Group-Size Effects and Parental Investment Strategies during Incubation in Joint-Nesting Taiwan Yuhinas (Yuhina brunneiceps)

2005·4.7 MB·English

by  Hsiao-Wei Yuan

Wilson Bulletin 117(3);306-312, 2005
GROUP-SIZE EFFECTS AND PARENTAL INVESTMENT
STRATEGIES DURING INCUBATION IN JOINT-NESTING TAIWAN
YUHINAS (YUHINA BRUNNEICEPS)
HSIAO-WEI YUAN,' SHENG-FENG SHEN,« KAI-YIN LIN,^ AND PEI-FEN LEE^'*
ABSTRACT. We investigated the effect of group size on incubation effort in Taiwan Yuhinas (Yuhina
hrunneiceps) at the Highlands Experimental Farm of National Taiwan University at Meifeng, Nantou County,
central Taiwan, during 2000 and 2001. The Taiwan Yuhina is a joint-nesting, cooperatively breeding species
endemic to Taiwan. We compared differences in parental investment among individuals of different sexes and
status, explored the effect ofgroup size on group incubation effort, and investigated whether individuals show
compensatory reductions incarewithrespecttothenumberoffemaleslaying. Constancyofincubationincreased
as group size increased. Alpha females exhibited a significantly greater incubation effort than other individuals,
but effort was similar among other group members. Both alpha males and females decreased their relative and
absolute incubation effort as group size increased (i.e., there was a compensatory reduction in parental effort).
However, beta pairs maintained a consistent but low incubation effort when either gamma pairs or an extra
ibnrdeievdiidnugalbijrodisn—edantheincgrreoauspe.iOnutrhestcuodnystaalnscoydoefmoinnscturbaattieodn.aRneecweivpoetden6tiJaullygr2o0u0p4-,siazcecebepnteefdit31forMacrocopher2a0t0i5v.ely
The effect of group size on individual fit- Study, Hatchwell (1999) showed that (1) care
ness is one of the most important aspects in tends to be additive when the probability of
understanding the evolution of sociality nestling starvation is high and (2) parents are
(Brown 1983, Kokko et al. 2001). In cooper- more likely to show compensatory reductions
atively breeding animals, individuals sharepa- in care when the chance of starvation is low.
rental effort with other group members. The In addition, Hatchwell hypothesized that male
optimal parental investment ofeach individual breeders may tend to exhibitcompensatoryre-
depends largely on the sum of other group ductions due to the uncertainty of parentage.
members’ parental efforts; that is, parental ef- Little research has been conducted on the
fort is affected by group size. Much attention parental investment strategies of cooperative
has been paid to how individual provisioning breeders during incubation (Vehrencamp
effort is affected by group size in helper-at- 1977, Heinsohn and Cockbum 1994, Kom-
the-nest systems (Hatchwell 1999). Two types deur 1994). Mammalian studies have demon-
ofprovisioning effort are recognized: additive strated that variation in the relative contribu-
and compensatory (Hatchwell 1999). Additive tions of individual helpers to different coop-
provisioning occurs when parents maintain the erative activities, such as nursing and guard-
same provisioning effort, regardless of the ing, is important (Clutton-Brock et al. 2003).
number ofhelpers; thus, the total provisioning Incubation is certainly an important compo-
rate increases as group size increases (Emlen nent ofreproductive success in most bird spe-
and Wrege 1991). On the other hand, com- cies and has been considered acostly behavior
pensatory provisioning occurs when total ef- (Visser and Lessells 2001, Reid et al. 2002b).
