Latitudinal gradients in onset date, onset temperature ...

Journal of Fish Biology (2007) 70, 441–450 doi:10.1111/j.1095-8649.2007.01315.x, available online at http://www.blackwell-synergy.com

Latitudinal gradients in onset date, onset temperature and duration of spawning of roach J. L APPALAINEN *†

AND

A. S. T ARKAN ‡

*Department of Biological and Environmental Sciences, P. O. Box 65, FIN-00014 University of Helsinki, Finland and ‡Istanbul University, Faculty of Fisheries, Ordu Cad. No: 200, 34470, Laleli, Istanbul, Turkey (Received 20 January 2006, Accepted 28 September 2006) Onset date, onset temperature and duration of spawning of roach Rutilus rutilus were related to latitude (40–66° N) and altitude (1–825 m) based on data from the literature over the whole geographic distribution of roach. Onset date was positively and duration was negatively correlated with latitude, while no correlation was found between onset temperature and latitude. No significant correlations were found between any of the analysed variables of spawning and altitude, probably because most of the analysed populations were below 300 m # 2007 The Authors altitude. Journal compilation # 2007 The Fisheries Society of the British Isles

Key words: altitude; latitudinal gradient; roach; spawning; temperature.

INTRODUCTION Roach Rutilus rutilus (L.) is a widespread, commonly occurring and often abundant cyprinid species in Europe, where it occurs in rivers, lakes, reservoirs and in brackish waters (Holcik, 1967; Peczalska, 1968; Kozlovskiy, 1992; Lappalainen et al., 2005; No˜ges & Ja¨rvet, 2005). Typical habitats for roach are slow-flowing or still, muddy waters (Hellawell, 1972; Vostradovsky, 1973). It spawns generally on vegetation, but it can spawn also on the remnants of vegetation, other debris or even on stones (Sva¨rdson, 1951; Holcik & Hruska, 1966; Goldspink, 1977; Mills, 1981; Kozlovskiy, 1992). The onset of spawning is synchronized by photoperiod, and water temperature is important in regulating the intensity and duration of spawning (Worthington et al., 1982; Jafri, 1990; No˜ges & Ja¨rvet, 2005). Spawning usually takes place in water temperatures between 8 and 17° C (Sva¨rdson, 1951; Holcik, 1967; Peczalska, 1968; Papadopol, 1970; Goldspink, 1979; Papageorgiou, 1979; No˜ges & Ja¨rvet, 2005). Vøllestad & L’Abeé-Lund (1987) found, however, a lower onset temperature (74° C) of spawning for roach, which they suggested to be an adaptation to the colder climate in Norway. A fish species in the northern hemisphere with a wide distribution range has to adapt to a simultaneous decrease in the length of the first growing season

†Author to whom correspondence should be addressed. Tel.: þ358 9 19158470; fax: þ358 9 19158257; email: jyrki.t.lappalainen@helsinki.fi

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J. LAPPALAINEN AND A. S. TARKAN

and an increase in the duration of the first winter with an increase in latitude. Some species show special adaptations for this kind of seasonality by increasing their growth rate or by decreasing their optimum temperature for growth as latitude increases (Conover, 1992; Jonassen et al., 2000). Such adaptations should be important, because the age-specific mortality of fishes is usually highest during the early life stages (Beyer, 1989; Pepin & Myers, 1991), which also highlights the importance of first growing season in shaping the life-history strategies for longer living fishes. The aim of the present study was to analyse latitudinal gradients in onset date, onset temperature and duration of spawning of roach. If onset temperature or duration of spawning decreases towards the north, this could indicate an adaptation by roach, that increases the duration of the first growing season for age 0 year juveniles and so minimizes the associated size-dependent mortality of juveniles shown to occur during the first winter in some lakes (54° N, Griffiths & Kirkwood, 1995; 61–62° N, Kirjasniemi & Valtonen, 1997). Theoretically, the shorter the first growing season, the smaller the age 0 year juveniles are at autumn (Kubecka, 1989; Mooij & Tongeren, 1990). These smaller sized juveniles should have increased risk of mortality during the first winter (Shuter & Post, 1990; Griffiths & Kirkwood, 1995; Kirjasniemi & Valtonen, 1997). Such winter mortality has been found to even set the northern limit of distribution range of three percids (Shuter & Post, 1990), but whether the same is important for roach too, is not known. MATERIALS AND METHODS Estimates for onset date, onset temperature and duration of spawning of roach were obtained from the literature (Table I). Besides latitude, the possible effects of altitude on spawning were also analysed. In some articles, these were both given, but some values were also obtained from geographical maps. Onset date was the number of days since the first of January, onset temperature used was from the beginning of spawning, and duration was the number of days between first and last observation of spawning in a location. If duration of spawning was shown for 2 years or as a range of days within a year a mean value was calculated (Sva¨rdson, 1951; Hansen, 1981; Vøllestad & L’Abeé-Lund, 1987). Spearman correlation (rs) analysis was used to study the relationships between spawning and both latitude and altitude. Because both latitude and altitude can be important simultaneously, however, the deviations from the diagonal of the relationship between onset date and latitude (Lappalainen et al., 2000) were also correlated with altitude (e.g. the possible effects of latitude were then taken into account). When the statistical significance of these deviations was estimated, the associated d.f. was reduced by one already used in the onset date and latitude correlation (Garcı´ a-Berthou, 2001).

