Table Of Content2
The Wilson Journal ofOrnithology 118(4):527—531, 2006
MAXIMUM DIVING DEPTH IN FLEDGING BLUE-FOOTED
BOOBIES: SKILL DEVELOPMENT AND TRANSITION
TO INDEPENDENCE
JOSE ALFREDO CASTILLO-GUERRERO AND ERIC MELLINK
1 1
—
ABSTRACT. We evaluated maximum diving depth and time spent at the nest offledging Blue-footed Boo-
bies (Sula nebouxii) at Isla El Rancho, Sinaloa, in the GulfofCalifornia, Mexico. Within three consecutive 10-
day post-fledging intervals, maximum diving depth was highly variable, but was not affected by sex, weight, or
body condition. During the first days of post-fledging flight, maximum diving depth increased rapidly. By the
second week after first flight, the plunge-dives ofjuveniles were almost as deep as those ofadults. Parental care
and attachment to the nest lasted several additional weeks (up to40days afterfirst flight). Although theirdiving
capacity rapidly reached a level similarto that ofthe adults, it appeared thatjuvenile boobies took much longer
in acquiring other foraging skills. Received 1 August 2005, accepted 5 July 2006.
The speed with which juvenile birds ac- es in the acquisition offoraging skills (Wheel-
quire foraging abilities has important impli- wright et al. 2003).
cations for the evolution of life histories The Blue-footed Booby (S. nebouxii) is a
(Wheelwright and Templeton 2003). It has sexually dimorphic seabird: females are larger
been hypothesized that parental care continues than males at fledging (Drummond et al.
until young birds acquire mobility and forag- 1991). Parental care continues for a 6-week,
ing skills adequate for survival. Additional pa- post-fledging period (Nelson 1978). During
rental care improves the survival of the off- this period, young birds fly out to sea but re-
spring, but decreases long-term survival ofthe turn to their nests, where they continue re-
parents (Burger 1980). ceiving food from the parents. In this study,
Juvenile birds face major challenges in we determined the maximum diving depths
learning how to identify foraging areas and (MDD) ofwild fledgling Blue-footed Boobies
MDD
developing foraging techniques as the period to (1) examine the ontogeny of and
of parental care ends (Burger 1980, Wheel- compare it with the diving depths achieved by
wright and Templeton 2003). The study of adults, and (2) examine the relationship be-
newly volant birds can help elucidate the pro- tween the development of diving skills and
cess of such learning. However, this is com- sexually related size dimorphism.
plicated in the wild, as fledglings can move METHODS
freely through the colony site. Most ofthe few
studies on the subject have focused on pas- Field work was conducted at Isla El Rancho
serines, which have a rather short transition to (25° 10' N, 108° 23' W), a sandy, 120-ha is-
independence (Moreno 1984, Wheelwright land in the south-central Gulf of California,
and Templeton 2003). In seabirds, the devel- Mexico, at the m—outh of Bahia de Santa Ma-
opment of foraging skills and its relationship ria-La Reforma a large coastal lagoon. The
to parental care are not well known (Yoda et colony studied was located on the northeast-
al. 2004). We are aware ofonly one such sea- ern part of the island among 4-m-high sand
bird study (Brown Booby, Sula leucogaster), dunes. About 500 pairs of Blue-footed Boo-
although the birds were raised by humans bies nested in an area of <1 ha, with a max-
(Yoda et al. 2004), which could have inter- imum density of 0.6 nests/m2.
fered with social learning processes. Even less Between January and May 2004, we visited
is known about possible intersexual differenc- the island 12 times for periods of 5 days and
monitored 100 nests and 108 chicks that we
had marked with unique combinations of col-
Sup1eCreinotrrdoedEenIsnevneasdtai,gaAt.ioRn2C7i3e2n,tfEfincsaenyaddae,EBdaujcaacCiaoln- or bands. During each visit, we checked the
ifornia, Mexico. nests daily, and weighed and measured (cul-
2Corresponding author; e-mail: men, ulna, and tarsus) all banded chicks every
[email protected] otherday. Sex was determined from the length
527
528 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 118, No. 4, December2006
of ulna at fledging (males = 191-207 mm; tively; homocedasticity: F149 = 3.96, P =
females = 213-233 mm; Drummond et al. 0.55).
