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INTRODUCTION
Predator Coccinellidae play a significant role in the biological control of pests in many agricultural crops (Biddinger et al., 2009; Obrycki, 2009; Weber and Lundgren, 2009), due to their ability to search out and consume pests (Vandenberg, 2002). The neotropical lady beetle, Eriopis connexa (Germar), consumes several types ofpreys, but prefers to attack aphids (Hagen, 1962; Oliveira et al., 2004). Eriopis connexa has been studied as potential predator against pests in horticultural crops in the Neotropical region (Sarmento et al., 2007; Duarte Gómez and Zenner de Polanía, 2009; Harterreiten-Souza etal., 2012). In Brazil, this species is also commonly associated with pests of cultivated species, including key pests (Venzon et al., 2009; Harterreiten-Souza et al., 2012; Rodrigues et al., 2013).
Predation is an important biotic factor that reduces pest insect populations in the natural environment and can reduce the use of insecticides for pest control (Wiedenmann and Smith, 1997; Sarmento et al., 2007). In biological control, the relationship between prey density and consumption rate is known as functional response (Abrams and Ginzburg, 2000; Jeschke et al., 2002). Functional response describes the behavior of the predator as a function of consumption at different densities, thus suggesting the maximum prey consumption, as well as the predator's potential in population control (Murdoch and Oaten, 1975). According to Solomon (1969), the increase in prey availability may lead the predator to increased consumption, up to a certain limit, because the opportunities to attack prey will increase over time.
Holling (1959) and Jervis and Kidd (1996) outline four fundamental types of functional response curves. Type I corresponds to the consumption of prey by the predator resulting in a linear increase. Type II occurs when the rate of predation decelerated reaching an asymptote. Type III involves a sigmoid relation also called S ascension, and Type IV establishes a dome-shaped curve. A predator that exhibits a type III functional response has greater potential to control prey population, because the proportion of prey attacked increases with increasing density (Fernandez-Arhex and Corley, 2003). However, type II functional response is most common for invertebrate predators (Van Lenteren and Bakker, 1976), because of satiation (e.g. predators) and ability to produce eggs (e.g. parasitoids), as well as restricted handling and attack time.
Thus, this study aimed to determine the functional response of the E. connexa lady beetles preying on the aphids Brevicoryne brassicae (Linnaeus, 1758) and Aphis craccivora Koch, 1854 at different densities.
MATERIAL AND METHODS
The experiments were conducted in the Entomology Laboratory from February 2017 to August 2017: Federal University of Alagoas (UFAL), Rio Largo, AL, Brazil.
Obtaining and Rearing of Predator and Preys
The lady beetles used in the experiment came from the rearing kept at the Insect Biological Control Laboratory of Universidade Federal Rural de Pernambuco -UFRPE. Adults and larvae were reared according to the methodology described in Rodrigues et al. (2013). The adults were raised in 500 mL plastic containers with lid opening covered with voile fabric to allow air circulation. Pieces ofpaper towel were placed inside the containers for oviposition substrate. The laid eggs were transferred daily to 500 mL plastic containers and held until hatching. Then, the larvae were transferred in 80 ml plastic containers at the density of two larvae per container. Inside the container, paper towel pieces of about 2 x 2 cm were placed as substrate for pupation. The insects were fed Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) eggs, and in the adult phase were also offered a diet based on brewer's yeast and honey (1: 1).
The Aphis craccivora colony originated from lima beans (Phaseolus lunatus L.) (Fabaceae) grown in an experimental field of UFAL, in Rio Largo, AL, Brazil. These aphids were reared in cowpea plants (Vigna unguiculata (L.) Walp.) (Fabaceae), cultivar (Vita 7), susceptible to black aphid (Valente et al., 2014). Cowpea plants were cultivated in 500 ml plastic cups containing soil and substrate in the ratio of 1:1 in cages protected with anti-aphid mesh (4.0 cm x 4.0 cm x 0.4 cm), kept in a greenhouse. Then, 15 days after planting, the plants were infested by apterous females placed with tweezers. At five-day intervals, the insects were transferred to new plants. This procedure was performed routinely to maintain breeding stock and use in studies.
