The control of meal termination in the locust

Anita. Behav., 1988, 36, 1216-1227

The control of meal termination in the locust

S. J. S I M P S O N * , M. S. J. S I M M O N D S t , A. R. W H E A T L E Y * & E. A. BERNAYSJ; * Department of Zoology and University Museum, University of Oxford, South Parks Road, Oxford

OX1 3PS, U.K. t Behavioural Entomology Group at Jodrill Laboratory, Royal Botanic Gardens, Kew, TW9 3AB, U.K.

Division of Biological Control, University of California, Berkeley, CA 94706, U.S.A.

Abstract. The relationship between the amount eaten during a meal, meal duration and ingestion rate was investigated in the locust, Locusta migratoria (L.). The results suggested a relatively simple model for the control of meal termination whereby a variety of exogenous and endogenous factors, including chemosensory stimuli provided by the food, the presence of other locusts nearby, age and deprivation- related factors, are integrated within the central nervous system and together contribute to the level of excitation present at the start of a meal. The amount of excitation determines both the mean rate of ingestion during the meal and the amount of inhibition needed to end the meal. Since much of the inhibitory feedback comes from gut stretch, meal size and mean ingestion rate are positively correlated, in fact increasing proportionally, and, hence, meal duration remains constant. At high levels of excitation, however, ingestion becomes rate limited and meal duration subsequently increases proportionally with meal size. Changes in the rate of ingestion throughout a meal were also investigated. The rate declined exponentially but, unlike in the rat, the initial ingestion rate remained constant with changes in excitation and the decay function varied such that small meals began at the same ingestion rate as large meals but the rate of decline was subsequently faster.

The pattern of feeding has been investigated in a wide range of animals: from horses to rats (Le Magnen & Devos 1980; Mayes & Duncan 1986), from chickens to zebra finches (Duncan et al. 1970; Siater 1974) and from locusts to caterpillars (Simpson 1982; Reynolds et al. 1986). In those cases where feeding occurs in bouts (meals), separ- ated by periods without eating, the pattern of feeding can be explained by two sets of mechanisms: those that determine when bouts begin and those that control bout termination. The pattern of feeding and the underlying regulatory mechanisms have been extensively studied in nymphs of the African migratory locust, Locusta migratoria L., and this animal now provides one of the best understood models for the control of feeding. Recent work on locusts has investigated the way in which the probability of a bout starting changes with time since the last meal, and how a variety of causal factors influences this probability (Simpson & Abisgold 1985; Simpson & Ludlow 1986; Abis- gold & Simpson 1987). Data on the termination of feeding bouts, also collected from studies of locusts feeding ad libitum, have, however, provided an apparent paradox.

When fifth instar locusts are fed seedling wheat,

analyses of log-survivorship curves show that the distribution of meal sizes does not differ significantly from a negative-exponential random model. Curves for meal durations, however, are significantly convex. In other words, the probability of a meal ending is apparently not related to the amount eaten during that meal but is related to time since the meal began. From these results Simpson (1982) concluded that a time-dependent factor, such as adaptation of taste receptors, is more important in regulating when a meal ends than is the amount eaten. Other experiments, however, show that the amount eaten is clearly important and that feedback from stretch receptors on the gut wall is involved in meal termination (Bernays & Chapman 1973; Simpson 1983; Roess- ingh & Simpson 1984). Cutting the nerves from these gut regions results in insects ingesting for considerably longer and eating much more during a meal.

One way of resolving this paradox was discussed by Simpson & Bernays (1983). Since meals eaten by locusts fed on wheat tend to be of a standard duration but of variable size it must follow that, on average, bigger meals are eaten faster than smaller ones. I fa higher ingestion rate is a result of a higher

1216

Simpson et al.: Meal termination in locusts 1217

level of excitation generated during a meal and this in turn requires a greater level of inhibition to overcome it, then meals will tend to be of a similar duration but variable in size. For example, a locust taking a meal that generates a level of excitation twice that of the previous meal will eat twice as fast and require twice as much gut stretch to stop the meal. Both meals will be of the same duration but the second will be twice the size of the first.

The aim of the work described in this paper was to test this hypothesis by investigating in detail the relationship between meal size, meal duration and ingestion rate during a test meal taken under a variety of conditions. Four experimental variables were incorporated into a factorial design: palatability of the food, age during the fifth instar, deprivation time, and the presence of other locusts. Each of these is known, either from published data or from preliminary experiments, to influence at least one of the three feeding parameters.

