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Inferences from bowhead whale ovarian and pregnancy data: age
estimates, length at sexual maturity and ovulation rates
J.C. GEORGE1, E. FOLLMANN2, J. ZEH3, M. SOUSA2, R. TARPLEY4, AND R. SUYDAM1
1. Department of Wildlife Management, Barrow, AK
2. University of Alaska Fairbanks, Fairbanks, AK
3. University of Washington, Department of Statistics, Box 354322, Seattle, WA, 98195-4322
4. School of Veterinary Medicine, St. George's University, Grenada, West Indies
Contact email: [email protected]
ABSTRACT
We used life history and reproductive data (number of corpora in both ovaries) to estimate mean ovulation rate,
length at sexual maturity, number of ova per estrous cycle, and age. For this analysis, we define ovulation as the
number of ‘readable’ corpora formed per year in both ovaries. We used data archive bh.corpora which included
data for 86 female bowhead whales, 75 with both ovaries examined. Of these 75, 35 were immature (0 corpora
albicantia (CA), 0 corpora lutea (CL)) and 40 were mature (at least 1 CA or CL). Corpora counted in a single ovary
ranged from 0 to 22, and 1 to 41 in both ovaries for mature females with both. Using logistic regression and
including data from bh.reproduction, we estimated length at maturity (females) to be 13.41 m. While no ovaries in
our sample had more than 1 CL, diameters of CAs in Tarpley and Hillmann (1999) suggest multiple ovulation is
possible, and was estimated to be ~1.13 corpora/estrous based on their data. To estimate ovulation rate we used data
from Barrow and Kaktovik where most whales are carefully examined for pregnancy and maturity. These examined
whales have known probability of being mature: 0 for immature and 1 for mature females. Since not all females are
examined for maturity, we estimated the probability that the unexamined females were mature as a function of body
length using data from bh.individual_whale and the logistic regression results. The denominator of the ovulation rate
estimate is the sum of the probabilities of being mature and the numerator is the number of females either pregnant
or having a CL. The estimated ovulation rate was 0.368/yr for an ovulation interval of 2.7yr. Estimates of ages for
the 40 mature females (with both ovaries available) were computed from CA counts, using the estimates of age at
sexual maturity, number of ova released per estrous and ovulation rate. Corpora age estimates are consistent with
those of George et al. (1999) and Rosa et al. (2004) using the aspartic acid racemization (AAR) technique. A
regression of AAR age on ‘corpora age’ results in an R2 value of 0.66. A problem with corpora age estimates is, of
course, that they cannot be calculated for males or immature whales. In contrast to AAR age estimates in George et
al. (1999) and Rosa et al. (2004), which lack very old females, these data suggest that some females may live nearly
as long as males. Of interest is whale 92B2 which was not used in this analysis since only one ovary was recovered,
but her single ovary held 20 corpora. This whale also had a stone implement lodged in the dorsal blubber, suggesting
she was very old (George et al., 1999). Estimated standard errors of the corpora ages are lower than those for AAR
ages. An attractive aspect of the corpora ageing technique is that corpora counts are relatively easy to do and there
is relatively little uncertainty in them. Our results suggest that CA counts give a reasonable estimate of age, past
pregnancies, and an upper bound for lifetime calf production.
KEYWORDS: BOWHEAD WHALE, REPRODUCTION, AGE ESTIMATION, OVULATION, CORPORA
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INTRODUCTION
The female reproductive system of placental mammals is a highly derived character that is unique to Class
Mammalia. Many other vertebrates are oviparous (lay eggs) but only Prototherian mammals (e.g., the duck billed
platypus) do this following internal fertilization. Young mammals develop within the uterus, are nourished via the
placenta and are born in various states of development. In the case of cetaceans, calves are anatomically and
physiologically prepared to cope with the rigors of life in ice-covered seas (precocial). However, most neonate
mammals are altritial requiring considerable parental care (Vaughan et al., 2000).
