Behavioral Ecology Advance Access published online on August 27, 2008
Behavioral Ecology, doi:10.1093/beheco/arn104
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Receiver identity modifies begging intensity independent of need in banded mongoose (mungos mungo) pups
Department of Zoology, Large Animal Research Group, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
Address correspondence to M.B.V. Bell. E-mail: mbvb2{at}cam.ac.uk.
Received 5 March 2008; revised 2 July 2008; accepted 10 July 2008.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Begging displays have been interpreted as honest indicators of offspring need, with variation in begging intensity reflecting variation in offspring internal state. However, recent empirical evidence suggests that offspring frequently adjust their begging in relation to social context and tailor begging to specific individuals or payoff schedules. This suggests that begging intensity is subject to strategic variation not directly linked to current need. Here I investigate pup begging in banded mongooses (Mungos mungo), a communally breeding carnivore where most pup care occurs in exclusive pup–helper pairs (termed the "escort" system). Natural observations reveal that pups associating with a helper who is not their usual escort reduce their begging rate and receive less food for a given begging rate. Using experimental escort removals, I demonstrate that even when there is a measurable increase in short-term need, pups associating with a helper who is not their usual escort beg at a lower rate and receive less food for a given begging rate. This strongly suggests that they reduce their begging rate in response to the reduction in feeding rate by their temporary helpers. I argue that variations in begging intensity not only may reflect variation in internal state but also may frequently reflect variation in an offspring's motivation to beg based on context-dependent changes in the payoffs of begging.
Key words: banded mongoose, begging, cooperative care, honest signaling, Mungos mungo, parent–offspring conflict.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Begging displays are widely expected to be accurate indicators of offspring need, with "honesty" maintained by the cost of begging (Godfray 1991
; Parker et al. 2002). Despite some uncertainty regarding the cost of begging (reviewed in Moreno-Rueda 2007), there is now abundant evidence that changes in begging intensity reliably indicate changes in internal state (Kilner and Johnstone 1997; Budden and Wright 2001; Wright and Leonard 2002). However, there is also increasing evidence that offspring frequently adjust their begging intensity in relation to external factors, independent of internal state, so that begging intensity may not always be a strict reflection of current need.
Intrabrood dynamics, for example, clearly have a strong influence on begging intensity, and offspring frequently adjust their begging effort in response to changes in begging by rivals or companions. In some species, offspring escalate their begging in response to increases by rivals (Smith and Montgomerie 1991; Price et al. 1996; Leonard et al. 2000; Krebs 2001; Neuenschwander et al. 2003), whereas in other species, offspring compensate for changes in a group signal and reduce their begging in response to an increase by companions (Roulin et al. 2000; Smiseth and Moore 2002; Bell 2007b). Moreover, relative rank within a brood often influences begging effort, and studies of species with pronounced brood hierarchies have demonstrated that senior offspring beg at lower intensities, yet receive more food, than their nest mates, even when short-term need is similar (Kilner 1995; Price et al. 1996; Lotem 1998; Cotton et al. 1999; Smiseth and Moore 2007). This is probably because senior offspring dominate access to food when parents approach, so they effectively exploit the begging effort of subordinates (Parker et al. 1989; Kilner 2003), though learning effects may also be important (Kedar et al. 2000; Grodzinski et al. 2008). To some extent, these dynamics have already been explored by and incorporated into evolutionarily stable strategy models of parent–offspring communication (e.g., Godfray 1995; Rodriguez-Girones et al. 2001; Johnstone 2004).
Even where companions or rivals have limited influence, differences in the way carers respond to begging are likely to exert considerable pressure on offspring to adjust their begging effort. Carers often have different decision rules when responding to changes in begging (Christe et al. 1996; Krebs 2001; Kilner 2002; Quillfeldt et al. 2004; Smiseth and Moore 2004), which may select offspring to beg in different ways to different carers (Stamps et al. 1989; Kolliker et al. 1998; Krebs and Magrath 2000; Kolliker and Richner 2004; Lotem and Winkler 2004; Roulin and Bersier 2007). This will be especially important where begging is costly because selection should act on offspring to maximize the return on their investment in begging, which means we might expect offspring to beg at higher intensities to more responsive carers (Kolliker et al. 2005; Bell 2008). A strong indication that begging intensity may be adjusted to match carer responsiveness comes from the increasing evidence for heritable variation in offspring begging, which often correlates with heritable variation in parental provisioning (reviewed in Kolliker et al. 2005).
