Latitudinal variation in fecundity among Arctic ... - Wiley Online Library

Journal of Fish Biology (2005) 67, 255—273 doi:10.1111/j.1095-8649.2005.00734.x, available online at http://www.blackwell-synergy.com

Latitudinal variation in fecundity among Arctic charr populations in eastern North America M. P O W E R *†, J. B. D E M P S O N ‡, J. D. R E I S T §, C. J. S C H W A R Z { A N D G. P O W E R ** *Department of Biology, University of Waterloo, 200 University Avenue West, Waterloo, ON, N2L 3G1, Canada, ‡Fisheries and Oceans Canada, Science Branch, P. O. Box 5667, St John’s, NL, A1C 5X1, Canada, §Fisheries and Oceans Canada, 501 University Crescent, Winnipeg, MB, R3T 2N6, Canada, {Department of Statistics and Actuarial Science, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada and **51 Glasgow Street, Conestogo, ON, NOB 1NO, Canada (Received 20 May 2004, Accepted 16 February 2005) Variation in fecundity was examined from 32 populations of Arctic charr Salvelinus alpinus in eastern North America covering a range of 37 latitude and extending from Maine, U.S.A., to northern Ellesmere Island in the Canadian Arctic. Populations were classed as dwarf, normal or anadromous and covered a suite of different habitat and climatic regimes. Fecundity varied with fork length (LF), with LF adjusted fecundity differing significantly among populations within each of the morphotypes implying that fecundity was a continuously responsive trait influenced by local environmental factors. Latitudinal variation in fecundity was also evident among morphotypes when the simultaneous effects of both latitude and LF were controlled. There was a significant trade-off between fecundity and egg size in two of five populations of anadromous Arctic charr, but no evidence in limited data from either normal or dwarf populations. In contrast with some other studies of fecundity in salmonids, there was no # 2005 The Fisheries Society of the British Isles evidence for a latitudinal cline in egg size. Key words: ecosystems/climate change; egg diameter; environmental influences; fecundity; latitude; Salvelinus alpinus.

INTRODUCTION As seen from studies of zooplankton (Rutherford et al., 1999; Gillooly & Dodson, 2000), marine invertebrates (Gallardo & Penchaszadeh, 2001), fishes (Leggett & Carscadden, 1978; L’Abeé-Lund et al., 1989; Fleming & Gross, 1990; Johnston & Leggett, 2002) and mammals (Ruggiero, 1994; Kendall et al., 1998), organism life-history characteristics often vary with latitude because of predictable changes in important environmental factors. Among the most important environmental factors which may vary with latitude is temperature, which for fish populations is known to influence growth rates and through growth to

†Author to whom correspondence should be addressed. Tel.: þ1 519 888 4567 ext. 2595; fax: þ1 519 746 0614; email: [email protected]