In adult mammals, ova develop within ovarian follicles, and are released when the follicle ruptures during
estrus. The follicles then transform into a corpus luteum (CL). If pregnancy occurs, the CL maintains the
pregnancy through hormone secretions, principally progesterone. Following pregnancy, or if pregnancy fails, the
CL regresses into a corpus albicans (CA). The corpus albicans is composed of fibrous scar tissue (Tarpley and
Hillmann, 1999) and in some mammalian orders, such as Cetacea, these appear to be retained in the ovary leaving a
“record” of ovulation.
The reproductive cycle of the bowhead is unclear, however, some aspects are known. Based on fetus
recoveries, conception likely occurs in March with birth about 14 months later (Reese et al., 2001). A single calf is
born the following spring (late April to early June) with a mode in late May. The calf is presumably nursed for less
than a year based on examinations of whales believed to be a year old (ingutuks). Relatively short lactation (~9
months) is characteristic of mysticete whales (Costa and Williams, 1999). Calving intervals are believed to be
about 3-4 years in length (Miller et al., 1992; Rugh et al., 1992; Koski et al., 1993).
If corpora are persistent in the ovary, then they offer a record of ovulation for a female. Early researchers
examining large samples of whales taken commercially suggested they were, in fact, persistent (Tarpley and
Hillmann, 1999). However, additional problems of interpretation exist. Questions that remain unresolved for
whales are 1) whether ovulation is induced or spontaneous, 2) the number of ova released during an estrus cycle, and
3) how many ovulations do not lead to fertilization and/or implantation. Uterine scars from pregnancies do not form
in cetaceans because of the epitheliochorial type of placental attachment (Vaughn et al., 2000).
Tarpley and Hillmann (1999) carefully assessed the diameter, regression, and persistence of 257 corpora.
CAs ranged in diameter from 6.3 cm to 0.3 cm. Histograms of CA diameter indicated a normal distribution with a
rather abrupt size break at about 0.5 cm. This is either evidence of maximum regression or sudden absorption, and
conclusions from Tarpley and Hillmann (1999) were tentative. However, based on a qualitative analysis of the
distribution of 41 CAs from whale 89B3, a very large female, they suggested that corpora were persistent (at least
for this animal).
Nerini et al. (1984) conducted some of the early investigations of corpora counts in bowhead whale
ovaries. Not surprisingly, she did not find a strong correlation between whale length and corpora number, since the
variation in age at length for mature bowheads is considerable.
To estimate age from corpora counts, several types of data are required and assumptions must be made.
These include:
i.
Corpora are persistent, or disappear at some known rate. In this analysis we assume they are
persistent.
ii.
Multiple ovulations during estrous must be quantified. An estimate of how often estrous occurs must
be obtained.
iii.
The average age at sexual maturity must be estimated.
We discuss these assumptions and data requirements in the text at some detail.
Based on the above discussion, the basic objectives of this paper are to:
i)
assemble all corpora count data into a database by whale identification number
ii)
test the possibility of using corpora counts to estimate the age of bowhead whales.
METHODS
We used new and published reproductive and life history data to estimate several statistics. These include: the mean
ovulation rate, the number of corpora in both ovaries, length at sexual maturity, age at sexual maturity and number
of ova per ovulation event. Throughout this paper, the terms ‘mature’ and ‘maturity’ refer to sexual maturity.
Bowheads likely reach physical maturity at a greater length and older age than sexual maturity (George et al., 1999).
For this analysis, we define ovulation rate as the number of ‘readable’ corpora formed per year in both ovaries.
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Corpora counts
We followed methods of Tarpley and Hillmann (1999) to prepare and ‘read’ the ovaries. After fixing in 10%
formalin, ovaries were sliced in 5 mm sections and the numbers of CLs and CAs were counted. The approximate
diameter of each CL was noted as well. Only whales for which both ovaries were examined were used to estimate
age, but the presence of a CL or CA in a single ovary defined a female as mature.
