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Population development of harbour seals Phoca vitulina in the Wadden Sea after the 1988 virus epizootic
In Collaboration with the Netherlands Institute for Sea Research
URNAL
‘SEA ELSEVIER
OF RESEARCE
Journal of Sea Research 38 (1997) 161-168
Population development of harbour seals Phoca vitulina in the Wadden Sea after the 1988 virus epizootic Peter J.H. Reijnders a,*, Edith H. Ries a, Svend Tougaard b, Niels Norgaard b, Gi.inter Heidemann ‘, Jochen Schwarz ‘, Ekkehard Vareschi d, Ilona M. Traut d aInstitute for Forestry and Nature Research, Dept. Aquatic Ecology, PO. Box 167, 1790 AD, Den Burg, The Netherlands ’ Fisheries and Maritime Museum, Tarphagevej 2, DK-6710, Esbjerg, Denmark ’Research and Technology Centre Westcoast, HafentGrm, D-25761, Biisum, Germany d Dept. Aquatic Ecology, University of Oldenburg, D-26111, Oldenburg, Germany
Received 31 January 1997; accepted 17 March 1997
Abstract
The mortality as a result of the 1988 virus epizootic amongst harbour seals Phoca vitulina in the North and Baltic Seas is estimated at 60% in the entire Wadden Sea. In the years 1989-1994, a prosperous recovery of the population has been observed which is reflected in a high post-epizootic rate of increase. The average annual rate of increase for the entire area was 16%, highest in The Netherlands (average 21%) and lowest in Denmark (average 10%). This rate of increase is significantly higher than in the pre-epizootic period 1976-1987, when the population increased at a rate of around 9% per year. The difference is partly attributed to a considerably lower initial juvenile mortality after the epizootic. The present first-year mortality is statistically significantly lower than in the 1970s. It is about equal in all regions and estimated at approximately 40%, whereas it was approximately 65% in the 1970s. The post-epizootic reproductive rate in The Netherlands is significantly higher: 21% on average, against 13% before 1988; it is also higher in Niedersachsen (21 vs. 16%), but lower in Schleswig-Holstein (19 vs. 23%), while in Denmark it has not changed (both 17%). It is hypothesised that the improved reproductive rate in The Netherlands might be a result of selective mortality during the epidemic, which within the adult female segment would have predominantly affected those not reproducing. It is emphasised that though the population is recovering well, its size of almost 8800 animals in 1994 is still only one quarter of an estimated reference figure of 37000 seals around 1900. How long the recovery will continue at its present rate depends on environmental conditions in the area, such as pollution, disturbance and food resources; nor can a recurrent flickering of the epidemic be excluded. Keywords:
population development; harbour seals; Wadden Sea; virus epizootic
1. Introduction The harbour seal Phoca vitulina population in the Wadden Sea can be regarded as a discrete popula* Corresponding
author. Fax: ,+31
[email protected]
(222) 319235; E-mail:
tion, with insignificant exchange with other North Sea or Baltic stocks (Drescher, 1979). The various subpopulations have been drastically depleted in the past as a result of overhunting (Reijnders, 1992). After hunting was at last stopped throughout the Wadden Sea in 1976, the population clearly started to recover (Reijnders et al., 1990). However,
1385-l 101/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII S1385-1 101(97)00031-2
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the phocine distemper virus epizootic in 1988 interrupted this recovery and the population is assumed to have been reduced by approximately 60% (Schwarz and Heidemann, 1994). To provide favourable conditions for a recovery of the Wadden Sea population, a long-term conservation and management plan was designed (CWSS, 1992). The development of that plan and implementation of related studies required close cooperation between the countries involved, and a comprehensive 5-year research plan was drafted. Results of these studies clearly indicate that after the epizootic the population has recovered prosperously, as reflected by the high post-epizootic rate of increase. This paper discusses the population development and the course of the parameters population size, reproductive rate and initial juvenile mortality, for the entire population as well as for the various subpopulations. 2. Methods
of Sea Research 38 (1997) 161-168 Table I Annual number of surveys carried out in each region of the Wadden Sea and date (week number) when the maximum number of seals (Tmax) in the entire Wadden Sea was obtained Year
1989 1990 1991 1992 1993 1993
Number of surveys NL
NS
SH
DK
9 9 I 9 9 8
10 6 10 10 9 I
15 12 11 10 7 8
10 12 14 11 13 9
NL = The Netherlands, NS = Niedersachsen, Holstein, DK = Denmark.
Tmax (week) 26 26 25 26 31 26
SH = Schleswig-
when low-tide occurred around midday and weather conditions were suitable. This was done to minimise the possibility of double counts due to interim movement of seals between areas. Notwithstanding, in some cases conditions were such that in a region alternative days had to be found.
2.1. surveys 2.2. Data processing The basic data for the analyses in this paper originate from census results obtained during aerial surveys carried out between 1989 and 1994. Traditionally, each of the countries bordering the Wadden Sea carried out these surveys in their own region, namely Denmark (DK), Schleswig-Holstein (SH), Niedersachsen (NS) and The Netherlands (NL). Seals in the Hamburg region are included in the surveys of Niedersachsen. For this project the survey flights were synchronised and designed to cover all the haul-out sites within each of the regions under, as far as possible, similar tidal stages within one flight. Usually eight to ten flights per year have been carried out in each region. The number of surveys per region are given in Table 1. The main data were collected during the pupping season. Therefore, four to five flights were performed in June and July to obtain the pupping curve (Reijnders, 1978). Information on the distribution and number of subadult and adult harbour seals in the Wadden Sea was also collected during these flights, but additional flights proved indispensable to complete the information on animals hauled out during the moult (August). Surveys were carried out in all regions simultaneously, or at most a few days apart, preferably
2.2.1. Maximum number of seals The number of seals (including pups) counted during the simultaneous census flights has to be regarded as a minimum estimate, as it can be expected that some individuals are not hauled out and thus missed during the survey. The annual minimum estimate of the harbour seal population in the entire Wadden Sea was derived from the highest sum of the counts in the different regions during each of the simultaneous surveys in that specific year. The dates at which this annual figure was obtained (T,,,) are given in Table 1. 2.2.2. Reproductive rates The reproductive rate for the separate regions is the maximum number of pups observed. It is expressed as a percentage of the maximum total number of seals (including pups) observed in that region during that simultaneous survey in the whelping period when the highest maximum for the entire Wadden Sea was obtained. The maximum number of observed seals is used here instead of the numbers born derived from a recruitment model (Fransz and Reijnders, 1978), since in several regions no
I?J.H. Reijnders et al./Joumal
