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J. Plankton Res. (2014) 36(1): 104– 116. First published online September 30, 2013 doi:10.1093/plankt/fbt095

Temperature effects on development and reproduction of copepods in the Humboldt Current: the advantage of rapid growth RUBEN ESCRIBANO1*, PAMELA HIDALGO1, VALENTINAVALDE´S2 AND LEISSING FREDERICK1 1

´ N, PO BOX DEPARTMENT OF OCEANOGRAPHY, UNIVERSIDAD DE CONCEPCIO

´ N, PO BOX UNIVERSIDAD DE CONCEPCIO

160

160 C, CONCEPCIOŃ, CHILE AND 2DOCTORAL PROGRAM OF OCEANOGRAPHY,

´ N, CHILE C, CONCEPCIO

*CORRESPONDING AUTHOR: [email protected] Received March 6, 2013; accepted September 4, 2013 Corresponding editor: Marja Koski

Egg production (EP) and egg development rate (DR) of Centropages brachiatus, Calanus chilensis and Paracalanus indicus, three abundant copepods in the Humboldt Current System, were experimentally assessed during spring – summer and autumn – winter periods between 2001 and 2012 in northern Chile (238S) and central/southern Chile (368S). EP was on average 43.3, 29.3 and 5.0 eggs female21day21in C. brachiatus, C. chilensis and P. indicus, respectively. C. chilensis and C. brachiatus displayed similar embryonic DR, whereas that of P. indicus was significantly faster. DR was significantly affected by season and location, being faster in the spring – summer and off northern Chile. DRs allowed estimates of temperature-dependent generation times (GT). Expected GTs for C. brachiatus and C. chilensis at mean observed temperatures in both places coincided with those derived from field studies. Estimates of GT could also explain the presence of multiple generations a year, upon continuous reproduction, and potentially in the absence of food limitation. Despite a low EP, P. indicus exhibited a high DR and expected GT in the range of 10– 20 days, explaining the existence of many generations a year as reported by field studies. Our findings provide evidence to support the hypothesis that population dynamics of these species may be fundamentally controlled by temperature in the coastal upwelling zone.

available online at www.plankt.oxfordjournals.org # The Author 2013. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]

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TEMPERATURE-DEPENDENT DEVELOPMENT OF COPEPODS

KEYWORDS: copepods; development; eggs; temperature; Humboldt current

I N T RO D U C T I O N In the highly productive Humboldt Current System (HCS) (Mann and Lazier, 1991; Kudela et al., 2005) copepods are distributed over an extensive latitudinal gradient (408) in the coastal upwelling zone. This HCS exhibits intermittent upwelling throughout the year off northern Chile (188– 308S) (Thomas et al., 2001), and is strongly seasonal off central/southern Chile (308– 408S) with intense upwelling in the spring – summer period and diminished upwelling or downwelling conditions in the autumn – winter (Sobarzo et al., 2007). Temperature along the latitudinal gradient of the HCS may vary .108C within the upper 50 m of the water column, where the most abundant species of copepods co-exist (Heinrich, 1973), apparently constrained by a shallow oxygen minimum zone (Escribano et al., 2009). In addition to the spatial variability and seasonal effects on temperature, the entire region is subjected to interannual changes in temperature regimes due to alternate cold (La Ninã) and warm (El Ninõ) phases of the El Ninõ Southern Oscillation cycle (Thomas et al., 2001; Collins et al., 2010). During “normal” or cold (La Ninã) years sea surface temperature ranges between 9 and 188C from the southern region (408S) to northern Chile (Strub et al., 1998), whereas during El Ninõ conditions a surface anomaly of up to þ48C can occur in the coastal region, mainly off northern Chile (Escribano et al. 2004). Meantime, in subsurface water (50 – 200 m), the dominant temperature range is between 8 and 128C (Strub et al., 1998). Copepods must adjust their vital rates to changing temperatures (Møller et al., 2012), so that the influence of temperature on individual copepods and populations must be considered as critical (Halsband-Lenk et al., 2002; Yang and Rudolf, 2010; Forster and Hirst, 2012), and this view becomes particularly relevant in the HCS considering the variety of sources for temperature variation. Temperature effects on reproduction and development rate (DR) are widely recognized as a key issue for understanding population dynamics of copepods (Mauchline, 1998; Bonnet et al., 2009; Dam, 2013). However, reproduction and development of copepods can also be affected by quality and quantity of food resources (Klein Breteler et al., 2005; Saiz and Calbet, 2007). In this regard, embryonic development might better represent a purely temperature-dependent rate, without food effects. Therefore, egg development time, which has also been

