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Functional Response and Predation Potential of Hyperaspis Campestris (Herbst 1783) (Coleoptera: ) on Opuntiae Cochineal Opuntiae (Hemiptera: Dactylopiidae) in Morocco

Mohamed El Aalaoui,1,4*, Rachid Bouharroud,1 Mohamed Sbaghi,2 Mustapha El Bouhssini,3 and Lahoucine Hilali,4 1Integrated Crop Production Unit, Regional Center of Agadir, National Institute of Agronomic Research, Morocco. Emails: [email protected] (Corresponding author) and [email protected], 2National Institute of Agronomic Research, Plant Protection Department, Scientific Division, Rabat Morocco. Emails: [email protected] 3 International Center for Agricultural Research in the Dry Areas (ICARDA), Rabat, Morocco. Email: [email protected] 4Faculty of Science and Technology of Settat, Morocco. Email: [email protected] *Corresponding author: [email protected],

Article Info Abstract: Volume 82 Functional response of the lady Hyperaspis campestris (Herbst 1783) Page Number: 5976 - 5985 to varying densities (1, 5, 10, 15, 20 and 25) of Dactylopius opuntiae Publication Issue: (Cockerell) young females (20 days old) were determined under controlled January-February 2020 conditions at 26±2°C, 60±10 % RH and 12:12 h L:D regime. The searching efficiency of H. campestris considerably decreased as prey density increased. The significant linear coefficient (P1) obtained by logistic regression had a negative indicating functional response type II. Attack rates (0.151, 0.101, 0.097, 0.122, 0.124 and 0.135) and handling times (3.848, 5.171, 5.417, 4.245, 4.356 and 3.940) for 1 to 25 density, respectively, were recorded using Holling‘s disc equation. Most of this handling time was spent in removing the wax covering and protecting the young females of the mealybug. H. campestris feeds on young females of D. opuntiae and could Article History therefore be an effective predator to regulate to low-density populations of Article Received: 18 May 2019 D. opuntiae. Revised: 14 July 2019 Accepted: 22 December 2019 Keywords: Biological control, Functional response, D. opuntiae, Publication: 29 January 2020 Hyperaspis campestris, Cactus

Introduction as cattle feed ( Kiesling 1999; Bouharroud Cactus is one of the most important et al. 2016). It is cultivated in Africa, economic crop worldwide (Kiesling 1999). Europe, Asia, America, Africa, Canada, It plays an critical role in the ecological Peru, Cuba, and other Caribbean islands system in semi-arid and arid areas, (Casas & Barbera 2002; Bravo Hollis & preventing desertification and preserving Scheinvar 1995; Griffith 2004). In , is also exploited as a Morocco, cactus was first introduced in vegetable source for human, and cladodes 1770 from south Africa and the cactus area

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has considerably evolved over the last two The damage caused by this scale pest to decades from 50 000 ha in 1998 to more fruit and cladodes in Mexico resulted than 150 000 ha at present as a result of higher production and economical costs drought (Bouharroud et al. 2016). Mann (Badii & Flores 2001; Portillo & Vigueras (1969) reported that there are 167 2006). Also in Lebanon and Israel a pest species associated to cactus risk analysis of the was carried out (Opuntiae ficus indica). Among these to protect natural areas covered by O. , Dactylopius opuntiae (Cockerell) ficus-indica (Spodek et al. 2014). D. is the most devastator pest of prickly pear opuntiae is mostly controlled by cactus in Mexico (Githure et al. 1999; organophosphate insecticides such as Portillo & Vigueras 2006), Brazil (Silva et cypermethrin and chlorpyrifos which can al. 2013), Israel and Spain (Spodek et al. affect human health, the environment, and 2014) and recently Morocco and others limit international commercial exchange Mediterranean areas (Bouharroud et al. (Vanegas-Rico et al. 2016). Many 2016; El Aalaoui et al., 2019a; El Aalaoui alternative strategies such as the use of et al., 2019b). This sap-sucking insect was predators have been used around the world first detected and identified in Morocco in to reduce pesticides use for D. opuntiae 2014 (Bouharroud et al. 2016) and caused control (Vigueras et al. 2009; Borges et al. severe damage to prickly pear in many 2013; Vanegas-Rico et al. 2016). Natural regions of kingdom. D. opuntiae feed enemies associated with Dactylopius directly on cladodes, and severe species include much predators belonging infestations inferior or equal to 75 % of the to Lepidoptera, Coleoptera, Diptera and cladode surface can result a death of the Neuroptera groups (Grissell 2004; El host plant (Mann 1969; Vanegas-Rico et Aalaoui et al., 2019b). Coccinellidae al. 2015). This hemipteran females have 3 Hyperaspis trifurcata and Chilocorus cacti life stages – egg, nymph or crawlers (2 are the most predators of D. opuntiae in instars), and adult, lived permanently USA and Mexico (Vanegas-Rico et al. attached to their host cladodes, and 2016). After detection of D. opuntiae in produce wax cottony that protects their Morocco, surveys were conducted in bodies against predators, and reduces the different cactus production areas with a potency of pesticides, the female survival view to find biological control agents with time varies from 90 to 128 days, also each the potential to be used as a predators female can laid more then 130 eggs, which against this scale pest. In July 2017, hatch almost simultaneously into crawlers Hyperaspis campestris was observed on (Badii & Flores 2001). whereas males cactus crop actively feeding on cactus have 5 life stages egg, nymph, pre-pupa, mealy bug (D. opuntiae) in Sidi Bennour, pupa and adult, male is short lived without region (Bouharroud et al. 2019). A few feeding and moves predominantly by studies showed the utilization of H. walking (Badii & Flores 2001). No campestris as biological control agent. informations are available today on Hyperaspis campestris Herbst was able to economical and environmental losses reduce the population of pulvinaria caused by D. opuntiae, in Morocco, where floccifera (Westwood) within two years of it is not native, around 400 ha of cactus release (Bogdanova 1956). Also damaged by this insect at Sidi Bennour in Hyperaspis spp. eggs are generally Doukkala region have been reported. The deposited near their prey, on the bark or cochineal is today present almost in all growth rings of twigs, but not inside the Morocco regions. In Brazil the degas scales (El-Ali 1972). However, in Hubbard caused by this scale pest were estimated at and Potter‘s (2005) study in Kentucky, $25 Million Dollar (Lopes et al. 2009). Hyperaspis spp. emerged only from under