adequate data exist for several years to run the recruitment model. For the entire Wadden Sea, the respective maximum numbers of pups are added and expressed as a percentage of the maximum for the entire area observed in the whelping period. 2.2.3. Initial juvenile mortality A method to estimate initial juvenile mortality, i.e. the mortality during the first weeks of life, in harbour seals is described in detail in Fransz and Reijnders (1978) and in Fransz (1979). In this recruitment model, the time from the first pup reported to the moment the maximum number of pups was observed (T,,,,,) and the total length of the whelping period (&) were used to provide a first estimate of the juvenile mortality rate (M>. Around this first estimate a series of different values for M were tried in the model to generate a curve with the best fit to the field data. Observations carried out in 1979 on individually recognisable pups showed that weaned pups stay at the breeding colony and haul out each low tide for another three weeks (van Wieren, 1981). However, similar data obtained by the two co-authors Norgaard and Tougaard (unpubl. data) between 19901995 show a different post-weaning behaviour of pups. After approximately four weeks the pups are weaned, and they do not haul out as frequently as during the lactation period. At six weeks of age, most pups leave the breeding area and the ones that stay haul out even less. Due to these factors, juvenile mortality could be overestimated if the original model was run for a period extending four weeks after the start of the whelping season. Furthermore, when pups grow more than about six to seven weeks old it becomes increasingly difficult to distinguish them from yearlings, and therefore in some regions this age group was no longer counted separately. The model therefore needed to be modified, taking into account the potential bias in relating observed pups to surviving pups. The modifications included correction factors for less frequent haul-out after four weeks of age (60% less), declining to no haul-out after six weeks of age. Because it becomes increasingly complicated with time to quantify the possible errors introduced, the model was applied only for up to seven weeks after the start of the whelping season. The observations on the abundance of pups in the course of the whelping season, carried out in the
of Sea Research 38 (1997) 161-168
163
different regions of the Wadden Sea during 19891994, formed the basic material used in the recruitment model. Data for the entire Wadden Sea were obtained from the pup-curves for each region. At a given Julian day, the number for each region was taken from the respective curve and added to provide the sum. The length of the whelping period for the entire Wadden Sea was obtained by the ending date of the last-starting whelping period in a region and that date was compared with the date of the region where the whelping period started first. 3. Results 3.1. Population
development
During the study period, from 1989 to 1994, a total of 237 aerial surveys were carried out in the various regions of the Wadden Sea. The annual maximum numbers of harbour seals counted in the Wadden Sea are shown in Fig. 1. The sum of the various regions indicates a minimum estimate of the actual size of the harbour seal population in the Wadden Sea. It is evident that the total numbers observed have been increasing substantially since 1989. By 1994, a total of almost 8800 animals were reported, more than twice the number observed in 1989. The annual rate of increase was on average
Fig. 1. Annual maximum numbers of harbour seals registered during simultaneous surveys in the various regions of the Wadden Sea, and the respective maximum for the entire Wadden Sea. NL = The Netherlands, NS = Niedersachsen, SH = SchleswigHolstein, DK = Denmark, Total = entire Wadden Sea.
P.J.H. Reijnders et al./Joumal
164
16%. The highest rate was observed among the stock in The Netherlands (21%), and the lowest in Denmark ( 10%).
3.2. Reproductive
rates
of Sea Research 38 (1997) 161-168
[sfjl
m NL
20 10 -
The reproductive rates for the various regions and the whole area are given in Fig. 2. Apart from 1989, when in some regions the epidemic had a direct effect on numbers born, the figures are approximately equal in all regions and fluctuate around 20%. The figures for Denmark are somewhat lower than those for other regions.
Ol
1
NS
r-l
20 -
10 0
3.3. Initial juvenile
mortality
-
20
For reasons such as logistics and inclement weather conditions, not all surveys in each of the various regions provided adequate results each year for the recruitment model to be run reliably. Therefore we decided to use, as an example, the most complete data set for each region for one given year. Those are: The Netherlands, 1993; Niedersachsen, 1992; Schleswig-Holstein, 1994; Denmark, 1993. These are complemented by data for the total Wadden Sea in the years 1993 and 1994. The results are shown in Fig. 3 and Fig. 4, respectively. The corresponding data on length of the whelping period, mortality rate and initial juvenile mortality (total mortality during the first 6 weeks) are given in Table 2.
Area
NL NS SH DK Wadden Sea Wadden Sea
Year
1993 1992 1994 1993 1993 1994
Pups/births
0.71 0.70 0.73 0.71 0.70 0.70
rates (M) and initial after the start of the stocks in the various Wadden Sea
1,
M
CM
(days)
(day-‘)
(%)
37 35 37 34 44 44
0.022 0.024 0.020 0.024 0.020 0.020
33 36 31 37 34 34
NL = The Netherlands, NS = Niedersachsen, Holstein, DK = Denmark.
SH = Schleswig-
SH
10
-
0 I
DK
1
20IO-
7_-_-
OI
Total
1
20
10 Table 2 Length of whelping period (1,). mortality juvenile mortality in the first six weeks whelping (CM) in different years for the regions and for the population in the entire
r1
0I
1989
mu 1990
1991
1992
1993
1994 Years
Fig. 2. Percentage of pups from maximum numbers of harbour seals (including pups) counted in the various regions of the Wadden Sea during simultaneous flights in the whelping period. NL = The Netherlands, NS = Niedersachsen, SH = Schleswig-Holstein, DK = Denmark, Total = entire Wadden Sea.
4. Discussion 4.1. Population
development
During the study period the maximum number of harbour seals observed in the Wadden Sea more than
i?J.H. Reijnders et al./Journal
of Sea Research 38 (1997) 161-168
165
ICC
. 1500 .
*
IO00 . 500
. 0
I 190 Julian day
246
doubled, from - 4200 in 1989 to - 8800 in 1994. The annual rate of increase was on average 16%. The highest rate was observed among the stock in The Netherlands (2 l%), and the lowest in Denmark (10%). The virus epidemic in 1988 affected most harbour seal populations in Europe. After the epidemic annual rates of increase in some areas differed from those observed in the Wadden Sea: Heide-Jorgensen et al. (1992) reported rates close to zero for the population in the Skagerrak/Kattegat between 1988 and 1990, thereafter increasing to 26%. In the Wash, the population increased by only a few percent annually (J. Harwood, pers. comm.).
0
20
40
60
80
100
Days
Fig. 4. Numbers of pups surveys (left-hand diagrams) cruitment curves based on (right-hand diagrams). Bold line = number of surviving of pups.
Fig. 3. Numbers of pups counted during aerial surveys (left-hand diagram) in the various regions and recruitment curves based on the recruitment model calculations (right-hand diagrams). Bold line = number of pups born, dashed line = number of surviving pups, thin line = observed number of pups. NL = The Netherlands, NS = Niedersachsen, SH = Schleswig-Holstein, DK = Denmark.
