Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future STAN BOUTIN Department of Zoology, University of Alberta, Edmonton, Alta., Canada T6G 2E9 Received March 3 1, 1989 BOUTIN, S . 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can. J. Zool. 68: 203-220. I reviewed 138 cases in which terrestrial vertebrates received supplemental food under field conditions. These cases are strongly biased toward small-bodied herbivores in north temperate environments. Most studies address population level questions and have supplied food over a short term (< 1 year) and on a small spatial scale (to less than 50 individuals). Individuals receiving supplemental food usually had smaller home ranges, higher body weights, and advanced breeding relative to those on control areas. The typical population response to food supplementation was two- to three-fold increase in density, but no change in the pattern of population dynamics. In particular, food addition did not prevent major declines in fluctuating populations. Researchers have failed to examine behaviour of individuals under conditions of supplemental food when addressing questions of population regulation. This review points to the need for researchers to conduct food supplementation experiments in tropical environments, on a larger scale, and over longer periods of time. BOUTIN, S. 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can.. J. Zool. 68 : 203-220. J'ai fait la rkvision de 138 ktudes sur les effets de I'addition de nourriture a des vertkbrks terrestres dans des conditions naturelles. Dans la plupart des cas, il s'agissait de petits herbivores vivant dans des milieux tempkrks nordiques. Dans la plupart de ces ktudes, on tentait de rksoudre les problkmes de densitk des populations et I'addition de nourriture durait assez peu longtemps (< 1 an) et se faisait B une petite kchelle spatiale (jusqu'a B moins de 50 individus). Les individus qui recevaient cette nourriture supplkmentaire avaient gknkralement un domaine vital plus petit, une masse corporelle plus grande et une p6riode de reproduction plus hitive que les individus de populations tkmoins. La rkponse dkmographique typique h l'addition de nouniture est une augmentation de la densitk par un facteur de 2 ou 3, mais la dynamique de la population ne change pas; notamment, l'addition de nourriture n'enraye pas le dkclin considkrable des populations de densitk fluctuante. Les chercheurs n'ont pas tenu compte du comportement d'individus face it I'addition de nouniture avant de considkrer les problemes dkmographiques. Cette synth6se permet de souligner l'importance d'exp6riences d'addition de nouniture dans des milieux tropicaux, h plus grande Cchelle, et pour des pkriodes de temps plus longues. [Traduit par la revue] Introduction No one would question that individuals and populations are ultimately limited by food supply. However, many ecological factors can act to reduce the proximate importance of food supply, and controversy continues to exist as to the role that food supply plays in shaping the patterns of life history, population dynamics, and community structure we see in nature (Lack 1954; Hairston et al. 1960; Sinclair 1975; Weins 1977; White 1978; Fretwell 1987; Oksanen 1988; Arcese and Smith 1988). Assessment of food limitation has been hampered by the dif- ficulty of determining actual food availability. Social behaviour, secondary plant compounds, and predation pressure can act to make apparently abundant resources inaccessible to some or all members of the population. An alternative to measuring food availability is to experimentally manipulate food supply. In this review, I examine studies where the food supply of terrestrial vertebrates was supplemented under field conditions. I could find only two cases in which food supply was experimentally reduced (Todd and Keith 1976; Ewald and Carpenter 1978). Most studies were designed to address questions of population limitation, but, more recently, they have also been concerned with behavioural responses to food addition. A few have dealt with effects of food supplementation at the community level. The review is divided into four main sections which address behavioural, life history, demographic, and community respon- ses to food addition. Within each section, I pose specific questions, present the data pertinent to the questions, and draw conclusions. As is often the case in ecology, the amount of empirical data is distressingly small. Who and where? I tried to include all published studies in which food supplies were manipulated under field conditions. This includes studies in which the population was enclosed, but under natural conditions otherwise. Food manipulation included addition of artificial food and alteration of natural food by fertilization. I did not include any so-called "natural" experiments where food supply changed independently of control by the experimenter, nor have I included provisioning studies of primates, as the latter have been reviewed elsewhere (Fa and Southwick 1988; Asquith 1989). I did not exclude any studies which failed to meet certain statistical design criteria such as proper controls and replication. The majority of studies, particularly those dealing with population-level questions, were not replicated. All studies had some form of control, although this may have been merely before and after comparisons. Table 1 lists 138 cases for which food supply was manipu- lated in terrestrial vertebrates. I considered a case to be a food addition to a single species in a localized area (food addition to more than one site during the same study was considered a single case). The 70 mammal, 58 bird, and 10 herpetologic cases include animals that range in body size from tadpoles to polar bears. However, all but seven studies dealt with animals weighing less than 2 kg. Most food additions have Can. J. Zool. Downloaded from www.nrcresearchpress.com by Ryerson University Library on 02/23/13 For personal use only.
Transcript
Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future
STAN BOUTIN Department of Zoology, University of Alberta, Edmonton, Alta., Canada T6G 2E9
Received March 3 1, 1989
BOUTIN, S . 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can. J. Zool. 68: 203-220.
I reviewed 138 cases in which terrestrial vertebrates received supplemental food under field conditions. These cases are strongly biased toward small-bodied herbivores in north temperate environments. Most studies address population level questions and have supplied food over a short term (< 1 year) and on a small spatial scale (to less than 50 individuals). Individuals receiving supplemental food usually had smaller home ranges, higher body weights, and advanced breeding relative to those on control areas. The typical population response to food supplementation was two- to three-fold increase in density, but no change in the pattern of population dynamics. In particular, food addition did not prevent major declines in fluctuating populations. Researchers have failed to examine behaviour of individuals under conditions of supplemental food when addressing questions of population regulation. This review points to the need for researchers to conduct food supplementation experiments in tropical environments, on a larger scale, and over longer periods of time.
BOUTIN, S. 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can.. J. Zool. 68 : 203-220.
J'ai fait la rkvision de 138 ktudes sur les effets de I'addition de nourriture a des vertkbrks terrestres dans des conditions naturelles. Dans la plupart des cas, il s'agissait de petits herbivores vivant dans des milieux tempkrks nordiques. Dans la plupart de ces ktudes, on tentait de rksoudre les problkmes de densitk des populations et I'addition de nourriture durait assez peu longtemps (< 1 an) et se faisait B une petite kchelle spatiale (jusqu'a B moins de 50 individus). Les individus qui recevaient cette nourriture supplkmentaire avaient gknkralement un domaine vital plus petit, une masse corporelle plus grande et une p6riode de reproduction plus hitive que les individus de populations tkmoins. La rkponse dkmographique typique h l'addition de nouniture est une augmentation de la densitk par un facteur de 2 ou 3, mais la dynamique de la population ne change pas; notamment, l'addition de nourriture n'enraye pas le dkclin considkrable des populations de densitk fluctuante. Les chercheurs n'ont pas tenu compte du comportement d'individus face it I'addition de nouniture avant de considkrer les problemes dkmographiques. Cette synth6se permet de souligner l'importance d'exp6riences d'addition de nouniture dans des milieux tropicaux, h plus grande Cchelle, et pour des pkriodes de temps plus longues.
[Traduit par la revue]
Introduction No one would question that individuals and populations are
ultimately limited by food supply. However, many ecological factors can act to reduce the proximate importance of food supply, and controversy continues to exist as to the role that food supply plays in shaping the patterns of life history, population dynamics, and community structure we see in nature (Lack 1954; Hairston et al. 1960; Sinclair 1975; Weins 1977; White 1978; Fretwell 1987; Oksanen 1988; Arcese and Smith 1988).
Assessment of food limitation has been hampered by the dif- ficulty of determining actual food availability. Social behaviour, secondary plant compounds, and predation pressure can act to make apparently abundant resources inaccessible to some or all members of the population. An alternative to measuring food availability is to experimentally manipulate food supply. In this review, I examine studies where the food supply of terrestrial vertebrates was supplemented under field conditions. I could find only two cases in which food supply was experimentally reduced (Todd and Keith 1976; Ewald and Carpenter 1978). Most studies were designed to address questions of population limitation, but, more recently, they have also been concerned with behavioural responses to food addition. A few have dealt with effects of food supplementation at the community level. The review is divided into four main sections which address behavioural, life history, demographic, and community respon- ses to food addition. Within each section, I pose specific questions, present the data pertinent to the questions, and draw
conclusions. As is often the case in ecology, the amount of empirical data is distressingly small.