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adult females. The body length measured 2 in (1980-81) and (1996-97). The rainfall to 5 mm (Van Goethem 1975; Gunst annual average of 30 years is 330 mm. 1978). The head is yellow with black on Temperature varies in -1°C (Dec-Jan) and upper side hidden by from 40 to 45 (July-August). For soil there pronotum(Bouharroud et al. 2019). The are two zones: Zone 1: Vertisol with an anterior pronotum border was yellow and angular structure over the first 15 cm and the sides are partially yellow(Bouharroud with high moisture content, deep up to 1.5 et al. 2019). The red spot is typically m, difficult to work in dry conditions. placed at three-quarter part of elytron. The Zone 2: Light soil with a clay-sand-silty humeral spots is absent (Van Goethem hydromorphic structure with an alkaline 1975). Ph (Khattabi et al. 2004). A version modified of the ‗cut cladode technique‘ of The functional response is defined by the Aldama-Aguilera and LlanderalCazares number of preys devoured by predator in (2003) described by Vanegas-Rico et al. well determined time and is a good (2016) was used to follow the age and to indicator of the efficiency of a biological increase numbers of scale insect. The control agent as a predator of prey attacked cladodes were then maintained (Fernàndez-Arhex & Corley 2004). Most under controlled conditions at 26±2 °C, coccinellids showed type II response 60±10 % RH and 12:12 h L:D regime and (Gunog & Donald 2011). Many models the colony was allowed to develop for use have adopted in the past to explain the in experiments. interaction between predator and prey (Omkar 2004). Holling disc equation was Predator source the most model used to describe this During surveys, the adults of Hyperaspis interaction (Holling 1959, Fenlon & campestris were collected from cactus Malcolm 2006). This method is frequently plantations in Zemamra locality, identified used to calculate handling time parameters, (Bouharroud et al. 2019; El Aalaoui et al. the attack rate and maximum attack 2019b), and maintained on cladodes coefficient of predators (Omkar 2004). infested with D. opuntiae until there use The aim of this study was to determine the under controlled conditions (26±2°C and type of functional response of 60±10% relative humidity) at the H.campestris on D. opuntiae, to estimate experimental station of INRA (National its predation parameters (handling time Institute of Agronomic Research, and attack rate), and to have an idea about Morocco) in Zemamra. Adults were kept the suitability of this ladybeetle as a in entomological cages (80-80-80cm) predator of Opuntiae scale in Morocco. comprised of a wooden frame with a mesh fabric to allow ventilation. Access to water Material and Methods was ensured via a white cotton inserted Mealybug source into a 25 ml glass vial of water. To provide Opuntia ficus-indica cladodes no infested food the cladodes attacked with D. were used for Dactylopius opuntiae opuntiae nymphs were introduced into the rearing. The Opuntiae scale (D. opuntiae) cages (Vanegas-Rico et al. 2016). During colony was established from specimens rearing a mixture diet with honey, collected from zemamra locality. This area brewer‘s yeast and water in a ratio of is located at the following coordinates: 40%:40%:20% was offered. Dreyer et al. longitude W8° 22, latitude N 32° 21 and (1997) reported that honey increase altitude 168m. The estate is in the semi- survival time of Hyperaspis notata arid ecological zone. Rainfall varies Mulsant. between 112.6-607 mm/year respectively