-. Li!iJ 1994
2000
counted during simultaneous aerial in the entire Wadden Sea and rethe recruitment model calculations line = number of pups born, dashed pups, thin line = observed number
In the harbour seal population of the Wadden Sea, such high rates of increase as in the 19891994 period are unprecedented. After a similar low population size during the late 1970s the entire population increased by only 9% per year, despite full protection from hunting (Reijnders et al., 1990). This increase was also different in the various subpopulations: 12% in Denmark (Tougaard, 1989; Bogebjerg et al., 1991), 8% in Schleswig-Holstein, 7% in Niedersachsen and 8% in The Netherlands. 4.2. Reproductive
rates
Before the epidemic, substantial differences in reproductive rates existed among the various areas of the Wadden Sea, ranging from 13% in The Netherlands to 23% in Schleswig-Holstein. Since 1989 these rates have fluctuated around 20% in all regions except in Denmark, where the average is 17%. Especially in The Netherlands, the reproductive rate is significantly higher than before. This holds also for Niedersachsen, but to a lesser extent. An explanation might be that a selective mortality occurred during the epidemic. During the 1988 epidemic, high mortalities were observed in the colonies *in which pollutant levels were relatively high (Hall et al., 1992; Simmonds et al., 1993). Similarly, individ-
I?J.H. Reijnders et al./Joumal
166
uals with higher pollutant levels may have shown higher mortality. Pup production in The Netherlands and in Niedersachsen before 1988 was too low to sustain the local population. This has been ascribed to impairment of reproduction in females with high organochlorine pollutant levels (Reijnders, 1986). It is also known that high organochlorine pollutant levels reduce the immunological response (Brouwer et al., 1989; de Swart et al., 1994; Ross et al., 1995, 1996). Therefore, we hypothesise that in the pre1988 Dutch and German populations female seals still reproducing lost sufficient pollutants via pups and lactation to markedly improve their immunological conditions and thus to increase their chances of survival. According to this hypothesis we would expect higher mortality of non-reproducing females and of males, who also have no extra means to excrete pollutants. We have no data to show differences in female mortality during the epidemic. For the males, we found a mortality of 65% in Denmark; for the other regions we found no sex-related mortality. The first-year class was almost totally lost during the epidemic (Schwarz and Heidemann, 1994). The improved reproductive rate could therefore be partly of an arithmetical nature since the denominator in the division is smaller than before. However, that contribution can only be marginal. Before the epidemic, the one-year-old animals would constitute 910% of the population and that missing compartment only brings pup production up by -C 2%. The pup percentages are expected to level off within a few years because of gradual changes in the population structure, in particular an increase in the proportion of immature animals. When these age classes enter the reproductive segment of the population, pup percentages might either increase or decrease further, depending on the levels of exposure of these animals to environmental pollutants causing reproductive failure. 4.3. Initial juvenile
mortality
The simulation model is based on the assumption that the births are normally distributed over the whelping season. The data points on the right-hand side of the curves (the end of the whelping season) fit the curves less accurately than the data points on the left side (the beginning of the whelping season). This
of Sea Research 38 (1997) 161-168
is due to the stronger influence of mortality. Furthermore there is a greater possibility of underestimating the number of pups due to changes in haul-out behaviour and dispersal during the second part of the whelping period. However, the fit is considered good enough to conclude that the distribution of births is in agreement with the provision to follow a Gaussian frequency distribution. Because of the assumptions on normal distribution of births and haul-out tendencies of pups, the provided estimates on mortality rates should be regarded as indices of pup mortality. There was apparently little variation in the mortality rates between the different areas as well as between each of the areas and the total Wadden Sea. On average, the initial juvenile mortality - up to 6 weeks after the start of the whelping season amounted to approximately 34%. The additional mortality during the rest of their first year has to be estimated indirectly. An indication can be obtained by comparing the number of dead and live pups collected by nursery stations (Ecomare, Norddeich and Pieterburen, pers. comm.) in the first 6 weeks with the number collected in the other 46 weeks of their first year. That ratio was 4 : 1 and implies that another 8.5% mortality has occurred during the rest of the first year. This figure for post-breeding mortality is similar to data from other harbour seal populations, where values of around 8% were found (Harkiinen, 1987). This brings the present first-year mortality in the harbour seal population in the Wadden Sea to 42.7% (A 2.14 SD, n = 6). First-year mortality in the 1970s was estimated to be 60% in the seal population in the Dutch Wadden Sea and in that of Schleswig-Holstein (Reijnders, 1978; Reijnders et al., 1981). However, apparently the post-breeding mortality both in the Dutch and in the Schleswig-Holstein seal population at that time was slightly underestimated. The original estimate for the Dutch population was based on the difference between the calculated number of pups born and pups present in September, which revealed an average mortality of 57%. An additional mortality of 3% was assumed for the rest of their first year. That assumption was apparently not correct. This can be shown by recalculation of the additional post-breeding first-year mortality in the Dutch seal population during the end 1970s by the same procedure as mentioned for the post-epizootic period and with data for
P.J.H. Reijnders et al. /Journal of Sea Research 38 (1997) 161-168
