J. Zool., Lond. (1996) 240, 581-591

Reproductive biology of female striped dolphin (Stenella coeruleoalba) from the western Mediterranean

N. C A L Z A D A ' , A. AGUILAR, T . B. S0RENSEN' A N D c. LOCKYER3 ' University .f Barcelona, Department of Animal Biology, Faculty of' Biology, 08028 Barcelona,

Spain 'Zoological Institute, University of Copenhagen, 15 Universitetsparken, DK-2100 Copenhagen,

Denmark 'Sea Mammal Research Unit, High Cross, Mudingley Road, Cambridge, CB3 OET U K

(Accepted 8 November 1995)

(With 2 figures in the text)

Data on age and length at sexual maturity, calving interval, lactation period, and ovulation and pregnancy rates were analysed from 84 female striped dolphin collected during the Mediterranean morbillivirus epizootic. Age was determined by counting growth layer groups in tooth dentine, and reproductive status was determined by the macroscopic examination of the ovaries and the uterus. Age at sexual maturity (ASM) was estimated using two different methods; giving average estimates of 12 and 12.3 years. The average length at sexual maturity was 187cm and the calving interval was four years. The annual pregnancy rate (APR) was calculated using two different criteria. In the first, only females that were pregnant at the time of death, as evidenced by the presence of a foetus, were incorporated in the calculations. This method gave an estimate of 8.9% as the apparent pregnancy rate of the dolphins killed by the epizootic. The second method incorporated in the calculations females that were pregnant at the time of death and females that had young corpus albicans in the ovaries and a distended uterus. This method is considered to reflect the true pregnancy rate of the population and gave an estimate of 25%. Estimates of ovulation rate (0.401) and lactation period (16 months) were considered to be potentially affected by the disease and, therefore, biased. These estimates reflect a peculiar situation of the diseased dolphins but are useful for comparative purposes. Estimates of ASM and APR, parameters which are not likely to be affected by the disease, differed markedly from those of other Stenella populations and could indicate a density-dependent response, possibly reflecting food limitations.

Introduction

The striped dolphin (Stenella coeruleoulba) is the most common cetacean in the Mediterranean Sea. Until now only fragmentary information was available about its population biology, obtained mainly from records of single stranded animals and from sightings (Wale, 1985; Duguy et al., 1988; Aguilar, 1991). Previous studies on the biology of the Mediterranean striped dolphin include those by Aguilar (l991), in which determination of calving period, body length and weight at birth, and sex ratio were determined.

The recent morbillivirus epizootic that affected the Mediterranean striped dolphins, killing thousands of animals (Duignan et ul., 1992; Domingo et al., 1992; Aguilar & Raga, 1993), provided enough material to study various biological parameters of the species. In the present paper, reproductive parameters of the female Mediterranean striped dolphin (Stenella

58 1

x; 1996 The Zoological Society of London

587 N C A L Z A D A E T A L

cuerulcwulhm) are estimated. D a t a on age and length a t sexual maturi ty , lactation period, calving interval, and ovulation and gestation rates are analysed. T h e estimates reached give an idea o f the s ta tus of the populat ion pr ior t o the morbillivirus epizootic. Biological indices obtained f r o m this mortality could provide an impor tan t tool to assess the impact of future changes in environ- mental conditions or fishing interactions in the Mediterranean Sea and increase o u r ability t o predict striped dolphin populat ion growth or decline.

Material and methods

A total of 84 females was analysed: 56 mature, 23 immature. 4 foetuses and 1 neonate were obtained from animals that had been affected by the morbillivirus epizootic off the Mediterranean coast from 1990 to 1993. All had been found stranded along the Spanish coast in the area between Valencia, Catalonia, and the Balearic Islands. Animals from other regions were not analysed, because body size variation has been reported to occur in this species between different oceanographical regions of the Mediterranean Sea (Calzada & Aguilar. 1995).

There are differences in the sample size for the various parameters measured because complete data for each specimen were not always available. Length was measured in a straight line from the tip of the jaw to the notch between the flukes. Age was determined by counting growth layer groups (GLCs) in tooth dentine of decalcified and stained longitudinal sections; each GLG was assumed to represent one year (Myrick et ul., 19x3; Calzada, Lockyer & Aguilar. 1994). Some of these preparations were also cross-checked by American and Japanese colleagues.