To date, however, the effect of variation in carer responsiveness on begging has generally focussed on nest-bound chicks in biparental systems. Nestlings are restricted in their choice of carers, are exposed to direct competition with nest mates over the allocation of food, and have extremely limited scope for movement in response to changes in profitability. In contrast, offspring in cooperative species are exposed to a greater number of potential carers, among which there may be considerable variation in motivation or ability to feed (Cockburn 1998; Heinsohn and Legge 1999; Cant and Field 2001; Clutton-Brock 2002; Griffin and West 2003). Moreover, once offspring become mobile, they are able to approach specific individuals and interact with them while they forage, as opposed to waiting passively for them to return to a nest. This may have important consequences for begging behavior because it allows offspring to assess the profitability of begging to different individuals and choose which to accompany (treating different helpers as different foraging "patches": Slagsvold 1997; Kolliker et al. 1998; Budden and Wright 2001, 2005; Hodge et al. 2007).
Banded mongooses (Mungos mungo) are an ideal system in which to investigate the effect of carer identity on pup-begging effort because packs contain a large number of potential helpers (median = 24 adults, range 5–40); yet, each pup forms an exclusive association with a single adult (termed it is "escort," Cant 1998), with whom it spends >70% of its time, and from whom it receives the vast majority of its food (median = 100%; Gilchrist 2004; Hodge 2005; Bell 2007b). However, pups are occasionally separated from their escorts and may approach other helpers before returning to their escorts. Separations usually only last a few minutes, but half of all observed pups form temporary associations lasting a whole day with helpers who are not their usual escorts which last for a whole day (Bell 2007b).
Here I investigate whether escorts and "temporary" helpers respond in different ways to begging and whether pups react by adjusting their begging effort. I use both natural observations and temporary escort removal experiments to determine if helpers who are not usual escorts show any difference in provisioning and ask whether pup begging changes as a result. I expected helpers who were not regular escorts to be less responsive to begging, whereas I expected pups to react to this by reducing their begging effort. I based this expectation on the fact that begging appears to be costly in banded mongooses (when pups were induced to beg at a higher rate while provisioning rate remained the same, they gained weight at a lower rate: Bell 2007b). Previous work also suggests that banded mongoose pups are sensitive to variation in the payoffs of begging and act to maximize their return on an investment in begging (changes in begging intensity after deprivation were adjusted to exploit variation in the way escorts responded to changes in begging: Bell 2008). Temporary associations with other helpers therefore provide an opportunity to investigate whether a change in social context influences begging behavior independent of a change in state.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Study site and data collection
Between May 2003 and August 2005, I observed 565 banded mongooses and monitored 68 breeding attempts from 13 packs in Queen Elizabeth National Park, Uganda (0°12'S, 27°54'E) (for habitat and climate details, see Cant 2000
). All individuals were habituated to close (<5 m) observation on foot, and accurate ages (±2 days) were known for most of the population (92%). Individuals aged 0–3 months were classified as "pups," and >3 months as "helpers" (animals as young as 3 months have been observed provisioning pups, Bell MBV, personal observation).
All animals were tattooed for permanent identification, whereas for field identification, fully grown animals were fitted with color-coded plastic collars (weight 1.5 g, regularly checked to ensure a loose fit) (for trapping and marking procedure, see Cant 2000). Growing animals and some well-habituated animals were given unique haircuts. To monitor condition, animals were trained to step on an electronic laboratory scale (accuracy ± 1.5 g) before foraging in the morning (ca., 0730 h), and condition was calculated as the residual from a linear regression of mass (grams) over age (days). Animals were weighed again after foraging in the evening (ca., 1830 h) and hourly weight change calculated as the change in weight (grams) divided by time between weighing sessions (hours).
