Behavioral Ecology Vol. 10 No. 1: 41-47
© 1999 International Society for Behavioral Ecology
Maternal expenditure in the polygynous and monomorphic guanaco: suckling behavior, reproductive effort, yearly variation, and influence on juvenile survival
Department of Animal Ecology and Program in Ecology and Evolutionary Biology, 124 Science II, Iowa State University, Ames, IA 50011-3221, USA
Address correspondence to R. J. Sarno, Laboratory of Genomic Diversity, FCRDC/NCI, Building 560, Room 11-12, Frederick, MD 21702-1201, USA. E-mail: rjsarno{at}mail.ncifcrf.gov.
Received 29 August 1997; accepted 15 June 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We investigated patterns of maternal expenditure and its influence on juvenile survival in the polygynous monomorphic guanaco (Lama guanicoe) in southern Chile from 1990 to 1994. Birth weight and growth rate (until age 1) of males and females were similar. Suckling rates of males and females were not significantly different, although mothers of males rejected suckling attempts more often than mothers of females during fall and winter. Mothers with sons terminated suckling bouts in equal proportion as did mothers with daughters. Our estimated level of reproductive effort for guanacos falls within the range of species exhibiting no sex-biased maternal expenditure on offspring. Mean yearly birth weight was negatively correlated with population density. Mean suckling time throughout the year differed among cohorts, as did the mean number of suckling attempts and rejected suckling attempts per hour throughout the year. Juvenile survival was estimated until age 1. Of the model with five covariates including juvenile sex, birth weight, adult female aggression toward taggers, mean suckling time, and population density, only mean suckling time and population density were significantly related to survival. The risk ratio for mean suckling time indicates that the risk of mortality increases as suckling time increases, whereas the risk ratio for population density indicates that the risk of mortality decreases as population density increases. Under some conditions increasing population density may be correlated with lower offspring birth weight, yet enhanced juvenile survival. This effect on survival was possibly associated with the number of predators on the study area from year to year.
Key words: Chile, guanaco, Lama guanicoe, maternal expenditure, survival.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The amount of maternal expenditure (ME), the time and energy needed to raise offspring (Clutton-Brock, 1991
; Hogg et al.,
1992), in ungulates can vary depending on offspring sex
(Clutton-Brock, 1991), the ratio of
offspring birth weight to maternal weight (Byers and
Moodie, 1990), and population density, which appears to influence
maternal condition (Clutton-Brock et al.,
1987; Skogland, 1990).
One or more of these factors likely influence offspring birth weight, suckling
behavior, growth rates, and ultimately survival during the period of parental
care.
Differential ME on juveniles of one sex is hypothesized to evolve when one
sex suffers greater juvenile mortality and/or greater variance in lifetime
reproductive success (Maynard Smith,
1980; Trivers and Willard,
1973; Willson and Pianka,
1963). Greater ME on male offspring has been documented in
polygynous dimorphic ungulates
(Bérubé
et al., 1996; Clutton Brock et al.,
1982; Festa-Bianchet,
1989; Hogg et al.,
1992; Wolff,
1988; but see Green and Berger,
1990), in which increased expenditure may either augment survival
and/or enhance reproduction by influencing traits important to mating success,
such as body condition and body size. Males generally suffer greater juvenile
mortality (Clutton-Brock et al., 1985),
and in at least one species show greater variance in reproductive success than
females as adults (Clutton-Brock et al.,
1988).
Conversely, in various ungulates exhibiting seemingly equal magnitudes of
polygyny and size dimorphism as those in which ME has been cited, ME is equal
between the sexes (Byers and Moodie,
1990; Carl and Robbins,
1988; Gauthier and Barrette,
1985; Mueller and Sadleir,
1980; Robbins and Moen,
1975). Byers and Moodie (1990)
propose that the comparative level of reproductive effort in ungulates (i.e.,
offspring birth weight0.75/maternal weight0.75), not the
degree of adult size dimorphism, is the best predictor of biased ME on
offspring. Sex-biased ME is limited because the amount of energy that mothers
must provide to support rapid offspring growth rates prevents extra
provisioning of sons. Although a species may exhibit adult size dimorphism,
juvenile males are unable to evolve higher growth rates than juvenile females
during the period of parental care because mothers are already providing the
physiological maximum amount of energy possible to both sexes.