MATERIALS AND M E T H O D S

Experimental Animals Locusts were reared in the Department of Zoo-

logy, Oxford. As female nymphs moulted to the fifth (penultimate) instar they were collected over a 6-h period and placed at a density of about 20 per container into 5-1itre celluloid and aluminium cylinders. They were given ample seedling wheat and bran and kept under a 12:12 light:dark regime at 30_+ 1 °C. Even illumination was provided during light phases by overhead fluorescent strip lights. The day before testing, each insect was put into a clear plastic container measuring 17x 12 x 6 cm with an expanded aluminium perch and plenty of seedling wheat.

Experimental Procedure Insects were tested on day 1, day 4 or day 6

during the 10-day long fifth instar (the day of moulting being termed day 0). Nymphs were observed from 2 h after lights-on, by which time each insect should have fed at least once since their fast which normally occurs during the last 3-8 h of the dark phase. As each locust completed a meal of wheat during the course of ad libitum feeding its food was removed and the insect was then deprived for 2, 5 or 8 h (+ 15 min). The criteria used to define a meal were the same as those used for the subsequent test meal and are described below.

Fifteen minutes before the end of their allocated deprivation time five locusts were weighed to + 1 mg and placed into clean containers, either alone or with two others of the same age and sex. These extra nymphs could be distinguished from the test insect by a very small dab of correction fluid placed on the crest of their pronotum. The spot was allowed to dry before the insect was placed into its box. The five containers were visually screened from each other, and, after a further 5 min, a quantity of seedling wheat was added to each of them. The wheat had been grown on capillary matting until it was 15 cm tall. On the day of the experiment the top 5 cm was cut off and then dipped either into a solution of distilled water with 1 ml/litre of detergent (Micro, International Pro- ducts Corporation, Trenton, New Jersey, U.S.A.) or else into 1 M sucrose solution with 1 ml/litre detergent. The detergent ensured that the solutions coated the blades evenly. The wheat was then allowed to drain for 3-4 h. Sufficient of either sugared or control wheat was added to each experimental chamber so that the test insects were never more than 3 cm from food.

After the food was added the behaviour of the locusts was recorded every 10 s. A digital timer signalled each 10-s interval, whereupon the observer (SJS) would scan across the array of boxes and call the behaviour of each locust to the recorder (ARW), who was positioned elsewhere in the room. The following behavioural categories were used.

(1) Locomoting: walking about the container. (2) Ingesting: when a blade of wheat could be

seen entering the mouth. Usually the locust holds a blade between its foretarsi and pulls the food towards the mandibles as it chews.

(3) Chewing: a pause during ingestion when the locust stopped pulling food into its mouth and simply masticated.

(4) Pausing: standing still but not ingesting or chewing.

The meal was considered to have ended when at least 4 min without chewing or ingesting had elapsed following a period of at least 60 s of ingesting or chewing. The mean duration of feeding periods less than 60 s was only 7 s and it seems apparent that these represent a separate class of feeding bouts to 'meals'. The behaviour of the insects suggests that very short periods of feeding are part of the acceptance sequence rather than maintained ingestion (Bernays & Simpson 1982). The 4-min criterion for meal termination was based

1218 Animal Behaviour, 36,4

Table L F-ratios from the factorial ANOVA for a variety of parameters of the test meal

% of meal spent: Mean Meal

Meal Meal ingestion size/no. duration size rate ingests';"

Source df (min) (mg) (mg/min) (mg) Ingesting Chewing Lt~omoting Pausing

Age (A) 2 8.7*** 20.5*** 6.8** 4.8** 2.3 6.4** 11.4"** 1.5 Deprivation (D) 2 3.0 18.6"** 2.4 3.0 0.4 6"4** 3.7* 2-9 Phagostimulation (P) I 0.1 3"5 6-9** 5.0* 5'0* 6-5* 11.1"* 12-6"** Crowding (C) 1 0'0 1.6 3"8 0.2 8.1"* 0.9 0.1 3.9