shown to depend on egg size and on species (McLaren, 1995; Bonnet et al., 2009), can be used to study temperature-dependent development. Size must be considered because of its allometric relationship with physiological rates (Peters, 1983; Forster et al., 2011), whereas species-dependent effects are most likely related to temperature adaptation from low to high latitudes (McLaren et al., 1969; Lee et al., 2003). In the HCS, the copepod community is numerically dominated by small (,2 mm length) and medium size (2–3 mm length) copepods (Hidalgo et al., 2010). Among them, the calanoids Centropages brachiatus, Calanus chilensis and Paracalanus indicus are very abundant and widely spread (Heinrich, 1973; Hidalgo et al., 2010). C. brachiatus and C. chilensis show a similar distribution off northern Chile (Gonza´lez and Marıń, 1998), and also a similar annual life cycle characterized by continuous reproduction and production of several generations throughout the year (Hidalgo and Escribano, 2008). New cohorts for these species can appear at any season, such that all stages, including eggs may be found year-round in the upwelling zone, both in northern Chile (Hidalgo and Escribano, 2008) and central/southern Chile (Hidalgo and Escribano, 2007). Development and growth of C. chilensis and even their annual production have been suggested to be temperature dependent (Escribano et al., 1997; Escribano and McLaren, 1999). P. indicus is widely distributed from the equator to the southern Patagonian waters (Heinrich, 1973; Marıń and Antezana, 1985), and it is the most abundant copepod in the upwelling zone off Chile (Escribano et al., 2007). This species is multigenerational off northern Chile and also off central/southern Chile (Escribano et al., 2007). These three species are freespawning copepods and previous studies on egg production (EP) rates have been carried out for C. brachiatus and P. indicus (Vargas et al., 2006) and for C. chilensis (Escribano et al., 1996; Poulet et al., 2007). Variability in EP within and between species is certainly an important issue to consider when understanding copepod dynamics. In this study, based on laboratory experiments, we assessed EP variability and the embryonic DRs of the three copepod species. We compared the species and examined regional and seasonal effects on EP and embryonic DRs. Our main aim was to compare interspecific responses of EP and DR to variable temperature, and how these responses may provide insights in understanding the processes controlling population dynamics of these species in the HCS.

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METHOD Study area and field data Experiments on EP and embryonic DRs of the three species were carried out during contrasting seasons (spring–summer and autumn–winter), and at two wellseparated locations in the HCS: Mejillones (238S) and Concepcioń (368S) (Fig. 1). Mejillones is a Peninsula including the Bay of Mejillones and Bay of Antofagasta. This area is a very active upwelling center off northern Chile (Marıń et al., 2001), with intermittent upwelling year-round and high primary production (.2 mg C m22 day21) at all seasons (Rodriguez et al., 1991). Concepcioń is also considered to be a very active upwelling site of the Humboldt Current, characterized by a strong seasonality of upwelling mainly in the spring–summer period (Sobarzo et al., 2007). Temperature and phytoplankton biomass, measured as concentration of Chlorophyll a (Chl a), were assessed at both places throughout the study period. In

Fig. 1. The Humboldt Current region in the Eastern south Pacific off Chile and Peru, illustrating the two upwelling sites: Mejillones (northern Chile) and Concepcioń (Central/southern Chile) where copepods were captured to conduct experiments on egg production (EP) and development rate of eggs (DR) as a function of temperature.

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Mejillones, CTD casts, using a SeaBird SBE 19 plus CTD, deployed down to 50-m depth, and water samples for Chl a measurements (at five depths) were obtained four times a year (seasonal sampling). In Concepcioń, CTD casts and Chl a measurements (nine depths) were made each month down to 80 m at Station 18 (368300 S– 738070 W) between 2002 and 2012 (Escribano and Morales, 2012). Chl a was measured with fluorometric methods after filtration with GF/F (0.7 mm) filters. Methods to measure Chl a are described in Morales and Anabaloń (Morales and Anabaloń, 2012).

