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Pandalus Borealis) Females Subject to Different Temperature and Feeding Conditions

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Pandalus Borealis) Females Subject to Different Temperature and Feeding Conditions Marine Biology (2005) 147: 895–911 DOI 10.1007/s00227-005-1633-6 RESEARCH ARTICLE Sophie Brillon Æ Yvan Lambert Æ Julian Dodson Egg survival, embryonic development, and larval characteristics of northern shrimp (Pandalus borealis) females subject to different temperature and feeding conditions Received: 25 May 2004 / Accepted: 31 March 2005 / Published online: 18 May 2005 Ó Her Majesty in Right of Canada As represented by the Minister of Fisheries and Oceans 2005 Abstract Laboratory experiments on ovigerous females Maine (Bergstro¨ m 2000). This species is a protandric of northern shrimp (Pandalus borealis) were used to as- hermaphrodite. Each individual matures and functions sess the effects of temperature and food ration on female first as a male, passes through a transitional or inter- condition during incubation and examine how combined sexual phase, and becomes a female (Shumway et al. effects of temperature and female condition influenced 1985). In the Gulf of St. Lawrence, ovigerous females egg survival, embryonic development, and larval char- are generally concentrated at 150- to 350-m depth acteristics. Ovigerous females were maintained at 2°C, (Simard and Savard 1990) where temperatures range 5°C, and 8°C and fed on a low (three times/week; 2– from 2°Cto6°C (MPO 2001). However, in its south- 2.7% W/W) or high ration (five times/week at satiation). ernmost limit in the Gulf of Maine, temperature can The increase in temperature accelerated the develop- exceed 6°C and even reaches 9°C during some periods of mental time of the eggs but their survival at 8°C was the year (Apollonio et al. 1986; Koeller 2000). reduced. Conversion efficiency of yolk reserves in Fluctuations in the abundance of northern shrimp, developing embryos was significantly reduced at ele- Pandalus borealis, have been observed in some popula- vated temperatures and larvae hatching at 2°Cand5°C tions such as in the Gulf of Alaska (Anderson 1999), were significantly larger and heavier than those hatching Gulf of Maine (Apollonio et al. 1986), Barents Sea (Lysy at 8°C. The experimental design did not result in any and Dvinina 1991), and Scotian Shelf (Koeller 2000). effect of food ration on the energetic condition of fe- Important declines in the landings of northern shrimp in males or on egg characteristics and their biochemical Alaska and Gulf of Maine during the last half of the composition. However, lower energy reserves were ob- 1970s led to the closure of these fisheries for a few years served for females held at 8°C. (Apollonio et al. 1986; Anderson and Piatt 1999). These declines were attributed to an increased exploitation of stocks and/or responses to changes in environmental conditions. Relationships between fluctuation in abundance and Introduction seawater temperature regime have been established for some populations (Apollonio et al. 1986; Lysy and The northern shrimp is largely distributed in the Dvinina 1991; Anderson 1999; Anderson and Piatt Northwest Atlantic from the Davis Strait to the Gulf of 1999). In the Gulf of Alaska, declines in the abundance of several pandalid species occurred quickly following water column warming (Anderson 1999). It was hypothesized that the mechanism controlling long term Communicated by R.J. Thompson, St. John’s variations in fecundity and, perhaps, changes in popu- S. Brillon Æ J. Dodson lation size was water temperature (Apollonio et al. De´ partement de biologie, Faculte´ des sciences et de ge´ nie, 1986). High fecundity in the mid-1960s and late 1970s Universite´ Laval, Pavillon Alexandre-Vachon, Ste-Foy, Quebec, corresponded with periods of low April–July offshore G1K 7P4, Canada bottom water temperatures in the southwest Gulf of Y. Lambert (&) Maine while low fecundity in the late 1960s and early Fisheries and Oceans Canada, Institut Maurice-Lamontagne, 1970s corresponded with high offshore bottom water 850 route de la mer, Mont-Joli, Quebec, G5H 3Z4, Canada E-mail: [email protected] temperatures at the same time of the year (Apollonio Tel.: +1-418-7750599 et al. 1986). In the Barents Sea, shrimp biomass was Fax: +1-418-7750740 associated with the spring temperature occurring 2 or 896 3 years before (Lysy and Dvinina 1991). The highest were less tolerant of warmer temperature after becoming level of biomass was observed when spring surface and female (Apollonio et al. 1986) but no experiments in bottom water temperatures were 1–3°C lower than in controlled conditions have confirmed this hypothesis. situations where the biomass was at its lowest level. Moreover the effect of food availability on female con- A marked effect of temperature on the length of the dition, egg survival, and embryonic development has not incubation period was observed in ovigerous females of been examined. northern shrimp (Stickney and Perkins 1977; Nunes The objective of this study was to examine, under 1984). Egg mortality, however, was