A x D 4 1-3 1.4 1-7 0'5 6"3*** 2.4* 1.7 1"5 A x P 2 0-2 0.3 0.4 0'3 0-2 0.7 1.3 1"0 A x C 2 0-8 1.0 0.1 0"5 0.3 0.1 0.4 0.4 D x P 2 0.9 3"3* 6.2** 5'8** 1.8 1.4 2.1 4.0* D x C 2 0-3 0.5 0-2 0"0 0.1 0"0 0.4 1.0 P x C 1 0.2 0.0 0.4 0.0 2'9 0"9 0.S 0"0

A x D x P 4 0.7 0-5 0.7 1.5 0.2 I-6 1.9 1.2 A x D x C 4 1-7 I.S 0'3 0'3 0-9 0-1 1.1 0.4 A x P × C 2 1.2 0.3 0.9 0.1 2.0 1.7 0.6 0.3 D x P x C 2 0.0 0.8 0.9 0'0 l-I 1"2 0.4 0"0

A x D x P x C 4 0.6 0"7 0.4 0.2 1.3 0'3 0-7 0'7

Residual 144

Total 179

Locomoting Latency and to feed

pausing (min)

6.1"* 0.3 4.6* 0"9

19.1"** 0.1 2.5 1.6

1.6 0-9 0,7 1-5 0.4 0-2 3,6* 2.2 0.2 0.4 0.4 0.5

1.8 0.5 0.8 0"3 0"2 0.4 0"0 0.2

0"2 0.7

* P < 0.05; ** P<0.01; *** P < 0 . 0 0 1 .

? "Ingests': number of 10-s recordings during the meal in which the locust was ingesting food.

on log-survivorship curves for the distribution of gaps between periods of feeding shown by locusts fed ad libitum on wheat (Simpson 1982). In the vast majority of cases, however, the end of a meal was clearly evidenced by the insect moving away from the food and entering the resting position on the perch. This quiescent behaviour is characteristic of inter-feed periods (Simpson 1982).

After all five test-insects had finished feeding they were reweighed along with any faeces produced by them since the premeal weighing. The weight difference between the start and end of the meal gave the meal size. Insects that had not fed after 30 min since the food was added were not used in the analyses. Nymphs were tested only once. Data were collected from 180 insects.

R E S U L T S

Data for a variety of feeding parameters, appro- priately transformed where necessary, were ana- lysed in a factorial analysis of variance. F-ratios from these analyses are presented in Table I. Fisher's protected LSD test was used to compare pairs of means. Percentage changes are used in the

following sections to summarize differences. These are based simply on mean values and are used for descriptive purposes only.

Meal Size

Meal size was significantly influenced by age during the instar, increasing by 42% from day 1 to day 4 and by only a further 7% from day 4 to day 6 (Table I, Fig. 1). Meal size was also significantly affected by deprivation, being 44% larger after 5 h than after 2 h of deprivation, but not increasing further from 5 to 8 h without food. The presence of sugar on the wheat resulted in meals being 37% larger after 2 h of deprivation, but had no effect after 5 or 8 h without food (Fig. 1). Meal size was not significantly different in locusts fed alone or with two others in the same container (7% larger when crowded).

Meal Duration

Meal duration was significantly influenced only by age during the instar, remaining constant from day 1 to day 4 but then increasing by 29% from day 4 to day 6 (Table I, Fig. 1). Meals increased in duration, but not significantly (P> 0'05), by 22%


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Overall Ingestion Rate

Overall ingestion rate, as derived from meal size/ meal duration, was significantly affected by age and by phagost imulat ion. There was also a significant interaction between deprivation and phagost imu- lation (Table I). Ingestion rate increased by 25%

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Figure 3. Values for meal size divided by the number of 10-s recordings during the meal when the locust was ingesting food (referred to on the y-axis as meal size/no. ingests). This gives a measure of rate of food intake during periods of ingestion. Statistically significant effects from the factorial design (see Table I) are plotted. In the left graph each point is the mean of 60 insects, while in the right graph, N = 30. Bars__+ SEM.

from day 1 to day 4 and then decreased by 13% from day 4 to day 6 (Fig. 1). Meals of plain wheat were eaten 38% faster after 5 h than after 2 h deprivation, but then remained constant from 5 to 8 h. Ingestion rate on sugared wheat was not influenced by deprivation time, sugared wheat being eaten 49% faster than plain wheat after 2 h without food. At 5 and 8 h deprivation, ingestion rate on plain and sugared wheat was similar (Fig. 1). Meals were eaten 10% faster when nymphs were crowded than when they were alone, but the difference fell just outside the 5% level of signifi- canoe.

