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Keywords:

  •  behavioural plasticity;
  • cross-fostering experiment;
  • foraging efficiency;
  • parental age;
  • timing of breeding

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    An increase in average breeding performance with age and experience among younger age classes has been recorded in numerous studies of iteroparous breeders. An important component of this pattern is thought to be improvements in foraging performance, resulting in delivery of more or better quality food to offspring by older, more experienced individuals.
  • 2
    Young, inexperienced breeders may exhibit lower foraging efficiency or foraging effort, and it has been predicted that differences in foraging performance with age and experience will be more marked when environmental conditions are poor. However, as the timing of breeding generally differs with age and experience, intrinsic differences in foraging abilities are typically confounded by variation in extrinsic conditions, and hence food availability.
  • 3
    To disentangle these effects, we experimentally manipulated the timing of breeding in European shags, Phalacrocorax aristotelis Linnaeus. We used a cross-fostering protocol, such that naive, young birds reared their chicks at the same time as older, experienced individuals. Our design produced simultaneous chick rearing during two periods in the same breeding season that differed markedly in environmental conditions: early, when conditions were good; and late, when conditions were poorer. We examined foraging efficiency, foraging effort and amount of food delivered to offspring by the two classes of breeder. We predicted that any differences in foraging performance would be more marked under the poorer conditions later in the season.
  • 4
    We found that experienced parents delivered more food than naive parents, irrespective of the time of season. This was due partly to the consistently higher foraging efficiency of the experienced parents. In addition, experienced parents adjusted their foraging effort to the environmental conditions. Early in the breeding season, they made less foraging effort than naive parents. Under the poorer foraging conditions, experienced parents increased their foraging effort but naive parents did not, being either unable or unwilling to do so.
  • 5
    Our results suggest that an increase in foraging efficiency, and the capacity to adjust foraging effort in response to food availability, are important components of the observed improvements in breeding performance with age and experience.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

An improvement in the average breeding performance of younger age classes is a widespread phenomenon among iteroparous breeders (Clutton-Brock 1988; Newton 1989). Such age-related changes are generally closely coupled to acquisition of experience in a variety of different spheres (Pärt 1995). Much of the observed improvement in breeding success is likely to be mediated through changes in foraging ability, which will affect the capacity to provide for offspring successfully, and may also affect the scheduling of breeding events (Stearns 1992).

Foraging performance can be considered in terms of the rate of energy gain (foraging efficiency) and the total time spent foraging (foraging effort); together these give a measure of the amount of food gained. An improvement in foraging efficiency with age has been reported in several avian studies (Jansen 1990; Desrochers 1992; Galbraith et al. 1999). Foraging effort in relation to age has also been investigated in birds, although no clear patterns have emerged (Pugesek 1981; Reid 1988; Galbraith et al. 1999). Furthermore, several authors (e.g. Sydeman et al. 1991) have predicted an interaction between age or experience and extrinsic conditions on foraging performance, with differences more apparent when feeding conditions are poor. However, it is generally also the case that younger, less experienced individuals breed later in the season, on average (Perdeck & Cavé 1992). Thus simple comparisons between breeder categories are usually confounded by differences in extrinsic conditions, as food availability is generally lower later in the season. To overcome this problem, we examined the foraging performance of young, naive and older, experienced European shags (Phalacrocorax aristotelis Linnaeus) that had been manipulated experimentally so that they were rearing offspring at the same time, during both the early and later parts of the same breeding season. Our protocol enabled us to examine the effect of experience, and of the interaction between experience and environmental conditions, on foraging performance. Foraging performance in the European shag has been shown to determine timing of breeding (Daunt et al. 2006), and young, naive breeders lay significantly later in the season than older, experienced breeders (Potts, Coulson & Deans 1980; Aebischer 1993). When experimentally manipulated to breed concurrently, experienced pairs have a consistently higher breeding success than naive pairs (Daunt et al. 1999, 2001). Here we examine whether these differences in breeding success are mediated through the foraging performance (foraging effort, foraging efficiency and amount of food delivered) of birds subjected to these experimental manipulations.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

experimental protocol

The study was carried out in 1998 on the Isle of May, south-east Scotland (56°11′ N, 02°33′ W). Age and experience are tightly coupled in European shags. Changes in breeding performance in relation to age are manifest largely in differences between pairs containing a 2-year-old male breeding for the first time, and pairs containing a male older than 2 with at least 1 year's breeding experience (Potts et al. 1980; Aebischer 1993). Foraging performance was measured in males from these two experience classes (hereafter ‘naive’ and ‘experienced’). The age of 2-year-olds was known because they had been ringed as chicks and/or from their distinctive plumage characteristics (Potts 1971), and all were breeding for the first time (European shags never attempt to breed at 1 year). For the experienced group, individuals had been ringed either as chicks, in which case their exact age was known, or as breeding adults, thus their minimum age was known; all had at least 1 year's previous breeding experience. Although no independent effect of female age has been recorded in European shags, female and male age are highly correlated within pairs (rs = 0·56, P < 0·001; Daunt et al. 1999).

