Seasonal, meteorological, tidal and diurnal effects on ... · Introduction Monitoring pinniped...

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ORIGINAL PAPER Seasonal, meteorological, tidal and diurnal effects on haul-out patterns of harbour seals (Phoca vitulina) in Iceland Sandra Magdalena Granquist 1,2 Erlingur Hauksson 3 Received: 6 March 2015 / Revised: 5 February 2016 / Accepted: 7 February 2016 Ó Springer-Verlag Berlin Heidelberg 2016 Abstract It is of critical importance to identify factors that affect harbour seal haul-out patterns to improve the accuracy of harbour seal censuses. In this study, haul-out patterns of harbour seals (Phoca vitulina) were investigated during different conditions at several major haul-out sites on Vatnsnes peninsula, NW Iceland (65°40 0 N and 20°48 0 W), over the 2008–2011 period. A seasonal haul-out pattern was detected among the seals, with the maximum number of seals on land found in July for most of the sites. Analyses of data for harbour seals on Vatnsnes indicate that the main pupping period occurs during late May to the beginning of June and moulting during late July to early August. Abundance at the sites increased with rising air temperature and decreased with increased windspeed and rising tides. However, no evidence that precipitation or cloud cover affected haul-out behaviour of the seals was detected. The diel haul-out pattern was investigated thor- oughly in one of the haul-out sites and the results under- lined the effect of tidal flucturation, air temperature and wind direction on the haul-out behaviour of harbour seals in the area. Results from this study can be used to improve the survey design when estimating the population size of harbour seals in Iceland and applied more broadly to the study of haul-out behaviour of harbour seals. Keywords Harbour seal Haul-out Diurnal pattern GLM Iceland Introduction Monitoring pinniped populations is of great importance for their management and conservation. Aerial counting sur- veys of harbour seals (Phoca vitulina) provide information about the total number of seals on land, and the number of counted individuals may serve as a population index for between-year comparisons (Gilbert et al. 2005; Lonegran et al. 2013). Stakeholders such as government agencies, however, often demand an estimate of the whole popula- tion. Since pinnipeds only spend part of their time on land, the total number of seals in the population has to be esti- mated by models incorporating the number of counted individuals together with the probability of seals spending time on land (Simpkins et al. 2003; ICES 2007; Lowry et al. 2008; Bjørge et al. 2010; Hauksson and Einarsson 2010; Harvey and Goley 2011). To improve the survey design and increase the accuracy of harbour seal censuses made from aerial surveys, it is of critical importance to identify those conditions under which the seals are most likely to haul out of the water (i.e., to rest on land). One reason for hauling out may be to reduce the pre- dation risk from marine predators such as killer whales (Orcinus orca) (Watts 1992; London et al. 2012). Since harbour seals usually haul out in groups, the individual predation risk is decreased further (Hamilton 1971). Har- bour seals give birth and nurse their pups on land, and it has been frequently described that harbour seals haul out to a larger extent during the pupping and nursing periods (Boulva and McLaren 1979; Hauksson 1993). Another reason for hauling out may be that seals save energy by & Sandra Magdalena Granquist [email protected] 1 The Icelandic Seal Center, Brekkugata 2, 530 Hvammstangi, Iceland 2 Institute of Freshwater Fisheries, Keldnaholt, 112 Reykjavı ´k, Iceland 3 Vo ¨r Marine Research Center at Breiðafjo ¨rður, Norðurtangi 3, 355 O ´ lafsvı ´k, Iceland 123 Polar Biol DOI 10.1007/s00300-016-1904-3

Transcript of Seasonal, meteorological, tidal and diurnal effects on ... · Introduction Monitoring pinniped...

Page 1: Seasonal, meteorological, tidal and diurnal effects on ... · Introduction Monitoring pinniped populations is of great importance for ... of Iceland 2013). Day of the year, windspeed,

ORIGINAL PAPER

Seasonal, meteorological, tidal and diurnal effects on haul-outpatterns of harbour seals (Phoca vitulina) in Iceland

Sandra Magdalena Granquist1,2 • Erlingur Hauksson3

Received: 6 March 2015 / Revised: 5 February 2016 / Accepted: 7 February 2016

� Springer-Verlag Berlin Heidelberg 2016

Abstract It is of critical importance to identify factors

that affect harbour seal haul-out patterns to improve the

accuracy of harbour seal censuses. In this study, haul-out

patterns of harbour seals (Phoca vitulina) were investigated

during different conditions at several major haul-out sites

on Vatnsnes peninsula, NW Iceland (65�400N and

20�480W), over the 2008–2011 period. A seasonal haul-out

pattern was detected among the seals, with the maximum

number of seals on land found in July for most of the sites.

Analyses of data for harbour seals on Vatnsnes indicate

that the main pupping period occurs during late May to the

beginning of June and moulting during late July to early

August. Abundance at the sites increased with rising air

temperature and decreased with increased windspeed and

rising tides. However, no evidence that precipitation or

cloud cover affected haul-out behaviour of the seals was

detected. The diel haul-out pattern was investigated thor-

oughly in one of the haul-out sites and the results under-

lined the effect of tidal flucturation, air temperature and

wind direction on the haul-out behaviour of harbour seals

in the area. Results from this study can be used to improve

the survey design when estimating the population size of

harbour seals in Iceland and applied more broadly to the

study of haul-out behaviour of harbour seals.