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indirectly affect important life-history attributes that determine population dynamics (Wootton, 1990; Elliott, 1994). Among salmonid populations, temperature has been shown to influence movement and migration (Jonsson, 1991), migration timing (Berg & Berg, 1989), smolting (Power, 1981; McCormick et al., 1998), growth rate (Brett et al., 1969; Jensen et al., 2000), age-at-maturity (Power, 1981; Scarnecchia, 1983; L’Abeé-Lund et al., 1989) and fecundity (Fleming & Gross, 1990). Of these life-history attributes fecundity is particularly important. Fecundity combined with survivorship directly influences population dynamics through its effect on the intrinsic rate of population increase as expressed by the Euler-Lotka equation (Roff, 1992). Differences in fecundity exist within species, often among geographically isolated populations, and among individuals within the same population depending on size and age (Bagenal, 1978) and may represent either phenotypic or genetic causes (Roff, 1992; Hendry & Stearns, 2004). Accordingly, fecundity and the factors which influence it are of interest to many including evolutionary ecologists, fishery managers or those attempting to understand the potential effects of largescale ecosystem changes (e.g. climate change) on a fish species. One species that is likely to be significantly affected by large-scale patterns of ecosystem change is Arctic charr Salvelinus alpinus (L.) (ACIA, 2004). The species is circumpolar in distribution with a latitudinal range that extends in eastern North America from northern Ellesmere Island (c. 84 N), south to New England (c. 43 N). Within the eastern North American range, as well as in Europe, several distinctive life-history types are known including anadromous, normal and dwarf Arctic charr (Nordeng, 1983). Populations with access to the sea can contain both anadromous and non-anadromous forms, typically indistinguishable on the basis of morphometric and meristic characteristics. Anadromous populations over-winter, reproduce and pass early life-history stages in fresh water. From c. ages 2 to 9 years, regular seasonal migrations for summer feeding in nearshore marine areas commence (Johnson, 1980). Populations without access to the sea conduct their entire life-history in fresh water, usually in lakes. Throughout the distributional range of the species morphological variation is characteristic of lacustrine populations (Klemetsen & Grotnes, 1980; Hindar & Jonsson, 1982; Riget et al., 1986; Walker et al., 1988; Snorrason et al., 1994; Pavlov, 1997; O’Connell & Dempson, 2002). Morphotypes may be distinguished on the basis of a number of traits including habitat usage, individual growth rate, age and size at sexual maturity, time and place of spawning, body colouration, and morphological and meristic characteristics (Lindstro¨m & Andersson, 1981; Sparholt, 1985; Jonsson et al., 1988; Mills, 1989; Parker & Johnson, 1991; Reist et al., 1995; Klemetsen et al., 1997; Adams et al., 1998; O’Connell & Dempson, 2002). In eastern North America morphotypes are found in allopatry and sympatry (Reist et al., 1995; O’Connell & Dempson, 2002) throughout the distributional range. Within the diversity of basic Arctic charr life-history strategies there is considerable complexity and much remains to be explained about variations in traits among and within populations. This is partly because most life-history studies of Arctic charr have been completed over comparatively short periods of time or focused on single populations (Jensen & Berg, 1977; Johnson, 1989; Dempson & Green, 1985). Studies that have sought to compare populations have typically #

2005 The Fisheries Society of the British Isles, Journal of Fish Biology 2005, 67, 255—273

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been restricted to a limited geographic area or have compared only a handful of populations. Genetics aside (Wilson et al., 1996; Brunner et al., 2001), few studies have attempted a detailed zoogeographic analysis of population lifehistory variable patterns. Exceptions include the literature-based studies of Venne & Magnan (1989) and Tallman et al. (1996) that, respectively, examined life-history variations along a north-south gradient for a selection of landlocked populations and statistical differences in the life-history characteristics of migratory and non-migratory populations from across the distributional range of the species, and the Vøllestad & L’Abeé-Lund (1994) study that modelled the reproductive investment in European and North American Arctic charr. Neither the study by Venne & Magnan (1989) nor Tallman et al. (1996) explicitly considered the effect of morphotype on observed trait variation. In the cases of Tallman et al. (1996) and Vøllestad & L’Abeé-Lund (1994) data were mixed from distinctive geographic zones (e.g., Europe and eastern Canada) whose major climate moderating factors (e.g., the Gulf Stream and Labrador Current) and climates differ substantially. The mixture of data from different climatic regimes at similar latitude may have obscured patterns of latitudinal variation inherent within climate zones by increasing the apparent variability in the data. Accordingly, the general aim of the present study was to augment the availability of zoogeographic analyses of variability in Arctic charr life-history traits through an investigation of patterns in species fecundity and egg diameter along a latitudinal gradient of c. 37 from the southern to the northern extent of the distributional range in eastern North America (Maine, insular Newfoundland, Labrador, Que´bec, Baffin Island and Ellesmere Island). Specifically, the hypotheses were tested that among eastern North American populations of Arctic charr: (1) latitude and morphotype are significant determinants of fecundity and egg diameter and (2) since various authors have identified evidence and consequences of a trade-off between fecundity and egg size (Fleming & Gross, 1990; Jonsson & Jonsson, 1999; Olsen & Vøllestad, 2003; Einum et al., 2004), that there is evidence of a trade-off between egg number and size in populations of eastern North American Arctic charr.

