INTRODUCTION
⌅The functional response of a predator describes the number of prey that an individual consumes as the density of the prey increases (11. Holling CS. The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol. 1959; 91(5):293-320. DOI: 10.4039/Ent91293-5.). It is an important concept in the field of ecology and evolution, also useful in the understanding of population dynamics at different trophic levels (22. Jeschke JM, Laforsch C, Diel P, Diller JGP, Horstmann M, Tollrian R. Predation. In: Mehner T, Tollrian, eds. Encyclopedia of Inland Waters (Second Edition); Elsevier. 2022: 207-221pp. https://doi.org/10.1016/B978-0-12-819166-8.00016-5 ). The predator will consume a greater number of prey as density increases, and the maximum number of prey it can consume is determined by satiety (maximum consumption capacity) or by the maximum time available to manipulate the prey (22. Jeschke JM, Laforsch C, Diel P, Diller JGP, Horstmann M, Tollrian R. Predation. In: Mehner T, Tollrian, eds. Encyclopedia of Inland Waters (Second Edition); Elsevier. 2022: 207-221pp. https://doi.org/10.1016/B978-0-12-819166-8.00016-5 ). The functional response is considered a criterion that allows the evaluation of the potential of a predator to be used as a biological control agent within a pest management program (33. Uiterwaal SF, DeLong JP. Multiple factors, including arena size, shape the functional responses of ladybird beetles. J Appl Ecol. 2018; 55(5):2429-2438. https://doi.org/10.1111/1365-2664.13159 , 44. Hassanzadeh-Avval M, Sadeghi-Namaghi H, Fekrat L. Factors influencing functional response, handling time and searching efficiency of Anthocoris minki Dohrn (Hem.: Anthocoridae) as predator of Psyllopsis repens Loginova (Hem.: Psyllidae). Phytoparasitica. 2019; 47(3):341-350. https://doi.org/10.1007/s12600-019-00739-w , 55. Munyaneza J, Obrycki JJ. Functional response of Coleomegilla maculata (Coleoptera: Coccinellidae) to Colorado potato beetle eggs (Coleoptera: Chrysomelidae). Biol Control. 1997; 8(3):215-224. DOI: 10.1006/bcon.1997.0509.).
There are three types of functional responses, the type I response describes a linear increase in the number of prey consumed until a maximum consumption rate is reached, where the number of consumed prey remains constant despite the increase in prey density. In the type II functional response, the rate of consumption by a predator rises at a decelerating intake rate as prey density increases, until reaching an asymptote (hyperbolic curve) at which the rate of consumption remains constant regardless of increases in prey density. The type III response is described as a sigmoid curve, at low densities the number of consumed prey is reduced, but as the number of prey increases the rate of consumption also increases, until the limit is reached (44. Hassanzadeh-Avval M, Sadeghi-Namaghi H, Fekrat L. Factors influencing functional response, handling time and searching efficiency of Anthocoris minki Dohrn (Hem.: Anthocoridae) as predator of Psyllopsis repens Loginova (Hem.: Psyllidae). Phytoparasitica. 2019; 47(3):341-350. https://doi.org/10.1007/s12600-019-00739-w , 66. Fernández-Arhex V, Corley J. La respuesta funcional: Una revisión y guía experimental. Ecol Austral. 2004;14(1):83-93., 77. Escolástico C, Cabildo M, Claramunt R, Claramunt T. Ecología II: comunidades y ecosistemas. Madrid, España: Universidad Nacional de Educación a Distancia; 2013; 299pp. ISBN: 9788436251616.).