fort is comparatively constant and breeding Incubation among cooperative breed—ers is es-
individuals reduce their parental effort in re- pecially interesting to study because i—n con-
sponse to increasing levels ofeffortby helpers trast to the cues received from nestlings par-
(Brown et al. 1978). In a detailed comparative ents and helpers receive no cues from the eggs
as to how much care is being given by other
Nat'iSocnhaoloTlaiowfanFoUrneisvt.r,yTaainpdeiRe1s06o,urTcaeiwCaonn.servation, groWuep imnevmebsetirgsa.ted the effect of group size on
2Inst, of Ecology and Evolutionary Biology and incubation effort in a joint-nesting passerine,
Dept, of Life Science, National Taiwan Univ., Taipei the Taiwan Yuhina {Yuhina hrunneiceps, here-
106, Taiwan. after referred to as yuhina). Our study focused
hav3ioCru,rrCeonrtnealdldrUensisv;.,DeItphta,cao,fNNYeur1o48b5i3o,loUgSyA.and Be- on whether additive and compensatory in-
Corresponding author; e-mail: [email protected] vestment strategies, developed in the context
306
Yuan et al. • PARENTAL INVESTMENT IN TAIWAN YUHINAS 307
I
— —
ofnestling provisioning, are also applicable to dividuals both males and females consis-
incubation effort. We explicitly considered tently chased and displaced same-sex mem-
two issues. First, we explored the effect of bers of their group. In larger groups, gamma
group size on total incubation effort. Second, individuals were chased by both alpha and
we investigated whether individuals exhibited beta individuals (see Yuan et al. 2004 for fur-
compensatory reductions in care by compar- ther details). Sex of all banded individuals
ing the differences in parental investment (97% of the birds that we observed were col-
strategies between individuals of different sex or-banded) was assigned tentatively in the
and status with respect to the number of field based on observations of singing and
breeding pairs. copulation; later, gender was verified against
sex-specific genetic markers via PCR (Fri-
METHODS
dolfsson and Ellegren 1999).
Study population.—The Taiwan Yuhina, a Incubation.—We observedmdiurnal incuba-
Timaliine babbler, is endemic to Taiwan (Cle- tion bouts from blinds 10-15 from nests by
ments 2000). Since Yamashina (1938) first de- using 15 X 40 image-stabilized binoculars.
scribed the species’ communal nesting behav- We recorded incubation effort at 21 nests of
iors, there has been no detailed study of this 11 breeding groups from June to August in
species. We have been studying a color-band- 2000 and from March to August in 2001. The
ed population of Taiwan Yuhinas since 1995 mean total observation time for each nest was
at the Highlands Experimental Farm of Na- 683 min (range = 252-1,096 min) and the
: tional Taiwan University at Meifeng, Nantou mean continuous observation period was 414
1 County, central Taiwan (24° 05' N, 121° 10' min (range = 235-839 min). We successfully
j E; 2,150 m in elevation). During June 2000, identified most individuals (89 ± 2.4%) in-
I average daytime and nighttime temperature volved in incubation at each nest. We ob-
was 25.2° C and 12.2° C, respectively. The served incubation effort during the first 10
study site has been described in detail else- days of the incubation period (mean = 5.69
where (Yuan et al. 2004). The yuhinas’ breed- days ± 2.33 SD o—f observation per nest).
ing season lasts 6 months, usually from March Data analysis. Constancy of incubation
or April to August or September. Yuhinas (i.e., the time that the eggs are in contact with
build open-cup nests 1-15 m above ground in any adult bird, expressed as the percentage of
various substrates along forest edges. Mostju- time eggs were incubated; Deeming 2002) dif-
veniles (78%) disappear from the study area fered from nest to nest. A mixed model was
i after their hatch year; therefore, most (92%) originally used to deal with the problem of
I new group members are not closely related. repeated measurement of different nest at-
Breeding groups comprise one to three mo- tempts within the same group. However, be-
! nogamous pairs (mode = 2 pairs) and some- cause “group” (indicating different breeding
times one extra male. Within each group, there group) had a negative component of variance,
GEM
) pisaiarsliwnietarh haillerapracirhsy ocfonstorciibaultliyngmosnoomgeamegoguss. tthhies mciaxseed(Smcohdalell 1w9a9s1);eqtuhievraelfeonrte,toGEM waisn
'I The combined clutch size increases as group used.
size increases. However, the average number Individual incubation effort was assessed in
of eggs laid by each female decreases with two ways; as relative incubation elfort (RIE)
' We
increasing group size (Yuan et al. 2004). Ac- and as absolute incubation effort (AIEL).
