Reproductive traits of tropical deep-water pandalid shrimps (Heterocarpus ensifer) from the SW Gulf of Mexico

ARTICLE IN PRESS Deep-Sea Research I 57 (2010) 978–987

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Reproductive traits of tropical deep-water pandalid shrimps (Heterocarpus ensifer) from the SW Gulf of Mexico Patricia Briones-Fourza´n n, Cecilia Barradas-Ortı´z, Fernando Negrete-Soto, Enrique Lozano-A´lvarez ´noma de Me´xico, Instituto de Ciencias del Mar y Limnologı´a, Unidad Acade´mica Puerto Morelos. Ap. Postal 1152, Cancu ´ n, Quintana Roo 77500, Me´xico Universidad Nacional Auto

a r t i c l e in f o

a b s t r a c t

Article history: Received 30 October 2009 Received in revised form 20 March 2010 Accepted 23 April 2010 Available online 15 May 2010

Heterocarpus ensifer is a tropical deep-water pandalid shrimp whose reproductive features are poorly known. We examined reproductive traits of a population of H. ensifer inhabiting the continental slope (311–715 m in depth) off the Yucatan Peninsula, Mexico (SW Gulf of Mexico). Size range of the total sample (n ¼ 816) was 10.4–38.9 mm carapace length. Females grow larger than males, but both sexes mature at 57% of their maximum theoretical size and at  30% of their total lifespan. Among adult females, the proportion of ovigerous females was high in all seasons, indicating year-round reproduction. Most females carrying embryos in advanced stages of development had ovaries in advanced stages of maturation, indicating production of successive spawns. In the autumn, however, the proportion of ovigerous females and the condition index of these females were lower compared to other seasons. This pattern potentially reflects a reduction in food resources following the summer minimum in particulate organic carbon flux to the deep benthos, as reported in previous studies. Spawns consisting of large numbers (16024 7 5644, mean7 SD) of small eggs (0.045 70.009 mm3) are consistent with extended planktotrophic larval development, an uncommon feature in deep-water carideans. Egg number increased as a power function of female size but with substantial variability, and egg size varied widely within and between females. There was no apparent trade-off between egg number and egg size and neither of these two variables was influenced by female condition. These results indicate iteroparity and a high and variable reproductive effort, reflecting a reproductive strategy developed to compensate for high larval mortality. The present study provides a baseline to compare reproductive traits between Atlantic populations of this tropical deep-water pandalid. & 2010 Elsevier Ltd. All rights reserved.

Keywords: Caridea Deep-sea reproduction Pandalid shrimps Reproductive trade-offs

1. Introduction The family Pandalidae (Crustacea: Decapoda: Caridea) is a cold-water family of mainly epibenthic shrimps occurring from shallow depths in boreal waters to depths of about 2000 m in tropical regions (Holthuis, 1980; Chace, 1985; Bauer, 2004). Reproductive strategies differ widely between pandalid species as they exhibit a variety of sexual systems (gonochorism, protandrous hermaphroditism, or partial protandric hermaphroditism with primary males or primary females) and types of reproduction (semelparity vs. iteroparity), even within the same genus (e.g., Pandalus) (Correa and Thiel, 2003; Bauer, 2004). However, the species grouped in the tropical deep-water genus

Abbreviations: BW, body weight; CL, carapace length; CLmax, size of largest specimens in the sample; CL50, size at which 50% of females are ovigerous; CLN, maximum theoretical size; SOM, size at the onset of sexual maturity; RSOM, relative size at the onset of sexual maturity ( ¼ SOM/CLN); ES, egg size; EMV, eggmass volume; IRP, index of reproductive potential; PI, productivity index; RO, reproductive output. n Corresponding author. Tel.: + 52 998 871 0367x145; fax: + 52 998 871 0138. E-mail address: [email protected] (P. Briones-Fourza´n). 0967-0637/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2010.04.009

Heterocarpus are gonochoristic (King and Moffit, 1984) and typically iteroparous (King and Butler, 1985; Dailey and Ralston, 1986; Roa and Ernst, 1996). The type-species of the genus is Heterocarpus ensifer A. Milne Edwards, 1881, which was originally described from specimens collected at a depth of  400 m off the Caribbean island of Barbados (Milne Edwards, 1881). In the western Atlantic, this species occurs at depths of 170–885 m from North Carolina (USA) to Brazil, including the Gulf of Mexico and Caribbean sea (Holthuis, 1980; Lozano-A´lvarez et al., 2007, and references therein). In the eastern Atlantic, it occurs at depths of 88–1278 m from the Iberian peninsula to the Congo, including the archipelagos of Azores, Madeira, Canaries and Cape Verde, and in the Spanish Mediterranean (Tuset et al., 2009, and references therein). H. ensifer has also been reported as occurring in the Indo-west Pacific and southwestern Indian oceans (Holthuis, 1980; Crosnier, 1988; Poupin, 1994); however, based on extensive morphological comparisons, several authors have concurred that only the specimens from the Atlantic and the SW Indian ocean (and possibly also those from Hawaii, Kiribati, and the Marquesas in the Pacific) correspond to the species described by Milne Edwards (Crosnier and Forest, 1973; Chace, 1985; Crosnier, 1988;

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Poupin, 1994). Therefore, the contention of King and Butler (1985) that H. ensifer is a short-lived, semelparous species is questionable (Poupin et al., 1990), as their samples were collected in Fiji, a location within the Pacific region where the taxonomic identity of ‘‘H. ensifer’’ specimens has not been resolved (Poupin, 1994). Understanding the reproductive strategies of a species is important because they play a major role in its biogeography and the dynamics of its populations (Stearns, 1976; Sastry, 1983; Ramı´rez-Llodra, 2002). For example, in species that occur along broad latitudinal or longitudinal gradients, local genetic variation and/or phenotypic plasticity may result in differing reproductive features between populations (Gorny et al., 1992; Via et al., 1995; Wehrtmann and Lardies, 1999; Marshall et al., 2008). This may well be the case for H. ensifer but, to our knowledge, only three studies have addressed reproductive features of populations of H. ensifer from different Atlantic locations. In Martinique, Paulmier and Gervain (1994) compared the size distribution of males and females and estimated preliminary growth parameters for both sexes combined. In the SW Gulf of Mexico, LozanoA´lvarez et al. (2007) used regression techniques to compare ontogenetic changes in relative growth between males and females. In the eastern Atlantic, Tuset et al. (2009) estimated growth parameters for each sex and found preliminary evidence of a latitudinal gradient in the abundance of H. ensifer and in the extent of its reproductive period. All three studies reported the presence of ovigerous females in every season, but neither examined reproductive traits based on the number and size of eggs produced by local females. Egg production is an important ecological and evolutionary trait as it reflects maternal investment and influences both maternal and offspring fitness (Marshall et al., 2008), and because the supply of new individuals is an important driver of marine population dynamics (Underwood and Keough, 2001). Due to