not affected by laboratory conditions, the combined effects of temper- temperature (Stickney and Perkins 1977). An inverse ature and food ration on the energetic condition of relationship was observed between fecundity and water ovigerous female of northern shrimp and how combined temperature; fecundity of shrimp at 3°C and 6°C being effects of female condition and temperature influence greater than fecundity at 8–9°C (Nunes 1984). Based on egg survival, embryonic development and larval char- morphometric characteristics of eggs and larvae, it was acteristics. Experimental results on female condition, egg concluded that optimum temperature for reproductive and larval production and characteristics were also processes was within a narrow range of temperature compared to observations in the wild. Laboratory between 3°C and 6°C (Nunes 1984). Larger larval size experiments were conducted at three temperatures and and lower egg mortality were observed at these tem- two food rations. Temperatures of 2°C, 5°C, and 8°C peratures. were selected as these represent temperatures where Larval size and condition at hatching affect the ability ovigerous females are usually found in their distribu- of the larvae to begin exogenous feeding. During their tional area in the North Atlantic. development, embryos rely on yolk reserves for their nutritional needs. Growth during this period of yolk dependence is determinant for later survival (Braum Materials and methods 1967). Rate of yolk absorption and incubation time are temperature dependent and the conversion efficiency of Shrimp collection yolk into tissue is affected by the temperature at which embryos are developing (Heming 1982). To date, no Ovigerous females of northern shrimp (carapace length studies have examined the pattern of energy utilization 20–30 mm) were captured using a rigid frame trawl during embryogenesis in northern shrimp and the cor- (150 m depth) in the St. Lawrence estuary near Ri- responding characteristics of larvae at hatching. Rate of mouski, Que´ bec in late October 2001 and April 2002. utilization of organic reserves during embryogenesis had Following capture, shrimp were transported to the been studied, however, for other shrimps species (Weh- Maurice Lamontagne Institute and kept in 670-l rect- rtmann and Graeve 1998; Wehrtmann and Kattner angular tanks at a temperature of 5°C under natural 1998; Nates and McKenney 2000; Narciso and Morais photoperiod (latitude 49°45¢N) and salinity (>28 psu). 2001; Morais et al. 2002) and marine invertebrates such In late October 2001, a sample of 60 females was taken as lobsters (Pandian 1970a, 1970b; Sasaki et al. 1986; at random prior to the start of the experiments to Attard and Hudon 1987) and crabs (Biesiot and Perry determine female condition, and egg number and char- 1995; Petersen and Anger 1997; Gardner 2001). Few acteristics in field conditions at the beginning of the studies have examined the link between egg character- experiment. Three hundred and sixty shrimp also istics and characteristics of the larvae at hatching captured in October were then assigned at random to (Sasaki et al. 1986; Nates and McKenney 2000; Gimenez the tanks with the different experimental treatments. In and Anger 2001). the spring of 2002, 25 ovigerous females caught prior to During the incubation period, northern shrimp em- the hatching period of larvae in the St. Lawrence estuary bryos are carried in a mass attached to the pleopods of were isolated in tanks and followed during the hatching the female. Parental care is provided to the embryos period to determine female condition, larval production through pleopod movements, which bring oxygen to and characteristics in the wild. embryos (Baeza and Fernandez 2002). This behavior is probably essential for their normal development. Larger energy expenditures have been reported for some crab Experimental design species with this increase in the activity of ovigerous females (Fernandez et al. 2000; Baeza and Fernandez The laboratory experiment was conducted between 2002). Thus, the energetic condition of ovigerous fe- November 2001 and July 2002. The experimental set-up males may play an important role in the development of was made up of three semi-open seawater systems, each the embryos. Major costs experienced by females during system having two tanks with a capacity of 670 l the incubation period are associated with maintenance (2.23 m2 area, 0.30 m depth). Each system had a head and parental care since no molt occurs during that tank with a capacity of approximately 125 l, a sand filter period. Energy reserves available for maintenance and and a heat pump to regulate water temperature. Sea- activity are influenced by food availability and temper- water flow to each tank was of 15 l minÀ1 and new ature. It has been hypothesized that northern shrimp seawater flow through each system was 2.5 l minÀ1. 897 Temperature treatments of 2°C, 5°C, and 8°C were The CF was expressed with the formula: randomly assigned to each system and the two tanks of 2:6 each system were divided into two equal parts with a CF ¼ðW =CL Þ100 partition.
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