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Experimental procedure respectively. If P1 is negative, that Each adult of H.campestris was placed represent functional response type II and if individually in Petri dishes (9.5 cm P1 is positive that indicates prey density- diameter) and starved for three days in dependent predation and thus represent a order to standardize their hunger. A fixed functional response type III. number of scale pest adults young females Both, random attack equation (Rogers (20 days) were collected and added to each 1972) and Holling disc equation (1959)— Petri dish to obtain a prey density of 1, 5, 푁푒= 푎푇푁0/(1+a 푁0 푇ℎ) — were adopted 10, 15, 20 or 25. D. opuntiae, young to calculate the functional response females are acceptable prey for H. parameters (handling time (Th) and attack campestris due to their smaller size rate (푎)): 푁푒 represent the number of scale (personal observation). For a given pest consumed by each ladybeetle, 푎 predator, there is a size of acceptable prey represent the attack rate of predator, 푁0 the (Sabelis 1992). After 24 h, the adults initial number of scale pest offered, 푇 is predators were eliminated and young the experiment duration (24 hours) and 푇ℎ females consumed were recorded (Flores the prey handling time estimated. et al. 2013). Completely randomized block design with ten replicates were used The ladybeetle searching efficiency ( 퐸 ) for each predator-prey density combination was recorded using the equation E= 푁푒/N0 and all experiment was replicated three (Flores et al. 2013). The high number of times. To preserve prey density for each scale pest females consumed (푁푒푚) and predator, prey replacement was done prey searching time (푇푠) were recorded during the period of the study (24 hours) 푇 using the equations: 푁푒푚 = (Elliot (Rogers 1972). All experiments of this 푇ℎ study were done under controlled 2003) and 푇푠 = 푇 − 푇ℎ푁푒 (Juliano & Williams 1987). conditions (26±2 °C, 60±10 % RH and 12:12 h L:D regime). The significance difference in number of Functional response supping scale pest females consumed at The functional response type was recorded different densities, in maximum attack by logistic regression fitted to the rate, and in searching time was recorded proportion of adult females devoured using analysis of variance ANOVA (SPSS 2012). For searching efficiency, Fisher test 푁푒/N0 against the number of adult females was adopted for multi-comparisons offered (N0) using the XLSTAT (XLSTAT 2017). This kind of regression provides between significant treatment effects more admirable results than the linear where they appeared, using STATISTICA (ver. 6) software. regression of 푁푒 against N0 (Pervez 2005). The equation reported by Juliano (2001) describes the relationship Results The results showed a significant difference between 푁푒/N0 and N0 is as follows: (F = 20.686, df = 5, p < 0.05) between the 2 number of preys devoured by 푁푒 /N0=(exp(P0+P1N0+P2N0 +P3N 3 2 3 H.campestris at different prey densities. 0 ))/(1+exp(P0+P1N0+P2N0 +P3N0 )), The maximum consumption was recorded at densities between 15 and 25 prey, and it was significantly higher (p<0.05) than that Where P0, P1, P2 and P3 indicated the intercept coefficient, linear coefficient, recorded at the lowest densities (1, 5, 10) quadratic coefficient and cubic coefficient (Fig 1; Fig 2).

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Fig 1 Numbers of D. opuntiae young females consumed by H. campestris at different prey densities (푇= 24 h).

A B

Fig 2. Adults of Hyperaspis campestris from prickly pear plantations infested with D. opuntiae in Morocco, A. Hyperaspis campestris feed on D. opuntiae young females, B.

The highest coefficient of determination 0.122, 0.124 and 0.135) and handling (R2= 0.9765) indicated that cubic times (3.848, 5.171, 5.417, 4.245, 4.356 polynomial was the model that gave the and 3.940) for 1 to 25 density, best fit (p<0.05) to the observed data (푁푒), respectively, were determined using with. Attack rates (0.151, 0.101, 0.097, Holling‘s disc equation (Table1).