Keywords Harbour seal � Haul-out � Diurnal pattern �GLM � Iceland

Introduction

Monitoring pinniped populations is of great importance for

their management and conservation. Aerial counting sur-

veys of harbour seals (Phoca vitulina) provide information

about the total number of seals on land, and the number of

counted individuals may serve as a population index for

between-year comparisons (Gilbert et al. 2005; Lonegran

et al. 2013). Stakeholders such as government agencies,

however, often demand an estimate of the whole popula-

tion. Since pinnipeds only spend part of their time on land,

the total number of seals in the population has to be esti-

mated by models incorporating the number of counted

individuals together with the probability of seals spending

time on land (Simpkins et al. 2003; ICES 2007; Lowry

et al. 2008; Bjørge et al. 2010; Hauksson and Einarsson

2010; Harvey and Goley 2011). To improve the survey

design and increase the accuracy of harbour seal censuses

made from aerial surveys, it is of critical importance to

identify those conditions under which the seals are most

likely to haul out of the water (i.e., to rest on land).

One reason for hauling out may be to reduce the pre-

dation risk from marine predators such as killer whales

(Orcinus orca) (Watts 1992; London et al. 2012). Since

harbour seals usually haul out in groups, the individual

predation risk is decreased further (Hamilton 1971). Har-

bour seals give birth and nurse their pups on land, and it

has been frequently described that harbour seals haul out to

a larger extent during the pupping and nursing periods

(Boulva and McLaren 1979; Hauksson 1993). Another

reason for hauling out may be that seals save energy by

& Sandra Magdalena Granquist

[email protected]

1 The Icelandic Seal Center, Brekkugata 2, 530 Hvammstangi,

Iceland

2 Institute of Freshwater Fisheries, Keldnaholt, 112 Reykjavık,

Iceland

3 Vor Marine Research Center at Breiðafjorður, Norðurtangi 3,

355 Olafsvık, Iceland

123

Polar Biol

DOI 10.1007/s00300-016-1904-3

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spending time on land during periods of warm and calm

weather compared with spending time in cold waters (Pauli

and Terhune 1987a; Watts 1992). Harbour seals also haul

out more during the moulting period when they shed their

fur since being on land elevates the skin temperature,

which can induce a faster moult (Feltz and Fay 1966; Ling

1970; Reder et al. 2003; Cronin et al. 2009; Paterson et al.

2012). Because of the largest fraction of harbour seals

spending time on land during the pupping and/or moulting

periods, these periods are usually chosen for aerial count-

ing surveys (Mogren et al. 2010).

A number of studies have explored the effects of various

environmental factors on pinniped haul-out behaviour

(Gaspari 1994; Bondo-Harders 2003). Several meterologi-

cal factors that affect the number of harbour seals hauling

out have been identified, for example, windspeed and wind

direction (Brasseur et al. 1996; Bondo-Harders 2003;

Simpkins et al. 2003), temperature (Pauli and Terhune

1987a; Brasseur et al. 1996; Reder et al. 2003; Simpkins

et al. 2003), cloud cover (Pauli and Terhune 1987a; Grel-

lier et al. 1996) and precipitation (Pauli and Terhune

1987a; Grellier et al. 1996; Simpkins et al. 2003). Fur-

thermore, authors have also described diurnal haul-out

patterns, with more seals hauling out during low tide. This

may be explained by haul-out sites becoming more

exposed and easier to access for the seals during low tide.

Other studies have suggested that it is more effective for

seals to forage during high tide when possible littoral

organism prey species visit the watercovered littoral zones

(e.g. Pauli and Terhune 1987b; Reder et al. 2003; Renner

2005). Several authors have also shown that the time of day

can affect the harbour seal haul-out pattern, with a haul-out

peak occurring at midday, which might partly be explained

by the air temperature usually peaking at midday. Age and

gender may also explain some of the variability in haul-out

behaviour (Thompson and Rothery 1987; Thompson et al.

1989; Kovacs et al. 1990; Harkonen et al. 1999).

Relationships between conditions affecting the propor-

tion of hauled-out seals in a population are complex and

hence tend to be quite variable not only between years, but

also between locations because of site-specific differences

(e.g. Terhune and Almon 1983; Hauksson 1985; Gaspari

1994; Grellier et al. 1996; Watts 1996; Reder et al. 2003;

Patterson and Acevedo-Gutierrez 2008; Mogren et al.

2010). Such local variation in harbour seal haul-out pat-

terns indicates that population- or site-specific analyses of

conditions affecting haul-out patterns may be required to

obtain the highest possible accuracy in population esti-

mates (Mogren et al. 2010).

