Grey Seal Teeth As Indicators of Climate Variability. ICES CM 2004

ICES CM 2004/K:27

Not to be cited without prior reference to the author

Grey Seal teeth as Indicators of Climate Variability

M.O. Hammill

Institute Maurice Lamontagne, Box 1000, Mont-Joli, QC. G5H 3Z4

Tel: +418-775-0580 Fax: +418-775-0740 Email: [email protected]

Abstract

The impacts of environmental changes on life history parameters of marine mammals are poorly understood. This may be due to the large spatial scales that must be examined to describe environmental changes and their impacts on biological aspects of most species. Annual growth layers in the teeth of marine mammals have long been used to determine age of individual animals. In some species, changes in tooth structure also provide a record of life-history changes such as age at sexual maturity, or records of major climatic events eg El Nino. In this study, growth layer development in longitudinal sections (N=400) of Northwest Atlantic grey seal

(Halichoerus grypus) canine teeth were examined. Age, sex, and a large scale environmental variable, Minimum Cold Intermediate Layer Temperature (MCILT) all had a significant effect

(p<0.05) on the thickness of the first Growth Layer Group (GLG1), while only sex had a significant effect on the thickness of GLG2. GLG1 of males was thicker than that of females. In both sexes, GLG1 thickness declined with age. GLG1 thickness was standardized to remove the effects of age and sex and the resulting deviations were compared to changes in MCILT. During the time series (1965-1998), standardized GLG1 thickness was positively correlated with changes in MCILT (p<0.05). Correlations were also observed between fish stock biomass and MCILT.

Grey seal pups begin entering the water during February-March at which time they must also learn to feed. Changes in GLG1 thickness likely reflect the foraging success of pups during their first year of nutritional independence. Although MCILT is only one measure of environmental conditions, changes in this factor have important ecosystem effects that can also be detected at higher trophic levels.

2 Introduction

Understanding the importance of environmental variability and its linkages to changes in ecosystem properties is complicated by the differing, but often coupled time and spatial scales involved. Spatial changes may affect overall resource abundance, while temporal changes will affect the timing of resource availability with respect to the needs of the consumer. In fisheries biology, the match-mismatch hypothesis links survival of fish larvae to their ability to encounter and eat sufficient plankton prey to avoid starvation. Differences in the match between the timing of prey abundance and fish larvae can lead to significant interannual variations in fish recruitment (Brander et al. 2001). Factors such as temperature, precipitation and windstress are only a few of a suite of key environmental variables having an impact on population processes of both marine (Basson 1999;Brander, K.M. et al. 2001; O’Brien et al. 2000; Planque and Frédou

1999; Carscadden et al. 2000) as well as terrestrial ecosystems which may ultimately fall under the control of large scale global climate processes (Post and Stenseth 1999; Post et al. 1999).

One such well known phenomenon is the El Niño Southern Oscillation (ENSO), which is normally associated with the southern hemisphere, but has significant effects on both terrestrial and marine ecoystems around the world (Holmgren et al. 2001; Hofman and Powel 1998).

Another is the North Atlantic Oscillation (NAO), which has been associated with far-reaching ecosystem effects. Recent studies have identified links between NAO index variability and large herbivore populations (Milner et al. 1999; Post and Stenseth 1999), large mammalian predators

(Post et al. 1999), marine fish and zooplankton (O’Brien et al. 2000; Planque and Taylor 1998) and higher trophic level seabirds (Thompson and Ollason 2001), but have not as yet identified potential links with top trophic level marine mammal predators.

Annual growth layers in pinniped teeth are commonly used to determine age of individual animals (Laws 1962; Mansfield 1991; Bernt et al. 1996). In some species, these layers can be linked to annual events in the life cycle of individuals such as the moult, parturition, fasting and lactation (Bengston 1988; Mansfield 1991; Boyd and Roberts 1993). Changes in tooth growth patterns have been associated with large scale climatic changes in the Southern Ocean (Boyd and

Roberts 1993), but such large scale environmental effects have not been reported in North

Atlantic pinnipeds.