1991). Fledging (age at first flight) was in- We used linear regressions to assess wheth-
MDD
ferred when a bird with complete juvenile er might be a function of weight or
plumage left its nest site and returned with body condition. Residuals from the regression
clean feet (feet were covered with excrement of weight on culmen length were used as a
before the first trip to sea). For most birds, we body condition index. Using residuals ofa re-
could estimate the exact age at fledging (es- gression between weight and body measure-
timates were ± 2 days in some cases). ments as an index of condition is adequate
From 20 April to 26 May, we estimated when measurement errors and variations in
MDD
by attaching a capillary tube (Tygon, 8 body size are low (Schulte-Hostedde et al.
mm
internal diameter; Burger and Wilson 2005); the major assumption to be met is that
1988) to the lower side of a booby’s central the relationship between variables is linear,
rectrix. Tubes were recovered one day after which was the case in our study (r2 = 0.73,
application. A total of 99 capillary tubes pro- P < 0.001). To explore the relationship be-
duced usable data: 67 from fledglings (48 in- tween days since first flight and time spent at
dividuals, 15 ofwhich provided data for more the nest, we used a mixed ANOVA-ANCOVA
than one date), 17 from adult males, and 15 model, with gender serving as the fixed factor
from adult females. In addition, we estimated and days since fledging included as a covari-
the amount of time that young spent at their ate. All statistical tests were considered sig-
nests by monitoring 38 nests hourly during nificant at a = 0.05, and reported values are
14-hr diurnal periods. means ± SD.
We tested the data for normality and homo-
RESULTS
cedasticity with Kolmogorov-Smirnov and
Levene’s tests, respectively, for every group Female Blue-footed Booby chicks reached
to be compared. We used parametric proce- their maximum pre-fledging weight (2,071 ±
dures when both requirements were met. We 125.2 g) between 60 and 75 days ofage, while
grouped the MDD data for post-fledging ju- males reached it (1,628 ± 117.5 g) between
veniles into 5-day age intervals. We then con- 60 and 70 days of age. Females were signifi-
ducted a Mann-Whitney U-test to compare the cantly heavier than males (/4954 = 18.43, P <
MDD attained by male and female fledglings 0.001). After reaching their maximum weight,
for each 5-day period. female chicks lost 8.5% of their weight and
We used a mixed-model ANOVA-ANCO- weighed 1,830 g ± 72.2 at first flight, whereas
VA for comparing 5-day periods (normality: males lost 7% and weighed 1,470 g ± 63.5.
D = 0.17-0.39; homocedasticity: F439 = 0.98, Males began to fly earlier than females (83.4
P = 0.42) to evaluate the possible effects of ± 2.64 and 87.9 ± 3.8 days of age, n = 23,
ontogeny on MDD. The number ofdays since n = 19, respectively; U = 67, P < x0.001).
M2DD
first fledging was included as a covariate, with within any given period was highly var-
the 5-day periods as the fixed factor. Multiple iable (Fig. 1), and there were no statistical dif-
flights ofthe same bird in 10-day intervals (1- ferences between male and female fledglings
ct1w0o,emWepe1na1r-aef2dod0u,ultwnaidmntadhlneo/>-2tae1snsitdgsdnfaifeyfoimsrcaadalnfeettpeMerdnDifdfleDfenedtrg(ei3nsn.cag4e)msp±wleeb2sr.e.1e- 9(U=,1-=U159,d1=6aP,y2s5P=.a5f=0,t.e3P0r4.;f3=i8r6;st-0.11f510l2i-;g1dhat51:y6sdn:-a2xyns0=:xd=n9a,yxs6n=:,2nnl=2,n=6=,2 49=U,,
rmespaencdtiv3e.l6y;±/ 1=.60m.,33,nxP==105.7a3n;dnonr2ma=lit1y7:, n2W=e6,diUd =not11,dePte=ct0.a8n3).effect of daxte on
D = 0.22 and 0.23, respectively; homocedas- MDD, per se (F = 3.31, P = 0.10), but
ticity: F131 =MD1.D7, P = 0.26). Therefore, we despite great withi1>n38-interval variability, MDD
pooled the of both sexes to compare increased with time since first flight through-
MDD =
adult with that of juveniles that had out the first 15 days offlight (0-5 days 1.68
fledged at least 15 days previously. We tested ± 0.66 m, 6-10 days = 2.69 ± 0.81 m, 11-
for age-related differences in MDD using a 15 days = 3.02 ± 0.53 m; F439 = 3.64, P =
/-test (normality: D = 0.19 and 0.13, respec- 0.012; Fig. 1). By 16-20 days (3.11 ± 0.76
—
P
Castillo-Guerrero and Mellink • DIVING DEPTHS OF FLEDGING BOOBIES 529
4.5
35
4.0
7
1.5
1.0 * * * *
1-5 6-10 11-15 16-20 21-40 Adults
Days since fledging
FIG. 1. Maximum diving depth ofBlue-footed Boobies increased rapidly during the first 15 days aftertheir
first flight at Isla El Rancho, Sinaloa, Mexico, 2004. Fledglings then dived almost as deep as adults. Means ±
SE (white zone) and 95% confidence intervals (whiskers) are shown. Sample size is indicated above whiskers.