Table 1 Effect of density upon the instantaneous rate of discovery and the handling time. Density N0 Inst. rate of discovery Handling times (Th) (푎) 1 0.151±0.053 3.848±1.686 5 0.101±0.015 5.171±0.742 10 0.097±0.016 5.417±0.930 15 0.122±0.018 4.245±0.646 20 0.124±0.027 4.356±1.219 25 0.135±0.031 3.940±0.841

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The predator searching efficiency (퐸) significantly decreased as prey density increased from 1 to 15 and does not significantly change from 15 to 25 (Fig 3).

Fig 3 Searching efficiency of H. campestris at different D. opuntiae female densities. Bars with different letters are significantly different according to the Fisher test (alpha= 0.05).

In addition, a change in adult handling and 25 densities, respectively (Table 2). It time indicates a change in the response significantly increased as scale pest level, which is determined by females density increased from 1 to 25 (f= instantaneous rate of discovery (푇/푇ℎ) or 5.701, df= 5, p< 0.05). The total searching maximum attack rate. Maximum attack time decreased significantly and the total rate values were 3.961, 4.056, 4.260, handling time increased (p<0.05) at 5.440, 5.701, and 6.214 for 1, 5, 10, 15, 20 different scale pest densities (Fig 4).

Table 2 Maximum attack rates (푇/푇ℎ) estimated for all six densities of D. opuntiae. Mean values of 푇ℎ estimated by non-linear least squares regression using Holling‘s ―disc equation‖.

Density N0 1 5 10 15 20 25 Max. 3.961 4.056 4.260 5.44 5.70 6.21 attack rate ±1.75 ±1.03bc ±1.14b ±0.59a ±1.40a ±1.43 (푇/푇ℎ) c c bc b a Bars with different letters are significantly different according to the Tukey‘s test (alpha=0.05).

Fig 4 Inverse relationship between the total handling time (Tht) and total searching time (Tst) of H. campestris preying on D. opuntiae young females, obtained by the estimated parameter 푇ℎ and the equation 푇푠 = 푇 − 푇ℎ푁푒.

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Discussion high D. opuntiae females density can be A negative value of linear coefficient (P1 comparable with field conditions where = -0.675) obtained by logistic regressions the prey density is also high (Omkar of proportion of scale pest females 2004), due to heavy D. opuntiae consumed ( 푁푒 /N0) against number of infestation. Also Akhtaruzzaman & females initially provided (N0) to adults of Ahmad (1998) recorded that handling time ladybeetle H.campestris over 24 hours, of each predator was higher at lower pest indicated that the functional response density. Variation in predator and prey exhibited by this predator was type II size, predator voracity, predator satiation (Holling 1959). Many types of functional time, predator hunger levels, predator response are described for ladybird species digestive ability, predator walking speed (Hodek 1996). Among these types, type ІІ and accessibility to prey are the most and ІІІ considered most important factors that must be affected total handling (Murdoch et al. 2003), because most time of each biological control agent natural enemies show these types. Oaten & (Pervez 2003, Omkar 2004). Although Th Murdoch (1975) reported that response and 푎 were generally constant at all type II may destabilize biological control densities of prey and consumed prey is agent-prey interactions and is theoretically density dependent, in practice this is not less able to remove prey populations usually true even in a functional response compared to response type III. Hassell et type II (Flores et al. 2013). The highest al. (1977) reported that in the response Maximum attack rates recorded at hight type II, consumed prey intensity does not prey density (25 females) may be increase with prey density. In same case explained by these suggestions: the Hodek & Honek (1996) recorded that engorgement of predator on the first prey hungry predators completely devour the they encounter then become less limited preys they encounter and then competent to exploit the prey, the predator utilize subsequent prey with progressively consumes more than the minimum reduced voracity. The decrease of the required for growth when prey is abundant proportion of prey consumed with (Honek 1996), or the combination of these increasing of prey density, may be due to factors. the effect of various phenomena, such as the size of experimental arena, handling Feeding on D. opuntiae young females and time and degree of hunger of the shorter life cycle of H.campestris in ladybeetle (O‘Neil & Stimac 1985, 1988). comparison with D.opuntiae could be Prey handling time of the predator was beneficial for its use as a predator for the relatively higher (ranging 3.848±1.686– control of this scale pest. The searching 5.417±0.930 hours) at different densities efficiency of H.campestris at different of D. opuntiae females (1 to 25 females). D.opuntiae young female densities Because of D. opuntiae females cover indicates that it may become less potent at themselves with white waxy cottony and high scale pest densities. Therefore, remain attached to the cladode, H.campestris would be an effective H.campestris spent most of the 푇ℎ predator at the early stages of the invasion, cleaning the waxy cotonny to access the this is the case today in many regions of adult females bodies (Flores et al. 2013). Morocco. H.campestris adult consumes This ―cleaning‖ process uses time not first and second instar crawlers of D. required by other predatory insects that opuntiae but cannot consume gravid have direct access to their uncovered prey females (personal observation). A few (Flores et al. 2010; Flores et al. 2013). studies showed the utilization of The experimental data on handling time at H.campestris in biological control.

