Behavioral Ecology Vol. 10 No. 3: 270-274
© 1999 International Society for Behavioral Ecology
Foraging innovation is inversely related to competitive ability in male but not in female guppies
Sub-Department of Animal Behaviour, Department of Zoology, University of Cambridge, Madingley, Cambridge, CB3 8AA, UK
Address correspondence to K. N. Laland. E-mail: knl1001{at}hermes.cam.ac.uk
Received 14 April 1998; revised 22 August 1998; accepted 22 October 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Foraging success is likely to affect hunger level and motivation to locate and exploit novel food sources in animals. We explored the relationship between scramble competition for limited food and foraging innovation in the guppy (Poecilia reticulata), predicting that poor competitors would be more likely to innovate when presented with novel foraging tasks. Among males, we found that latency to complete novel foraging tasks was correlated both with weight gain and number of food items consumed, suggesting that poor competitors are more likely to innovate. However, among females there was no relationship between innovative tendency and either weight gain or foraging success. We suggest that this sex difference may reflect parental investment asymmetries in males and females, and we predict similar sex differences in other species.
Key words: animal proto-culture, foraging, guppies, innovation, Poecilia reticulata, scramble competition.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Animals often respond to novel ecological and social challenges, or physiological stresses, with new or modified acquired behavior patterns, or innovations (Kummer and Goodall, 1985
; Lee, 1991).
Innovation is an important component of behavioral plasticity, vital to the
survival of individuals in species with generalist or opportunistic lifestyles
(Lefebvre et al., 1997).
Moreover, the diffusion of a new behavior through a population is typically
thought to follow from the innovation of a single individual. However, despite
being fundamental to several significant research programs, including those
investigating foraging behavior, behavioral plasticity, and the social
learning and transmission of information, little is known about which
individuals form new behavior patterns or what ecological variables influence
innovation (Kummer and Goodall,
1985; Lee, 1991).
It is unclear whether animal innovation should be regarded as a personality
trait (associated with particularly clever or creative individuals), a
state-dependent variable (e.g., foraging innovation may be driven by hunger),
or whether it results from exposure to pertinent ecological stimuli (e.g., a
sudden change in the environment).
The best known examples of innovation in animal populations are novel
behavior patterns that facilitate the extraction, preparation, and processing
of food. These include the washing of potatoes and wheat by Japanese macaques,
Macaca fuscata, tool use in chimpanzees, Pan troglodytes,
and other primates, and milk-bottle-top opening by British titmice,
Parus spp. (Beck,
1980; Fragaszy and Visalberghi,
1990; Goodall,
1964; Hinde and Fisher,
1951; Kawai, 1965;
McGrew, 1994). Lefebvre et al.
(1997) described 322 separate
cases of feeding innovation in birds. In all such examples, a novel food
source is used, or exploited more efficiently, as a result of the innovation.
Other examples of innovation function in a social domain. For example, Goodall
(1986) described a male
chimpanzee that augmented his threat display by banging together empty
kerosene cans, a behavior that coincided with a dramatic rise in dominance
status.
Although compelling evidence is scarce, observations of natural animal
populations suggest that particular classes of individuals may be prone to
innovation. There is at least anecdotal evidence that innovators often differ
from the remainder of the group in some characteristic, such as rank, age, or
sex. Katzir (1982,
1983) found that mid- to
low-ranking jackdaws, Corvus monedula, were first to enter a novel
space or eat a new food, with top-ranking birds typically being second or
third. Primate studies appear to indicate that innovators are frequently on
the outskirts of the social group (Kummer
and Goodall, 1985). For instance, Sigg
(1980) found that peripheral
female hamadryas baboons, Papio hamadryas hamadryas, were
significantly better at learning novel tasks than central females. In their
review of novel tool use tasks among capuchins, Fragaszy and Visalberghi
(1990) found no evidence for
individuals possessing a "characteristic propensity" to show
innovative behavior.
To date, virtually all of the relevant empirical data on innovation in
animals stems from observations of natural populations. Inevitably such
reports have an anecdotal quality. In several instances, the novel behavior
has been observed only once, and in a single individual
(Kummer and Goodall, 1985).
Some behavior patterns are slightly idiosyncratic, and many such reports
require clarification before it can be certain that the behavior concerned is
more than a random or accidental event, or that it serves the function
attributed to it. There are numerous experimental studies demonstrating that
particular individuals, or species, are capable of solving a novel problem
(Köhler,
1925; Tomasello et al.,
1987; Visalberghi and
Fragaszy, 1990); however, the majority of such experiments have
not investigated within-species variation in problem-solving ability, and
there are surprisingly few experimental studies of problem solving that focus
on sex, age, or dominance-rank differences
(Hutt, 1973).