m) and 21-40 days (3.18 ± 0.55 m; Fig. 1) time at the nest after their first flight (r2 =
since flight, MDD stabilized. The 15juveniles 0.33, P < 0.001), with no differences between
for which we had >1 MDD value (there were males and females (F129 = 0.11, P = 0.73).
2 values for 9 birds and >2 for 6 birds) ex- After 25 days of flight, some individuals left
hibited a similar tendency: during the first 10 the nest for at least the entire daylight period.
days after fledging, dives were shallower than Other young birds remained at their nests for
they were during the 11-20 day interval (1- >40 days (Fig. 2).
10 days = 2.12 ± 0.70 m and 11-20 days =
3.03 ± 0.90 m, tn = -2.44, P = 0.032). Birds DISCUSSION
for which we had >2 records made shallower Blue-footed Booby parents reduce their
dives during the first 10 days after fledging provisioning to offspring just before the nest-
than they did >21 days post-fledging (1-10 lings take their first flights (sensu Nelson
days = 1.94 ± 0.35 m and >21 days = 3.42 1978; JAC-G unpubl. data). This reduction
± 0.69 m, t4 = 5.05, P = 0.007); there were may stimulate fledging and encourage the
no significant differences between the two lat- fledglings to develop foraging skills away
er periods (11-20 days = 2.64 ± 0.71 m and from their nest. Juveniles make their first
>21 days = 2.90 ± 0.96 m, t7 = -0.51, P = plunge dives on their first day of flight (every
0.62). recovered capillary tube showed evidence of
MDD
of juveniles that had flown for at immersion, including four that were attached
least 15 days did not differ from that of adult to birds just prior to their first flight).
birds (2.99 ± 0.75 m and 3.51 ± 1.88 m, re- Clearly, 15 days of learning were enough
spectively, t5A = -1.27, P = 0.26). Weight forjuveniles to dive almost as deep as adults.
was not correlated with diving depth within Based on our observations, the fledglings
sex (males: P = 0.71; females: P = 0.90). The made their first plunges at low angles and
MDD
regression between and body condition from low heights. As the days passed, the
also was not significant ( = 0.23). birds increased the plunge height and dives
Juvenile birds progressively reduced their became more vertical. During the first days
530 THE WILSON JOURNAL OF ORNITHOLOGY • Vol. 118, No. 4, December2006
70
1
o Males • Females
~
60
</)
CD oo
~
50
^
2
c Q
<D - 40 -
CL £
Cl
C/5
0
ro 30
E
c 20
0
o
0
10
0
5 10 15 20 25 30 35 40
Days since fledging
FIG. 2. The percent of diurnal time fledgling Blue-footed Boobies spent at the nest decreased with time
since their first flight (r2 = 0.33, P < 0.001) at Isla El Rancho, Sinaloa, Mexico, 2004. This relationship is
described by the equation tn = 0.5147 - 0.107 X days since fledging, where tn = percentage ofdiurnal time at
nest.
after initiation of flight, fledglings also tended after fledging, while others required >40 days
to fly in groups around the island, suggesting to do so.
that social interactions might facilitate their It is unlikely that temporal changes in the
development of diving and, perhaps, foraging depth at which prey were found affected our
MDD
skills. recorded in fledglings. Our data did not
For several weeks after their first flight, exhibit any effects of date, and fledglings did
fledglings continued begging for food from not exhibit much synchrony in dates of first
their parents. Juveniles of other species usu- flight that could confound our data. Some
ally cease begging when foraging for them- fledglings were already independent by the
selves becomes more profitable (Moreno time others began to fly and, in some cases,
1984, Heinsohn 1991, Wheelwright and Tem- >2 months had passed between early- and
pleton 2003); thus, the young birds in our late-fledging birds. We did not find evidence
study apparently required several additional of temporal patterns in adult MDDs.