Behavioral observations were carried out by the author and a field assistant, using handheld PSION II data loggers (model LZ-64), running purpose-written programs where each individual in a pack and each target behavior were preallocated to a key combination, allowing observers to record rapid behavioral data without a break in observation. When experimentally removing an animal, we distracted the target animal with droplets of milk dispensed from a hamster water bottle, then grasped it by the scruff of the neck, and put it into a covered box trap (Tomahawk Live Trap Co., Tomahawk, WI). In a few cases, target animals were too nervous to catch by hand, so we baited the trap and used a string release for the door.
This research was carried out under license from Uganda National Council for Science and Technology and all procedures approved by Uganda Wildlife Authority.
Study animal
Banded mongooses live in large family groups (average number of adults = 29, range 5–40) and are one of the few cooperative species where subordinates regularly breed (median number of breeding females = 4, range 1–12). Females give birth in synchrony, producing large communal litters (median communal litter size = 5, range 1–23) which remain in dens for 3–4 weeks. When pups emerge from the den, they spend 3–5 days approaching different helpers, after which individual pups form stable associations with a single adult helper (their escort) and remain associated with that animal until independence (ca., 9–13 weeks) (Cant 1998; Gilchrist 2004). Adults who do not become escorts thereafter provide very little pup care during that breeding attempt (Gilchrist 2004; Bell 2007b). Escorts are generally young, nonbreeding males (1–3 years old) or breeding females who contributed to the current litter (Gilchrist 2004; Hodge 2005). Associations are initiated and maintained by the pups, with escorts following a relatively passive "feed the nearest begging pup" rule (Gilchrist 2004; Hodge 2005), and escorts do not preferentially associate with close relatives (Hodge SJ, unpublished data). During a foraging session, pups follow escorts closely (usually within 10 cm), begging constantly with a high-pitched, bird-like chirp (average call rate = 34.4 calls per min ± 0.73 standard error [SE], maximum = 80; calculated from data on 63 pups—see below).
The pup–escort relationship, pup begging, and escort feeding
To quantify associations between pups and helpers, we carried out 2 h of scan observations each day once new litters started foraging. Every 5 min, for each pup, we recorded distance to (±10 cm) and identity of the nearest helper. At the end of each session, we classified a helper as an escort if the same pup was within 2 m for 
40% of scans. We defined a helper as a pup's "usual" escort after recording the same pup–helper pair on at least 5 consecutive observation sessions (average time between the first and last of the consecutive observation sessions = 5 days, range 3–17). Later analysis showed that pups spent a median of 94% of observed time with their usual escort but that approximately 50% of pups spent at least 1 day in association with a different helper (Bell 2007b). These switches never lasted longer than a day, and no pup was observed to spend more than 30% of observation sessions in association with a helper who was not their usual escort (Bell 2007b).
When pup habituation allowed, we conducted focal watches on pups, following each pup for 20 min, counting begging calls using a handheld clicker and recording ad libitum food items provided by helpers and found by pups themselves. At the end of every minute, we recorded the number of begging calls during that minute and the identity of every helper who was within 2 m of the pup for 20 s. For each focal watch, we calculated average pup-begging rate, helper provisioning rate, and pup self-feeding rate per minute observed. Analysis was restricted to pups observed for 3 observation sessions to give a total of 549 focal watches on 31 female and 32 male pups from 16 litters in 5 packs, with an average litter size of 4.8 (range 1–17) and ranging in age from 28 to 81 days. All focal watches were carried out within 1 h of emergence from the den in the morning, minimizing the effects of provisioning through the morning, and standardizing as far as possible the state of all pups observed. Some focal watches were excluded in some analyses because data were missing for certain variables (due to rain, equipment failure, or hostile megafauna).
The effect of separation from escorts
To investigate the effect of separation from escorts on begging rate, I analyzed a subsample of 279 focal watches on 63 pups from the period of peak begging (35–55 days), when there is no significant change in begging with age (linear regression F1,278 = 0.01, r2 < 0.0001, not significant). For each focal watch, I calculated average begging rate per minute in the absence of any helpers (>2 m from any helper); in the presence of the escort only; and in the presence of the escort and other helpers. I then used this to calculate grand averages for each pup (so for each pup, I had average begging rate across all focal watches when >2 m from any helper; when in the presence of the escort only; and when in the presence of the escort and a variable number of other helpers). I then constructed a linear mixed model (LMM) with average begging rate per minute as the response variable. I fitted number of helpers within 2 m as a factorial fixed effect, and as random factors, I fitted individual identity (estimated variance component = 87.2, SE = 22.1) and litter identity (estimated variance component = 18.5, SE = 21.4). I performed the same analysis using average number of food items per minute found by the focal pup itself (square root transformed), with the same random factors (individual identity: estimated variance component = 0.004, SE = 0.0026; litter identity: estimated variance component = 0.00057, SE = 0.0012).
