2009 Bobeand Labbe GCEonline

See discussions, stats, and author profiles for this publication at: https://www.researchgate.
net/publication/276267038
Egg and sperm quality in fish
Article in General and Comparative Endocrinology · January 2012
CITATIONS READS
474 1,556
1 author:
Catherine Labbe
French National Institute for Agriculture, Food, and Environment (INRAE)
221 PUBLICATIONS 2,617 CITATIONS
SEE PROFILE
Some of the authors of this publication are also working on these related projects:
CRIOBIV View project
Reproduction biotechnology View project
All content following this page was uploaded by Catherine Labbe on 06 January 2020.
The user has requested enhancement of the downloaded file.

YGCEN 10331 No. of Pages 14, Model 5G
11 March 2009 Disk Used
ARTICLE IN PRESS
General and Comparative Endocrinology xxx (2009) xxx–xxx

1
Contents lists available at ScienceDirect
General and Comparative Endocrinology

journal homepage: www.elsevier.com/locate/ygcen
2 Egg and sperm quality in fish
F
3 Julien Bobe *, Catherine Labbé
OO
4 INRA, UR1037 SCRIBE, IFR140, Ouest-Genopole, F-35000 Rennes, France
5
a r t i c l e i n f o a b s t r a c t
7
2 1
8 Article history: Fish egg quality can be defined as the ability of the egg to be fertilized and subsequently develop into a 22
PR
9 Received 23 October 2008 normal embryo. Similarly, sperm quality can be defined as its ability to successfully fertilize an egg and 23
10 Revised 16 February 2009 subsequently allow the development of a normal embryo. In the wild or under aquaculture conditions, 24
11 Accepted 20 February 2009
the quality of fish gametes can be highly variable and is under the influence of a significant number of 25
12 Available online xxxx
external factors or broodstock management practices. For these reasons, the topic of gamete quality 26
has received increasing attention. Despite the significant efforts made towards a better understanding 27
13 Keywords:
of the factors involved in the control of gamete quality, the picture is far from being complete and the 28
14 Gamete
15 Teleost
control of gamete quality remains an issue in the aquaculture industry. Some of the factors responsible
D 29
16 Aquaculture for the observed variability of gamete quality remain largely unknown or poorly understood. In addition 30
17 Developmental competence very little is known about the cellular and molecular mechanisms involved in the control of egg and 31
18 Oocyte sperm quality. In the present review, the molecular and cellular characteristics of fish gametes are pre- 32
TE
19 Environment sented with a special interest for the mechanisms that could participate in the regulation of gamete qual- 33
20 ity. Then, after defining egg and sperm quality, and how can it can be accurately estimated or predicted, 34
we provide an overview of the main factors that can impact gamete quality in teleosts. 35
Ó 2009 Published by Elsevier Inc. 36
EC
37
38
39 1. Introduction The present review is therefore aiming at (i) briefly presenting 60

the molecular and cellular characteristics of fish gametes with spe- 61
40 The control of reproduction is a key issue in aquaculture and cial attention paid to the molecular actors that could play a key 62
RR
41 one of the limiting factors of the reproductive success is the quality role in the regulation of gamete quality, (ii) defining what is egg 63
42 of male and female gametes. Gamete quality in the wild, or in cap- and sperm quality and how can it can be accurately estimated or 64
43 tivity, is influenced by many factors and is sometimes highly vari- predicted, and (iii) providing an up to date review of the factors 65
44 able. For this reason, gamete quality has received increasing that can impact gamete quality in teleosts. 66
45 attention and many studies have characterized the effect of specific
factors on egg or sperm quality. The issue of fish egg (Kjörsvik et al.,
CO
46 2. Molecular and cellular characteristics of fish gametes 67

47 1990; Brooks et al., 1997) and sperm (Billard et al., 1995) quality
48 has previously been reviewed. Yet, the picture of the factors that 2.1. Egg 68
49 can significantly affect gamete quality remains incomplete. The
50 relative effects of each factor on gamete quality can be highly var- The unfertilized egg or female gamete is an oocyte arrested 69
51 iable and are not always well characterized. In addition, the defini- in metaphase of the second meiotic division. This metaphase 2 70
UN
52 tion of gamete quality is not always consistent among existing oocyte is the final product of the oogenetic process that oc- 71
53 studies and several types of indicators have been used to assess curred within the ovary throughout oogenesis (Tata, 1986). 72
54 gamete quality. Finally, the knowledge of the role of some intracel- As a consequence, the coordinated assembly of the egg can 73
55 lular gamete components on the quality of the gamete has bene- last for a very long time, up to several years in some species. 74
56 fited from recent studies, including genomic-based investigations Hence, the incorporation, synthesis, and processing of egg com- 75
57 that have provided new hints on the long-term process of under- ponents that occur during oogenesis play a key role in the 76
58 standing what is and what makes a good egg and a good coordinated assembly of a good quality oocyte that will, once 77
59 spermatozoon. fertilized, develop into a normal embryo. The main characteris- 78
tics of egg assembly, including the increase in egg volume 79
resulting from massive incorporation of yolk proteins during 80
vitellogenesis have been extensively studied and previously re- 81
* Corresponding author. Address: Fish Reproduction Group, INRA SCRIBE UR1037,
Campus de Beaulieu, 35042 Rennes Cedex, France. Fax: +33 2 23 48 50 20. viewed (Wallace and Selman, 1981, 1985; Brooks et al., 1997; 82
E-mail address: Julien.Bobe@rennes.inra.fr (J. Bobe). Patino and Sullivan, 2002; Mommsen and Korsgaard, 2008) 83
0016-6480/$ - see front matter Ó 2009 Published by Elsevier Inc.