The Brevicoryne brassicae colony was collected in cabbage plants of cv. Georgia, Brassica oleracea var. acephala D.C. (Brassicaceae), naturally infested in the field, in the UFAL Olericulture Sector, in Rio Largo, AL. These insects were transported to the laboratory and screened to remove parasitized individuals. They were then transferred to potted kale plants and kept in cages with anti-aphid mesh (1.0 m x 1.0 m x 0.5 m) in a greenhouse.
Functional Response of Eriopis connexa on the aphids Brevicoryne brassicae and Aphis craccivora
The predation rate of the lady beetle E. connexa on the aphids B. brassicae and A. craccivora was determined at different prey densities. This bioassay used fourth instar larvae and one-day-old adults of E. connexa and apterous adult aphids of B. brassicae and A. craccivora. Larvae and adult lady beetles used in the study were deprived of food for 24 hours to regulate the level of satiety. Six aphid densities were tested (20, 40, 50, 60, and 70) for both species with 15 replicates per density. The densities were established from the average rate of daily consumption obtained in preliminary tests.
The aphids were offered on 5.0 cm diameter leaf discs. The aphid B. brassicae was offered on cassava leaf discs, while the aphid A. craccivora was offered on cowpea leaf discs. Beforehand, the leaves were washed with water, neutral detergent, and 0.5 % sodium hypochlorite. When dry, the leaf discs were placed in 6.5 cm diameter Petri dishes lined with filter paper lightly moistened with distilled water and subsequently infested with the prey at respective densities. The transfer of prey was carried out with the aid of tweezers. After transfering the aphids to the plates, they were closed with PVC plastic film for 24 hours for the insects to settle. Fourth instar larvae along with adult lady beetles were individually transferred to Petri dishes according to the corresponding treatment, where they remained for 24 h. After that period, we recorded the number of live aphids remaining in each replicate and control without the presence of the predator, as well as the number of live lady beetle in each treatment.
In the first analysis step, the shape of the functional response curve was determined by logistic regression for the proportion of prey consumed as a function of the original prey densities per predator using Proc CATMOD in the SAS program, following the protocol described in Juliano (1993). Initially, the cubic model was tested because of its ability to capture all possible variations of the functional response curves. Then, the terms of the equation were reduced until their significance was obtained. The sign of the linear term of the equation generated from the proportion of prey consumed/killed by prey density was used to determine the type of functional response. When not significant, it indicates Type I functional response; a negative indicates Type II functional response; and a positive functional response indicates Type III. The parameters determined in the second step were handling time (Ht) and attack rate (a') of the functional response. These parameters were estimated by non-linear regression using the least squares method (PROC NLIN of the SAS) according to the methodology described by Juliano (1993) and compared by 95 % confidence interval.
RESULTS AND DISCUSSION
The mean prey consumption by fourth instar larvae and adults of E. connexa at different densities of adult B. brassicae and A. craccivora tended to stabilize at higher densities, resulting in a type II functional response curve. The estimated attack rate and handling time were, respectively, 0.026 and 0.0.34 h-1 for larvae and 0.029 h-1 and 0.60 h-1 for adults preying on B. brassicae; and 0.59 and 0.35 h-1 for larvae and 0.70 and 0.95 h-1 adults preying on A. craccivora (Tables 1 and 2). Both larvae and adult E. connexa increased the number of aphids preyed on with increased prey density until reaching asymptote. They consumed a maximum mean of 30.3 and 31.6 of B. brassicae and 36.3 and 34.6 of A. craccivora, of larvae and adults, respectively.
Table 1 Holling disc equation and functional response type of Eriopis connexa larvae and adults preying on the aphids Brevicoryne brassicae and Aphis craccivora. 1 Intercept. 2 Linear coefficient. 3 Quadratic coefficient- 4 Functional response
Table 2 Handling time and attack rate of Eriopis connexa larvae and adults fed with the aphids Brevicoryne brassicae and Aphis craccivora.