The attack rate, handling time and exposure time of the prey to the predator are the factors that determine the functional response of a predator (88. Li Y, Rall BC, Kalinkat G. Experimental duration and predator satiation levels systematically affect functional response parameters. Oikos. 2018; 127(4):590-598. https://doi.org/10.1111/OIK.04479 , 99. Pervez A. Functional responses of coccinellid predators: an illustration of a logistic approach. J Insect Sci. 2005; 5(1):5. https://doi.org/10.1093/jis/5.1.5 ). Handling time is a term that involves different aspects of the predator's behavior, since it refers to the time it takes for the predator to capture, subjugate, kill, and digest the prey (1010. Sakaki S, Sahragard A. A new method to study the functional response of Scymnus syriacus (Coleoptera: Coccinellidae) to different densities of Aphis gossypii. J Asia Pac Entomol. 2011; 14(4):459-462. https://doi.org/10.1016/j.aspen.2011.07.003., 1111. DeLong JP. Predator ecology: Evolutionary ecology of the functional response. Oxford, U.K.: Oxford University Press. 2021; 176 pp. ISBN-13: 9780192895509.). Handling time and attack rate are inversely proportional, high handling time leads to low attack rates, since the predator will spend a longer time on each prey reducing the number of attacks per unit of time. On the other hand, high attack rates are the consequence of short handling time (77. Escolástico C, Cabildo M, Claramunt R, Claramunt T. Ecología II: comunidades y ecosistemas. Madrid, España: Universidad Nacional de Educación a Distancia; 2013; 299pp. ISBN: 9788436251616.).
Novius punicus (Gordon) and Novius cardinalis (Mulsant) (Coleoptera: Coccinellidae) are predators of the Colombian fluted scale Crypticerya multicicatrices Kondo and Unruh (Hemiptera: Monophlebidae: Iceryini), which was reported as an invasive insect in the archipelago of San Andrés, Providencia and Santa Catalina in 2010 (1212. Kondo T, Rincón DF, Pérez-Álvarez R, Vásquez Ordóñez AA, González G. Capítulo 9. Uso de depredadores como agentes de control biológico para insectos plaga. In: Cotes AM, ed. Control biológico de fitopatógenos, insectos y ácaros. Volumen 1. Agentes de control biológico. Bogotá, Colombia: Editorial Agrosavia. 2018; 486-543., 1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394.). After a search for natural enemies in the place of origin of this pest (continental region of Colombia), these two coccinellid species were considered as potential control agents for this fluted scale (1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394.). The species N. punicus is native to the New World (1414. González G, Kondo T. Geographical distribution and phenotypic variation of Anovia punica Gordon (Coleoptera: Coccinellidae: Noviini), a predatory ladybeetle of fluted scales (Hemiptera: Coccoidea: Monophlebidae). Insecta Mundi. 2014; 0398:1-6., 1515. Pang H, Tang XF, Booth RG, Vandenberg N, Forrester J, McHugh J, et al. Revision of the Australian Coccinellidae (Coleoptera). Genus Novius Mulsant of tribe Noviini. Museum and Institute of Zoology, Polish Academy of Sciences. Annal Zool. 2020; 70(1):1-24.) and preys on scale insects of the tribe Iceryini such as Icerya purchasi Maskell and Crypticerya montserratensis (Riley and Howard) (1616. Kondo T, Gullan P, González G. An overview of a fortuitous and efficient biological control of the Colombian fluted scale, Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae: Iceryini), on San Andres island, Colombia. Acta Zool Bulg., Suppl. 2014;6:87-93.). Novius punicus is an important natural enemy of C. multicicatrices (1717. Kondo T, Manzano MR, Cotes AM. Biological Control in Colombia. In: van Lenteren JC, Bueno VHP, Luna MG, Colmenarez YC, eds. Biological Control in Latin America and the Caribbean: Its Rich History and Bright Future. Wallingford, Oxfordshire, U.K.: CAB International; 2020; 124-161 pp.), demonstrating a great predatory capacity on this pest. The immature and adult stages of this coccinellid feed preferably on the eggs of the fluted scale; however, it can also feed on nymphs (1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394.). It is common to find larvae of this predator inside the ovisacs of adult fluted scales, where they hold their eggs. This species is the main one responsible for the reduction in the populations of C. multicicatrices on the islands of San Andrés, Providencia and Santa Catalina in 2013 (1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394.). On the other hand, Novius cardinalis, until recently known as Rodolia cardinalis, is a species native to Australia (1414. González G, Kondo T. Geographical distribution and phenotypic variation of Anovia punica Gordon (Coleoptera: Coccinellidae: Noviini), a predatory ladybeetle of fluted scales (Hemiptera: Coccoidea: Monophlebidae). Insecta Mundi. 