Naive pairs laid 12 days later than experienced pairs on average (experienced, 6 May ± 7 days, n = 38; naive, 18 May ± 6 days, n = 38; t74 = 7·54, P < 0·001). We manipulated the timing of hatching using a cross-fostering protocol (for full details see Daunt et al. 1999). A four-way swap was carried out, comprising two experienced and two naive pairs matched for clutch size and, within each experience class, for laying date (n = 17 swaps with a clutch size of three; n = 2 swaps with a clutch size of two). No pairs reared their own young, with control pairs receiving a clutch from the same experience class, and experimental pairs receiving a clutch from the other experience class. As a consequence, experimental naive and control experienced pairs hatched chicks (from eggs laid by experienced pairs) early in the season, while experimental experienced and control naive pairs hatched chicks (from eggs laid by naive pairs) late in the season.

Indirect evidence from the behaviour of European shags indicated that environmental conditions differed markedly early and late in the season, enabling us to examine whether the effect of experience on foraging performance varied with conditions. In the Isle of May breeding population as a whole (consisting of 621 pairs), some broods were left unattended by adults late in the season, an unusual event indicating that both parents had to forage simultaneously to obtain sufficient food for their offspring (28% of nests not part of the experiment left broods unattended late in the season; no records early in the season; n = 43).

Of the 76 nests in the experiment, foraging performance of 18 experienced males (10 early in the season, eight late) and 20 naive males (10 early in the season, 10 late) was recorded during the guard phase, approximately mid-way through chick rearing, using VHF telemetry. By alternating between the experience classes on a daily basis, the date that radio tracking took place did not differ between the experience classes (experienced early: 30 June ± 3 days; experienced late: 15 July ± 4; naive early, 30 June ± 3; naive late, 17 July ± 3; general linear model (GLM): experience, F1,35 = 0·21, P = 0·65; time of season, F1,36 = 30·56, P < 0·001; interaction term, F1,34 = 0·06, P = 0·81). Brood age at radio tracking (range 14–31 days) did not differ with parental experience, but was older late in the season because the spread of laying dates was narrower than that of radio tracking dates (GLM: experience, F1,35 = 0·63, P = 0·43; time of season, F1,36= 23·70, P < 0·001; interaction term, F1,34 = 0·59, P = 0·45). The two experience classes were matched for brood size, which declined late in the season (Generalized Linear Model (GLM) with binomial errors and a logit link function: experience, χ2 = 0·45, P = 0·50; time of season, χ2 = 3·96, P < 0·05; interaction term, χ2 = 0·03, P = 0·86). The combination of an increase in brood age and decline in brood size with time of season resulted in no difference in brood biomass, a determinant of foraging effort and food load in shags (Wanless, Harris & Russell 1993b; GLM: experience, F1,36 = 1·96, ns; time of season, F1,35= 1·43, ns; interaction term, F1,34 = 0·03, ns).

Males were caught and a VHF radio transmitter (Biotrack Ltd, Wareham, UK; mass 20 g, ≈1·5% of body mass) was attached to two central tail feathers with Tesa tape. Each bird was weighed and wing length (maximum flattened chord), tarsus length, and head and bill length were measured. We recorded no adverse effects resulting from handling. Tag attachment took place at dusk each day, and the first trip after dawn was tracked. We targeted the first foraging trip since it followed a long fast (European shags on the Isle of May do not feed at night during the breeding season) and is therefore likely to be more revealing of foraging performance, as both naive and experienced adults, and their brood, will have fasted for a similar period. Birds were radio tracked from a station at 73 m a.s.l., using a system consisting of two parallel eight-element Yagi aerials joined by a 2-m crosspiece, attached to a 5-m mast that allowed the aerials to rotate through 360°. The aerials were connected to an ATS R4000 scanning receiver, operating in the 173 MHz band. A typical foraging trip consisted of a flight out to the feeding site, a series of dives with periods between dives on the sea surface, and a return flight to the colony. From the strength and consistency of the signal, it is possible to determine a precise time–activity budget, namely whether the bird is flying (strong, continuous signal), swimming on the sea surface (unsteady, continuous signal), or diving (signal disappears; Wanless, Harris & Morris 1991; Wanless et al. 1993a). An estimate of foraging location is obtained from dead-reckoning, using the bird's bearing and flight duration (Wanless et al. 1991). Birds at this colony typically favour three main foraging areas, two areas inshore of the island along the mainland coast north and west to north-west, respectively, and close to the island in any direction (Wanless et al. 1991).