We explored the hypothesis that hungry individuals or poor competitors may
be driven by hunger to innovate to locate food by investigating the
correlation between innovation and past foraging success in small populations
of guppies. Guppies are an excellent model system for research into animal
innovation. Social transmission of foraging information has been clearly
demonstrated in guppies (Laland and
Williams, 1997), and it would be valuable to establish which
individuals are most likely to generate the foraging innovations. Social
learning in guppies is also implied in other contexts, such as mate choice
(Dugatkin and Godin, 1993) and
avoidance learning (Sugita,
1980). In addition, guppies have been found to exhibit significant
variation in the tendency to inspect unfamiliar predators
(Magurran et al., 1993), which
may reflect variation in a more general response to novel situations and
thereby influence foraging innovation. For instance, if guppies exhibit
variation in boldness or risk aversion, which is expressed in a number of
different contexts, this variability might influence innovation to locate and
exploit novel foods. Moreover, in addition to the substantial behavioral
literature on guppies, they have a number of practical advantages: they are
easy and inexpensive to keep in small populations as a consequence of their
small size and simple feeding requirements. In the wild, the guppy feeds on
several prey types in varied locations
(Dussault and Kramer, 1981) and
prefers to live in groups of conspecifics
(Magurran et al., 1995). Our
experimental paradigm imitates a scenario in which individuals move away from
the shoal to locate a novel food source.
We predicted that those fish least successful at scramble competition would be the individuals most likely to innovate when presented with novel foraging tasks. We tested the hypothesis directly by (1) monitoring over a 2-week period the change in weight of individuals in two mixed-sex populations of guppies, (2) recording the success of each individual at scramble competition, and (3) introducing into each population novel maze tasks, recording each fish's time to complete the task. These tasks required subjects to swim a series of mazes to locate hidden food sources. We predicted that there would be a positive relationship between weight gain and time to innovate, as measured by the time taken to complete the novel foraging tasks. We also predicted that there would be a positive relationship between number of food items previously consumed in scramble competition and time to innovate.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Subjects and apparatus
Our subjects were 32 adult guppies, 16 male and 16 female, purchased from Neil Hardy Aquatics. Subjects were chosen to represent a range of sizes, with females ranging in mass from 0.13 g to 1.14 g (
± SE =
0.57±0.07 g) and males varying between 0.15 g and 0.58 g (
± SE = 0.35 ± 0.04 g). Female fish were thus significantly
larger than males (t test: t30 = 2.71, p
<.025). Domestic rather than wild guppies were use because their
distinctive coloration allows recognition of individuals of both sexes while
avoiding stressful marking procedures. We studied two populations to increase
the power of the analysis. Fish were housed in standard 60x30x33 cm aquaria, with a water depth of 30 cm, maintained at 25°C. Novel foraging tasks were presented to populations of fish by introducing the task apparatus into the aquaria. Each novel task involved swimming through a maze apparatus, placed 10 cm from the end of the tank, and into a goal zone containing a floating feeder. The mazes were opaque white PVC dividing partitions, each containing a hole through which the fish could swim to the other end of the tank. A partition 10 cm in front of the maze allowed the apparatus to be set up while excluding the fish, with the raising of this partition signifying the beginning of a trial. A second partition slid directly behind the maze, being pushed down completely to close the hole on the goal-zone side once a trial had ended. The goal zone contained a concealed floating feeder of red plastic 30 mm in diameter and 6 mm deep. Small quantities (approximately four items) of freeze-dried bloodworm were placed in these feeders. For task 1, the maze apparatus was a partition with a 5x5 cm square, centrally located hole at the bottom of the tank. For task 2, the maze was a partition with a plastic, cylindrical, upright tunnel (height 6.5 cm, entrance diam 8 cm) covered in dark green cellophane in front of a square, centrally located 5x5 cm hole at the top of the partition. Here, the fish had to swim up the tunnel and then across through the hole to reach the food source. Dark green cellophane was used to cover the tunnel, as a see-through maze could confuse the fish. Guppies are not known to show any preference for or against the color green. For task 3, the maze apparatus in task two was turned upside down so that fish had to swim downward and then across through a hole at the bottom of the tank. These three tasks were designed to be of increasing difficulty.
Procedure
Subjects were separated into two populations of 16 fish, each with equal
numbers of males and females, and a range of different sizes. We weighed each
fish and noted its distinctive color markings so that it could be identified.