Who and where? I tried to include all published studies in which food supplies
were manipulated under field conditions. This includes studies in which the population was enclosed, but under natural conditions otherwise. Food manipulation included addition of artificial food and alteration of natural food by fertilization. I did not include any so-called "natural" experiments where food supply changed independently of control by the experimenter, nor have I included provisioning studies of primates, as the latter have been reviewed elsewhere (Fa and Southwick 1988; Asquith 1989). I did not exclude any studies which failed to meet certain statistical design criteria such as proper controls and replication. The majority of studies, particularly those dealing with population-level questions, were not replicated. All studies had some form of control, although this may have been merely before and after comparisons.
Table 1 lists 138 cases for which food supply was manipu- lated in terrestrial vertebrates. I considered a case to be a food addition to a single species in a localized area (food addition to more than one site during the same study was considered a single case). The 70 mammal, 58 bird, and 10 herpetologic cases include animals that range in body size from tadpoles to polar bears. However, all but seven studies dealt with animals weighing less than 2 kg. Most food additions have
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204 CAN. J. ZOOL. VOL. 68, 1990
TABLE 1 . Studies that have manipulated food supplies under field conditions for terrestrial vertebrates; the geographic location, habitat, diet of the primary species involved, and the primary level of anlysis (individual, population) are also provided
Locationa ~ a b i t a t ~ Dietc ~ n a l ~ s i s ~ Reference
teu tna tna tna tna tna tna tna tna tna tna tna teu tna teu teu teu tro teu teu tna tna tna bna tna tna tna tna teu sca tna sca sca teu sca teu teu teu sca sca sca tr 0
tna sca bna tna tna tna tna teu tna tna sca
tna tna tna teu aus
inse SC
SC
inse ca c a in ne he he inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse inse se SC
SC
SC
SC
inse in in in inse inse inse
Newton and Marquiss (1981) Ewald and Bohwer (1982) Searcy (1979) Wimberger ( 1988) Ewald and Bransfield (1987) Ewald and Orians (1983) Powers (1 987) Ewald and Carpenter (1 978) Ewald and Bransfield (1987) Mock et al. (1987) Berner and Grubb (1 985) Heinrich (1988) Yom-Tov (1 974) Berner and Grubb (1985) Dijkstra et al. (1982) Harris (1978) Horsfall (1 984) van Riper (1984) Watson et al. (1984) Watson and O'Hare (1979) Berner and Grubb (1985) Arcese and Smith (1988) Smith et al. (1980) Desrochers et al. (1988) Brittingham and Temple (1988) Samson and Lewis (1979) Samson and Lewis (1979) Berner and Grubb (1 985) Krebs (1971) Kallander (1 98 1) Berner and Grubb (1985) Bromssen and Jansson (1980) Jansson et al. (198 1) Kallander ( 1974) Kallander (198 1) Van Balen (1980) Krebs (1971) Grubb (1987) Ekman (1987) Bromssen and Jansson (1980) Jansson et al. (1981) Wong (1983) Reese and Kadlec (1984) Hogstedt (1 98 1) Hochachka and Boag (1987) Knight ( 1988) Berner and Grubb (1985) Franzblau and Collins (1980) Wasserman (1983) Davies and Lundberg (1984, 1985) Berner and Grubb (1985) Berner and Grubb (1985) Enoksson and Nilsson (1983)
Pulliam and Dunning (1987) Tamm (1985) Crossner (1 977) Kacelnik ( 1984) Catterall et al. (1982)
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TABLE 1 . (continued)
Location" ~ a b i t a t ~ Dietc ~ n a l ~ s i s ~ Reference
Mammals Community studye Antechinus stuartii Apodemus sylvaticus
Peromyscus leucopus, P . maniculatus Peromyscus maniculatus
Peromyscus polionotus Community studye Sciurus carolinensis
Sciurus niger
tna aus teu sca te u tna tna beu sca teu teu sca bna tna tna bna bna bna bna bna bna beu sca tna tna tna tna tna tna tna tna tna aus tna aus aus tna tna tna tna tna '
he in inse inse inse ca ca he he he he he he se ca he he he he he he he he he he he he he he he he inse inse inse inse inse inse inse he he he inse inse inse inse inse inse inse inse inse inse se se se se se se se se se
Abramsky (1978) Dickman ( 1 988) Flowerdew (1972) Hansson (197 1) Watts (1970) Lyndaker ( 1987) Todd and Keith (1976) Banach (1986) Hasson (197 1) Watts (1970) Andrzejewski (1975) Ims (1987) Gilbert and Krebs (198 1) Sullivan et al. (1983) Calhoon and Haspel (1989) Vaughan and Keith (198 1) Vaughan and Keith (198 1); Keith (1989) Windberg and Keith (1976) Krebs et al. ( 1 9 8 6 ~ ) Krebs et al. (1986b); Smith et al. (1988) Boutin (1984) Monaghan and Metcalfe (1985) Hasson (197 1) Krebs and DeLong (1 965) Ostfeld (1986) Ford and Pitelka (1984) Cole and Batzli (1978) Desy and Thompson (1983) Taitt and Krebs (1983) Taitt et al. (1981) Taitt and Krebs (198 1) DeLong (1 967) Newsome (1970) Newsome et al. (1976) Bomford ( 1987) Bomford and Redhead (1987) Vickery (1 984) Young and Stout (1 986) Verme (1965) Ozoga and Verme (1982); Ozoga (1987) DelGiudice et al. (1989) Young and Stout (1986) Bendell (1 959) Hansen and Batzli (1979) Hansen and Batzli (1978) Wolff (1985) Gilbert and Krebs (198 1) Vickery ( 1984) Fordham (197 1) Taitt (198 1) Smith (1971) Brown and Munger (1985); Bowers etal . (1987) Kenward (1985) Havera and Nixon (1980) Lima et al. (1985) Lima and Valone (1986) Newman and Caraco (1987) Newman et al. (1988) Baumgartner (1938) Havera and Nixon (1980)
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CAN. J . ZOOL. VOL. 68, 1990
TABLE 1 . (concluded)
Location" ~ a b i t a t ~ Dietc ~ n a l ~ s i s ~ Reference
Dobson (1979) Dobson and Kjelgaard ( 1 985 a , 1985 b ) Lord and Casteel (1960) Mares et al. (1976) Giraldeau and Kramer ( 1 982) Mares et al. ( 1 982) Sullivan and Sullivan (1982) Hurly and Robertson ( 1 987) Lunn and Stirling (1985)
Rose (1982) Stamps and Tanaka (198 1 ) Licht (1974) Andrews ( 1 976) Guyer (1988a, 1988b) Smith ( 1 983)
Simon (1975) Ferguson et al. (1983) Waldschmidt (1983) Ferguson et al. ( 1 982); Ferguson and Fox ( 1 984)
"Location: tna, temperate North America; teu, temperate Europe; bna, boreal North America; tro, tropical; sca, Scandinavia; beu, boreal Europe; aus, Australia; arc, arctic. bHabitat: fo, forest; sh, shrub; gr, grassland; ma, marsh; tu, tundra; me, marine estuary; po, pond; ot, other. 'Diet: he, herbivore; ca, carnivore; in, insects; inse, insects and seeds; se, seed; sc, scavenger; ne, nectarivore. dAnalysis: p, population; i , individual; c, community. 'Community study involving a number of rodent species.
involved herbivores (57, including seed eaters and nectarivores), omnivores (47, insect and seed eaters), and insectivores (1 9). Food has been supplemented in carnivores only eight times. Clearly, the primary targets of food addition studies, i.e., small-bodied herbivores, reflect the ease with which their food supply can be manipulated.
The majority (70%) of food addition studies have been conducted in north temperate regions and another 20% were conducted in boreal areas. The tropics have been the location for food supplementation studies in only nine cases; seven of these involved lizards. Sixty-one percent (85) of the studies were conducted in forested habitat, 12% (20) in grassland, and 12% (18) in shrubland. Thus, the geographic distribution of food addition studies is extrcmely limited.