RESULTS L A T I TU D E A N D SP A W N I N G

The relationship between onset date and latitude was significant (n ¼ 27, rs ¼ 0521, P < 001) [Fig. 1(a)], but onset temperature and latitude was non-significant (n ¼ 22, rs ¼ 0135, P > 005) [Fig. 1(b)]. Onset date and temperature of spawning were correlated (n ¼ 21, rs ¼ 0439, P < 005), and duration of

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# 2007 The Authors 2007 The Fisheries Society of the British Isles, Journal of Fish Biology 2007, 70, 441–450

Spawning

Site, country

Latitude (° N)

Altitude (m)

Onset date (number of days since 1 January)

Onset temperature (° C)

Duration (days)

Estimation method

Sources

Lake Sapanca, Turkey Lake Volvi, Greece Lake Banyoles, Spain

4000 4066 4210

30 37 172

91 91 121

13 10 —

60 14 30

G G G

Lake Aydat, France Lake Geneva, France Middle Danube Delta, Slovakia Danube Delta, Slovakia Klicava Reservoir, Czech Republic River Meuse, Belgium

4565 4650 4800

825 372 114

151 141 91

14 17 11

— 14 60

G V G

Tarkan, 2006 Papageorgiou, 1979 Vila-Gispert & Moreno-Amich, 2000, 2003 Jamet & Desmolles, 1994 Gillet & Dubois, 1995 Bastl, 1995

4800 5007

114 269

— 132

9 185

— 5

— V

Papadopol, 1970 Holcik & Hruska, 1966

5035

150

132

14

—

G

5043

307

110

—

G

Rinchard & Kestemont, 1996; Kestemont et al., 1999 Sko´ra, 1972

5050

—

135

—

—

G

Cowx, 1990

5068 5100 5100 5283

— — — 1

135 132 136 145

143 — — 141

1 — 14 5

V G G G

Mills, 1981 Penczak et al., 1977 Mann, 1973 Goldspink, 1977

5297 5350

75 10

135 145

14 162

19 1

V V

Diamond, 1985 Diamond, 1985

Prezeczyce Reservoir, Poland Rivers Exe and Culm, England River Frome, England River Pilica, Poland River Stour, England Lake Tjeukemeer, The Netherlands The Lake, England Ledson’s Bridge, England

40

LATITUDINAL VARIATIONS IN SPAWNING OF ROACH

# 2007 The Authors Journal compilation # 2007 The Fisheries Society of the British Isles, Journal of Fish Biology 2007, 70, 441–450

TABLE I. Spawning of roach by locations and literature sources (latitude is in decimals)

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444

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TABLE I. Continued Spawning

#

Altitude (m)

Onset date (number of days since 1 January)

Onset temperature (° C)

Duration (days)

Estimation method

Szczecin Firth, Poland Lakes, Estonia Rivers, Estonia Lake Ma¨laren, Sweden Vollebekken, Norway

5380 5850 5850 5933 5969

0 33 50 0 50

121 125 121 151 130

14 87 78 17 74

21 5 3 25 21

G V V V G

Lake Øyeren, Norway Lake Saimaa, site 1, Finland Lake Saimaa, site 2, Finland Lake Jyva¨sja¨rvi, Finland Lake Konnevesi, Finland Lake Kiutaja¨rvi, Finland

5983 6115

101 76

130 144

— 10

18 3

G G

Peczalska, 1968 No˜ges & Ja¨rvet, 2005 No˜ges & Ja¨rvet, 2005 Sva¨rdson, 1951 Vøllestad & L’Abeé-Lund, 1987 Hansen, 1981 Karels & Oikari, 2000

6132

76

147

9

3

G

Karels & Oikari, 2000

6223 6258 6600

783 95 2248

145 152 159

13 16 14

4 4 6

G G G

Kortet et al., 2003 Kortet et al., 2004 Lind et al., 1973; Lind & Kukko, 1974

Site, country

G, maturity of gonads and regular sampling in spawning areas; V, visual observation of spawning roach or their eggs.