Despite numerous studies investigating ME in ungulates, few have focused on
polygynous, monomorphic species. Patterns of ME in horses (Equus
caballus) show that gestation is longer for male fetuses and that
juvenile males suckle more often and acquire more milk than females
(Berger, 1986;
Boyd, 1988;
Duncan et al., 1984).
In this study we examined maternal expenditure in the guanaco (Lama
guanicoe). Field studies on this population have been conducted since
1979. Newborns have been marked and weighed since 1987
(Franklin and Johnson, 1994), and
survival of radio-collared juveniles was studied from 1991 to 1996.
Additionally, data regarding population dynamics as well as life histories of
adults have been collected.
The objectives of this study were to (1) compare pre-and postbirth ME on sons and daughters based upon juvenile birth weight, growth rate, and suckling behavior, (2) assess the level of ME among years and identify possible factors influencing these differences, and (3) investigate the influence of ME on individual juvenile survival until age 1.
One might predict greater ME on sons for two reasons. First, Behl
(1992) estimated that juvenile male
survival was lower than that of females by approximately 10% (p
=.86). Second, reproductive success among adult males appears to be most
variable. At 3 years of age and older, adult males seasonally defend food
resources essential to females, thereby resulting in a resource-defense
polygyny mating system (Franklin, 1983).
Between 15% and 20% of all adult males breed in any given year,
and the number of copulations may differ by as much as 11 times among breeding
males (Jurgensen, 1985). Reproductive
success of adult males is positively correlated with the number of adult
females on their territories (Jurgensen,
1985). During the breeding season the majority of adult females
occupy relatively few territories, yet they use the same territories year
after year. Thus, high site-fidelity by adult males tends to accentuate
differences in reproduction among adult males and between adult males and
females. A male's ability to successfully defend a territory may depend on
aggression, mobility, and body condition. Conversely, adult females generally
reproduce for the first time at age 3, produce 1 offspring/year beginning in
spring (November), and breed with a 0.75 probability each year.
Mean body weight of adult males and females is similar. Raedeke
(1979) reports similar length and mean
weight of adult females and males from Tierra del Fuego. Besides larger
canines, adult males possess no other secondary sexual characteristic that
distinguishes them from adult females. Because of adult monomorphism and
presumed equal birth weights and growth rates of juvenile males and females,
one could also hypothesize equal ME on sons and daughters.
If there is sex-biased ME in guanacos, we predict significant differences
in birth weight, and/or growth rates, and/or suckling behavior between
juvenile males and females. Additionally, the estimated rate of reproductive
effort should vary between 0.022 and 0.149 (as in
Byers and Moodie, 1990). If there are no
sex differences in ME, aside from observing no differences in the previously
mentioned variables, the birth weight:maternal weight ratio should be
>0.157 (Byers and Moodie, 1990).
Because certain components of ME are likely to be correlated with
population density, which varies over time, we wanted to examine the
consistency of the level (e.g., birth weight, suckling behavior) of ME among
years. Population density, for example, can affect offspring birth weight
(Skogland, 1990). We also assessed the
influence of ME on individual juvenile survival. Survival of juvenile
ungulates can be influenced by offspring sex, birth weight, and population
density (Caughley, 1970;
Clutton-Brock et al., 1985;
Clutton-Brock et al., 1987;
Sauer and Boyce, 1983;
Skogland, 1985,
1990). Survival is also likely linked to
offspring suckling behavior. Additionally, maternal protection of offspring
(i.e., aggression toward researchers attempting to capture and tag newborns)
could be considered a form of ME (Trivers,
1972) and may influence offspring survival. Maternal aggression
may indicate an adult female's propensity to protect her newborn from other
con-specifics and/or potential predators. We are not aware of any previous
attempts to relate variables of ME to individual juvenile survival.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The study was conducted from 20 November 1990 to 1 March 1994 in Torres del Paine National Park (51°3' S, 72°55' W) located in the eastern foothills of the Andean mountain range of southern Chile. The park encompasses 2400 km2 and provides almost undisturbed habitat for wildlife. The study area was a 40-km2 "peninsula" ranging from 200-400 m in elevation, bordered by large lakes to the south, north, and west and a sheep ranch to the east. The landscape was open with rolling hills, vegetation was rarely >1 m high, and animals were easily observed. Grasses (Festuca gracillana, Anarthrophyllum patagonium) and shrubs (Mulinum spinosum, Senecio patagonicus, and Berberis buxifolia) dominate this pre-Andean steppe (Pisano, 1974)
. Habituation of this
protected population facilitated approach on foot to within 5-10 m of guanacos
without their retreat.
