Effects of Food Deprivation on the Development of Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae)

BIOLOGICAL CONTROL

Effects of Food Deprivation on the Development of Coleomegilla maculata (De Geer) (Coleoptera: Coccinellidae)

TM Santos-Cividanes^I; ACR dos Anjos^II; FJ Cividanes^III; PC Dias^IV

^IAgência Paulista de Tecnologia dos Agronegócios, Ribeirão Preto, SP, Brasil

^IIAgro Energia Santa Luzia Ltda, Nova Alvorada do Sul, MS, Brasil

^IIIDepto de Fitossanidade, Fac de Ciências Agrárias e Veterinárias, UNESP, Jaboticabal, SP, Brasil

^IVDepto de Parasitologia, Instituto de Biociências de Botucatu, Univ Estadual Paulista, Campus de Botucatu, Botucatu, SP, Brasil

^{Correspondence}

ABSTRACT

The lady beetle Coleomegilla maculata (De Geer) is a natural enemy of several insect pests and feeds on pollen and nectar to survive periods when prey is scarce. The effect of the feeding interval on the development, survival, fecundity, and longevity of C. maculata was determined. Newly hatched larvae of C. maculata were reared individually and fed with eggs of the Mediterranean flour moth Anagasta kuehniella (Zeller) at intervals of one, two, and three days under controlled conditions (23 ± 1ºC; 60 ± 10% RH; 12 h phtophase). The duration of larval instars and the total larval stage was prolonged as the feeding interval increased. The larval period lasted on average 9.2 ± 0.19 days when the larvae were fed daily with prey, and 14.6 ± 0.48 days when food was offered at three-day intervals. There was an inverse relationship between food intervals, survival, and weight of larvae and adults of the coccinellid. Survival rate of larvae fed daily was 76.8%, while the rate was 50.0% and 23.4% for larvae fed every two and three days, respectively. Coleomegilla maculata showed fecundity of 781.1 ± 149.02, 563.4 ± 80.81 and 109.0 ± 103.0 eggs when fed daily and at intervals of two and three days, respectively.

Keywords: Biology, biological control, lady beetle, predator, prey availability

Introduction

Agricultural ecosystems contain large numbers of predatory insects and Coccinellidae represents 90% of such beneficial insects that act as natural controls of insect pests (Iperti 1999, Musser & Shelton 2003).

The lady beetle Coleomegilla maculata (De Geer) is widely distributed in Canada, in the United States, and in Central and South America (Gordon 1985). It is a natural enemy of aphids, mites, and eggs and larvae of coleopterans and lepidopterans (Hodek 1973, Weeden et al 2007), and also feeds on pollen and nectar to survive periods when prey is scarce (Hodek & Honek 1996, Lundgren et al 2004).

Studies on the development and reproduction of C. maculata have been determined on several kind of diets such as eggs of Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae), aphids as Aphis gossypii Glover and Schizaphis graminum Rondani (Hemiptera: Aphididae) (Rondon et al 2006, Michaud & Jyoti 2008) and pollen (Michaud & Grant 2005, Pilorget et al 2010). However, Lundgren et al (2004) pointed out that C. maculata reaches the adult stage and it is able to reproduce on a diet composed solely of pollen and water.

The ability to survive and reproduce even in periods of prey scarcity is one characteristic that qualifies an efficient predator (Declercq & Degheele 1992). Therefore, this important attribute must be considered when choosing insect predators for use as pest-control agents (Nakashima & Hirose 1999).

Scarcity of prey can adversely affect the development, survival, and fecundity of lady beetles (Obrycki et al 1998, Agarwala et al 2001, Schüder et al 2004), and food deprivation seems to differently affect each insect species (Phoofolo et al 2008, 2009).