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morphological constraints of the female body, there is usually a trade-off between egg number and size between and within species (Smith and Fretwell, 1974). An intraspecific trade-off between egg number and size has been demonstrated in many crustaceans, especially in semelparous species (Mauchline, 1988; Poulin, 1995), including some caridean shrimps (Clarke, 1993a). However, this trade-off has been more difficult to demonstrate in species wherein females are iteroparous or use adult-acquired resources for reproduction (review in Fox and Czesak, 2000), traits that may result in a variable reproductive effort (i.e., the rate at which resources in excess of maintenance and activity requirements are diverted into reproduction rather than growth) (Stearns, 1976; Clarke, 1987; Ramı´rez-Llodra, 2002). The aim of the present paper was to examine population structure, sex ratio, critical sizes and ages pertaining to reproductive activities, reproductive period, type of reproduction, brood size, reproductive effort, and the potential trade-off between egg number and egg size in H. ensifer shrimps from the SW Gulf of Mexico. Based on studies conducted in other congeneric species (King and Butler, 1985; Dailey and Ralston, 1986), we hypothesized that these interrelated traits would reflect iteroparity and a substantial variation in reproductive effort for this species.

2. Materials and methods 2.1. Study area and biological samples The continental slope off the Yucatan peninsula (SW Gulf of Mexico, Fig. 1) is a steep escarpment with a highly complex topography from which information on decapod crustaceans in general is very scant (Wicksten and Packard, 2005; EscobarBriones et al., 2008). The broad Yucatan shelf and adjacent upper

Fig. 1. Schematic map of study area showing the approximate location of sampling stations yielding catches of Heterocarpus ensifer in each cruise. Shown are the 200 and 500 m isobaths.

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Table 1 Summary of sampling data for the five cruises. Season/year

Date

Depth range (m)

Average depth (m)

N total shrimps

Percentage of adults

Autumn/1985 Winter/1986 Summer/1989 Summer/2005 Spring/2007

October 20–21 February 4–8 August 15–17 August 11–12 June 1–7

340–470 425–715 375–414 352–456 311–461

411 514 386 415 412

366 107 60 246 37

63 95 98 94 74

Only sampling stations that yielded catches of Heterocarpus ensifer are considered.

slope are under the influence of a seasonal subsurface upwelling of Caribbean water originating from depths of 220–250 m in the Yucatan channel (Merino, 1997). During the spring and summer, this water intrudes over the eastern Yucatan shelf without breaking the water surface and moves westward across the shelf, creating a two-layered water column. The upwelling weakens in the autumn and ceases during the winter, when cold fronts bring strong northerly winds that mix the water column (Merino, 1997). These seasonal changes in the strength of the subsurface upwelling potentially modulate the flux of organic matter reaching the upper slope (Barradas-Ortiz et al., 2003). Specimens of H. ensifer were collected in several sampling stations on the continental slope of the Yucatan peninsula during five research cruises of the R/V Justo Sierra aimed to survey the benthic fauna from the upper slope (200–715 m in depth). The cruises were conducted at different seasons in different years: October 1985 (autumn, three sampling stations), February 1986 (winter, four stations), August 1989 (summer, three stations), August 2005 (summer, three stations), and June 2007 (spring, four stations). Sampling gear consisted in baited bottom-set traps (121 cm  91 cm  40 cm, mesh size of 1.25 cm) and, where possible, benthic trawl nets (24 m mouth aperture; 4.5 cm stretched mesh body and 1.5 cm stretched mesh cod-end). Specimens of H. ensifer occurred at depths of 311–715 m (Table 1), but did not occur at depths o311 m. Shrimps were fixed on board and preserved in 70% ethanol, but routine morphometric measurements were performed within several weeks after collection. These measurements included carapace length (CL, from the posterior margin of the orbit to the posterior edge of the carapace), measured with vernier calipers to the nearest 0.1 mm, and body weight (BW) measured to the nearest 0.01 g after blotting excess moisture. Sex of individual shrimps was determined by examination of the shape of the endopods of the first pleopods and the presence or absence of the appendix masculina on the endopods of the second pleopods (King and Moffit, 1984). In females, the presence or absence of an egg mass was recorded. 2.2. Size distribution, sex ratios and reproductive sizes and ages Data from all cruises were pooled to examine size distribution, overall sex ratio and sex ratio as a function of size (Wenner, 1972), and to compare the mean sizes of males and females across the entire size range. For each sex, we estimated the following critical sizes pertaining to reproductive activity: size at the onset of sexual maturity (SOM, considered as the size of the smallest males with appendices masculinae and the size of the smallest ovigerous females), size of the largest individuals in the sample (CLmax), maximum theoretical size (CLN, estimated by dividing CLmax by 0.95) (Pauly, 1984), and relative size at the onset of maturity (RSOM, which is the ratio of SOM to CLN) (Charnov, 1990; Anger and Moreira, 1998). For females, we also estimated the mean size at maturity, CL50 (i.e., the size at which 50% of the female population was ovigerous) using a logistic regression of