In Iceland, 10 harbour seal censuses were carried out

between 1980 and 2011 (Hauksson and Einarsson 2010;

Granquist et al. 2011). The latest survey conducted in 2011

resulted in an estimated population size of 11,000

individuals (95 % confidence interval 8000–16,000 indi-

viduals) (Granquist et al. 2011; Marine Research Institute

of Iceland 2013). Day of the year, windspeed, tidal height

and hours to solar noon have been suggested as factors that

may affect the haul-out probability of harbour seals in

Icelandic conditions (Hauksson 1993, 2010). Based on

these indications all Icelandic abundance surveys have

been conducted mainly during August, with counts made

within ±3 h of low tide. However, previous studies of the

factors affecting the haul-out probability in Iceland were

restriced to the summer time and based on a rather limited

number of observations. In addition, previous Icelandic

studies were based on aerial surveys, meaning that data

were only recorded during days when the weather was

good enough to manoeuvre a small airplane. There is

therefore a lack of information regarding the seasonal

variation in harbour seal haul-out behaviour for Icelandic

environmental conditions and further there is very little

understanding of how meterological factors may affect

haul-out patterns of harbour seals living under Icelandic

conditions.

The aim of the study was to test factors affecting the

haul-out behaviour of Icelandic harbour seals. Through

observation of harbour seals on seven haul-out sites on

Vatnsnes peninsula, NW Iceland, we invstigated the pos-

sible effects of season, height of tide, time of day and

meteorologic factors (air temperature, cloud cover, precip-

itation, wind speed and wind direction) on haul-out patterns.

In addition, we tested the diurnal effect more thoroughly at

one of the haul-out sites (Illugasstadir). An increased

knowledge regarding what factors need to be taken into

consideration when estimating population sizes from counts

can improve aerial survey design and population estimation

models. Results from the present study could hence be

applied for harbour seal management and conservation

purposes in both Icelandic conditions and elsewhere.

Methods

Study area

Vatnsnes peninsula, NW Iceland (65�400N, 20�480W)

(Fig. 1), is one of the areas in Iceland with the highest

density of harbour seals (Hauksson 2010). During the

2008–2011 period, harbour seal abundance was monitored

in seven breeding and haul-out sites on Vatnsnes pennin-

sula: Svalbard, Naggur, Illugastadir, Hindisvik, Krossanes,

Osar and Bjargaos (Fig. 1; Table 1). Seal-watching sites

have recently been established at some of the sites (Gran-

quist and Nilsson 2013; Granquist and Sigurjonsdottir

2014), while Hindisvik is a former seal-watching site

where seal watching has been prohibited since 2008. The

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Bjargaos estuary is an inlet for some of the richest salmon

rivers in the northwestern part of Iceland. In the estuary,

harbour seal pups have been hunted in nets or shot since

several years before the study to protect salmon fishing

interests, although not between 2008 and 2010. In 2011,

however, several seals were shot in the estuary (Fig. 1;

Table 1).

Monitoring of seals

Seals on land were counted by a land-based observer

equipped with 7 9 50 binoculars and situated approximately

100 m from the seals with the exception of Bjargaos,

where the seals were counted from a distance of 1.5 km

using a field-scope Leica Televidd 77 20—60 9 77 zoom.

At Vatnsnes tides are diurnal with an interval of 12 h and

25 min between low tides. To investigate effects of sea-

son and meterological variables on haul-out behaviour,

harbour seals were monitored at the seven haul-out sites

during low tide (±2.5 h) of every spring tide between

January and November throughout the years 2008–2011

(Table 1). Due to bad weather conditions and visibility, it

was not possible to conduct observations during the

December spring tide in any of the years. To investigate

GREENLAND

ICELAND

VATNSNES

NORWAY

Hindisvik

Illugastadir

BjargaosSvalbard

Osar

Naggur

Krossanes

Arctic circle

Fig. 1 Map of Iceland indicating the location of the Vatnsnes peninsula and the Vatnsnes peninsula with the seven sites included in the study

marked

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the effects of time of day and tide height on the haul-out

pattern, more frequent observations were made between

June and August (three times per week at various times

and tidal states for comparison). All observations were

carried out during the day and none were recorded at

night. The data were somewhat unbalanced, with obser-

vations lacking for some sites in 2008, 2009 and 2011. At

Krossanes observations were only made in 2010 and

2011. Furthermore, no observations were made at Osar

and Bjargaos estuaries in 2008, and the data from Bjar-

gaos collected in 2011 were excluded from the analyses

because of seal hunting in the area (Table 1).

Possible diurnal patterns in harbour seal haul-out

behaviour were further investigated in one of the sites

(Illugastadir). From June to August in the period

2008–2011 2-h observation sessions were performed

twice every observation day and the seals were counted

with 15-min intervals during the observation sessions.

The observation sessions were initiated at different times

and distributed between 08:00 and 21:00 over 113 days.

The observations were made from a fixed point between

two cliffs, where the observer could not be easily detected

by the seals. To minimise observer bias, the recordings

were standardised by regularly performed inter-observer

reliability tests (agreement between observers [95 %).

