00

ANIMAL BEHAVIOUR, 2006, 71, 1021–1028doi:10.1016/j.anbehav.2005.06.021

Parents increase their parental effort when aided by helpers

in a cooperatively breeding bird

JULIANA VALENCIA* , CARLOS DE LA CRUZ†, JUAN CARRANZA* & CONCHA MATEOS*

*Biology & Ethology Unit and yZoology, University of Extremadura

(Received 18 February 2005; initial acceptance 24 March 2005;

final acceptance 14 June 2005; published online 20 March 2006; MS. number: 8473)

In cooperatively breeding species, parents may be assisted by other individuals to feed the young. Howbreeding parents react when they receive help is poorly understood. Evidence suggests that parents usuallymaintain their feeding effort when starvation of chicks is common, and reduce it when other risks such aspredation are more important for chick survival, although some recent examples do not fit this pattern. Inno case, however, have parents been found to increase their effort when they have helpers. We investi-gated this issue in a rarely studied cooperative breeder, the azure-winged magpie, Cyanopica cyanus.Breeders increased their provisioning rate when aided by helpers. However, chick starvation was rareand it was equally so in nests with and without helpers. The incidence of predation, conversely, was sig-nificantly lower in the presence of helpers. Helpers provisioned at a lower rate than parents but bufferedthe effect of adverse conditions in bad years in the nests they assisted. To our knowledge, these findingsshow for the first time that parents can increase their investment in the current brood in the presenceof helpers, a result that does not seem to have been covered by current theory of cooperative breeding.

� 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

The way in which breeders respond to the contribution ofhelpers in cooperatively breeding birds is a key questionfor our understanding of the adaptive nature of helping. Ifhelpers contribute to feeding the chicks, breeders can reacteither by reducing their parental effort compensatingly orby maintaining the same level of care. This decision mayhave consequences for the success of the current breedingattempt, but also for the chances of having more broods inthe same season or even in future seasons by affectingbreeders’ survival. Hatchwell (1999), based on the ideassuggested by Emlen & Wrege (1991), has proposed thatparents will show a compensatory reduction in care inthe presence of helpers depending on the nature of themain causes of chick mortality. Thus, if the main causeof nest failure is starvation, parents should not reducecare and the helpers’ contribution will be additive. In con-trast, if starvation is rare and other factors such as preda-tion have greater impact on nest success, parents willshow a compensatory reduction in care according to the

Correspondence and present address: J. Valencia, Unidad de Biologıa yEtologıa, Facultad de Veterinaria, Universidad de Extremadura, 10071Caceres, Spain (email: juliana@unex.es). C. Cruz is at Area deZoologıa, Facultad de Ciencias, Universidad de Extremadura, 06071Badajoz, Spain.

10203–3472/06/$30.00/0 � 2006 The Association for the S

helpers’ contribution. This relation may be modulatedby the number of helpers, by adult survival rate and bysex differences in parental roles (Hatchwell 1999).

Although a comparative survey supports the associationbetween starvation and additive parental behaviour(Hatchwell 1999), it may often be difficult to place a givenspecies or population within such a simple dichotomy. Forexample, Luck (2002) has shown that habitat fragmenta-tion may modulate the relative importance of nestlingstarvation by affecting the foraging efficiency of breedersand helpers. One consequence is that breeders of a singlespecies may respond with compensatory or additiveparental strategies depending on the ecological condi-tions. As with most generalizations, the study of casesthat may depart from a general rule is valuable for under-standing the robustness of the relation between helpingand parental care and the underlying factors maintainingit, as well as for understanding the role of other elementsthat may complicate the system. For instance, in the coop-eratively breeding laughing kookaburra, Dacelo novagui-neae, the main cause of lost productivity is partial broodloss from starvation, but helpers fail to increase overallprovisioning, and helpers themselves, as well as breeders,reduce their feeding contributions compensatingly asadditional helpers are recruited (Legge 2000). One possibleexplanation is that kookaburras place more value on load

1tudy of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

ANIMAL BEHAVIOUR, 71, 51022

lightening than on reducing chick starvation, which sug-gests that the relative importance of present and future re-production has a role (adult survival, for instance; see e.g.Khan & Walters 2002).

To provide a framework to clarify the huge variation inthe extent of help, Heinsohn (2004) has recently proposeda general decision-making model of alloparental care,which combines the types of benefits for breeders andhelpers and how helping entails present and future coststo individuals. This model, and other theoretical litera-ture, does not include the possibility that parents may in-crease their contribution, nor is there empirical evidencefor this. However, preliminary observations on the cooper-atively breeding azure-winged magpie, Cyanopica cyanus(Valencia 2002) suggested that parents may react to thepresence of helpers by increasing their reproductive effort,which may be highly relevant for our understanding ofthe interactions between breeders and helpers.