the form Y ¼1/[1+ exp  (a+ b CL)], where CL is the size of females (continuous independent variable, X), Y is a dichotomous dependent variable with a value of either 0 (egg mass absent) or 1 (egg mass present), and a and b are the regression coefficients. The logistic transformation linearizes the model and predicts continuous values for Y that stay within the 0–1 boundaries. As the Y-axis indicates the proportion of 1s (egg mass present) at any given value of X, when Y ¼0.5, CL50 ¼  a/b (Tuset et al., 2009). To estimate the age of H. ensifer at each of these critical sizes, we used von Bertalanffy’s growth parameters (t0, K and LN) derived by Paulmier and Gervain (1994) from their samples of H. ensifer from Martinique. However, as these authors obtained smaller shrimps at ‘‘shallow’’ depths (200–370 m) and larger shrimps at ‘‘deeper’’ depths (480–600 m), they estimated one set of parameters for the ‘‘shallow’’ population (t0 ¼ –3.383, K¼ 0.0487 month  1, CLN ¼39.99 mm) and another set of parameters for the ‘‘deep’’ population (t0 ¼–2.437, K ¼0.0664 month  1, CLN ¼40.90 mm). Although this procedure was likely unwarranted as the mean size of individuals within Heterocarpus species tends to increase with depth (Dailey and Ralston, 1986; Tuset et al., 2009), we used both sets of parameters as proxies to estimate the age (in months) at SOM, CLmax and CL50 for our samples of H. ensifer. Although the presence of immature individuals varied widely among cruises (see Table 1), adult individuals—which were the main target of our study—constituted a large proportion of shrimps in all cruises. With the caveats that the cruises were conducted in different years and were widely spaced in time, we considered the adult portion of the sample (individualsZSOM) from each cruise as representative of the season in which that cruise was conducted. We used a general linear model (Howell, 2002) to compare the mean sizes between sexes (fixed factor with two levels, adult males and females) and seasons (fixed factor with five levels corresponding to the five cruises). The dependent variable (size) was previously transformed to Ln(CL +1) to increase homogeneity of variances. In each season, departures from a 50% sex ratio in adult shrimps were compared with separate Yates-corrected w2 tests (Zar, 1999). 2.3. Adult females: reproductive activity and physiological condition To determine the extent of the reproductive period and a potential seasonality in reproductive activity, we compared the seasonal percentage of occurrence of ovigerous females (relative to the total number of adult females) with a w2 contingency table (Zar, 1999). Also, because egg production may be influenced by maternal condition (Clarke, 1993a), we computed a morphometric index of physiological condition [the ratio of Ln(BW+ 1) to Ln(CL+1)] for all ovigerous females and subjected these data to a general linear model to test for the effect of season. The degree to which ovigerous females in a population are producing successive broods is indicated by the relationship between the degree of embryo development and the degree of

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ovarian development. Following Bauer (1986), degree of embryo development was classified as: stage 1, early embryos with no visible blastoderm; stage 2, blastoderm distinct, no eye development; stage 3, embryos with eyes, abdomen not free from cephalothorax; stage 4, embryos near hatching, little yolk, large eyes. Degree of ovarian development was classified as: stage 1, no noticeable ovarian development; stage 2, vitellogenic oocytes distinct but ovary small; stage 3, ovary with vitellogenic oocytes filling more than half but not all the space above the cardiac stomach; stage 4, ovary completely filling that space (Bauer, 1986). We tested for a relationship between stage of embryo development and stage of ovarian development with a w2 contingency table. For comparison, we also determined the stage of ovarian development in a sample of non-ovigerous females.

2.4. Egg number, egg size and reproductive output Egg number and size were only estimated from ovigerous females collected in the summer of 2005, as these variables were not routinely measured in previous cruises and few ovigerous females were collected in the spring of 2007. In addition, only females carrying recently spawned eggs (embryo stages 1–2) were used, as egg size in pandalids tends to increase with embryo development and egg loss may occur across the incubation period (Ohtomi, 1997; Wehrtmann and Andrade, 1998; Rosa et al., 2007; Oh et al., 2008). From the egg mass of each of 40 females (size range 25.5–37.5 mm CL), we took a random subsample of 10 eggs to measure their individual length and width under a stereoscopic microscope with a calibrated ocular micrometer. The size ( ¼volume, mm3) of each egg was estimated with the equation for oblate spheroids, V¼1/6(pW2L), where V¼volume, W¼width and L¼length (Rosa et al., 2007). The size of the 10 eggs was averaged for each female and the coefficient of variation (CV) was used to examine variability in egg size within and between females (Clarke, 1993b). Egg number was estimated for 60 females (25.0–37.5 mm CL), including the 40 females used to estimate egg size. As the eggs of H. ensifer are very small and tightly packed, we removed the entire endopods with the attached egg mass and dried them at 45 1C for 24 h. This procedure facilitated the separation of the eggs, which were then sieved, cleaned of any remaining debris with fine pincers, and weighed on an analytical scale to the nearest 0.001 g. We separated three 0.01 g subsamples and counted the eggs in each subsample under a stereoscopic microscope. The average number of the three subsamples was used to calculate total egg number. For each female, the average egg size was multiplied by total egg number to estimate the eggmass volume (EMV, mm3). Egg size, egg number and EMV were separately regressed on CL and BW. Reproductive output (RO), measured as the ratio of the weight of the fresh egg mass to female weight, is an index of investment by a population in offspring production (Clarke et al., 1991; Anger and Moreira, 1998; Wehrtmann and Andrade, 1998). However, given that we did not weigh the fresh egg masses, we used the ratio of EMV to BW as a proxy for RO, which was regressed on CL. To examine for a trade-off between egg number and size, we first removed the potential effect of female weight on these two variables by replacing the measures of egg number and size with the residuals about the regressions of egg number on female weight (egg number residuals) and of egg size on female weight (egg size residuals). Egg size residuals were then regressed on egg number residuals (Clarke, 1993a; Poulin, 1995). A trade-off would be indicated by a negative relationship, but a substantial variation in reproductive effort by females would tend to obscure this relationship (Clarke, 1993a; Fox and Czesak, 2000). To examine

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for a potential effect of female condition on egg number and size, the effect of female size on condition was also removed. This was done by replacing the condition index of females with the residuals about the regression of Ln(BW+ 1) on Ln(CL+1) (condition residuals) given that, after spawning, females in poor condition would be expected to have a large negative residual and females in good condition a large positive residual (Clarke, 1993a). Egg number residuals and egg size residuals were then separately regressed on condition residuals. 2.5. Size-dependent reproductive indices Kanciruk and Herrnkind (1976) devised an index of reproductive potential (IRP) and a productivity index (PI) that allow, respectively, for determination of the female size classes that contribute most to the total egg production and for comparisons on egg productivity between different size classes. For each size class, IRP ¼(A  B  C)/D, where A is the proportion of females relative to the total number of adult females, B is the proportion of ovigerous females within that particular size class, C is the average number of eggs produced by females in that size class and D is a constant that is computed by setting the IRP of a specific size class to 100 as the standard (any size class can be chosen to have an IRP of 100 because this does not change the ratios of the IRP between different size classes) (Kanciruk and Herrnkind, 1976). PI ¼E/A, where E is the proportion of eggs produced by females in that size class relative to the total production of eggs. To estimate IRP and PI, we categorized the entire sample of adult females into 2-mm CL size classes.