Behavioural changes with food addition Home range size
The general empirical relationship between home range size and body size has led researchers to argue that home range size is largely a function of resource requirements and availability (McNab 1963; Harestad and Bunnell 1979). Table 2 shows that food addition led to a decrease in home range size in 19 of 23 cases, which lends support to this argument. However, more recent models suggest that territory size is a function of intruder pressure as well as resource availability (Hixon 1980; Schoener 1983). Addition of food alters both factors simultaneously because intruders (immigrants; see Table 5) are also attracted to the supplemental food. Boutin (1 984) used radiotelemetry to monitor movements of snowshoe hares during food supplemen- tation. Many animals immigrated to the food addition area and some of these took up residence, but others commuted from home ranges well off the food addition site. Mares et al. (1982)
adding food, by cropping individuals. Home range size de- creased with food addition in the absence of increased intruder pressure.
Territorial display rate Results of food addition experiments also indicate that
individuals alter display rates and types of display according to resource levels on the territory. Ewald and Carpenter (1978) lowered the resources available on hummingbird territories; the birds then spent less energy defending and more time off their territory, as predicted by economic territory models. Other studies suggest that the birds respond to short-term resource depression by using relatively inexpensive territorial displays. As the quality of the resource increased, so did the frequency of more costly defence displays (Ewald and Orians 1983). Tamm (1985) found that humiingbirds increased their display activity with increasing resources on their territory, as was the case in red-winged blackbirds (Searcy 1979) and juvenile lizards (Stamps and Tanaka 1981). Powers (1987) varied food quality on the breeding territory of male Anna's hummingbirds and found that territory size did not vary with energy available, but the degree to which the food resource was defended depended on food quality.
Social organization Only six studies have examined changes in social organiza-
tion with food supplementation. Ostfeld (1986) and Ims (1987) found that female voles became more aggregated and allowed increased overlap of home ranges with extra food. When food was in short supply, females defended exclusive areas.
Monaghan and Metcalfe (1985) attracted brown hares to a concentrated food source. Although normally solitary, the hares congregated at the feeding site and showed some of the benefits
were able to control intruder pressure among chipmunks, while associated with group behaviour: decreased vigilance and
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TABLE 2. Studies that have examined behavioural responses to food addition (-, decrease; +, increase; *, examined in study; blank, not examined)
C . albus C . americana C . corm C . cristata L . lagopus M . carolinus P . atricapillus P . bicolor P . carolinensis P . montanus Parus sp. P. pubescens P. erythrophthalmus 0 P. modularis -
R . satrapa S . carolinensis S . europaea -
S . calliope S . vulgarus
Mammals C . latrans C . rufocanus -
E . townsendii -
L. americanus - L. europaeus M . californicus -
M . townsendii - -
N . insignis P . leucopus,
P . maniculatus 0 P. leucopus P . maniculatus -
S . carolinensis
T . striatus
T . hudsonicus
Reptiles A . aeneus -
N . humilis 0 S . jarovi -
S . undulatus - U. stansburiana 0
Ewald and Rohwer (1982) Searcy ( 1979) Wasserman (1 983) Ewald and Bransfield (1987) Powers (1 987) Ewald and Carpenter (1 978) Ewald and Orians (1 983) Ewald and Bransfield (1987)
* Mock et al. (1 987) Berner and Grubb (1985)
* Heinrich (1 988) Berner and Grubb (1985) Watson et al. (1984) Berner and Grubb (1 985) Desrochers et al. (1 988) Berner and Grubb (1985) Berner and Grubb (1985) Ekman (1 987) Grubb (1987) Berner and Grubb (1985) Franzblau and Collins (1 980) Davies and Lundberg (1985) Berner and Grubb (1985) Berner and Grubb (1985) Enoksson and Nilsson (1983) Tamm (1985) Kacelnik ( 1984)
* Monaghan and Metcalfe ( 1985) Ostfeld (1 986) Taitt et al. (1981) Taitt and Krebs (1 98 1) Taitt and Krebs (1983) Vickery (1984)
Wolff (1985) Hansen and Batzli (1978) Taitt (1981) Vickery (1 984) Stapanian and Smith (1984) Newman and Caraco (1987) Kenward (1985) Newman et al. (1988) Lima and Valone (1986) Lima et al. (1985) Mares et al. (1976) Mares et al. (1982) Giraldeau and Kramer (1982) Hurly and Robertson (1987)
Stamps and Tanaka (198 1) Guyer (1988a, 1988b) Simon (1975) Ferguson et al. (1983) Waldschmidt (1983)
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208 CAN. J. ZOOL. VOL. 68, 1990
increased foraging when in larger groups. When the food source was clumped, aggression between individuals increased and dominant individuals were more likely to monopolize the food source. Lyndaker (1987) supplied food at two different rates to coyotes in two large enclosures. Group size was larger in the enclosure receiving more food.
Ekman (1987) supplied flocks of willow tits with extra food. Flock members responded by spending more time being vigilant and at sites less exposed to predators. When sunflower seeds were provided so costs of obtaining them were low, flock size did not change. When the seeds were made more difficult to obtain, flock size decreased. Ekman (1987) argued that this was due to increased cost of flock foraging.
Ewald and Rohwer (1982) supplied red-winged blackbird territories with food dispersed in two ways. When a single feeder per territory was used, there was an increase in polygyny, but this was not the case when the number of feeders per territory was increased. The authors argue that the latter was due to males defending smaller territories because of an increase in intruder pressure. In dunnocks, food addition led to decreased territory size of females, which in turn led to increased polygyny because males could monopolize more females (Davies and Lundberg 1984).
Food addition has been used to test hypotheses concerning why birds forage in mixed species flocks. If birds forage in these flocks to increase their chances of finding food, an increase in food supply should lead to more foraging by single individuals or in single species flocks. This prediction has been supported in two different studies (Berner and Grubb 1985; Grubb 1987).
Foraging behaviour Food supplementation has been used to test some optimal
foraging models. Vickery (1984) supplied two types of food that varied in caloric gain per handling time to three species of small mammals. In all cases, food items with the highest net energy gain were preferred, as predicted, but the consumption of the less profitable item varied with its abundance, which was not predicted.
There have been a series of food addition studies with grey squirrels to examine how predation hazard affects diet choice and patch use. Lima et al. (1985) found that squirrels utilized artificial patches in a manner predicted by a model that incorporated predation risk, i.e., the tendency to carry a food item to protective cover decreased with increasing distance from cover and increased with item size. Other studies have shown that squirrels trade off foraging efficiency for minimization of predation risk (Newman and Caraco 1987; Newman et al. 1988). Lima and Valone (1986) found that squirrels also rejected more profitable, but small, food items in favor of larger, less profitable items that could be carried back to protective cover for consumption.
To summarize, food addition studies to terrestrial vertebrates have shown that these organisms respond by altering foraging patterns, aggressive levels, and home range size. The level and distribution of supplemental food can affect overall social organization by altering group size and the spatial relationship of males and females.
Effects of food addition on life history Initiation of reproduction
Table 3 lists the studies that measured changes in reproduc- tive parameters in response to food addition. The breeding season was advanced and (or) extended in 33 of 39 cases in
which it was examined. Breeding intensity of adult females (i. e. , proportion breeding) increased in 18 of 25 studies, all but 1 involving mammals. Juvenile females responded in four of five cases. Age at first reproduction decreased with food addition in the five cases where it was measured (Bendell 1959; Hansen and Batzli 1978; Taitt 198 1 ; Ford and Pitelka 1984; Dobson and Kjelgaard 1985 b).
Clutch and litter size Only 4 of 13 avian studies showed an increase in clutch size
after food addition. Arcese and Smith (1988) argued that clutch size may be limited by genetic and developmental factors, except under conditions of density dependent limitation by food supply. They observed an increase in clutch size of song sparrows with food addition during high densities, but not during low densities (Smith et al. 1980). Increased clutch size also seems to occur with food addition when natural food supplies are relatively poor (poor territories with European sparrow hawks (Newton and Marquiss 198 l) , and poor years with kestrels (Dijkstra et al. 1982)). Davies and Lundberg (1985) found no increase in clutch size in dunnocks after food addition. They hypothesized that larger species may be more likely than smaller ones to increase clutch size with supplemen- tal food because the formation of eggs is more likely to delay reproduction (it takes longer to gather reserves for formation of the egg) in larger species. This hypothesis is not supported by the food addition experiment of Arcese and Smith (1988).