those years. A figure of 9% was obtained and that brings the total first year mortality for that period to 66% instead of 60%. For Schleswig-Holstein, Reijnders (l.c.) used data from Drescher (1975) and again underestimated the post-breeding mortality. By using the more accurate data on the annual distribution of first-year mortality provided in Drescher (1979) the first-year mortality could be estimated in a different way and was found to be 65%. The first-year mortality in the harbour seal population in the entire Wadden Sea in the 1970s was estimated at 65.9% (f 4.0 SD, IZ = 8). Comparison of the above data for the 1970s with the post-epizootic data reveals that the present postepizootic first-year mortality is significantly lower (Student’s t-test, P < 0.01) than in the 1970s. However, it is still higher than in other harbour seal populations. For the Swedish west coast, Hark& nen (1987) assumes 30-35%, Bigg (1969) quotes 25% for British Columbia and Boulva (1973) reports 25% for Sable Island (east Canada). Disturbance may contribute to the comparatively high mortality among harbour seals in the Wadden Sea (Brasseur et al., 1996; Drescher, 1979; Reijnders et al., 1981; Vogel, 1994; Brasseur and Reijnders, 1994). 4.4. Prospects It is emphasised that the population is recovering well, though its size of nearly 8800 animals in 1994 is still only one quarter of an estimated reference figure of 37 000 seals around 1900. This figure was obtained by back-calculating how large the population must have been to sustain a given hunting pressure. The calculations start with the initial state of the population in 1960 (when aerial surveys started in all regions), an assumed range for net rate of increase, and known annual hunting records (Reijnders, 1992). How long the recovery will continue at its present rate depends on the pressure of environmental conditions such as pollution and disturbance; nor can the prospect of a recurrent flickering of the epidemic be excluded. Acknowledgements The Bezirksregierung Weser-Ems provided the survey data for Niedersachsen. The European Com-
167
mission partly funded the joint seal project under grant NORSPA 92- l/INT/OO4, B4-3030/92/01009 1. The Common Wadden Sea Secretariat administratively coordinated the joint seal project. We thank Wim Wolff and Sophie Brasseur for comments on the data and manuscript and George Fransz for modifying the recruitment model. References Bigg, M.A., 1969. The harbour seal in British Columbia. Fish. Res. Bd. Can. Bull. 172, l-33. Boulva, J., 1973. The harbour seal Phoca vitulina concolor in eastern Canada. Ph.D. Thesis, Dalhousie Univ., Nat. Lib. Ottawa, Canada, 134 pp. Bogebjerg, E., Tougaard, S., Madsen, J., Norgaard, N., 1991. Status of the harbour seal Phoca vitulina in the Danish waters, 1976-1989, and short term effects of the epidemic in 1988. Dan. Rev. Game Biol. 14, I-16. Brasseur, S.M.J.M., Reijnders, P.J.H., 1994. Invloed van diverse verstoringsbronnen op het gedrag en habitatgebruik van gewone zeehonden: consequenties voor de inrichting van het gebied. IBN-rapport 1 13. Brasseur, S.M.J.M., Creuwels, J., van der Werf, B., Reijnders, P.J.H., 1996. Deprivation indicates necessity for haul-out in harbor seals. Mar. Mamm. Sci. 12, 6 19-624. Brouwer, A., Reijnders, P.J.H., Koeman, J.H., 1989. Polychlorinated biphenyl (PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the common seal Phoca vitulina. Aq. Tox. 15, 99-106. CWSS, 1992. Sixth trilateral Governmental Wadden Sea Conference. 1991. Ministerial Declaration - Seal Conservation and Management Plan. Common Wadden Sea Secretariat, Wilhelmshaven, Germany, 55 pp. de Swart, R.L., Ross, P.S., Vedder, L.J., Timmerman, H.H., Heisterkamp, S., van Loveren, H., Vos, J.G., Reijnders, P.J.H., Osterhaus, A.D.M.E., 1994. Impairment of immune function in harbour seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23, 155-159. Drescher, H.E., 1975. Zur Biologie der Seehunde in SchleswigHolstein. Paper presented at 49th Congress of the German Society of Mammalogy 8-12 September, 1975, Innsbruck (mimeo). Drescher, H.E., 1979. Biologie, (ikologie und Schutz der Seehunde im Schleswig-Holsteinischen Wattenmeer. Beitr. Wildbiol. 1, Landesjagdverband Schleswig-Holstein, Meldorf, Germany, pp. l-73. Fransz, H.G., 1979. Estimation of birth rate and juvenile mortality from observed numbers of juveniles in a mammal population with normally dispersed reproduction. Ecol. Model. 7, 125-133. Fransz, H.G., Reijnders, P.J.H., 1978. Estimation of birth rate and juvenile mortality from observed numbers of juveniles in a seal population with normally dispersed reproduction. ICES CM 1978/N:7.
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HLkSnen, T., 1987. Feeding ecology and population dynamics of the harbour seal Phoca vitulina in Kattegat-Skagerrak. Ph.D. Thesis, Univ. Goteborg, Sweden. Hall, A., Laws, R.J., Wells, D.E., Harwood, J., Ross, H., Kennedy, S., Allchin, C.R., Campbell, L.A., Pomeroy, PI?, 1992. Organochlorine levels in common seals (Phoca vitulina) which were victims and survivors of the 1988 distemper epizootic. Sci. Tot. Environm. 115, 145-162. Heide-Jorgensen, M.-P, Hlrkonen, T., Aberg, P., 1992. Longterm effects of epizootic in harbor seals in the KattegatSkagerrak and adjacent areas. Ambio 21, 511-516. Reijnders, P.J.H., 1978. Recruitment in the harbour seal Phoca vitulina population in the Dutch Wadden Sea. Neth. J. Sea Res. 12, 164-179. Reijnders, P.J.H., 1986. Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324, 456457. Reijnders, P.J.H., 1992. Retrospective population analysis and related future management perspectives for the harbour seal Phoca vitulina in the Wadden Sea. Neth. Inst. Sea Res. Spec. Publ. Ser. 20, 193-197. Reijnders, I?J.H., Drescher, H.E., van Haaften, J.L., BogebjergHansen, E., Tougaard, S., 1981. Population dynamics of the harbour seal in the Wadden Sea. In: Reijnders, P.J.H., Wolff, W.J. (Eds.), Marine Mammals of the Wadden Sea. Balkema, Rotterdam, pp. 19-32. Reijnders, P.J.H., Ries, E.H., Traut, I.M., 1990. Robbenbestande. In: Lozan, J.L., Lenz, W., Rachor, E., Watermann, B., von
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Westemhagen, H. (Eds.), Warnsignale aus der Nordsee. Paul Parey, Berlin, pp. 320-324. Ross, P.S., de Swart, R.L., Reijnders, P.J.H., van Loveren, H., Vos, J.G., Osterhaus, A.D.M.E., 1995. Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbour seal fed Baltic sea herring. Environm. Health Perspect. 103, 162-167. Ross, P.S., de Swart, R.L., Timmerman, H.H., Reijnders, P.J.H., Vos, J.G., van Loveren, H., Osterhaus, A.D.M.E., 1996. Suppression of natural killer cell activity in harbour seals (Phoca vitulina) fed Baltic Sea herring. Aq. Toxicol. 34, 71-84. Schwarz, J., Heidemann, G., 1994. Zum Status der Bestlnde der Seehund- und Kegelrobbenpopulationen im Wattenmeer. In: Lozan, J.L., Rachor, E., Reise, K., von Westernhagen, H., Lenz, W. (Eds.), Warnsignale aus dem Wattenmeer. Blackwell, Berlin, pp. 296-303. Simmonds, M., Johnston, I!, French, M.C., 1993. Organochlorine and mercury contamination in UK seals. Vet. Rec. 20, 291295. Tougaard, S., 1989. Monitoring harbour seal Phoca vitulina in the Danish Wadden Sea. Helgol. Meeresunters. 43, 347-356. van Wieren, S.E., 1981. Broedbiologie van de gewone zeehond Phoca vitulina in het Nederlandse waddengebied. Report State Institute for Nature Management, Den Burg, The Netherlands. Vogel, S., 1994. Ausma8 und Auswirkungen von Storungen auf Seehunde. In: Lozan, J.L., Rachor, E., Reise, K., von Westemhagen, H., Lenz, W. (Eds.), Warnsignale aus dem Wattenmeer. Blackwell, Berlin, pp. 303-308.