doi:10.1016/j.ygcen.2009.02.011
Please cite this article in press as: Bobe, J., Labbé, C. Egg and sperm quality in fish. Gen. Comp. Endocrinol. (2009), doi:10.1016/j.ygcen.2009.02.011
ARTICLE IN PRESS
2 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx
84 (see also the oogenesis review in this issue). Besides yolk pro- 2.2. Sperm 150
85 teins, the ovulated oocyte (unfertilized egg) contains many
86 other components such as maternal mRNAs, proteins, vitamins 2.2.1. Sperm membrane characteristics 151
87 and hormones. To date, our knowledge of the hormonal con- The plasma membrane of the spermatozoa head tightly overlays 152
88 tent of unfertilized eggs is limited. Several studies reported the nucleus and only a thin cytoplasmic layer remains between the 153
89 the presence of thyroid hormones (Tagawa and Hirano, 1987), plasma membrane and the nucleus. At the midpiece level, some 154
90 cortisol (Hwang et al., 1992) and several sex steroids (Feist folding of the plasma membrane along the axoneme root results 155
91 et al., 1990). Despite several studies aiming at manipulating in the superposition of membrane layers. In some species, includ- 156
92 the hormonal content of the egg, the function of the hormonal ing Salmonidae and Percidae, the plasma membrane surrounding 157
93 egg content remains poorly investigated to date. Maternally- the axoneme presents paired lateral extensions resembling a heli- 158
94 inherited mRNAs and proteins accumulate in the oocyte coid fin all along the tail. Such lateral ribbons are not observed in 159
95 throughout oogenesis (Tata, 1986; Howley and Ho, 2000; Pele- Labridae, for example, whereas in Sparidae, 2, 1 or no lateral rib- 160
F
96 gri, 2003). After fertilization, those maternal factors support bons are reported, depending on the species (reviewed by Lahnste- 161
97 early embryonic development until activation of zygotic tran- iner and Patzner, 2008). 162
OO
98 scription and thus play a pivotal role during early embryogen- The spermatozoa plasma membrane plays a major role in motil- 163
99 esis. The initiation of zygotic transcription occurs during the ity activation. The sensing of ionic changes, responsible for the ini- 164
100 ‘‘maternal-embryo transition” (MET). In fish, as in other lower tiation of flagellar beating upon sperm release in water, (see 165
101 vertebrates, MET occurs at the mid-blastula stage and is also Section 2.2.5.) takes place across this membrane. Many ion chan- 166
102 known as ‘‘mid-blastula transition” (MBT) (Kane and Kimmel, nels are described in fish sperm plasma membrane and progestin 167
103 1993). In rainbow trout (Oncorhynchus mykiss), inhibition of receptors involved in motility were characterized in seatrout 168
PR
104 maternal mRNA translation using cycloheximide resulted in de- (Cynoscion nebulosus) (Tubbs and Thomas, 2008). As spermatozoa 169
105 layed embryonic cleavage (Nagler, 2000). In addition, the func- do not bear an acrosome in teleosts, sperm plasma membrane is 170
106 tion of maternal factors in the developing embryo depends on also a key component of gamete fusion, and some components 171
107 a precise plan of storage and localization in the oocyte that is were described in rainbow trout: GM3, a ganglioside localized in 172
108 initiated during oogenesis. Recent molecular analyses using the sperm head, was shown to be involved in sperm binding to 173
109 newly available genomic tools have shown that some maternal D eggs (Yu et al., 2002). Some uncharacterized proteins localized in 174
110 mRNAs exhibited a differential abundance in eggs of varying the head region were also shown to be involved in fertilization 175
111 quality (Aegerter et al., 2005; Bonnet et al., 2007b). The nature (Beck et al., 1992). At the biophysical level, membrane lipids will 176
112 and abundance of maternal mRNAs stored in the eggs thus ap- determine membrane fluidity whereas both proteins and lipids 177
TE
113 pears to be important to ensure a full developmental compe- will contribute to the overall permeability to water and ions. Lipids 178
114 tence of the oocyte. Similarly, the spatial distribution of in rainbow trout sperm plasma membrane were extensively stud- 179
115 specific maternal mRNAs within the oocyte (e.g. animal pole) ied (Muller et al., 1994; Labbe et al., 1995; Pustowka et al., 2000; 180
116 is important to specify the dorso/ventral axis of the embryo Muller et al., 2008). The molar cholesterol to phospholipid ratio 181
117 (Bally-Cuif et al., 1998; Howley and Ho, 2000). It was also ranges between 0.4 and 0.6. Among phospholipid classes, phospha- 182
EC
118 shown in zebrafish that the micro RNA miR-430 could acceler- tidyl choline represents 50% of the total phospholipids, with a 183
119 ate the deadenylation of target mRNAs, including numerous localization in the outer leaflet, whereas phosphatidyl serine 184
120 maternal mRNAs thus suggesting its participation in maternal (10%) and phosphatidyl ethanolamine (30%) are enriched in the in- 185
121 mRNA clearance during embryogenesis (Giraldez et al., 2006). ner leaflet. The polyunsaturated fatty acid 22:6n 3 is well repre- 186
122 These recent studies have provided new hints on the molecular sented (more than 10% of the total fatty acids), leading to an 187
RR
123 mechanisms involved in the regulation of egg quality in fish. unsaturated to saturated ratio as high as 1.30. From the low plasma 188