i cording to data from microsatellitc genetic calculated RIE by dividing each individuaTs
markers, mean reproductive skew (the parti- incubation time by the group's total incubation
i tioning of reproduction among same-sex in- time. We calculated AIE by dividing each in-
I dividuals within social groups) is low (Yuan dividual’s incubation time by total observation
et al. 2004), and all breeding pairs contribute time (group’s total incubation lime + time
to nest building, incubation, and provisioning during which nest was unattcndetl). We ana-
(H-WY unpubl. data). lyzed individual incubation efl'ort (R1I{ and
Alpha and beta individuals were identified A1E4 by using the residual maximum likeli-
by observing chasing and displacement be- hood (RPA1E) algorithm (mixed model) in
havior among group members. Particular in- SPSS 12.0 (SPSS. Inc. 2003) with normal er-
—
308 THE WILSON BULLETIN • Vol. 117, No. 3, September2005
TABLE 1. Results from a mixed model (residual
maximumlikelihood, REML)ofrelativeincubationef-
fort (RIE) for breeders ofalpha and beta pairs ofTai-
wan Yuhinas inNantouCounty,centralTaiwan,2000-
(%)
2001
.
Effect df F p
incubation
Intercept 1, 8 15.59 0.004
of Sex 1, 34 4.21 0.048
Status 1, 8 5.94 0.040
Group size 1, 7 1.89 0.21
Constancy Sex X status 1, 34 4.68 0.038
Status X group size“ 1, 8 2.99 0.12
Sex X group size 1, 34 1.53 0.23
Extra X group size 1, 6 0.09 0.77
®Status X group size was included in the model as a random factor.
Estimateofvariance = 33.90 ± 46.37(SE).
Numberofbreedingpairs
FIG. 1. Relationship between group size (number out this paper. All tests are two-tailed, with a
ofbreedingpairs) andincubationconstancyforTaiwan significance criterion of P < 0.05.
Yuhinas in Nantou County, central Taiwan, 2000-
2001. Larger groups had significantly greaterconstan- RESULTS
cSyE.ofSaimncpulbeatsiioznet(hnaunmbsmearlloefrngerstosu)pss.hEorwrnorabbaorvseabraers±. Factors influeticing constancy ofincubation
and individual contributions to incubation.
Constancy ofincubation (% oftime eggs were
troerrmsstruccatnurbees,fiitntewdh.iRcahnbdoothmftiexremdsacnodntrraonldfoomr ignrcouubpatseidz)e (wGasLM,sigFni12f1ica—ntl7y.32i,nfPlue=nce0d.01b4^y;
the use of repeated measurements within a Eig. 1), but not by month ofbreeding (F^^i
given group, nest (different nest attempts of 0.20, P = 0.25), number of previous nesting
egaacmhmgarobuipr)d,s,paainrdsteaxttursa(mi.ael.,esalwpihat,hobuettam,aatnesd aafttteermpfitrsst incuba=tio0n-2(9Pi7,,2iP~ =0.407.55,9)P, =or0.d5a0y)s.