Length and age at sexual maturity
We used binary logistic regression to estimate the length at maturity. The data archives bh.corpora and
bh.reproduction provided data on females known to be either immature or mature on the basis of corpora counts,
ovary size or pregnancy. We scored whales as mature (1) based on the presence of corpora or a fetus or immature
(0) if these were absent. One whale (79WW1) was scored as mature in the absence of corpora data because her
ovaries were extremely large (13kg). If only one ovary was examined and no corpora were found, we did not
classify the whale as immature and include it in the analysis unless it was very small; e.g. 84S2 (14.4m) was not
classified, but 02B5 (8.5m) was treated as immature. The logistic regression model is:
⎛ p ⎞
⎟⎟ = β 0 + β 1 × BL
log⎜⎜
⎝1− p ⎠
where log is the natural logarithm, p is the probability that a female bowhead with body length BL is sexually
mature, and β0 and β1 are the parameters to be estimated. Given the parameters, the length LSM at which the
probability is 0.5 that the whale is mature can easily be estimated. Since p = 0.5, p/(1 – p) = 1 and log(1) = 0.
Therefore
LSM =
− β0
β1
.
The estimated probability that a female bowhead with body length BL is mature is
Pr(mature|BL) = exp( β 0 + β 1 × BL ) / [1 + exp( β 0 + β 1 × BL )].
To determine ASM, the mean age at sexual maturity, we compute the mean of ages estimated from aspartic
acid racemization data in the bh.aspartic_age data archive (George et al., 1999; Rosa et al., 2004). We include
females with lengths at which, according to Pr(mature|BL), there is a 2% or better chance that sexual maturity is
reached. However, we omit whales in this size range if they are known from corpora counts to be well past the age
at sexual maturity, and we adjust ages of whales with only one CA by subtracting the ovulation interval. The
ovulation interval (yr) is computed as 1/OR, where OR is the “ovulation rate” defined earlier. Note that our use of
the term ovulation rate differs slightly from other studies, and we assume that ovulations (and pregnancies) result in
a readable CA. We estimate V(ASM), the variance of ASM, by the sample variance of the ages from which ASM was
estimated.
Ovulation rate
A crude estimate of ovulation rate (yr-1) (OR) can be obtained by dividing the number of females with a CL or fetus
by the number of mature females. We used whales from fall harvests at Barrow and Kaktovik for this calculation
since whales from these villages were most consistently examined by biologists. In addition, there is a higher
probability of missing a small spring fetus than a larger fall fetus. Since not all females are examined for maturity,
we estimated Pr(mature|BL) as described in the previous section and used it in the following manner:
OR =
∑ pf
∑ mf
where the sums are over harvested potentially mature females; pf = 1 if the harvested female has a CL or fetus, pf =
0 otherwise; and mf = the probability that the harvested female is mature. We treat females 12m or more in length
as potentially mature; the shortest female found to date with a CL or fetus was 12.6m long (whale 99B6). The
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longest female verified to be immature was 14.2m long. We therefore set mf = 1 for whales >15m long, as well as
for those known to be mature from corpora or pregnancy data. For females 12-15m long not known to be mature, mf
= Pr(mature|BL). Since OR can be viewed as the probability that a mature whale ovulates in a given year,
Pr(ovulation) = OR × Pr(mature), so this way of calculating mf gives the correct weight to potentially mature whales
whose status is uncertain, all of whom contribute pf = 0 to the numerator. We estimate the variance of OR by
V (OR) = OR × (1 − OR )
∑ mf .
Number of ova per estrous
Plots of CA diameters in Tarpley and Hillmann (1999) were examined to estimate the mean number of ova per
estrous cycle. If the largest and presumably most recent corpora from the same ovary had the same diameter, it was
assumed that they represented multiple ova from the same estrous n event. If there was a unique largest corpora, we
assumed that it represented a single ovulation for that year. In either case, if the mean number of ova released, AR,
is greater than one, then corpora counts must be adjusted downwards accordingly as described below. The variance
of AR was estimated as the square of the standard error of the mean.
Ages estimated from corpora for mature whales
The estimated age of the whale is
age = ASM + TCA×1/(AR×OR)
where ASM = mean age at sexual maturity, TCA = total CAs counted from both ovaries, AR = mean number of ova
released per ovulation event, and OR = ovulation rate. If corpora are counted without error, an estimated variance
of the age estimate (derived by the delta method) is:
V(age) = V(ASM) + [TCA/(AR×PR)2]2 × [PR2×V(AR) + AR2×V(PR) – V(AR)×V(PR)].