In agroecosystems, coccinellids are subject to alterations in prey availability according to biotic and abiotic factors (Phoofolo et al 2008). Prey availability in the ecosystems is an important factor that influences the development and growth of coccinellids, reducing their adult size, what can affect their potential as predators and thus influence their efficiency as biological control agents (Agarwala et al 2008, Phoofolo et al 2009). In the present study, we determined the effect of the feeding interval on larval performance and reproductive traits of C. maculata in the laboratory by offering prey at intervals of one, two and three days. This information can contribute in the evaluation of the potential of this predator as a biological control agent.

Material and Methods

Adults of C. maculata were collected in a cornfield in Andradina municipality, São Paulo state, Brazil. The insects were transferred to the laboratory and kept in five pairs in containers (10 cm high by 10 cm diameter). Each container was covered internally with sulfite paper as a substrate for egg laying. The adults were given eggs of Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) as a food source disposed at the bottom of the cage along with inflorescences of sorghum and a mixture of yeast and honey (1:1) brushed on a strip of Parafilm®. Water was supplied by moistened cotton placed in 10ml jars. The internal covering of the containers was changed daily, and the eggs were kept in Petri dishes (12 cm in diameter). The newly hatched larvae were fed with A. kuehniella eggs until pupation.

To evaluate the development of C. maculata, newly hatched larvae were isolated and fed with A. kuehniella eggs offered at intervals of one, two, and three days. The amount of eggs offered in each one of these intervals was 3.0 ± 0.10 mg, 5.5 ± 0.29 mg, 11.6 ± 0.69 mg, 24.5 ± 1.52 mg and 16.4 ± 0.94 mg, respectively, for first, second, third and fourth instars and adults. Each experimental unit consisted of a glass tube (8 cm in height by 2.5 cm in diameter) containing one individual of the predator and the prey eggs. The number of larvae assigned to each treatment was 30, with each larva being considered a replicate. The insects were kept under controlled conditions (23 ± 1ºC, 60 ± 10% RH, 12h photophase). The following biological parameters were evaluated: duration and survival of each instar; fresh weight of larvae at six and eight days of age; and duration and survival of the larval, pupal, and larva-adult stages.

In the adult stage the lady beetles were fed at the same intervals as the larvae. Pairs of C. maculata were tested for the feeding intervals of one and of two days. Only two pairs of adults originated from larvae subjected to feeding at three day intervals. The adult insects were weighed 24h after emergence and were observed daily to evaluate the pre-oviposition, oviposition, and post-oviposition periods, daily and total egg-laying capacity, and longevity.

To evaluate the young and adult stages, we used a completely randomized design and submitted the data to analysis of variance and whenever differences were detected, averages were compared by the Tukey test (P < 0.05).

Results and Discussion

Except for the first instar, the duration of the remaining instars of C. maculata increased with the feeding interval. Larvae fed daily remained longer in the first instar than did those fed with A. kuehniella eggs at two-day intervals. However, there was no statistically significant difference in the duration of the first instar between the larvae fed at intervals of one and three days (Table 1).

The C. maculata larvae fed at three-day intervals had longer development periods from the second to the fourth instars (Table 1). The variation in duration of the instar as a function of the feeding interval was more pronounced in the fourth instar. This probably occurred because during this instar the predator consumes more prey than in the previous ones (Lanzoni et al 2004), what may represent 80% of their total prey consumption (Hodek & Honek 1996).

Phoofolo et al (2008) reported similar results in relation to this study. These authors evaluated the development of coccinellid H. axyridis during the fourth instar when fed with the aphid S. graminum at intervals of one, two, three, four, and five days. They observed that the development time of this stadium increased significantly with the period of food restriction.

In the present study, the development time of the larval and larval-adult stages of C. maculata lengthened as the feeding interval increased, but the pupal period was not influenced by the feeding interval to which the predator was submitted (Table 1), as observed for C. maculata, H. convergens, and H. axyridis (Phoofolo et al 2008).

Coleomegilla maculata larvae offered prey daily, developed 1.1 and 5.4 days faster when compared to larvae fed at two- and three-day intervals, respectively (Table 1).