124 For instance, a sharp decrease in the mRNA levels of nucleo- membrane permeability to water assessed in Labbe and Maisse 189
125 plasmin (npm2) is observed during egg post-ovulatory ageing (2001), it can be extrapolated that rainbow trout spermatozoa do 190
126 in rainbow trout (Oncorhynchys mykiss), a period when egg not possess aquaporins which would facilitate water penetration. 191
127 quality progressively decreases (Aegerter et al., 2005). Interest-
128 ingly, nucleoplasmin is a maternal-effect gene critical for nu- 2.2.2. Cytoskeleton 192
CO
129 clear and nucleolar organization and embryonic development Most studies on sperm cytoskeleton are focused on the flagellar 193
130 (McLay and Clarke, 2003; Burns et al., 2003). Similarly, a dif- axoneme. In most fish species, the axoneme bears the typical 194
131 ferential abundance of prohibitin 2 (phb2) mRNA was observed arrangement of nine pairs of peripheral microtubules and one pair 195
132 betweens eggs of varying quality in rainbow trout (Bonnet of central microtubules, although some species do not possess the 196
133 et al., 2007b). Phb2 is a highly conserved protein originally central microtubules such as the eel (Anguilla anguilla) (Gibbons 197
UN
134 know as a chaperone protein also involved in a broad range et al., 1983). Each microtubule is organized into a cylinder whose 198
135 of cellular functions (Mishra et al., 2006). In addition to mater- walls are made by 13 adhering protofilaments, the later being com- 199
136 nal mRNAs, the ovulated oocyte also contains proteins that posed of polymerized tubulin dimeres. The sliding of one doublet 200
137 have been synthesized during oogenesis. Recently, proteomic from the adjacent doublet is mediated by inner and outer rows 201
138 analysis of the developing oocyte has led to the identification of dynein arms acting as force-generating ATPases with rotating 202
139 of protein in the full-grown zebrafish (Danio rerio) and sea arms. When the dynein arms attached to a given microtubule dou- 203
140 bream (Sparus aurata) oocyte (Knoll-Gellida et al., 2006; Ziv blet undergo an ATP-dependent binding–bending–unbinding to 204
141 et al., 2008). These studies have shed light on the protein rep- the adjacent microtubule doublet, the resulting sliding-induced 205
142 ertoire of the unfertilized egg. However, the contribution of tension initiates flagellar curvature. This sequence is proposed to 206
143 identified proteins in the regulation of egg quality requires fur- be the basic step towards flagellar beating (see the extensive 207
144 ther investigation. Very recently, a protein differentially ex- description by Cosson, 2008a). Actin is also found closely associ- 208
145 pressed in European sea bass (Dicentrarchus labrax) eggs of ated to the plasma membrane. 209
146 poor and high quality was identified (Crespel et al., 2008). Fur-
147 ther investigations are now required to functionally character- 2.2.3. Nucleus 210
148 ize the participation of this candidate protein in the Sperm nucleus organization is very different depending on fish 211
149 regulation of fish egg quality. species. Most nuclei show an invagination in which the axoneme 212
ARTICLE IN PRESS
J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 3
213 will be anchored. As a consequence, nucleus shape will determine et al., 1997; Inaba et al., 1993). How the whole network will ulti- 278
214 the strength of flagellar attachment to the head. In rainbow trout mately lead to microtubule sliding and movement initiation is still 279
215 (Billard, 1983) and in other Salmonidae, the elongated nucleus pre- under investigation. 280
216 sents an invagination whose depth is about one third of the nu-
217 cleus length. In other species, this invagination can reach more 2.2.5. Sperm energetics 281
218 than two third of the nuclear length (Sweetfish (Plecoglossus altiv- Spermatozoa energy metabolism provides for the basal energy 282
219 elis) (Ohta et al., 1993); red mullet (Mullus barbatus) (Lahnsteiner demand in quiescent conditions (storage in the male ducts, in vitro 283
220 and Patzner, 1998)) or it can be only a minor depression as in loach storage) and for the high energy demand upon motility activation 284
221 (Misgurnus anguillicaudatus) and goldfish (Carassius auratus) (Ohta (reviewed by Ingermann, 2008). Spermatozoa capacity to metabo- 285
222 et al., 1993). lize exogenous and/or endogenous substrates will mostly depend 286
223 Nuclear proteins in fish sperm will also vary according to the on the fish reproductive strategy. Spermatozoa from species under- 287
224 species. As an example, sea bass (Dicentrarchus labrax) and North- going internal fertilization will be able to metabolize extracellular 288
F
225 ern pike Esox lucius nuclei contain only protamines whereas striped substrate, a feature similar to that found in mammals and birds. 289
226 red mullet (Mullus surmuletus), carps (Cyprinus carpio, Ctenophar- One reason is that some substrates can be found in the female fluid 290
OO
227 yngodon idella), goldfish and sea bream (Sparus aurata) nuclei con- in which spermatozoa are released. This is true for Guppy (Poecilia 291
228 tain only histones (Munoz-Guerra et al., 1982; Saperas et al., reticulata) and Surfperch (Cymatogaster aggregata) spermatozoa 292
229 1993a, 1993b), and rainbow trout nuclei contain both protamines where glycolysis in the presence of extracellular glucose was dem- 293