We use only CA in computing the age estimate. This is because we define maturity by the presence of
corpora or a fetus. So the year a female attains sexual maturity, she should have exactly 1 CL and/or early (not
term) fetus, and her age is estimated by ASM (Fig. 1). Now suppose she has 1 CL and 1 or 2 CAs. Then she has just
1 or 2 ovulation intervals to add to ASM. And so on. Now suppose she has no CL, but 1 CA. Then she reached
sexual maturity some fraction of an ovulation interval ago, so the first CA , if there is no CL, should only contribute
a fraction of an ovulation interval. However, to simplify, we give all CAs the same weight. As we will see below,
the uncertainty about the interval represented by the first CA is a minor source of uncertainty compared to other
sources accounted for in V(age).
We also assume that the corpora can be counted with negligible error. This assumption is discussed later.
Comparisons with aspartic acid age estimates
Some of the whales examined had age independently estimated using the aspartic acid racemization (AAR)
technique (George et al., 1999; Rosa et al., 2004). These age estimates were regressed against the number of
corpora as a means of estimating ovulation rates. We also compared AAR ages with the ages estimated from
corpora counts.
RESULTS and DISCUSSION
Corpora counts
The data archive bh.corpora included data on 86 female bowhead whales. Corpora counted in a single ovary ranged
from 0 to 22. There was no significant difference in number of corpora in the right versus left ovary among the
mature whales (P-value = 0.3, paired t-test), but the magnitude of the difference ranged from 0 to 9. Therefore,
except for the length at maturity analysis, we restricted our analyses to the 75 whales that had both ovaries examined
for corpora. Of these 75, 35 were immature (0 CA, 0 CL) and 40 were mature (at least 1 CA or CL).
The distributions of both CA and CA+CL for the mature whales with both ovaries examined were highly
skewed. Although 2 whales with only one ovary examined had counts of 20 and 22 CA respectively, only 4 of the
40 whales with both ovaries examined had 18 or more total corpora. Basic statistics are shown in Table 1 and the
distribution of total corpora in Fig. 2.
None of the ovaries had more than one CL.
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Length and age at maturity
From the 86 females in the bh.corpora archive and 37 potentially pregnant females from the bh.reproduction
archive, we assembled a data set with 98 females known to be either mature or immature. The smallest known
mature female was whale 99B6, a 12.6m female early in her pregnancy. The largest female known to be immature
was whale 83B2, 14.2m. The 35 immatures included 6 whales between 13 and 13.9 m, all the rest were < 12.3 m.
The results of the logistic regression were β0= -32.840, β1 = 2.448 (Table 2). The estimated length at which
the probability is 0.5 that the whale is mature is LSM = 13.41m. Pr(mature|BL) in the range of lengths in which over
95% of the whales likely reach maturity ranges from 0.03 at BL = 12m to 0.98 at BL = 15m (Fig 3).
The increase in Pr(mature|BL) over Pr(mature|BL-0.1m) is 0.016 or more from BL = 12.4 through BL =
14.5 and is <0.015 outside that range, suggesting that around 2% or more of females reach maturity with each
increase of 0.1m in length within that range. This range, not surprisingly, corresponds well to the range within
which the smallest known mature and largest immature female fall. To estimate age at sexual maturity (ASM), we
therefore use ages determined by the aspartic acid racemization technique for females in this size range.
The only such whales in the bh.aspartic_age archive are 96B4, 96B6, 96B10, 99B6, 99B18 and 00B2. Of
these whales, we know from corpora counts that 96B4 (10CA) and 00B2 (5 CA) are well past ASM and therefore
should be omitted. The remaining whales can be used: 99B6 can reasonably be assumed to be newly mature, 99B18
has a CA and a CL so is at least one ovulation interval past sexual maturity, and the remaining two whales are of
unknown maturity status. Ages computed from the two D/L ratio measurements available for 99B18 differ as much
from each other as they do from the estimates for the other whales because of D/L ratio measurement error (Rosa et
al., 2004). We therefore use both age estimates for this whale along with one age for each of the three other whales
in estimating ASM and V(ASM). The mean of the ages is ASM = 24.4 with sample variance V(ASM) = 26.7,
corresponding to SD(ASM) = 5.2. Another method of estimating ASM (and its SD) is baleen ages (Lubetkin, et al
2004).
