Effect of energetic cost to maintain the trap for myrmeleon brasiliensis (neuroptera, myrmeleontidae) in its development and adult size/Efeito do custo energetico com a manutencao da armadilha de myrmeleon brasiliensis (neuroptera, myrmeleontidae) no seu desenvolvimento e no tamanho dos adultos.
Antlion larvae (Neuroptera, Myrmeleontidae) are sit-and-wait predators that build funnel-shaped traps in sandy soil to catch their prey (Farji-Brener, 2003). This foraging strategy implies that the larvae need to invest time and energy in building their traps rather than pursuing their prey. The selection of a favorable site for the construction of these traps is based mainly on the availability of dry and sandy soil, the availability of prey and intraspecific competition (Prado et al., 1993; Faria et al., 1994). If one of these factors negatively affects their foraging, larvae may migrate in search of more favorable locations. However, in this case the antlion larva must bear a high energy cost because the decision of sit-and-wait predators to relocate their trap is analogous to the decision of active predators to leave their present patch to find a more attractive one (Harwood et al., 2003; Miyashita, 2005).
Griffiths (1985) observed that the maintenance of traps constructed by antlion larvae of the species Myrmeleon quinquemaculatus Hagen, 1853 required a high energy cost and larvae that had their funnel destroyed had a 50[degrees] o lower growth rate compared to larvae whose funnel suffered no disturbance. Additionally, Lucas (1985) observed that the metabolic cost associated with the construction of traps increased positively with the size of the trap and negatively with temperature. Thus, the metabolic cost for maintenance of traps affected the size of the builders of these traps.
In addition to affecting the size of the larva, the energy cost to maintain the trap can affect adult size. In many orders of insects the size of the adult has a strong genetic component and their growth is determinant. However, in other orders the adult's size can be affected by the size of the larva and its nutritional quality (Boggs and Freeman, 2005; Kolss et al., 2009). As a consequence, antlion larvae that have their trap destroyed and consequently show reduced growth may result in smaller adults. Aside from a lower growth rate and success in capturing prey their reproductive success also can be affected because final size tends to be related to female fecundity (Honek, 1993).
Given that the larvae Myrmeleon brasiliensis (Navas, 1914) select protected sites to build their traps and that trap maintenance has a high energy cost (Lima and Faria, 2007), we expected that constant maintenance and reconstruction of the trap would negatively affect larval development and the adult emergency conditions since the larvae would cease to accumulate the energy resources required for their full development. Based on the these considerations, the objective of this study was to observe, under laboratory conditions, how the energy cost of the maintenance of traps of M. brasiliensis larvae affected: 1) larval development time, 2) time spent in the pupal stage, 3) larval mortality rate and 4) adult size.
2. Material and Methods
Myrmeleon brasilienses larvae were collected in Aquidauana, Mato Grosso do Sul, Brazil, in an Area of Permanent Protection (APA) (20, 26'25"S, 55, 39'21"W) belonging to the State University of Mato Grosso do Sul. The experiments were conducted in the Zoology laboratory of the Federal University of Mato Grosso do Sul (UFMS) on the campus in Campo Grande, Mato Grosso do Sul, Brazil.
Collections of larvae of M. brasilienses were made on October 15,2008, February 5,2009, May 3,2010 and June 17,2010. Search for the larvae was done ramdomly and when found they were collected with the aid of a spoon and placed in plastic bags with sand from the collection site and then were brought to the laboratory of Zoology of the UFMS. In the laboratory, larvae were measured (head-abdomen) by a digital caliper (resolution of 0.01 mm), to confirm the larval instar. Only the first instar larvae were used in the experiments. Approximately 50 larvae were collected on each day.
In the laboratory each larva was placed in an individual transparent plastic containers (13 cm deep and 10 cm in diameter), containing sterilized sand brought from the collection site. The plastic containers containing the larvae were in laboratory conditions of temperature, humidity and ambient light.
After the larvae were placed in plastic containers, an accomodation period of 24 hours was maintained to permit trap formation by the larvae. After this period, all larvae were fed daily by manually placing oneDrosophila melanogaster Meigen, 1830 larva into the center of the funnel of each antlion larva.
The effect of disturbance on the development of M. brasiliensis larvae was tested experimentally. In the control treatment, larvae did not have their trap disturbed. In the manipulated experiment, M. brasiliensis had their traps disturbed three times a week, respecting a minimum time of one hour after they were fed. The trap handling consisted in a total destruction with the aid of a brush, so that the hopper cannot be perceived, i.e. the sand surface being uniform. The handling procedure lasted approximately 10 seconds. Each larva was accompanied until adult emergence and any larva that did not complete its development within a maximum period of 200 days was excluded from the analyses.