The azure-winged magpie is a social corvid (Cramp &Perrins 1994), occurring in the eastern Palaearctic, Asiaand the Iberian Peninsula (Goodwin 1986). Its breedingsystem is colonial and the presence of helpers at the nesthas been reported in both the Japanese subspecies, C. c.japonica (Hosono 1983; Komeda et al. 1987) and the Iberiansubspecies, C. c. cooki (Valencia et al. 2003). Helpersreported in both study areas were mainly males, but bothjuvenile and adult birds could become helpers. This speciesis a good model for studying the contribution of helpersbecause pairs do not differ in territory quality: all birdscan forage in a group throughout the home range areaaround the breeding colony (Cramp & Perrins 1994; Valen-cia et al. 2003). On the other hand, azure-winged magpiesare single brooded; they very rarely have a second broodand whether they do is not related to the presence ofhelpers (Valencia et al. 2000). Hence, helpers cannot in-crease the number of nesting attempts in one season.Therefore, some of the variables involved in most cooper-ative breeding systems are naturally controlled in thisspecies.

We monitored a marked population of azure-wingedmagpies over 3 years, with the objective of studying howbreeders modify their parental behaviour in the presenceof helpers. We analysed the provisioning effort ofhelpers and breeders, and explored the evidence for therelative incidence of starvation and predation in nestfailure.

METHODS

Study Area and Population

The study area is 22 km north of the city of Badajoz,Spain (39 �030N, 6 �480W), in the middle of the species’Iberian distribution (Sacarrao 1967). The predominanthabitat is a dehesa (open holm oak, Quercus ilex, wood-land). The climate is typically Mediterranean, with dryhot summers and mild wet winters. Azure-winged magpiesin this area breed between late March and early July(Valencia et al. 2002). Since 1992, azure-winged magpiesin this population have been captured and marked withmetal and coloured plastic rings.

Period of Study and Data Collection

The data presented here refer to three breeding seasons:1995–1997. Breeding conditions were poor in 1995 afterseveral years of drought but were better in 1996 and 1997(Valencia et al. 2003).

At the beginning of the nesting period we inspectedevery tree in the area and marked it if a nest was present.Fieldwork lasted until the last chicks fledged, usually inearly July. The whole area was searched for nests at leastonce per week, and different portions of the area weresearched every 2 days, so that every tree in the area wasinspected at least twice a week.

Every nest found was checked (at least once every 2days) and intensively monitored until the chicks fledged.Observations for every nest were made with a telescopefrom a hidden position for at least 1 h every 2 days. Nestswere observed for 1–15 h each, but we included in theanalyses only those nests observed for at least 3 h.

For most nests, we identified both members of thebreeding pair. In those cases where only one member ofthe pair was marked, we assumed that the other memberremained the same because pairs proved to be highlystable during the breeding season (Valencia et al. 2003).The sex of breeders was assigned according to their behav-iour; individuals that incubated the eggs and brooded theyoung were assumed to be females (Goodwin 1986;Hosono 1966; Komeda et al. 1987).

Early monitoring of every nest from the laying periodusually allowed us to record the identity of both membersof the breeding pair before the chicks hatched. Helpersusually joined the breeding group after the chickshatched, and in a few cases during the laying period butnever at the beginning of laying, so we could alwaysdistinguish them from the male breeder.

We used provisioning rates as a measure of individualcontribution to parental care, and computed them as thenumber of feeding visits by a particular bird per h ofobservation. Provisioning visits in the azure-winged mag-pie are actual feedings. This was checked after the periodof study (in 2000 and 2002). In 23 nests when chicks were10–11 days old, we took samples of food items brought tothe nest, by using the neck ligature method (Mellott &Woods 1993). We observed the nest from a hidden posi-tion for 1.5 h, identified every bird that made a feedingvisit, and immediately removed the content of the chicks’throats. In total we collected 93 feeding samples: 60 frommale breeders, 20 from female breeders and 13 fromhelpers. In all 93 feeding samples, the visit resulted ineffective feeding and we did not observe any case of afalse feeding visit without the bird delivering food to thenest.

The age of the brood was recorded as the age of the first-hatched chick. Losses of individual chicks were recordedwhen nests were checked. The causes of these losses wereclear in some cases, for instance when a particular chickwas known to be sick or malnourished. When lossesaffected bigger chicks they were probably a result of anaccident or partial predation. Since chicks varied inweight, we assumed that starvation should affect thesmallest chick first. Therefore, losses of chicks other than

VALENCIA ET AL.: MAGPIE COOPERATIVE CARE 1023

the smallest one were not considered to be caused bystarvation. Some losses of runt chicks might not havebeen from starvation. However, we recorded as starvationall individual losses of the smallest chick in the brood. Insome, but not all cases, we had evidence of this becausethe chick was known to be malnourished. Therefore, thiscriterion is likely to overestimate the actual incidence ofstarvation.