Here I examine the hypothesis that the pattern of growth layer deposition in the canine teeth of grey (Halichoerus grypus) seals in the Gulf of St Lawrence during the first year are linked to environmental changes as represented by a large scale oceanographic environmental variable, the Cold Intermediate Layer (CIL) Index.

Materials and Methods

The Gulf of St. Lawrence (Gulf) is a highly stratified semi-enclosed sea in eastern Canada

(Fig. 1). It is characterized by the deep (300-400 m) Laurentian Channel, which traverses the

Gulf from Cabot Strait to Honguedo Strait. A second deep channel (100-200 m) extends to the north of Anticosti Island through Jacques Cartier Strait. The area to the south of the Laurentian

Channel is quite shallow (< 75 m). The area is ice-covered for 5 months of the year but the extent is highly variable between years (Markham 1980).

The Cold Intermediate Layer is a layer of cool water sandwiched between a warm surface layer, formed by the sun’s warming of the upper portions of the water column in spring, and a deep warmer, but more saline and hence denser layer of water. This three layered structure is replaced in winter by a two layered structure as fall and winter storms lead to significant mixing

4 of the surface and intermediate layers (Fig. 2)(Gilbert and Pettigrew 1997). It is not clear what factors affect the volume and minimum temperature attained by the CIL during winter. A significant negative correlation has been observed between the NAO index and the CIL core temperature, but is not as strong as expected (r=-0.28), suggesting that other local factors also play a part in its formation and intensity (Gilbert and Pettigrew 1997).

Samples used in this study were obtained from animals that had been hunted between

1970 and 2000 for scientific reasons. Canine teeth (N=400) were extracted from the lower jaw and sectioned longitudinally (≈150 µm thick) (Mansfield 1991). The ages of individual animals were determined at the time of collection and these ages were used to obtain a selection of animals born between 1965 and 1998. The teeth were read in transmitted light under a dissecting microscope using a polarizing filter to improve contrast. Age was determined by counting Growth Layer Groups (GLG) and compared to the stated age to check for errors and to ensure consistency in identification of the GLG in the cementum (Fig. 3). The thickness of the first (GLG1) and second (GLG2) growth layer groups, total dentine and total cementum thicknesses were measured using an ocular micrometer.

For comparisons across years, variables were standardized using : (x ij –x mean ij )/sij, where

th x is the measurement for the sex and age group and xmean is the mean for the ij group and s is the standard error for the ijth group.

Results

Among grey seals differences in the thickness of the first and the second growth layer group were observed between readers, sex and with age (ANCOVA: p<0.0001). Generally the first GLG was thicker in males than among females (Fig. 4). Among older animals, there was a

5 marked reduction in the thickness of the first GLG between age 1 and age 2. For the dentine and cementum, no reader effect was observed, but differences in thickness were observed between sexes and with age (ANCOVA : dentine-reader interaction p=0.39; dentine-age interaction p=0.0001; dentine-sex interaction, p=0.0001. ANCOVA : cementum- reader interaction p=0.858; cementum-age interaction p=0.0001; cementum-sex interaction, p=0.0004).

The thickness of the dentine was not related to sex, but did increase with total body length, an index of body size (ANCOVA: dentine-sex interaction p=0.07; dentine-length interaction p<0.001). Cementum thickness was related to sex and to total length (ANCOVA: cementum-sex interaction p=0.02; cementum-length interaction p<0.001).

The normalized value of GLG1 was correlated with the minimum temperature (Tmin ) of the CIL when the animal was born (r=0.4, p<0.05), correlated with Tmin of the CIL one year prior to its birth (r=0.4, p<0.05) and negatively correlated to the thickness of the CIL layer one year prior to its birth (r= -0.4, p<0.05)(Fig. 5). A stronger correlation was observed between the normalized values of cementum thickness and the climate variables Tmin two years prior to birth

(r=0.6 , p<0.05) and the CIL thickness one and two years prior to the birth of the animal (r=-0.5, p<0.05). The normalized value of length was also correlated with Tmin of the CIL during the year of the animal’s birth (r=0.53, p=0.005). No significant relationship was observed between the climate variables and GLG2 or thickness of the dentine layer.