Esar i i inu t iot I of' i ~ p ~ ~ l i i ~ t i w 1 riic ts

Reproductive tracts were fixed and stored in 10% neutral buffered formalin. Before fixation, the flat diameter of the uterine horns was nieasured at their midlength; mammary glands were measured and checked for gross indication of lactation; ovaries were weighed to the nearest 0.1 g and, once fixed, sliced by hand into longitudinal sections approximately 2 mm thick with a scalpel. Sections were examined under a dissecting microscope for classification of ovarian scars. Ovarian corpora were scored in 3 categories: corpora lutea (CL). young (YCA). and medium and old corpora albicantia (CA) (Marsh & Kasuya, 1984). The mean diameter of each corpus was calculated by measuring the 3 largest planes to the nearest mm. Slices of selected ovaries were prepared for histological examination when there was any doubt as to thc classification of the corpora. Each sample was dehydrated in acidified 2.2-dimethoxypropane, rinsed in toluene. embedded in paraplast and sectioned at 8 pn. Sections were stained with haematoxylin and eosin and mounted in entellan.

Estirmtioti uf r t p m h c t i w puranieters

The parameters ainalysed in this study were: average age and length at sexual maturity, ovulation rate, annual pregnancj rate. calving interval and lactation period. In order to allow comparison between populations, the age ;it sexual maturity and the pregnancy rate were estimated with more than one method. The different reproductive parameters were estimated as follows:

Arrruge uge m i l lrtigth (it sesiiul mcituritj' I c1s111 u i d h i ) Sexual maturity i s attained when females ovulate for the first time. Evidencc of ovulation is determined by

the presence in one of the ovaries of at least one corpus luteuni or corpus albicans at any stage of development (Perrin & Reilly. 1984). It has been estimated in different ways by various authors (De Master, 1984: Hohn. 1989). In our study, 2 different estimators were used to determine ASM.

REPRODUCTIVE PARAMETERS I N STRIPED DOLPHINS 553

Sum oftlzeJraction immature. This method estimates the sum of the fraction of immature animals in each age class where mature and immature specimens are present. This sum is added to the first age class, in which a maturc specimen occurs (Hohn, 1989):

j = age of the youngest mature animal in the sample k = age of the oldest immature animal in the sample I,, = number of immature animals in the sample aged a N,, = total number of animals aged a (mature + immature) x,, = number of age classes combined to obtain a sample size of >2 in age class a

When there were fewer than 2 specimens in an age class, the age classes were combined until at least 2 specimens were included. When age classes were combined, the fraction of immature specimens was multiplied by the number of age classes combined.

This method was also used for estimating average length at sexual maturity.

Age ut which 50% of the females are mature. A linear regression was fitted to the fraction of mature specimens within each age class. The regression included the age of the youngest sexually mature individual and the age of the oldest sexually immature individual.

Ovulation rate Estimation of ovulation rate is based on the assumption that the scars from the corpus albicans persist

indefinitely. Estimation was made by fitting a linear regression to the corpus-count/age, and assuming that the slope of the regression corresponds to the rate at which corpora are formed. The regression line was obtained by the least squares method (Zar, 1984).

Annual pregnancy rate (apr) Annual pregnancy rate was calculated as the percentage of pregnant females divided by the length of

gestation in years (Perrin & Reilly, 1984). Since most of the samples were collected during the morbillivirus epizootic, and the reproductive cycle of mature females that died might have been altered by abortions caused directly or indirectly by the disease, the percentage of pregnant females was calculated using 2 different criteria: (I) the presence of a foetus; in this way, only females that were pregnant a t the time of death were included; (ii) the criteria used for pregnancy incorporate not only females with a foetus, but also females with C L or YCA and uterine distension. With this method, the females included were those pregnant at the time of death, females that apparently had recently aborted (as indicated by the presence of a YCA and a distended uterus), and females with milk in their mammary glands, a distended uterus, and a YCA. This method is considered to be less affected by the incidence of disease and, therefore, more reflective of the true pregnancy rate of the population.

Calving interval (CI)

as the inverse of the annual pregnancy rate, C1 = l/APR (Perrin & Reilly, 1984). The calving interval is an estimate of the period between parturitions in mature females. It was calculated

Lactation period The duration of lactation period was estimated as the ratio of lactating to pregnant females (Perrin &

Reilly, 1984). Lactating females were identified visually by slicing the mammary gland and checking for the presence of milk. Pregnant females were identified as those fulfilling criterion (ii). Females with milk in their

584 N . C A L Z A D A E T A L .

niammary glands and a distended uterus without a foetus "ere considered to bclong to the pregnant category i n the calculalions (see Discussion). None of the females with a foetus was lactating.