Ethical Note

To catch birds we used wire cages (2 � 2 m and 2 mhigh) with two funnel-shaped entrances and a removabletop. During the breeding period (March–July), cages werecontinuously in the field with the top open and we fre-quently put food inside, so that the birds became usedto entering them to feed. To catch birds, we closed thetop so that birds entered through the gates but they couldnot leave the cage. The closed cage was continously ob-served. When birds entered, the observer approached. Ifthe birds were already marked, we simply opened thetop to liberate them. If not, we caught them with a pieceof cloth. Every bird was then weighed, measured, ringedand released after a few minutes. This procedure hasbeen used in the study area since 1992. Birds never suf-fered any harm during capture, and they frequently re-turned to feed in the cage very quickly after release,even on the same day.

To analyse the food items provided to the chicks by theircarers, we used plastic bridles which were put as a softligature around the chicks’ necks when they were 10–11days of age, for 1.5 h. During this time we observed anyprovisioning visits to the nest. When a provisioning visitoccurred, we approached the nest and removed the fooditems from the chicks’ throats. After the observation periodwe removed the ligatures and gave the chicks a portion ofegg and meat paste to compensate for the food removed.We did the experiment in 23 nests, and another 45 wereobserved as controls. Chicks were never manipulatedmore than once. Experimental manipulation did not causeany difference in the number of fledglings per nest (experi-mental nests: X� SE ¼ 4:00� 1:60; control nests: 3.63 �1.81; Mann–Whitney U test: U ¼ 109, N1 ¼ 15, N2 ¼ 19,P ¼ 0.24). Manipulation did not affect the provisioningrate of male breeders (experimental nests: 2.73 � 1.39,N ¼ 30; control nests: 2.10 � 1.19, N ¼ 19; ANCOVA withage and brood size as covariate: F1,45 ¼ 0.76, P ¼ 0.389) orfemale breeders (experimental nests: 2.38 � 1.83, N ¼ 30;controls: 2.05 � 1.68, N ¼ 19; ANCOVA with age and broodsize as covariate: F1,45 ¼ 0.04, P ¼ 0.842). The Consejerıa deAgricultura y Medio Ambiente of Junta de Extremadura pro-vided the authorization for the experiments.

Data Analysis

We analysed our data on provisioning rate by using thelinear mixed-model procedure fitted by restricted maxi-mum likelihood (REML). Linear mixed models can be usedto model data with correlated and nonconstant variability.

With this procedure we could control for systematicdifferences between nests and individuals in provisioningrates, while simultaneously controlling for fixed effects:year of study, nestling age, brood size, sex of parents,status of the carer (parents or helpers) and size ofworkforce. Because there were few female helpers we didnot consider the sex of helpers. The factor size ofworkforce (number of helpers) was introduced in themodels as a discrete variable, which took values fromzero (when only parents were seen during a provisioningobservation period) to three (when three or more helperswere seen provisioning the nestlings). In cases where theworkforce size did not contribute significantly to themodel, we removed the variable number of helpers fromthe analysis and added the discrete variable ‘helped?’instead. This variable took only two values: zero (onlyparents) and one, when one or more helpers were seenprovisioning the nestlings. The variables nestling age andbrood size were introduced in the models as covariates.Thus, to improve the linearity of the relation betweenthese covariates and the provisioning rate, the dependentvariable was square-root transformed.

The random factors nest and individual were includedto control for nonindependence between observations ofthe same nest, as well as nonindependence of observa-tions of the same individuals at different nesting attempts.The nested term individual (nest) was finally fitted asa random term in the models to control for nonindepen-dence of different individuals working at the same nest.Mixed models built this way showed the best-fittingvalues of the information criteria (SPSS software, SPSSInc., Chicago, IL, U.S.A.). For the fixed factors, the best-fitting model was constructed by first including all effectsand their meaningful interactions (only two-way interac-tions), and then by sequentially dropping and addingindividual terms until all terms included in the modelwere significant. We used the type III F tests to assess thesignificance of fixed terms because our models wereunbalanced.

We carried out three analyses of provisioning ratebecause, as in the study by MacColl & Hatchwell (2003),there were inherent imbalances in the data set sincehelpers provisioned only at helped nests whereas parentsmay be either helped or not, and most helpers were males,which would have made the interpretation of models dif-ficult (MacColl & Hatchwell 2003). First, we analysed theprovisioning rate of parents, both males and females. Inour case, to test for differences between parents dependingon whether they were helped or not, we created the vari-able parents’ status with four levels: helped males, un-helped males, helped females and unhelped females. Inthe second analysis, we modelled the provisioning rateof males (fathers and helpers) to compare helpers, helpedmale parents and unhelped male parents (male status vari-able). Finally, the third model was constructed to analysethe total rate of provisioning delivered by all carers at thenest. In this model, only the nest factor was consideredas a random effect. Normality tests of residuals for all threeanalyses were nonsignificant (either the Kolmogorov–Smirnov test, after Lilliefor’s significance correction, orthe Shapiro–Wilk test).