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Bogdanova (1956) reported that 6. BOUHARROUD R., EL AALAOUI M., H.campestris Herbst was able to reduce BOUJGHAGH M., HILALI L., EL the population of pulvinaria floccifera BOUHSSINI M. & SBAGHI M. 2019. New (Westwood). Scale populations were Record and Predatory Activity of Hyperaspis reduced below the economic injury level campestris (Herbst 1783) (Coleoptera: Coccinellidae) on Dactylopius opuntiae two years after release (Bogdanova 1956). (Hemiptera: Dactylopiidae) in H. campestris Herbst, a predator of scale Morocco. Entomological News 128 (2): 156- insects on citrus, grapes and other 161. subtropical crops, was release against 7. BORGES L.R., SANTOS D.C., FALCAÕ Pulvinaria floccifera (Westwood) H.M. & DA SILVA D.M. 2013. Selection of (Bogdanova 1956). Hyperaspis spp. were cactus pear clones regarding resistance to also able to reduce Eulecanium cerasorum carmine cochineal Dactylopius opuntiae (Cockerell) fecundity by 48% (Robayo (Dactylopiidae). Acta Horticulurae 995: 359– 2015). Much previous research on 366. biocontrol potential around the world 8. BRAVO HOLLIS H. & SCHEINVAR L. reported that biological control agents 1995. El interesante Mundo de las cactäceas. Mexico, National Council of Science and predation could be modulated by other Technology. predators (Kratina et al. 2009), the density 9. CASAS A. & BARBERA G. 2002. of the prey, the diversity and density of Mesoamerican domestication and diffusion. other non-prey species (Kratina et al. In P.S. Nobel, ed. Cacti: Biology and uses, 2007). Abiotic factors can also modify the pp.143–162. Berkeley, CA, USA, University functional response of predators. So of California Press. further studies under Morocco ecological 10. DREYER B.S., NEUENSCHWANDER P., system conditions need to be carried out to BAUMGÄRTHER J. & DORN S. 1997. confirm the predation potential of Trophic influences on survival, development H.campestris on D. opuntiae in Morocco. and reproduction of Hyperaspis notata (Coleoptera: Coccinellidae). Journal of Applied Entomology 121: 249–256. References 11. EL AALAOUI M., BOUHARROUD R., 1. ALDAMA-AGUILERA C. & LLANDERAL- SBAGHI M., EL BOUHSSINI M., HILALI CÁZARES C. 2003. Cochineal: comparison of L. & Dari K. 2019a. Comparative toxicity of production methods in cut cladodes. different chemical and biological insecticides Agrociencia 37: 11–19. against the scale insect Dactylopius opuntiae 2. AKHTARUZZAMAN M. & AHMAD M. and their side effects on the predator 1998. Handling time, interference constant, Cryptolaemus montrouzieri. Archives of quest constant and area of discovery of Phytopathology and Plant Protection 52 (1- coccinellid predators. Journal of Agricultural 2): 155-169. Science (Thailand) 31: 342–351. 12. EL AALAOUI M., BOUHARROUD R., 3. BADII H.M. & FLORES E.A. 2001. Prickly SBAGHI M., EL BOUHSSINI M. & Hilali, pear cacti pests and their control in Mexico. L. 2019b. Predatory potential of eleven native The Fla Entomol 84: 503–505. Moroccan adult ladybird species on different 4. BOGDANOVA N.L. 1956. Hyperaspis stages of Dactylopius opuntiae campestris Herbst (Coleoptera: (Cockerell)(Hemiptera: Coccinellidae) as the destroyer of Dactylopiidae). EPPO Bulletin 49(2), 374- chloropulvinaria floccifera west 379. (Homoptera: coccidoidea). Entomologi 13. EL-ALI A.A. 1972. A biosystematic study of cheskoeo bozreniz 35: 311-322. Hyperaspini of California with emphasis on 5. BOUHARROUD R., AMARRAQUE A. & the immature stages. Ph.D. dissertation, QESSAOUI R. 2016. First Report of the University of California, Berkeley. Opuntia Cochineal Scale Dactylopius 14. ELLIOT J.M. 2003. A comparative study of Opuntiae (Hemiptera: Dactylopiidae) in the functional response of four species of Morocco. EPPO Bulletin 46 (2): 308–10.

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