3. Results 3.1. Size distribution and sex ratios The total sample consisted of 816 shrimps, 412 males (size range: 10.5–36.0 mm CL) (Fig. 2a) and 404 females (10.4–38.9 mm CL) (Fig. 2b). The overall mean sizes ( 7SE) of males (28.0 70.30 mm CL) and females (28.370.31 mm CL) did not differ significantly (F1, 814 ¼0.001, p¼0.987). Overall sex ratio (50.5% males, 49.5% females) did not differ significantly from unity (Yates-corrected w2 ¼ 0.060, df ¼1 and p ¼0.806), but sex ratio varied as a function of size (Fig. 3). Percentages of males and females did not depart significantly from 50% over the size classes represented by immature and newly mature individuals, but then males accumulated over a few size classes and then females accumulated until reaching 100% in the largest size class (Fig. 3). The smallest males with appendices masculinae measured 21.5 mm CL and the smallest egg-bearing females measured 23.5 mm CL (Table 2). These SOM values were consistent with SOM values estimated with regression techniques by LozanoA´lvarez et al. (2007) (21–22 mm CL for males and 23–24 mm CL for females). CLmax values for males (36.0 mm) and females (38.9 mm) (Table 2) yielded CLN estimates of 37.9 and 40.9 mm, respectively. Thus, RSOM was 0.57 for both sexes. CL50 for females was estimated as 26.1 mm using the constants derived from the logistic equation (a¼  7.7576, b¼0.2975). The two sets of ages at these critical sizes (Table 2) estimated using each of the two sets of growth parameters derived by Paulmier and Gervain (1994), indicate that male and female H. ensifer have a multi-annual lifespan (age at CLmax) and a substantial reproductive span (age at CLmax minus age at SOM) (Table 2). In total, 641 adult shrimps (302 females, 339 males) were obtained. The overall sex ratio of adult shrimps did not depart significantly from 50% (Yates-corrected w2 ¼2.022, df ¼1 and

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Table 2 Heterocarpus ensifer. Carapace length (size, mm) and age (months) of males and females at critical sizes pertaining to reproductive activities. Critical sizes

SOM CL50 CLmax

Males

Females

Size

Age 1

Age 2

Size

Age 1

Age 2

21.5

19.2

13.7

36.0

50.7

34.4

23.5 26.2 38.9

21.6 25.2 77.3

15.3 17.9 48.0

Two potential ages (age 1, age 2) at each size were estimated using two different sets of von Bertalanffy growth parameters (from Paulmier and Gervain, 1994) (Age 1: t0 ¼  3.383, K¼0.0487 month  1, CLN ¼ 39.99 mm; Age 2: t0 ¼  2.437, K¼0.0664 month  1, CLN ¼40.90 mm). (SOM: size at the onset of sexual maturity, CL50: size at which 50% of females are mature, CLmax: size of largest specimens in the sample).

Fig. 2. Heterocarpus ensifer. Size-frequency distribution of (a) total males and (b) total females. Fig. 4. Heterocarpus ensifer. Mean (+SE) carapace length (mm) of adult males and females by season, and seasonal percentages of females. Numbers in columns denote sample sizes.

size of adult shrimps was significantly affected by sex (F1, 631 ¼9.109, p ¼0.003) and season (F4, 631 ¼13.576, po0.001), but not by the interaction term (F4, 631 ¼ 1.786, p ¼0.130). Thus, mean sizes of males and females followed a similar seasonal pattern, with the smallest values in the spring of 2007 (the smallest sample) and the largest in the winter of 1986 (Fig. 4). The latter was probably due to the deeper depth range of collection for the winter samples relative to the other seasons (see Table 1), as the mean size of H. ensifer tends to increase with depth (Paulmier and Gervain, 1994; Tuset et al., 2009).

3.2. Adult females: reproductive activity and physiological condition Fig. 3. Heterocarpus ensifer. Sex ratio as a function of size. The horizontal dashed line represents 50% (1:1 sex ratio). Displayed are the percentages of males; significant departures from a 1:1 sex ratio are indicated by asterisks (np o0.05, nn p o 0.01 and nnnp o0.001). Numbers in parentheses at the bottom of the X-axis denote sample sizes.

p ¼0.155), but sex ratios differed from unity in four of the five seasonal samples (Fig. 4). The two smallest samples were strongly biased towards females (summer 1989, p ¼0.004; spring 2007, p o0.001). A bias towards males occurred in two other samples (autumn 1985, p ¼0.013; summer 2005, p¼0.026), while sex ratio was more balanced in the winter of 1986 (p ¼0.488). The mean

In total, 82.5% of all adult females were carrying eggs. In every 2-mm size class across the size range of adult females, there were far more ovigerous (69–94%) than non-ovigerous females, except for the size class that included newly mature females (23.1–25 mm CL, 43% ovigerous) (see Fig. 2b). Ovigerous females also outnumbered non-ovigerous females in every season, but their percentages differed significantly with season (w2 ¼27.992, df¼4 and p o0.001) (Table 3). The difference was due to a lower proportion of ovigerous females in the autumn (64.8%) compared to the other seasons (89.4–91.7%). When the autumn sample was removed from the comparison, the remaining seasons did not differ significantly (w2 ¼0.099, df ¼3 and p ¼0.992). The mean

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Table 3 Heterocarpus ensifer. Seasonal percentages of ovigerous females relative to total numbers of adult females (Z 23.5 mm carapace length), and condition index (mean 7 standard error) of ovigerous females. Season/year

Autumn/1985 Winter/1986 Summer/1989 Summer/2005 Spring/2007

Adult females

Ovigerous females

N total

%

91 47 41 99 24

Condition index a

64.8 89.4b 90.2b 89.9b 91.7b

0.6927 0.007a 0.756 7 0.007b 0.756 7 0.009b 0.780 7 0.006b 0.735 7 0.019ab

Similar superscript letters along a column denote statistically similar groups.

Fig. 5. Heterocarpus ensifer. Degree of ovarian development (stage 1: no development to stage 4: fully mature) in non-ovigerous females and relationship between degree of embryo development (stage 1: newly spawned to stage 4: about to hatch) and degree of ovarian development in ovigerous females. Numbers in parentheses at the bottom of the X-axis denote sample sizes.

condition index of ovigerous females also differed significantly with season (F4, 238 ¼22.180, po0.001), with the lowest value in the autumn, an intermediate value during the spring, and higher values in the remaining seasons (Table 3). All stages of ovarian development (especially stages 2–4) were observed in non-ovigerous females (Fig. 5). In ovigerous females, by contrast, most females that had recently spawned (embryo stage 1) had ovaries with little development (ovarian stages 1 and 2), whereas most females carrying embryos in advanced stages of development (embryo stages 3 and 4) had ovaries in advanced stages of maturation (Fig. 5). Therefore, the null hypothesis of no relationship between embryo development and ovarian development was rejected (w2 ¼79.121, df ¼9 and po0.001).