Changes in overall ingestion rate The increase of 25% from day 1 to day 4 was

partly due to a change in the percentage of the time during a meal spent ingesting. On day 4 insects spent 8% more time ingesting and 9% less time chewing than on day 1. The effect was most marked after 2 h of deprivation, when % time spent ingesting increased by 26% from day 1 to day 4 (Fig. 2). The percentage of the meal spent pausing and locomoting did not vary from day 1 to day 4 (Fig. 2).

The more important contributor to the increase in overall ingestion rate was an increase in the rate at which food was eaten during periods of ingesting. The ratio of meal size to the number of 10-s

recordings during the meal in which the insect was observed to be ingesting rose by 16% from day 1 to day 4 (Fig. 3).

The decline of 13% from day 4 to day 6 was not due to a change in the percentage of the meal spent ingesting, which fell by only 1% from day 4 to day 6. The percentage of the meal spent chewing rose by 9%, this increase being especially marked after 8 h of deprivation when it was accompanied by decline in % time spent ingesting of 15% (Fig. 2). The increase in % time spent chewing from day 4 to day 6 was mainly at the expense of time spent lo¢omoting during a meal, which declined by 77%.

The main reason for the decline in ingestion rate from day 4 to day 6 was the fact that insects ate more slowly when ingesting on day 6. The ratio of meal size to the number of 10-s recordings during the meal in which the insect was ingesting declined by 16% (Fig. 3).

The increase of 42% from 2 to 5 h deprivation when feeding on plain wheat was partly a result of insects spending more time ingesting during the meal: % time spent ingesting increased by 21%, while % time spent chewing increased by 41%. The time spent pausing and locomoting declined by 70% and by 52%, respectively, (Fig. 2).

Insects also ate faster while ingesting when they had been deprived for 5 h compared with 2 h deprivation, meal size/number of recordings in which the locust was ingesting increasing by 32% (Fig. 3).

The 49% increase when feeding on sugared rather than plain wheat after 2 h deprivation was in part a result of nymphs spending more time during the meal ingesting: % time ingesting was 16% higher and % time chewing was 39% higher on sugared wheat. Time spent pausing and locomoting fell accordingly (by 70% and 81%, respectively; Fig. 2). Insects also ingested sugared wheat at a greater rate, with the ratio of meal size to the number of 10-s recordings during the meal in which the insect was ingesting being 38% higher than on plain wheat (Fig. 3).

The 10% increase when feeding in a crowd than when alone occurred because nymphs spent significantly more time (10%) ingesting during the meal. The percentage of the meal spent pausing, Iocomot- ing and, to a lesser extent, chewing were all lower, but not significantly so, in crowded insects (Fig. 2).

There was no significant effect of crowding on the rate at which food was eaten during periods of ingestion.

Simpson et al.." Mea l termination in locusts 1221

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Figure 4. Values for various parameters of the test meal plotted against the size of the meal. Data are pooled from the whole experiment, the meal size for each of the 180 insects being placed into one of the 30 mg size classes 0-30 mg, 31-60 mg, 61-90 rag, etc. Each point is the mean + SEM, the number of locusts contributing to each mean being given above the points in A. Values in parentheses below the meal size categories in A give the mean meal size for that category. Thus there were 22 insects that took a meal of 31-60 mg, the mean of these being 44 mg.

Latency to Feed

The time from the addition o f food to the test container and the commencement of a meal aver- aged 4.9 min and did not vary significantly with any of the experimental variables (Table I).

Meal Size, Duration and Ingestion Rate

The results presented so far indicate that meal duration was less affected by the experimental variables tested than was meal size (Table I); however, it did not remain constant. In order for meal durat ion to be conserved, overall ingestion rate must increase proportionally with meal size. When the data from the whole experiment were pooled (Fig. 4A), ingestion rate increased almost

proportionally with meal size up to meals of about 150 mg (ingestion rate rose 6.2 times from 2.7 to 16.8 mg/min as meal size increased 7'6 times from 18 to 137 mg). As a result, meal durat ion increased only slightly, f rom 6.0 to 8.5 min (Fig. 4B). However, for meals larger than 150 mg, ingestion rate did not change and meal durat ion increased proportionally with meal size.