In mammals, it is often difficult to determine litter size and so there are only eight food addition studies that measured litter size; five of these showed an increase in litter size. In one other case, the trend was toward larger litters in food addition areas, but the difference was not significant (Bomford and Redhead 1987). Bendell (1959) found no difference in litter size in an introduced island population of Peromyscus given supplemen- tal food relative to unsupplemented populations. Lunn and Stirling (1985) found no increase in litter size in polar bears with access to garbage dumps.
In all studies that showed an increase in clutch or litter size, the increase brought sizes to the level seen in good habitats or in good years. The only exception to this was a study of snowshoe hares by Vaughan and Keith (198 1) where they found litter sizes of snowshoe hares to be higher by 1.3 young in supplemented populations than ever seen in natural populations for that area.
Only two studies examined reproductive parameters in reptiles. Guyer (1988a, 1988 b) found that clutch size increased in Norops humilus, whereas Rose (1982) found that Amolis acutus increased in body weight, but not clutch size, after food addition.
Body weight and growth rate Many studies have used changes in body weight or growth
rate as indicators of changes in condition. Table 4 shows that body weights of adults (25 of 34 cases; G-test = 7.8, P < 0.01) and juveniles (13 of 20 cases; G-test = 1.8, P > 0.5) increased with food addition and growth rates of juveniles improved in 20 of 22 cases.
Increased energy available from food addition could be shunted into increased somatic growth or reproduction. The information given above shows that both can occur, but only two studies have used food addition experiments to examine the relative allocation of energy to growth and reproduction (Dobson and Kjelgaard 1985b; Guyer 1988b). Dobson and Kjelgaard (1985 b) added food to populations of ground squir- rels at high and low elevations. They found that the proportion
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TABLE 3. Changes in reproductive parameters during food manipulation studies of terrestrial vertebrates (+, increase; 0 , no change; blank, not examined); breeding intensity refers to females only
- - ---
Breeding - - - -
Intensity Litter or Clutch Season
size length Adults Juveniles Reference
Birds A. nisus A. phoeniceus C. corone F . tinnunculus F . atra M . melodia
Newton and Marquiss (198 1 ) Ewald and Rohwer (1982) Yom-Tov ( 1974) Dijkstra et al. (1982) Horsfall ( 1 984) Arcese and Smith (1988) Smith et al. (1980) Bromssen and Jansson ( 1 980) Kallander ( 1 974) Bromssen and Jansson ( 1 980) Wong (1983) Reese and Kadlec ( 1 984) Hogstedt (198 1 ) Hochachka and Boag (1987) Knight (1988) Davies and Lundberg (1985)
+ Sullivan et al. ( 1 983) Vaughan and Keith (1981) Vaughan and Keith ( 1 98 1 ) Windberg and Keith (1976) Krebs et al. ( 1 9 8 6 ~ ) Krebs et al. (19866) Boutin (1984)
+ Ford and Pitelka (1984) Cole and Batzli ( 1 978) Desy and Thompson (1983) Taitt and Krebs (1983) Taitt and Krebs (198 1 ) DeLong ( 1 967) Newsome (1970) Bomford (1987) Bomford and Redhead ( 1987) Verme (1965) Ozoga (1987) Bendell ( 1 959) Hansen and Batzli (1979)
0 Hansen and Batzli (1978) Gilbert and Krebs (1981) Fordham ( 1 97 1 ) Taitt (198 1 ) Havera and Nixon (1980) Havera and Nixon (1980)
+ Dobson and Kjelgaard (1985 b) Sullivan and Sullivan (1982) Lunn and Stirling (1985)
C. glareolus
C. rutilus E. townsendii L. americanus
M . californicus M . ochrogaster M . pennsylvanicus M . townsendii
M . musculus
0. virginianus
P. leucopus
P . maniculatus
S . carolinensis S . niger S . columbianus T. douglasii U. rnaritimus
Amphibians and reptiles A. acutus N . humilis
Rose (1982) Guyer (1988a, 1988 b)
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210 CAN. J. ZOOL. VOL. 68, 1990
TABLE 4. Changes in body weight and growth rate of terrestrial vertebrates receiving food supplementation (+ , increase; 0, no change; blank, not examined)
Body weight Growth
Adults Juveniles rate Reference
Birds A. nisus C . albus C . corone F . arctica M . melodia
P . atricapillus P . cristatus P . montanus P . pica S . vulgaris
Mammals A. sylvaticus C . glareolus
C . rutilus E . townsendii L . americanus
M . californicus M . ochrogaster M . pennsylvanicus M . townsendii
M . musculus 0. nutalli P . gossypinus P . leucopus
P . maniculatus
S . carolinensis S . niger S . columbianus U . maritimus
Amphibians and reptiles A. acutus A . aeneus A . cristatellus A . limifrons A . oculatus N . humilis P . triseriata S . undulatus U . stansburiana
Newton and Marquiss (1981) Mock et al. (1987) Yom-Tov (1 974) Harris (1978) Arcese and Smith (1988) Smith et al. (1980) Brittingham and Temple (1988) Bromssen and Jansson (1980) Bromssen and Jansson (1980) Hogstedt (198 1) Crossner ( 1977)
Flowerdew (1 972) Banach (1986) Andrzejewski (1 975) Gilbert and Krebs (1981) Sullivan et al. (1 983) Vaughan and Keith (198 1) Windberg and Keith (1976) Krebs etal. (1986~); Smith etal. (1988) Krebs et al. (1986b) Boutin (1984) Krebs and DeLong (1965) Cole and Batzli (1978) Desy and Thompson (1983) Taitt and Krebs (1983) Taitt et al. (1981) Taitt and Krebs (198 1) DeLong (1 967) Young and Stout (1986) Young and Stout (1986) Hansen and Batzli (1979) Hansen and Batzli (1978) Gilbert and Krebs (198 1) Fordham (1 97 1) Taitt (1981) Havera and Nixon (1980) Havera and Nixon (1980) Dobson and Kjelgaard (1985b) Lunn and Stirling (1985)
Rose (1982) Stamps and Tanaka (1 98 1) Licht (1 974) Andrews (1 976) Andrews (1 976) Guyer (1988a, 1988 b ) Smith (1983) Ferguson et al. (1983) Waldschmidt (1 983) Ferguson and Fox (1984)
of energy devoted to reproductive effort increased in food- found that males increased in body size whereas females supplemented populations, at both high and low elevations, as increased egg production. This reflected the different selection compared with control populations. The relative increase was pressures on males (competition for mates) and females greatest at high elevation, a site where squirrels tended to have (reproduction). However, this may not always be the case as smaller litters and lower average body weights. Guyer (1988a, others have found that female lizards increase fat stores, rather 1988 b) supplied additional food to anolis lizard populations and than reproduction, with food addition (Licht 1974; Rose 1982).
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The above studies show that life history traits are phenotypically plastic and sensitive to food availability.
To summarize, food addition studies with terrestrial verte- brate populations in temperate environments show that timing of breeding, age at first reproduction, and growth rates are usually limited by food availability. Litter or clutch size is affected less by food supply, particularly in birds, but does increase with food addition when natural conditions are poor or when high densities lead to density-dependent food limitation.
Demographic consequences of food addition I found a total of 66 cases (26 birds, 38 mammals, 2 reptiles)
in which changes in population density or rate of growth was measured in response to food addition (Table 5). This includes some 42 different species, all but 3 of which were primarily first-order consumers (16 herbivores, 8 seed eaters, 39 seed and insect eaters). Two-thirds of these studies added food for a single year or less. There were 19 cases in which food was added over a full year and 23 cases in which food was added in multiple years. I listed relative changes after food addition for each year in multiyear studies and for each experiment when more than one type of food addition was performed in a single study. The size of area covered by the food addition varied considerably between studies, but tended to be larger in birds than in mammals. In the case of mammals, it was less than 10 ha in all but six cases. The number of individuals receiving supplemental food varied from 1 to 300, but in 74% of the cases, was 50 individuals or less. In general then, food supplementation studies designed to examine questions of population dynamics have been short term and conducted on a relatively small spatial scale.
