Ecological effects on morphometric
development of the Indian Eagle Owl Bubo
bengalensis
Satish Pande 1 &
Neelesh Dahanukar 2
1Ela Foundation, C-9, Bhosale Park,
Sahakarnagar-2, Pune, Maharashtra 411009, India
2Indian Institute of Science Education
and Research, Sai Trinity, Garware Circle, Pune, Maharashtra 411021, India
Email: 1 pande.satish@gmail.com,2 n.dahanukar@iiserpune.ac.in (corresponding
author)
Date
of publication (online): 26 April 2011
Date
of publication (print): 26 April 2011
ISSN
0974-7907 (online) | 0974-7893 (print)
Editor: Mario Melletti
Manuscript
details:
Ms # o2609
Received 20 October 2010
Final received 18 February 2011
Finally accepted 21 March 2011
Citation: Pande, S.
& N. Dahanukar (2011). Ecological
effects on morphometric development of the Indian Eagle Owl Bubo bengalensis. Journal of Threatened Taxa 3(4):
1677-1685.
Copyright: © Satish
Pande & Neelesh Dahanukar 2011. Creative Commons Attribution 3.0 Unported
License. JoTT allows unrestricted use of this article in any medium for
non-profit purposes, reproduction and distribution by providing adequate credit
to the authors and the source of publication.
Author Details: Satish Pande is a fellow of the
Maharashtra Academy of Sciences. He is an interventional vascular radiologist and associate professor of
radiology at B.J. Medical College, Pune and post-gradute guide for Radiology.
He conducts research in ecology and field ornithology and has conducted several
surveys. He has made several video films on raptors (eagles, falcons and owls)
ecology, marine ecosystem and conservation. Neelesh Dahanukarworks in ecology and evolutionary biology with an emphasis on mathematical and
statistical analysis.
Author
Contribution: SP conducted field study. ND performed statistical
analysis. Both SP and ND wrote the paper.
Acknowledgements:We thank Amit Pawashe, Kumar Pawar, Dr. M.N. Mahajan, Unmesh Barbhai,
Banda Pednekar, Prashant Deshpande and late Pramod Pawashe for assistance in
field work. Cornelius Mascarenhas checked the English language, Ela Foundation,
Pune supported the study. We thank the Forest Department for their support and
necessary permissions. We thank an anonymous referee for constructive
suggestions on the earlier draft of the manuscript. We are also grateful to Dr. Hemant Ghate and Department of
Environmental Sciences, University of Pune.
Abstract: Univariate analysis based on logistic
growth curve fitting and multivariate analysis using principle component
analysis (PCA) were used to analyze complex patterns and correlations in
morphometric data from 16 individuals of the Indian Eagle Owl Bubo bengalensis from
the Deccan Plateau. Wing chord
length, tarsus length, claw length, beak length, tail length and weight were
measured from hatching until fledging (1-58 days old) . A logistic growth curve
showed a good fit for all characters. Different characters showed different growth patterns according to their
function in the developing nestling. PCA analysis revealed that different morphological characters are
loosely coupled together during growth, and this could be attributed to the
behavioural ecology of nestlings. By comparing the patterns in our data with data published from southern
India, we also show that there is plasticity in the development in these
geographically isolated populations.
Keywords: Bubo bengalensis, development, morphometry, principle
component analysis.