For 14 days food items (a mixture of live bloodworm, Chironomus spp.,
freezedried bloodworm, or standard tropical fish flaked food) were dropped
into the tanks in a manner designed to enhance scramble competition and to
maximize variation in foraging success. This involved dropping food items
individually, or in twos or threes, into the central region of the tank. When
the food had been consumed, further food items were added in the same manner.
Approximately 40 food items were given to each tank on each feed. During each
feeding session only one food type was presented in order to minimize the
opportunity for individuals to specialize on food types. We fed subjects in
this manner three times daily, at 0900, 1300, and 1700 h. On days 10-14,
subjects were fed exclusively on freeze-dried bloodworm because this food
consisted of small but distinct items, each of which could only be eaten by a
single fish. For this 5-day period, as a measure of competitive foraging
ability, we recorded which fish ate each food item. After feeding was complete
on the 14th day, we weighed all the fish again and recorded their change in
weight over the 2-week period.
On days 15-17, at 0900 h, we presented subjects in the two populations with three innovation tests, one a day, and recorded the latency to complete the task for each fish. The maze apparatus was introduced into the tanks at the beginning of each trial and removed immediately after it had been completed. If all fish had not completed the task after 20 min had elapsed the trial was terminated, and unsuccessful fish were allocated this time. We summed the innovation times across the three tasks to minimize any confounding effects generated by completion of a maze by chance or by following another fish. During this 3-day period, once a day, at 1700 h, subjects were given further food items in the same manner as described above.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The number of food items consumed during the 5-day monitoring period ranged from 7 to 87, this 12-fold difference demonstrating significant variation between individuals in foraging success. Similarly, weight change ranged from a loss of 0.04 g to a gain of 0.20 g. Foraging success correlated significantly with weight gain (r =.476, p =.005), indicating that success in scramble competition was indeed a major factor determining weight change. There was a significant correlation between initial mass and number of food items consumed (r =.486, p =.004) and between initial mass and weight change (r =.366, p =.039), indicating that larger fish outcompeted smaller fish in scramble competition. Females (
± SE = 40.25 ± 4.67) consumed more
food items than males ( ± SE = 26.56 ± 3.99; independent
t test: t30 = 2.23, p =.03), but the
difference in weight gain between females ( ± SE = 0.06 ±
0.02 g) and males ( ± SE = 0.03 ± 0.01 g) was not
significant (independent t test: t30 = 1.36,
p =.18, ns).
The time to complete each of the three innovation tasks was summed to give
an overall measure of innovative tendency (total latency to innovate). Across
all fish, the correlation between total latency to innovate and weight change
approached significance (r =.336, p =.06). Similarly, the
correlation between total latency to innovate and foraging success also
approached significance (r = 0.297, p = 0.09). However,
closer inspection reveals that these relationships across all fish result
principally from the males (Figure
1). Males showed a strongly significant correlation between total
latency to innovate and weight change (r =.692, p =.002) and
a weaker, but notable, relationship between total latency to innovate and
foraging success (r =.460, p =.06). Females, in contrast,
exhibited no significant relationship between total latency to innovate and
weight change (r =.098, p =.72, ns) and total latency to
innovate and foraging success (r =.203, p =.46, ns). Despite
this finding, the total latency to innovate for females ( = 1530 s) was
less than that for males ( = 1559 s), although not significantly so.
Males in population 1 showed a strongly significant correlation between total
latency to innovate and weight change (r =.74, p =.04), and
a similar strong correlation was found in population 2 (r =.63,
p =.09). In contrast, females in both population 1 (r =.06,
p =.88) and population 2 (r =.34, p =.41) did not
show a strong correlation between total latency to innovate and weight change.
Thus, the two populations, in separation, provide a replication of our main
finding.
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As guppies are shoaling fish, it is possible that some fish may have
followed others through the maze. If fish had followed each other at random,
following would not be able to account for the correlations between weight
change, foraging success, and total latency to innovate, described above.
However, if following was size assortative, or was significantly more frequent
in one sex, in theory it might be able to account for some of our findings.