230 and histones (Avramova et al., 1983; Christensen et al., 1984). It onstrated (Gardiner, 1978). On the contrary, spermatozoa from spe- 294
231 is accepted that nucleus protein types will determine the extent cies undergoing external fertilization cannot rely on the medium to 295
232 of chromatin condensation. Chromatin condensation in turn is provide for their energy supply. This may explain why these cells 296
PR
233 known to enhance DNA resistance to chemically or mechanically- present a poorer ability to metabolize extracellular substrate. In 297
234 induced damages. It is likely that species differences observed in rainbow trout spermatozoa, no extra cellular glucose metabolism 298
235 sperm DNA stability are linked to species differences in chromatin was detected (Terner, 1962). However, this poor affinity for glucose 299
236 organization, although this issue has not been extensively studied can be compensated for by a more efficient tricarboxylic acid incor- 300
237 in fish spermatozoa. poration, as demonstrated in several species with extracellular pyru- 301
vate, lactate or glyoxylate (Terner and Korsh, 1963a, 1963b; Mounib, 302
238
239
2.2.4. Mechanism responsible for the initiation of sperm motility
In Salmonidae, motility of testicular spermatozoa cannot be
D 1967). Spermatozoa inability to metabolize extracellular glucose is
proposed to be due to a poor membrane permeability to glucose
303
304
240 activated (Morisawa and Morisawa, 1986) whereas during sperma- (Gardiner, 1978) rather than to some deficiency in glucolysis en- 305
TE
241 tozoa migration down the sperm ducts, spermatozoa acquire the zymes, as enzymatic capacity for intracellular glycolysis was dem- 306
242 potential for motility activation (Morisawa et al., 1993; Koldras onstrated in Salmonidae and Cyprinidae (Lahnsteiner et al., 1992, 307
243 et al., 1996). This maturation was shown to be caused by the semen 1993). Upon motility activation when spermatozoa are released in 308
244 pH increase (Morisawa and Morisawa, 1988), leading to an in- water, spermatozoa face a huge energy demand to induce and sus- 309
245 crease in intracellular AMPc (Miura et al., 1992; Morisawa et al., tain flagellar movement. Adenylate cyclase will mediate cAMP in- 310
EC
246 1993). This maturation event was poorly investigated in other spe- crease at the onset of motility activation and dynein ATPase 311
247 cies, but it is often admitted that storage of testicular spermatozoa activity will allow axonemal microtubules sliding during move- 312
248 in a buffer, at or above pH 8, favours the sperm’s ability to respond ment. These processes are greatly responsible for the rapid ATP con- 313
249 to the motility initiation signal. sumption described in most species such as rainbow trout (Christen 314
250 When mature spermatozoa are released in the external med- et al., 1987), common carp (Cyprinus carpio) (Perchec et al., 1995), sea 315
RR
251 ium, extracellular ionic changes induce motility activation (re- bass, and turbot (Scophthalmus maximus) (Dreanno et al., 1999a, 316
252 viewed by Morisawa, 1994). In most species, difference in 1999b, 2000). ATP stores accumulated in quiescent spermatozoa 317
253 osmolality between seminal plasma and water is the main trigger are the most readily available energy supply for sustaining motility 318
254 of sperm motility. In Salmonidae however, the decrease in extra- after activation (see the recent review by Ingermann, 2008), espe- 319
255 cellular K+ is the sperm motility activator (Morisawa and Suzuki, cially in species whose sperm mitochondria present a low basal 320
256 1980). Some egg factors can also stimulate motility hyper activa- capacity for oxidative phosphorylation, such as in Salmonidae. 321
CO
257 tion as shown in herring (Clupea palasii) (Morisawa et al., 1992; Maintenance of ATP level during motility can also be provided by 322
258 Oda et al., 1998). The molecular events making a link between io- creatine phosphate (Robitaille et al., 1987; Dreanno et al., 1999b) 323
259 nic changes and motility initiation were recently reviewed by Ina- and to some extent by monosaccharides as shown by Lahnsteiner 324
260 ba (2008). The cascade was especially well studied in Salmonidae, et al. (1992) in the chub (Leuciscus cephalus). 325
261 but also in Cyprinidae. Dilution of external K+ induces intracellular At the morphological level, the number of mitochondria is var- 326
K+ efflux and intracellular Ca2+ increase. This triggers membrane
UN
262 iable depending on the species. Salmonidae spermatozoa possess a 327

263 hyperpolarization. Adenylate cyclase activation, and cAMP in- single ring-shaped mitochondria, resulting from the fusion of sev- 328
264 crease were reported in Salmonidae, but not in Cyprinidae (Krasz- eral mitochondria, whereas Blenniidae and Labridae have up to 6 329
265 nai et al., 2000). All these events have been demonstrated to be mitochondria (see the very well documented review of Lahnsteiner 330
266 involved in motility activation (Morisawa and Okuno, 1982; Mor- and Patzner (2008)). However, as reported by Lahnsteiner and 331
267 isawa and Ishida, 1987; Boitano and Omoto, 1992; Kho et al., Patzner (2008) no relationship between the number or arrange- 332
268 2001). Again, the link between cAMP increase and motility initia- ment of mitochondria and functional differences in energetic 333
269 tion at the axoneme level was mainly investigated in Salmonidae. capacity of the spermatozoa could be highlighted in interspecies 334