Does food supplementation lead to increased population growth or density?
Fifty of 66 (G-test = 16.07, P < 0.001) cases showed a positive response (increased density or rate of population growth) to food addition. If all possible comparisons (seasons, years) are examined, breeding density increases occurred 64% ( n = 67; G-test = 5.46, P < 0.05) of the time whereas density increases, as measured by averaging over the entire period of food addition, occurred 75% ( n = 73; G-test = 19.65, P < 0.001) of the time. These values are not statistically different (G-test = 2.08, P > 0.2). The average relative density increase was slightly lower for breeding than for average densities (2.4 and 2.6, respectively). The greatest density increase was tenfold, but there were only nine instances in which the relative increase was fourfold or greater.
I attempted to classify each comparison according to the density (high or low, as indicated by the authors) and rate of population change of the control population (increasing, stable, or declining) during the food addition. Populations were as likely to show a relative population increase with food addition, regardless of whether the control population was increasing (80%, n = 1 3 , stable (70%, n = 3 l) , or declining (73%, n = 15). There were only seven cases that were classed as having high control densities and four of these showed a relative increase. There were 13 cases in which control densities were classed as low and 7 of these showed a relative increase. This relatively low value was usually because the control population underwent an increase in density at the same time as the supplemented population did.
Finally, I examined cases in which the authors had assessed relative environmental conditions (poor, fair, or good) during
the experiment. Populations responded to food addition more frequently when conditions were rated as poor than when rated as fair to good (87% vs. 39%, n = 15 and 18, respectively; G-test = 8.4, P < 0.01) and the relative response was also greater when conditions were poor (2.8 vs. 1.6; F = 1 1.47, P < 0.005, df = 1,3 1). In general, then, food supplementation leads to a two- to three-fold increase in density. Populations are less likely to respond when environmental conditions are fair to good.
Of the 16 cases (9 birds, 7 mammals) which showed no relative increase with food addition, two, and possibly a third, attributed the lack of response to the supplemental food being of inadequate nutritional quality (Havera and Nixon 1980; Krebs and DeLong 1965). Three studies involved small sample sizes (Samson and Lewis, 1979, tufted titmouse; Berner and Grubb, 1985, golden-crowned kinglet; Young and Stout 1986, golden mouse) and two others measured density increase as occupancy of territories in previously unoccupied habitats (Yom-Tov 1974; Hogstedt 198 1). Of the remaining eight studies, four were conducted during fair to good environmental conditions (Cal- houn and Haspel 1989; Desrochers et al. 1988; Pulliam and Dunning 1987; Hansen and Batzli 1979), and one was conduct- ed while the control population was undergoing rapid increase (Smith et al . 1980). Two cases involved fluctuating populations that were undergoing declines when the food was added (Newsome et al . 1976; Krebs et al. 1986b). This leaves only two cases, both of which involved species of parids and measured breeding densities only (Krebs 197 1 , great tit; Brittingham and Temple, 1988, black-capped chickadees).
There is strong evidence then, that food supply frequently limits population density. What about population regulation? Table 5 shows that extra food frequently alters rates of reproduction, survival, and immigration. However, it is diffi- cult to make general comparisons because of differences in the timing of food addition and in the question being addressed. This is particularly true for comparisons between studies of birds and mammals. As a consequence I will examine each group separately.
Food supplementation and population regulation in birds Lack (1954) argued that winter food supply determines
survival over the winter and subsequent breeding density of bird populations. This hypothesis has been the focus of most food addition studies with birds and it has been tested in 12 cases (Krebs 197 1; Samson and Lewis 1979; Van Balen 1980; Smith et al. 1980; Kallander 198 1 ; Jansson et al. 198 1 ; Desrochers et al. 1988; Brittingham and Temple 1988). Survival rate was improved in all of the six cases where it was measured (Smith et al. 1980; Van Balen 1980; Jansson et al. 198 1 ; Desrochers et al. 1988; Brittingham and Temple 1988). However, breeding densities were increased in only 6 of 12 cases (Krebs, 197 1, blue tits; Samson and Lewis, 1979, black-capped chickadees; Van Balen, 1980, and Kallander, 1974, great tit; Jansson et a l . , 1981, tits). The response to food addition appears to be dependent on food availability at the time of the experiment. Van Balen (1980) found a strong correlation between beech mast and breeding densities of great tits in Holland. Food supplementation altered survival and breeding density when the mast crop was poor, but not when it was good. The same pattern holds true in the remaining cases, which showed greater response when conditions were poor compared with when they were good.
Few studies have examined the effect of food supplementa-
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TA
BL
E 5. D
emog
raph
ic r
espo
nses
of
terr
estr
ial v
erte
brat
es to
foo
d ad
ditio
n (t
he d
urat
ion
(sea
sona
l (s)
or
full
yea
r (y
) of
foo
d ad
diti
on,
area
of
food
add
itio
n,
a ro
ugh
esti
mat
e of
the
num
ber
of i
ndiv
idua
ls re
ceiv
ing
food
(N
), re
lativ
e ch
ange
in
dens
ity (
bree
ding
sea
son
(BR
) an
d av
erag
e (A
VE
) fo
r th
e en
tire
foo
d ad
ditio
n pe
riod
), m
etho
d of
cal
cula
ting
rel
ativ
e ch
ange
, de
mog
raph
ic s
tatu
s of
the
con
trol
pop
ulat
ion
(D,
dens
ity)
, en
viro
nmen
tal
cond
itio
ns (
EC
) du
ring
th
e fo
od a
ddit
ion,
gen
eral
com
men
ts,
and
fact
ors
resp
onsi
ble
for
the
incr
ease
(su
rviv
al (
ad,
adul
ts; j
uv,
juve
nile
s),
imm
igra
tion
(0
, pro
duct
ivit
y (P
)) a
re
also
sho
wn;
bla
nk s
pace
s in
dica
te th
at t
he i
nfor
mat
ion
was
not
ava
ilab
le
Rel
ativ
e C
ontr
ol
chan
ge
stat
usb
Sur
viva
l A
rea
Dur
atio
n (h
a)
N
BR
A
VE
M
etho
da
D
Size
E
Cc
com
men
tsd
ad
juv
I P
R
efer
ence
Bir
ds
C. a
mer
ican
a s
C. c
oron
e s
C. c
rist
ata
s L
. lag
opus
Y
Ber
ner
and
Gru
bb (
1985
) +
Yom
-Tov
(1 9
74)
+ B
erne
r an
d G
rubb
(1 9
85)
Wat
son
et a
l. (1
984)
+
e
Wat
son
and
O'H
are
(197
9)
M. c
arol
inus
M
. mel
odia
P
. at
rica
pillu
s
Ber
ner
and
Gru
bb (
1 985
) S
mit
h et
a1.
(19
80)
Des
roch
ers
et a
l. (1
988)
Sam
son
and
Lew
is (
1979
) B
ritt
ingh
am a
nd T
empl
e (1
988)
P.
bico
lor
s S
P.
caer
uleu
s s S
Sam
son
and
Lew
is (
1 979
) B
erne
r an
d G
rubb
(19
85)
+ K
rebs
(19
71)
Kal
land
er ( 1
9 8 1)
P . c
arol
inen
sis
s P
. cri
stat
us
s P
. maj
or
s
Ber
ner
and
Gru
bb (
1985
) +
+ Ja
nsso
n et
a1.
(19
8 1)
+
Kal
land
er (
1 98
1)
+ +
Van
Bal
en (
1980
)
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TA
BL
E 5.
(con
tin
ued
)
Rel
ativ
e C
ontr
ol
chan
ge
stat
usb
Sur
viva
l A
rea
Dur
atio
n (h
a)
N
BR
A
VE
M
etho
da
D
Size
E
Cc
com
men
tsd
ad
juv
I P
Ref
eren
ce
P. m
onta
nus
P. p
ica
P. p
ubes
cens
R
. sat
rapa
S.
car
olin
ensi
s S.
pass
erin
a
Mam
mal
s A
. Jla
vico
lus
A. s
ylva
ticus
C. g
lare
olus
C. r
utilu
s
E. t
owns
endi
i Y
F. s
ylve
stri
s s
L. a
mer
ican
us
s
M. c
alif
orni
cus
Y S
M. oc
hrog
aste
r Y
M. p
enns
ylva
nicu
s y
M. t
owns
endi
i s
Kre
bs (
1971
) Ja
nsso
n et
al.