All observations made at Illugastadir were used to assess

the diurnal effects; however, when analyses of the sea-

sonality and effect of meteorological and tidal variables

were carried out (see above), only two randomly chosen

counts from each day were included for Illugastadir in

order to match the data collection to the six other haul-out

sites.

Tide height and time to low tide were calculated using

the method presented in the Tide Almanac published by the

Icelandic Coast Guard (Icelandic Coast Guard 2009, 2010,

2011). Cloud cover (% of sky covered with clouds)

and precipitation (raining = 1; not raining = 0) were

recorded during every observation. Information about air

temperature and wind speed were obtained from the Ice-

landic Meteorological Institute.

Statistical analyses

The relationship between the total number of harbour seals

at the different sites and possible explanatory variables was

analysed with generalised linear models (GLMs), or gen-

eralised additive modelling (GAM), generalised linear

mixed modelling (GLMM) and generalised additive mixed

modelling (GAMM) in cases where correlations between

the observations were found (Zuur et al. 2009). All possible

prediction variables, as well as interactions between vari-

ables, were included in the initial models (two models;

seasonal and environmental). We examined whether the

following variables affected the haul-out pattern of the

seals: year, season (measured as day of the year), time of

day, height of tide and meterological variables (precipita-

tion, cloud cover, temperature, wind speed and wind

direction). The importance of the association of each

variable with the number of hauled-out seals was deter-

mined by individually deleting one variable at a time and

examining changes in the Akaike information criteria

(AIC), deviance and maximum likelihood of the models.

Only the variables that were found to have a significant

(p\ 0.05) relationship with the number of hauled-out seals

were kept in the final models. In cases of correlations

between different possible predictor variables [estimated

with Pearson’s product moment correlation (rp) or Spear-

man’s rank correlation rho (rs)], only one of the variables

was included in the final model. Due to warmer tempera-

tures during the summer, there was a correlation between

the day of the year and temperature (rp = 0.32, t = 18.61,

df = 2990, p\ 0.001); hence, the temperature data were

excluded from the model where seasonality (day of the

year) was investigated. Further, time to midday was highly

correlated with height of tide (rp = -0.13, t = -7.04,

df = 2991, p\ 0.001); time to midday was correlated with

Table 1 Haul-out sites, habitat

descriptions, seal watching

occurrences and total numbers

of observations (n) for the

different years

Haul-out site Habitat description Seal watching n2008 n2009 n2010 n2011

Svalbard Rocky skerries Yes 54 101 57 39

Naggur A small skerry No 34 100 90 43

Illugastadir Rocky skerries Yesa 450 834 641 38

Hindisvik Rocky shore and skerries Nob 29 49 51 39

Krossanes Rocky shore and skerries No – – 40 35

Osar Lagoon estuary, sandy shore Yes – 44 49 41

Bjargaos River estuary, sandy shore Noc – 45 46 –

a Except May 20–June 20b Seal watching was permanently prohibited in 2008c Disturbances due to salmon fishing and seal hunting

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time to low water (rp = 0.05, t = 3.23, df = 2991,

p = 0.001) and tide height and time to low water were

correlated (rp = 0.05, t = 2.50, df = 2991, p = 0.01)

since observations were only carried out during the day.

The effect of time of day on haul-out behaviour was

therefore excluded from the models investigating season

and meterological effects on haul-out behaviour.

The negative binomial distribution was used as the basis

for the GLM analysis, which turned out to give a better fit

than the Poisson distribution. The negative binomial dis-

tribution’s GLM routine estimates the dispersion parameter

theta (/) and standard errors of the parameters. In GAM,

GAMM and GLMM the value of the calculated / from the

negative binomial GLM was used in fitting of the data. The

fit of models was investigated with residual deviance (RD),

null deviance (ND), deviance explained [(ND - RD)/ND]

(AIC) and the 2 9 log likelihood (Zuur et al. 2009).

Neither the seasonal nor diurnal (Illugastadir) data

showed a significant trend in abundances of harbour seals

in relation to years in the 2008–2011 period. Therefore,

data were pooled for all years in the analysis. Since the size

of the different haul-out sites varied substantially with

regard to the average number of seals observed, the site

was included as a variable in all models: a fixed or random

variable depending on the model type.

At Illugastadir, where several daily data points were

available, diurnal effects on haul-out behaviour were fur-

ther investigated by plotting haul-out data in relation to

hours from low tide (TLW) using a locally weighted

regression procedure for fitting a regression curve by

smoothing the dependent variable (TLW) as a function of

the independent variable (harbour seal counts)—loess

smoothing. All statistical analyses were performed in R (R

Development Core Team 2009) and using the MASS

library (Venables and Ripley 2002).

Results

Effect of seasonal factors

The mean number of seals hauling out in each month on

the different sites is described in Table 2. At all sites,

seasonality in haul-out patterns was detected, with the

maximum average for most sites observed in July. At

Illugastadir, the average number of seals hauling out was

similar for both July and August, while in the estuary

(Bjargaos) the maximum number of seals hauled out in

June (Table 2).