For figures, tables -- click here
INTRODUCTION
Growth rates are subject to selection based on the
ecological and environmental factors. Interspecific variations in growth rates
are often attributed to a trade-off between growth and yield rate in terms of
biomass (Ricklefs 1979; Urban 2007). Fast-growing organisms spend more energy per unit time and thus
contribute to less biomass or offspring size; however, they are vulnerable to
predators for shorter periods. On
the other hand, slow-growing organisms require less energy per unit time and
thereby permit larger family size; however, they are more prone to
predation. Even within a
particular species, there could be different growth patterns, and these could
be related to geographical locations (Caley & Schwarzkopf 2004),
nutritional stress (Negro et al. 1994) and other environmental factors
(Ricklefs 1979; King & Hubbard 1981). It has been previously observed that within the same individual,
different body parts have different rate of growth (Springer 1979; Bortolotti
1984; Kristan et al. 1996; Nagarajan et al. 2002; Penteriani et al. 2005) and
this is often attributed to the compromise between allocation of tissue to
embryonic and mature functions (Ricklefs 1979). There are population variations in growth patterns, and
different body parts also differ in their growth rates. This fact suggests that within the same
species, growth patterns of different body parts in different populations can
differ. This plasticity in the
development is gaining increased attention (Yearsley et al. 2004), as it can
shed light on the ecology of growth and help in understanding stressors in the
conservation of threatened species.
Studies on the development of nestlings, their
ecological interpretations and plasticity in development are relatively rare
for Indian birds. In the current
study we have focused on these aspects of development in the Indian Eagle Owl Bubo bengalensis (Franklin), until recently considered a subspecies of
the Eurasian Eagle Owl Bubo bubo (Linnaeus) but now recognized as a species in its own
right (Wink & Heidrich 1999; Penhallurick 2003). The distribution of the Indian Eagle Owl is restricted to
outer hills of the western Himalayas to about 1500m, and rarely up to 2400m
altitude, and extends from western and central Nepal to the entire Indian
peninsula (Ali & Ripley 1969; Pande et al. 2003). Detailed information is available concering feeding
behaviour (Ramanujam 2006), intimidating behaviour in nestlings (Ramanujam
2003a) and adults (Ramanujam 2004), calling behaviour (Ramanujam 2003b) and
other acoustic and visual traits
(Ramanujam 2007). However, a
detailed account of nestling development is not available, although some
preliminary observations on nesting (Eates 1937), parental care (Dharmakukarsinhji 1940) and
development of the young (Ramanujam & Murugavel 2009) do exist.
In this study we have undertaken a detailed
quantitative analysis of nestling development from hatching to fledging of
Indian Eagle Owls from the Deccan Plateau of India. We have tried to correlate the patterns in development of
different body parts with the ecology of the organism. We have also compared the patterns in
development observed in our study with those observed in the study by Ramanujam
& Murugavel (2009) to better understand the plasticity in development of B. bengalensis in western and southern Indian populations.
METHODS
We studied 10 nests south of Pune (Fig. 1).
Morphometry of 16 nestlings from hatching till fledging at 58 days was
recorded, with data entered serially for each nestling identified by a numbered
aluminium ring placed on the tarsus. At around 25 days of age nestlings leave the nest even when unable to
fly, but despite roosting away from the nest they remain dependent on their
parents for food. Thus it was not
possible to get data from all 16 individuals, and as a result the sample size
decreased after 33 days of age (Table 1) and a total of 319 measurements were
available for each of the six characters, namely, wing chord length (carpal
joint to the tip of the longest primary with the wing in neutral position),
tarsus length (ankle joint to the attachment of toes where measurements were
taken using flexion at proximal and distal joints), tail length (from the root
of tail to the tip by flexing the tail upwards), beak length (the exposed part
of the culmen from the cere to the tip), claw length (middle claw from
insertion to tip) and body mass. We used Vernier calipers (least count 0.001mm), wing-stop and tail
rulers (least count 0.1mm) for measurements and Pesola spring scales (least
count 0.1g) to determine the body mass. Body mass was taken at sunset, allowing the Indian Eagle Owl forages at
dusk or at night, this assured an empty stomach, which minimized the effect of
meals. This also caused minimal
disturbance to the nestling and assured uniformity in methodology.
To each biometric character we fitted a logistic model
to understand its growth pattern and growth rate (Ricklefs 1979). The logistic
equation is:
a
Character value = --------------------------
1 + b . exp (- c . Age)
Where a, b and c are positive constants. Constant a is the maximum possible value of the character,
constant b is the delay in growth associated with the lag phase
and constant c is the growth rate. The goodness of fit was determined by coefficient of
determination, R2.