Experimental design and procedures The experiments were performed between mid-2001 and beginning of 2002 at Mejillones, whereas in Concepcioń they took place in 2003, 2004 and thereafter in 2011 (Table I). The basic experimental design consisted in the capture of live females, using standard plankton nets of 200-mm mesh size and non-filtering cod ends, from coastal waters. All samples were taken in the upper 50-m layer and under daylight conditions. Live samples were immediately diluted in seawater and transported to the laboratory within 1 – 2 h. Sorting of females was carried out in cold rooms at nearly in situ temperature, as measured at 10-m depth, using CTD profiles obtained at the same stations. Once a sufficient number of females could be sorted (20– 30 females for each temperature), they were individually incubated in 100 mL vials containing filtered (0.7 mm) seawater at five to six different temperatures, and observed thereafter every 1 – 2 h under the microscope inside the temperature-controlled cold rooms. Observations every hour were made for temperatures higher than 108C and every 2 h for ,108C. When eggs could be observed in the vials, the females were removed and the eggs counted. Observations of the eggs continued every 1 and 2 h and egg hatching time was recorded by counting the eggs at each observation, and when possible by observing and counting swimming nauplii. Observations were maintained up to a maximum of 48 h or until all the eggs had hatched. Nominal temperatures applied to incubations of females and eggs were chosen so as to cover the observed temperature range at both locations in the upper 50 layer (Thomas et al., 2001), but extending the lower limit down to 5.5 or 68C. To maintain temperatures near constant, the vials containing the eggs were kept immersed in small (10 L) circulation baths. For each experiment, between three and six controlled temperatures were applied and for each period between one and five experiments were conducted. Table I summarizes the information for location and seasonal periods, number of temperatures and numbers of females used for each experiment.

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Table I: Summary of experiments conducted to assess egg production (EP), hatching success and embryonic development rate (DR) of three planktonic copepods, Centropages brachiatus, Calanus chilensis and Paracalanus indicus at two upwelling sites of the Chilean Humboldt Current: Mejillones (MEJ: northern Chile 238S) and Concepcioń (CONCE: Central/south of Chile, 368S) under the effect of controlled temperatures Species

Location

Dates

Season

No. Exp.

No.T.

N

C. brachiatus

MEJ MEJ CONCE CONC MEJ MEJ CONCE CONCE CONCE

October 2001 August 2001 March 2004 September 2003 January 2002 July 2001 January 2003 August 2003 November 2011

Spring Winter Summer Spring Summer Winter Summer Winter Spring

2 5 2 1 2 2 3 3 1

6 5 6 4 5 5 4 4 3

21 61 90 78 42 42 30 29 30

C. chilensis P. indicus

No. Exp. is the number of performed experiments on each occasion, No.T. is the number of experimental temperatures and N is the total number of egg clutches for estimating development rate.

Data analysis

in its linear form is,

We assessed egg production rate (EP), which is the traditional measurement of EP, by counting the number of eggs spawned daily by a female. Depending on temperature and species and on occasions, there was more than one spawning event within a 24-h period, but EP was calculated as the total number of eggs spawned in a 24-h period. We tested species differences in EP and hatching success using a one-way ANOVA. ANOVA was also used to test temperature, location and seasonal effects on EP. A K–S Kolgomorov–Smirnov test was applied to assess normality, and the ANOVA was thus applied to log-transformed data in all cases to ensure an approximate normal distribution. Embryonic duration for each temperature (DT) was estimated from the time between egg spawning and egg hatching. Both, egg spawning and egg hatching were obtained as the median time between two consecutive observations (1 or 2 h). Since some females spawned in small groups of eggs within a few hours, DT was estimated separately for these small clutches. Embryonic DR was thereafter estimated as DR ¼ 1/DT, with DT expressed in days. The DR of copepod eggs as a function of temperature has been previously analyzed with the Bele´hradek equation (McLaren, 1995), but we also fitted data to an exponential model and tested both equations for the goodness-of-fit. The equation showing best fit was the exponential one, expressed as,

Thereafter, we fitted Equation (2) with a regression Model I to log-transformed data of DR, as Ln (DR þ 1) to avoid the use of negative values, and the effect of location and season on the fitted regressions was tested with a general linear model (GLM). For each regression, ANOVA was applied to test the regression significance and to obtain standard errors of fitted parameters. To test seasonal effects on EP and DR, all the experimental dates were assigned to two seasonal conditions: spring-summer and autumn-winter. Both seasonal conditions have been clearly characterized in the coastal zone off Chile as upwelling and non-upwelling seasons (Escribano et al., 2004). In order to explore how the DRs might influence the dynamics of these species, we estimated a temperaturedependent generation time (GT) for each species. It was first assumed that embryonic duration represented 5% of total GT, as previously found for C. chilensis (Escribano et al., 1997). Thereafter, the “equiproportional rule” of development (Corkett et al., 1986) was applied on the basis that total development time depended only on temperature. This means, the absence of food effects on development, as previously suggested for C. chilensis (Escribano and McLaren, 1999) and C. chilensis and C. brachiatus (Hidalgo and Escribano, 2008). Thus GT was estimated as,

DR ¼ a eðb T Þ ;

GT ¼ 100 ð5DRÞ1 ;

where DR ¼ development rate (day21), T ¼ temperature (8C), and a and b are empirical constants. This function

where GT (day) and DR (day21) are defined as above. DR as a function of temperature was derived from

Ln (DR) = Ln ðaÞ þ b T :

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Equation (2) after conversion from the previous logtransformation. Estimates of temperature-dependent GTs with Equation (3) were thereafter compared with field observations of GT and the number of generations a year as obtained in previous works (Hidalgo and Escribano, 2007, 2008).