ANIMAL BEHAVIOUR, 71, 51024

RESULTS

Provisioning Rates of Parents

Parents (helped or unhelped) increased their provision-ing rate with increasing age of the chick and brood size,but females increased their rate more rapidly than males asnestlings aged (Table 1, Fig. 1). There were significant dif-ferences in provisioning rates depending on the sex of par-ents and whether they were helped or not (parents’ statusvariable in Table 1, Fig. 1). Males brought food more fre-quently than females did, but both sexes increased theirprovisioning rate when helped (mean difference in pre-dicted values from the model �SE: helped males minusunhelped males: 0.127 � 0.029; t231 ¼ 4.45, P < 0.001;helped females minus unhelped females: 0.231 � 0.029;t231 ¼ 8.10, P < 0.001; P values corrected by the Games–Howell procedure). Both male and female parents in-creased their provisioning rate significantly with the sizeof the workforce (F3,462 ¼ 9.58, P < 0.001), but only fromnests with no helpers to nests with one helper. Therewas no further significant increase (or decrease) with theaddition of more helpers (Fig. 2). Finally, parents did notchange their provisioning rate in response to the differ-ences between years.

Fathers and Helpers

Helped fathers contributed more than unhelped fathers,and both did much more than helpers (Table 2; parameterestimates: helped fathers minus helpers: X� SE ¼ 0:293�0:115; t167 ¼ 2.53, P ¼ 0.012; unhelped fathers minushelpers: 0.199 � 9.04 � 10�2; t162 ¼ 2.20, P ¼ 0.029). Allmales increased their provisioning rate with increasingage of chicks, although the increase was weaker for helpers(Fig. 3a), and with brood size (Fig. 3b). Fathers’ provision-ing rate varied significantly with the number of helpers(F3,400 ¼ 30.84, P < 0.001), showing a significant increasewhen assisted by one helper, but neither fathers norhelpers changed their contribution when further helperswere present (Fig. 4). Males (either fathers or helpers) didnot change their provisioning rate in response to the dif-ferences between years.

Table 1. Provisioning rate for parents: results from a mixed model(REML)

Effect df F P

Parents’ status 3,250 55.268 <0.0001Nestling age 1,282 107.526 <0.0001Brood size 1,126 14.693 <0.0001Nestling age*parents’ status 3,290 9.900 <0.0001

Only significant (P > 0.05) main effects and interaction terms areshown. ‘Parents’ status’ refers to a variable with four levels: helpedmale, unhelped male, helped female and unhelped female. Thenested term individual (nest) was included in the model as a randomfactor. Estimate of its variance � SE was 0.008 � 0.004 (WaldZ ¼ 1.78, P ¼ 0.074).

Prov

isio

nin

g ra

te (

visi

ts/h

)

Age of nestlings (days)

(a)

0.5

0.7

0.9

1.1

1.3

1.5

1.7

1.9

0.5

0.7

0.9

1.1

1.3

1.5

1.7

1.9

0 2 4 6 8 10 12 14 16

Brood size

(b)

0 1 2 3 4 5 6 7 8

Figure 1. Relations between provisioning rate and (a) nestling age

and (b) brood size for parents (both males and females) when

they were helped or unhelped. Symbols show predicted valuesfrom the model (Table 1) with other parameters set to their mean

values. C: Helped male; B: unhelped male; :: helped female;

6: unhelped females. Number of nests (N ) for brood sizes 1–7: 1,

6, 11, 19, 21, 19, 12 and 16, 10, 21, 38, 38, 15, 6 for helped andunhelped nests, respectively.

00.20.40.60.8

11.21.41.61.8

2

0 1 2 ≥3

Number of helpers

Prov

isio

nin

g ra

te (

visi

ts/h

)

Figure 2. Provisioning rate for male (,) and female (-) parents de-pending on the size of the workforce, measured as number of

helpers in addition to parents (from no helpers to three or more

helpers). Bars show predicted values from the model (X � SE; Table

1) with other parameters set to their mean values. Number of nests(N ) for nests with 0, 1, 2 and more than 2 helpers: 144, 56, 13 and

21, respectively.

VALENCIA ET AL.: MAGPIE COOPERATIVE CARE 1025

Total Provisioning Rates

Nests with helpers received significantly higher totalprovisioning rates than nests without helpers (parameterestimates: helped nests minus unhelped nests: X� SE ¼0:439� 8:98� 10�2; t88.41 ¼ 4.89, P < 0.001; Table 3) andin both cases they increased with increasing age of chicksand brood size (Fig. 5).

Table 2. Provisioning rate for males: results from a mixed model(REML)

Effect df F P

Male status 2,173 3.820 0.024Nestling age 1,209 9.083 0.003Brood size 1,98 15.304 <0.0001Nestling age*male status 2,214 2.654 0.073

Male status refers to a variable with three levels: helper, helped maleparent and unhelped male parent. The term nestling age*male statuswas left in the final model because of its near significance. Thenested term individual (nest) was included in the model as a randomfactor. Estimate of its variance � SE was 0.017 � 0.007 (WaldZ ¼ 2.56, P ¼ 0.010).