We captured, sexed, and weighed newborn chulengos (juveniles between birth
and age 1) (Franklin and Johnson, 1994)
between 18 November and 10 December 1990-1992. We caught 98% of
chulengos within 24 h after birth, and we used capture weight as a measure of
birth weight and thus prenatal ME. Eighty-four percent of the captures
occurred between 20 November and 3 December. We tagged chulengos in both ears
with individually numbered ear tags. We also fitted most chulengos with
radio-transmitters mounted on expandable collars (modified from
Keister et al., 1988). We captured 99
chulengos in 1990, 100 in 1991, and 98 in 1992, or about 20% of each
cohort. We used data from wild-born, captive-reared chulengos (raised with
their mothers), to compare growth rates between males and females from birth
until 1 year of age.
We observed chulengo behavior from 0830 h to 1800 h during spring
(September-November), summer (December-February), and fall (March-May), and
from 1000 h to 1600 h during winter (June-August). We observed all randomly
located focal chulengos for 1 h (Altmann,
1974). We followed all marked chulengos from birth until they
dispersed from family groups unaccompanied by their mothers or until they
died. There were no instances in which a radio-collared chulengo emigrated
from the peninsula. One to four investigators were in the field year-round,
for a total of 4020 h of observation.
During each hour of observation, we collected information on suckling behavior including total suckling time, number of suckling attempts and rejections, and the number of suckling terminations by mothers with sons versus mothers with daughters. Because of the reduction in the frequency of suckling bouts by the end of summer (February), we analyzed suckling data by months from November to February, and thereafter by the seasons fall, winter, and spring. We considered a chulengo suckling when we observed it on the teat. A suckling attempt was noted as such when a chulengo lowered its head, raised its tail, and approached the teat. We recorded a rejected suckling attempt when the mother (1) moved away from her chulengo while it was reaching for her teat, (2) lifted her leg in order to block access to her teat, (3) or spit at the approaching chulengo. The chulengo terminated suckling by relinquishing the teat and walking away. Mothers terminated suckling bouts either by walking away from the suckling chulengo or by lifting a hind leg. If a chulengo paused while suckling, we subtracted that time from the total suckling time.
We tested for within-year differences between males and females in mean
suckling time/h, suckling bout duration, number of suckling attempts, and
rejected suckling attempts/h using Student's t test. We analyzed
among-year differences in these variables as well as comparing birth weights
and growth rates of male and female chulengos using standard ANOVA techniques.
We used chi-square analysis to test if (1) sons and daughters terminated
suckling bouts equally, (2) mothers rejected suckling attempts based on
offspring sex, and (3) mothers terminated suckling bouts based upon offspring
sex. We also examined the relationship between suckling behavior and chulengo
birth weight using Pearson correlation. We related mean cohort birth weight to
population size and meteorological data (mean seasonal temperature and total
seasonal precipitation) from 1987 to 1993 and used Pearson correlation and
standard regression techniques to analyze these relationships. All data were
analyzed using SAS software (SAS Institute,
1989).
We calculated sample size (n) for our suckling data based on the number of marked animals observed during a given time period (i.e., we used the mean of all observations for each chulengo), not on the number of observations for each animal. Because the individual was the unit of measure, we believe that our unweighted means best describe the means and variances of our variables.
The Kaplan-Meier product limit estimator of survival for staggered entry
(Pollock et al., 1989;
White and Garrott, 1990) was calculated
until 365 days of age. Chulengos were censored because of collar loss, radio
failure, or when we were not certain of an individual's death
(Pollock et al., 1989). We compared
survival functions between males and females using procedure LIFETEST
(Allison, 1995;
SAS Institute, 1989). The Cox
proportional hazards model (procedure PHREG;
Allison, 1995) was used to relate
mortality rate to explanatory variables. We screened potential explanatory
variables by measuring their correlation with the logarithm of failure times
[ln(T)] before attempting to model the hazard. Based on this
screening, chulengo sex, birth weight, mother aggression toward taggers,
population density, and mean suckling time were considered.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Birth weight, growth rate, and reproductive effort
Birth weights of males and females were not significantly different from each other (F1,288 = 0.59, p =.44). There was a significant difference among years, however (F2,288 = 4.55, p =.01), but no year-by-sex interaction (F2,288 = 0.01, p =.99; Table 1). Growth rates of chulengo males and females did not differ (F1,65 = 1.63, p =.203), nor was there a sex-by-season interaction (F3,65 = 0.31, p =.816). At 1 year of age, weights of chulengo females (mean = 42.0 kg, SE = 1.6, n = 28) and males (mean = 40.6 kg, SE = 1.28, n = 39; t = 2.0, df = 65, p =.472) were similar.