The lengthening of the development period is a mechanism that allows insects to survive to inadequate nutrition during the larval stage, as it allows insects to extend their feeding activity to acquire enough food resources to complete growth (Shafiei et al 2001). Probably, if C. maculata has a prolonged larval stage under field conditions, this should provide more opportunity to the coccinellid to find and consume large quantities of prey. However, it is not advantageous to prolong pupal stage due to an increase in mortality risk by natural enemies and/or weight loss (Phoofolo et al 2008).

The survival of C. maculata instars was not significantly influenced by the feeding interval, except for the second instar (Table 1). However, survival during the larval and larval-adult stages was lower for specimens fed at three-day intervals in comparison with those fed daily. During larval development, survival rate was 76.8% when fed daily, while 50.0% when fed every two days. Under conditions of food availability at intervals of three days, the amount of prey consumed by C. maculata larvae was not sufficient to promote development and growth, since only 23.4% reached the adult stage. According to Schüder et al (2004), lady beetle larvae react to a shortage of food by developing more slowly, but a lower amount of food increases mortality at all immature stages. Obrycki et al (1998) also reported lower survival rates of C. maculata as a function of food deprivation. According to them, when C. maculata larvae were offered 20 individuals per day of the pea aphid A. pisum, 86% of them survived, but when they were only provided with one aphid a day, the survival rate fell to 63%.

The weight of C. maculata decreased as the feeding interval increased (Fig 1). Larvae submitted to intervals of two and three days without feeding were lighter, with the heaviest larvae (9.0 mg and 20.0 mg, respectively) occurring at six and eight days of age daily fed with A. kuehniella eggs. Fourth instars showed a particularly increase in body weight, even in conditions of scarcity of food, because of their need to store energy for pupation.

The adults weight decreased with the feeding interval (Fig 1) as observed when the species was fed aphids as prey, with shortage of food during the larval stage being the a possible cause of the reduced size of predators, including that observed under natural conditions in agricultural ecosystems (Obrycki et al 1998).

Adults of C. maculata fed at one and two day intervals did not show any significant difference with respect to the pre-oviposition, oviposition, and post-oviposition periods (Table 2). Also, we did not find any significant difference in the fecundity and longevity of C. maculata as a function of food deprivation at two tested feeding intervals. Females with availability of prey at intervals of two days, besides a lower body mass, showed fecundity similar to females that were prey-fed daily (Table 2). Only four C. maculata larvae fed at three day intervals reached adult stage, resulting in two couples. Therefore, no statistical analysis was performed. In this treatment, the pre-oviposition, oviposition and post-oviposition periods were 66.0 ± 17.0; 52.0 ± 51.0 and 9.0 ± 3.33 days, respectively. Longevity of females was 125.5 ± 30.5 days and 37.0 ± 29.0 days for males; daily and total fecundity were 4.0 ± 1.97 eggs and 109.0 ± 103.0 eggs, respectively.

When the coccinellid was supplied with prey at two and three day intervals, larval stage was prolonged and the weight of larvae and adults were reduced. However, under these conditions of food restriction the predator demonstrated ability to survive and reproduce. These characteristics are important as coccinellids that feed on aphids live in habitats with seasonal variations in prey availability, since aphid populations are ephemeral (Agarwala et al 2008). Yet, the ability to survive and complete development when deprived of food is an indication of an important adaptive strategy that should allow lady beetles to cope with the highly unpredictable and variable food resources in nature (Phoofolo et al 2008).