2014; 0398:1-6., 1515. Pang H, Tang XF, Booth RG, Vandenberg N, Forrester J, McHugh J, et al. Revision of the Australian Coccinellidae (Coleoptera). Genus Novius Mulsant of tribe Noviini. Museum and Institute of Zoology, Polish Academy of Sciences. Annal Zool. 2020; 70(1):1-24.) and preys mainly on species of the family Monophlebidae. Novius cardinalis has been used in successful biological control programs for I. purchasi (1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394., 1717. Kondo T, Manzano MR, Cotes AM. Biological Control in Colombia. In: van Lenteren JC, Bueno VHP, Luna MG, Colmenarez YC, eds. Biological Control in Latin America and the Caribbean: Its Rich History and Bright Future. Wallingford, Oxfordshire, U.K.: CAB International; 2020; 124-161 pp.). It was introduced to Colombia in 1948 to control I. purchasi in urban areas (1212. Kondo T, Rincón DF, Pérez-Álvarez R, Vásquez Ordóñez AA, González G. Capítulo 9. Uso de depredadores como agentes de control biológico para insectos plaga. In: Cotes AM, ed. Control biológico de fitopatógenos, insectos y ácaros. Volumen 1. Agentes de control biológico. Bogotá, Colombia: Editorial Agrosavia. 2018; 486-543.) and it has been reported preying on eggs and nymphs of C. multicicatrices (1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394.). Both species of coccinellid predators play an important role in reducing the population levels of C. multicicatrices in urban areas of Colombia where it occurs. For this reason, the objective of this study was to determine the functional response of N. punicus and N. cardinalis on eggs and first-instar nymphs of C. multicicatrices, respectively.
MATERIALS AND METHODS
⌅Insect rearing
⌅The individuals of N. punicus and N. cardinalis used in the experiments were taken from a rearing colony kept under laboratory conditions in Agrosavia, Caribia Research Center (temperature: 27.9 ± 2 °C, relative humidity: 65.3 ± 9.7 %). Individuals brought from the field were regularly added to the breeding stock to maintain genetic diversity within the population. Rectangular transparent plastic containers measuring 28 cm long x 18 cm wide and 13 cm high were used for maintaining the insects; the lid had a metal mesh (1 mm hole diameter) for ventilation. An average of 30 adult coccinellids were housed per container. Adults of N. punicus were fed with live adults of C. multicicatrices with fully developed ovisacs. On the other hand, the feeding of the adults of N. cardinalis consisted of first-instar nymphs of the fluted scale; in addition, the diets for both coccinellids were supplemented with pollen to stimulate oviposition. Individuals of C. multicicatrices used for feeding the coccinellids were collected in the field or brought from a breeding colony established in mesh house conditions; in both cases the host plant was mango (Mangifera indica L. variety “Azúcar”). Before offering the fluted scales as food, the specimens were checked to ensure that they were healthy (without fungi or affected by other natural enemies).
Every third day, 20 to 40 adult fluted scales were added to each N. punicus rearing plastic container (described above), and these were arranged in 9 cm diameter Petri dishes. Because the adults of the fluted scales also served as an oviposition substrate, the Petri dishes extracted from the rearing containers were preserved in order to recover larvae and pupae of N. punicus from the remains of the fluted scales, which were kept individually until the number of specimens needed for the experiments were obtained. In the case of N. cardinalis, plant structures infested with nymphs of C. multicicatrices were deposited in each rearing container every three days. When the plant structures were removed from the rearing containers, they were put under observation to recover coccinellid larvae, which were then kept individually in Petri dishes until the number of specimens necessary for the experiments was reached. The individuals of the two species of coccinellids that were not used in the trials were used to reinforce the breeding stock.
Functional response experiment
⌅The experiment was carried out under laboratory conditions at the Colombian Agricultural Research Corporation - Agrosavia, Caribia Research Center, (temperature: 27.9 ± 2.0 °C, relative humidity: 65.3 ± 9.7 %, photoperiod of 12:12 (h) Ligth to Dark), the abiotic variables were taken using a data logger (OM-EL-USB-2-LCD Omega®). In a completely randomized design, the coccinellid individuals were approximately 10 days old and were housed individually as larvae to ensure that they were age-compliant and that they had not mated before the trials. Although female coccinellids are commonly more voracious than males, we were not able to sex the adults by external morphological characters; therefore, the analyses were made for the adult stage regardless of sex related differences in prey consumption. This limitation should be taken into account when considering the results obtained.