Univariate analysis based on the logistic regression
was capable of depicting the growth pattern in a given character. However, to understand the simultaneous
development of different characters we used multivariate technique called Principle Component Analysis
(PCA). PCA is a statistical
technique that reduces the dimensionality of the multivariate data while
retaining most of the variation in the data set. It can be used as an effective method to understand the
structure in the data and relationships between various variables. To account for the unit and scale
differences between different morphological characters we used PCA on the
correlation matrix of the variables. We performed Bartlett’s sphericity test with the null hypothesis that
there is no correlation significantly different from zero between the variables
and alternative hypothesis that at least one of the correlations between the
variables is significantly different from zero (Harris 2001). Correlation biplot was plotted to
visualize PCA results (Legendre & Legendre 1998). All
statistical analysis were performed in Statistica 10® and figures were
prepared in Microsoft EXCEL 2003® and CorelDraw X4®.
In the current study we have applied PCA in a
different manner than what has been already suggested. Research focusing on the
evolution of ontogenic patterns and understanding the allometric relationships
in growth have often used modified PCA using covariance matrix for each age
group separately so as to remove the effect of size and shape from the final
analysis (Anderson 1963; Klingenberg 1996; Badyaev & Martin 2000). Even though these techniques are more
robust to the scale differences they are mathematically rigorous and relatively
difficult to interpret. On the
other hand we have used the PCA technique for a different purpose. We have used PCA and the resulting
biplot simply as a convenient way to understand the simultaneous effect of
different variables on the growth pattern. To nullify the size and scale effect we have used PCA on the
correlation matrix rather than the covariance matrix as suggested by Sommers
(1986). An important reason why we
do not use the alternate PCA method is that when comparing the growth patterns
in our study with the previous study by Ramanujam & Murugavel (2009) we
only have the information about the mean value of the character at a given age. As a result PCA method suggested by
Anderson (1963), Klingenberg (1996) and Badyaev & Martin (2000) cannot be
used for the data provided in Ramanujam & Murugavel (2009).
RESULTS AND DISCUSSION
Average value of various morphometric characters at
different ages are given in Table 1. The plots of character value against age (Fig. 2) showed good fit to the
logistic growth curve equation (all regressions were significant at p <
0.001). The parameters for the
logistic growth model are given in Table 2, where we observe that the growth
rates of different morphological characters increase in the ascending order
from beak, tail, tarsus, wing, claw to weight. Growth patterns of Indian Eagle
Owl are comparable to the growth patterns observed for other raptors (Springer
1979; Bortolotti 1984; Kristan et al. 1996; Nagarajan et al. 2002; Penteriani
et al. 2005), but there are subtle differences which could be attributed to the
ecology of Indian Eagle Owl.
Beak length was about 40% of its asymptotic value at
hatching. This could be because of
the possible role of the beak in breaking the egg shell. Beak underwent less lag phase and
increased rapidly till 20 days of age and then its growth slowed down. At hatching, tarsus was about 20% of
its asymptotic value. It underwent
a lag phase for first four days after hatching and then it increased rapidly
till about 30 days of age and then its growth slowed down. Claws were completely absent at birth
but they appeared in two to four days. Their growth followed short lag till first five days then they grew very
rapidly till 20 days of age after which their growth slowed down. Rapid growth and early maturation of
above three characters, namely beak, tarsus and claw, reflects their early
functioning in nestling development. As the ground dwelling nestlings desert the nest by walking out of the
nest at about 25 days of age and roost away from the nest, the early
development of tarsi is essential for its survival.