Prov

isio

nin

g ra

te (

visi

ts/h

)

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

1.9

0 2 4 6 8 10 12 14 16

Age of nestlings (days)

(a)

Brood size

(b)

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

1.9

0 1 2 3 4 5 6 7 8

Figure 3. Relations between provisioning rate and (a) nestling age

and (b) brood size for male parents (when helped and not helped)and male helpers. Symbols show predicted values from the model

(Table 2) with other parameters set to their mean values. C: Helped

male; B: unhelped male; >: helpers.

Total provisioning rates were also affected by the factoryear, but only for nests without helpers. During the yearwith the worst environmental conditions within the periodof study, 1995, total provisioning rates per nest in nestswithout helpers were lower than in 1996 and 1997 (meandifference in predicted values from model in Table 3 �SE: 1996 minus 1995: 0.295 � 0.062; t70 ¼ 4.70, P < 0.001;1997 minus 1995: 0.223 � 0.059; t89 ¼ 3.77, P ¼ 0.001;P values corrected by the Games–Howell procedure).However, the effect of helpers in 1995 was remarkablyhigh (parameter estimates: helped nests minus unhelpednests in 1995: X� SE ¼ 0:430� 155; t82 ¼ 2.77, P ¼ 0.007)and, as a consequence, total provisioning rates for thewhole sample of nests in 1995 were higher than in 1997(parameter estimates: 1995 minus 1997: X� SE ¼ 0:796�0:250;t61.6 ¼ 3.18, P ¼ 0.002).

To analyse the effect of the size of the workforce on totalprovisioning rates, we removed the variable helped? fromthe mixed model in Table 3 and added the variable num-ber of helpers in its place. Since there was no compensa-tory reduction in provisioning rates, the addition of newmembers to the group resulted in increased total provi-sioning rates for the brood (Fig. 6). The only nonsignifi-cant difference was between having one or two helpers,probably caused by low sample size.

Prov

isio

nin

g ra

te (

visi

ts/h

)

00.20.40.60.8

11.21.41.61.8

2

0 1 2Number of helpers

≥3

Figure 4. Provisioning rate for male parents (,) and helpers (-)

depending on the size of the workforce, measured as number ofhelpers in addition to the male parent (from no helpers to three or

more helpers). Bars show predicted values from the model (X � SE;

Table 2) with other parameters set to their mean values.

Table 3. Total provisioning rate: results from a mixed model (REML)

Effect df F p

Year 2,51 3.933 0.026Helped? 1,63 79.467 <0.0001Nestling age 1,132 82.508 <0.0001Brood size 1,55 5.619 0.021Year*helped? 2,73 4.151 0.020Brood size*year 2,54 3.991 0.024

Variable helped? refers to helped versus unhelped nests. Only signif-icant (P > 0.05) main effects and interaction terms are shown. Theterm nestling age*male status was left in the final model becauseof its near significance. Estimate of variance � SE for the random fac-tor (nest) was 0.007 � 0.008 (Wald Z ¼ 0.906, P ¼ 0.36).

ANIMAL BEHAVIOUR, 71, 51026

Partial Losses and Starvation

The presence of helpers was not related to the proba-bility of partial losses. Twelve of 30 nests with helpers, andnine of 26 without helpers, suffered the loss of somechicks (Fisher’s exact test: P ¼ 0.784). The average

Tot

al p

rovi

sion

ing

rate

(vi

sits

/h)

1.2

1.4

1.6

1.8

2

2.2

2.4

2.6

2.8

3

0 2 4 6 8 10 12 14 16

Age of nestlings (days)

(a)

1.4

1.6

1.8

2

2.2

2.4

2.6

2.8

0 1 2 3 4 5 6 7 8

Brood size

(b)

Figure 5. Relations between total provisioning rate and (a) nestlingage and (b) brood size for helped (C) and unhelped (B) nests.

Symbols show predicted values from the model (Table 3) with other

parameters set to their mean values.

0

0.5

1

1.5

2

2.5

3

3.5

0 1 2 >2

Number of helpers

Tot

al p

rovi

sion

ing

rate

(vis

its/

h)

Figure 6. Total provisioning rates for different sizes of workforce,measured as number of helpers in addition to the male parent

(from no helpers to three or more helpers). Bars show predicted

values from the model (X � SE; Table 3) with other parameters set

to their mean values.

mortality of a chick from partial losses � SD was0.13 � 0.19 and was not different in nests with helpers(0.13 � 0.19) and without helpers (0.12 � 0.18; Mann–Whitney test: Z ¼ 0.189, N1 ¼ 30, N2 ¼ 26, P ¼ 0.850).The number of lost chicks was also not different in nestswith and without helpers (Mann–Whitney test:Z ¼ 0.600, N1 ¼ 30, N2 ¼ 26, P ¼ 0.548).