Estimated LSM = 13.41m is quite consistent with other estimates. Koski et al. (1993) estimated female
length at sexual maturity as 13-13.5m from photogrammetric data. Because of stretching when whales are landed
(George et al., 2004), we might expect estimates from harvest data to be longer. On the other hand,
photogrammetric estimates depend on seeing a cow with a calf, and estimates based on corpora counts do not
require a successful pregnancy, only an ovulation. It may be that miscarriages and/or neonatal mortality are higher
among the smallest/youngest mature females; hence smaller whales may be detected as mature in the harvest sample
than in the photogrammetry sample.
Ovulation rate and mean number of ova per ovulation event
In the bh.individual_whale archive, there were 39 females > 12m, harvested on known dates in the fall (August
through October) at Barrow or Kaktovik between 1976 and 2003. We restricted attention to those years because
only in those years was it reasonable to assume that all females landed were carefully examined for evidence of
ovulation and/or pregnancy. Two of these whales were known from corpora data to be immature and were not
considered further. Of the remaining 37, 21 were known to be mature from corpora or pregnancy data, 3 were
assumed mature because their lengths were >15m, and the remaining 13 had mf set to Pr(mature|BL) in the
denominator of OR. The number of mature females in the denominator was estimated to be 28.54. Among the 21
known mature whales, 10 were known to be pregnant and/or had a CL observed and 1 could not be conclusively
identified as pregnant or with a CL. In the numerator of OR, that whale, 76B20, was assigned pf = 0.5 instead of pf
= 1. The resulting estimated ovulation rate was OR = 10.5/28.54 = 0.368 with estimated V(PR) = 0.0081,
corresponding to SE(PR) = 0.090. The ovulation interval was estimated to be 1/0.368 = 2.7yr.
Based on examination of plots in Tarpley and Hillmann (1999), of the largest and probably most recent
corpora from the same ovary, multiple ovulations may have occurred in 4 of 38 ovulation events (38 ovaries). The
maximum was 3 CAs for whale 82WW1. The mean number of ova released per event was AR = 1.13. If this is
representative of multiple ovulations, then corpora counts must be adjusted downwards accordingly as described
below. The variance of AR was estimated to be V(AR) = 0.00451, corresponding to standard error SE(AR) = 0.067.
In some cases, CAs from different were close in size, so we may have underestimated OR to some extent.
Ovulation rates estimated from landed whales have several potential biases. Biases could result from: i)
failure to detect CL or early pregnancies, ii) difficulties in determining if females are mature, and iii) failure to
account for mature females that were NOT harvested because they were accompanied by a calf. These biases can be
minimized considerably if only fall animals are used – but not eliminated. In fall, fetus size has consistently been
about 1.5m which is relatively easy for a biologist or hunter to detect. Also, mothers do not always swim closely
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with their calves or may have lost their calf, and, at times, may not be avoided by hunters. There are a couple of
examples in the fall hunt (Tarpley and Hillmann, 1999) in which lactating females were taken accidentally. On the
other hand, some calves appear to remain with their mothers for approximately 10 months and so, some avoidance
of mothers with calves is likely during the fall harvest as well. Also, mothers with calves avoid nearshore waters
less than 20 m deep (Koski and Miller, 2004) and that habitat preference may introduce a slight negative bias to the
fall harvest in the proportion of females with calves. This might produce a slight upward bias in the
ovulation/pregnancy rate estimate.
Corpora counts seemed relatively low in our dataset, with a median of 9 per animal. It could be that most
female bowheads in the BCBS population have had less than 10 calves in their lifetime. However, four females had
over 20 corpora suggesting that either some females are quite old, that fecundity is highly disproportionate between
females, or both.
There were no whales observed with more than one corpus luteum. This suggests either that the release of
multiple ova is extremely rare or that only one develops into a CL during pregnancy. Nerini et al., (1984) reported
that one bowhead had two active CLs, and we know of one observation by Eskimo hunters of twin calves; but no
bowheads have been observed with twin calves in any aerial or ice-based survey. Still, the possibility of multiple
ovulations within a year exists. This might happen if, say, an early pregnancy fails.