Results

Reprodirrtiw triict

Reproductive tracts from 84 females were examined: 28 dolphins, all younger than 10 years, were immature and 56 were mature. Milk was found in the mammary glands of 19 dolphins. Five mature females had a CL (diameters ranging from 19 to 26.5 mm) and every one carried a foetus. YCAs with diameters ranging from I 1 to 2 1.3 mm were found in 1 1 specimens; nine of these females also presented uterine distension, indicating recent parturition or abortion; two had uterine diameters falling in the range of diameters that corresponded to females with older CAs, indicating that they had probably ovulated shortly before death. The rest of the females examined had medium or old CAs, with diameters that ranged from 2 to 9.8mm. Figure 1 compares the width of the largest uterine horn in females that were classified according to the type of corpora present in their ovaries. Females with old or medium CAs had uterine widths below 26 mm; only one had a distended uterus, which was presumably pathological. Most of the females with YCAs had uteri that measured between 30 and 54nim. The largest widths (>70 mm) belonged to females with CLs.

Ovaries weighed less than 1.Og up to 6 years of age. Ovarian weight increased gradually to about 11 years. after which there was a rapid increase in weight due to the development of ovarian corpora. This change occurred at a body length of 180cm.

Age (it .sc~.uucr/ m1turirj .: In our sample, average age at attainment of sexual maturity (ASM) was obtained with two estimators. The youngest sexually mature female was 10 years old and the oldest immature was I5 years old. ASM using the sum of the immature fractions gave an estimate of 12.3 years (S.E. = 0.269) and the estimate for the age at which 50% of the females are mature was 12 years (S .E. = 0.087).

Average length at attainment of sexual maturity was calculated using the sum of fraction iinniature method, giving an estimate of I87 cm (S.E. = I .05). The shortest mature female was 182 cm long and the oldest immature 194cm. Knowledge of size at sexual maturation is important since i t allows estimation of maturity when only length data are available.

Owfuiinn rctic: The factors to be taken into account when estimating ovulation rates are: first, individual variation; second, environmental factors; and third, age-related changes in ovulation rates (e.g. Gambell, 1973; Perrin. Coe & Zweifel, 1976; Marsh & Kasuya, 1984).

In our sample. the regression equation fitted to the corpus count/age in animals older than nine years was:

j ' = 0.401 (.Y) - 2.95

where I ' indicates the number of corpora and s indicates the age in years. The slope, 0.401, corresponds to the ovulation rate of the population.

REPRODUCTIVE PARAMETERS I N STRIPED DOLPHINS 585

16-

14 -

12 - 2 10- II 8- F LI 6-

4-

2-

C a, 0-

Uterine diameter in specimens with CAs

161 I

25 0 10 14 18 22 26 30 34 38 42 46 50 54 58 62 66 >70

Uterine diameter in specimens with YCAs 16

12

:: 0 10 14 18 22 26 30 34 38 42 46 50 54 58 62 66 >70

Uterine diameter in specimens with CLS

FIG. 1. Comparison of the width ofthe uterine horn between females that had in their ovaries a different type ofcorpora.

586 N . C A L Z A D A E T . 4 L

Arinucil pregnanc:1~ rut(’ I A P R ) : Using criterion (i), only five out of 56 mature females were pregnant, giving a proportion of pregnant females of 0.089. As commented above, this corresponds to the apparent pregnancy rate of diseased females. When dividing this figure by the gestation period of one year. as estimated by Aguilar (1991), APR was estimated as 8.9%.

However. using criterion ( i i ) gives 25% (9 YCA and 5 CL out of 56 mature females), a figure that falls between the normal ranges for other Stenellu species (Perrin & Reilly, 1984).

Calving i n f ~ ~ r i d : Calculated as the inverse of the annual pregnancy rate. Given that the APR has been estimated above as 0.25, the calving interval is calculated at four years.

Lricturion period: Assuming that gestation lasts 12 months, the estimated lactation period is 16 months.