The specimens chosen for the experiment were subjected to a 24-hour fast before the start of the experiment to standardize the hunger stimulus. The experimental units were composed of an adult coccinellid and different densities of the prey. For N. punicus, the prey population densities evaluated were 10, 25, 50, 100, and 200 eggs of C. multicicatrices. With N. cardinalis, densities of 10, 20, 50, 100, and 150 first-instar nymphs of C. multicicatrices were offered in the section of a mango leaf, where they were attached. In both cases, the coccinellids were kept individually in 9 cm diameter glass Petri dishes with dry filter paper at the bottom. The number of repetitions for each evaluated prey density was 10. The fluted scale prey was offered for a period of 24 hours, when the number of remaining prey was counted.
Statistical analysis
⌅For statistical data analysis the R v. 3.4.1 program (1818. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria; 2017. Available from: https://www.R-project.org/ [Accessed 02.06.2021]) was used, and for the functional response analysis the (frair) package (1919. Pritchard DW, Paterson RA, Bovy HC, Barrios O'Neill D. Frair: an R package for fitting and comparing consumer functional responses. Methods Ecol Evol. 2017; 8(11):1528-1534.) was used. In this study, the methodology described by Paterson et al. (2020. Paterson RA, Dick JT, Pritchard D, Ennis M, Hatcher MJ, Dunn AM. Predicting invasive species impacts: a community module functional response approach reveals context dependencies. J Anim Ecol. 2015; 84(2):453-463. https://doi.org/10.1111/1365-2656.12292.) was used to identify the type of functional response described by our data, conducting a logistic regression based on the proportion of consumed prey against the number of offered prey (frair: frair_test). If the result of the logistic regression is a significantly negative first-order term, then the data fit a type II functional response (2121. Juliano SA. Non-linear curve fitting: predation and functional response curves. In: Scheiner S, Gurevitch, J, eds. Design and Analysis of Ecological Experiments. Oxford: Oxford University Press. 2001; 178-196.).
Since the logistic regression indicated that the data for the two species of coccinellids fit a type II curve, the random predator equation (66. Fernández-Arhex V, Corley J. La respuesta funcional: Una revisión y guía experimental. Ecol Austral. 2004;14(1):83-93.) was used to describe the functional response. This equation defines a model where prey density decreases over time. The equation is as follows:
Where Ne is the number of eaten prey; N0 is the number of initial prey; T is the total time (for this experiment it is 24 h), α is the attack rate; and Th is the handling time. The model was adjusted using maximum likelihood estimation (frair: frair_fit).
RESULTS
⌅The results of the logistic regression show that the two species of coccinellids have a type II functional response. For both cases, the estimated value was negative and statistically significant (Table 1), which indicates that the curve of the proportion of eaten prey fits a function with a decreasing rate, characteristic of a type II functional response.
| Predator | Estimated | S.E. | Z-value | Pr (> |z|) |
|---|---|---|---|---|
| N. punicus | -0.0117 | 0.0006 | -21.295 | < 2.2 e-16 *** |
| N. cardinalis | -0.0100 | 0.0008 | -12.553 | < 2.2 e-16 *** |
*** Statistical significance at P < 0.001; Standard Error: S.E.
The functional response adjusted by the random predator equation for N. punicus and N. cardinalis are shown in Figures 1a and 1b, respectively. In the case of N. punicus, it can be observed that the relationship between the number of consumed prey and their density followed the typical curve of the type II functional response, clearly reaching an asymptote that shows the maximum rate of consumption of eggs of the fluted scale by this predator in a 24-hour period. On the other hand, the graph that describes the functional response of N. cardinalis feeding on first-instar nymphs of C. multicicatrices does not clearly show the predation limit in 24 hours, so it can be assumed that this coccinellid reaches its maximum rate of consumption at densities higher than those tested in this study.