Figure 4C and D shows what contributed to the change in overall ingestion rate as meal sizes rose. As meal size increased from less than 30 mg up to 60 mg there was a rapid increase in the percentage of the meal spent ingesting and chewing and an equally rapid decline in the time spent pausing and locomoting. Beyond 60 mg, however, there was only a slight increase in % time spent ingesting. The amount eaten while ingesting (meal size/number of


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Figure 5. Exponential curves for change in ingestion rate throughout meals of various sizes. Ingestion rate per min is estimated as meal size divided by the total number of 10-s recordings during the meal in which the locust was ingesting, multiplied by the number of 10-s recordings in that minute when the insect was ingesting. Each curve is based upon data from insects whose meal size fell within a specified 30 mg size range (see Fig. 4), the mean meal size for each category being given on the curves. Curves were fitted by least squares regression. Values for the y intercept (initial ingestion rate) and decay function are given in Fig. 5B. Meal size 44 mg, r=0.924, F=23.2, SE=0.26, N-----22; meal size 78 rag, r=0.967, F=72.5, SE=0.08, N=22; meal size 105 rag, r=0.939, F=52.5, SE=0.11, N=37; meal size 137 rag, r=0.944, F=57.2, SE=0'05, N-----32; meal size 164 rag, r=0.891, F=38.3, sE=0-9, N=39; meal size 192 mg, r=0-933, F=80.6, SE=0.10, N=19; meal size 221 rag, r=0-600, F=7.3, SE =0-29, N=5.

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recordings in which the locust was ingesting), however, continued to increase steadily up to meal sizes of 150 mg but thereafter remained constant.

Changes During a Meal

The effect of meal size on ingestion rate during a meal was investigated by pooling data from the experimeht into the same meal size categories as used for Fig. 4. Because actual amounts eaten during consecutive minutes during a meal were not measured, an indirect measure of consumption had to be used. The only behaviour of those recorded that involves movement of food from the plant into the animal is ' ingesting'. By dividing meal size by the total number of times the insect was recorded to be ingesting during the meal and multiplying this figure by the number o f times it was ingesting in consecutive minutes throughout that meal, an approximate measure o f ingestion rate changes was derived (Fig. 5). This assumes that the same amount of food is eaten during ingesting at the start of a meal as at the end of that meal. As has already been demonstrated, the ratio of amount eaten to the total number o f recordings during the meal when the locust was ingesting varied between treatments such that it was larger for big meals than for small ones (Fig. 4D). It may be that the steepness of the decline in ingestion rate is underes- t imated in Fig. 5. However, it is highly unlikely that they are overestimated. To test whether the initial ingestion rate during a meal was estimated accu- rately, measures of actual ingestion rate were


recorded from locusts deprived on day 1 for 2 or 5 h and provided with 2 cm lengths of seedling wheat weighing 15 +__ 1 mg. Ingestion rate was recorded on the basis of the time taken to eat such pieces of wheat as the meal progressed. There was no correlation between ingestion rate during the first minute of the meal and meal size (y= 17+0.02x; range in meal size 38-248 mg, N=15, r=0.33, F = 1"58). Initial ingestion rate was 19-4 + 1.0 (SE), as predicted in Fig. 5.

The curves in Fig. 5 were derived by fitting an exponential model to the data. Not surprisingly, linear and quadratic models also fitted the data significantly well. No matter which of the models is fitted, however, the key features remain that ingestion rate at the start of a meal is independent of meal size, whereas the rate of decline during the meal is fastest for small meals. The exponential fits are shown in Fig. 5 since they provide the most parsimonious explanation of the underlying physiology (see Discussion).

D I S C U S S I O N

Meal Size Versus Ingestion Rate

The data presented in this paper suggest a relatively simple model for the control of meal termination. A variety of exogenous and endogenous factors, including chemosensory stimuli provided by the food, the presence of other locusts nearby, age and deprivation-related factors, are integrated within the central nervous system and together contribute to the level of excitation present at the beginning of a meal. The amount of excitation determines both the rate of ingestion and the amount of inhibition needed to end the meal. Since much of the inhibitory feedback comes from gut stretch when insects are fed palatable food (Bernays & Chapman 1973; Simpson 1983), meal size and ingestion rate are positively correlated, in fact increasing proportionally, and, hence, meal duration remains constant. However, at high levels of excitation, ingestion becomes rate limited before meal size does. Beyond this point meal duration cannot remain constant and so increases proportionally with meal size.