Sources



Latitude (° N)


445

Onset of spawning (number of days since 1 January)

170 160

(a)

150 140 130 120 110 100 90 80 35

40

45

50

55

60

65

70

40

45

50

55

60

65

70

40

45

50

55

60

65

70

Temperature at onset (° C)

20 18

(b)

16 14 12 10 8 6 35

Duration of spawning (days)

70 60

(c)

50 40 30 20 10 0 35

Latitude (° N)

FIG. 1. Relationships between latitude and (a) onset date of spawning, (b) onset temperature of spawning and (c) duration of spawning of roach (see Table I).

spawning showed significant negative correlations both with latitude (n ¼ 22, rs ¼ 0462, P < 005) [Fig. 1(c)] and with onset date of spawning (n ¼ 23, rs ¼ 0665, P < 0001). A L T I T U D E A N D SP A W N I N G

All relationships between spawning and altitude were non-significant (onset date: n ¼ 23, rs ¼ 0101, P > 005; onset temperature: n ¼ 21, rs ¼0123, P > 0 05; duration of spawning: n ¼ 21, rs ¼ 0273, P > 005) (Fig. 2). The deviations # 2007 The Authors Journal compilation # 2007 The Fisheries Society of the British Isles, Journal of Fish Biology 2007, 70, 441–450

446


Onset of spawning (number of days since 1 January)

170 (a)

160 150 140 130 120 110 100 90 80 –100

0

100

200

300

400

500

600

700

800

900

0

100

200

300

400

500

600

700

800

900

0

100

200

300

400

500

600

700

800

900

20 Temperature at onset (° C)

(b)

18 16 14 12 10 8 6 –100 70

Duration of spawning (days)

(c) 60 50 40 30 20 10 0 –100

Altitude (m)

FIG. 2. Relationships between altitude and (a) onset date of spawning, (b) onset temperature of spawning and (c) duration of spawning of roach (see Table I).

from the relationship between onset date and latitude [Fig. 1(a)] were also nonsignificantly correlated with altitude (d.f. ¼ 22, rs ¼ 0207, P > 005). DISCUSSION The three variables used to estimate spawning date of roach were initially evaluated using two simple methods based on either 1) regular sampling on spawning

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grounds and examinations of female gonads, or 2) visual observations of spawning of roach (G and V in Table I). The latter should be the most accurate method, but is not always possible. Of the three variables analysed, duration of spawning may be the most difficult to evaluate in the field, and therefore may also be the most inaccurate of these three variables. No statistical differences, however, were found between the two methods (G and V in Table I) in relation to onset date or onset temperature, but differences were apparent in estimates of the duration of spawning (Mann–Whitney U-tests). When analysed only on the maturity of gonads (method G), duration showed similar significant relationships (rs) with both latitude and onset of spawning as shown with all data. These additional analyses and the results suggest that the duration of spawning may be shorter than that estimated based only on maturity of gonads, but that the observed relationships between latitude and duration and between latitude and onset date may be real. The statistical analyses used here were based on rs analysis, which uses only the relative ranks of the variables, and only the order of duration of spawning in different populations is important, not the absolute value. The positive relationship found here between onset date of spawning and latitude has been also shown for two percid species occurring in Europe: perch Perca fluviatilis L. (Thorpe, 1977) and pikeperch Sander lucioperca (L.) (Lappalainen et al., 2003). Pikeperch spawning was delayed both at high altitude and in deep spawning grounds (Lappalainen et al., 2003). Here, altitude seemed to have little effect on spawning of roach, probably because most of the analysed populations were located at low altitudes (mean altitude 119 m). Because the two populations located at the highest altitudes (Lake Aydat, Jamet & Desmolles, 1994; Lake Geneva, Gillet & Dubois, 1995) showed later onset dates than the other roach populations situated at lower altitudes and similar latitudes, however, an effect of altitude on roach spawning cannot be ruled out. More data of spawning on roach from higher altitudes are needed to study these relationships more closely. Optimum temperature for embryonic development of roach eggs is between 12 and 24° C, while 26° C all eggs will die (Herzig & Winkler, 1985). Based on the data analysed here, roach populations which start their spawning near 8° C seem to take higher risks than those starting later. The risk seems to be connected with the latitudinal location of the population, because the risk appears to increase northwards. Most of the data analysed by Herzig & Winkler (1985), however, were based on studies completed with southern populations. Thus, these temperature limits should be also analysed with eggs from northern populations of roach to evaluate whether any adaptations in embryonic development in relation to latitude or temperature exists. Duration of spawning of roach decreased northwards. Roach has the synchronous oogenesis of a monospawner species, and each female spawns only one batch of eggs per season (Mackay & Mann, 1969; Cowx, 1990). Thus, the observed pattern suggests that the synchrony among females is more obvious northwards. Such a pattern of reduced duration towards higher latitudes should be advantageous for both juveniles and adults taking part in spawning. Had spawning taken 30 days instead of the 3–6 days found in northern latitudes (>61° N), then the risk that at least part of the temperature needed for growth could be lost should increase, which should further increase the risk # 2007 The Authors Journal compilation # 2007 The Fisheries Society of the British Isles, Journal of Fish Biology 2007, 70, 441–450

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of juvenile mortality during the first winter. Besides, this pattern of spawning behaviour should also maximize adult fitness, because better growth should give more options for adults in energy allocations. Therefore, decreased duration of spawning should maximize age 0 year juvenile growth and minimize their winter mortality, but also should maximize the potential reproductive output of adults during the next spawning.

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