The calculated parameters of the random predator equation are shown in Table 2. The attack rate of N. punicus on eggs of C. multicicatrices is higher than that observed in N. cardinalis preying on nymphs of Colombian fluted scale. On the other hand, the calculated handling time for N. cardinalis is 0.34 hours, and for N. punicus is 0.64 hours.
| Predator | Parameter | Estimate | S.E. | Z-value | Pr (> |z|) |
|---|---|---|---|---|---|
| N. punicus | α | 0.1191 | 0.0125 | 9.487 | < 2.2 e-16 *** |
| Th | 0.6423 | 0.0268 | 23.973 | < 2.2 e-16 *** | |
| N. cardinalis | α | 0.0542 | 0.0041 | 13.312 | < 2.2 e-16 *** |
| Th | 0.3441 | 0.0225 | 15.263 | < 2.2 e-16 *** |
*** Statistical significance at P < 0.001; Standard Error: S.E.
DISCUSSION
⌅Some authors have reported that there may be factors inherent to the experiment that make it difficult to differentiate between the curves that are characteristic of a type II and type III functional response, for example, not offering different numbers of prey at low densities, or not establishing an evaluation time that is in accord with the biological characteristics of the insect (66. Fernández-Arhex V, Corley J. La respuesta funcional: Una revisión y guía experimental. Ecol Austral. 2004;14(1):83-93., 2222. Rogers D. Random search and insect population models. J Anim Ecol. 1972; 1:369-383. https://doi.org/10.2307/3474 ). Logistic regression is an effective way to distinguish between type II and type III functional responses (2121. Juliano SA. Non-linear curve fitting: predation and functional response curves. In: Scheiner S, Gurevitch, J, eds. Design and Analysis of Ecological Experiments. Oxford: Oxford University Press. 2001; 178-196.). Carrying out a comparison using the proportion of eaten prey at different densities allows greater sensitivity in the differentiation of the curves that represent type II and type III functional responses.
Different equations can be used to describe the functional response of a predator, each of them is used to estimate different values for the attack rate and handling time. Rogers (2222. Rogers D. Random search and insect population models. J Anim Ecol. 1972; 1:369-383. https://doi.org/10.2307/3474 ) established that the random predator equation predicts the number of attacks that a predator can carry out in a given period of time, in a system where the exploitation of prey is allowed. This equation is suitable for systems where the density of the prey decreases as the predator consumes them (2121. Juliano SA. Non-linear curve fitting: predation and functional response curves. In: Scheiner S, Gurevitch, J, eds. Design and Analysis of Ecological Experiments. Oxford: Oxford University Press. 2001; 178-196.); that is, experiments where the prey are not replaced to maintain a constant density throughout the evaluation. It is common to find the type II functional response in predators of the family Coccinellidae [e.g. Sakaki and Sahragard (1010. Sakaki S, Sahragard A. A new method to study the functional response of Scymnus syriacus (Coleoptera: Coccinellidae) to different densities of Aphis gossypii. J Asia Pac Entomol. 2011; 14(4):459-462. https://doi.org/10.1016/j.aspen.2011.07.003.)]; this type of functional response is characterized by a decreasing proportion of eaten prey as prey density increases (1010. Sakaki S, Sahragard A. A new method to study the functional response of Scymnus syriacus (Coleoptera: Coccinellidae) to different densities of Aphis gossypii. J Asia Pac Entomol. 2011; 14(4):459-462. https://doi.org/10.1016/j.aspen.2011.07.003.); in addition, the maximum rate of consumption is determined by the handling time of the prey (55. Munyaneza J, Obrycki JJ. Functional response of Coleomegilla maculata (Coleoptera: Coccinellidae) to Colorado potato beetle eggs (Coleoptera: Chrysomelidae). Biol Control. 1997; 8(3):215-224. DOI: 10.1006/bcon.1997.0509., 66. Fernández-Arhex V, Corley J. La respuesta funcional: Una revisión y guía experimental. Ecol Austral. 2004;14(1):83-93.).
The experiments reported here were carried out in a relatively small area so the prey density per unit area could be very high, increasing the encounter rate between predator and prey and reducing the search time; on the other hand, the sedentary habit and size of the prey does not represent a major challenge for their submission by the predators. Thus, the difference in handling times presented by these species may be mainly due to their ability to consume and digest prey. In addition, Munyaneza and Obrycki (55. Munyaneza J, Obrycki JJ. Functional response of Coleomegilla maculata (Coleoptera: Coccinellidae) to Colorado potato beetle eggs (Coleoptera: Chrysomelidae). Biol Control. 1997; 8(3):215-224. DOI: 10.1006/bcon.1997.0509.) mentioned that the resting time can be an important component of the total handling time that a predator has on a given prey.