(198
1)
Hog
sted
t (1 9
8 1)
K
nigh
t (1
988)
B
erne
r an
d G
rubb
(1 9
85)
Ber
ner
and
Gru
bb (
198
5)
Ber
ner
and
Gru
bb (
1985
) P
ulli
am a
nd D
unni
ng (1
987)
Han
sson
(1 97
1)
Flo
wer
dew
(197
2)
Han
sson
( 19
7 1)
Han
sson
(1 97
1)
And
rzej
ewsk
i (1 9
75)
Gil
bert
and
Kre
bs (
1 98
1)
Sul
liva
n et
al.
(198
3)
Cal
hoon
and
Has
pel (
1989
) K
rebs
et
al. (
19
86
~)
Kre
bs e
t a
l. (1
986b
) B
outin
(1 9
84)
Kre
bs a
nd D
eLon
g (1
965)
Fo
rd a
nd P
itel
ka (
1984
)
Col
e an
d B
atzl
i (19
78)
Des
y an
d T
hom
pson
(19
83)
Tai
tt a
nd K
rebs
(1 9
8 1)
Tai
tt e
t al
. (19
81)
Tai
tt a
nd K
rebs
(19
83)
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TA
BL
E 5. (
conc
lude
d)
Rel
ativ
e C
ontr
ol
chan
ge
stat
usb
Surv
ival
A
rea
Dur
atio
n (h
a)
N
BR
A
VE
M
etho
da
D
Size
E
Cc
com
men
tsd
ad
juv
I P
R
efer
ence
M.
mus
culu
s Y
0.79
S s
0.82
0. nu
tall
i P
. go
ssyp
inus
P
. le
ucop
us
P. m
anic
ulat
us
S 2
Y 0.
84
S
P. p
olio
notu
s Y
1.8
S. c
arol
inen
sis
s 13
S. n
iger
Y
80
s 13
S. c
olum
bian
us
Y 1.
2
T. s
tria
tus
s 0.
4 T
. dou
glas
ii
Y 18
Rep
tiles
A
. ae
neus
s
0.00
01
N.
hum
ilis
s
0.07
DeL
ong
(1 96
7)
Bom
ford
(1 9
87)
Bom
ford
and
Red
head
(1
987)
N
ewso
me
(197
0)
New
som
e et
al.
(19
76)
You
ng a
nd S
tout
(19
86)
You
ng a
nd S
tout
(19
86)
Han
sen
and
Bat
zli
(197
9)
Han
sen
and
Bat
zli
(197
8)
Ben
dell
(19
59)
Gil
bert
and
Kre
bs (
198 1
)
Ford
ham
(19
71)
Tai
tt (
198 1
)
Smit
h (1
97 1
)
4 H
aver
a an
d N
ixon
(19
80)
Bau
mga
rtne
r ( 1
93 8
) H
aver
a an
d N
ixon
(19
80)
10
0 +
+ +
Dob
son
and
Kje
lgaa
rd
0 +
+ +
(19
85
~)
0 +
++
0
+ +
+
+ M
ares
et a
l. (
1976
) +
+ +
Sull
ivan
and
Sul
liva
n +
+ +
(198
2)
+ St
amps
and
Tan
aka
(198
1)
+ +
+ +
Guy
er (
1988
a, 1
988b
)
"Met
hod
1, r
atio
of
expe
rim
enta
l to
con
trol
den
sity
; 2,
rat
io o
f ch
ange
s in
exp
erim
enta
l de
nsit
y be
fore
ver
sus
afte
r fo
od a
ddit
ion
to s
ame
for
cont
rol
area
s; 3
, fin
ite c
hang
e in
exp
erim
enta
l po
pula
tion
s be
fore
ver
sus
afte
r fo
od a
ddit
ion,
con
trol
pop
ulat
ion
unch
ange
d; 4
, es
tabl
ishm
ent
of n
ew t
erri
tori
es i
n un
used
hab
itat;
5, c
ompa
riso
n of
fin
ite y
earl
y po
pula
tion
cha
nges
for
exp
erim
enta
l an
d co
ntro
l ar
eas;
6, c
ompa
riso
n of
rat
es o
f po
pula
tion
gro
wth
for
exp
erim
enta
l an
d co
ntro
l po
pula
tion
s.
*Dem
ogra
phic
sta
te o
f co
ntro
l po
pula
tion
: 1,
hig
h de
nsit
y; 2
, lo
w d
ensi
ty; 3
, inc
reas
ing;
4,
stab
le; 5
, dec
lini
ng.
'Env
iron
men
tal
cond
itio
ns:
1, p
oor;
2, f
air;
3, g
ood.
dC
omm
ents
: 1
, fe
rtil
ized
; 2,
foo
d re
mov
ed p
rior
to
the
star
t of
the
bre
edin
g se
ason
; 3,
sm
all
sam
ple
size
s; 4
, fo
od s
uppl
ied
may
hav
e be
en n
utri
tion
ally
ina
dequ
ate;
5,
popu
lati
ons
encl
osed
and
pre
- da
tors
exc
luse
d; 6
, cov
er m
anip
ulat
ed;
7, c
over
and
pre
dati
on m
anip
ulat
ed;
8, v
arie
d th
e nu
ritio
nal
qual
ity
of fo
od; 9
, foo
d su
ppli
ed a
t dif
fere
nt l
evel
s; 1
0, fo
od a
ddit
ion
cond
ucte
d a
two
diff
eren
t el
evat
ions
. 'P
rodu
ctiv
ity
was
mea
sure
d as
an
incr
ease
in
broo
d si
ze.
f~o
~u
lati
on
be
cam
e es
tabl
ishe
d on
an
isla
nd w
here
non
e ha
d ex
iste
d be
fore
.
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13Fo
r pe
rson
al u
se o
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tion on reproductive success in birds (Tables 3 and 5; see also, Martin, 1987). With two exceptions, all studies ceased addition at or before the time of hatching. Arcese and Smith (1988) supplemented a song sparrow population during the breeding season in a year of high density. They found that females with additional food produced four times the number of young that control females produced and this output matched that of females at low population density.
Watson et al. ( 1984) manipulated food supplies of red grouse by fertilization in three separate experiments. They were attempting to determine if breeding density was determined by a "direct nutrition" hypothesis (birds alter their aggressive behav- iour as a result of summer nutrition) or by an "indirect" hypothesis (nutrition of laying hens affects aggressiveness). The first two experiments, conducted when control populations were declining slightly and then increasing, produced support for both hypotheses. In each case, experimental densities were higher. The final experiment, conducted while control popula- tions were declining sharply, produced no response. Watson et al. (1984) concluded that variation in food quantity and quality could not explain the observed fluctuations in density.
Food supplementation and population regulation in mammals Relative to birds, mammals have received supplemental food
for longer periods of time (17 versus 2 cases where food was added for an entire year) and most seasonal food additions have occurred during the breeding season rather than over the winter (Table 5). Many of these studies have addressed the question of whether or not food limitation is responsible for seasonal and (or) multiyear population declines. I will consider demographic responses to food supplementation of mammals showing seasonal fluctuations separately from those showing multian- nual fluctuations.
Various species of Peromyscus and Apodemus show yearly fluctuations in density with numbers being lowest in spring and summer, rising to peak levels in autumn after the recruitment of juveniles, and then declining over the winter. In general, food addition produces increased densities through immigration (Fordham 197 1 ; Flowerdew 1972; Gilbert and Krebs 198 1 ; Taitt 198 1 ; Young and Stout 1986). Food addition advances breed- ing, increases reproduction, and can improve juvenile survival to trappable age. However, overall summer survival of adults and recruitment of juveniles is not improved and summer densities remain unchanged (Fordham 197 1 ; Flowerdew 1972; Hansen and Batzli 1978, 1979; but see Gilbert and Krebs, 198 1, and Taitt, 198 1). Early autumn densities have been increased with food addition (Gilbert and Krebs 198 1 ; Hansen and Batzli 1978).