Where possible, birds were caught immediately on their return after the foraging trip (experienced early, n = 7; experienced late, n = 6; naive early, n = 6; naive late, n = 4) and the stomach contents obtained by flushing the stomach with water (under licence; for full details see Wanless et al. 1993b). No birds showed any adverse effects from this procedure.

foraging effort

We quantified foraging effort for each foraging trip as the duration of the three principal activities: flight, swimming on the sea surface, and diving.

amount and type of food per foraging trip

The food load obtained was drained and the wet mass taken. Each prey item was identified, and its length measured. We recorded lesser sandeels (Ammodytes marinus), butterfish (Pholis gunnellus), dragonet (Callionymus lyra), unidentified wrasse (Labridae sp.) and unidentified crustacea. Mass of each species was derived from available length/mass equations (Harris & Hislop 1978; D.A.D. Grant, unpublished data), and for 20 out of 23 food samples we could record prey species biomass proportions. Given the small number of species and the dominance of lesser sandeels in the diet, we carried out a single analysis on the proportion of the diet consisting of this species.

foraging efficiency

Foraging efficiency was calculated as the ratio of energy gained (in kJ) to energy expended (in kJ) multiplied by the assimilation efficiency (77%; Grémillet, Schmid & Culik 1995).

Energy gained was obtained by calculating energetic content of food loads. For those containing lesser sandeels (A. marinus), the energy content was derived from the equation: energy (kJ) = 0·0031 length3·745 (Hislop, Harris & Smith 1991). For the remaining species, we multiplied the mass by an energy density of 5 kJ g−1 (Hislop et al. 1991). The energy content of the load was the sum of the prey species’ energy values.

We converted the time–activity budget to energy expended using activity-specific energy costs taken from the literature. Flight costs were calculated from Pennycuick (1989, updated: http://www.bio.bris.ac.uk/people/staff.cfm?key = 95). Wing span was calculated from wing length, using the equation wing span = (2·752 × wing length) + 0·360 (derived from breeding adult males in 1999, n = 18, r2 = 0·71). Aspect ratio was set at 6·85 (Pennycuick 1997), and air pressure at 1·23 kg m−3 (0·5 m a.s.l., the approximate flying height). The chemical power expended at a speed of 15·4 m s−1 (Pennycuick 1997) was used. Data on double-crested cormorants (Phalacrocorax auritus, a similarly sized species) taken from Enstipp, Grémillet & Jones (2006) were used for the costs of diving (26·22 W kg−1 for deep diving at 11 °C, the sea temperature during the study), incorporating the dive : pause cost ratio from great cormorants (Phalacrocorax carbo; Grémillet et al. 2003). The costs of swimming on the sea surface (12·73 W kg−1 in water at 11 °C) were taken from Enstipp et al. (2006).

statistical analysis

General linear models were used, with experience (naive vs experienced) and time of season (early vs late) entered as factors. The sine of bearing was taken to remove circularity, and the proportion of lesser sandeels in the diet was arcsine-transformed. Non-significant effects were sequentially dropped from models until the most parsimonious model was obtained.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

foraging effort and location

There was evidence of an increase in foraging effort as the breeding season progressed, with time spent flying and diving both significantly longer late in the season. There was a significant interaction between experience and time of season on time spent diving, with experienced males spending less time diving than naive males early in the season, and the converse being the case late in the season. Time spent on the sea surface did not differ with experience class or time of season, although the interaction approached statistical significance (Fig. 1; Table 1).

image

Figure 1. Mean (± SE) (a) duration of flights; (b) duration of diving; (c) duration on sea surface by naive (○) and experienced (•) males, early and late in the season.