MATERIALS AND METHODS Data on fecundity in 32 eastern North American, principally Canadian, Arctic charr populations were obtained from the Department of Fisheries and Oceans Canada (DFO) archives, personal archives or the published scientific literature (Grainger, 1953; Kircheis, 1976; Rombough et al., 1978; Boivin, 1994). Populations used in the study are identified by water-body name, latitude ( N), sample size, population morphotype and data source in Table I and plotted in Fig. 1. Only those locations for which individual observations of fecundity were available were used in statistical analyses. Eastern North America was defined to include all land mass areas east of 80 W including: Maine, the Canadian Maritime Provinces, insular Newfoundland, Labrador, Que´bec, and the eastern Arctic Islands of Baffin, Devon and Ellesmere. Arctic charr populations were categorized by morphotype. Dwarf lacustrine populations were defined as populations in which the observed maximal fork length (LF) of mature individuals did not exceed 22 cm as categorized or identified in the literature (Parker & Johnson, 1991). Normal lacustrine populations were those where maximal lengths of >50% of mature individuals exceeded 25 cm. Where lacustrine morphotypes potentially occurred in sympatry, additional life-history, morphological or meristic data #


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TABLE I. Populations of Arctic charr sampled, latitude of sample site, sample size, population type and information source. D, dwarf population where maximal size ¼ 22 cm LF; N, lake-resident populations where individuals grow to sizes 25 cm LF; A, anadromous populations. Map reference corresponds to the number used to plot locations in Fig. 1. *, Populations for which mean fecundity data were available for discussion but excluded from detailed statistical analyses Map reference Latitude ( N )

Population Floods Pond Lac Francais1 Godaleich Pond Trinity Pond Gander Lake Gander Lake Long Pond Candlestick Pond Matamek Lake Voisey’s Bay Fraser River Webb Bay Okak Bay Lac Ducreux

1 2 3 4 5 5 6 7 8 9 10 11 12 13

4445 4643 4811 4825 4855 4855 4950 4958 5022 5618 5639 5646 5728 5747

Ikarut River Charr Lake Lac Noname

14 15 16

5809 5811 5815

Saglek Fiord Leaf River George River Nachvak Fiord Sannirarsiq2 Sappukait2 Sylvia Grinnell Cumberland Sound Nettilling Lake Cumberland Sound Ellesmere Lakes3 Lake Alexandra Murray Lake Lake Hazen Kilbourne Lake

17 18 19 20 21 22 23 24 25 26 27 28 29 30 31

5829 5839 5847 5903 5912 5928 6344 6549 6629 6632 8052 8147 8120 8150 8153

n

Type

3 — 34 12 36 8 29 13 13 3 15 30 9 35

N* N* D D N D D D N A* A A A N*

162 A 36 D 36 N* 7 15 6 14 9 9 23 80 2 63 10 13 5 34 10

A A A A A A A A* A* A* N* N N N N

Information source Kircheis (1976) Venne & Magnan (1989) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) Rombough et al. (1978) G. Power (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) Fraser (1981); G. Power (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) Fraser (1981); G. Power (unpubl. data) DFO (unpubl. data) G. Power (unpubl. data) Grainger (1953) DFO (unpubl. data) Boivin (1994) Boivin (1994) Grainger (1953) Moore (1975) DFO (unpubl. data) Moore (1975) Parker & Johnson (1991) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data) DFO (unpubl. data)

1

Sample size was not reported. Data represent size-class reported means of individual samples. 3 Data combined from individuals obtained from four adjacent lakes as described by Parker & Johnson (1991). DFO, Department of Fisheries and Oceans Canada. 2

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FIG. 1. Map indicating the general location of Arctic charr populations included in this study. Numbers refer to sample locations specified in Table I and are ordered by increasing degrees of latitude. The sympatric populations of Gander Lake, Newfoundland are represented by a single number.