Size-assortative shoaling has been reported in guppies
(Lachlan et al., 1998). We
investigated these possibilities by defining following as any instance when a
fish completed a maze 10 s or less after an earlier fish in the same tank. By
this criterion, there were 20 instances of following out of the 96 latency
times. We observed that, in general, the fish swam the maze alone, but
occasionally, a pair or three fish would enter the goal zone together. There
was no significant difference between the weight of followers (
± SE = 0.48 ± 0.05 g) and leaders ( ± SE = 0.48
± 0.05 g; independent t test: t38 = 0.11,
p =.92, ns), nor any significant correlation between them (r
=.11, p =.64). There was no evidence that one sex was more likely to
follow or be followed than the other. Thirteen of the 20 cases of following
were by males (
2 = 1.8, df = 1, p >.1, ns); 10 of
the 20 leaders were male. Seventeen out of 32 fish followed at some point; 17
out of 32 fish were leaders. Only 6 fish were both followers and leaders,
indicating that most followers were not leaders, and vice-versa. When cases of
following are removed, the relationship between weight change and total
latency to innovate remains strong in males (r =.58, p =.02)
and not females (r =.205, p =.45). Collectively, these
findings do not support the hypothesis that the pattern of results are an
artifact of following.
Thus males show a strong correlation between weight change and time to
innovate, with weight change accounting for nearly 50% of the variance in
innovation time. However, females show no equivalent relationship. A similar
pattern is found for foraging success, and the results are replicated in the
two populations. One interpretation of these findings is that males are indeed
driven to innovate by hunger stress, but will devote their energy to mating
when they are not subject to such stress. Observations from the laboratory,
where, on average, a male displays to females seven times in 5 min
(Farr and Herrnkind, 1974), and
from the wild, where females receive a sneaky mating attempt every minute
(Magurran and Seghers, 1994),
certainly suggest that, when able, males will prioritize mating. Consistent
with this reasoning is the observation that there is a much weaker correlation
between foraging success and weight gain in males (r =.27, p
=.31) than in females (r =.52, p =.04), perhaps suggesting
that males burn off energy derived from food in courtship, rather than
investing in growth. In contrast, females are constantly searching for new
food sources, irrespective of past foraging success. Among guppies, females
have indeterminate growth, and there is a strong link between energy intake,
growth and fecundity, whereas males essentially stop growing when they reach
sexual maturity (Constanz,
1989; Dussault and Kramer,
1981). It may be that female guppies are inherently more curious
and investigative about their surroundings than males because finding
high-quality food has a greater marginal fitness value for females than for
males. If this reasoning is correct, we predict similar results in other
species where maternal investment significantly exceeds paternal investment,
such as in most mammals. That is, in such species we predict (1) a stronger
relationship between competitive ability and foraging innovation in males than
in females and (2) greater levels of foraging innovation in females relative
to males.
The findings of this study have important implications for research into
animal social learning. Theoretical models have reached the conclusion that
seemingly broad environmental conditions favor vertically transmitted (i.e.,
transgenerational) cultural traditions
(Boyd and Richerson, 1985,
1988;
Feldman et al., 1996). This
finding was regarded by Boyd and Richerson
(1988) as
"troubling" when faced with the apparent rarity of such traditions
in animal populations. It is entirely possible that future research will find
that stable traditions are not quite as infrequent among animals as is
currently believed. However, until such evidence is available, it remains a
mystery why vertical cultural transmission is apparently rare among
animals.
Kummer and Goodall (1985)
found no shortage of innovation in primate populations, but these innovative
behaviors rarely spread. The findings of this study suggest that the dearth of
examples of stable traditions in animals may be a consequence of the
complexities of transmission dynamics in a social group, rather than a
reflection on the creativity or cognitive capabilities of animals. Various
authors have noted a tendency among fish for poor competitors to be on the
outskirts of the shoal or even to leave the shoal, being forced to shuttle
between patches (Krause, 1994;
Milinski, 1984). Primate
studies also appear to indicate that innovators are frequently on the
outskirts of the social group (Kummer and
Goodall, 1985; Sigg,
1980). On many occasions when ecological and technical innovations
occur in primate populations, the innovator is alone, or at least freed from
social distractions, and the innovating animal is rarely the dominant or
central individual in the population
(Fragaszy and Visalberghi,
1990; Kummer and Goodall,
1985). If the twin observations that it is poorer competitors that
innovate and that poorer competitors are on the outskirts of aggregations are
common to many species, much innovation will tend to be unobserved by other
animals, decreasing the chance of the novel behavior pattern spreading. This
may be one explanation for both the slow diffusion of new behaviors in the
wild (Kummer and Goodall,
1985) and the rarity of stable animal traditions
(Boyd and Richerson, 1988).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This work was supported by a Royal Society University Research Fellowship to Kevin Laland and a Biotechnology and Biological Sciences Research Council studentship to Simon Reader.
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