Results of the GAMM seasonal model using the value

of the theta from the negative binomial GLM on the sea-

sonal data, with sites and day of the year as a smoothing

term, explained 66.3 % of the variability in the data Table

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Polar Biol

123

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(Rad2 = 0.663, scale est. = 0.964 and n = 2228). The dis-

persion parameter for the negative binomial distribution (/)

was 1.76. All sites were significantly different from the

reference site Bjargaos (p\ 0.001) and all sites except

Naggur generally had a greater abundance of harbour seals

than the reference site Bjargaos (Table 2). The smoothing

term, day of the year, had an approximate significance of

p\ 0.001. Across all sites harbour seals were less likely to

haul out during winter than spring, summer and autumn.

Figure 2 shows that in general for the whole Vatnsnes area,

there was an indication of a bimodal haul-out pattern

during the summer months, one peak at the end of May/

beginning of June and a second in the end of July (Fig. 2).

When the sites were investigated individually, the curve of

hauling-out seals to the day of the year was bimodal, with

the first peak usually occurring at the end of May/begin-

ning of June and the second in late July/early August.

Bjargos was an exception, however, with only a single

peak observed in June (Fig. 3).

Effect of environmental factors

To test the dependency of hauling out on temperature and

other environmental variables, only data collected during

the summer months (June–September), when the temper-

ature was relatively constant, were used. The results of the

GLMM with / equal to 1.7 from the analysis of negative

binomial distribution using GLM indicated that harbour

seals were overall more likely to haul out when the air

temperature was warmer, windspeed was lower and heights

of tides were lower (Table 3). There was, however, varia-

tion between sites and all sites showed significantly dif-

ferent abundances of harbour seals compared to the

reference site of Bjargaos (p\ 0.001). The harbour seal

abundance was greater at most sites compared to the

reference site, the exceptions being Naggur and Svalbard

where the abundance was lower. The interaction between

sites and air temperature showed the highest variance

(Table 3). The GLMM model with sites as fixed effects and

site, air temperature, windspeed and tide height as random

effects gave an AIC of 18,281.8, a maximum log likelihood

of -9128.9 and a deviance of 18,257.8. A GLMM model

with the same variables, but with the sites as a random

effect, did not converge (Figs. 4, 5, 6). None of the other

meterological variables included in the initial model (cloud

cover, precipitation or wind direction) had an effect on the

model (Table 3).

There was a correlation between the abundance of har-

bour seals in many sites and the highest correlation was

found between Illugastaðir and Svalbard (Table 4). In the

GAMM used for estimating the effect of the variables of air

temperature, windspeed and tide height on the number of

harbour seals hauling out, sites were the fixed variables and

the former variables were used as smoothing terms. Sites

were all significantly different from the reference site

Bjargaos (p\ 0.001); the smoothing terms were significant

too: air temperature (p\ 0.001), windspeed (p = 0.04)

and tide height (p\ 0.001). The GAMM explained 62.5 %

of the variability of the data (Rad2 = 0.625, scale esti-

mate = 0.849 and n = 2055).

Diurnal effect and environmental variables

At Illugastadir, where several daily observations were

made, a clear diurnal pattern was found with the average

highest number of seals hauling out around low tide: i.e.

from 2 h before to 3 h after maximum low tide (Fig. 6).

Further, more seals hauled out with increasing air tem-

perature, at wind directions of 50� and 180�, and in the

summer (Fig. 7). The GAM results, indicating this,

Fig. 2 Estimated smoother for

the day of the year obtained by

the GAMM applied on the

number of harbour seals (Phoca

vitulina) hauling out; all data

combined for the Vatnsnes area

(indicated with an unbroken

line), 95 % pointwise

confidence bands (indicated

with broken lines) and residuals

from the GAMM (indicated

with dots)

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explained 38.5 % of the deviance, Rad2 = 0.5, unbiased risk

estimator (UBRE) = -0.18712, scale estimate = 1 and

n = 1921. All smooth terms were highly significant

(p\ 0.001) and the intercept was significantly different

from zero (p\ 0.001). The / for the negative binomial

distribution used in the GAM was 2.7.

Discussion

The results presented in this study are derived from a large

data set, spanning 4 full years, and are geographically

limited to Vatnsnes, NW Iceland. It is therefore extremely

valuable for elucidating the effect of both time of year and

environmental variables on the haul-out behaviour of har-

bour seals in the area.