270 Such a link involves a complex phosphorylation/dephosphoryla- comparisons. 335
271 tion sequence whose actors have been only partially characterized
272 so far. This includes the cAMP-dependant phosphorylation of the 3. What is egg/sperm quality and how can it be estimated or 336
273 15 kDa MIPP (movement-initiating phosphoprotein, (Morisawa predicted? 337
274 and Hayashi, 1985; Hayashi et al., 1987; Jin et al., 1994a, 1994b),
275 of the PKA (Itoh et al., 2003), and of the 22 kDa dynein light chain From a biological standpoint, the quality of a gamete can be de- 338
276 (Inaba et al., 1998, 1999). Regulation of protein phosphorylation by fined as its ability to fertilize or to be fertilized, and subsequently 339
277 proteasomes was also demonstrated (Inaba et al., 1998; Ohkawa develop into a normal embryo. However, the quality of gametes 340
ARTICLE IN PRESS
341 can also be defined differently depending on the specific biotech- 3.1.2. Sperm 405
342 nological applications that the gametes are to be used for, such as 3.1.2.1. Sperm motility. Apart from fertilization ability, sperm 406
343 cryobanking, nuclear transfer or androgenesis. Several types of crite- motility is an integrative quality parameter which will combine 407
344 ria can thus be used to quantitatively estimate egg and sperm qual- the quality of several cellular compartments responsible for motil- 408
345 ity; some of them being species-specific or application-specific. In ity activation and progressive movement sustaining. Among these, 409
346 the present chapter we will review the biologically relevant and bio- plasma membrane mediates the ionic motility activation signal 410
347 technologically relevant parameters that can be used to estimate and maintains the permeability barrier in order to prevent leakage 411
348 gamete quality. We will also discuss criteria that can be used, for in- of important intracellular components. Mitochondria activity re- 412
349 stance in aquaculture, to tentatively predict egg and sperm quality. sults in adequate energy stores, and axoneme structure and com- 413
position is responsible for the efficiency of spermatozoa 414
350 3.1. Quality estimators prior to fertilization movement. Motility analysis is very useful to compare different 415
experimental conditions such as collecting procedures, sperm dilu- 416
F
351 3.1.1. Egg tion medium, and sperm storage conditions. Sperm motility is also 417
352 The size and appearance of unfertilized eggs can tentatively be extensively used to assess the effect of biotechnologies such as 418
OO
353 used to evaluate or estimate the overall developmental potential of cryopreservation. Methods used to analyze fish sperm motility 419
354 the eggs after fertilization. For instance, the size of the egg was were recently reviewed by Cosson (2008b) and the reader is re- 420
355 sometimes considered to be beneficial for the future development ferred to this detailed book chapter for a comprehensive descrip- 421
356 of the embryo, especially in ecological studies. However, despite tion of the important steps in the determination of sperm 422
357 the large variations in egg weight that can be observed in fish with- motility. The simplest method for a rapid screening of sperm qual- 423
358 in the same species, very little data can support this hypothesis. In ity is the direct observation of the percentage of motile spermato- 424
PR
359 rainbow trout for instance, it was shown that under normal condi- zoa with a phase contrast or a dark field microscope using low 425
360 tions of temperature, post-ovulatory ageing, and husbandry prac- magnification (10 to 20 lenses). One possible source of discrep- 426
361 tices, small eggs produce similar rates of fertilization than larger ancies in this kind of analysis arises from sperm density during 427
362 ones (Bromage et al., 1992). observation. Too many or too few cells in the microscope field will 428
363 The appearance or morphology of unfertilized eggs has also lead to respectively overestimating or underestimating the motil- 429
364 sometimes been used to estimate the developmental potential of D ity percentage. Another source of underestimation lies in the stick- 430
365 the egg. In brown trout (Salmo trutta) females caught in the wild ing of the spermatozoa to the glass slide, and this can be easily 431
366 and transferred to an aquaculture facility, the distribution of lipid prevented by adding proteins (such as BSA) to the activating med- 432
367 droplets in the unfertilized eggs was shown to be reflective of em- ium. In all, this simple motility assessment is reliable for analysis of 433
TE
368 bryo survival at the eyed stage (Mansour et al., 2007). However, the sperm motility duration and that of global sperm motility capacity. 434
369 use of such estimators is limited under normal hatchery conditions In computer-assisted sperm analysis (CASA) (Kime et al., 1996; 435
370 and the lack of a consistent relationship between the distribution Rurangwa et al., 2001), video recording of the sperm movement 436
371 of lipid droplets and egg quality in hatchery-raised rainbow trout and analysis of several movement parameters will allow sperm 437
372 was recently stressed (Ciereszko et al., in press). Indeed, while ma- morphology to be assessed, together with sperm velocity, head 438
EC