URNAL
‘SEA ELSEVIER
OF RESEARCE
Journal of Sea Research 38 (1997) 161-168
Population development of harbour seals Phoca vitulina in the Wadden Sea after the 1988 virus epizootic Peter J.H. Reijnders a,*, Edith H. Ries a, Svend Tougaard b, Niels Norgaard b, Gi.inter Heidemann ‘, Jochen Schwarz ‘, Ekkehard Vareschi d, Ilona M. Traut d aInstitute for Forestry and Nature Research, Dept. Aquatic Ecology, PO. Box 167, 1790 AD, Den Burg, The Netherlands ’ Fisheries and Maritime Museum, Tarphagevej 2, DK-6710, Esbjerg, Denmark ’Research and Technology Centre Westcoast, HafentGrm, D-25761, Biisum, Germany d Dept. Aquatic Ecology, University of Oldenburg, D-26111, Oldenburg, Germany
Received 31 January 1997; accepted 17 March 1997
Abstract
The mortality as a result of the 1988 virus epizootic amongst harbour seals Phoca vitulina in the North and Baltic Seas is estimated at 60% in the entire Wadden Sea. In the years 1989-1994, a prosperous recovery of the population has been observed which is reflected in a high post-epizootic rate of increase. The average annual rate of increase for the entire area was 16%, highest in The Netherlands (average 21%) and lowest in Denmark (average 10%). This rate of increase is significantly higher than in the pre-epizootic period 1976-1987, when the population increased at a rate of around 9% per year. The difference is partly attributed to a considerably lower initial juvenile mortality after the epizootic. The present first-year mortality is statistically significantly lower than in the 1970s. It is about equal in all regions and estimated at approximately 40%, whereas it was approximately 65% in the 1970s. The post-epizootic reproductive rate in The Netherlands is significantly higher: 21% on average, against 13% before 1988; it is also higher in Niedersachsen (21 vs. 16%), but lower in Schleswig-Holstein (19 vs. 23%), while in Denmark it has not changed (both 17%). It is hypothesised that the improved reproductive rate in The Netherlands might be a result of selective mortality during the epidemic, which within the adult female segment would have predominantly affected those not reproducing. It is emphasised that though the population is recovering well, its size of almost 8800 animals in 1994 is still only one quarter of an estimated reference figure of 37000 seals around 1900. How long the recovery will continue at its present rate depends on environmental conditions in the area, such as pollution, disturbance and food resources; nor can a recurrent flickering of the epidemic be excluded. Keywords:
population development; harbour seals; Wadden Sea; virus epizootic
1. Introduction The harbour seal Phoca vitulina population in the Wadden Sea can be regarded as a discrete popula* Corresponding
author. Fax: ,+31
[email protected]
(222) 319235; E-mail:
tion, with insignificant exchange with other North Sea or Baltic stocks (Drescher, 1979). The various subpopulations have been drastically depleted in the past as a result of overhunting (Reijnders, 1992). After hunting was at last stopped throughout the Wadden Sea in 1976, the population clearly started to recover (Reijnders et al., 1990). However,
1385-l 101/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII S1385-1 101(97)00031-2
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the phocine distemper virus epizootic in 1988 interrupted this recovery and the population is assumed to have been reduced by approximately 60% (Schwarz and Heidemann, 1994). To provide favourable conditions for a recovery of the Wadden Sea population, a long-term conservation and management plan was designed (CWSS, 1992). The development of that plan and implementation of related studies required close cooperation between the countries involved, and a comprehensive 5-year research plan was drafted. Results of these studies clearly indicate that after the epizootic the population has recovered prosperously, as reflected by the high post-epizootic rate of increase. This paper discusses the population development and the course of the parameters population size, reproductive rate and initial juvenile mortality, for the entire population as well as for the various subpopulations. 2. Methods
of Sea Research 38 (1997) 161-168 Table I Annual number of surveys carried out in each region of the Wadden Sea and date (week number) when the maximum number of seals (Tmax) in the entire Wadden Sea was obtained Year
1989 1990 1991 1992 1993 1993
Number of surveys NL
NS
SH
DK
9 9 I 9 9 8
10 6 10 10 9 I
15 12 11 10 7 8
10 12 14 11 13 9
NL = The Netherlands, NS = Niedersachsen, Holstein, DK = Denmark.
Tmax (week) 26 26 25 26 31 26
SH = Schleswig-
when low-tide occurred around midday and weather conditions were suitable. This was done to minimise the possibility of double counts due to interim movement of seals between areas. Notwithstanding, in some cases conditions were such that in a region alternative days had to be found.
2.1. surveys 2.2. Data processing The basic data for the analyses in this paper originate from census results obtained during aerial surveys carried out between 1989 and 1994. Traditionally, each of the countries bordering the Wadden Sea carried out these surveys in their own region, namely Denmark (DK), Schleswig-Holstein (SH), Niedersachsen (NS) and The Netherlands (NL). Seals in the Hamburg region are included in the surveys of Niedersachsen. For this project the survey flights were synchronised and designed to cover all the haul-out sites within each of the regions under, as far as possible, similar tidal stages within one flight. Usually eight to ten flights per year have been carried out in each region. The number of surveys per region are given in Table 1. The main data were collected during the pupping season. Therefore, four to five flights were performed in June and July to obtain the pupping curve (Reijnders, 1978). Information on the distribution and number of subadult and adult harbour seals in the Wadden Sea was also collected during these flights, but additional flights proved indispensable to complete the information on animals hauled out during the moult (August). Surveys were carried out in all regions simultaneously, or at most a few days apart, preferably
2.2.1. Maximum number of seals The number of seals (including pups) counted during the simultaneous census flights has to be regarded as a minimum estimate, as it can be expected that some individuals are not hauled out and thus missed during the survey. The annual minimum estimate of the harbour seal population in the entire Wadden Sea was derived from the highest sum of the counts in the different regions during each of the simultaneous surveys in that specific year. The dates at which this annual figure was obtained (T,,,) are given in Table 1. 2.2.2. Reproductive rates The reproductive rate for the separate regions is the maximum number of pups observed. It is expressed as a percentage of the maximum total number of seals (including pups) observed in that region during that simultaneous survey in the whelping period when the highest maximum for the entire Wadden Sea was obtained. The maximum number of observed seals is used here instead of the numbers born derived from a recruitment model (Fransz and Reijnders, 1978), since in several regions no
I?J.H. Reijnders et al./Joumal