3.3. Egg number, egg size and reproductive output Egg numbers ranged from 3339 for a 25.5 mm CL female to 24,788 for a 34.3 mm CL female, with a mean ( 7SD) of 16,02475644 eggs. Egg number increased as a power function of CL (Fig. 6a, Table 4) and as a linear function of BW (Table 4), but about 40% of the variation in egg number was not accounted for by female size or weight. The mean (7SD) egg size for individual females varied from 0.03070.005 to 0.064 70.006 mm3 (overall average ¼0.045 70.009 mm3). Egg size was not significantly related with female size (Fig. 6b, Table 4) or weight (Table 4), and varied widely within and between females (range in

Fig. 6. Heterocarpus ensifer. Relationships between (a) egg number and carapace length (CL, mm), (b) egg size and CL, and (c) egg-mass volume and CL for ovigerous females collected in the summer of 2005.

CV¼3.5–36.0%, average¼16.4%), indicating that some females produced eggs of more disparate sizes than others. Egg-mass volume (EMV) ranged from 194.1 to 1312.9 mm3 and increased as a power function of CL (Fig. 6c, Table 4) and as a linear function of BW (Table 4), but EMV per gram of body weight (our proxy for RO) was not significantly related with female size (Table 4). After removing the effects of female weight and condition on egg number and size, no clear relationship emerged between egg size and number (r2 ¼ 0.006, p ¼0.655, Fig. 7a), egg number and female condition (r2 ¼0.061, p¼0.148, Fig. 7b) or egg size and female condition (r2 ¼0.019, p ¼0.419, Fig. 7c). 3.4. Size-dependent reproductive indices Although H. ensifer females are clearly capable of producing successive spawns, it remains to be determined how many

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Table 4 Heterocarpus ensifer. Relationships between different egg variables and female size (carapace length, CL, mm) or body weight (BW, g). Relationship

N

Equation

r2

p

Egg number (EN) vs. CL Egg number vs. BW Egg size (ES) vs. CL Egg size vs. BW Egg-mass volume (EMV) vs. CL Egg-mass volume vs. BW Reproductive output (RO) vs. CL

60 60 39 39 39 39 39

EN ¼ 0.0284 CL3.7845 EN ¼ 1322.7 BW  2621.7 ES ¼  0.0007 CL+ 0.0677 ES ¼  0.0009 BW+ 0.0584 EMV ¼ 0.0132 CL3.1081 EMV ¼ 47.588 BW+ 14.067 RO ¼35.194 CL+ 0.396

0.631 0.588 0.048 0.097 0.456 0.317 0.005

o 0.001 o 0.001 0.181 0.054 o 0.001 o 0.001 0.681

Egg size and egg-mass volume in mm3. Reproductive output was considered as the ratio of egg-mass volume/BW (N: sample size; r2: coefficient of determination).

spawns they can produce per year or whether larger females are capable of spawning more often than smaller females. Therefore, we conservatively assumed one spawn per year for ovigerous females of all sizes to compute IRP and PI, and chose the size class of 29.1–31 mm CL to compute the constant D ( ¼18.061). Females 31.1–33 mm CL had the highest IRP ( ¼151), followed by females 35.1–37 mm CL (IRP¼136) and 33.1–35 mm CL (IRP¼ 128). Thus, in conjunction, females 31.1–37 mm CL produced 64% of the total eggs (Table 5). However, the PI tended to increase with size (Table 5). The PI for the largest females (37.1–39 mm CL, PI ¼2.13) was 12 times as high as the PI for the newly mature females (23.1–25 mm CL, PI¼ 0.17).

4. Discussion

Fig. 7. Heterocarpus ensifer. Relationships between (a) egg size residuals and egg number residuals, (b) egg size residuals and female condition residuals, and (c) egg number residuals and female condition residuals for ovigerous females collected in the summer of 2005.

Our catches of H. ensifer were typically low with only a few sampling stations yielding substantial catches, probably reflecting the patchy distribution of suitable habitats for H. ensifer (muddy and sandy substrates, Tuset et al., 2009) over the complex and irregular topography of our study area. Regardless, some conclusions about the reproductive traits of H. ensifer may be drawn from the present study. The foremost conclusion is that, similar to other tropical deep-water pandalids (King and Butler, 1985; Thessalou-Legaki, 1992; Oh et al., 2008), H. ensifer has an iteroparous type of reproduction (rather than semelparous as suggested by King and Butler, 1985) as high percentages of ovigerous females occurred in all seasons and most ovigerous females with embryos in advanced development stages also had ovaries in advanced stages of maturation. Further examination of egg variables from ovigerous females collected in the summer of 2005 also supports this conclusion. For example, condition of these females was high but this had no influence on either egg number or egg size, and there was no apparent trade-off between these two variables. Also, egg size varied widely within and between females, and the size and weight of females failed to explain a substantial proportion of the variation in egg number. Sex ratio as a function of size followed the standard pattern for crustacean species wherein sex reversal does not occur and females grow larger than males (Wenner, 1972). This is the common pattern for Heterocarpus species (Dailey and Ralston, 1986; Poupin et al., 1990; Tuset et al., 2009) and for many other caridean species in which males do not depend on female defense or male/male aggressive displays to secure copulation, and a larger size for females represent an advantage for the production of more offspring (Bauer, 2004). Deep-water pandalids typically have extended reproductive periods (Poupin et al., 1990; Ohtomi, 1997; Company and Sarda , 1997; Chilari et al., 2005, Tuset et al., 2009) and this was the case for H. ensifer in our study area. However, there were proportionally less ovigerous females in the autumn compared

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985

Table 5 Heterocarpus ensifer. Estimation of the index of reproductive potential (IRP) and the productivity index (PI) for adult females arranged by 2-mm size classes (carapace length, CL). Size interval (CL, mm) 23.1–25 25.1–27 27.1–29 29.1–31 31.1–33 33.1–35 35.1–37 37.1–39 Total

No. of females

No. of ovig. fem. (Nov)

A

B

C

IRP

Egg production (Nov  C)

E

PI (E/A)

0.43 0.79 0.86 0.91 0.87 0.69 0.94 0.92

4750 6431 8513 11,053 14,111 17,750 22,037 27,040

5 26 45 100 151 128 136 54

28,502 141,484 255,393 552,655 832,550 710,003 749,245 297,442

0.01 0.04 0.07 0.15 0.23 0.20 0.21 0.08

0.17 0.43 0.63 0.86 1.05 1.05 1.79 2.13

3,567,275

1.00

14 28 35 55 68 58 36 12

6 22 30 50 59 40 34 11

0.05 0.09 0.11 0.18 0.22 0.19 0.12 0.04

306

252

1.00

The indices were calculated assuming one spawn per year. (A: proportion of females relative to total adult females; B: proportion of ovigerous females within size class; C: egg number for mid-point of size class; E: proportion of total egg production. IRP¼ (A  B  C)/D. The value of the constant D (¼18.061) in the equation was derived by setting the IRP to 100 for the 29.1–31 mm CL size class).