Partial losses may have different causes. Only 12 cases ofpartial losses could be regarded as starvation (seeMethods). Seven of them took place in nests with helpers(out of 30; 23%) and five in nests without helpers (out of26; 19%), and the difference was not significant (Fisher’sexact test: P ¼ 0.755). The mean proportion of chick lossesdue to starvation � SD was 0.05 � 0.11, (N ¼ 56). It was al-most identical in nests with helpers (0.05 � 0.10) and innests without helpers (0.05 � 0.12; Mann–Whitney test:Z ¼ 0.252, N1 ¼ 30, N2 ¼ 26, P ¼ 0.801), so helpers didnot appear to contribute to reduce starvation.

Predation on Whole Clutches or Broods

Of 126 nests found over the 3 years, 70 (55.6%) werelost before hatching from various causes, predation beingthe most likely. At this stage there were already somehelpers but it was difficult to assign individual helpers tonests (Valencia et al. 2003), and therefore we were unableto explore a potential effect of helpers on nest success atthis stage.

Of 56 nests for which at least one chick hatched,predation occurred in nine of 30 nests (30%) with helpersand 16 of 26 (61.5%) without helpers (Fisher’s exact test:P ¼ 0.030). The presence of helpers affected the chances ofa brood surviving until fledging (20 of 30 nests withhelpers compared to 8 of 26 without helpers: Fisher’s exacttest: P ¼ 0.015).

DISCUSSION

Our results clearly show that, in the azure-winged magpie,breeders do not reduce but even increase their parentaleffort when assisted by helpers, despite helpers contribut-ing to feeding the brood. Fathers provisioned more thanmothers and both increased their provisioning rate whenassisted by helpers, helped fathers being those whocontributed most. Parents and helpers increased theirprovisioning rate with increased brood size and age ofnestlings. Both parents increased their contribution inresponse to the arrival of the first helper. Neither parentsnor helpers reduced their feeding rates when furtherhelpers joined the group. As a consequence of non-compensatory responses, total provisioning rates in-creased as more individuals arrived in the breeding group.

Over the 3 years of study, male and female breedersmaintained their provisioning rates without differencesbetween years. However, the total provisioning rate pernest differed between years, the nests with helpers in 1995receiving the most. Environmental conditions in this yearwere the least favourable for breeding within the period ofstudy (after a 5-year drought), and it was in this year thatwe recorded the highest ratio of helpers to breeders

VALENCIA ET AL.: MAGPIE COOPERATIVE CARE 1027

(39.4%, compared with an average of 22.0% in 1996–1997) and the highest percentage of helped nests (73%,compared with 45.9% in 1996–1997; Valencia et al. 2003),so that the increased number of helpers per nest bufferedthe poor conditions of that year for breeding pairs.

As the size of a breeding group increases because of therecruitment of helpers, other members of the group, eitherbreeders or helpers, could reduce their provisioning rate,as in many cooperatively breeding birds (reviewed inHatchwell 1999; Wright & Dingemanse 1999; Legge2000; Khan & Walters 2002). However, in the azure-winged magpie, neither breeders nor helpers reduced theirprovisioning rate with the additional workforce at thenest, and even increased it.

Surprisingly, the possibility that breeders might react tothe presence of helpers by increasing their contributionhas not been considered by the existing empirical ortheoretical literature on cooperative breeding (reviewedin Koenig & Dickinson 2004). Strategies of breeders in co-operatively breeding avian species range from fully com-pensating to not changing their provisioning rate, sothat broods receive more provisioning as new helpersjoin the breeding group. Hatchwell (1999) reviewed studiesof 27 species of cooperatively breeding birds and showedthat chick starvation was associated with noncompensa-tory strategies by breeders and with a positive effect ofhelpers for the reproductive success of the group. Ourdata for the azure-winged magpie do not fit this frameworkbecause (1) the noncompensatory strategy was not associ-ated with starvation and (2) the strategy used by parents inresponse to helping was to increase their provisioning rate.

Our criteria for starvation may have overestimatedactual starvation by including some mortality caused bydiseases or partial predation affecting the smallest chick.Conversely, we are confident that partial losses affectingbigger chicks in a brood cannot be the result of starvation.Hence, we can be sure that the incidence of starvation wasequal to or lower than the figure considered here.Furthermore, the low incidence of starvation affectednests with and without helpers equally.

If predation is more important than starvation as a causeof chick mortality, why do azure-winged magpie breedersnot reduce their provisioning effort compensatingly? Onepossibility is that the relevant relation may not bebetween starvation and additive strategies but betweenthe probability of increased breeding success and bothadditive care and the costs to future reproduction associ-ated with care. For example, Legge (2000) showed that, inthe laughing kookaburra, starvation was common but thepresence of helpers failed to increase breeding success sig-nificantly, and breeders reacted by reducing their carewhen assisted by helpers. Similarly, parents might reducetheir effort only if this has positive effects on their survivalor future reproductive success. Khan & Walters (2002), forinstance, have shown for the red-cockaded woodpecker,Picoides borealis, that breeders survive better after reducingtheir workload in the presence of helpers. A general modelby Heinsohn (2004) stresses that the response of parentsto the aid of helpers should result from the combinationof the current benefits of increased care and the costs toparents in terms of reduction in future success.