Larval development time was considered as the time elapsed from the date of the collection until the moment when the larvae stopped building their funnels to pupate. Pupal development time lasted from the time when the larvae stopped building funnels (as explained above) until adult emergence. The number of larvae that died during the experiments was also recorded.
When the larvae stopped building funnels the plastic containers were covered with a fine plastic mesh screen to prevent escape of the adults. After emergence each adult was collected and had its body size (head-abdomen), anterior and posterior wing span and width measured using digital calipers (resolution of 0.01 mm).
Comparison of adult body size (head-abdomen), anterior and posterior wing span and width, larval developmental time and pupal development time between treatments was made using a Mann-Whitney test. The comparison between treatments regarding the number of dead larvae was evaluated by 2X2 contingency table using a G Test.
A total 121 M. brasiliensis larvae were subjected to the control treatment. Of these, 88 developed to adult emergence and 33 died. In the manipulated treatment 96 larvae were accompanied. Fifty developed to adult emergence, 30 larvae died and 16 remained in the larval stage for the length of the experiment (200 days).
The duration of larval development was higher among manipulated larvae (U = 474.00, p < 0.001). Among the larvae in control treatment the larval stage lasted 50.24 [+ or -] 29.01 days, and the larvae that were manipulated at the larval phase lasted 110.06 [+ or -] 47.81 days (see Figure 1).
Unlike the larval developmental time that was higher for the larvae whose funnels were disturbed, the pupal development time was lower for larvae that were part in this treatment (U = 990.50, p = 0.0011). For the larvae in the control treatment the pupal development time was 30.1 [+ or -] 7.48 days while for the ones in the manipulated treatment the pupal development time was 27.28 [+ or -] 11.05 days (see Figure 2).
There was no significant difference in mortality between treatments. In the control treatment from a total of 33 larvae, died (27.3%). In the manipulated treatment a total of 30 larvae died (31.25%).
The body size (head-abdomen), anterior and posterior wing span and width were significantly lower among adults emerged in the manipulated treatment (as shown in Table 1).
The results of this study indicated that the high energy cost, represented by the constant cost of reconstruction of traps, by M. brasiliensis larvae increased development time of larvae but decreased pupal development time. Probably these changes in development are due to the fact that the energy spent in the constant maintenance of the trap did increase the time that the larvae required to accumulate the sufficient amount of energy reserves to meet the minimum size that would allow them to change phase. At the same time, smaller energy savings may have afforded a more rapid metamorphosis, as the emerging adults in this situation (of constant disturbance) were smaller. Missirian et al., (2006) observed that although the size of adult M. brasiliensis may be affected by diet quality, the pupal development time did not change.
In general, insects need to attain a certain size or a certain energy reserve for changes such as pupation and adult emergence to occur (Gullan and Cranston, 2007). In the case of the antlion larvae, the duration of developmental stages (larval, pupal and adult) depends on several factors such as photoperiod, temperature, prey availability and body size (Scharfet al., 2009b) and this developmental process can be accelerated or retarded. Data from Eitz (1997) suggest that the process of change in Myrmeleon mobilis Hagen, 1888 can be accelerated in individuals that are well nourished and suffer less disruption to their traps. Missirian et al., (2006) observed that M. brasiliensis fed with a high energy diet also had an accelerated development. In contrast, it is possible that organisms that live in unstable environments show lower growth rates, even when prey are provided. This occurs because individuals who grow in adverse conditions are not adapted for a significant increase in their growth rate, even when exposed to better conditions (Scharfet al., 2009b).
Although most M. brasilierisis larvae pupate and emerged as adults, some larvae that had their traps destroyed did not complete their development over the time period of the study and remained in the larval stage. For many insects it is common to observe that in adverse situations their development can be interrupted by a period of dormancy called diapause (Gullan and Cranston, 2007). In the case of M. brasiliensis larvae there was no interruption in the activities of trap maintenance and feeding, probably what happened was just a reduction of their metabolic activities, which is common among predators they face a period of low energy reserves (Wang et al., 2006). Furanishi and Masaki (1981,1982) observed that Myrmeleon formicarins L. antlion larvae can reduce their metabolic rate to very low levels and that larval development can vary from three months to two years depending on the food supply.