to other seasons and the condition of these females was the poorest among all seasons. These findings may reflect changes in the local availability of food resources, which constitute an important limiting factor for many biological processes in the deep sea, including reproductive activities (Tyler, 1988; Ramı´rezLlodra, 2002; Barradas-Ortiz et al., 2003). Thus, for benthic species such as H. ensifer, growth and egg production may ultimately depend on the ability of individuals to acquire food as well as on the timing of food acquisition. We found no information on the diet of H. ensifer, but other deep-water pandalids are known to feed on benthic deposit-feeding fauna and small pelagic organisms from the benthic boundary layer (Fanelli and Cartes, 2004). Availability of food resources for the deep benthos largely depends on the flux of particulate organic carbon (POC) from the epipelagic zone, although there are time lags involved (Company et al., 2003; Fanelli and Cartes, 2004; Johnson et al., 2007). In the Gulf of Mexico, POC fluxes show maxima in the winter and minima in the summer (Melo-Gonza´lez et al., 2000; Biggs et al., 2008), and this pattern may be further modulated at the upper slope off the Yucatan peninsula by the seasonal cycle in the strength of the local subsurface upwelling (Merino, 1997). Although the occurrence of ovigerous females of H. ensifer and their corresponding condition indices were high in the two summer samples, both measures were much lower in the autumn sample, potentially reflecting a time lag between the levels of POC fluxes and the production of benthic biomass through the food chain. As the seasonal cruises were widely spaced in time, interannual variability may also account for some of the seasonal variability in our H. ensifer samples. However, examination of giant isopods (Bathynomus giganteus) collected from a similar depth range in these as well as in other cruises revealed that these animals also showed lower reproductive and feeding activities in late summer–autumn compared to other seasons (see BrionesFourza´n and Lozano-A´lvarez, 1991; Barradas-Ortiz et al., 2003). Both B. giganteus and H. ensifer are also opportunistic scavengers, but apparently this type of feeding may not be sufficient to mitigate the seasonal changes in availability of live prey. If adult females of H. ensifer in the population that we studied spawned only once per year, the production of eggs would depend more heavily on females 31.1–37 mm CL as shown by their higher IRPs. However, the PI tended to increase with size, indicating that large females may be more important to overall egg production than their numbers would suggest. In addition, large females would likely have greater potential for successive spawnings as they divert less energy to growing than small females (Ramı´rez-Llodra, 2002; Oh et al., 2008). Although both reproductive indices were estimated based on the numbers of newly spawned eggs, further studies are needed to determine whether or not egg loss occurs during

incubation in females of H. ensifer. For example, egg loss across incubation was estimated as 48% in females of H. reedi (Wehrtmann and Andrade, 1998) but was found to be negligible in females of H. sibogae (King and Butler, 1985). Interestingly, pandalid shrimps—irrespective of species, latitude, sexual system and type of reproduction—have a rather constant RSOM of about 0.54–0.56 (Charnov, 1990) and the RSOM that we estimated for H. ensifer (0.57) fits well into this pattern. These RSOMs indicate that pandalid shrimps start reproducing when they reach 54–57% of their maximum theoretical size. Anger and Moreira (1998) estimated smaller RSOMs (0.27–0.48) for tropical shallow-water carideans and suggested that these carideans mature earlier within the duration of their lifespan than pandalids do. However, this may not necessarily be so, as RSOM is based on size whereas lifespan is based on age. Our two sets of age estimates for H. ensifer at SOM, CL50 and CLmax show that both sexes have a multi-annual lifespan and a substantial reproductive span. In particular, the age of females at SOM and CL50 would correspond to 28–32% and 33–37%, respectively, of their total lifespan. Substantial reproductive spans have also been estimated for H. laevigatus, H. sibogae, H. gibbosus and H. reedi (King and Butler, 1985; Dailey and Ralston, 1986; Roa and Ernst, 1996). In summary, H. ensifer is an iteroparous species capable of producing thousands of small eggs (0.045 mm3 on average) per spawn, a feature consistent with its extended planktotrophic larval development (Gopala-Menon, 1972). Few deep-sea benthic carideans share these life-history traits [e.g., the Nematocarcinidae (Thatje et al., 2005) and the pandalid genera Heterocarpus and Plesionika (King and Butler, 1985; Company and Sarda , 1997; this study)], as the majority tend to produce a rather small number of large, yolky eggs per spawn, reflecting an abbreviated larval development (Bauer, 2004). For a species from the deep-sea benthos, an extended planktotrophic larval development would increase the potential for dispersal, but at the cost of subjecting the larvae to a greater environmental unpredictability (and thus higher and more variable mortality rates) than the adults, as the larvae would have to ascend to surface waters to find sufficient food for development then descend to the adult habitat as development ends (Sastry, 1983; Bauer, 2004). This life history trade-off would favor iteroparity (Stearns, 1976; Ranta et al., 2002) and an increased allocation of females to offspring number rather than size (Simons, 2006). Therefore, the repetitive production of thousands of small eggs by females of H. ensifer, and the large variability in egg size within and between females, likely reflect a dynamic bet-hedging to cope with uncertainty as to the likely habitat of the offspring (Marshall et al., 2008; Crean and Marshall, 2009). In other words, the high and variable reproductive effort of H. ensifer reflects a reproductive strategy to compensate for high larval mortality.

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Reproductive traits differ widely between populations of pandalid species (and other carideans) that have broad latitudinal distributions (e.g., Clarke, 1987; Clarke et al., 1991; Gorny et al., 1992; Wehrtmann and Lardies, 1999). This variation likely reflects a combination of phenotypic plasticity, local genetic differentiation, and maternal effects (Via et al., 1995; Marshall et al., 2008; Moran and McAlister, 2009). In populations that are also subjected to fishing pressure, reproductive traits may be further affected over the long term by the selective removal of the largest, more fecund individuals (Birkeland and Dayton, 2005). In general, H. ensifer is not subjected to fishing pressure (perhaps due to its relatively low abundance and patchy distribution) but it may be an incidental catch in current deep-sea fisheries targeting other, more valuable shrimp species that co-occur with H. ensifer over the eastern Atlantic and northern Gulf of Mexico. As there are currently no deep-sea fisheries in the SW Gulf of Mexico, the present study provides insight into the reproductive traits of a population of H. ensifer under conditions of null fishing disturbance and provides a baseline for comparative studies between different Atlantic populations of this tropical deep-water caridean.

Acknowledgements We thank the officers and crew of the R/V Justo Sierra for their skill during sampling operations over the complex topography of the study area, as well as the many graduate and undergraduate students that collaborated in the research cruises.