(e.g. growth rate, age and size at sexual maturity, head depth, maxillary length, dorsal ray counts, gill raker counts, habitat or feeding preferences) substantiating putative morphotypic differences were used to assign populations to morphotype classifications. Anadromous Arctic charr were defined as populations known to use near-shore marine areas for summer feeding. Data from DFO and personal archives consisted of individual specimen observations on LF (mm), mass (g), age (years), fecundity and geographic location (latitude and longitude), as well as egg diameter from a smaller sub-set of Arctic charr populations. #


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All data included in the study were obtained from summer or early autumn sampling programmes that used multiple meshed gillnets, typically in the range 38—114 mm, or weirs to monitor and sample studied populations. Fish were measured to the nearest mm and weighed to the nearest g. Fecundity was assessed following standardized procedures described in Bagenal & Braum (1978) and egg diameters were determined as means based on the measurement of multiple individual eggs. Population-specific individual and average fecundity data were used to estimate fecundity (F) and LF models following Bagenal & Braum (1978) as: F ¼ aLFb, where F defined individual or size-class fecundity, and a and b, respectively, were the estimated model constant and exponential coefficients. Inter-population comparisons of fecundity were completed for each morphotype using a general linear model (ANCOVA) standardized to a common LF as described in other investigations (Healey & Heard, 1984; Fleming & Gross, 1990): Yij ¼ m þ Si þ bZij þ Eij, where Yij ¼ fecundity of the jth fish at the ith site on the logarithmic scale (e.g. lnF), Si ¼ individual sampling sites, Zij is the covariate lnLF and Eij ¼ the error term. Tests for heterogeneity of slopes among sites were examined initially by fitting a more complex model with an interaction between the site and the covariate. There was no evidence that slopes differed among sites for anadromous (P ¼ 074) and dwarf morphs (P ¼ 010). For the normal morph, there was evidence that the common slope model did not fit (P ¼ 003). A detailed investigation of the data, however, showed that this was due to one site with very little variation in the LF covariate so that a few fish with more extreme values of the covariate had high leverage on the estimated slope. Furthermore, the r2 values in the common slope model were virtually identical, with the reduction in the residual (error) mean square indicating minimal improvement in precision that resulted in the acceptance of a common slope model. A similar fecundity analysis result has been reported by Winters et al. (1993). Analyses of egg size, confined to a sub-set of anadromous Arctic charr populations and where diameters were 20 mm, followed the analytical sequence outlined above. Egg diameters, however, were found to be invariant over length (P > 008) and differences among populations were subsequently examined by ANOVA. Standardized fecundity data were initially plotted against latitude to examine any potential association of latitude as a determinant of among-population fecundity variations. The model used assesses the effect of latitude after adjusting for the covariate LF with a separate analysis for each morph. Individual fish, however, are not entirely independent of each other within a specific site (e.g. they all experience common environmental and other factors that may affect fecundity), and so the analysis must not treat all fish across all sites as entirely independent of each other. The analysis must recognize that the effect of latitude operates on the site level rather than upon individual fish, while the effect of the covariate, LF, operates at the individual fish level. The simultaneous effects of both latitude and LF upon fecundity (Yjk) were examined using the following model for each morph: Yjk ¼ Sj þ b1Zjk þ b2Ljk þ Ejk, where the subscript jk represents fish k within site j, Sj is a random site component, Zjk is the covariate LF, Ljk is the covariate for latitude, Ejk is a random error component, b1 is the adjustment for lnLF and b2 is the putative effect of latitude. Such a model was fitted using Proc Mixed routine of SAS where the initial model also included an interaction term between latitude and LF that was found to be insignificant. A similar analysis was carried out for egg diameter on a sub-set of anadromous charr populations. To examine the fecundity of populations for which only mean values were available, data were standardized to a common LF following procedures described by Bagenal (1966), Fleming & Gross (1989) and Beacham & Murray (1993a) as: b Fs ¼ Fo LFs LFo 1 , where Fs ¼ the length-adjusted fecundity, Fo ¼ the observed (mean) fecundity, LFs ¼ the standard mean fork length of all fish of a given morph, LFo ¼ the observed mean fork length of the population in question and b is the slope of the regression of lnLF on lnLFo. Evidence of a trade-off between egg size (diameter) and fecundity was examined following the approach described by Olsen & Vøllestad (2003) where fecundity (ln scale) was the response variable, ln egg size (diameter) and lnLF were covariates and individual

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sample sites were treated as a class variable: Yjk ¼ Sj þ b1Zjk þ b2EDjk þ b3SjEDjk þ Ejk, where Yjk ¼ fecundity of the kth fish, Sj ¼ individual sampling sites, Zjk is the covariate LF, EDjk is the covariate for egg diameter and Ejk is a random error component. The coefficient b1 is the adjustment for LF; b2 is the effect of egg size (diameter), and b3SjEDjk is the potential interaction between egg diameter and sample location used to interpret the effect of egg size on fecundity among sampled populations.