373 jor morphological changes can routinely be observed in specific movement and overall percentage of motile sperm. Such analyses 439
374 cases, such as excessive post-ovulatory ageing times, significant produce a great deal of data, which is often difficult to correlate 440
375 differences in egg quality are also observed that can not be linked to specific sperm function. The method is however very useful in 441
376 to simple morphological criteria. comparing samples, especially using the clustering analysis devel- 442
377 Egg quality can also tentatively be predicted using indirect mea- oped by Martinez-Pastor et al. (2008) where changes in sperm 443
RR
378 surements such as physico-chemical parameters of ovarian or coe- cluster distribution within ejaculates are analyzed. Stroboscopic 444
379 lomic fluid in which the eggs are bathed. Several studies have analysis of flagellar beating using dark field microscope and higher 445
380 shown that low pH values of coelomic or ovarian fluid have been magnification lenses (Cosson et al., 1985) allowed for the explora- 446
381 associated with reduced egg quality. In turbot (Scophtalmus maxi- tion of the finest events along the axoneme (see the recent reviews 447
382 mus), the drop of egg quality during egg post-ovulatory ageing is of Cosson, 2008a, 2008b) together with the pattern of flagellar beat 448
383 associated with a drop of ovarian fluid pH (Fauvel et al., 1993). frequency over motility duration. However, incase some cellular 449
CO
384 Similar observations were made in rainbow trout (Lahnsteiner, defects should take place, parameters other than motility will have 450
385 2000; Aegerter and Jalabert, 2004). Indeed, proteomic analyses to be explored in order to describe more precisely the affected cel- 451
386 have shown that vitellogenin fragments originating from the eggs lular functions. 452
387 accumulate in coelomic fluid during post-ovulatory ageing (Rime
388 et al., 2004). The drop in coelomic fluid pH during post-ovulatory 3.1.2.2. Other estimators. Other sperm quality estimators are often 453
UN
389 ageing could therefore be induced by the presence of egg content based on morphological, biochemical and subcellular analyses. At 454
390 in the fluid. It was indeed shown in rainbow trout that broken eggs the subcellular level, plasma membrane quality is one estimator 455
391 could decrease the pH of coelomic fluid (Dietrich et al., 2007). It is of sperm quality. Plasma membrane integrity can be analyzed indi- 456
392 however noteworthy that the pH variation range during the post- rectly by the assessment of cytoplasmic components (enzymes, 457
393 ovulatory ageing process is limited (Lahnsteiner, 2000; Aegerter metabolites) whose release into the seminal fluid will reflect some 458
394 and Jalabert, 2004). In addition, no significant linear regression be- alteration in the membrane permeability barrier (Ciereszko and 459
395 tween pH and embryonic survival could be identified (Aegerter and Dabrowski, 1994; Zilli et al., 2004). One more direct measurement 460
396 Jalabert, 2004). In turbot, however, ovarian pH was correlated with of plasma membrane quality is based on the measurement of plas- 461
397 the fertilization rate but not with survival rate at the 4-cell stage. ma membrane impermeability to hydrophilic dyes. When the plas- 462
398 Taken together these observations suggest that egg quality can ma membrane is altered, these dyes, such as propidium iodide (PI) 463
399 not be accurately predicted using ovarian or coelomic fluid pH, or ethidium homodimer, will enter the cell and label the nucleus 464
400 especially when low egg quality is not induced by post-ovulatory DNA. The percentage of cells with a labeled nucleus (altered plas- 465
401 ageing or when other factors are involved (e.g. temperature) ma membrane) can be assessed by a flow cytometric analysis of 466
402 (Aegerter and Jalabert, 2004). In contrast, low pH could be useful the sperm population (Ogier de Baulny et al., 1997, 1999). Another 467
403 to estimate post-ovulatory ageing, especially in some species such plasma membrane quality test is based on membrane resistance to 468
404 as the turbot (Fauvel et al., 1993). osmotic shock (Marian et al., 1993). This test indistinctly reflects 469
ARTICLE IN PRESS
470 plasma membrane mechanical resistance to stretching upon water not be used as substitute estimators of sperm fertilization ability, 520
471 entry and plasma membrane permeability to water. In this test, but as partial descriptors of this ability. 521
472 exposure of spermatozoa to a hypo-osmotic media will induce
473 plasma membrane swelling and ultimately PI penetration. This 3.2. Fertilization success and early estimators 522
474 estimator was used to study the effect of broodstock rearing salin-
475 ity (Labbe and Maisse, 2001), or that of changes in plasma mem- Fertilization success is probably one of the earliest estimators 523
476 brane cholesterol content (Muller et al., 2008). that can be recorded to accurately estimate egg quality and it is 524
477 At the biochemical level, energy metabolism is also used as a the most integrative estimator of sperm quality. Indeed, the ability 525
478 sperm quality estimator. Most studies explored nucleotide concen- to fertilize or be fertilized is one of the key components of gamete 526
479 tration (ATP-ADP-AMPc, creatine phosphate (Geffen and Frayer, quality. In some species, recording of fertilization rates is relatively 527