The haul-out pattern of harbour seals in Vantsnes

depends on the time of year and we found a bimodal

temporal distribution during the summer in all haul-out

sites except for one. In addition, we observed a clear

positive effect of air temperature and negative effect of

Fig. 3 Ln (abundance) of harbour seals (Phoca vitulina) hauling out each decimal day of the year on the seven sites; data from all years

combined. Unbroken lines indicate the trend estimated with a loess smoother

Table 3 Results of the generalised linear mixed model (GLMM) fit

for abundance of harbour seals (Phoca vitulina) in relation to sites in

the Vatnsnes area and environmental variables by maximum likeli-

hood, with negative binomial / = 1.7, tide height (TH), windspeed

(WS) and air temperature (AT)

Random effects Variance SD Z value (p)

TH:WS:AT:site 4.379 2.093 –

WS:AT:site 0.0 0.0 –

AT:site 4.453 2.110 –

Site 0.0 0.0 –

Fixed effects Estimate SE Z value (p)

Intercept 1.8298 0.1070 17.101 (p\ 0.001)

Bjargaos Reference site – –

Hindisvık 2.6151 0.1264 20.685 (p\ 0.001)

Illugastadir 2.0908 0.1084 19.284 (p\ 0.001)

Krossanes 1.0713 0.1459 7.343 (p\ 0.001)

Naggur -0.5543 0.1191 -4.655 (p\ 0.001)

Osar 3.3092 0.1315 25.171 (p\ 0.001)

Svalbard 0.8307 0.1195 6.954 (p\ 0.001)

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windspeed on the number of harbour seals hauling out

during summer. We also found evidence that lower tide

heights resulted in more seals hauling out. Summer data

from Illugastadir further confirmed that seal haul-out pat-

terns follow changes in tide height over the course of each

day. The direction of the wind also influenced the number

of harbour seals hauling out and seals were more likely to

haul out when the wind direction was northeasterly (50�) or

southerly (180�). The northeasterly wind at Illugastadir is

directed landwards, and due to the topography at Illugas-

tadir the seals are sheltered when the wind blows in this

specific direction. Southerly winds blow along the coast

and the seals are also quite sheltered when the wind blows

in this direction.

At all sites some evidence of seasonality was observed

(Table 2; Figs. 2, 3). The overall minimum counts of

hauling-out harbour seals was observed in the winter

months, while the highest counts for most sites were

observed in July. This is to some extent in agreement with

earlier studies (Hauksson 1993, 2010). Although the stud-

ies of Hauksson (1993, 2010) were built on fewer obser-

vations, he found that at Vatnsnes (Hauksson 1993) and in

other areas of Iceland (Hauksson 2010) the maximum

number of harbour seals hauled out in July and August.

Similar patterns have also been found among harbour seals

in other areas of the world (e.g. Sullivan 1980; Renner

2005; Cronin et al. 2009; London et al. 2012). Previous

studies have suggested that harbour seals are more likely to

spend time on land during the pupping season while

nursing their young and again later during the moulting

period (Boulva and McLaren 1979; Hauksson 1993; Cronin

et al. 2009). Research on harbour seal females in Scotland

using radio-tracking has also shown that lactating females

spend more time feeding during the latter part of the lac-

tation period and less time hauling out (Thompson et al.

1994). The bimodal nature of the smoothing curve of

harbour seal abundance against the day of the year indi-

cates therefore that pupping of harbour seals on Vatnsnes

peninsula occurs in late May to early June, while the

moulting period occurs in late July to early August

(Figs. 2, 3) (Granquist and Hauksson unpublished).

The Bjargaos river estuary, leading to several important

salmon rivers (Gudbergsson 2012), was the only site in the

present study where a bimodal seasonal pattern was not

found. This may be due to the limited the number of

observations, or it may be that harbour seals use this area as

a feeding site rather than a resting site and hence spent

more time in this area feeding between the periods of

pupping and moulting. The estuary was moreover the only

area where the average maximum number of seals hauling

out peaked in June and a single peak found in late June for

this area supports this hypothesis, since it coincides with

salmon abundance in the estuary (Fig. 2). Prey availability

was however not further investigated in this study, pri-

marily because of the lack of data. A positive correlation

between the numbers of seals resting on land with air

temperature has also been described in some previous

studies (e.g. Watts 1996; Mogren et al. 2010, but see

Grellier et al. 1996), which suggests that seals save energy

by resting on land during warm periods (Pauli and Terhune

1987a; Watts 1992).

Neither precipitation nor cloud cover affected the har-

bour seal haul-out pattern in our models. Windspeed was,

however, found to affect the seals on Vatnsnes and at

Illugastadir wind direction affected haul-out patterns over

the summer months. The weather stations logging wind

speed and direction data were located between 20 and

40 km from the different haul-out sites investigated in the

study; therefore local variation in wind speed might have

affected the results. Further, effects of wind direction

Fig. 4 Estimated smoother for

air temperature obtained by the

GAMM applied on the number

of harbour seals (Phoca

vitulina) hauling out in the

Vatnsnes area (indicated with

an unbroken line), 95 %

pointwise confidence bands

(indicated with broken lines)

and residuals (indicated by dots)

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depend on site-specific topography and might hence have

been important at other sites than Illugastadir, although not

detected for methodological reasons.

All of the environmental factors tested in this study have

frequently been described to affect haul-out patterns in

other areas. Mogren et al. (2010), studying sites in Ves-

teralen, Norway, found that increased cloud cover resulted

in fewer seals hauled out in July (Mogren et al. 2010). A

relationship between cloud coverage and haul-out fre-

quencies has also been found in other studies (e.g. Pauli

and Terhune 1987a; Grellier et al. 1996). Wind speed (e.g.

