on the type of diets (P = 0.0301) (Fig. 2). Pair-wise com- robot (Qiagen) using the QIAamp DNA mini kit (Qiagen). parisons of effects of diet showed that the survival rate PCR in 25 µl reactions was performed with Illustra PuReTaq was significantly higher for ladybirds with mixed diet Ready-To-Go PCR Beads (GE Healthcare, Uppsala, Swe- compared to control (P = 0.04) and compared to powdery den) according to Chen et al. (2015) using primers for B. mildew (P = 0.0069). After Bonferroni adjustment, only graminis BF-F1 (5′-AAG CTA TGC GGA ACT TCG TTT-3′) the comparison between mixed diet and powdery mildew and BF-R (5′ - TT A GGA G TT TT G GCA AG T CCC-3′). The remains significant (P = 0.0288). Already after 3 days, the PCR program was as follows: 94 °C for 5 min, followed survival rate of ladybirds kept on powdery mildew alone by 35 cycles of [94 °C for 50 s, 68 °C for 50 s, 72 °C for was reduced to 44% which was significant compared to 50 s] followed by a final extension step at 72 °C for 10 min. ladybirds provided with a mixed diet (100%; P = 0.0085) Amplification products were sequenced at Macrogen (South or aphids (89%; P = 0.045), but not to the starvation con- Korea). Isolated guts of 17 ladybirds were individually trol (78%; P = 0.1469). These results clearly demonstrate DNA-extracted and analyzed with PCR for the presence of that feeding only on powdery mildew strongly reduced B. graminis. the survival rate of the ladybirds. The next considerable reduction of the survival rate was observed on day 9 when Statistical analyses only 22% of the control ladybirds were still alive compared to 78% still alive on the mixed diet (P = 0.001). Until day The number of visits to one or the other arm of the olfac- 6, the survival rate for ladybirds kept on the starvation tometer was compared using Wilcoxon matched pairs tests in control was at the same level as those kept on the mixed the SAS statistical package Dell Statistica software (2015). diet or on the aphids alone, but from day 9 and until the The survival data were analyzed using the non-parametric end of the experiment the survival rate on the starvation survival analysis approach proposed by Kaplan and Meier control was at the same level as on the powdery-mildew (1958). The Life test procedure of the SAS (2014) package diet. The mixed diet consisting of R. padi and powdery was used. The conclusions were based on the Log-rank test. mildew resulted in the highest survival rate, 78% at day 15, Pair-wise comparisons were adjusted for multiplicity using while 56% of the ladybirds reared on R. padi alone were the Bonferroni method. Tests comparing the survival at each alive at day 15 (Fig. 2). time point were performed as exact Chi-square tests, i.e., Chi-square tests where the p value was calculated using a randomization test approach, similar to Fisher’s exact test. 1 3 688 A. Radonjic et al. (a)10 Median 25%-75% 9 Min-Max n = 21 P = 0.0077 Fig. 2 Survival rate of ladybirds reared on four different diets; only barley, powdery-mildew infected barley, aphid-infested barley, and 0 barley with aphids and powdery mildew. The number of tested lady- P. mildew infected plants Undamaged plants birds per diet was 9. Different letters indicate significantly different values (Chi-Square test; P < 0.05) (b)10 Median 25%-75% Min-Max n = 23 Detection of powdery mildew in ladybird guts P = 0.0045 PCR was used to detect the presence of powdery mildew 6 in ladybird guts after different diets. All ladybirds feed- ing exclusively on powdery mildew had PCR products of the size corresponding to B. graminis. Also, one of the five starvation controls indicated the presence of powdery mildew. All of these PCR products were sent for sequenc- ing confirming that they belong to powdery mildew. In contrast, no PCR products were obtained for ladybirds fed exclusively on aphids while only one weak PCR product was observed for a ladybird that had the access to both Aphid infested plants Undamaged plants powdery mildew and aphids (Table 1). (c) Median 25%-75% Min-Max n = 22 Discussion P = 0.807 An observation of a high number of C. septempunctata 6 ladybirds in barley fields infected by powdery mildew, but with extremely low aphid abundance, prompted us to inves- tigate the mechanism of the high ladybird abundance imply- ing the possibility of their survival on powdery mildew. In this study, we have shown that the odor of plants infected 2 by powdery mildew, or the odor of aphid-infested plants, have strong attracting effects on walking behavior of lady - birds compared to the odor of unaffected plants (Fig. 1a). P. mildew infected plants Aphid infested plants Table 1 Presence of powdery mildew in ladybird guts after different Fig. 1 Olfactory responses of ladybirds, Coccinella septempunctata, diets as detected by PCR to different odor sources: a powdery-mildew infected plants and Control R. padi Powdery P. undamaged plants as control, b aphid-infected plants and undamaged mildew padi + Pow- plants as control, and c powdery-mildew infected plants and aphid- dery mildew infested plants. Box and whisker plots represent the cumulative num- ber of visits in the arm zone after ten observations. Each box includes Total number 5 4 4 4 the middle 50% of the data; the dot symbol denotes the median value. Number with Blumeria 1 0 4 (1) The whiskers (vertical lines) indicate a minimum or maximum num- graminis ber of visits of a tested insect; n number of tested insects, P probabil- ity calculated by Wilcoxon matched pairs test PCR