Another reaction of the larvae to the disturbance of their traps is relocation. When subjected to a stress situation such as the continual destruction of the trap, the antlion larva can react by relocating or reducing the size of their traps, or decreasing their respiratory rate during the ambush (Eitz, 1997). It is interesting to note that in no circumstance the larva stopped building its trap. This characteristic ensures that the larvae complete their development. However, a longer developmental time exposes the antlion larvae to risks such as cannibalism (Griffiths, 1991,1993) and the attack by parasito ids (Uchoa and Missirian, 2014).
As for mortality rate, it was expected that the constant rebuilding of the trap would increase this parameter since the larva would use more energy for the maintenance of the funnel. However, this study showed no difference in mortality between control and manipulated treatments. Possibly since these M. brasiliensis larvae were in the laboratory, away from weather and intra-specific competition, mortality depended only on intrinsic characteristics of each individual (morphological changes, for example). Studies with spiders have shown that the energy cost due to constant rebuilding of trap might affect aspects of their lifestyle, such as mortality (e.g. Venner et al., 2000, 2003). Lubin et al. (1993) observed a 40% increase in mortality when spiders needed to move to rebuild its traps. Probably in the natural environment, antlion larvae that must leave a site to build a trap in a more favorable area face problems such as lack of space for the construction of the funnel, intra-specific competition and cannibalism, that would result in a higher mortality rate. In the laboratory under controlled conditions, migration was not an influential factor on mortality.
Regarding adult size, the data from this study showed a negative relationship between the disturbance of the traps and the adult size of M. brasiliensis. A smaller adult size can affect the fitness of these organisms, since for many insect species, there is a strong and positive relationship between female size and fecundity (Sokolovska et al., 2000). Moreover, large size may favor life expectancy, sexual selection and reduce the risk of predation and increase resistance to periods of starvation (e.g. Blanckenhorn et al., 2007; Scharfet al., 2009a). The size of the adults can also affect their ability to fly, since these characteristics are related (e.g., larger wings provide longer flight) (Souza et al., 2009).
Scharfet al. (2009a) observed that adult antiions have a short life span and some do not even feed, only mate and die. Thus, to complete its life cycle they depend crucially on the body mass of larvae before pupation. Therefore, the development condition of the larva will be responsible for the characteristics of the adult.
In summary, an excessive energy cost may affect their development in negative ways (longer larval development time and reduced adult size). Thus, the reproductive success of adults depends on the performance of the larva, which should build their traps in stable environments that allow maintenance and and the same time success in capturing prey.
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T. N. Lima (a*) cmd D. C. R. Silva (b)
(a) Universidade Federal de Mato Grosso do Sul--UFMS, Campus Universitario de Aquidauana--CPAQ. Rua Oscar Trindade de Barros, 740, Bairro da Serraria, Unidade II, CEP 79200-000, Aquidauana, MS, Brazil
(b) Programa de Pos-graduacao em Biologia Animal, Universidade Federal de Mato Grosso do Sul--UFMS, Cidade Universitaria, s/n. CEP 79070-900. Campo Grande. MS. Brazil
* e-mail: tatianenlimaMgmail.com
Received: June 2. 2015 - Accepted: October 20. 2015--Distributed: February 28. 2017
(With 2 figures)
Caption: Figure 1. Distribution of M. brasiliensis larvae in the control and manipulated treatments in accordance with time (day) of larval development.
Caption: Figure 2. Distribution of M. brasiliensis larvae in the control and manipulated treatments in accordance to the time (day) of pupal development stage.
Table 1. Mean ([+ or -] SD) of body measurements of M brasiliensis and results of the Mann-Whitney test in the control and manipulated treatments. Treatment control Treatment manipulated Body size (head-abdomen) 20.1 [+ or -] 2.18 16.0 [+ or -] 2.36 Anterior wings span 50.0 [+ or -] 4.42 42.5 [+ or -] 3.86 Posterior wings span 44.5 [+ or -] 4.74 37.7 [+ or -] 3.49 Width forewing 5.6 [+ or -] 0.83 4.6 [+ or -] 0.46 Width hindwing 4.6 [+ or -] 0.61 3.8 [+ or -] 0.40 Result Mann-Whitney test U P Body size (head-abdomen) 312.00 p< 0.0001 Anterior wings span 89.00 p< 0.0001 Posterior wings span 92.50 p< 0.0001 Width forewing 218.50 p< 0.0001 Width hindwing 61.00 p< 0.0001