That meal size is influenced by the taste of the food and by deprivation is well known, both in vertebrates and in insects (Bernays & Simpson 1982; Le Magnen 1985). The effect of these on the rate of ingestion has received much less attention,

however. Dethier et al. (1956) showed that in the blowfly Phormia regina ingestion rate increased with sugar concentration up until very high con- centrations where viscosity limited intake. Both meal size and ingestion rate increased with increasing sugar concentration, but because meal size rose faster than did ingestion rate, meal duration also increased. Moorhouse et al. (1976) did not find any relationship between rate of intake and the stimu- lating power of the food in the locust Chortoicetes terminifera. The food used, however, was a range of sucrose solutions presented to insects restrained ventral side uppermost after being deprived of both food and water for 24 h. The effect of the deprivation period alone was likely to have overridden any effect on ingestion rate.

Le Magnen (1971) described experiments on rats, Rattus norvegicus, which showed the effects of 'orosensory stimulation' by the food and time of previous deprivation on ingestion rate during a meal. Three diets were used, the most palatable being stock diet with 10% corn oil and 15% cellulose added, the next being unadulterated stock diet, and the least palatable was stock diet with 0-125 % quinone hydrochloride. Ingestion rate was related to palatability, the maximum difference between the diets occurring after the shortest deprivation time. Ingestion rate was affected by the duration of deprivation but only up until 24 h. Meal duration also increased up to 24 h, but, except for the least palatable diet, remained constant from 24 to 48 h of deprivation. Meal size increased rapidly after deprivation of up to 24 h, and then continued to increase with further deprivation for the quinone-treated diet only.

Le Magnen suggested that 'hunger and palatability are algebraically additive in their determining effects on food eaten in the meal'. Together, they determine ingestion rate and the total amount eaten.

Bellisle et al. (1984) investigated the effect of deprivation and palatability on feeding in humans. Subjects were fed a food, ranked by themselves as being of high or low palatability, after 4 or 15 h of deprivation. Meal size increased both with increasing palatability and deprivation time, as did meal duration. Ingestion rate, however, did not differ statistically between diets or deprivation times.

The common feature of the studies on the locust, the blowfly, the rat and humans is that meal size is influenced both by palatability and by deprivation. The difference is the nature of the relationship

1224 Animal Behaviour, 36, 4

between meal size and ingestion rate. In each of the studies, except for the one on humans, meal size and ingestion rate were positively correlated. In locust nymphs feeding on seedling wheat, meal size and ingestion rate vary proportionally up until the point where ingestion is rate limited. In the rat and the blowfly, however, the relationship is not pro- portional, ingestion rate changing to a lesser extent than meal size. Thus, meal duration is less well conserved. Once mean ingestion rate reaches its limit in locusts, meal duration increases proportionally with meal size, as it does in humans. Whether such differences indicate real differences in the mechanisms controlling meal termination in these species or else simply reflect experimental techniques and choice of treatments is unclear.

The effect of age during the instar on meal size has been demonstrated previously in locusts fed ad libitum (Simpson 1982) or deprived for a standard period (Bernays & Chapman 1972). Meal size and ingestion rate increase up to mid-instar (days 4 to 5) then decline until feeding ceases a day prior to adult ecdysis. A similar change occurs in responsiveness to various stimuli and also in locomotor activity (Ellis 1951; Chapman 1954; Moorhouse 1971), suggesting that age-related changes in central nervous excitability may underlie the effect on meal size and ingestion rate.

Ingestion rate declined sooner than did meal size after mid-instar in the present study (Fig. 1), indicating that the two parameters, while changing proportionally under most situations, are not indissolubly linked.

The influence of crowding was less marked than other factors but there was nevertheless a suggestion that crowded insects ingested more quickly as a result of pausing and locomoting less during a meal. This evidently has some functional significance, considering that competition between individuals for food must be extreme in swarms which may reach densities of 3 x 10S/km 2 (Uvarov 1977).