480 1993; Saudrais et al., 1998; Zietara et al., 2004; Zilli et al., 2004), easy. This is especially true for species with transparent eggs such 528
481 and respiration activity (Lahnsteiner et al., 1998). Presence of ac- as cod (Gadus morua), turbot and yellowtail flounder (Limanda fer- 529
F
482 tive mitochondria was also measured on live spermatozoa with ruginea). This is, in contrast, much more difficult in fish species 530
483 fluorescent labeling of the negatively charged mitochondria and with opaque eggs. In rainbow trout for instance, it is necessary to 531
OO
484 cell sorting analysis (Ogier de Baulny et al., 1995, 1997). fix the egg and subsequently stain it with specific dyes (Fig. 1). 532
485 Quality of the nucleus DNA is increasingly explored with re- In the past, many studies have used the term ‘‘fertilization rate” 533
486 gards to the risk raised by sperm handling or sperm exposure to in an improper manner as it corresponded in fact to embryonic sur- 534
487 damaging chemical agents (Labbe and Maisse, 2001; Zilli et al., vival at much later stages. This is especially true in sperm studies 535
488 2003; Ciereszko et al., 2005). Comet assay is the most commonly where sperm fertilizing ability is assessed by the percentage of 536
489 used method to assess DNA stability in fish. This method is based developing embryos recorded at the easiest rather than at the ear- 537
PR
490 on the ability of damaged DNA strands to migrate faster than intact liest developmental stage. Thus, the fertilization rate is a good esti- 538
491 DNA in an acidic electrophoresis gel, leading to the occurrence of a mator of early developmental success but, depending on the 539
492 comet-like tail preceding the nucleus DNA bulk. Therefore, the species, not necessarily easy to monitor. 540
493 more DNA that is damaged, the bigger the comet tail is whereas It is also obvious that fertilization success is not necessarily 541
494 nuclei with an intact DNA show a homogenous round shape (Labbe reflective of further developmental success, as shown in several 542
495 et al., 2001). marine species (Shields et al., 1997). After fertilization, the embry- 543
496
497
It should however be stressed that whatever the sperm quality
parameter, it is often very difficult to correlate sperm grading in a
D onic cell starts to divide. The shape of the first embryonic cells and
the occurrence of abnormal cell division patterns have also been
544
545
498 quality test to the fertilization rate obtained with the same sperm. used as quality estimators in species with transparent eggs. In yel- 546
TE
499 One reason lies in the fact that fertilization of one egg requires only low tail flounder, abnormal cleavage resulted in early embryonic 547
500 one good spermatozoon taken from a huge sperm population. In- mortalities (Avery and Brown, 2005). It was also shown that blas- 548
501 deed, 200–2000 eggs are often fertilized with a suspension of tomere morphology was correlated with developmental success at 549
502 104–1010 spermatozoa. Sperm quality estimators give a picture of later stages (Shields et al., 1997; Kjørsvik et al., 2003). In Atlantic 550
503 the whole sperm population in which the weight of few spermato- cod, a recent study showed that abnormally cleaving embryos 551
EC
504 zoa is virtually detectable. As a consequence, improving the quality had significantly higher mortality than normal embryos. However, 552
505 of a small fraction of the sperm population will be sufficient to sig- both normal and abnormal eggs had similar mortality-rate trends 553
506 nificantly improve the fertilization success, although such and hatching success was not significantly different between nor- 554
507 improvement may not be detectable when assessing quality esti- mal and abnormal eggs. Together, these results indicate that an 555
508 mators such as sperm motility or membrane quality. Another rea- abnormal cleavage pattern does not necessarily result in embry- 556
RR
509 son is that sperm fertilizing ability depends upon many cellular onic failure (Avery et al., in press). Finally the buoyancy of pelagic 557
510 functions. It is therefore difficult to determine which combination eggs is often better for eggs able to develop normally as shown in 558
511 of estimators can faithfully integrate the weight of every required the red sea bream (Pagrus major) (Sakai et al., 1985) and other spe- 559
512 cellular parameter. However, this lack of correlation between the cies (Kjörsvik et al., 1990) even though this does not hold true for 560
513 fertilization rate and quality estimators should not conceal the all species (Brooks et al., 1997). 561
514 importance of sperm quality analyses. Quality estimators focus
CO
515 on specific cellular functions whose improvement can thereby be 3.3. Embryonic survival at several key steps 562
516 experimentally and individually investigated. This should ulti-
517 mately increase the size of the sperm population in which all the Embryonic survival at a specific embryonic step is one of the 563
518 requirements for sperm fertilization are met (Lahnsteiner et al., most common ways of characterizing the ability of the fertilized 564
519 1998; Zilli et al., 2004). To conclude, in vitro parameters should egg to successfully develop. Survival can thus be assessed at spe- 565
UN
Fig. 1. Normal (A) and abnormal (B) early embryonic cleavage in rainbow trout (Oncorhynchus mykiss).