At hatching, wing length was about 6% of its
asymptotic length and it underwent a long lag phase till about 25 days of age
after which it grew rapidly till fledging. Tail was completely absent at
hatching and it also went a long lag phase of growth for about first 30 days
after which it grew rapidly till fledging. At hatching the weight was about 4% of the asymptotic
weight. It underwent some lag phase in growth for first 11 days after which it
grew rapidly till 30 days of age and then the growth rate decreased. For the weight, even though logistic
growth curve shows a good fit, there is a sudden break in the growth pattern at
about 20 days of age (Fig. 2f). This sudden decrease in the weight could be attributed to the stress
faced by the nestling, which deserts the nest at this age, and roosts away from
it.
PCA could depict the complex patterns of morphological
changes with growth. PCA extracted
only one significant factor, with eigenvalue more than unity, which explained
94.90% of the total variability in the data. Second factor had an eigenvalue 0.212 and it explained 3.56%
of the total variation in the data. Together, the first two factors explained 98.46% of the total
variability in the data. Bartlett’s sphericity test suggested that the correlation between
variables was significantly different from zero (c2 =
4905.778, df = 15, p < 0.0001). Correlation biplot of PCA is given in Fig.
2. On the first PCA factor, the
scores of observations increased with age indicating that the first factor
depicted overall increase in the size. This was further supported by positive factor loading on F1 axis for all
different morphological variables indicating all characters increased in size
with age. On the second factor,
however, both factor scores for observations and different variables showed positive
and negative factor loading indicating that different morphological characters
showed different growth patterns.
We could see that claw and beak growth were coupled
together and their growth was rapid in early days of the development. Both the characters had short lag
period and they grew rapidly till 20 to 25 days of age after which their growth
rate decreased. Both characters are essential during the early development of
the nestlings. While the beak is
essential for breaking of the egg shell and during feeding, claws are essential
for defence during nestling competition, thus coupled growth of these
characters could be justified. Growth of tarsus and weight were loosely coupled
together and they had slightly more lag phase than beak and claw. Tarsus and weight grew rapidly up to 25
to 30 days of age and then they grew very slowly. Coupled growth of tarsus and weight can be attributed to the
behavioural ecology of Indian Eagle Owl. The nest of Indian Eagle Owl is made on the ground and we observed that
after 20 to 25 days of age the nestling leaves the nest by walking out. This explains why tarsus growth is
rapid till 20 to 25 days of age. The coupling of increased weight with tarsus length perhaps enable the
nestling to move from place to place by walking, because during this period
nestlings cannot fly. During this
phase, the nestling is still dependent on the parents for food and it is
stressed. After a long period of
lag, wing and tail growth starts. These two characters are coupled together and it is obvious because both
the wing and tail are required for flight. The differential pattern in development of the tarsus and
wing depicts an effective method of resource allocation for growth. Nestling Eagle Owl leaves the nest
before it can fly. Therefore,
tarsus, which is required for walking, develops rapidly before wings within the
first 25 days, while wing development shows a long lag phase of about 25 days
after which it starts growing rapidly.
In the above arguments we focused on the ecological
effects on differential growth patterns in different morphological characters
of Indian Eagle Owl. Even though
we justified our findings with the observed ecology of the bird it is likely
that the same species inhabiting different environments may have different
patterns in growth. To check out
whether such plasticity exists in development of the Indian Eagle Owl we
compared the findings of our study, a western Indian population of Indian Eagle
Owl from Deccan plateau, with the study by Ramanujam & Murugavel (2009), a
southern Indian population of Indian Eagle Owl from coastal region. This
comparison, however, should be taken with caution because Ramanujam &
Murugavel’s (2009) study is preliminary and has a smaller sample size. Nevertheless, there are some
interesting findings emerging from this comparison which can be explored
further.