We have assumed that the corpora can be counted with negligible error. However, a small experiment with
two people counting the corpora from the same whale independently should be conducted to verify this.
Corpora age estimates
Estimates of ages for the 40 mature females were computed from CA counts, using the estimates given above for
ASM, AR and OR. They are listed in Table 3 with their standard errors and shown against body length in Fig. 4.
The corpora age estimates are consistent with those of George et al. (1999) and Rosa et al. (2004) using the
AAR technique. A problem with corpora age estimates is, of course, that they cannot be calculated for immature
whales. Since ASM was estimated from AAR ages, we expect positive correlation between corpora and AAR ages
among the younger females. However, the oldest female ages estimated from corpora data were >100yr, as were
AAR ages for the oldest males in Rosa et al. (2004). Whale 92B2 was not used in this analysis since only one
ovary was recovered, but her single ovary had 20 corpora, so the total could well be ~40. This whale also had a
stone implement lodged in the dorsal blubber, suggesting she was very old (George et al., 1999). In contrast to
AAR age estimates in George et al. (1999) and Rosa et al. (2004), which lack very old females, the corpora data
suggest that some females may live nearly as long as males.
Our age estimates are sensitive to the estimated ovulation rate and interval, which are intern sensitive to the
length at sexual maturity (LSM). Estimates of LSM will become more precise as more intermediated sized whales
are examined for maturity.
Correlations with aspartic acid ages
Results of a regression of AAR age on ‘corpora age’ for eight females with both are shown in Fig 5. This depends
on which age is used for whale 99B7. Using the L2 value of 27yr from Appendix A of Rosa et al. (2004), the R2
value is 0.66 between the two ageing techniques. Using an age of 71yr, the L1 value, gives an R2 of 0.21. By either
measure, our results suggest that corpora counts are useful for ageing bowhead whales. It should be noted that the
SEs are lower for the ovulation ages than AAR ages.
An attractive aspect of this ageing technique is that corpora counts are relatively easy to do and there is
very little uncertainty in the corpora counts. The calving interval, while still uncertain, may not introduce error of
the magnitude noted in the AAR method.
Regressing corpora counts on aspartic acid age estimates suggests an ovulation rate of 0.311/yr, which,
considering the large errors in the AAR ages, agrees reasonably well with our more direct estimate of 0.37.
Do corpora counts represent pregnancies? Most likely. Based on several lines of evidence: our results,
the polyandrous mating system of Balaenids, and the long periods between reproductive events, it seems likely that a
receptive female would become pregnant during estrous. Some females will undoubtedly fail to become pregnant;
however, the CA counts probably give a reasonable estimate of past pregnancies.
Do pregnancies represent calf production? Some portion of these pregnancies will undoubtedly fail;
nonetheless, CA counts give an upper bound for lifetime calf production. Furthermore, because the number of
corpora is relatively small, it makes sense that many of these must be successful births or the BCBS stock would not
be increasing at its current estimated rate.
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ACKNOWLEDGEMENTS
We thank the Alaska Eskimo Whaling Commission (AEWC) and the Barrow Whaling Captains’ Association for
their confidence, guidance and support of our research. The postmortem examinations that we conduct on landed
whales often interfere with the butchering process. The whale hunters’ patience with us has been enormous. We
appreciate the field assistance of Dave Ramey, Victoria Woshner, Cheryl Rosa, Todd O’Hara, Matt Irinaga, Paul
Nader, Benny Akootchook, Cyd Hanns and many others; and the lab assistance of Thorsten Bentzen and Lara Dehn.
We recognize Mayor George N. Ahmaogak, Sr., and Dr. Thomas Albert, former Senior Scientist; Taqulik Hepa,
Deputy Director; and Charles D. N. Brower, Director of the North Slope Borough Department of Wildlife
Management for their steadfast support. We gratefully acknowledge funding provided by the North Slope Borough
Department of Wildlife Management and National Oceanic and Atmospheric Administration (through the AEWC).
Lisa Delarosa, Dolores Vinas, and April Brower provided office assistance.
REFERENCES
Costa, D.P, and Williams, T.M. 1999. Marine Mammal Energetics. Biology of Marine Mammals. Smithsonian.