References Anger, K., Moreira, G.S., 1998. Morphometric and reproductive traits of tropical caridean shrimps. J. Crustac. Biol. 18, 823–838. Barradas-Ortiz, C., Briones-Fourza´n, P., Lozano-A´lvarez, E., 2003. Seasonal reproduction and feeding ecology of giant isopods Bathynomus giganteus from the continental slope of the Yucatan Peninsula. Deep Sea Res. I 50, 495–513. Bauer, R.T., 1986. Sex change and life history pattern in the shrimp Thor manningi (Decapoda: Caridea): a novel case of partial protandric hermaphroditism. Bull. Mar. Sci. 170, 11–31. Bauer, R.T., 2004. Remarkable shrimps: Adaptations and Natural History of the Carideans. University of Oklahoma Press, Norman. ¨ Biggs, D.G., Hu, C., Muller-Karger, F.E., 2008. Remotely sensed sea-surface chlorophyll and POC flux at Deep Gulf of Mexico Benthos sampling stations. Deep Sea Res. II 55, 2555–2562. Birkeland, C., Dayton, P.K., 2005. The importance in fishery management of leaving the big ones. Trends Ecol. Evol. 20, 356–358. Briones-Fourza´n, P., Lozano-A´lvarez, E., 1991. Aspects of the biology of the giant isopod, Bathynomus giganteus A. Milne-Edwards, 1879 (Flabellifera: Cirolanidae), off the Yucatan Peninsula. J. Crustac. Biol. 19, 450–458. Chace Jr., F.A., 1985. The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine Expedition, 1907–1910, Part 3: families Thalassocarididae and Pandalidae. Smithson. Contrib. Zool. 411, 1–143. Charnov, E.L., 1990. Relative size at the onset of maturity (RSOM) is an interesting number in crustacean growth (Decapoda, Pandalidae). Crustaceana 59, 108–109. Chilari, A., Thessalou-Legaki, M., Petrakis, G., 2005. Population structure and reproduction of the deep-water shrimp Plesionika martia (Decapoda: Pandalidae) from the eastern Ionian Sea. J. Crustac. Biol. 25, 233–241. Clarke, A., 1987. Temperature, latitude, and reproductive effort. Mar. Ecol. Prog. Ser. 38, 89–99. Clarke, A., 1993a. Reproductive trade-offs in caridean shrimps. Funct. Ecol. 7, 411–419. Clarke, A., 1993b. Egg size and egg composition in polar shrimps (Caridea; Decapoda). J. Exp. Mar. Biol. Ecol. 168, 189–203. Clarke, A., Hopkins, C.C.E., Nilssen, E.M., 1991. Egg size and reproductive output in the deep water prawn Pandalus borealis Krøyer, 1838. Funct. Ecol. 5, 724–730. Company, J.B., Sarda , F., 1997. Reproductive patterns and population characteristics in five deep-water pandalid shrimps in the Western Mediterranean along a depth gradient (150–1100 m). Mar. Ecol. Prog. Ser. 148, 49–58. Company, J.B., Sarda , F., Puig, P., Cartes, J.E., Palanques, A., 2003. Duration and timing of reproduction in decapod crustaceans of the NW Mediterranean continental margin: Is there a general pattern? Mar. Ecol. Prog. Ser. 261 201–216.

Correa, C., Thiel, M., 2003. Mating systems in caridean shrimps (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Rev. Chil. Hist. Nat. 76, 187–203. Crean, A.J., Marshall, D.J., 2009. Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philos. Trans. R. Soc. B 364 (1520), 1087–1096. Crosnier, A., 1988. Sur les Heterocarpus (Crustacea, Decapoda, Pandalidae) du sudouest de l’oce´an Indien. Remarques sur d’autres espe ces ouest-Pacifiques du genre et description de quatre taxa nouveaux. Bull. Mus. Natl. d’Hist. Nat. Paris, 4e Se´ries 10 (A1), 57–103. Crosnier, A., Forest, J., 1973. Les crevettes profondes de l’Atlantique oriental tropical. Faune Trop. 19, 1–409. Dailey, M.D., Ralston, S., 1986. Aspects of the reproductive biology, spatial distribution, growth, and mortality of the deep-water caridean shrimp, Heterocarpus laevigatus, in Hawaii. Fish. Bull. 84, 915–925. Escobar-Briones, E.G., Gayta´n-Caballero, A., Legendre, P., 2008. Epibenthic megacrustaceans from the continental margin, slope and abyssal plain of the Southwestern Gulf of Mexico: factors responsible for variability in species composition and diversity. Deep Sea Res. II 55, 2667–2678. Fanelli, E., Cartes, J.E., 2004. Feeding habits of pandalid shrimps in the Alboran Sea (SW Mediterranean): influence of biological and environmental factors. Mar. Ecol. Prog. Ser. 280, 227–238. Fox, C.W., Czesak, M.E., 2000. Evolutionary ecology of progeny size in arthropods. Annu. Rev. Entomol. 45, 341–369. Gopala-Menon, P., 1972. Decapod Crustacea from the International Indian Ocean expedition: the larval development of Heterocarpus (Caridea). J. Zool. 167, 371–397. Gorny, M., Arntz, W.E., Clarke, A., Gore, D.J., 1992. Reproductive biology of caridean decapods from the Weddell Sea. Polar Biol. 12, 111–120. Holthuis, L.B., 1980. FAO species catalogue 1. Shrimps and prawns of the world. An annotated catalogue of species of interest to fisheries. FAO Fish. Synop. 125 1, 1–271. Howell, D.C., 2002. Statistical Methods for Psychology, fifth ed. Duxury, Pacific Grove. Johnson, N.A., Campbell, J.W., Moore, T.S., Rex, M.A., Etter, R.J., McClain, C.R., Dowell, M.D., 2007. The relationship between the standing stock of deep-sea macrobenthos and surface production in the western North Atlantic. Deep Sea Res. I 54, 1350–1360. Kanciruk, P., Herrnkind, W.F., 1976. Autumnal reproduction in Panulirus argus at Bimini, Bahamas. Bull. Mar. Sci. 26, 417–432. King, M.G., Butler, A.J., 1985. Relationship of life-history patterns to depth in deepwater caridean shrimps (Crustacea: Natantia). Mar. Biol. 86, 129–138. King, M.G., Moffit, R.B., 1984. The sexuality of tropical deepwater shrimps (Decapoda: Pandalidae). J. Crustac. Biol. 4, 567–571. Lozano-A´lvarez, E., Briones-Fourza´n, P., Gracia, A., Va´zquez-Bader, A.R., 2007. Relative growth and size at first maturity of deep water shrimp Heterocarpus ensifer (Decapoda, Pandalidae) from the southern Gulf of Mexico. Crustaceana 80, 555–568. Marshall, D.J., Allen, R.M., Crean, A.J., 2008. The ecological and evolutionary importance of maternal effects in the sea. Oceanogr. Mar. Biol. Annu. Rev. 46, 203–250. Mauchline, J., 1988. Egg and brood sizes of oceanic pelagic crustaceans. Mar. Ecol. Prog. Ser. 43, 251–258. ¨ Melo-Gonza´lez, N., Muller-Karger, F.E., Cerdeiro-Estrada, S., Pe´rez-de los Reyes, R., Victoria-del Rı´o, I., Ca´rdenas-Pe´rez, P., Mitrani-Arenal, I., 2000. Near-surface phytoplankton distribution in the western Intra-Americas Sea: the influence of ˜ o and weather events. J. Geophys. Res. 105, 14029–14043. El Nin Merino, M., 1997. Upwelling on the Yucatan shelf: hydrographic evidence. J. Mar. Syst. 13, 101–121. Milne Edwards, A., 1881. Description de quelques crustace´s macroures provenant des grandes profondeurs de la Mer des Antilles. Ann. Sci. Nat., Zool. Ser. 6 11 (4), 1–16. Moran, A.L., McAlister, J.S., 2009. Egg size as a life history character of marine invertebrates: is it all it’s cracked up to be? Biol. Bull. 216 226–242. Oh, C.W., Byun, J.H., Choi, J.H., Kim, H.W., 2008. Reproductive biology of Pandalus gracilis Stimpson, 1860 (Decapoda, Pandalidae) in the southeastern coastal waters of Korea. Crustaceana 81, 797–811. Ohtomi, J., 1997. Reproductive biology and growth of the deep-water pandalid shrimp Plesionika semilaevis (Decapoda: Caridea). J. Crustac. Biol. 17, 81–89. Paulmier, G., Gervain, P., 1994. Pˆeches experimentales des crustace´s profonds dans les eaux de la Martinique (Pandalidae, Nephropidae): prospections, rendement et biologie des espe ces. Direction des Ressources Vivants de l’IFREMER, Rapport Interne No. 94-04, 44pp. Pauly, D., 1984. Fish population dynamics in tropical waters: a manual for use with programmable calculators. ICLARM Stud. Rev. 8, 1–325. Poulin, R., 1995. Clutch size and egg size in free-living and parasitic copepods: a comparative analysis. Evolution 49, 325–336. Poupin, J., 1994. Faune Marine Profonde des Antilles Franc-aises. ORSTOM E´ditions, Collection E´tudes et The ses, Paris, 90pp. Poupin, J., Tamarii, T., Vandenboomgaerde, A., 1990. Pˆeches profondes aux casiers sur les pentes oce´aniques des ˆıles de Polyne´sie Franc-aise (N/O Marara, 1986/ 1989). ORSTOM, Notes et Documents d’Ocea´nographie No. 42, Tahiti, 103pp. Ramı´rez-Llodra, E., 2002. Fecundity and life-history strategies in marine invertebrates. Adv. Mar. Biol. 43, 87–170. Ranta, E., Tesar, D., Kaitala, V., 2002. Environmental variability and semelparity vs. iteroparity as life histories. J. Theor. Biol. 217, 391–396.