In our study population, the outcome of reproductiveattempts is highly variable, and the presence of helperscan notably increase the probability of success, both byincreased provisioning and by reduced predation. In thissituation, when parents rely on helpers it may be morebeneficial to ensure the success of the current brood thanto save investment for an unpredictable future. On theother hand, the effects on breeding success of increasedprovisioning rate may be more complicated than simplyan effect on the number of fledglings. For instance,a workforce increased by helpers may help increase thegrowth rate of chicks (J. Valencia, C. Cruz, J. Carranza &C. Mateos, unpublished data) and reduce the duration ofthe nestling phase, hence reducing exposure to nestpredation. In other words, the reduction in provisioningmight have other effects less evident than starvation, butstill important enough that it pays breeders not tocompensate when aided by helpers. However, whyazure-winged magpie parents increase their provisioningand why such a reaction has not been considered in theliterature on cooperative breeding remain to be explained.

Kokko et al. (2002) have suggested that parents maymaintain their provisioning effort to prevent the desertionof helpers. This can hardly apply in our case since for morethan 10 years of study in the same population we havenever observed a helper deserting once it had joineda breeding group. On the other hand, azure-winged mag-pies do not behave as if they were committed to a certainfixed level of parental care (‘sealed bid’ Sanz et al. 2000;Schwagmeyer et al. 2002), since our study shows thatthey are sensitive to the presence of other members ofthe breeding group (in this case helpers) and modify theircontribution by increasing it.

Increases in reproductive effort that are related tovariation in conditions affecting the probability ofbreeding success have already been described in contextsother than cooperative breeding. A classic group ofexamples are those generally known as differentialallocation (reviewed in Sheldon 2000), in which individ-uals can allocate parental resources depending on thecharacteristics (commonly attractiveness) of their mates.In some cases, the offspring increase in value becausethe mate provides genetic benefits, and in this respectthese cases differ from ours, but also, each member ofthe pair can adjust its own parental investment accord-ing to its mate’s investment. Most studies on negotiationof parental care focus on how one member of the paircompensates when the other reduces its care (handi-capping experiments; reviewed in Sanz et al. 2000), butalthough this is already a classic area of research, thetheoretical background of these interactions is stillpoorly understood (reviewed in Houston et al. 2005).Our case does not fit the common negotiation framework(McNamara et al. 1999) because when helpers providedcare parents did not reduce their effort. There is increas-ing evidence, however, that individuals may invest moreresources in the current breeding attempt when they per-ceive their mates are increasing their investment. Forexample, males may increase their parental effort whentheir females lay more eggs (Smith & Hardling 2000) oreggs of higher quality (Moreno & Osorno 2003; Moreno

ANIMAL BEHAVIOUR, 71, 51028

et al. 2004). In the common magpie, Pica pica, nest-buildingactivity by males may inform females about the males’willingness to invest in parental care. Soler et al.(2001) and De Neve & Soler (2002) showed that femalesincreased their reproductive effort when nests wereexperimentally enlarged or took longer to build. Thecommon feature in all these changes in reproductiveeffort by mates and the reaction of cooperative breedersto the presence of helpers that we found is the incre-ment in expected fitness return per unit of reproductiveinvestment. Parents’ responses might therefore haveevolved simply as an individual optimization of theirreproductive effort when the reproductive value ofoffspring has increased as a result of the addition ofhelpers, although theoretical modelling is required toderive specific predictions.

In conclusion, our data show for the first time thatcooperatively breeding birds can react by increasingparental effort in the presence of helpers, althoughcurrent models of alloparental care cannot account forthis result. Therefore, the relations between life historyvariables and the response of breeders to the presence ofhelpers may be more complicated than previously as-sumed and deserve further research.

Acknowledgments

We are grateful to M.A. Pitarch and the personnel ofValdesequera estate for permission and facilities, as well asto all the students who collaborated on the fieldwork. Twoanonymous referees made constructive comments on themanuscript.

References

Cramp, S. & Perrins, C. M. 1994. Handbook of the Birds of Europe,the Middle East and North Africa., Vol. VIII. Oxford: Oxford Univer-

sity Press.

De Neve, L. & Soler, J. J. 2002. Nest-building activity and layingdate influence female reproductive investment in magpies: an ex-

perimental study. Animal Behaviour, 63, 975–980.

Emlen, S. T. & Wrege, P. H. 1991. Breeding biology of white-

fronted bee-eaters at Nakuru: the influence of helpers on breeder

fitness. Journal of Animal Ecology, 60, 309–326.

Goodwin, D. 1986. Crows of the World. London: British Museum

(Natural History).

Hatchwell, B. J. 1999. Investment strategies of breeders in avian co-

operative breeding systems. American Naturalist, 154, 205–219.

Heinsohn, R. G. 2004. Parental care, load-lightening, and costs. In:

Ecology and Evolution of Cooperative Breeding in Birds (Ed. by W. D.