The Basis of Changes in Ingestion Rate

Changes in overall ingestion rate occurred as a result of varying both the proportion of a meal spent ingesting rather than chewing, pausing or locomoting, and the actual rate of eating while ingesting. The increase in overall ingestion rate which occurred as meal size rose was initially due to both of these (up to meals of 60 mg) but then the

proportion of time spent ingesting reached its limit and subsequent increases in overall ingestion rate were due to insects increasing the amount of food eaten during periods of ingestion. That the latter change is due to insects increasing the rate of jaw movements has been demonstrated by implanting myogram electrodes in jaw muscles of locusts deprived for 2, 5 or 8 h and then fed on plain or sugared wheat (Simpson, unpublished data). Seath (1977) showed by similar techniques that jaw movements during feeding in locusts are probably controlled by a central pattern generator, the output of which is modulated by mechanosensory input from the food. The suggestion is that other inputs, including chemosensory stimuli, age and deprivation-related factors, may also modulate the central pattern generator. Central pattern genera- tors that receive sensory modulation and regulate mouthpart movements are best known in molluscs (e.g. Benjamin 1983).

Changes During a Meal

Variation in ingestion rate during the course of a meal has been reported for a number of animals, including red-billed weaver birds, Quelea quelea (Clifton 1982), pigeons, Columba livia (Ziegler 1974), rats (Le Magnen 1971; McCleery 1977; Davis et al. 1978), mice, Mus musculus (Wiepkema 1971; Peterson 1976), domestic chicks, Gallus gallus (Clifton 1979), humans (Bellisle et al. 1984) and locusts (Moorhouse et al. 1976). Such changes appear to be due to one or both of two processes: the first acting most noticeably towards the beginning of the meal and the other towards the end. In some cases feeding begins at a high rate and then declines throughout the meal (e.g. domestic chicks). In other instances ingestion increases in rate over the first part of the meal and then either remains constant (e.g. red-billed weaver bird) or declines (e.g. the mouse, rat and pigeon).

Decline during the latter part of a meal, if it occurs, has generally been considered to reflect a build-up in negative feedbacks, while an increase in ingestion rate during the early stages of a meal has been interpreted by many authors as indicating the effect of positive feedback (see Clifton et al. 1984; Houston & Sumida 1985). Apparent absence of an initial build-up could indicate the lack of positive feedbacks, but, as pointed out by Clifton (1979) and latterly Houston & Sumida (1985), positive


feedbacks may still produce this pattern either because their effect builds up very quickly at the start of a meal, or else because ingestion rate is limited and, because it is maximal at the start, cannot rise during the early part of the meal.

The data from the present experiment show quite clearly that ingestion rate declined throughout the meal, but do not enable us to say whether or not there was an initial, rapid build-up at the start of a meal. The results do suggest a model for the control of decline in ingestion rate during feeding, however.

As already mentioned, excitation apparently determines the amount of inhibition required to end the meal, i.e. excitation sets the stop threshold. Since inhibition comes predominantly from gut stretch receptors, meal size reflects excitation. Excitation also determines the rate of ingestion, but ingestion is rate limited at a mean value throughout a meal (overall ingestion rate) of about 15 mg/min.

A decline in ingestion rate during a meal will occur if it is assumed that ingestion rate is conti- nually readjusted as the inhibitory consequences of eating (gut stretch) reduce net levels of excitation as the meal progresses. Thus, ingestion rate is limited in a negative feedback loop, producing an exponential decline in ingestion rate throughout a meal.

Previous models for the control of ingestion rate throughout a meal (e.g. McCleery 1977; Davis et al. 1978) have been based on changes in excitation (or its equivalent) resulting in variation in initial ingestion rate (I(0)), with the exponential decay function ( - b ) remaining constant. Hence

I(0) =fiE) and I(t)= I(0)x exp(-b t )

where the decay function - b , is a constant, E is excitation as the meal begins, and t is time during the meal. Negative feedbacks (n) build up during the meal, such that

T

n = S I ( t )d t 0

Excitation declines with the increase in n, until E = 0, when the meal ends.

As in the rat, ingestion rate in the locust apparently declines exponentially during a meal. However, the initial ingestion rate does not vary between meals of different sizes but the exponential decay function does, with the rate declining more quickly during small than large meals. It seems, then, that I(0) is constant and - b =fiE). The rate limit on overall ingestion rate throughout a meal

(Fig. 4A) would appear to be due to a minimum rate of decay rather than a maximum initial ingestion rate (Fig. 5B). Even if a rate limit (McFarland 1971; Houston & Sumida 1985) of 20 mg/min is introduced into the rat model the predicted curves do not fit the observed data (Fig. 6), although further data for actual rather than estimated ingestion rates during a meal are required before the latter model can be rejected with certainty.