adequate data exist for several years to run the recruitment model. For the entire Wadden Sea, the respective maximum numbers of pups are added and expressed as a percentage of the maximum for the entire area observed in the whelping period. 2.2.3. Initial juvenile mortality A method to estimate initial juvenile mortality, i.e. the mortality during the first weeks of life, in harbour seals is described in detail in Fransz and Reijnders (1978) and in Fransz (1979). In this recruitment model, the time from the first pup reported to the moment the maximum number of pups was observed (T,,,,,) and the total length of the whelping period (&) were used to provide a first estimate of the juvenile mortality rate (M>. Around this first estimate a series of different values for M were tried in the model to generate a curve with the best fit to the field data. Observations carried out in 1979 on individually recognisable pups showed that weaned pups stay at the breeding colony and haul out each low tide for another three weeks (van Wieren, 1981). However, similar data obtained by the two co-authors Norgaard and Tougaard (unpubl. data) between 19901995 show a different post-weaning behaviour of pups. After approximately four weeks the pups are weaned, and they do not haul out as frequently as during the lactation period. At six weeks of age, most pups leave the breeding area and the ones that stay haul out even less. Due to these factors, juvenile mortality could be overestimated if the original model was run for a period extending four weeks after the start of the whelping season. Furthermore, when pups grow more than about six to seven weeks old it becomes increasingly difficult to distinguish them from yearlings, and therefore in some regions this age group was no longer counted separately. The model therefore needed to be modified, taking into account the potential bias in relating observed pups to surviving pups. The modifications included correction factors for less frequent haul-out after four weeks of age (60% less), declining to no haul-out after six weeks of age. Because it becomes increasingly complicated with time to quantify the possible errors introduced, the model was applied only for up to seven weeks after the start of the whelping season. The observations on the abundance of pups in the course of the whelping season, carried out in the
of Sea Research 38 (1997) 161-168
163
different regions of the Wadden Sea during 19891994, formed the basic material used in the recruitment model. Data for the entire Wadden Sea were obtained from the pup-curves for each region. At a given Julian day, the number for each region was taken from the respective curve and added to provide the sum. The length of the whelping period for the entire Wadden Sea was obtained by the ending date of the last-starting whelping period in a region and that date was compared with the date of the region where the whelping period started first. 3. Results 3.1. Population
development
During the study period, from 1989 to 1994, a total of 237 aerial surveys were carried out in the various regions of the Wadden Sea. The annual maximum numbers of harbour seals counted in the Wadden Sea are shown in Fig. 1. The sum of the various regions indicates a minimum estimate of the actual size of the harbour seal population in the Wadden Sea. It is evident that the total numbers observed have been increasing substantially since 1989. By 1994, a total of almost 8800 animals were reported, more than twice the number observed in 1989. The annual rate of increase was on average
Fig. 1. Annual maximum numbers of harbour seals registered during simultaneous surveys in the various regions of the Wadden Sea, and the respective maximum for the entire Wadden Sea. NL = The Netherlands, NS = Niedersachsen, SH = SchleswigHolstein, DK = Denmark, Total = entire Wadden Sea.
P.J.H. Reijnders et al./Joumal
164
16%. The highest rate was observed among the stock in The Netherlands (21%), and the lowest in Denmark ( 10%).
3.2. Reproductive
rates
of Sea Research 38 (1997) 161-168
[sfjl
m NL
20 10 -
The reproductive rates for the various regions and the whole area are given in Fig. 2. Apart from 1989, when in some regions the epidemic had a direct effect on numbers born, the figures are approximately equal in all regions and fluctuate around 20%. The figures for Denmark are somewhat lower than those for other regions.
Ol
1
NS
r-l
20 -
10 0
3.3. Initial juvenile
mortality
-
20
For reasons such as logistics and inclement weather conditions, not all surveys in each of the various regions provided adequate results each year for the recruitment model to be run reliably. Therefore we decided to use, as an example, the most complete data set for each region for one given year. Those are: The Netherlands, 1993; Niedersachsen, 1992; Schleswig-Holstein, 1994; Denmark, 1993. These are complemented by data for the total Wadden Sea in the years 1993 and 1994. The results are shown in Fig. 3 and Fig. 4, respectively. The corresponding data on length of the whelping period, mortality rate and initial juvenile mortality (total mortality during the first 6 weeks) are given in Table 2.
Area
NL NS SH DK Wadden Sea Wadden Sea
Year
1993 1992 1994 1993 1993 1994
Pups/births
0.71 0.70 0.73 0.71 0.70 0.70
rates (M) and initial after the start of the stocks in the various Wadden Sea
1,
M
CM
(days)
(day-‘)
(%)
37 35 37 34 44 44
0.022 0.024 0.020 0.024 0.020 0.020
33 36 31 37 34 34
NL = The Netherlands, NS = Niedersachsen, Holstein, DK = Denmark.
SH = Schleswig-
SH
10
-
0 I
DK
1
20IO-
7_-_-
OI
Total
1
20
10 Table 2 Length of whelping period (1,). mortality juvenile mortality in the first six weeks whelping (CM) in different years for the regions and for the population in the entire
r1
0I
1989
mu 1990
1991
1992
1993
1994 Years
Fig. 2. Percentage of pups from maximum numbers of harbour seals (including pups) counted in the various regions of the Wadden Sea during simultaneous flights in the whelping period. NL = The Netherlands, NS = Niedersachsen, SH = Schleswig-Holstein, DK = Denmark, Total = entire Wadden Sea.
4. Discussion 4.1. Population
development
During the study period the maximum number of harbour seals observed in the Wadden Sea more than
i?J.H. Reijnders et al./Journal
of Sea Research 38 (1997) 161-168
165
ICC
. 1500 .
*
IO00 . 500
. 0
I 190 Julian day
246
doubled, from - 4200 in 1989 to - 8800 in 1994. The annual rate of increase was on average 16%. The highest rate was observed among the stock in The Netherlands (2 l%), and the lowest in Denmark (10%). The virus epidemic in 1988 affected most harbour seal populations in Europe. After the epidemic annual rates of increase in some areas differed from those observed in the Wadden Sea: Heide-Jorgensen et al. (1992) reported rates close to zero for the population in the Skagerrak/Kattegat between 1988 and 1990, thereafter increasing to 26%. In the Wash, the population increased by only a few percent annually (J. Harwood, pers. comm.).
0
20
40
60
80
100
Days
Fig. 4. Numbers of pups surveys (left-hand diagrams) cruitment curves based on (right-hand diagrams). Bold line = number of surviving of pups.
Fig. 3. Numbers of pups counted during aerial surveys (left-hand diagram) in the various regions and recruitment curves based on the recruitment model calculations (right-hand diagrams). Bold line = number of pups born, dashed line = number of surviving pups, thin line = observed number of pups. NL = The Netherlands, NS = Niedersachsen, SH = Schleswig-Holstein, DK = Denmark.