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Our estimated level of reproductive effort for guanacos (birth weight0.75/maternal weight0.75) is 0.191 (chulengos, mean = 12.7 kg, SE = 0.10, n = 295, range 9-16 kg; adult females, mean = 115.4 kg, SE = 1.86, n = 23, range 101-130 kg). Additionally, we estimated the level of reproductive effort throughout the range of chulengo and adult female weights. Only adult females that weighed >105 kg which produced chulengos weighing 9 kg (reproductive effort 0.153) fell within the range of those species that could provide additional energy on offspring of one sex.
Suckling behavior
There were no significant differences between male and female chulengos in
either mean suckling time/h (unequal variance t = 0.001, df = 245.8,
p =.999; Figure 1),
suckling bout duration (t = 0.86, df = 261, p =.390), number
of suckling attempts/h (unequal variance t = 0.48, df = 216.7,
p =.631; Figure 2), or mean
number of rejected suckling attempts/h (unequal variance t = 0.59, df
= 179.5, p =.554; Figure 2,
Table 2).
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In fall and winter male chulengos (meanfall = 0.85 attempts/h,
SE = 0.08, n = 94; meanwinter = 0.60, SE = 0.11,
n = 75) attempted to suckle significantly more often than females
(meanfall = 0.65, SE = 0.08, n = 80;
meanwinter = 0.31 attempts/h, SE 0.05, n = 96;
unequal variance tfall = 2.15, df = 154.7, p
=.033; unequal variance twinter = 2.26, df = 135.6,
p =.026). The mean number of rejected suckling attempts/h of males in
fall (mean = 0.41, SE = 0.66, n = 94) and winter (mean = 0.36, SE =
0.09, n = 75) was also significantly higher than those of females
(mean fall = 0.24, SE = 0.03, n = 96; mean winter = 0.14, SE =
0.04, n = 80; unequal variance tfall =
2.38, df = 142, p =.019; unequal variance
twinter = 2.10, df = 96.9, p =.038;
Figure 2). Although mothers terminated the
greatest number of suckling bouts (67%), there was no difference in the
number of suckling terminations between mothers with sons versus mothers with
daughters (
2 = 2.74, df = 1, p =.98).
There was a negative correlation between mean suckling time/h and birth weight (r = -.169, n = 224, p =.021). There was no correlation between the mean number of suckling attempts/h and birth weight (r = -.096, n = 224, p =.150), nor between the mean number of rejected suckling attempts/h and birth weight (r = -.011, n = 224, p =.090).
Yearly variation in birth weight and suckling behavior
Mean cohort birth weight was significantly negatively correlated with
population density on the peninsula (r = -.871, p =.011,
N = 7; Figure 3). The slope
of the fitted regression line (y = 13.90 - 0.0008x) suggests that for
an increase in population size of 500 animals (throughout the range of
observed population sizes), mean chulengo birth weight decreased by
approximately 0.4 kg. There was no significant correlation between mean cohort
birth weight and mean seasonal temperature nor between birth weight and total
seasonal precipitation in either winter (r = -.02, -0.63, N
= 7, p =.97,.13) or spring (r =.35, -.39, n = 7,
p =.44,.39) from 1987 to 1993.
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Mean suckling time/h throughout the year differed significantly among cohorts (F2,257 = 5.21, p =.006), but mean suckling bout duration throughout the year did not differ significantly (F2,257 = 1.17, p =.312; Figure 4) among cohorts. There were significant differences among cohorts in the mean number of suckling attempts/h (F2,257 = 7.58, p <.001) and mean number of rejected suckling attempts/h (F2,257 = 6.38, p =.002; Figure 5).