Temporary changes in helper association
To investigate the effect of temporary association with a different helper on the profitability of begging, I identified 33 pups (17 females, 16 males) from 14 litters that spent at least one day associated with a helper who was not their usual escort. I only included cases where pups were within 2 m of the same adult for 40% of observation time (i.e., the temporary helpers met the same criteria as regular escorts during those observation sessions). Cases where pups did not consistently associate with the same adult throughout an observation session were excluded. Using all focal watches for these pups (n = 210), I constructed a LMM with items fed to the focal pup per minute of observation time spent within 2 m of the helper (square root transformed) as the response variable. As random factors, I fitted pup identity (estimated variance component = 0.00059 ± 0.00040 SE) and litter identity (estimated variance component = 0.00201 ± 0.00101 SE). As fixed effects, I fitted pup-begging rate (calls per minute of observation time spent within 2 m of the helper) and a 2-level factor denoting the type of association (with the focal pup's usual escort or with the temporary helper). For the full list of explanatory variables tested, see Table 1. I chose these initial variables because previous analysis suggested that they might influence the dynamics of the pup–escort relationship (Gilchrist 2004; Hodge 2005; Bell 2007b, 2008).
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For these same pups, I compared pup self-feed rate (food items found per minute) when in association (within 2 m) of their escort or temporary helper and when alone (> 2 m from any helper) and hourly weight gain (grams per hour) for either the day before or the day after the temporary switch (chosen randomly) with the same measurements for the day that they spent with the temporary helper. I averaged measurements for pups who switched more than once (n = 16 pups, average number of days spent with a different helper = 2 ± 0.01 SE). Any differences are unlikely to be effects of rainfall (Wilcoxon, n = 33, W = 233, P > 0.5) or temperature (Wilcoxon, n = 33, W = 136, P = 0.21).
Experimental escort removal
To investigate the effect of experimentally induced association with a different helper on pup begging, I conducted a series of escort removal experiments. On control mornings, we carried out focal watches on 23 pups when the pack started foraging (ca., 0745 h). The following morning, we removed their escorts as they emerged from the den (c. 0730 h). After removal, we waited for at least 10 min to ensure packs were foraging normally (average time from removal to focal start = 13 min, range 10–28 min) ans then carried out focal watches on the pups whose escorts had been removed. To minimize any effects of pup age on behavior after escort removal, we carried out removals within 20–25 days after pups first emerged (average age = 48 days, range 44–53). Subsequent analysis confirmed that there was no significant effect of pup age on proportion of time spent alone after escort removal (linear regression, F1,21 = 0.07, P = 0.8).
I constructed a LMM with items fed to the focal pup per minute of observation time spent within 2 m of the temporary helper (square root transformed) as the response variable. I fitted pup identity as a random factor (estimated variance component = 0.00217 ± 0.00367 SE). As fixed effects, I fitted pup-begging rate (calls per minute of observation time spent within 2 m of the helper) and a 2-level factor denoting the treatment (control: with usual escort; experimental: usual escort removed and pup in association with the temporary helper).
Statistical analysis
I carried out simple parametric tests in Minitab (all tests 2 tailed) and constructed linear models using Genstat 8.1 (Lawes Agricultural Trust, Rothamsted, Harpenden, UK). Where analysis involved repeated sampling of the same individual or from within the same litter, I used LMMs. These are similar to general linear models but allow both fixed and random terms to be included. Random terms allow the analysis to take account of repeated measures (Schall 1991) and were included for each level of repeated measurement. In these cases, the variance components were estimated using the restricted maximum likelihood method, and random terms were retained in the model unless the variance component was found to be unmeasurable (<10–5). I sequentially dropped all potential explanatory terms until only terms whose elimination would have significantly reduced the explanatory power of the model remained. The significance of a term was derived by dropping it from the final model (if it was part of the final model) or adding it to the final model and then dropping it (if it was not part of the final model) (after Crawley 2002). I tested all 2-way interactions but only present those explaining significant variation. I present the effect sizes of all significant terms—these are parameter estimates from the models and can be interpreted as the change in y per unit change in x. For categorical variables, such as sex, one level of the factor is set at 0 and the effect is relative to that factor level.
