A study of the searching behaviour of certain insects feeding on aphids

The searching behaviour of insect predators in relation to the behaviour of their prey has received very little attention, with two notable exceptions. Fleschner (1950, Hilgardia 20 : 233-265) studied the searching capacity of the larvae of three predators of the citrus red mite. Banks (1954, Brit. J. anim. Behav., 2 : 37-38; 1957, Brit, J. anim. Behav., 5 : 12-24) studied the searching behaviour of individual coccinellid larvae on plants. No attempt, however, has been made to study the searching ability of all the instars of a particular insect predator.
The aim of the present laboratory study has been to determine the searching ability of all the larval instars and the adult, and the rate of increase, of the predatory coccinellid beetle, Adalia decempunctata (L.), when feeding upon the nettle aphid, Microlophium evansi (Theob.). The results have been used to test certain assumptions made by Volterra (1931, in Chapman, R.N., Animal ecology, New York) and Nicholson (1933, J. Anim. Ecol., 2 : 132-178) in their mathematical formulations of the interaction of predator and prey populations.
Predispersal behaviour.
A. decempunctata lays its eggs in batches of from 3-30 eggs, Soon after hatching, first hatched larvae will attack and eat unhatched eggs of the same batch, but will not attack either dead or living newly emerged larvae. Just prior to dispersal from the egg shells, 12-24 hours after emergence, the first hatched larvae will consume dead or freshly emerged larvae. Eggs which fail to hatch at the time when the majority of the batch do so do not normally hatch successfully. The delay in attack on freshly emerged or dead larvae allows for considerable variation in the time of hatching.
Orientation of larvae
Larvae are negatively geotactic, and positively phototactic These responses guide the larvae to the apices of the plant stems, the area of the plant favoured by their prey. In searching the lower surface of a leaf, larvae tend to follow irregularities of the leaf surface such as the rim or veins, where most nettle aphids are also found.
Thoroughness with which larvae search an area
Well fed larvae tend to recross their tracks more frequently than starved individuals of the same instar, so that at high aphid population densities they turn more frequently, and so confine their search to a relatively small area. This maintains larvae in an area where prey is diffusely aggregated. Starved first instar larvae recross their tracks more frequently than starved larvae of succeeding instars, and therefore confine their search to a relatively smaller area and have less chance of finding aphid colonies.
Starved fourth instar larvae search an area which their responses to gravity and light lead them to occupy less thoroughly as the period of starvation increases, and consequently leave such an area more quickly than if prey were abundant.
Efficiency in capturing prey
On average, first instar A.decempunctata at a larvae are able to capture only one first instar aphid of every five encountered, but there is an increase in efficiency in capturing prey after the first capture is effected, and as the larvae increase in age. The coccinellid is most efficient in capturing young aphids. Efficiency of adults lies between that of second and third instar larvae.
M. evansi attempts to avoid capture by an approaching coccinellid by walking out of its path, dropping off the plant, or by rhythmical kicking. When approached by a relatively large coccinellid, it drops. If the coccinellid is small, and moving slowly, the aphid walks away from it or performs rhythmical kicking movements. This kicking occurs most frequently when an adult aphid is approached by a first instar coccinellid, and doe not appear to be directed at the coccinellid, although it often results in the aphid kicking the larva and causing it to change direction.
If seized by a coccinellid larva smaller than itself, the aphid is able to kick the larva away or pull the captured appendage free. Where both aphid and larva are similar in size, the aphid has less chance of pulling an appendage free. However, it may wax the coccinellid by means of an oily liquid exuded from the siphunculi. The oily liquid is placed on the head of the coccinellid, where it spreads and solidifies, becoming wax like. Waxing was first noted by Büsgen (1891, Jena. Z. Naturw., 25 : 339-428) who stated that it served to protect aphids against certain predators. More recent workers, however, doubt its protective function. The present observation clearly support the opinion of Büsgen, as waxing results in a temporary immobilization of the coccinellid and often enables the aphid to escape.
M. evansi has less chance of avoiding capture when approached from the rear than from the front. Most individuals on nettle stems face downwards, and those on the leaves towards the petiole. As a coccinellid tends to move up the stem and moves on to a leaf from the petiole, this orientation enables the aphid to see approaching coccinellids.
The availability of other species of aphid to A. decempunctata larvae is also considered. Aphid species which do not react to the presence of an A. decempunctata larva by moving away, and appear helpless, are usually either attended by ants, distasteful to, or are capable of effectively waxing this predator. The fact that aphids which appear helpless are the most conspicuous, because they are highly coloured or tend to be gregarious, could very well have given rise to the general impression that aphids are helpless and sedentary.
Survival of larvae
The following observations were made on larvae placed with a fixed number of aphids in separate 7.5 cm. × 2.5 cm. specimen tubes, each containing a nettle leaf.
The chance of a first instar larva capturing its first aphid depends upon the number of aphids provided each day. Having once captured an aphid, a larva's chance of capturing a second is greater than was its chance of capturing the first, partly because of an increase in the efficiency in capturing prey.
For 50% survival, the larvae of successive instars of A. decempunctata require a greater number of aphids to be provided each day. Larvae also spend a greater length of time in each successive instar. The rate of development of larvae depends upon the number of aphids provided each day, and is greatest when a large number of aphids is provided.
When few aphids are provided each day, few or no larvae survive to become adults. However, even when a large number of aphids is provided some mortality occurs about the time of moulting.
Size and weight of the adults are greater when larvae are provided with a large number of aphids each day. Adults emerging from pupae taken in the field are of the same average size and weight as those reared from larvae provided with 20 third instar aphids each day.
An index of the relative aphid population densities required for 50% survival in each instar of coccinellid larva has been calculated, taking into consideration: 1) the age distribution of a nettle aphid population in the field attacked by A. decempunctata, 2) the efficiency of the larvae in capturing M. evansi, 3) the area which larvae of each instar can cover, 4) the number of aphids required for 50% survival by the larvae of each instar, and 5) the proportion of time spent feeding by larvae in each instar. First instar larvae require an aphid population density many times greater than that required by fourth instar larvae. The actual value of the index depends chiefly upon the age distribution of the aphid population being attacked. Therefore, for first instar larvae to survive, adult A. decempunctata must oviposit in young and relatively dense aphid populations.
Adult activity and oviposition
Egg batches of A. decempunctata on Tilia x vulgaris in the field are to be found either on leaves infested with aphids or close to infested ones. Since adult females are less active when well fed, they tend to remain in the close vicinity of aphids, and as the rate of maturation of eggs is greater when adults are well fed, the chance of eggs occurring close to aphids is farther increased.
The searching behaviour of A. decempunctata larvae and adults would lead them to concentrate their attack in those areas most heavily infested with aphids. Therefore, at low overall prey population densities the number of encounters between A. decempunctata and its prey would be greater than expected by random search in the sense used by Nicholson (1933), or the probability relationship used by Volterra (1931). Therefore, theories based on the assumption of random search must be used with caution.
Rate of increase
An index of the rate of increase of A. decempunctata has been calculated, taking into consideration the number of eggs laid per unit time and the survival of the larvae at a particular aphid population density. Over the range of aphid population densities used there is a linear relationship between the rate of increase and the logarithm of the prey population density. Therefore, whilst Nicholson's and Volterra's assumption that survival and reproductive rate are a function of the prey population density is valid for A. decempunctata, the actual function is not the one they use in their calculations.