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There were also differences in the proportion of chulengo suckling attempts
rejected by mothers among cohorts (1990 = 43%, 1991 = 47%, 1992 =
32%; 2 = 48.4, df = 2, p <.0001).
Finally, the number of suckling bouts that mothers terminated also differed
significantly among cohorts (63% in 1990, 67% in 1991, and
72% in 1992; 2 = 11.0, df = 2, p
=.004).
Chulengo survival
Because all radio collars fell off of chulengos born in 1990 (n =
99), survival is based on the 1991 and 1992 cohorts. We estimated survival
(
) of 160 chulengos until 1 year of age (mean
chulengo = 0.513, SE = 0.04. Although
between males and females was not
significantly different (log rank 2 = 0.775, df = 1,
p =.379), male survival ( = 0.486, SE
= 0.058) was lower than that of females ( =
0.536, SE = 0.054). Of the model with five covariates including chulengo sex,
birth weight, adult female aggression toward taggers, mean suckling time, and
population density, only mean suckling time and population density were
significantly related to
(Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Pre- and postbirth maternal expenditure and estimated reproductive effort
Maternal expenditure in sons and daughters appears equal. Prebirth ME did not differ between sons and daughters, as birth weight did not differ between the sexes. There was also no obvious differential postbirth maternal expenditure. Growth rates of chulengo males and females were similar. Additionally, neither sex appeared to garner significantly more milk than the other, nor did either sex consistently suckle longer than the other in each month-season.
We predicted that heavier chulengos should have greater energetic requirements than lighter chulengos and that we would observe a positive relationship between chulengo birth weight and mean suckling time, mean number of suckling attempts/h, and/or mean number of rejected suckling attempts/h. The nonsignificant correlation between chulengo birth weight and suckling time/h and number of suckling attempts/h did not support our hypothesis. Although we observed a significant negative correlation between mean suckling time/h and birth weight, we do not believe that this relationship is biologically meaningful because of the low r value. An alternative hypothesis, however, is that larger chulengos empty the udder faster and obtain the same amount of milk over a shorter period.
It is puzzling that the number of suckling attempts by male chulengos in
fall and winter was significantly higher than that of females, but not
significantly different from that of females during the rest of the year. If
one sex required more energy than the other because of differential growth
rates, for example, then differences in suckling behavior should have emerged
at some point and continued throughout the year. If chulengo males remained in
family groups longer, then perhaps one could infer that males garner more
energy; chulengo males, however, disperse from family groups before
females (Franklin, 1983;
Garay et al., 1995).
Variation in adult female weight could represent vastly different levels of
ME for small and large mothers, considering the range of birth weights and
maternal weights that we observed. Based on Byers and Moodie's
(1990) estimation of maternal reproductive
effort, only adult females weighing >105 kg which produced the lightest
chulengos (9 kg) possessed the energetic capacity to invest more energy on one
sex of offspring. Large mothers producing small offspring apparently did not
apportion additional milk, because suckling time was not related to birth
weight. All other estimates of reproductive effort yielded values that fell
within the range of those species showing no differential ME on offspring.
Thus, our data on birth weight, growth rate, and suckling behavior of males
and females are aligned with Byers and Moodie's
(1990) hypothesis because our calculated
level of reproductive effort for guanacos (0.191) falls within the range of
those species exhibiting no sex-biased ME on offspring.
Yearly variation in maternal expenditure
We observed a density-dependent effect on mean yearly birth weight. One of
the likely social consequences of increased population density was more
intense feeding competition. Adult females probably garnered less energy in
higher density years, and as a result, produced lighter offspring. Effects of
population density on growth, fecundity, and birth weight have also been
demonstrated in other populations of mammals
(Bérubé
et al., 1996; Caughley,
1970; Clutton-Brock et al.,
1982; Geist,
1971; Grubb,
1974; Klein,
1968; Sinclair,
1977; Skogland,
1985).