Ethical note
Escort removals took 5–10 min, and packs were not usually disturbed because adults seldom gave distress calls when trapped. We kept removed animals in their traps, which were large enough to allow free movement (trap dimensions = 66 x 23 x 23 cm; average banded mongoose body length = 52 cm). We covered the traps with a blanket and stored them on the floor of a shed with access to water, but no food (I carried out subsequent observations investigating the effect of temporary deprivation on provisioning). Removed escorts spent an average of 10.5 h out of the group (±0.1 SE) and were released in the late evening after the pack had finished foraging (ca., 1830). Escorts were accepted back with minimal aggression (usually subjected to anal marking by dominant animals) and pup–escort associations never broke down as a result of experimental manipulation (Bell MBV, unpublished data).
Adults of this age are frequently separated from their packs for up to 11 h—they remain behind in the den as babysitters (Cant 2003). This means that the period of deprivation experienced by these animals was well within the natural range. However, removing animals and keeping them in traps is likely to be considerably more stressful. To minimize this stress, we 1) captured animals in pairs because a companion seemed to reduce distress; 2) placed traps in a cool, darkened shed, covered by a blanket, because darkness calmed the animals, and they usually spent most of the removal period asleep; 3) provided an ad-lib source of water from a hamster water bottle; 4) checked animals at least once an hour to monitor for signs of distress or injury; and 5) ensured that the shed in which they were stored was left undisturbed and was secure from ants, predators, and toxins.
Animals lost an average of 48.4 g (±4.01 SE) during removal (an average of –3.4 ± 0.22% SE of body weight). This is in comparison to an average gain of 49.4 g (±5.4 SE) across a similar time period on unmanipulated days (an average of +3.5 ± 0.4% SE of body weight). Removal had no discernible effect on behavior after release—animals showed no increase in wariness toward observers and allowed themselves to handle and weigh as before removal. In many cases, animals would voluntarily reenter a trap within minutes of release, indicating that they had not formed a negative association with the trap.
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RESULTS |
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Separation from escorts
Pups begged at very low rates when >2 m away from their escorts but found food for themselves at significantly higher rates (LMM
2 = 8.76, P < 0.001). They started begging at a significantly higher rate as soon as they started to associate with their escorts (LMM 2 = 253.26, P < 0.0001) but found food for themselves at significantly lower rates. The presence of any additional helpers after that had no significant effect on begging or self-feeding, until there were more than 5 helpers present, when there was a small reduction in begging. This reduction may be because such dense concentrations of animals usually only occurred at very rich point sources of food (such as large dung piles) or when the pack had been disturbed in some way and was about to start moving. However, it is also possible that focal pups were responding to the presence of pups associated with other adults because previous work revealed that pup begging is influenced by the begging of companions (Bell 2007b).
Temporary changes in helper association
On days when pups temporarily switched their associations, they spent significantly more time entirely on their own (>2 m from any helper) (Wilcoxon, n = 33, W = 407.0, P = 0.008). When not on their own and associating with the helper who was not their usual escort, they begged at a significantly lower rate than when they had been associating with their usual escorts (paired t-test, n = 31, t = –2.16, P = 0.039; Figure 1a). These temporary helpers provisioned them at a significantly lower rate than their usual escorts (paired t-test, n = 33, t = –3.18, P = 0.003; Figure 1b). The reduction in begging was probably because the profitability of begging to a different helper was reduced: when statistically controlling for begging rate, helpers who were not a pup's usual escort provisioned at significantly lower rates (LMM 2 = 6.10, P = 0.013; Table 1). Pups appeared to be able to compensate for the shortfall in provisioning by finding significantly more food for themselves during the periods they spent on their own (paired t-test, n = 33, t = 2.52, P = 0.017; Figure 1c), and they gained weight at a similar rate to days when they associated with their usual escorts (paired t-test, n = 18, t = 0.63, P = 0.54; Figure 1d), suggesting that there was no change in short-term need.