Discussion

The morbillivirus epizootic affected estimates of reproductive parameters in three ways. First, the age distribution of the sample was biased because of the higher mortality of individuals older than about 14 years and younger than two, with low contribution of individuals of intermediate age, which include both young mature and old immature dolphins (Calzada, Lockyer & Aguilar, 1994): secondly, owing to the seasonal onset of the disease (Aguilar & Raga, 1993), most of the carcasses were recovered during the summer months. so samples from other periods of the year are under-represented in the study; and thirdly, diseased animals probably had impaired reproductive cycles and a higher percentage of spontaneous abortions when compared to a ‘normal’ population.

Pregnant females were under-represented due to abortions, and lactating females were under- represented because of the ceasing of lactation due to calf mortality. When estimating the pregnancy rate only by the presence of a foetus or CL, as is common practice in cetacean studies, the result differed substantially from estimations for other delphinid populations, giving a low value of 8.9%. We believe that the most probable explanation for such a low estimate is the high number of spontaneous abortions directly or indirectly caused by the disease, as suggested by the high proportion of specimens without neonatal line in tooth dentine (from 12 individuals younger than one year, seven were foetuses). This line marks the point of parturition due to disturbances in the nutrition of the animals in the immediate post-partum period (Perrin & Myrick, 1980).

Moreover, abortions and recent parturitions are also suggested by the abnormally high percentage of YCA (21%) in the sample, in contrast to other studies carried out in Stenellu species (Perrin of al., 1976). Since CL regression is very rapid (Hirose, Kasuya & Kazihara, 1970) and probably occurs in less than 15 days (Perrin e f a/., 1976), the use of YCAs in the calculation of this parameter was considered appropriate. Therefore, females with YCA that had aborted during the reproductive season, as evidenced by uterine distension, were included in the proportion of pregnant females, and this estimate was considered to represent more reliably the overall pregnancy rate for the population. In our sample, the diameters of YCAs and CLs were not substantially different (Fig. 2). YCA were large ( 1 1-21 mm) when compared to medium and old CAs (2--9.8 mm), but close to or even overlapping CLs (19-26 mm) of pregnant females. Moreover, of the 12 individuals with YCAs, 10 had obvious distension of the uterus, indicating post-partum females and recent abortions (Fig. I ) . Females with milk in their mammary glands, YCA and uterine distension were included in the pregnant category since the expulsion of the

REPRODUCTIVE PARAMETERS I N STRIPED DOLPHINS

l01

10- 9- 8- 7-

2’ 6- K

D 2 5 -

; 4- 3 - 2 1 -

0

581

I I 1 I , , I I I

:: 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

CL Diameter

F I G . 2 . Frequency distribution of diameters of the different ovarian corpora: (a) corpus albicans (CA); (b) young corpus albicdns (YCA) and (c) corpus luteurn (CL).

588 N . C A L Z A D A E T A 1

uterine contents in near-term abortions induces milk secretion. Concentrations of oestrogen, progesterone, and prolactin rise progressively during gestation; after expulsion of the placenta, the rapid decline in circulating oestrogen, which inhibits the action of prolactin, allows milk secretion (Ganong. 1985). This explains that recently aborted females still presented milk in their mammary glands and. therefore, these animals were included in the pregnant category.

The infection also potentially affected the number of lactating females recovered. Calf mortality during the die-off was high (Calzada ef d.. 1994) and therefore, the mean duration of lactation was probably shortened. If this was so, the number of lactating females was under- represented in our sample and the actual duration of the lactation period is expected to be somewhat longer than the value obtained in this study. Unfortunately, the use of alternative methods, such as the cowicalf method, which assumes that for each lactating cow there should also be a suckling calf in the sample, or by the analysis of stomach contents, which allows a direct determination of the age at which the calf shifts from milk to solid food, was not possible because of sampling limitations.

ASM is used to compare the status of cetacean populations, but comparisons should only be made when estimates are obtained by the same methods. The sum of the immature fraction is considered insensitive to changes in the age distribution of the population and accepted as the most precise for the calculation of ASM (Hohn, 1989). The age at which 50% of the females are mature was used by K ~ S L I Y ~ (1976. 1985) to calculate ASM in striped dolphins off the Pacific coast of Japan. Comparison between the Mediterranean and Japanese populations is thus possible since estimates are obtained in the same manner. In our study, both methods gave similar estimates. so we suggest that the most reliable value for the population falls around 12 years. This value is remarkably high when compared to other striped dolphin (Kasuya, 1972, 1976, 1985) or Srcncllr populations (S . longirostris and S. utrcnuata) (Perrin & Reilly, 1984) from other areas (Table I ) .