George, J.C., Bada, J., Zeh, J., Scott, L., Brown, S., O’Hara, T. and Suydam, R. 1999. Age and growth estimates of
bowhead whales (Balaena mysticetus) via aspartic acid racemization. Canadian Journal of Zoology. 77:571-80.
George, C., Koski, B., Rugh, D. 2004b. Body stretching of bowhead whales during hauling and butchering during
the subsistence hunt. SC/56/BRG9.
Koski, W.R. and G.W. Miller. 2004. Habitat selection by different size classes of bowhead whales in the central
Beaufort Sea during late summer and autumn. (unpublished manuscript).
Koski, W.R, Davis, R.A., Miller, G.W. and Withrow, D.E. 1993. Reproduction. pp. 239-69. In: J.J. Burns, J. J.
Montague and C.J. Cowles (eds.) The Bowhead Whale. Special publication No. 2 of the Society of Marine
Mammalogy. i-xxxvi + 787pp.
Lubetkin, S., Zeh, J., Rosa, C., and George, J.C. 2004. Deriving von Bertalanffy age-length relationships for
bowhead whales (Balaena mysticetus) using a synthesis of age estimation techniques. SC/56/BRG3.
Miller, G. W., Davis, R.A., Koski, W.R., Crone, M.J., Rugh, D.J., Withrow, D.E. and Fraker, M.A. 1992. Calving
intervals of bowhead whales: an analysis of photographic data. Rep. int. Whal. Commn 42:501-6.
Nerini, M.K., Braham, H.W., Marquette, W.M. and Rugh, D.J. 1984. Life history of the bowhead whale, Balaena
mysticetus (Mammalia: Cetacea). J. Zool., London 204:443-68.
Reese, C.S., Calvin, J.A., George, J.C. and Tarpley, R.J. 2001. Estimation of fetal growth and gestation in bowhead
whales. J. Am. Stat. Assoc. 96:915-23.
Rosa, C., George, J.C., Zeh, J., O’Hara, T. Botta, O. and Bada, J. 2004. Update on age estimation of bowhead
whales using aspartic acid racemization. Paper SC/56/BRG6.
Rugh, D.J., Miller, G.W., Withrow, D.E. and Koski, W.R. 1992. Calving intervals of bowhead whales established
through photographic identifications. J. Mamm. 73 (3):487-490.
Tarpley, R.J. and Hillmann, D.J. 1999. Observations on ovary morphology, fetal size and functional correlates in
the bowhead whale Balaena mysticetus. Final Report to the Department of Wildlife Management, North Slope
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Vaughan, T.A., Ryan J.M., Czaplewski, N.J. 2000. Saunders College Publishing, Orlando, FL. 565 pp. +
Appendices.
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Table 1
Basic corpora count statistics for mature whales with both ovaries examined, N= 40. The mode for Total CA is NA
because counts of 1, 5, 6, 9 and 12 were each seen in 4 whales, other counts in fewer whales.
Statistic
Mean
SD
Minimum
Mode
25th percentile
Median
75th percentile
Maximum
Total CA
10.2
8.7
1
NA
5
9
12
41
CA+CL
10.7
8.7
2
2
5
9
12.5
41
Table 2
Parameters from logistic regression of maturity status on body length (BL) to estimate Pr(mature|BL).
Parameter
β0
β1
Value
-32.840
2.448
SE
9.404
0.683
T-value
-3.492
3.584
8
SC/56/BRG8
Table 3
Estimated “ovulation” ages for mature female bowhead whales using corpora data. Data are sorted by body length.
*99B7 age estimates from two D/L determinations were 27 and 71. WhaleID = the whale identification number,
TotCA = total CAs counted; TotCL = total CL counted, BL = body length (m), baleen = baleen length (cm), OA =
ovulation age, OA-se = standard error of the ovulation ages, AARage = aspartic acid racemization age (Rosa et al.,
2004), AARse = standard error of AAR age.