R E S U LT S Environmental conditions Throughout the study period, time series observations allowed us to assess variability in temperature and Chl a at both places. Temperature clearly reflected the differences between locations (Fig. 2). In Mejillones the water column is warmer, with an average surface temperature of 16.98C, with a weak seasonal signal and with stratified condition prevailing year-round (Fig. 2A). The complete range of temperature in the upper 50 m was between 10.5 and 21.78C and the mean temperature at 10-m

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depth was 15.038C. In contrast, Concepcioń showed a strong seasonal temperature signal, with a mean surface temperature of 13.48C, less thermal stratification in the autumn – winter period (Fig. 2B), and surface warming and more stratified conditions in the spring – summer. The complete range of temperature in the upper 50 m was between 9.6 and 18.18C for the whole period. Food conditions, as assessed by Chl a measurements, also showed marked differences between Mejillones and Concepcioń. In Mejillones the average Chl a in surface water was 6.1 mg Chl a m23 and at 10-m depth 7.2 mg Chl a m23 during the entire period. At this location, Chl a in the upper 20 m remained .2 mg m23 during the study period and also exhibited a weak seasonal signal, but with some interannual variation (Fig. 3A). In Concepcioń Chl a reaches a maximum every spring– summer with concentrations up to .20 mg m23, but in the autumn–winter Chl a diminishes to ,1 mg m23, and this seasonal pattern repeats every year (Fig. 3B). The mean Chl a in surface water was 4.6 mg m23 for the entire study period and the range in the upper 20 m was between 0.1 and 53.1 mg Chl a m23.

Fig. 2. Spring– summer (S– S) and autumn– winter (A– W) variation of temperature in the upper 50 m layer of Mejillones (A) during 2011–2006, and Concepcioń (B) during the period 2002–2012. At Mejillones the contours were constructed from four seasonal profiles of CTD per year at 1 m depth resolution, and at Concepcioń from monthly CTD profiles (1 m resolution). The black arrows at the bottom of each panel indicate the dates when copepods were sampled to conduct experiments on egg production (EP) and development rate (DR).

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Fig. 3. Spring– summer (S –S) and autumn– winter (A– W) variation of phytoplankton biomass, measured as Chlorophyll a, in the upper 50 m layer of Mejillones (A) during 2011– 2006, and at Concepcioń (B) during the period 2002–2012. At Mejillones the contours were constructed from measurements of Chl a at five depths four times a year (seasonal sampling), and at Concepcioń from monthly measurements of Chl a at six depths. The black arrows at the bottom of each panel indicate the dates when copepods were sampled to conduct experiments on egg production (EP) and development rate (DR).

Egg production Mean EPs for each species, with data pooled from all the experiments at both locations, and all seasonal periods, are shown in Table II. These mean values of EP were significantly different among species (F2,344 ¼ 226.2, P , 0.001) with C. brachiatus having the greatest EP and P. indicus with a much lower value. Mean values of EP separated by location and seasonal periods for the three species are illustrated in Fig. 4. Seasonal effects on EP could be tested in C. brachiatus for Mejillones and in P. indicus for both places. EP of C. brachiatus was significantly lower in the spring – summer at Mejillones (F1,123 ¼ 3.9, P , 0.05), and there were also significant differences between locations (F1,123 ¼ 7.5, P , 0.01), whereas for P. indicus there were no seasonal or location effects on EP (F1,156 , 1.0, P . 0.05). Hatching success could also be assessed in the three species after 48 h of observation. The mean hatching

success was lower in C. chilensis than in C. brachiatus and P. indicus, which had a similar value (Table II). Since adult females were subjected to variable experimental temperatures while spawning, it was thought that EP could be affected by changes in temperature after a short conditioning period (,24 h). These potential effects were tested by a regression analysis between EP as a function of temperature for all EP data pooled from locations and periods. There were no significant positive or negative effects of temperature on EP in any of the three species. Temperature effects on EP were nonsignificant in C. brachiatus (F1,124 ¼ 0.55, P . 0.05), in P. indicus (F1,156 ¼ 0.52, P . 0.05) and in C. chilensis (F1,61 ¼ 0.78, P . 0.05).