-. Li!iJ 1994
2000
counted during simultaneous aerial in the entire Wadden Sea and rethe recruitment model calculations line = number of pups born, dashed pups, thin line = observed number
In the harbour seal population of the Wadden Sea, such high rates of increase as in the 19891994 period are unprecedented. After a similar low population size during the late 1970s the entire population increased by only 9% per year, despite full protection from hunting (Reijnders et al., 1990). This increase was also different in the various subpopulations: 12% in Denmark (Tougaard, 1989; Bogebjerg et al., 1991), 8% in Schleswig-Holstein, 7% in Niedersachsen and 8% in The Netherlands. 4.2. Reproductive
rates
Before the epidemic, substantial differences in reproductive rates existed among the various areas of the Wadden Sea, ranging from 13% in The Netherlands to 23% in Schleswig-Holstein. Since 1989 these rates have fluctuated around 20% in all regions except in Denmark, where the average is 17%. Especially in The Netherlands, the reproductive rate is significantly higher than before. This holds also for Niedersachsen, but to a lesser extent. An explanation might be that a selective mortality occurred during the epidemic. During the 1988 epidemic, high mortalities were observed in the colonies *in which pollutant levels were relatively high (Hall et al., 1992; Simmonds et al., 1993). Similarly, individ-
I?J.H. Reijnders et al./Joumal
166
uals with higher pollutant levels may have shown higher mortality. Pup production in The Netherlands and in Niedersachsen before 1988 was too low to sustain the local population. This has been ascribed to impairment of reproduction in females with high organochlorine pollutant levels (Reijnders, 1986). It is also known that high organochlorine pollutant levels reduce the immunological response (Brouwer et al., 1989; de Swart et al., 1994; Ross et al., 1995, 1996). Therefore, we hypothesise that in the pre1988 Dutch and German populations female seals still reproducing lost sufficient pollutants via pups and lactation to markedly improve their immunological conditions and thus to increase their chances of survival. According to this hypothesis we would expect higher mortality of non-reproducing females and of males, who also have no extra means to excrete pollutants. We have no data to show differences in female mortality during the epidemic. For the males, we found a mortality of 65% in Denmark; for the other regions we found no sex-related mortality. The first-year class was almost totally lost during the epidemic (Schwarz and Heidemann, 1994). The improved reproductive rate could therefore be partly of an arithmetical nature since the denominator in the division is smaller than before. However, that contribution can only be marginal. Before the epidemic, the one-year-old animals would constitute 910% of the population and that missing compartment only brings pup production up by -C 2%. The pup percentages are expected to level off within a few years because of gradual changes in the population structure, in particular an increase in the proportion of immature animals. When these age classes enter the reproductive segment of the population, pup percentages might either increase or decrease further, depending on the levels of exposure of these animals to environmental pollutants causing reproductive failure. 4.3. Initial juvenile
mortality
The simulation model is based on the assumption that the births are normally distributed over the whelping season. The data points on the right-hand side of the curves (the end of the whelping season) fit the curves less accurately than the data points on the left side (the beginning of the whelping season). This
of Sea Research 38 (1997) 161-168
is due to the stronger influence of mortality. Furthermore there is a greater possibility of underestimating the number of pups due to changes in haul-out behaviour and dispersal during the second part of the whelping period. However, the fit is considered good enough to conclude that the distribution of births is in agreement with the provision to follow a Gaussian frequency distribution. Because of the assumptions on normal distribution of births and haul-out tendencies of pups, the provided estimates on mortality rates should be regarded as indices of pup mortality. There was apparently little variation in the mortality rates between the different areas as well as between each of the areas and the total Wadden Sea. On average, the initial juvenile mortality - up to 6 weeks after the start of the whelping season amounted to approximately 34%. The additional mortality during the rest of their first year has to be estimated indirectly. An indication can be obtained by comparing the number of dead and live pups collected by nursery stations (Ecomare, Norddeich and Pieterburen, pers. comm.) in the first 6 weeks with the number collected in the other 46 weeks of their first year. That ratio was 4 : 1 and implies that another 8.5% mortality has occurred during the rest of the first year. This figure for post-breeding mortality is similar to data from other harbour seal populations, where values of around 8% were found (Harkiinen, 1987). This brings the present first-year mortality in the harbour seal population in the Wadden Sea to 42.7% (A 2.14 SD, n = 6). First-year mortality in the 1970s was estimated to be 60% in the seal population in the Dutch Wadden Sea and in that of Schleswig-Holstein (Reijnders, 1978; Reijnders et al., 1981). However, apparently the post-breeding mortality both in the Dutch and in the Schleswig-Holstein seal population at that time was slightly underestimated. The original estimate for the Dutch population was based on the difference between the calculated number of pups born and pups present in September, which revealed an average mortality of 57%. An additional mortality of 3% was assumed for the rest of their first year. That assumption was apparently not correct. This can be shown by recalculation of the additional post-breeding first-year mortality in the Dutch seal population during the end 1970s by the same procedure as mentioned for the post-epizootic period and with data for
P.J.H. Reijnders et al. /Journal of Sea Research 38 (1997) 161-168