WhaleID TotCA TotCL BL baleen OA
99B18
1
1
13
342
27
97B8
2
0
13.6 260
29
93B17
5
0
13.6
36
01B17
2
0
13.9 255
29
92B7
1
1
14.2
27
81S2
5
1
14.2 344
36
76B20
6
0
14.3
39
96B4
10
0
14.4 300
48
00B2
5
0
14.5 273
36
92B10
5
0
14.6 320
36
00B3
11
1
14.6
51
92B3
15
0
14.6
60
89B2
6
1
14.7 280
39
99B16
1
1
14.8
27
88KK1
6
1
14.9 297
39
90B4
10
1
14.9 274
48
92B9
9
0
15
46
85WW2
12
1
15.1 320
53
95B8
1
1
15.2
27
99B7*
4
1
15.4
34
00B4
9
0
15.4
46
93B20
3
1
15.5
32
88G1
9
1
15.7 301
46
87B5
11
1
15.7 300
51
87B6
12
0
15.7 330
53
85WW1
6
0
16.2 355
39
81KK3
9
0
16.2 340
46
92B4
12
0
16.2 360
53
03B9
25
1
16.4 344
85
82WW2
7
0
16.5 280
41
81WW3
27
1
16.5
89
97B10
13
1
16.7 320
56
02B2
17
0
16.7 352
65
89B3
41
0
16.9 405
123
86KK2
12
0
17.2 356
53
81KK1
8
0
17.4 362
44
82WW1
16
0
17.6
63
86WW2
4
1
17.7 345
34
00B5
16
1
18.9 331
63
02B3
34
0
19.2 409
106
OA-se AARage
5
29
5
6
5
5
6
6
8
43
6
26
6
8
41
10
6
5
39
6
8
8
9
5
6
27
8
52
5
8
8
9
6
8
9
16
7
17
9
11
25
9
7
11
6
11
66
21
AARse
12
13
8
13
12
12
14
15
9
SC/56/BRG8
Year
0 Month
Type J F M
1
A MJ J A S O N D J
2
F M A M
J J A S O N D J
3
F M A MJ J A S O N D J
4
F M
A MJ J A S O N D J
5
F M
prep OC pregnancy
CL forms
3 yr prep 0C pregnancy
CL forms
B
lactation
CA transition
rest
CA regresses
4 yr prep 0C pregnancy
CL forms
B
lactation
CA transition
rest
CA regresses (in size)
B
A MJ J A S ON D J
F MA M
lactation
prep OC pregnancy
CL forms
B
Fig. 1. Diagram of possible reproductive cycles for bowhead whales. Rows 1 and 2 show details for possible 3year and 4-year calving intervals, respectively.
14
12
10
8
6
4
Std. Dev = 8.80
2
Mean = 10.7
N = 39.00
0
0.0
5.0
10.0
15.0
20.0
25.0
30.0
35.0
40.0
TOTCORP
Fig. 2. Distribution of total corpora for 40 bowhead whales in which both ovaries were examined. Note that nearly
all females had less than 18 corpora but 4 (10%) had 25 or more.
10
SC/56/BRG8
AA
AA
A
A
AAA
A
AA
A
A
A A
A
AA
A
A
A
A
A
A
A
A
A
A
Predicted probability
1.00000
AA
A
0.75000
A
A
A
0.50000
A
A
A
0.25000
A
A
A
A
A AA
A
A
A
A
A
AA
A
AA
0.00000
7.5
A
A
AA
A
10.0
12.5
15.0
17.5
bodylen
Fig. 3. Plot showing the results of the logistic regression of bowhead body length and maturity.
20
19
Body Length (m)
18
17
16
15
14
13
12
20
40
60
80
100
120
140
Ovulation Age (yr)
Fig. 4. Plot of ovulation age by length. These data suggest that some females grow quite old (> 100 yr) which was
only the case for males reported in George et al. (1999) and Rosa et al. (2004).
11
SC/56/BRG8
80
70
y = 0.8828x + 3.7389
R2 = 0.6645
AAR age (yr)
60
50
40
30
20
10
0
0
10
20
30
40
50
60
70
80
Ovulation Age (yr)
Fig. 5. Plot of aspartic acid racemization age estimates and corpora counts. Note that the lower age estimate (27 yr)
for whale 99B7 was used in this plot. With this small sample, there appears to be good agreement between these
two independent ageing methods.
12