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It is possible that while in association with temporary helpers, pups reduced their begging rate because they invested more effort in foraging for themselves (a trade-off seen in meerkats; Kunc et al. 2007
; Thornton 2008). However, comparing self-feed rates while in association with (within 2 m of) usual escorts or temporary helpers revealed no significant differences (paired t-test, n = 33, t = 0.36, P = 0.72).
Temporary escort removal experiment
When their escorts were experimentally removed, pups spent significantly more time entirely on their own (Wilcoxon, n = 22, W = 231, P < 0.0001). When not on their own, they spent brief periods associated with a temporary helper, during which they begged at a significantly lower rate than when they had been associating with their usual escorts. They reduced their begging even further when on their own (>2 m from a helper) (Figure 2; repeated measures analysis of variance, F2,42 = 72.94, P < 0.001; Tukey's post hoc tests: with escort vs. with other helper: q = –11.69, P < 0.001; with other helper vs. alone: q = –4.61, P = 0.006).
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Although their usual escorts were removed and the experimental pups were associating with the temporary helper, pups were provisioned at a significantly lower rate than when they had been with their usual escorts (paired t-test, n = 21, t = –6.39, P < 0.00001; Figure 3a). The reduction in begging was probably because the profitability of begging to a different helper was reduced: for a given begging rate, temporary helpers provided less food than usual escorts (LMM
2 = 26.31, P < 0.001; Table 2, Figure 4). They were able partially to compensate for this shortfall by finding significantly more food for themselves when foraging on their own (>2 m from any helper) (paired t-test, n = 21, t = 3.99, P = 0.001; Figure 3b). However, they were unable to completely compensate, and across the whole experimental day, they gained weight at a significantly lower rate than when their escorts were present (paired t-test, n = 23, t = –2.46, P = 0.022; Figure 3c), suggesting that there was an increase in short-term need.
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As with natural shifts, there was no evidence that the reduction in begging rate while associating with a temporary helper was the result of an increase in foraging effort: comparing self-feed rates while in association with (within 2 m of) usual escorts or temporary helpers revealed no significant differences (paired t-test, n = 21, t = 0.28, P = 0.78).
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DISCUSSION |
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This study indicates that banded mongoose pups adjust their begging effort independent of changes in short-term need: they drastically reduce their begging rate when separated from their escorts by more than 2 m, and they are sensitive to carer identity, reducing their begging rate when associating with helpers who are less responsive to their begging. Reduced begging occurs despite no evidence for a reduction in short-term need—in fact, during the experimental escort removal, there is evidence for an "increase" in short-term need. In contrast, previous work on banded mongooses demonstrated that in the presence of their usual escorts, pups who had been experimentally deprived significantly increased their begging rate (Bell 2008
). Whereas Bell (2008) indicated that changes in begging intensity after deprivation were adjusted to exploit variation in the way escorts responded to changes in begging, the current study indicates that changes in begging intensity need not indicate changes in state at all, but instead may reflect changes in the benefit of begging generated by changes in social context.
Where offspring are exposed to multiple potential carers and where these carers vary in their contributions to care, offspring may be selected to identify traits that correlate with generosity when making decisions about which carer to approach and how much to invest in begging (similar to females identifying traits that correlate with genetic quality or paternal investment in males when making mating decisions). These decisions may be based on experience during previous interactions or on cues provided by the carers. At a simple level, different sex or age categories frequently differ in their contributions to care (Cockburn 1998; Heinsohn and Legge 1999; Cant and Field 2001; Clutton-Brock 2002; Griffin and West 2003), so any cues (such as plumage dimorphism) that reveal this information are likely to be exploited by offspring. On a more subtle level, many conspicuous behavioral and morphological cues often correlate with measures of individual "quality" (Andersson and Simmons 2006), which in turn may well correlate with ability or motivation to care for offspring. Even short-term changes in carer condition may generate cues that provide information to offspring. For example, variation in carotenoid-based pigmentation frequently correlates with both medium (e.g., Hill and Montgomerie 1994) and short-term nutritional condition (Velando et al. 2006) and has also been shown to provide information about levels of parental investment (e.g., Hill 1991; Velando et al. 2005).