those years. A figure of 9% was obtained and that brings the total first year mortality for that period to 66% instead of 60%. For Schleswig-Holstein, Reijnders (l.c.) used data from Drescher (1975) and again underestimated the post-breeding mortality. By using the more accurate data on the annual distribution of first-year mortality provided in Drescher (1979) the first-year mortality could be estimated in a different way and was found to be 65%. The first-year mortality in the harbour seal population in the entire Wadden Sea in the 1970s was estimated at 65.9% (f 4.0 SD, IZ = 8). Comparison of the above data for the 1970s with the post-epizootic data reveals that the present postepizootic first-year mortality is significantly lower (Student’s t-test, P < 0.01) than in the 1970s. However, it is still higher than in other harbour seal populations. For the Swedish west coast, Hark& nen (1987) assumes 30-35%, Bigg (1969) quotes 25% for British Columbia and Boulva (1973) reports 25% for Sable Island (east Canada). Disturbance may contribute to the comparatively high mortality among harbour seals in the Wadden Sea (Brasseur et al., 1996; Drescher, 1979; Reijnders et al., 1981; Vogel, 1994; Brasseur and Reijnders, 1994). 4.4. Prospects It is emphasised that the population is recovering well, though its size of nearly 8800 animals in 1994 is still only one quarter of an estimated reference figure of 37 000 seals around 1900. This figure was obtained by back-calculating how large the population must have been to sustain a given hunting pressure. The calculations start with the initial state of the population in 1960 (when aerial surveys started in all regions), an assumed range for net rate of increase, and known annual hunting records (Reijnders, 1992). How long the recovery will continue at its present rate depends on the pressure of environmental conditions such as pollution and disturbance; nor can the prospect of a recurrent flickering of the epidemic be excluded. Acknowledgements The Bezirksregierung Weser-Ems provided the survey data for Niedersachsen. The European Com-
167
mission partly funded the joint seal project under grant NORSPA 92- l/INT/OO4, B4-3030/92/01009 1. The Common Wadden Sea Secretariat administratively coordinated the joint seal project. We thank Wim Wolff and Sophie Brasseur for comments on the data and manuscript and George Fransz for modifying the recruitment model. References Bigg, M.A., 1969. The harbour seal in British Columbia. Fish. Res. Bd. Can. Bull. 172, l-33. Boulva, J., 1973. The harbour seal Phoca vitulina concolor in eastern Canada. Ph.D. Thesis, Dalhousie Univ., Nat. Lib. Ottawa, Canada, 134 pp. Bogebjerg, E., Tougaard, S., Madsen, J., Norgaard, N., 1991. Status of the harbour seal Phoca vitulina in the Danish waters, 1976-1989, and short term effects of the epidemic in 1988. Dan. Rev. Game Biol. 14, I-16. Brasseur, S.M.J.M., Reijnders, P.J.H., 1994. Invloed van diverse verstoringsbronnen op het gedrag en habitatgebruik van gewone zeehonden: consequenties voor de inrichting van het gebied. IBN-rapport 1 13. Brasseur, S.M.J.M., Creuwels, J., van der Werf, B., Reijnders, P.J.H., 1996. Deprivation indicates necessity for haul-out in harbor seals. Mar. Mamm. Sci. 12, 6 19-624. Brouwer, A., Reijnders, P.J.H., Koeman, J.H., 1989. Polychlorinated biphenyl (PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the common seal Phoca vitulina. Aq. Tox. 15, 99-106. CWSS, 1992. Sixth trilateral Governmental Wadden Sea Conference. 1991. Ministerial Declaration - Seal Conservation and Management Plan. Common Wadden Sea Secretariat, Wilhelmshaven, Germany, 55 pp. de Swart, R.L., Ross, P.S., Vedder, L.J., Timmerman, H.H., Heisterkamp, S., van Loveren, H., Vos, J.G., Reijnders, P.J.H., Osterhaus, A.D.M.E., 1994. Impairment of immune function in harbour seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23, 155-159. Drescher, H.E., 1975. Zur Biologie der Seehunde in SchleswigHolstein. Paper presented at 49th Congress of the German Society of Mammalogy 8-12 September, 1975, Innsbruck (mimeo). Drescher, H.E., 1979. Biologie, (ikologie und Schutz der Seehunde im Schleswig-Holsteinischen Wattenmeer. Beitr. Wildbiol. 1, Landesjagdverband Schleswig-Holstein, Meldorf, Germany, pp. l-73. Fransz, H.G., 1979. Estimation of birth rate and juvenile mortality from observed numbers of juveniles in a mammal population with normally dispersed reproduction. Ecol. Model. 7, 125-133. Fransz, H.G., Reijnders, P.J.H., 1978. Estimation of birth rate and juvenile mortality from observed numbers of juveniles in a seal population with normally dispersed reproduction. ICES CM 1978/N:7.
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HLkSnen, T., 1987. Feeding ecology and population dynamics of the harbour seal Phoca vitulina in Kattegat-Skagerrak. Ph.D. Thesis, Univ. Goteborg, Sweden. Hall, A., Laws, R.J., Wells, D.E., Harwood, J., Ross, H., Kennedy, S., Allchin, C.R., Campbell, L.A., Pomeroy, PI?, 1992. Organochlorine levels in common seals (Phoca vitulina) which were victims and survivors of the 1988 distemper epizootic. Sci. Tot. Environm. 115, 145-162. Heide-Jorgensen, M.-P, Hlrkonen, T., Aberg, P., 1992. Longterm effects of epizootic in harbor seals in the KattegatSkagerrak and adjacent areas. Ambio 21, 511-516. Reijnders, P.J.H., 1978. Recruitment in the harbour seal Phoca vitulina population in the Dutch Wadden Sea. Neth. J. Sea Res. 12, 164-179. Reijnders, P.J.H., 1986. Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324, 456457. Reijnders, P.J.H., 1992. Retrospective population analysis and related future management perspectives for the harbour seal Phoca vitulina in the Wadden Sea. Neth. Inst. Sea Res. Spec. Publ. Ser. 20, 193-197. Reijnders, I?J.H., Drescher, H.E., van Haaften, J.L., BogebjergHansen, E., Tougaard, S., 1981. Population dynamics of the harbour seal in the Wadden Sea. In: Reijnders, P.J.H., Wolff, W.J. (Eds.), Marine Mammals of the Wadden Sea. Balkema, Rotterdam, pp. 19-32. Reijnders, P.J.H., Ries, E.H., Traut, I.M., 1990. Robbenbestande. In: Lozan, J.L., Lenz, W., Rachor, E., Watermann, B., von
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Westemhagen, H. (Eds.), Warnsignale aus der Nordsee. Paul Parey, Berlin, pp. 320-324. Ross, P.S., de Swart, R.L., Reijnders, P.J.H., van Loveren, H., Vos, J.G., Osterhaus, A.D.M.E., 1995. Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbour seal fed Baltic sea herring. Environm. Health Perspect. 103, 162-167. Ross, P.S., de Swart, R.L., Timmerman, H.H., Reijnders, P.J.H., Vos, J.G., van Loveren, H., Osterhaus, A.D.M.E., 1996. Suppression of natural killer cell activity in harbour seals (Phoca vitulina) fed Baltic Sea herring. Aq. Toxicol. 34, 71-84. Schwarz, J., Heidemann, G., 1994. Zum Status der Bestlnde der Seehund- und Kegelrobbenpopulationen im Wattenmeer. In: Lozan, J.L., Rachor, E., Reise, K., von Westernhagen, H., Lenz, W. (Eds.), Warnsignale aus dem Wattenmeer. Blackwell, Berlin, pp. 296-303. Simmonds, M., Johnston, I!, French, M.C., 1993. Organochlorine and mercury contamination in UK seals. Vet. Rec. 20, 291295. Tougaard, S., 1989. Monitoring harbour seal Phoca vitulina in the Danish Wadden Sea. Helgol. Meeresunters. 43, 347-356. van Wieren, S.E., 1981. Broedbiologie van de gewone zeehond Phoca vitulina in het Nederlandse waddengebied. Report State Institute for Nature Management, Den Burg, The Netherlands. Vogel, S., 1994. Ausma8 und Auswirkungen von Storungen auf Seehunde. In: Lozan, J.L., Rachor, E., Reise, K., von Westemhagen, H., Lenz, W. (Eds.), Warnsignale aus dem Wattenmeer. Blackwell, Berlin, pp. 303-308.