The Holling disc equation fit the results for the different stages of the E. connexa lady beetle on the different densities of both aphids (Table 1). When the proportion of prey consumed decreased for both larvae and adults of E. connexa, for both species of aphids, the number of preys consumed increased (Fig. 1 and 2). Pervez and Omkar (2005), studying the predation behavior ofthree lady beetle species Cheilomenes sexmaculata (Fabr.), Propylea dissecta (Mulsant) and Coccinella transversalis (Fabr.) (Coleoptera: Coccinellidae) on aphids A. craccivora and Myzus persicae (Sulzer), observed that all the lady beetles presented type II functional response for both preys. However, the handling time was quite varied among lady beetle species. The predators used in the Pervez and Omkar (2005) had longer handling time than the one found in this study. This demonstrates that each predator exhibits different predatory behavior with increased availability of prey; some are more voracious, especially those exhibiting shorter handling time and higher attack rates. (Mills, 1982; Ofuya and Akinbohungbe, 1988; Pervez, 2004). Handling time is an important variable of a predator's effectiveness and consumption rate, since it reflects the time that they take to kill, consume, and digest the prey (Veeravel and Baskaran, 1997).
Figure 1 (a) Functional response of fourth instar larvae and (b) adults of Eriopis connexa in different densities of the aphid Brevicoryne brassicae. (c) Functional response of fourth instar larvae and (d) adults of Eriopis connexa at different densities of aphid Aphis craccivora.
This was clear in the present study, in which the attack and handling time were varied between the two aphid species offered. Both larvae and adults of E. connexa exhibited a less handling time and a lower attack rate praying on B. brassicae, than on A. craccivora (Table 1), which resulted in a higher predation on the latter species. This result was somewhat expected due to their different size, as well as other characteristics related to quality of prey, reflected in the prey species, as well as the age of the predator. Vieira et al., (1997) found that fourth instar larvae of Scymnus (Pullus) argentinicus (Weise, 1906) (Coleoptera: Coccinellidae) used less handling time and preyed on older instars of Schizaphis graminum (Rond.) (Hemiptera: Aphididae). This response of the predator can be attributed to the opportunity to encounter prey, which are greater depending on availability, time, and size. An increase in the availability of prey may lead to an increase in consumption, because prey is encountered more frequently, resulting in the consumption of an additional number of prey, even though the predator is already satiated (Garcia, 1990).
Type II functional response found for larvae and adults (Fig. 1) of E. connexa for both species of aphids, involves deceleration of the number of aphids consumed, due to the increase in their availability, and is the most common type of predation response among coccinellids (Atlihan and Ózgókce, 2002; Pervez and Omkar, 2005; Britto et al., 2009; Saleh et al., 2010; Atlihan et al., 2010). These results are also consistent with those obtained by Ofuya and Akingbohungbe (1988), in which the predator Cheilomenes luneta (Fabr.), feeding on the aphid A. craccivora presented a Type II functional response. Bortoli et al. (2014), evaluating the functional response of larvae and adults of lady beetle Cryptolaemus montrouzieri (Mulsant, 1850) on the cochineal Planococcus citri, also obtained type II functional response, for both phases.
Variable patterns of predation behavior are also a feature of E. connexa, which has various strategies when preying on different organisms. The lady beetle C. sanguinea (Linnaeus, 1763) presents type II response when preying on Tetranychus evansi (Thomas, 1878) (Acari: Tetranychidae). However, when the prey was the aphid Macrosiphum euphorbiae (Baker and Pritchard, 1960) (Hemiptera: Aphididae), it showed a type III functional response (Sarmento et al., 2007), which characterizes a predation behavior change according to the type of available prey.
These results are relevant because the potential consumption of the studied aphid species by the lady beetle E. connexa is not known, although this lady beetle has been observed associated with infestations of these aphids (Rodrigues et al., 2013; Costa et al., 2018). Future research should focus on the biological performance of this lady beetle species feeding on these preys, as well as other pests common in bean and brassica crops. The susceptibility of E. connexa to insecticides recommended for use in these crops should be tested to conserve this lady beetle populations in crops. This species of lady beetle has shown high resistance to pyrethroid insecticides, which do not or minimally control aphids (Torres et al., 2015; Costa et al., 2018), but are commonly used to control leafhoppers in host cultures of these aphids. Therefore, maintaining E. connexa in these agroecosystems is important for apply integrated pest management. This could validate the predation of B. brassicae by this lady beetle in the field, since they are commonly associated with brassica crops.