band of the correct size, but too weak to be sequenced 1 3 Observations in odor field Observations in odor field Observations in odor field The phytopathogen powdery mildew affects food-searching behavior and survival of Coccinella… 689 No differences in ladybird attraction between barley plants (56% dead at day 3), whereas ladybirds residing on control infected by powdery mildew and aphid-infested plants were barley plants (and thus considered starving) started to die observed (Fig. 1c). These results suggest that the odors of much later (80% still alive at day 6). High intake of less attacked/damaged plants can provide important signals for appropriate food may have a toxic effect and may potentially ladybirds in their search for essential and non-essential cause their death. How predatory ladybirds cope with toxin food. The highest survival rate of ladybirds was observed burden may depend on their energy status as well as their on plants with aphids and powdery mildew while the low- ability to withstand toxins. Well-fed predators may be able to est survival rate was found for ladybirds living on plants invest more in detoxification (Sherratt et al. 2004). In order infected with powdery mildew alone, indicating that a mixed to improve its energy status, ladybirds may consume non- diet consisting of non-essential and essential food is benefi- preferable food to get balanced range of important nutrients, cial. Powdery-mildew infection can thus be an additional resulting in a better survival rate than only on a non-pref- stimulus for predatory ladybirds in the search of more diver- erable or preferable food source (Fig. 2), as is assumed by sified food, but alone it is not an appropriate diet for them. the model of self-selection of optimal diets (Waldbauer and Finding appropriate food for predatory insects is partially Friedman 1991). The fungi in mixed diet, as shown in pre- guided by emission of plant volatiles induced by insect feed- vious studies (Triltsch 1997, 1999; Sutherland and Parrella ing (Ninkovic et al. 2001; de Vos and Jander 2010) making 2009), can thus be important seasonal food for ladybirds. attacked plants attractive for natural enemies (Gencer et al. Taken together, data from this study and observations 2017), a phenomenon described as “cry for help” (Dicke made in the field, show that odors released from stressed and Baldwin 2010). Different plant stresses can induce plants can attract ladybirds to habitats with the presence changes in chemical composition of volatiles (Li et al. of both non-essential and essential food. Such foraging 2013; Ninkovic et al. 2011, 2013). For instance, the odor behavior suggests that ladybirds choose a feeding site with of barley plants infested by R. padi make them attractive for diversified food that may increase their survival rate via a C. septempunctata (Ninkovic et al. 2001). In this study, we balanced diet. show that the odor of plants infected by powdery mildew can Acknowledgements This study is dedicated to the late Professor Jan have significantly stronger attracting/arresting effects on C. Pettersson, for his kindness, endless scientific support, and his selfless- septempunctata than the odor of undamaged plants, almost ness that always will be remembered. The study was financially sup- at the same level as the odor of aphid-infested plants. For ported by the Swedish Research Council for Environment (FORMAS) (Project Number 2014-225) and by the Ministry of Education, Science mycophagous ladybirds it is known that they are attracted and Technological Development of the Republic of Serbia (Project by “moldy” odorants reported as fungal volatiles, but not by Number III 46008) and by the Carl Tryggers Stiftelse för Vetenskaplig elevated quantities of several compounds also present in the Forskning (Project Number 12:333). We gratefully acknowledge Pro- volatiles of healthy plants (Tabata et al. 2011). Interestingly, fessor Ulf Olsson for statistical support and Dr. Dimitrije Markovic for valuable comments. ladybirds did not prefer the odor of aphid-attacked plants over the odor of plants infected by powdery mildew, sug- Author contributions AR and VN conceived and designed the study; gesting that either the different types of plant stresses induce AR performed experiments; VN performed statistical analysis of similar compounds and/or that the ladybirds are attracted to the data; AR and VN drafted the manuscript; OT performed DNA both kinds of damages. For either of these options, the data analyses; VN and OT finalized the manuscript. All authors read and suggest that the odors induced can be important signals for approved the paper. ladybirds in their food-searching behavior. Open Access This article is distributed under the terms of the Crea- Powdery mildew developed on the leaf surface has tive Commons Attribution 4.0 International License (http://creat iveco been considered to be consumed accidentally by ladybirds mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- (Sutherland and Parrella 2009). Instead, our molecular tion, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the analysis of gut content of ladybirds that had only access to Creative Commons license, and indicate if changes were made. powdery mildew showed that they are able to consume it actively. However, their survival was significantly affected; after only 3 days almost 56% were dead and after 15 days the mortality of all individuals reached 78%. 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