Harders 2003; Simpkins et al. 2003) as well as wave action

(Pauli and Terhune 1987a; Thompson 1989) has been

suggested to affect the haul-out frequency of harbour seals

by several authors and Simpkins et al. (2003) found that

maximum haul-out occurred at a wind speed of 10 miles/h.

Fig. 5 Estimated smoother for

combined effects of air

temperature and windspeed

obtained by the GAMM applied

on the number of harbour seals

(Phoca vitulina) hauling out in

the Vatnsnes area (indicated by

unbroken lines), 95 % pointwise

confidence bands (indicated by

broken lines) and residuals

(indicated by dots)

Fig. 6 Estimated smoother for

tide height obtained by the

GAMM applied to the number

of harbour seals (Phoca

vitulina) hauling out in the

Vatnsnes area (unbroken line),

95 % pointwise confidence

bands are indicated by broken

lines, and residuals of the

GAMM are indicated by dots

Table 4 Correlation of fixed

effects (sites) in the GLMM fitSites Intercept Hindisvık Illugastaðir Krossanes Naggur Osar

Hindisvık -0.828

Illugastadir -0.954 0.791

Krossanes -0.711 0.590 0.680

Naggur -0.828 0.689 0.796 0.593

Osar -0.792 0.657 0.757 0.564 0.660

Svalbard -0.865 0.718 0.828 0.617 0.723 0.687

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However, Brasseur et al. (1996) observed that air temper-

ature had a larger effect than wind speed on the haul-out

behaviour of harbour seals in captivity and Grellier et al.

(1996) did not find any consistent effect of wind speed or

wind chill-adjusted temperatures on the number of harbour

seals hauling out in Morey Firth, Scotland. Evidence that

harbour seals haul out less during percipitation has also

been reported (Pauli and Terhune 1987a; Grellier et al.

1996; Simpkins et al. 2003).

The effect of time of day could not be assessed sepa-

rately in this study because it was highly correlated with

tide height. A negative correlation between increasing tide

height and harbour seal abundance was found for all sites

in the study (Fig. 6). At Illugastadir, where several daily

observations were made during the summer months to

investigate diurnal effects more thoroughly, the highest

number of seals was on average observed on land around

low tide, from 2 h before to 3 h after maximum low tide.

These findings therefore further underline a diurnal haul-

out pattern (Figs. 7, 8). Tidal state was previously sug-

gested to be an important factor influencing haul-out pat-

terns of harbour seals on the coast of Iceland (Hauksson

1985). Hauksson (2010) observed that tide height, time of

day and wind force significantly affected the haul-out

behaviour of Icelandic harbour seals in the 1980–2006

period. Harbour seals following a diel tidal haul-out cycle

is in agreement with previous studies and often numbers on

shore were found to peak near midday (e.g. Yochem et al.

1987; Reder et al. 2003; Simpkins et al. 2003; Renner

2005; Cronin et al. 2009; London et al. 2012). Further,

Cronin et al. (2009) found individual variation in the

influence of time of day on haul-out behaviour.

The variation in haul-out behaviour found between sites

in the present study was greater than anticipated, taking

into consideration their geographical proximity. However,

local and between-year variation in haul-out behaviour has

been reported by several authors (e.g. Terhune and Almon

1983; Hauksson 1985; Watts 1996; Reder et al. 2003;

Patterson and Acevedo-Gutierrez 2008; Mogren et al.

2010) and suggested reasons for the variation are demo-

graphic changes within the population (Thompson 1989;

Harkonen et al. 1999; Reder et al. 2003), differences in

topography and habitat types (Hauksson 2010), ice cover-

age (Calambokidis et al. 1987; Lesage et al. 2004), fluc-

turations in prey availability (Thompson 1988; London

et al. 2012) or anthropogenic disturbance (Henry and

Hammill 2001; Granquist and Sigurjonsdottir 2014;

Andersen et al. 2014). Furthermore, although harbour seals

Fig. 7 Total number of harbour seals (Phoca vitulina) in relation to hours from low tide, fitted with a linear loess smoother. The 12 observation

days with the highest frequency of observations are shown as examples in the figure

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often have been described to show high site fidelity to their

haul-out sites (e.g. Yochem et al. 1987; Dietz et al. 2013;

Andersen et al. 2014), these factors may also cause annual

variation in preferred sites. In some cases harbour seals

also move between feeding and breeding areas (Thompson

1989), which are nevertheless often in similar locations

(Suryan and Harvey 1998).

Testing individual variation due to gender or age was not

possible in this study because of the large distance from

which the animals were observed. Such factors may never-

theless affect the haul-out behaviour of harbour seals (e.g.

Thompson and Rothery 1987; Kovacs et al. 1990; Harkonen

et al. 1999; Reder et al. 2003); hence, extrapolating infor-

mation regarding haul-out behaviour from a few haul-out

areas to a whole population is unsuitable (Mogren et al.

2010). As an example, Harkonen et al. (1999) showed in

their study that no age/sex group of harbour seals was rep-

resentative for the whole population in terms of haul-out

behaviour.