Development rates As expected, the time between egg spawning and egg hatching (DT) varied extensively depending on species

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Table II: Egg production (EP), hatching success and mean embryonic development time (DT) of three copepod species from two locations, Mejillones (238S) and Concepcioń (368S) at the coastal upwelling system off Chile Species

EP (eggs female21day21) mean + SE

Hatching success (%) mean + SE

n1

DT (d) mean + SE

n2

Temp. (8C)

C. brachiatus C. chilensis P. indicus

43.3 + 2.43 29.3 + 1.97 5.0 + 2.71

58.5 + 4.93 32.0 + 3.93 51.9 + 2.99

141 63 158

1.60 + 0.004 1.42 + 0.009 0.39 + 0.012

173 79 185

6.0–19.8 5.5–18.9 7.4–23.0

n1 is the number of females and n2 is the total number of egg clutches from which DT was assessed. DT represents the average for the entire range of experimental temperatures (Temp.).

Fig. 4. Egg production (EP) of three copepods Centropages brachiatus, Calanus chilensis and Paracalanus indicus from two coastal upwelling sites in the Humboldt Current: Mejillones (238S) and Concepcioń (368300 S), under two seasonal conditions: spring– summer and autumn–winter. EP for C. chilensis was only estimated at Concepcioń during the spring– summer season. Vertical lines are standard errors. Experiments were performed in different years between 2001 and 2012.

and temperatures. Species differences are illustrated by estimates of the mean DT shown in Table II. Despite the temperature-dependency, DT was clearly shorter (9 h) in P. indicus in comparison with 1.5 days in the other two species (Table II). Embryonic times (DT) were converted to DR and data from the three species were separated by location and seasonal period (spring – summer or autumn – winter). The linear regression model (Equation 2) was thus fitted to Ln(DR þ 1) as a function of temperature. The relationship between DR and temperature was highly significant in all cases, except for P. indicus from Mejillones during the spring – summer season (Table III). Fitted regressions for C. brachiatus are shown in Fig. 5. Both at Mejillones (Fig. 5A) and Concepcioń (Fig. 5B) eggs appeared to develop faster during the spring than in winter. In C. chilensis, we only had data for Concepcioń during the spring, but the fitted regression seemed closer to that obtained previously (Escribano et al., 1998) for the spring season at Mejillones (Fig. 6).

P. indicus exhibited a much more variable pattern compared with the other species. At Mejillones (Fig. 7A) in the spring – summer DR was independent of temperature, such that eggs under low temperature (,108C) could develop as fast as those in high temperature (188C), whereas in the autumn – winter period DR exhibited the expected and significant positive relationship with temperature. Meantime, at Concepcioń seasonal effects on DR were reflected in marked changes in the slope of the regressions with an apparently faster response of DR to temperature in the spring –summer (Fig. 7B). The GLM analysis applied for C. brachiatus and P. indicus revealed significant differences between species and also significant effects of location and season on the developmental responses to temperature (Table IV). Species responses to temperature can also be examined by comparing the slopes of the regressions (Table III). C. brachiatus had a higher slope than C. chilensis revealing a faster response to temperature change, although the mean DT of this species (Table II) was longer (1.6 days) indicating a slower DR (mean ¼ 0.63 day21), compared with C. chilensis (mean DR ¼ 0.71 day21). Meanwhile, P. indicus displayed a much higher slope than the other two species, as well as the fastest egg development (mean DR ¼ 2.56 day21). Regarding location and seasonal effects on DR, it was found that DR was significantly higher during the spring– summer compared with autumn–winter and at Mejillones compared with Concepcioń. This was found for C. brachiatus and P. indicus. Some of the location and seasonal effects on the egg response to temperature can also be assessed by looking at the slopes of the regressions (shown in Table III). For instance, in Mejillones the slope of the autumn–winter regression for C. brachiatus is significantly lower than that of the spring–summer period (t-test2,1 ¼ 5.0, P , 0.01), whereas the slope of Mejillones is greater than that of Concepcioń (t-test2,1 ¼ 2.0, P , 0.05) for the same spring–summer period. In P. indicus the slope obtained at Mejillones was lower than those at Concepcioń, although there was more variability in the