in odd numbered groups), and sex. However, Individual RIE differed between sexes (group
the only interaction term we used in the anal- sizes combined, alpha and beta birds com-
ysis ofalpha’s andbeta’s incubation effortwas bined: 23.13 ± 2.38% for males, 35.64 ±
“group” X “status” because all other factors 3.64% for females) and status class (group
had a negative component of variance (Schall sizes combined, males and females combined:
1991). The incubation effort of gamma pairs 36.34 ± 2.91% for alpha birds, 17.63 ±
and extra males were excluded in all analyses 2.33% for beta birds), and there was a signif-
dguaemmtao ptahierisr asfmfaelcltedsagmrpoluep ssiizzeesa.ndHo“weexvterra”, idciadntnostexdifXferstabteutsweinetnertahcetiosnex(eTsab(lPe =1).0.A1I8=E)
was used as a categorical variable to see if an or between birds of different status (P
extra male would affect other individuals’ in- 0.11), but there was a significant interaction
cubation effort. Least significant difference between sex and status (Table 2). Pairwise
(LSD) post hoc pairwise comparisons were comparisons show that alpha females contrib-
used to compare individual effort for each sex uted more than all other birds in RIE (group
and social rank. sizes combined): alpha female (45.73 ±
Given that sex and status had a significant 3.93%) versus alpha male (26.94 ± 3.23%, P
interaction effect, we also use a mixed model < 0.001); alpha female versus beta female
REML to analyze factors affecting alpha (18.28 ± 3.87%, P < 0.001). Alpha females
pairs’ and beta pairs’ incubation efforts sep- also contributed more than all other birds in
arately. However, group fitted as the random AIE (group sizes combined): alpha female
term had a negative component of variance, (34.16 ± 2.54%) versus alpha male (20.22 ±
so the mixed model is equivalent to GLM in 2.44%, P < 0.001); alpha female versus beta
this analysis. We report means ± SE through- female (15.92 ± 3.35%, P = 0.001). There
Yuan et al. • PARENTAL INVESTMENT IN TAIWAN YUHINAS 309
TABLE 2. Results from a mixed model (residual
maximum likelihood, REML) of absolute incubation
effort (AIE) for breeders of alpha and beta pairs of
Taiwan Yuhinas in Nantou County, central Taiwan,
2000-2001
.
Effect df F p
Intercept 1, 6 10.87 0.018
Sex 1, 28 1.91 0.18
Status 1, 5 3.74 0.11
Group size 1, 5 0.20 0.67
Sex X status 1, 28 4.37 0.046
Status X group size"* 1, 5 1.63 0.26
Sex X group size 1, 28 0.40 0.53
Extra X group size 1, 3 0.48 0.54
Status X group size was included in the model as a random factor.
Estimateofvariance= 17.02 ± 30.77(SE).
FIG. 3. Mean (± SE) absolute incubation effort
(AIE) of(A) females and (B) males in different group
sizes (number ofbreeding pairs) ofTaiwan Yuhinas in
Nantou County, central Taiwan, 2()()()-20()1. Sample
size (number of nests) shown above bars.
were no significant differences among other
individuals in either RIE or AIE (Figs. 2 and
3).
Incubation effort between sexes and ^roup
—
sizes ofdifferent status. Because there was a
strong sex X status interaction, we further an-
alyzed alpha anti beta pairs separately. RIE of
alpha fctnalcs was greater than that of alpha
males (CiEM, /*', ,7 = 6.43, P = 0.016: Fig. 2)
and RIE; of the three group sizes differetl
(males anti females ct>mhinetl, alpha birtls
s(iRzIFeEIs)G(.onfu2m.(bA)erMfeeoamfanblree(se±dain,ndSgE()pBa)irremsl)aatloievfseTiaininwcdiuafbnfaetYrieuonhntingearfsfoouriptn t3)2n.ly3)3: 4±6.233.97±% 2.(.tw3t8)% b(rteueitelibnrgeepdaiinrsg),paiarn)d,
Nantou County, central Taiwan. 2(KK)-2(K)1. Sample 22.32 ± 4.32% (three breetling pairs) (/'i ^7 =
size (number of nests) shown above bars. 16.24, P < 0.001; Fig. 2). Fhere was no in-
310 THE WILSON BULLETIN • Vol. 117, No. 3, September 2005
teraction between sex and group size (F,37 - gain more benefit from larger groups in terms
37 p = 0.25) or between the extra male and of lightening their work load. This may ex-
gIrou^p size (F,37 = 0.03, P = 0.87). AIE of plain why the survival probabilities of alpha
alpha pairs differed marginally between the females, but not alpha males, increase with
sexes (group sizes combined): 20.22 ± 2.44% group size (Shen 2002).