ARTICLE IN PRESS ´n et al. / Deep-Sea Research I 57 (2010) 978–987 P. Briones-Fourza

Roa, R., Ernst, B., 1996. Age structure, annual growth, and variance of size-at-age of the shrimp Heterocarpus reedi. Mar. Ecol. Prog. Ser. 137, 59–70. Rosa, R., Calado, R., Narciso, L., Nunes, M.L., 2007. Embryogenesis of decapod crustaceans with different life history traits, feeding ecologies, and habitat: a fatty acid approach. Mar. Biol. 151, 935–947. Sastry, A.N., 1983. Ecological aspects of reproduction. In: Vernberg, F.J., Vernberg, W.B. (Eds.), The Biology of Crustacea, vol. 8. Academic Press, New York, pp. 179–270. Simons, A.M., 2006. Selection for increased allocation to offspring number under environmental unpredictability. J. Evol. Biol. 20, 813–817. Smith, C.C., Fretwell, S.D., 1974. The optimal balance between size and number of offspring. Am. Nat. 108, 499–506. Stearns, S.C., 1976. Life-history tactics: a review of the ideas. Quart. Rev. Biol. 51, 3–47. Thatje, S., Bacardit, R., Arntz, W.E., 2005. Larvae of the deep-sea Nematocarcinidae (Crustacea: Decapoda: Caridea) from the Southern ocean. Polar Biol. 28, 290–302. Thessalou-Legaki, M., 1992. Reproductive variability of Parapandalus narval (Crustacea: Decapoda) along a depth gradient. Estuar. Coast. Shelf Sci. 35, 593–603. ˜ alvo, J.A., Delgado, J., Pinho, M.A., Santana, J.I., Biscoito, M., Tuset, V.M., Pe´rez-Pen Gonza´lez, J.A., Carvalho, D., 2009. Biology of the deep-water shrimp

987

Heterocarpus ensifer (Caridea: Pandalidae) off the Canary, Madeira and the Azores islands (northeastern Atlantic). J. Crustac. Biol. 29, 507–515. Tyler, P.A., 1988. Seasonality in the deep sea. Oceanogr. Mar. Biol. Annu. Rev. 26, 227–258. Underwood, A.J., Keough, M.J., 2001. Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In: Bertness, M.D., Gaines, S.D., Hay, M.E. (Eds.), Marine Community Ecology. Sinauer, Sunderland, pp. 183–200. Via, S., Gomulkiewicz, R., de Jong, G., Scheiner, S.M., Schlichting, C.D., van Tienderen, P.H., 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10, 212–217. Wehrtmann, I.S., Andrade, G., 1998. Egg production in Heterocarpus reedi from northern Chile, with a comparison between iced and living females. Ophelia 49, 71–82. Wehrtmann, I.S., Lardies, M.A., 1999. Egg production in Austropandalus grayi (Decapoda, Caridea, Pandalidae) from the Magellan region, South America. Sci. Mar. 63 (Suppl. 1), 325–331. Wenner, A.M., 1972. Sex ratio as a function of size in marine Crustacea. Am. Nat. 106, 321–350. Wicksten, M.K., Packard, J.M., 2005. A qualitative zoogeographic analysis of decapod crustaceans of the continental slopes and abyssal plain of the Gulf of Mexico. Deep Sea Res. I 52, 1745–1765. Zar, J.H., 1999. Biostatistical Analysis fourth ed. Prentice-Hall, Upper Saddle River.