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Table III: Summary statistics after fitting exponential equations to the temperature-dependent embryonic development rate (DR) for three copepod species, Centropages brachiatus, Calanus chilensis and Paracalanus indicus from two areas of the upwelling zone off Chile: Mejillones (MEJ) and Concepcioń (CONCE) Species

Location

Season

Ln(a)

b + SE

F-ratio

P-value

C. brachiatus

MEJ MEJ CONCE CONCE MEJ MEJ CONCE CONCE

S-S A-W S-S S-S S-S A-W S-S A-W

20.050 0.001 0.008 0.177 21.051 20.112 21.260 20.251

0.042 + 0.002 0.035 + 0.001 0.040 + 0.002 0.031 + 0.002 20.007 + 0.009 0.078 + 0.012 0.162 + 0.037 0.110 + 0.011

777.8 1495.8 598.3 315.3 0.6 42.3 19.1 91.9

,0.001** ,0.001** ,0.001** ,0.001** ,0.430ns ,0.001** ,0.001** ,0.001**

C. chilensis P. indicus

The study was carried out during the spring–summer (S–S) and autumn –winter (A –W) seasons. The exponential model was fitted in its log-linear form as: Ln (DR þ 1) = Ln ðaÞ þ b Temp. Linear fitting was tested by ANOVA after least square regression models. **Highly significant effects (P , 0.01), ns, non-significant (P . 0.05).

Fig. 6. The embryonic development rate (DR) of Calanus chilensis, as a function of temperature, from laboratory experiments performed at Concepcioń during a spring–summer condition Linear regressions were fitted on log-transformed data of DR (Ln(DR þ 1)). Statistics for fitted linear regressions are shown in Table III. 95% CL ¼ confidence limits for the regressions. The regression line for the location of Mejillones (gray line) was obtained from Escribano et al. (Escribano et al., 1998) for comparison purposes.

Fig. 5. The embryonic development rate (DR) of Centropages brachiatus as a function of temperature from two locations of the Humboldt Current: Mejillones (A), under two seasonal periods, spring–summer or autumn– winter, and Concepcioń (B) only under spring–summer condition. Linear regressions were fitted on log-transformed data of DR (Ln(DR þ 1)). Statistics for fitted linear regressions are shown in Table III. 95% CL ¼ confidence limits for the regressions.

regressions as shown in Fig. 7, so that there are no significant differences in the regression slopes between locations and seasons (t-test2,1 , 1.0, P . 0.05). The relationship between EP and DR is shown in Fig. 8 for the three species. Within species DR varies independently from EP, but when comparing species the reproductive patterns are revealed. In P. indicus, there is a high variance of DR and lower variance in EP, whereas in C. brachiatus and C. chilensis EP is more variable and DR has less variability. This species clearly develops much faster than C. brachiatus and C.

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Table IV: General linear model (GLM) analysis to test location and seasonal effects on the temperature-dependent embryonic development rate (DR) of two copepod species, from the upwelling zone off Chile, Centropages brachiatus and Paracalanus indicus from Mejillones (238S) and Concepcioń (368S), and two seasonal periods: spring– summer and autumn– winter. Source of variance C. brachiatus Temperature Location Season Error P. indicus Temperature Location Season Error

df

MS

F-ratio

P-value

1 1 1 169

3.300 0.021 0.040 0.002

1524.1 9.9 18.8

,0.001** 0.002** ,0.001**

1 1 1 181

2.321 6.684 1.249 0.091

23.5 67.7 12.7

,0.001** ,0.001** ,0.001**

DR as a function of temperature was described by an exponential model in its log-linear form, Ln (DR þ 1) = Ln ðaÞ þ b Temp. **Highly significant effects (P , 0.01).

Fig. 7. The embryonic development rate (DR) of Paracalanus indicus as a function of temperature from two locations of the Humboldt Current: Mejillones (A) and Concepcioń (B) and under two seasonal periods, spring–summer and autumn–winter. Linear regressions were fitted on log-transformed data of DR (Ln(DR þ 1)). Statistics for fitted linear regressions are shown in Table III. 95% CL ¼ confidence limits for the regressions. The relationship between DR and temperature for the spring–summer condition in Mejillones was non-significant (ANOVA P . 0.05).

chilensis which exhibit different EP values, but are similar in their DRs.