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Table 1.  Results of general linear models on the effect of experience and time of season on time spent flying, diving and on the sea surface
Time spent:ExperienceTime of seasonInteraction
FPdfFPdfFPdf
Flying0·560·46356·420·02362·320·1434
Diving0·400·53344·340·04344·570·0434
On sea surface2·450·13360·750·39353·620·0734

There was no difference in directional bearings between experience classes, although there was a significant difference with time of season, with no directional preference early in the season, but birds mainly foraging north-west of the island late in the season. Together with the changes in flight durations, it was apparent that the area close to the colony was favoured early in the season, whereas most birds foraged close to the mainland north-west of the island late in the season (sine of bearings of foraging birds in relation to tracking station: experienced early, 0·10 ± 0·28; experienced late, –0·68 ± 0·14; naive early, –0·16 ± 0·23; naive late, –0·38 ± 0·19; GLM: experience, F1,35 = 0·00, P = 1·00; time of season, F1,36 = 4·92, P = 0·03; interaction term, F1,34 = 1·57, P = 0·21).

amount and type of food per foraging trip

Experienced males returned to the colony with food loads of significantly higher mass than naive males both early and late in the season (experienced early, 73·7 ± 17·1 g; experienced late, 89·6 ± 27·5 g; naive early, 36·9 ± 14·3 g; naive late, 23·5 ± 10·5 g; GLM: experience, F1,21 = 6·64, P = 0·02; time of season, F1,20= 0·03, P = 0·87; interaction term, F1,19 = 0·53, P = 0·48).

The proportion of lesser sandeels in the diet did not differ with experience, but declined with time of season (experienced early, 0·84 ± 0·14; experienced late, 0·55 ± 0·23; naive early, 0·96 ± 0·04; naive late, 0·25 ± 0·25; GLM: experience, F1,17 = 0·08, P = 0·78; time of season, F1,18 = 6·78, P = 0·02; interaction term, F1,16 = 1·20, P = 0·29).

foraging efficiency

Foraging efficiency was significantly higher among experienced males than naive males, and was lower late in the season in both experience classes (Fig. 2; GLM: experience, F1,20 = 5·63, P = 0·03; time of season, F1,20= 4·48, P = 0·04; interaction term, F1,19 = 0·61, P = 0·44). This effect was apparent despite a significant difference between naive and experienced birds in energetic cost per unit time while diving and on the sea surface (Table 2), because experienced males were significantly heavier than naive males (experienced males, 1·94 ± 0·12 kg; naive males, 1·86 ± 0·11; GLM: experience, F1,36 = 4·04, P = 0·05; time of season, F1,35 = 1·42, P = 0·24; interaction term, F1,34 = 0·77, P = 0·39). This was principally due to a tendency for experienced males to be structurally larger (first principal component of a principal components analysis on the three morphometric measurements taken: wing length = 0·649, tarsus = 0·865, head and bill = 0·601; GLM: experience, F1,36 = 3·60, P = 0·07; time of season, F1,35 = 0·94, P = 0·34; interaction term, F1,34 = 0·69, P = 0·41).

image

Figure 2. Mean (± SE) foraging efficiency on foraging trips by naive (○) and experienced (•) males, early and late in the season.

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Table 2.  Energetic cost per unit time (kJ h−1) of each activity for two experience classes of breeding shags: parameter estimates (mean ± SE) and results of general linear models
ActivityParameter estimatesExperienceTime of seasonInteraction
NaiveExperiencedFPFPFP
Flight561·6 ± 10·6588·2 ± 12·82·620·121·160·290·540·47
Diving174·5 ± 2·5183·5 ± 2·36·680·010·040·840·100·76
Sea surface85·4 ± 1·188·8 ± 1·34·040·051·420·240·770·39

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Our results suggest that higher survival of chicks (Potts et al. 1980; Aebischer 1993; Daunt et al. 1999) and improved growth of sons of experienced pairs (Daunt et al. 2001) is achieved through a combination of higher foraging efficiency and greater capacity to adjust foraging effort. This combination buffers the food gain of older, experienced pairs against fluctuations in environmental conditions. Our confidence in these effects is strengthened by the fact that our study was biased towards higher-quality naive birds – those breeding males that had successfully reached mid-chick rearing, and were matched for brood size with experienced pairs, making differences between the experience classes harder to detect.