Vole populations undergo more variable population fluctua- tions than do mice and these fluctuations have a multiannual pattern often characterized by abrupt "spring" declines (Taitt and Krebs 1985). Most food additions have been conducted to determine if increased food supply can prevent major popula- tion declines (Krebs and DeLong 1965; Cole and Batzli 1978; Taitt et al. 1981; Taitt and Krebs 1983; Desy and Thompson 1983; Ford and Pitelka 1984). In all but one case, the populations continued to decline despite supplemental feeding. However, Ford and Pitelka (1984) found that food addition in a predator-free environment slowed a population decline and stabilized densities of California voles while the control population declined to extinction.
Krebs and DeLong (1965) supplied California voles with food for a year during which the population showed a slight
increase, followed by a steady decline to low densities. This is the only food addition experiment with voles that did not result in higher population densities. Cole and Batzli (1 978) suggested that this was due to the supplemental food being nutritionally inadeqate. However, voles on the food grid had growth rates well above those on the control grid, suggesting that the food was nutritionally adequate. A possibility that was not consid- ered is potential competition with house mice. DeLong (1967) published the results of food addition experiments with a series of house mouse populations, one of which occupied the same area as the vole population studied by Krebs and DeLong (1965). The house mouse population underwent a five-fold increase and densities peaked when the vole population began to decline (see Fig. 3 of DeLong , 1967, and Fig. 1 of Krebs and DeLong, 1965). The high density of house mice may have inhibited growth of the vole population.
Cole and Batzli (1978) and Desy and Thompson (1983) supplemented food for populations of prairie voles and meadow voles, respectively. In both cases the food-supplemented population increased to double the density of the control, but then declined in synchrony with the control. In the study by Cole and Batzli (1978), supplemental food prevented a spring decline, but not a multiannual decline. Taitt et al. (1 98 1) and Taitt and Krebs (198 1, 1983) manipulated food, cover, and predation in Townsend voles during the period of spring decline. Supplemental food increased density, but did not prevent the spring decline. Populations declined in a density- dependent manner regardless of the experimental treatment (Taitt and Krebs 1983).
House mouse (Mus musculus) populations in Australia also show large fluctuations and Newsome (1970) tested the hypoth- esis that mouse plagues do not occur every year because of normally low food supplies during winter. He was able to create a plague by supplying food during winter, but the rate of population growth was considerably lower at high density, even in the presence of supplemental food. Bomford and Redhead (1987) manipulated food quality and female density in autumn when food quantity is normally high. They found that food with a higher protein content than natural food led to increased reproductive activity. Bornford (1987) also found that breeding in spring increased by food quantity and quality is unimportant.
Snowshoe hares undergo population cycles with major declines every 9-1 1 years (Keith et al. 1984; Krebs et al. 1986a). Hares were supplied with laboratory rabbit chow in winter during an increase, peak, and decline (Krebs et al. 1986a; Smith et al. 1988). The population doubled on food addition sites, but declined in synchrony with or soon after control populations. A second experiment in which natural food in the form of felled mature spruce was provided in the winter of a decline produced the same result (Krebs et al. 19866). However, Vaughan and Keith (1981) supplemented hares in pens stocked at low and high densities. Food-supplemented groups showed higher reproductive rates and survival, particu- larly of juveniles, relative to controls. In high density pens without supplemental food, they found reproductive and surviv- al rates similar to those observed in unenclosed populations during periods of decline (see also Keith, 1989). It is possible that Krebs et al. (1986a, 1986b) were unable to prevent a cyclic decline in hares with food addition because of heavy predation pressure on the food addition areas (Boutin et al. 1986).
In general, then, food addition tends to increase the amplitude of seasonal or multiannual fluctuations in mammalian popula- tions, but it does not alter the overall pattern of population
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2 16 CAN. J. ZOOL. VOL. 68, 1990
change. Food-supplemented populations are usually higher than control populations, but the timing and rate of population change are similar. The low recruitment of juveniles in summer in populations with seasonal fluctuations cannot be altered by food addition nor can ,the pattern of major declines in popula- tions showing multiannual fluctuations.
Finally, I examined 16 cases in which mammalian popula- tions received food over the winter (DeLong 1967; Hansson 197 1 ; Flowerdew 1972; Andrzejewski 1975; Hansen and Batzli 1978; Cole and Batzli 1978; Taitt and Krebs 1981; Sullivan and Sullivan 1982; Sullivan et al. 1983; Desy and Thompson 1983; Boutin 1984; Dobson and Kjelgaard 1985a; Krebs et al. 1986a, 1986b) to test Lack's (1954) hyothesis. Survival was improved in seven of these cases (Flowerdew 1972; Sullivan and Sullivan 1982; Sullivan et al. 1983; Boutin 1984; Dobson and Kjelgaard 1985a; Krebs et al. 1986~) . Changes in breeding density were measured in 11 cases and 9 of these showed an increase when food was added over the winter (Flowerdew 1972; Andrzejew- ski 1975; Hansen and Batzli 1978; Taitt 1981; Sullivan and Sullivan 1982; Sullivan et al. 1983; Desy and Thompson 1983; Boutin 1984; Dobson and Kjelgaard 1985 a; Krebs et al. 1986a, 1986b). Thus, mammals are less likely than birds to show improved survival over the winter with food addition (7 of 16 versus 6 of 6; Fisher exact test, P = 0.046), but they are more likely to show increased breeding densities (9 of 11 versus 6 of 12; Fisher exact test, P = 0.19).
Population declines in the presence of supplemental food There have been nine cases where food additions were
performed on fluctuating populations in an attempt to prevent population declines (Krebs and DeLong 1965; Cole and Batzli 1978; Taitt et al. 1981; Taitt and Krebs 1983; Desy and Thompson 1983; Ford and Pitelka 1984; Watson et al. 1984; Krebs et al. 1986a, 1986b). The only study that actually prevented a decline was done in a predator-free environment (Ford and Pitelka 1984). There is good evidence, then, that major declines cannot be prevented by food addition alone. However, it would be premature to reject the hypothesis that food availability is somehow involved in these declines. Future studies should employ a two-factor design that can examine food, predation, and their interaction. This is especially important since most food additions have been done on a spatial scale that is very small for predators and predator swamping of food addition sites could easily occur (Boutin et al. 1986).
Community structure Despite the importance of competition in community organi-
zation and the underlying assumption of resource limitation, I could find only four studies that manipulated food supply on a community scale (Abramsky 1978; Brown and Munger 1985; Bowers et al. 1987; Dickman 1988). Abramsky (1978) added alfalfa pellets and oats to an area of short grass prairie. The result was an increase in species diversity of the small mammal community through the addition of a new species. In another experiment, he increased productivity of the grasses by addition of nitrogen and water. There was no increase in species diversity in this instance, despite the addition of two new species, because ,the resident species normally present avoided the area. Abramsky interpreted ,these results as supporting MacArthur's (1972) prediction that an increase in scarce resources leads to an increase in species diversity. It is unclear whether the addition
Brown and co-workers (Brown and Munger 1985; Bowers et al. 1987) added seeds of varying size to a desert rodent community. The result was an increase in density of the largest seed eater (Dipidomys spectabilis) and a subsequent reduction in the second largest species (D. merriami, D. ordii). This result was independent of the size of seed added (small, large, mixed) or the method of administration (constant or pulsed). They also found that ,the addition of seed had no effect on the spatial use of microhabitats by the seed-eating rodents in the community (Bowers et al. 1987). These results supported the argument that the desert rodent community was organized largely by competition, with density of smaller granivorous rodents being inversely related to the density of the largest granivore .
Dickman (1988) examined the effects of a major competitor, Antechinus swainsonii, on the sex ratio of A. stuartii. Higher densities of A. swainsonii lead to more female-biased sex ratios in A. stuartii and removal of A. swainsonii or food addition reverses this pattern. Sons of mothers that received food were heavier and had higher survival rates than those from control females. Dickman (1988) argued that the addition of food allowed females to increase the amount of parental investment and thus produce more costly males.