The differences observed in the parameters (α) and (Th) in the studied species reflect different feeding strategies. Novius punicus optimized the attack rate (α) by specializing in an immobile and confined prey (eggs in ovisac), but it showed a longer handling time (Th); in contrast, N. cardinalis had a lower attack rate (α) for a mobile prey (first-instar nymphs), which compensated with a shorter handling time (Th). This last characteristic is related to high rates of prey consumption.
FoRAGE (Functional Responses from Around the Globe in all Ecosystems) is a specialized database that includes more than 2000 entries of functional response experiments for all kinds of predators (2323. Uiterwaal SF, Lagerstrom IT, Lyon SR, DeLong JP. Data paper: FoRAGE (Functional Responses from Around the Globe in all Ecosystems) database: a compilation of functional responses for consumers and parasitoids. BioRxiv.2018. https://doi.org/10.1101/503334 ), among these, multiple coccinellid species. To put into context, the values of the parameters estimated in this experiment for N. punicus and N. cardinalis, the findings reported by other authors for functional response experiments with adults of various coccinellids species and various prey are summarized in Table 3.
The search efficiency values found in this study are similar to those reported by De Bortoli et al. (2424. De Bortoli SA, Gravena AR, Vacari AM, De Laurentis VL, De Bortoli CP. Resposta funcional da joaninha Cryptolaemus predando cochonilha branca em diferentes temperaturas e substratos vegetais. Rev Caatinga. 2014; 27(3):63-71.) for adults of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) (α = 0.01-0.05) preying on Planococcus citri (Risso) (Hemiptera: Pseudococcidae). In contrast, the handling time values are much lower than those reported for C. montrouzieri (Th = 0.94-3.36 hours) in the above experiment (2424. De Bortoli SA, Gravena AR, Vacari AM, De Laurentis VL, De Bortoli CP. Resposta funcional da joaninha Cryptolaemus predando cochonilha branca em diferentes temperaturas e substratos vegetais. Rev Caatinga. 2014; 27(3):63-71.), but much higher than those of other species with more mobile prey (Table 3).
| Predator (Coleoptera: Coccinellidae) | Prey | α (h-1) | Th (h) | T(°C) | Experimental unit |
Information source |
|---|---|---|---|---|---|---|
| Cryptolaemus montrouzieri Mulsant | Planococcus citri (Hemiptera: Pseudococcidae) | 0.03 | 1.47-7.61 | 25 | Petri dish 15 cm diameter | (2424. De Bortoli SA, Gravena AR, Vacari AM, De Laurentis VL, De Bortoli CP. Resposta funcional da joaninha Cryptolaemus predando cochonilha branca em diferentes temperaturas e substratos vegetais. Rev Caatinga. 2014; 27(3):63-71.) |
| Cryptolaemus montrouzieri Mulsant | Planococcus citri (Hemiptera: Pseudococcidae) | 0.01-0.05 | 0.94-3.36 | 30 | Petri dish 15 cm diameter | (2424. De Bortoli SA, Gravena AR, Vacari AM, De Laurentis VL, De Bortoli CP. Resposta funcional da joaninha Cryptolaemus predando cochonilha branca em diferentes temperaturas e substratos vegetais. Rev Caatinga. 2014; 27(3):63-71.) |
| Cheilomenes sexmaculata (Fabricius) | Aphis craccivora, Myzus persicae (Hemiptera: Aphididae) | 1.06 0.9 |
0.09 0.1 |
26-28 | Glass Beaker 8 x 11 cm | (99. Pervez A. Functional responses of coccinellid predators: an illustration of a logistic approach. J Insect Sci. 2005; 5(1):5. https://doi.org/10.1093/jis/5.1.5 ) |
| Propylea dissecta (Mulsant) | A. craccivora, M. persicae (Hemiptera: Aphididae) | 0.94 0.7 |
0.18 0.24 |
26-28 | Glass Beaker 8 x 11 cm | (99. Pervez A. Functional responses of coccinellid predators: an illustration of a logistic approach. J Insect Sci. 2005; 5(1):5. https://doi.org/10.1093/jis/5.1.5 ) |
| Coccinella transversalis Fabricius | A. craccivora, M. persicae (Hemiptera: Aphididae) | 1.05 0.94 |
0.09 0.14 |
26-28 | Glass Beaker 8 x 11 cm | (99. Pervez A. Functional responses of coccinellid predators: an illustration of a logistic approach. J Insect Sci. 2005; 5(1):5. https://doi.org/10.1093/jis/5.1.5 ) |