DISCUSSION A large clutch size, as assessed by EP, could be a strategy to maximize the number of offspring (Bunker and Hirst, 2004; Kiørboe and Hirst, 2008), as in that exhibited by Centropages brachiatus, having a single spawning of over 100 eggs per female. This is usual for Centropages spp. with EPs .80 eggs female21 day21 (Kiørboe and Sabatini, 1995). Meantime, Calanus chilensis maintained a mid-range EP of 30 eggs female21 day21, similar to other Calanus species (Mauchline, 1998). In contrast, the low EP of Paracalanus indicus is remarkable, with no .10 eggs spawned at any one time, and often under five eggs. Although EP of freeliving and parasitic copepods varies extensively through

Fig. 8. The relationship between embryonic development rate (DR) and egg production (EP) in three copepods, Centropages brachiatus, Calanus chilensis and Paracalanus indicus from two locations of the Humboldt Current: Mejillones and Concepcioń. DR was log-transformed as Ln(DR þ 1).

copepod families, many calanoids, especially broadcast spawning species, exhibit EP .20 eggs female21day21 (Poulin, 1995; Kiørboe and Sabatini, 1995). However, small calanoid copepods of the genus Paracalanus seem to produce fewer eggs (Go´mez-Gutie´rrez and Peterson, 1999). Among the factors affecting EP, temperature has been suggested as important (Ban, 1994; Richardson and

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Verheye, 1998). However, our data did not show significant effects of temperature on EP, as also found by Bonnet et al. (Bonnet et al., 2009). Quality and quantity of food have also been suggested to be important factors affecting EP of copepods (Richardson and Verheye, 1998; Møller et al., 2012). Our experiments were performed under a variety of conditions and the observed seasonal variance in EP may reflect some food effects on EP. Seasonal effects on EP of copepods have been shown in many regions and species (Checkley, 1980; Kiørboe and Sabatini, 1995; Richardson and Verheye, 1998; Hansen et al., 2010). In our study area, EP can occur year-round and perhaps without food limitation (Escribano and McLaren, 1999; Hidalgo and Escribano, 2008). Although Chl a may decrease in the autumn–winter period (Fig. 3), small heterotrophic organisms (flagellate, ciliate) and small diatoms can prevail during those seasons, both at Mejillones (Iriarte and Gonza´lez, 2004) and Concepcioń (Morales and Anabaloń, 2012), and this heterotrophic/alternate diet can effectively sustain copepod feeding and reproduction during the low-Chl a season (Vargas et al., 2006). Hatching success may also be affected by food (Ianora et al., 2004; Vargas et al., 2006). In our experiments, we noticed that hatching success of C. chilensis was lower than that of C. brachiatus and P. indicus. C. chilensis seem more dependent on diatoms than the other two species (Vargas et al., 2006), and therefore may be more severely affected by potentially deleterious diatoms (Poulet et al., 2007). Extremely low temperature (,78C) might also affect hatching success, or retard embryonic development (Mauchline, 1998). Perhaps, observations longer than 48 h at low temperatures might have revealed some slowdeveloping eggs, as found in similar species (Kiørboe and Sabatini, 1995), although we noticed that at 48 h nonhatching eggs showed signs of disintegration, indicating they were unviable. Despite the low EP, P. indicus has become the numerically dominant species in coastal waters of the Humboldt Current (Heinrich, 1973; Hidalgo et al., 2010). The spawning frequency of this species is unknown, but is probably high, because all life stages can be found year-round (Escribano et al., 2007), indicating continuous reproduction. A fast DR may promote continuous reproduction, because young stages can reach maturity shortly, and thus can assure a continuous supply of gravid females. Therefore, a fast DR appears to be the strategy of P. indicus for sustaining populations at high levels and achieving dominance in the HCS. DRs of C. brachiatus and C. chilensis respond similarly to temperatures. It is therefore not surprising that their annual life cycles are quite similar too (Hidalgo and Escribano, 2008), and they tend to coexist in time (Hidalgo and Escribano, 2008) and space (Gonza´lez and Marıń, 1998).

If embryonic DRs represent the species responses to temperature, we can estimate species generation time (GT) by using egg DRs. Escribano et al. (Escribano et al., 1997) found that egg DR of C. chilensis at any temperature was 5% of total development time between egg hatching and adulthood. This means an “equiproportional” development by which each stage occupies a fixed proportion of total development time, as proposed by Corkett et al. (Corkett et al., 1986). Applying this rule, we estimated GT for a broad range of temperatures between 4 and 248C for both upwelling sites (Fig. 9). At Mejillones GT for C. brachiatus is 22 days in the spring–summer and nearly 24 days in the autumn–winter at 178C, which is the mean surface temperature at this site, whereas GT of P. indicus at this temperature might be as short as 8 days. On the other hand, at Concepcion (Fig. 9B) GT for C. brachiatus and C. chilensis become similar at temperatures .158C with an estimate of 24 and 22 days at 158C for C. brachiatus and C.