Received 09 October 2009 and accepted 26 August 2010

Edited by Madelaine Venzon - EPAMIG

• Agarwala BK, Bardhanroy P, Yasuda H, Takizawa T (2001) Prey consumption and oviposition of the aphidophagous predator Menochilus sexmaculatus (Coleoptera: Coccinellidae) in relation to prey density and adult size. Environ Entomol 30: 1182-1187.
• Agarwala BK, Yasuda H, Sato S (2008) Life history response of a predatory ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), to food stress. Appl Entomol Zool 43: 183-189.
• Declercq P, Degheele D (1992) Influence of feeding interval on reproduction and longevity of Podisus sagitta (Het: Pentatomidae). Entomophaga 37: 583-590.
• Gordon RD (1985) The Coccinellidae (Coleoptera) of America and North of Mexico. J N Y Entomol Soc 93: 1-912.
• Hodek I (1973) Life history and biological properties, p.70-75. In Hodek I (ed) Biology of Coccinellidae. The Hague, W. Junk N. V, 260p.
• Hodek I, Honek A (1996) Ecology of Coccinellidae. Dordrecht, Kluwer Academic Publishers, 464p.
• Iperti G (1999) Biodiversity of predaceous Coccinellidae in relation to bioindications and economic importance. Agric Ecosyst Environ 74: 323-342.
• Lanzoni A, Accinelli G, Bazzocchi GG, Burgio G (2004) Biological traits and life table of the exotic Harmonia axyridis compared with Hippodamia variegata and Adalia bipunctata (Col.: Coccinellidae). J Appl Entomol 128: 298-306.
• Lundgren JG, Razzak AA, Wiedenmann RN (2004) Population responses and food consumption by predators Coleomegilla maculata and Harmonia axyridis (Coleoptera: Coccinellidae) during anthesis in an Illinois cornfield. Environ Entomol 33: 958-963.
• Michaud JP, Grant AK (2005) Suitability of pollen sources for the development and reproductionof Coleomegilla maculata (Coleoptera: Coccinellidae) under simulated drought conditions. Biol Control 32: 363-370.
• Michaud J P, Jyoti JL (2008) Dietary complementation across life stages in the polyphagous lady beetle Coleomegilla maculata Entomol Exp Appl 126: 40-45.
• Musser FR, Shelton A (2003) Predation of Ostrinia nubilalis (Lepidoptera: Crambidae) eggs in sweet corn by generalist predators and the impact of alternative foods. Environ Entomol 32: 1131-1138.
• Nakashima Y, Hirose Y (1999) Effects of prey on longevity, prey consumption, and egg production of the insect predators Orius sauteri and O tantillus (Hemiptera: Anthocoridae). Ann Entomol Soc Am 92: 537-541.
• Obrycki JJ, Giles KL, Ormord AM (1998) Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117: 279-285.
• Phoofolo MW, Elliott NC, Giles KL (2009) Analysis of growth and development in the final instar of three species of predatory Coccinellidae under varying prey availability. Entomol Exp Appl 131: 264-277.
• Phoofolo MW, Giles KL, Elliott NC (2008) Larval life history responses to food deprivation in three species of predatory lady beetles (Coleoptera: Coccinellidae). Environ Entomol 37: 315-322.
• Pilorget L, Buckner J, Lundgren JG (2010) Sterol limitation in a pollen-fed omnivorous lady beetle (Coleoptera: Coccinellidae). J Insect Physiol 56: 81-87.
• Rondon SI, Price JF, Cantlife DJ (2006). Developmental time, reproduction, and feeding of two subspecies of Coleomegilla maculata (Coleoptera: Coccinellidae) in the laboratory. Fla Entomol 89: 85-88.
• Schüder I, Hommes M, Larink O (2004) The influence of temperature and food supply on the development of Adalia bipunctata (Coleoptera: Coccinellidae). Eur J Entomol 101: 379-384.
• Shafiei M, Moczek AP, Nijhout HF (2001) Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Physiol Entomol 26: 173-180.
• Weeden CR, Shelton AM, Yaxin L, Hoffman MP (2007) Biological control: a guide to natural enemies in North America. Cornell University. Available at: <http://www.nysaes.cornell.edu/ent/biocontrol/predators/coleomeg.html >. Accessed in: 23 Mar 2007.

Publication Dates

• Publication in this collection
  14 Mar 2011
• Date of issue
  Feb 2011

History

• Received
  09 Oct 2009
• Accepted
  26 Aug 2010