| Harmonia axyridis (Pallas) | Myzus persicae (Hemiptera: Aphididae) | 2.55 | 0.16 | 25 | Petri dish 9 cm diameter | (2525. Seko T, Miura K. Functional response of the lady beetle Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) on the aphid Myzus persicae (Sulzer) (Homoptera: Aphididae). Appl Entomol Zool. 2008; 43(3):341-345.) |
The functional response parameters of the predators N. punicus and N. cardinalis reflect the result of the specialization of these coccinellids in consuming scale insect prey of the tribe Iceryni (1313. Pinchao EC, Sotelo P, González G, Kondo T. Biological data on Anovia punica Gordon (Coleoptera: Coccinellidae), a predator of Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae). Neotrop Entomol. 2017; 47(3):385-394., 1616. Kondo T, Gullan P, González G. An overview of a fortuitous and efficient biological control of the Colombian fluted scale, Crypticerya multicicatrices Kondo & Unruh (Hemiptera: Monophlebidae: Iceryini), on San Andres island, Colombia. Acta Zool Bulg., Suppl. 2014;6:87-93.), where the developmental stages on which they carry out the greatest predation (eggs and first-instar nymphs) are of low mobility or are contained in the ovisac of adult females. These characteristics make N. punicus a species with a high affinity to its main prey and less prone to attack other non-target species.
Some authors have pointed out that for functional response studies to be useful to evaluate the potential of a species as a biological control agent, it is necessary to carry out the experiments in such a way as to include the greatest number of conditions that the insect predator will encounter in the field (1010. Sakaki S, Sahragard A. A new method to study the functional response of Scymnus syriacus (Coleoptera: Coccinellidae) to different densities of Aphis gossypii. J Asia Pac Entomol. 2011; 14(4):459-462. https://doi.org/10.1016/j.aspen.2011.07.003., 2626. Islam Y, Shah FM, Shah MA, Khan MM, Rasheed MA, Rehman SU, et al. Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects. 2020; 11(9):583. https://doi.org/10.3390/INSECTS11090583 , 2727. Messina FJ, Hanks JB. Host plant alters the shape of the functional response of an aphid predator (Coleoptera: Coccinellidae). Environ Entomol. 1998; 27(5):1196-1202. DOI: 10.1093/ee/27.5.1196.). Messina and Hanks (2727. Messina FJ, Hanks JB. Host plant alters the shape of the functional response of an aphid predator (Coleoptera: Coccinellidae). Environ Entomol. 1998; 27(5):1196-1202. DOI: 10.1093/ee/27.5.1196.) showed that the characteristics of the plant where the prey is found can alter the functional response of the predator. These authors found that Propylea quatuordecimpunctata L. (Coleoptera: Coccinellidae), showed a different type of functional response (type II or type III) when feeding on the aphid Diuraphis noxia Mordvilko (Hemiptera: Aphididae) depending on the architecture of the leaf, especially because of the shelter that these structures provide to the prey (2727. Messina FJ, Hanks JB. Host plant alters the shape of the functional response of an aphid predator (Coleoptera: Coccinellidae). Environ Entomol. 1998; 27(5):1196-1202. DOI: 10.1093/ee/27.5.1196.).
CONCLUSIONS
⌅The coccinellids N. punicus and N. cardinalis are both important predators of eggs and first-instar nymphs of C. multicicatrices, respectively. Both coccinellids have a type II functional response, in which the proportion of prey consumed decreases as the prey density increases. The attack rate and handling time parameters observed for N. punicus and N. cardinalis reflect the specialization of both species in consuming prey from the tribe Iceryini, in particular, eggs and newly emerged first-instar nymphs of the adult female fluted scales. Taking into account the experimental conditions of the study, it can be said that the differences in the number of consumed prey observed between N. punicus and N. cardinalis are mainly due to their ability to consume the prey. The present experiment is a first step in evaluating the potential of these coccinellid species to be used in a management program for C. multicicatrices.