Comparison of logistic growth curve parameters for
both the studies is given in Table 2. All the morphological characters had smaller growth rate and less lag
phase in southern Indian population than the western Indian population. To understand whether the growth rates
affect the size at fledging we compared different morphological characters
using unpaired t test assuming unequal variance. Except for beak length, which was marginally larger in the
western Indian population (t = 13.1025, p = 0.0485), no other character, namely
tarsus, wing and weight, differed significantly between the two populations
(tail was not measured in the southern population). The asymptotic weight of southern Indian population was
higher than that of western Indian population (ca. 19% larger). This finding coupled with the fact that
growth rate of weight was lesser in southern Indian population than in western
Indian population, possibly reflects the growth rate versus yield tradeoff,
which suggests that higher growth rate is coupled with lower yield and vice
versa (Gadgil & Bossert 1970). This trade off is an outcome of natural selection acting on partitioning
the resources either to increase growth rate or yield but not both (Gadgil
& Bossert 1970). An
interesting outcome of this comparison is that even though the growth rates of
characters in southern Indian population were lower than the western Indian
population, both achieved maturity at same time, and this could be attributed
to the smaller lag phases in southern Indian population.
A more direct comparison can be done based on the PCA
analysis of growth (Fig. 4). To
keep minimum discrepancies in comparisons we considered only a subset of our
data from 10 days onwards. For both
populations, PCA was done on mean values of the characters as actual data was
not available for Ramanujam & Murugavel (2009). Similar to the western Indian population, southern Indian
population showed correlated growth among tarsus and weight. However, the pattern in growth for wing
and beak was different. Unlike in
the western Indian population, the beak length, in southern Indian population,
increased till fledging, while wing grew along with tarsus and weight, with
relatively shorter lag period than in the western Indian population. This has a significant contribution on
the behavioural ecology of the nestling and explains the development plasticity
in the two populations.
Behaviour of the nestling regarding the nest
abandonment prior to gaining the ability of flight is an important stage in the
life of several owl nestlings (Duncan 2003; Austing & Holt 1966). In the western Indian population, we
observed that between 23 and 28 days from hatching the chicks abandon the nest
and move a few meters away from it which could be possibly attributed to the
adaptive strategy of the nestling to escape predation from ground predators and
avoid the poor nest hygiene. Dharamkumarsinhaji’s (1940) bewildering experience of mysterious
disappearance of the Indian Eagle Owl chick around 23rd day in his
observation from Saurashtra could be the same phenomenon which points out to
the fact that the age at which the nestling deserts the nest is same. Surprisingly, in the southern Indian
population, the nestlings leave the nest much later on 35 days of age
(Ramanujam & Murugavel 2009). Furthermore, we observed that since the wing development in western
Indian populations starts rapidly only at the age of 25 days, the nestling that
deserts the nest at 25 days of age cannot fly at all. They fly only from the
age of 58 days. This is also
consistent with the observations made on Great Horned Owl Bubo virginianus, which leaves the nest around 21 days of age but can
fly only at the age of 60 days (Austing & Holt 1966). Surprisingly, in the southern Indian
population, as the lag phase of wing growth is less (Table 2), the nestling
that deserts the nest around 35 days of age is capable of gliding (Ramanujam
& Murugavel 2009). These
differences between the western Indian and southern Indian populations reflect
the plasticity in development of the Indian Eagle Owl.
Even though it is difficult to pinpoint the exact
reasons for the differences in the growth patterns in western and southern
Indian populations, habitat characteristics and food availability may be
playing an important role. Ramanujam & Murugavel (2009) have stated that their study area is an
environmental disaster with severe habitat degradation. On the contrary, our study area in the
western India is relatively undisturbed with rocky areas, grasslands and
agricultural fields that sustain high rodent populations, which is the
preferred prey of the Indian Eagle Owl (Ramanujam 2006). Such constraint on the availability of
energy to the nestling is considered as a major limiting factor for its growth
(Ricklefs 1984).
In conclusion, in this study we have given a detailed
quantitative account of growth patterns in different morphological characters
of Indian Eagle Owl. We also tried
to correlate the growth patterns with relevant ecological observations. We further showed that growth patterns
in southern Indian and western Indian populations vary suggesting that there is
plasticity in the development of this owl. However, our reasoning of ecological effects on growth is
still limited because we have not considered other factors like predation,
population size and density (Ricklefs 1984) that may have profound effects on
growth and growth rate.
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