Fig. 9. Expected generation time (GT) as a function of temperature in three copepods species, Centropages brachiatus, Calanus chilensis and Paracalanus indicus, from two locations of the Humboldt Current: Mejillones (A) and Concepcioń (B) under spring–summer and autumn–winter conditions. The shaded area represents the observed range of temperature at both places during the study period (2001– 2012).

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chilensis, respectively. However at the mean temperature of 12.48C at 10 m depth in Concepcioń, expected GTs are 38 and 32 days For C. brachiatus and C. chilensis, respectively. At that temperature, P. indicus can have a variable range of GT between 11 and 20 days. In field studies, GT and the number of generations a year (NGY) of C. chilensis and C. brachiatus have been assessed from Mejillones (Hidalgo and Escribano, 2008). This work used a 2-year time series sampling and was able to detect 15 generations of both species a year, with an average GT of 20 days for C. chilensis and 22 days for C. brachiatus. Our estimates of GT using embryonic DRs are within the range of 22– 24 d for C. brachiatus, at temperatures between 16 and 178C (see Fig. 9A), which is the usual temperature range of surface water in Mejillones. Similarly, at Concepcioń, Hidalgo and Escribano (Hidalgo and Escribano, 2007) also estimated GT and NGY for C. brachiatus and C. chilensis from field samples. They suggested 10 and 12 generations a year for C. brachiatus and C. chilensis, respectively, with GT in the range of 30– 35 days for C. brachiatus and 25– 30 days for C. chilensis. Again, our temperature-dependent estimates of GT can reproduce these field observations. In this region, the surface temperature is in the range of 12– 138C. For these temperatures, our estimates are quite consistent with these observations (see Fig. 9B), suggesting GTs in the range of 29– 32 and 25– 27 days for C. brachiatus and C. chilensis, respectively. For the same temperature range, P. indicus might have a GT in the range of 11– 20 days with the potential to produce .30 generations a year if reproduction was continuous. The assumption that generation times can be solely explained by temperature is difficult to sustain. GT varies extensively, within and among species, as reviewed by Mauchline (Mauchline, 1998). Both field and laboratory findings have shown that food quantity/quantity can influence development of copepods (Mauchline, 1998). Development of small nauplii can also be greatly affected by food resources (Rey et al., 2001). Nevertheless, if food supply is high, diverse and available year-round, and copepod species can feed effectively (Vargas et al., 2006), so as to sustain continuous reproduction, it may be possible that temperature can explain at least a large proportion of copepod development with implications for their population dynamics. In fact, even during the warming event 1997 –98 El Ninõ, when food resources were supposedly depleted, C. chilensis increased in abundance, apparently due to accelerated development under warmer conditions (Ulloa et al., 2001). Other factors may also influence GT in nature. Copepod cohorts can actually delay their development for several reasons. For example, high mortality can increase GT when acting on non-synchronous cohorts

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(Hirst and Kiørboe, 2002), or cohorts can simply be delayed because of seasonal adjustment or after a phenological response (Yang and Rudolf, 2010). Delayed cohorts may occur more often in strongly seasonal environments, such as Concepcioń, where reproductive activity clearly becomes more intense in the spring and diminishes during the winter (Vargas et al., 2010). In the world ocean copepod populations show a strong dependence on temperature. For example, development and growth rates (Huntley and Lopez, 1992), reproduction rates (Halsband-Lenk et al., 2002; Bonnet et al., 2009), body size (Forster et al., 2011) and even sex ratio (Lee et al., 2003), may all be temperature dependent processes. Furthermore, it seems safe to assume a temperature dependency when there is no food shortage, which is a condition easily achieved in a controlled laboratory environment (Lee et al., 2003). However, the question of whether this occurs in nature is not easily answered. Nevertheless, mid-latitude copepods, like those inhabiting highly productive upwelling systems, may indeed have their dynamics fundamentally controlled by temperature, as our findings suggest.

AC K N OW L E D G E M E N T S The collaboration with the Universidad de Antofagasta was essential to carry out the experiments at Mejillones (northern Chile). The completion of this paper was achieved at the CNRS Banyuls-sur-Mer Observatory (France), supported by the LIA MORFUN Program. Comments from three anonymous reviewers greatly contributed to improve earlier versions of the work. REDOC.CTA Project of Universidad de Concepcioń also supported this work.

FUNDING This work was supported by Grant FONDECYT 1110539 of the Chilean Commission for Science and Technology (CONICYT).

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