Postnatal ME also appeared to vary over time. The 1991 cohort had the
highest mean birth weight, but exhibited the lowest mean annual suckling
time/h. Because of the significant negative correlation between mean annual
birth weight and population density, we infer that higher mean birth weight
indicates relatively better adult female body condition. Fewer animals on the
peninsula meant more food for residents. Pollard's
(1993) study on domestic alpacas (close
relatives of the guanaco) suggests that adult female guanacos in good
condition can produce higher quality milk and/or more milk. Chulengos suckling
from mothers in good condition may receive more milk per unit suckling time
than they would from mothers in poor condition. In domestic species, more milk
in the mammary gland creates higher internal pressure, and offspring generally
receive more milk per unit suckling time (Heald,
1985). In some species of mammals adult females in poor condition
produce less milk, resulting in an inverse relationship between offspring
suckling behavior and milk production (Hall et al.,
1979; Louden et al.,
1983; Mendl and Paul,
1989). Thus it seems plausible that better and/or more milk might
reduce suckling time by chulengos, and it could explain the lower mean
suckling time and mean number of suckling attempts/h of chulengos born in
1991.
Mothers terminated the greatest proportion of suckling bouts for chulengos born in 1992, suggesting that adult females were in the relatively poorest condition in this year compared to 1990 and 1991. Furthermore, the winter of 1992 was the most severe during the study. Perhaps nursing termination is more indicative of adult female body condition because it suggests decreased milk availability. There is a possible inverse correlation between mean suckling time and population density. Clearly, more data are needed to address this issue.
Maternal expenditure and chulengo survival
Behl (1992) reported that annual
survival of male chulengos was consistently lower than females by 10%
(p =.086). We observed no significant difference between male and
female survival until age 1. Sex-differential survival in mammals has been
generally observed in dimorphic species
(Clutton-Brock, 1991;
Ralls et al., 1980), in which juvenile
males appear to be more susceptible to food shortages
(Clutton-Brock et al., 1985). Because
guanacos are monomorphic and juveniles males and females exhibit similar
growth rates, we predicted comparable survival between the sexes.
Chulengo survival is significantly related to mean suckling time and population density. The risk ratio for mean suckling time indicates that the risk of mortality increases as suckling time increases, while the risk ratio for population density indicates that the risk of mortality decreases as population density increases. We initially predicted the opposite relationships between these variables and survival.
Perhaps chulengos that suckled longer were in poorer condition and/or received relatively less milk from their mothers. These individuals may have also been suffering from some other malady and thus were at a higher risk of mortality. Additionally, mothers nursing juveniles may not be as vigilant to predators.
Although juvenile survival decreases in response to increasing population
density in other ungulate populations (Caughley,
1970; Clutton-Brock et al.,
1987; Sauer and Boyce,
1983; Skogland, 1985,
1990), we observed the opposite trend in
this guanaco population. Puma predation, the leading cause of juvenile
mortality, possibly influenced this trend. Between 1991 and 1992 the
population size of guanacos increased by approximately 25%, while the
number of chulengos killed by pumas decreased by 26% (n = 12
less kills). As population density of guanacos increased, the risk of
mortality by pumas decreased. Although population density has often been cited
as having a negative impact on juvenile survival, this may not always be the
case. Various factors could dampen this effect, and we suggest that one of
them may be the consistency of predation from year to year.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank the Chilean National Forestry and Park Service (CONAF) and the administration at Torres del Paine National Park for their assistance and collaboration, particularly G. Santana, J. Toro, and N. Soto. We thank S. Jenkins, R. Koford, M. Peacock, and K. Shaw for comments on earlier versions of the manuscript. Insightful reviews at the later stages by M. Festa-Bianchet, W. Johnson, J. Wolff, and C. Vleck greatly improved the paper. D. Cox, P. Hinz, and H. Stern provided statistical advice. A. Anderson, M. Bank, C. Bergman, T. Chladny, J. Cleckler, A. Engh, E. Gaylord, K. Gaylord, K. Guderian, P. Heaven, K. Nielsen, I. O'Connell, W. Prexl, J. Rathje, J. Reed, S. Shoemaker, C. Solek, B. Soppe, K. Stueckrath, T. Sulser, and N. Varley provided field assistance. B. Gonzalez of Universidad Católica-Santiago provided data regarding chulengo growth rates and adult female weights. Capture, handling, and blood exportation permits were issued by Servicio Agricola y Ganadero (SAG) in Punta Arenas, Chile. Permits to import guanaco blood samples into the Unites States were issued by the USDA to W.L. Franklin and R.J. Sarno. This study was supported by Patagonia Research Expeditions, National Science Foundation grant no. BSR-9112826, and Organization of American States grant no. 19104.
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