If offspring exploit cues that provide information about carer responsiveness, this could generate selection on carers to broadcast signals that inform offspring about the profitability of begging, as has been suggested for yolk androgens (Muller et al. 2007). This in turn may exert selection on carers to exaggerate features that induce offspring to beg at higher rates, thereby manipulating them to reveal more accurate information about true need. Ultimately, this may lead to an arms race similar to that seen with sexual signals, and it is intriguing to speculate that it may partly explain species with equally brilliant plumage in both sexes (e.g., rollers). To my knowledge, no experiments have investigated the effect of manipulating the features of carers on offspring begging.
In banded mongooses, it is not clear how pups obtain information about differences in carer responsiveness. The obvious alternatives are that 1) pups initially beg as intensely to temporary helpers as to escorts and then over time reduce their begging because the payoffs are smaller, 2) pups are already aware that helpers other than their escorts are not as responsive, based on previous interactions, or 3) pups use cues generated by the temporary helpers to estimate their likely responsiveness (an obvious candidate being the contact calls given while foraging, which are individually distinct, Muller and Manser 2008). It is, however, impossible to test these with current data.
Where the payoffs of begging vary and where offspring have the opportunity to forage for themselves, they are likely to adjust both begging effort and the relative effort they invest in self-feeding over begging (Smiseth and Moore 2002). The results presented here suggest that banded mongoose pups attempt to compensate for reductions in the profitability of begging by increasing the amount of time they spend foraging for themselves: when pups voluntarily associated with temporary helpers, who provided less food than their usual escorts, they spent more time foraging on their own, found more food for themselves while on their own, and gained weight at the same rate as when associating with their usual escorts. This raises the question as to why pups associate with an escort at all, rather than always foraging for themselves. It may be that there are longer term costs to self-foraging for extended periods, including metabolic costs (Thornton 2008) and increases in predation risk (Bell 2007a). It is also likely that self-feeding is not always as effective as begging for food, something indicated by the experimental escort removal, where pups were unable to compensate fully for reduced provisioning and gained weight at lower rates.
A final question raised by this study is why banded mongoose pups occasionally associate with helpers who are not their usual escorts if these animals are so much less responsive to begging. One possibility is that pups are prospecting for better feeders in response to temporary reductions in provisioning by usual escorts due, for instance, to reduced condition or lower foraging success. Alternatively, they may be monitoring variation in helper generosity, similar to the way that foraging bumblebees specialize on the most productive flower species, but periodically test other species to track changing rewards over time (a behavior termed "minoring," Heinrich 1979; Goulson 1999). This would allow pups to make informed decisions about which helpers to approach should their escorts become less responsive or even be depredated.
In general, it seems likely that selection will act on offspring to extract information from carers about changes in the costs and benefits of begging and to rapidly alter their begging effort in response to such changes. There are 2, overlapping, contexts where this is especially likely: 1) where offspring are exposed to multiple potential carers and 2) where ecological conditions change over the short term. Although considerably more work is required to fully understand these dynamics, the parallels between offspring begging and adult foraging behavior are clear (Slagsvold 1997; Kolliker et al. 1998; Budden and Wright 2001, 2005). Future experiments manipulating the generosity of individual carers to determine the effect on begging, particularly in species with mobile and partially self-feeding offspring, will provide valuable insights into the flexibility of begging strategies.
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FUNDING |
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Natural Environment Research Council studentship (NER/S/A/2002/10344).
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ACKNOWLEDGEMENTS |
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Francis Mwanguhya helped collect data and carry out experiments. Corsin Muller provided invaluable advice in the field. The Uganda National Council for Science and Technology and the Uganda Wildlife Authority provided permission to carry out research in Queen Elizabeth National Park, Uganda, as part of a long-term study supported by Mike Cant, Tim Clutton-Brock, and Marta Manser. I am grateful to Andy Radford, Rebecca Kilner, Rufus Johnstone, Tim Clutton-Brock, Joah Madden, and 3 anonymous reviewers for valuable comments.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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