Discussion

Seals (Order Pinnipedia, Families Phocidae, Otariidae and Odobenidae) comprise a group of K-selected species characterized by long life-spans, late maturity and low reproductive rates

(Stearns 1976). In many ecosystems they are apex predators that integrate environmental conditions over broad temporal (decades) and spatial (100s of kilometres) scales. These suites of

6 characteristics complicate attempts to evaluate links to environmental variability, because significant population effects are only observed under the most extreme conditions (eg lack of ice leading to significant changes in juvenile survival. Sergeant 1991), or the necessary data time-series is not available. The correlation between GLG thickness of grey seal canine teeth and the CIL index provides a means of examining large scale, less extreme environmental effects on a high level marine predator. It is unlikely that changes in CIL temperatures directly affect GLG thicknesses in young grey seals. Instead, they are likely mediated through foraging success.

Pups that are more successful in foraging will develop a thicker GLG1 than less successful pups.

Less variability would be expected among older animals because they would already have learned how to forage effectively and through experience would have developed a greater suite of potential foraging areas.

The northwest Atlantic grey seal occurs along the Atlantic coast of North America between Cape Chidley at the northern tip of Labrador and southeastern United States (Lesage and Hammill 2001). Whelping occurs during December to February. The majority of pups are born on Sable Island, with a second major colony pupping on the pack ice in the southern Gulf of

St. Lawrence. The pups remain on land or ice, beside their mother until they are weaned after a short lactation (≈16 days), and begin to forage about a month later (Bowen 1991; Lesage and

Hammill 2001). Grey seals are primarily piscivores. The foraging success of naïve pups will depend on a combination of where the animal is located, the number of encounters that it makes with potential prey of an appropriate size, and an individual’s ability to develop a capture technique.

Compared to adults, newly weaned pups have a less varied diet of smaller fish and prey more on pelagic species (Hammill unpublished data). Species such as herring, mackerel and capelin are important prey species of grey seals in some areas in the Gulf of St. Lawrence.

7 Biomass/ condition information for both herring and mackerel from the Gulf of St. Lawrence show significant correlations with changes in CIL temperatures. Thus years in which conditions are favourable to fish prey, would have favourable cascading effect on grey seals.

Acknowledgements

I would like to thank V. Lafouest and R. Labbé for reading the seal teeth and J.-F.

Gosselin for help with the figures. I would also like to thank F. Gregoire, for information on mackerel, V. LaFouest, D. Gilbert and F. Proust for pulling together much of the material, their helpful discussions, and comments and I look forward to their help at the next step.

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Figure 1. Map of the Gulf of St. Lawrence. Animals used in this study were collected from the southern Gulf, and around Anticosti Island.

100

200

300 Winter

400

500

0 0

101000

202000 Summer 300 300 400 400 500 500

Figure 2. Two layered system typical of winter in the Gulf of St. Lawrence, with a cold, often ice covered layer on top of a warmer, but more dense layer below (top figure). In summer a three layered system, with a cold intermediate layer (CIL) lying between a warm layer at the surface and a deep, more dense layer lying underneath (bottom panel). Depth is in metres.

Figure 3. Longitudinal section of grey seal canine. Numbers illustrate the individual growth layer groups (GLG).

45 Females 40 Males 35 m

µ 30 25 20 15 10 GLG1 5 0123456 Age (years)

Figure 4. Change in thickness of the first growth layer group (GLG) with age of male and female Grey seals.

1.5 GLG1 CIL 1.0

0.5

0.0

Standardized data -0.5

-1.0 1965 1970 1975 1980 1985 1990 1995

Year

Figure 5. Annual changes in normalized values of the first growth layer group (GLG1) thicknesses of grey seal teeth and the cold intermediate layer index with year.