weeks to become adequate foragers. Similar Despite the Blue-footed Booby’s distinct
to other sulids (Burger 1980, Yoda et al. sexual dimorphism in size and gender-influ-
2004), the Blue-footed Boobies at El Rancho enced differences in growth and date of first
exhibited gradual separation from their par- flight (Torres and Drummond 1999; this
ents. Based on our observations, we hypoth- study), we found no gender differences in
esize that there are two periods in the devel- MDD. Given the limitations of capillary
opment of foraging skills: (1) an initial rapid tubes, however, further study of the relation-
improvement in the depth attained during ship between sexual dimorphism in size and
plunge-dives, followed by (2) improvement in booby diving performance is warranted. It
other behaviors, such as locating and captur- seems that fledging Blue-footed Boobies de-
ing prey. Presumably, once birds begin catch- velop plunge-diving skills and attain MDDs
ing fish, begging frequency and presence at similar to those of adults relatively quickly.
the nest decrease. Some juveniles apparently However, this does not imply that juvenile
achieved this level ofindependence at 25 days feeding success and/or foraging performance
-
Castillo-Guerrero and Mellink • DIVING DEPTHS OF FLEDGING BOOBIES 531
is equivalent to that of adults. Their nest at- cations for avian sex ratios. American Naturalist
tendance and insistent begging for long peri- 138:623-641.
ods indicate that foraging for themselves, Heinsohn, R. G. 1991. Slow learningofforagingskills
andextendedparental care incooperativelybreed-
along with developing prey-finding and prey- ing White-winged Choughs. American Naturalist
capturing skills, delays the full independence 137:864-881.
of young Blue-footed Boobies. Moreno, J. 1984. Parental care of fledged young, di-
vision oflabor, and developmentofforagingtech-
ACKNOWLEDGMENTS niques in the Northern Wheatear (Oenanthe oen-
We aregrateful toCONACYTandSEMARNATfor Nelsaonnt,heJ.).BA.u1k9781.01T:h7e41S-u7l5i2d.ae: gannetsand boobies.
funding. A. Aguilar, and the M. A. Gonzalez-Bernal Oxford University, Oxford, United Kingdom.
family provided logistical support. M. Pradoand E. A. Schulte-Hostedde, A., B. Zinner, J. S. Millar, and
Penalozaassisted during field work. J. Awkermanpro- G. J. Hickling. 2005. Restitution ofmass-size re-
vided editorial advice. S. Herzka, E. A. Schreiber, D. siduals: validating body condition indices. Ecol-
J. Anderson, and an anonymous reviewer greatly im- ogy 86:155-163.
proved this manuscript; we are grateful to all ofthem. Torres, R. and H. Drummond. 1999. Does large size
make daughters of the Blue-footed Booby more
LITERATURE CITED expensive than sons? Journal of Animal Ecology
68:1133-1141.
Burger, J. 1980. The transition to independence and Wheelwright, N. T. and J. Templeton. 2003. Devel-
postfledging parental care in seabirds. Pages 367 opment offoraging skills and the transition to in-
447 in Behaviorofmarine animals, vol. 4 (J. Bur- dependence injuvenile Savannah Sparrows. Con-
ger, B. L. Olla, and H. E. Winn, Eds.). Plenum, dor 105:279-287.
New York. Wheelwright, N. T., K. A. Tice, and C. R. Freeman-
Burger, A. E. andR. P. Wilson. 1988. Capillary-tube Gallant. 2003. Postfledging parental care in Sa-
depthgauges fordivinganimals: an assessmentof vannah Sparrows: sex, size and survival. Animal
their accuracy and applicability. Journal of Field Behaviour 65:435-443.
Ornithology 59:345-354. Yoda, K., H. Cono, andY. Naito. 2004. Development
Drummond, H., J. L. Osorno, R. Torres, C. Garcia- of flight performance in the Brown Booby. Pro-
Chavelas, and L. H. Merchant. 1991. Sexual ceedings of the Royal Society of London, Series
size dimorphism and sibling competition: impli- B (suppl.) 27LS240-S242.