The change in the decay function with excitation could be due to either a variation in the responsiveness of gut stretch receptors to incoming food or a change in the inhibitory effect of stretch receptor inputs on the central nervous system. There are no available data to enable these two possibilities to be distinguished.

While there are obvious benefits in ingesting at a high rate at the start of each meal, there are probably also advantages to eating more slowly as the meal progresses. Locusts lack the ability to digest cellulose and it is likely that the efficiency of digestion is related to the area of parenchyma exposed during mastication. Preliminary work (Simpson, unpublished data) suggests that the particle size of chewed food decreases and degree of separation of abaxial and adaxial leaf surfaces increases towards the end of a meal. Locusts in the field have been observed to feed in bouts of similar length to those seen in the laboratory (Ellis 1951), so such effects are presumably of functional significance to insects in the wild.

The assumption has been made in the discussion so far that maximal levels of excitation occur close to the start of the meal (whether or not there is an initial build-up) and, thereafter, levels are whittled away by the build-up in inhibitory feedbacks but do not decline during the meal of their own accord. In other words, if negative feedbacks could be removed entirely, feeding would continue at a constant rate until muscular fatigue occurred. Unfortunately it is not possible to 'sham feed' locusts but experiments in which gut nerves are sectioned, thus removing stretch receptor input to the central nervous sytem, lead to a considerable prolongation of meal duration (Bernays & Chap- man 1973). Levels of excitation are almost certainly maximal close to the start of a meal but do decline if phagostimulation does not continue (see Barton Browne 1975; Simpson & Bernays 1983). Conti- nued phagostimulation during feeding and the generation of an enhanced 'central excitatory state'

1226 Animal Behaviour, 36, 4

(Dethier et al. 1965; Barton Browne et al. 1975) apparently serve to maintain levels of excitation throughout the meal, as required by the model.

Another assumption is that inhibition comes solely from gut stretch. While this is probably the case on a palatable food such as seedling wheat (see Simpson & Bernays 1983, al though see Barton Browne et al. 1976, and Roessingh & Simpson 1984, for data suggesting an additional extra- gastric volumetric feedback) the presence o f deter- rent compounds in the food can cause early meal termination. Bernays & Chapman (1972) showed with fifth instar Locusta nymphs that more palatable grasses are eaten in larger quantities during a meal and at faster overall rates than are less palatable grasses. Blaney & Duckett (1975) placed small glass capillaries filled with various solutions over the maxillary palps and then fed the locusts either grass or a relatively unstimulating unleavened bread. Smaller meals o f grass were eaten when the tubes contained deterrents (0-1 u NaC1 or 0-01% azadirachtin) than when they were empty. Also, larger meals o f unleavened bread were eaten if the tubes containined 0.1 M sucrose solution. Surprisingly, in no case did the solutions in the tubes influence ingestion rate, al though the criteria used for defining meal durat ion were not given. It is important in calculating meal durat ion to include intra-bout pauses; their exclusion would obviously alter measures o f overall ingestion rate.

It is important to keep in mind that the models derived here for the locust are based on measure- ments from a large number of individuals. Smooth curves of changing ingestion rate during a meal produced in this way do not, of course, mean that individual insects behave in such a manner. Curves such as those in Fig. 5 also do not distinguish whether a decline in ingestion rate is due to insects eating at a slower rate during periods o f ingestion or to insects pausing more frequently or for longer as the meal progresses (see Clifton 1979). Such issues are currently being investigated.

Further work is required both to develop the model introduced here and to investigate its functional significance. It is evident, though, that the locust continues to provide a useful comparison with vertebrates for the study of the control of feeding. In fact, an experimental study of similar scope to the present one has not been attempted on any vertebrate as yet. If it were to be, the compari- sons with the locust would undoubtedly be valuable.

A C K N O W L E D G M E N T S

Many thanks to Dr A. I. Houston for helpful discussion, and to Dr P. G. Clifton for his valuable comments on the manuscript.

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(Received 3 July 1987; revised 23 October 1987; MS. number: 3049)

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The control of meal termination in the locust