Koenig & J. L. Dickinson), pp. 67–80. Cambridge: Cambridge Uni-versity Press.

Hosono, T. 1966. A study of the life history of blue magpie (I).Breeding biology. Miscellaneous Reports of the Yamashina Institute

of Ornithology and Zoology, 4, 327–347.

Hosono, T. 1983. A study of the life history of blue magpie (II).

Breeding helpers and nest-parasitism by cuckoos. Journal of the

Yamashina Institute of Ornithology, 15, 63–71.

Houston, A. I., Szekely, T. & MacNamara, J. M. 2005. Conflict be-

tween parents over care. Trends in Ecology and Evolution, 20, 33–38.

Khan, M. Z. & Walters, J. R. 2002. Effects of helpers on breeder sur-

vival in the red-cockaded woodpecker (Picoides borealis). Behav-

ioral Ecology and Sociobiology, 51, 336–344.

Koenig, W. D. & Dickinson, J. L. 2004. Ecology and Evolution of

Cooperative Breeding in Birds. Cambridge: Cambridge University Press.

Kokko, H., Johnstone, R. A. & Wright, J. 2002. The evolution of

parental and alloparental effort in cooperatively breeding groups:when should helpers pay to stay? Behavioral Ecology, 13, 291–300.

Komeda, S., Yamagishi, S. & Fujioka, M. 1987. Cooperative breed-ing in azure-winged magpies, Cyanopica cyana, living in a region

of heavy snowfall. Condor, 89, 835–841.

Legge, S. 2000. Helper contributions in the cooperatively breeding

laughing kookaburra: feeding young is no laughing matter. Animal

Behaviour, 59, 1009–1018.

Luck, G. W. 2002. The parental investment strategy of an avian

cooperative breeder differs between a fragmented and an unfrag-

mented landscape. American Naturalist, 160, 809–814.

MacColl, A. D. C. & Hatchwell, B. J. 2003. Sharing of caring: nes-

tling provisioning behaviour of long-tailed tit, Aegithalos caudatus,parents and helpers. Animal Behaviour, 66, 955–964.

McNamara, J. M., Gasson, C. E. & Houston, A. I. 1999. Incorporat-ing rules for responding into evolutionary games. Nature, 401,

368–371.

Mellott, R. S. & Woods, P. E. 1993. An improved ligature technique

for dietary sampling in nestling birds. Journal of Field Ornithology,

64, 205–210.

Moreno, J. & Osorno, J. L. 2003. Avian egg colour and sexual selec-

tion: does eggshell pigmentation reflect female condition and

genetic quality? Ecology Letters, 6, 803–806.

Moreno, J., Osorno, J. L., Morales, J., Merino, S. & Tomas, G.2004. Egg colouration and male parental effort in the pied fly-catcher Ficedula hypoleuca. Journal of Avian Biology, 35, 300–304.

Sacarrao, G. F. 1967. Remarques sur la variation geographique de la

Pie-bleue, Cyanopica cyanus (Pall.) dans la Peninsula Iberique,specialment and Portugal. Arquivos do Museu Bocage, 1, 241–248.

Sanz, J. J., Kranenbarg, S. & Tinbergen, J. M. 2000. Differentialresponse by males and females to manipulation of partner contri-

bution in the great tit (Parus major). Journal of Animal Ecology, 69,

74–84.

Schwagmeyer, P. L., Mock, D. W. & Parker, G. A. 2002. Biparental

care in house sparrows: negotiation or sealed bid? Behavioral

Ecology, 13, 713–721.

Sheldon, B. C. 2000. Differential allocation: tests, mechanisms and

implications. Trends in Ecology and Evolution, 15, 397–402.

Smith, H. G. & Hardling, R. 2000. Clutch size evolution under

sexual conflict enhances the stability of mating systems. Proceed-ings of the Royal Society of London, Series B, 267, 2163–2170.

Soler, J. J., De Neve, L., Martınez, J. G. & Soler, M. 2001. Nest sizeaffects clutch size and the start of incubation in magpies: an exper-

imental study. Behavioral Ecology, 12, 301–307.

Valencia, J. 2002. Factores ambientales y comportamiento repro-

ductor en el rabilargo (Cyanopica cyanus). Ph.D. thesis, Universi-

dad de Extremadura.

Valencia, J., de la Cruz, C. & Carranza, J. 2000. Second broods in

a Mediterranean cooperatively-breeding corvid: the azure-winged

magpie. Etologıa, 8, 17–19.

Valencia, J., de la Cruz, C. & Carranza, J. 2002. Timing of breeding

in the azure-winged magpie in Spain. Etologıa, 10, 17–22.

Valencia, J., de la Cruz, C. & Gonzalez, B. 2003. Flexible helping

behaviour in the azure-winged magpie. Ethology, 119, 545–558.

Wright, J. & Dingemanse, N. J. 1999. Parents and helpers compen-

sate for experimental changes in the provisioning effort of othersin the Arabian babbler. Animal Behaviour, 58, 345–350.