RESULTS The 32 populations or stocks for which information were available were distributed between latitudes 44 45 0 N to 81 53 0 N. Of those populations, six, 11 and 15, respectively, were classified as dwarf, normal and anadromous. Morphologically differentiable sympatric populations were identified in only two instances: Gander Lake, Newfoundland (O’Connell & Dempson, 2002) and Lake Hazen, Ellesmere Island (Reist et al., 1995). In the case of Lake Hazen, fecundity data for only a single morphotype (normal) were available for this study. Statistical analyses of variation among and within morphs were limited to those specific sites for which raw data were available and sample sizes consisted of at least five individuals (n ¼ 23), while discussion of material also included the incorporation of nine additional sites for which literature mean values were available. Fecundity of sampled dwarf Arctic charr ranged from 29 to 304 (mean ¼ 115; CV ¼ 53%), while fecundity of normal Arctic charr varied from 55 to 3539 (mean ¼ 805; CV ¼ 95%). With respect to anadromous samples, fecundity varied from 1000 to 10 692 (mean ¼ 4180; CV ¼ 37%). VARIATION WITHIN MORPHOTYPES

Fork length explained 60% of the variation in fecundity of anadromous Arctic charr with variability increasing with length [Fig. 2(a)]. ANCOVA of LFadjusted fecundity indicated significant differences among individual sampling locations (Table II). Adjusted mean fecundity varied by a factor of 168 ranging from a mean S.E. of 4635 396 eggs for George River fish (map reference 19: Ungava Bay) to 2762 120 eggs for Sylvia Grinnell fish (map reference 23: Baffin Island) (Fig. 1). In general, however, Arctic charr populations in Labrador had higher fecundity than anadromous populations elsewhere. For normal Arctic charr, variation in LF explained 83% of the variability in fecundity [Fig. 2(b)]. ANCOVA of LF-adjusted fecundity also indicated significant differences among individual sample locations (Table II). Adjusted mean fecundity varied by a factor of 23 ranging from a mean S.E of 782 50 eggs at Matamek Lake (map reference 8: Quebec) to 338 34 eggs for fish from Murray Lake, Ellesmere Island (map reference 29) (Fig. 1). Length similarly explained 67% of the variation in fecundity of dwarf Arctic charr [Fig. 2(c)]. ANCOVA of LF-adjusted fecundity indicated significant differences among populations (Table II). Adjusted mean fecundity varied by a factor of 190 from a mean S.E. of 139 8 eggs at Godaleich Pond (map reference 3: Newfoundland) to 73 3 eggs at Charr Lake (map reference 15: Labrador). For anadromous Arctic charr, LF explained only 8% of the variation observed in egg diameter of the sub-set of populations (P < 0001) for which data were #


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FIG. 2. Relationships between fecundity and fork length for (a) anadromous, (b) normal and (c) dwarf populations of Arctic charr from eastern North America. The curves were fitted by (a) y ¼ 0625x2224 (r2 ¼ 0596, n ¼ 299, P < 0001), (b) y ¼ 00889x25617 (r2 ¼ 0833, n ¼ 111, P < 0001) and (c) y ¼ 01208x25116 (r2 ¼ 0672, n ¼ 132, P < 0001).

available. There were, however, significant differences among sample locations (r2 ¼ 044, P < 0001) with adjusted mean egg diameter varying from c. 43 mm at Fraser River to c. 28 mm at Ikarut River, Labrador. For normal and dwarf Arctic charr, LF explained 35% (P ¼ 0002) and 14% (P ¼ 0002) of the variation in egg size, but limited sample sizes precluded meaningful comparisons among individual sample locations. #


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Number of populations Number of specimens Model r2 Source of variation Coefficient estimate

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F 1186 011 57341 4861 009 90061 1772 019 8040

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