(males), 34.16 ± 2.54% (females) (Fj37 = In this study, alpha females contributed sig-
3.78, P = 0.059; Fig. 3). AIE of alpha pairs nificantly more to diurnal incubation effort
also differed between group sizes (males and than other individuals. Yuan et al. (2004)
females combined, alpha birds only): 31.44 ± found that female yuhinas also contribute
3.20% (one breeding pair), 25.80 ± 3.11% more to nocturnal incubation. Female-biased
(two breeding pairs), and 20.53 ± 4.19% asymmetry in parental care has long been at-
(three breeding pairs) (F137 = 4.04, P = tributed to a sex-bias in the uncertainty ofpar-
0.043; Fig. 3). Again, the interaction between entage (Trivers 1972, Queller 1997). In co-
sex and group size (F137 = 0.40, P = 0.53) operatively breeding species, it has been ar-
and the interaction between the extra male and gued that selection favors male survival over
group size (Fi37 = 0.29, P = 0.59) were not parental care, whereas in females, selection fa-
significant. In beta pairs, all factors tested vors behavior that promotes offspring surviv-
above did not significantly affect either RIE al, largely due to the fact that females have a
or AIE. greater confidence of parentage (Cockbum
1998, Hatchwell 1999). Extra-group paternity
DISCUSSION is high in yuhinas (21.4%; H-WY unpubl.
To our knowledge, this is the first study data), and it seems appropriate to adopt the
showing that constancy of incubation increas- parentage uncertainty hypothesis to explain
es with increasing group size. Greater con- the high incubation effort of alpha females,
stancy of incubation may provide a more sta- but not males. However, in mostjoint-nesting
ble thermal environment, resulting in more species, the male does the bulk of incubating,
rapid embryo development (Deeming 2002). especially at night (Vehrencamp 2000, Veh-
This suggests that sharing the incubation ef- rencamp and Quinn 2004). A possible func-
fort does not necessarily lead only to “load tional explanation—for males taking over noc-
lightening” of other breeders (Brown and turnal incubation which is energetically ex-
Brown 1981, Crick 1992). Breeders may also pens—ive and imposes a greater risk of preda-
maintain the same level of incubation effort, tion is that it allows their mates to produce
thus increasing overall incubation effort as larger clutches, lay replacement clutches, or
more individuals participate. This response contribute more to nestling care (Vehrencamp
may be analogous to the “additive” effects of 2000). Moreover, the low incidence of extra-
helpers during nestling provisioning (Hatch- group paternity in those joint-nesting species
well 1999), presumably increasing the fitness may promote greater contributions ofparental
of breeders by increasing the number of off- care among the males (review in Cockbum
spring. 1998); yuhinas, on the other hand, exhibit a
Here, we showed that both alpha males and greater extent of extra-pair paternity. There-
females reduced their incubation effort when fore, different fitness components must be
more individuals were present in the group. considered to predict patterns of variation in
Beta pairs, however, maintained a constant ef- parental investment strategies in complex so-
fort when more individuals participated in in- cial groups.
cubation. This phenomenon explains why Although parental investment strategies de-
constancy of incubation varies positively with veloped according to provisioning effort can
group size. Attracting additional group mem- be analogous to incubation effort, as we have
bers reduces the cost ofparental care for alpha shown above, we believe that there are some
individuals while providing improved incu- important differences that need further exam-
bation constancy. Given that the alphafemales ination. For example, are there any differences
contribute more to incubation than other in parental investment strategies with respect
members of their respective groups, it is rea- to incubation effort and provisioning, and, if
sonable to expect that alpha females could so, why? For cooperatively breeding mam-
Yuan et al. • PARENTAL INVESTMENT IN TAIWAN YUHINAS 311
mals, much more attention has been given to support. Finally, we greatly appreciate the volunteers
comparing division oflabor ofdifferent activ- from the NTU Nature Conservation Students’ Club
ities, such as babysitting, pup feeding, and and School ofForestry and Resource Conservation, in
particular H.-Y. Hung, I.-H. Chang, K.-D. Zhong, and
guarding, than for birds (Clutton-Brock et al. S.-W. Fu for their help in the field. This study was
2003). In birds, Magrath and Komdeur (2003) supported by the National Science Council and the
also argued that the tradeoffs between parental Council ofAgriculture, Taiwan.
effort and mating effort have more commonly
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