Reproductive rates are thought to vary as population size changes relative to carrying capacity (Fowler, 1981). When population abundance declines, there is an increase in per capita availability of resources and the condition of the individuals improves, therefore increasing female reproductive output. This translates into decreases in age at maturation and increases in pregnancy rates (Eberhardt & Siniff, 1977). Kasuya (1985) showed evidence of density depen- dence in the heavily exploited striped dolphin of Japan, reporting that ASM in females decreased from 9.7 years in 1956-58 to 7.4 years in 1968-70. Data published by Kasuya & Miyazaki (1975) have also shown a decrease in the lactation period in this population. When comparing the

Mediterranean striped dolphin

Japaricsc striped dolphin

Source Oldest immature (years) Youngest mature (years) ASM (years) APR ("10)

Lactation period (months)

This stud? 15 10 11 25

> I 6

Kasuya. 1976 11.5 7.5 9

70.9 13

Ranges for other Stcneilri

Perrin & Reilly. 1984 _._ - ~~ ._

6 12 3 8 4-10

25 40 13-27

REPRODUCTIVE PARAMETERS IN STRIPED DOLPHINS 589

striped dolphin from Japan with those from the Mediterranean, pronounced differences were noted in the values of reproductive parameters (Table I).

The ASM determined in our study, 12 years, differs markedly from the 9.7 or 7.4 years estimated by Kasuya (1985). This difference appears too large to be explained by the effect of randomness in the sample, and cross-checking with Japanese colleagues rules out the possibility that it can be attributed to differences in the techniques used for the determination of age and reproductive status. Comparison of other reproductive parameters are shown in Table 1. The value for the lactation period may have been biased in our case by the incidence of the disease. The results of the present study differ not only from those obtained in conspecific populations, but also from the range of values commonly obtained in congeneric ones (Table I).

Taking into account observed density-dependence responses in mammal populations, these differences may suggest that, while the striped dolphin population off Japan reflects large availability of food caused by a decrease in dolphin abundance in recent years (Anon., 1993), the western Mediterranean population could follow the opposite course and be either in equilibrium or suffering constraining food limitations. In this situation, the condition of the Mediterranean dolphins would be expected to be poor, leading to lowered reproductive rates by increases in ASM and decreases in APR.

The low reproductive rates found in this study, compared to other populations, could be due to the over exploitation of most fish and cephalopod resources in the Mediterranean Sea during the last decades, particularly in the continental shelf areas (Caddy & Griffiths, 1990). The Mediterranean striped dolphins base their diet on a number of species, such as the blue whiting (Micromesistius poutassou), the bogue (Boops boops), the anchovy (Engraulis encrasicholus), the hake (Merluccius merluccius) or the squid (Histioteuthis spp.) (Wurtz & Marrale, 199 1; Pulcini, Carlini & Wurtz, 1992), which are intensely exploited throughout the region. Overall, commercial species are estimated to represent up to 68% of the total number of species on which striped dolphin prey (Wurtz, Pulcini & Marrale, 1992).

Further substantiating this hypothesis, the morbillivirus epizootic that affected the population from I990 to I992 was suggested to have been triggered by the scarcity of food and a subsequent impoverishment of individuals’ physical conditions. This weakening might have favoured infection and transmission of the disease (Aguilar & Raga, 1993). The relationship between food availability, body condition, and susceptibility to disease has been demonstrated in a number of animal species, and the role of disease as a determinant factor in the population dynamics of large mammals is well established (Fowler, 1987).

Since the condition of individuals and populations reflect environmental conditions, popula- tion status can be determined by the use of biological variables that undergo density-dependent change. However, this relationship may be inverted so that indices can be used as indicators of changes in the carrying capacity of the environment (Fowler & Siniff, 1992). Until more data are available, management policies directed towards striped dolphins should take into account the potential interaction of the population’s food resources with the fisheries operating in the region in order to guarantee the maintenance of the population at its current levels.

Funding for this research was provided by the National Institute for the Conservation of Nature (ICONA) and by project NAT9 I - 1 128-C04-02 of the Interministry Commission for Science and Technology (CICYT) of Spain. N. Calzada was funded by an FPI fellowship from the Ministry of Education and Science of Spain. We thank Dr A. Hohn and Dr N. Miyazaki for their review of tooth sections. We owe particular thanks to Dr M. Durfort for the use of the laboratory.

590 N . C'ALZADA E T .AL

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