General discussion Database limitations
Since the British Ecological Society published its symposium on animal populations in relation to their food resources (Watson 1970), there have been over 130 cases in which terrestrial vertebrates have received supplemental food. Almost 100 of these have been published since 1980. Despite this rapidly growing database, our ability to assess general ecologi- cal patterns of response to food addition is disappointing. Most studies have involved small-bodied herbivores that live in temperate environments. Therefore, it is still not possible to compare responses of large and small organisms (Caughley and Krebs 1983), herbivores and carnivores, or tropical and temperate environments.
It may never be possible to provision large-bodied carnivores at the scale relevant to questions of population dynamics and "natural" experiments may be the only alternative. However, it is surprising that I could not find any studies of the demographic response to food addition by ungulates. A relatively common management practice is to supply food to deer or elk during severe winters. Unfortunately, no one has monitored the effect of this food addition beyond the observation that many individuals are attracted to the feeding area. The long-term population effects remain unknown. The studies by Verme (1965) and Ozoga (1987) are welcome exceptions.
This review emphasizes the need for researchers to expand the ecological conditions under which food additions are performed. I was particularly surprised at the paucity of food supplementation studies conducted in tropical regions. Does this pattern mean that researchers consider food limitation to be relatively unimportant in tropical systems? This seems unlikely and it may, instead, reflect the emphasis on observational rather than manipulative experiments. Food supplementation experi- ments in the tropics would provide particularly useful informa- tion to compare life history responses of organisms with results obtained in more seasonal temperate areas.
of new spec-ies to the experimental plots was a result of an Population limitation and regulation and food supplementation absolute increase in resources or to the addition of a new Most food addition studies have addressed questions of resource (i.e., an increase in the resource spectrum). population regulation and limitation and it is here that we can
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draw some general conclusions. There are two consistent outcomes. The first is a twofold increase in population density, confirming the conclusion of Gilbert and Krebs (1981). When breeding density increased after food supplementation, in 26 of 43 cases the amount of increase was between 1.5-2.5 times (Table 5). This occurred in 3 1 of 57 cases when average density was considered. Thus, in temperate environments at least, terrestrial vertebrate populations are frequently limited by food supply. The second consistent outcome of food supplementa- tion experiments is that even though birth rate, immigration, and survival are frequently altered by foods supplementation, the general pattern of population dynamics is not. Even in the presence of presumably unlimited food, populations do not continue to increase.
I offer the following possible explanations as to why food supplementation studies have produced these results: (i) factors other than food become limiting after a doubling of density; (ii) even though food is thought to be provided ad libitum, it becomes limiting after a doubling of density because the way it is distributed does not allow access to all individuals; (iii) the true response to food addition is much less than a doubling and most of the increase is due to an effectively larger census area (animals immigrate from off the study site); and (iv) food additions have not been conducted continuously over a long enough period and over a large enough area to produce greater increases.
There have been few experiments that address these possibili- ties. Predation has been manipulated along with food supply for Townsend voles, but this did not lead to more than a twofold increase in density (Taitt et al. 198 1; Taitt and Krebs 1983). However, Ford and Pitelka (1984) were able to prevent a major population decline in California voles by excluding predators and adding food. There have been no demographic studies that varied the manner in which food was supplied in any systematic way. In fact, there has been little attention paid to how food is administered. In many cases it was supplied from highly concentrated sources. This may allow dominant individuals to monopolize these sources or lead to a situation where interaction rate is so high at the feeders that the net benefits of the food are minimal (see Monaghan and Metcalfe 1985). Researchers have made little attempt to observe behavioural interactions at feeding sites to address this problem. It is crucial that future studies have some assessment of how individuals gain access to the supplemental food or that they compare the effects of administering the food in different ways.
The possibility that the usual twofold increase in density is simply due to immigration of animals from surrounding habitats is a problem of spatial scale. Densities, particularly in mam- mals, are usually estimated by mark-recapture data obtained from a livetrapping grid. Comparisons of densities of control and food addition grids assume that the effective trapping area is the same for each site. This may not be true if food supplementa- tion leads to increased movement of individuals surrounding the grid (Boutin 1984; Mares et al. 1976).
Pulliam and Dunning (1987) argued that food is often supplied on a spatial scale that is relevant to the question of habitat choice by individuals, but not to questions of population regulation. Table 5 shows that many studies have supplied food to 20 individuals or less and immigration is a common response to food addition. When increased reproduction and survival do occur (Table 5), it does not alter the pattern of population change. It is possible that food supplementation merely creates small "postage stamp" source habitats (Pulliam 1988) that export most of the increased production to surrounding areas.
The result is that density increase is limited to two- to three-fold by dispersal.
These ideas can be tested by altering the way food supple- mentation experiments are performed. We must increase both the temporal and spatial scales over which food is supplied. In addition, the behaviour of individuals receiving supplemental food must be monitored to determine if they have free access to the food and if dispersal in and out of the food-supplemented area increases relative to control areas. It is interesting to note that primate groups that have been provisioned for as long as 35 years continue to increase in density to as much as 10 times their original size (Asquith 1989).
Food additions, population dynamics, and individual behaviour
To date, most studies have addressed the effects of food addition at the population level. There has been no attempt to link the recent approach of studying population dynamics and behaviour from an individual perspective with food addition studies (Clutton-Brock and Albon 1985). Clutton-Brock and Albon (1985) hypothesized that behavioural factors act to concentrate the food shortage on certain individuals. Most food addition studies have considered only average responses of the population and have paid no attention to the behavioural interactions between individuals over food. In the crudest sense, food addition studies have shown that home range or territory size decreases and immigration increases with food addition (Tables 2 and 5), but we have learned little about how resources are allocated among individuals and how this, in turn, affects the behavioural and life history options open to an individual. The studies by Ostfeld (1986), Ims (1987), and Davies and Lundberg (1984) show how effective food addition studies can be at examining the relationship between food supply and social organization. Behavioural ecologists have begun to use food manipulations effectively to test hypotheses of optimal foraging and flocking behaviour by working at the individual level. Hopefully population ecologists will follow suit.
Response to food addition under different environmental conditions
Although the average density increase was twofold with food addition, there was a greater tendency for no response to occur when general environmental conditions were fair to good. Unfortunately, it is difficult to determine how frequently these "good" conditions occur in nature because many researchers have failed to place their experimental manipulations back into the natural context (i.e., what were relative control conditions and densities like). Studies that have done so or have added food to the same area, but at different population densities, have produced particularly useful results and should serve as models to researchers in the future (Smith et al. 1980; Arcese and Smith 1988; Pulliam and Dunning 1987). Experiments that supply food at different levels would also be helpful in this context (Taitt and Krebs 1981).
Researchers have also tended to pursue a "single factor" approach to food supplementation. I have already pointed out that social behaviour could be changed by food supplementation, and levels of predation are likely to change as well. Predators may be attracted to these high-density areas (Boutin et al. 1986) and concentrated food sources may serve to make the individu- als receiving food more vulnerable. Researchers must attempt to monitor these factors during food supplementation. An alterna- tive would be to perform food removal experiments. What percentage of available production must be removed before we see a reduction in reproduction, survival, or density?
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218 CAN. J. ZOOL. VOL. 68, 1990
To conclude, food addition studies have become increasingly common in the literature in the past 10 years. With this increase has come a broadening in scope to address not only questions of population dynamics but of behavioural and community ecology as well. However, this review indicates that the scope of envi- ronments and species that have received supplemental food is still limited. It would be premature to argue that the utility of food addition experiments is past. On the contrary, food addition studies in new environments and on new species that concentrate on the response of individuals should provide useful information to assess general ecological questions.
Acknowledgements Rick Lewis organized most of the initial database. Zena
Tooze and Mike Blower reworked countless tables and earlier drafts of this manuscript. I thank Richard Moses, Jean-Pierre Ouellet, Pamela Asquith, Scott Gilbert, Walt Klenner, Karl Larsen, Adam Watson, Lloyd Keith, and an anonymous re- viewer for providing useful comments on an earlier draft. This work was supported by an Unemployment Insurance Job Crea- tion Section 38 Program from the Unemployment and Immigra- tion Commission of Canada and by a Natural Sciences and Engineering Research Council operating grant (No. A3361).
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