In order to manipulate naive and experienced pairs to rear young simultaneously, we caused an increase in incubation duration for experienced experimental pairs, and an equivalent reduction in naive experimental pairs. Extended incubation may be advantageous if body condition improves during incubation (Gaston & Hipfner 2006). In contrast, pairs with reduced incubation have less time in which to increase condition. However, if this effect was important, we would expect improved foraging performance in birds with extended incubation compared with those of the same experience – experimental experienced and control naive males would outperform control experienced and advanced naive males, respectively. This was not what we found. Rather, both naive and experienced birds late in the season had a lower foraging efficiency than their same-experience counterparts early in the season, and the experienced birds whose breeding was delayed had significantly higher foraging effort than their earlier breeding controls. Alternatively, incubation may be costly, as experimental manipulations of incubation have demonstrated (Heaney & Monaghan 1996). However, the experienced controls had a higher foraging efficiency and brought back more food than naive experimental birds, despite having a greater incubation demand as they had incubated for longer. Similarly, experienced experimental birds had a higher foraging efficiency and amount of food obtained than naive controls. Thus our test for differences in foraging performance between experience classes was conservative, as the experienced birds performed better despite increased incubation demands.

The improvement in foraging efficiency with age and experience accords with previous studies (Jansen 1990; Desrochers 1992; Galbraith et al. 1999), but ours is the first to demonstrate that the capacity to adjust foraging effort in response to changing extrinsic conditions improves with experience. There was strong evidence that environmental conditions declined late in the season, with study birds, irrespective of experience, travelling significantly further to find food, foraging for longer, and switching from their favoured prey (the lesser sandeel; Harris & Wanless 1991) to other species (principally butterfish, P. gunnellus). Conditions were so poor that over a quarter of breeding pairs throughout the colony spent a proportion of the time foraging simultaneously, leaving the broods unattended. The precise mechanism underlying this change was not clear, but it appears that the availability of lesser sandeels declined, and depletion of prey in the vicinity of the colony may also have been a contributory factor (Birt et al. 1987). Both experience classes foraged in similar locations early and late in the season, but faced with deteriorating conditions, experienced individuals increased the amount of time spent foraging. Plasticity in foraging effort is probably an important strategy to buffer the young against fluctuating environmental conditions, and ensures that food delivered to the offspring is maintained despite a decline in foraging efficiency. In contrast, a lack of plasticity in foraging effort in naive birds in response to food availability may be a contributory factor in their poorer average breeding success. Although our study was carried out exclusively on males, both sexes share provisioning duties in this species (Wanless et al. 1993b). It is possible that the poor performance of naive males may, in part, be a response to reduced chick demand resulting from a greater contribution made by their females. However, age and experience are correlated within pairs, so it is likely that the contribution of the female is additive rather than compensatory. Thus the foraging performance of males is likely to be crucial in mediating the differences in chick survival and growth observed between naive and experienced pairs (Daunt et al. 1999, 2001).

Three main hypotheses have been put forward to explain age-related improvements in breeding performance among iteroparous species: improvements in competence (Curio 1983); reproductive restraint by younger age classes (Williams 1966); and differential survival/recruitment giving rise to differences in the phenotypic range represented within age classes (Smith 1981; Nol & Smith 1987). Furthermore, it has proved challenging to disentangle age from experience as the two are highly correlated (Pärt 1995). We are unable to establish whether the difference in foraging efficiency between the young, naive and older, experienced birds in our study resulted from within-individual changes or selection for higher-quality individuals in older, experienced age classes. Furthermore, it is not clear whether naive birds did not increase effort because they were unable to do so, or because they were showing reproductive restraint. The greater body size of experienced individuals suggests that differential mortality among small and large individuals may be an important mechanism driving differences in foraging performance with age and experience. However, longitudinal studies are required to establish unequivocally whether improvements in foraging abilities result from within-individual changes, or from selection resulting in higher average quality among older, more experienced age classes.

Among seasonally breeding species, breeding is timed to coincide with the peak availability of food (Lack 1968). The poorer foraging abilities of naive breeders may prevent them from attaining breeding condition as rapidly as experienced breeders, resulting in later relative timing of breeding when foraging conditions are generally poorer. Whatever the underlying mechanisms, our study suggests that the effects of age and experience on reproductive performance in seasonally breeding species is driven by differences in foraging performance exacerbated by a seasonal decline in environmental conditions.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We wish to thank all those people who have ringed European shags on the Isle of May, in particular the Isle of May Bird Observatory Trust. Many thanks to Helen Whittaker for help with fieldwork, and Scottish Natural Heritage for access. F.D. was supported by a NERC CASE Studentship (with CEH) and the Louise Hiom Trust.

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  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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