It has been suggested that differences in habitat types

can be a reason for between-site variation in the haul-out

pattern (Thompson 1989; Hauksson 2010) and this may

partly explain the between-site variation that we found in

this study despite the closeness of the haul-out sites. In

haul-out sites covered by water at high tide, it is impossible

for the seals to haul out as the water rises, while at other

locations seals might be able to move higher up when the

water starts to rise and hence haul out longer, and in the

latter case the state of tide height will have less effect

(Thompson 1989). All of the sites included in the present

study are partly covered during high tide, although Hin-

disvık and Krossanes are the sites least affected by tides in

this study. Some areas are more exposed to wind or waves

than others, causing weather-dependent variation in haul-

out feasibility between different sites (Pauli and Terhune

1987a; Thompson 1989), despite geographical closeness,

although this was not tested in the present study.

In cases where predator abundance is high, harbour seals

may prolong their haul-out bouts to avoid predation (London

et al. 2012), but on Vatnsnes the predation risk for harbour

seals is considered to be low (Granquist and Sigurjonsdottir

2014). However, in several studies harbour seals have been

described to change their haul-out pattern because of

anthropogenic disturbance (Watts 1996; Henry and Hammill

2001; Acevedo-Guiterrez and Cendejas-Zarelli 2011;

Granquist and Sigurjonsdottir 2014). Acevedo-Guiterrez and

Cendejas-Zarelli (2011) found that in areas where artificial

noise levels are high, seals chose to haul out during the night

when the disturbance was smaller. Tourism may also affect

haul-out behaviour, both when it comes to choosing the site

and the time to haul out. London et al. (2012) showed that

harbour seals changed their haul-out pattern because of

human disturbance and preferred to haul out during the night

in August and September because of high human distur-

bance, while this pattern was reversed in October and

November. Other studies have reported changes in preferred

haul-out areas due to anthropogenic disturbance associated

with tourism, with seals moving to more remote skerries

(Henry and Hammill 2001; Granquist and Sigurjonsdottir

2014). Although disturbance due to humans was not

Fig. 8 The Illugastadir site, west coast of Vatnsnes, W-Hun., NW

Iceland. Estimated smoothers for environmental variables: air tem-

perature (left top), wind direction (right top), hours to low water (left

bottom) and day of the year (right bottom) obtained by the GAM

applied on the abundance of harbour seals (Phoca vitulina) indicated

by unbroken lines. Broken lines indicate 95 % pointwise confidence

bands and dots show residuals

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included in the study, Vatnsnes is a popular tourist area in

Iceland, including activities such as seal watching, and with

increasing numbers of tourists in the area, it is important that

human disturbance is taken into consideration in calcula-

tions. Granquist and Sigurjonsdottir (2014) found that har-

bour seals on Illugastadir, Vatnsnes, moved to skerries

further away from the mainland during periods of the

summer when the highest number of visits are made by

tourists to the area, although there was no evidence to

suggest that the seals moved away from the area. Further,

the majority of seals were hauling out during the peak of the

tourist season, indicating that the effects of tourists on the

haul-out site at Illugastadir were small (Granquist and Sig-

urjonsdottir 2014). At the other sites in the present study, the

effect of tourism on harbour seal haul-out behaviour has

not been investigated and it is therefore not possible to say

whether or not haul-out patterns are affected.

Conclusions

In this study, we found evidence for a seasonal haul-out

pattern among the seals, with the maximum number of

seals on land found in July for most of the sites. Bimodal

smoothing curves of abundance on a day-of-the-year basis

indicate that the main pupping period is in late May and

early June for harbour seals at Vatnsnes while the main

moulting period is in late July to early August. Abundance

at the sites increased with rising air temperature and

decreased with rising tides during summer. These findings

strengthen the already enforced method used in the aerial

census of harbour seals in Iceland to count at ±3 h of low

tide and to carry out the census during the moulting period.

However, earlier censuses have been carried out during

August and since the present study indicates that the

moulting period starts earlier, in the middle of July at most

sites, starting to conduct the harbour seal census in Iceland

in the middle of July should be considered. Practically,

counting early in the summer may be complicated since

many areas in Iceland are protected during June because of

eiderduck (Somateria mollissima) nesting and flying over

nesting sites is prohibited. During years with normal

weather conditions, eiderduck nesting is finished by the

middle of July. Notably, the variation in haul-out behaviour

found between the sites, despite their close proximity,

underlines the need for care when extrapolating results

obtained from a few sites to investigate a larger area.

Acknowledgments We would like to thank Helgi Gudjonsson,

Ester Cacho Sanchez, Laila Arranda Romero and Eva Haunss for

assistance in the field. Thanks to the landsowners at Vatnsnes, espe-

cially at Illugastadir and Hindisvık. Earlier versions of this manuscript

were improved by comments from Anders Angerbjorn, Ian Bytheway

and anonymous reviewers.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict

of interest.

Ethical standards This article does not contain any studies with

human participants performed by any of the authors. All applicable

international, national and/or institutional guidelines for the care and

use of animals were followed.

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