ARTICLE IN PRESS
566 cific stages such as the eyed stage, hatching, and yolk-sac resorp- instance, suboptimal levels of vitamin E resulted in reduced larval 626
567 tion stage, which can be monitored in most fish species. It is also survival and increased developmental abnormalities (reviewed in 627
568 noteworthy that monitoring survival at successive developmental Izquierdo et al., 2001). The detrimental effect of a diet with insuf- 628
569 steps can be extremely valuable to characterize the timing of ficient amounts of vitamin A and E has been recently reviewed 629
570 embryonic mortalities that can significantly differ between differ- (Palace and Werner, 2006) and will not be discussed further here. 630
571 ent experimental treatments (e.g. broodstock breeding conditions, It seems however well accepted that vitamin A is important for 631
572 effect of sperm cryopreservation) (Kopeika et al., 2003; Bonnet embryo and larval development (Izquierdo et al., 2001; Palace 632
573 et al., 2007a). and Werner, 2006). Similarly, suboptimal levels of ascorbic acid 633
in the diet can lead to low embryonic survival at the eyed stage 634
574 3.4. Embryonic malformations in rainbow trout (Blom and Dabrowski, 1995). In contrast, experi- 635
mental data on the effect of the carotenoid content of broodstock 636
575 The occurrence of embryonic or larval malformations is a valu- diet on egg quality are controversial (Izquierdo et al., 2001) and 637
F
576 able tool to fully characterize the developmental potential of fertil- will not be further discussed here. Finally, essential fatty acids 638
577 ized eggs. In rainbow trout, it was shown that specific breeding are also required to ensure normal embryonic and larval develop- 639
OO
578 conditions of brood fish induce specific or predominant types of ment and deficiencies or unbalanced diets generally result in re- 640
579 malformations in the offspring (Bonnet et al., 2007a). For instance, duced egg viability, low embryonic survival, and embryonic 641
580 long-term post-ovulatory ageing of the eggs has been associated malformations (Leray et al., 1985; Izquierdo et al., 2001). 642
581 with a high occurrence of the ‘‘cyclop” malformation (Aegerter In summary, it seems clear that major food restriction or long- 643
582 et al., 2004; Bonnet et al., 2007a). Larval malformation can also re- term deficiencies in essential components, such as vitamins or 644
583 veal sperm damage, especially after cryopreservation, as shown by essential fatty acids, will impair broodfish fecundity, egg quality 645
PR
584 Horvath and Urbanyi (2000) in African catfish (Clarias gariepinus). and embryo development. However, some of the studies aiming 646
585 Such an effect was however not shown in the rainbow trout (Labbe at characterizing the effect of broodstock nutrition on egg quality 647
586 et al., 2001). One explanation is that some species may have more have been conducted in species for which nutritional requirements 648
587 resistant DNA than others. It is also likely that, in many cases, were not fully characterized, thus leading to reproductive perfor- 649
588 sperm DNA defects were repaired after fertilization by the egg re- mances lower than what had been reported using natural diets. 650
589 pair system, as demonstrated by Kopeika et al. (2004) in the loach D This is especially true for newly domesticated species, or for spe- 651
590 (Misgurnus fossilis). cies that require specific breeding conditions (e.g. photoperiod 652
and temperature) to complete their gametogenesis and spawning 653
591 4. What are the factors that can affect egg or sperm quality? in captivity. In this case, it is likely that the use of nutrients by 654
TE
brood fish and their incorporation into the yolk will be affected 655
592 4.1. Nutrition by external factors such as photoperiod and temperature that are 656
known to control vitellogenesis (see Section 4.2 below). For all 657
593 Broodstock nutrition is an important factor susceptible to affect the above reasons, it should thus be stressed that many existing 658
594 not only fecundity and gametogenesis but also gamete quality, and observations on the effect of a specific component of the diet on 659
EC
595 existing work has been extensively reviewed (Kjörsvik et al., 1990; reproductive performance could be species-specific and/or experi- 660
596 Brooks et al., 1997; Izquierdo et al., 2001). It is well accepted in the ment-specific. 661
597 literature that broodstock nutrition can significantly impact repro-
598 ductive performance and this topic has been specifically reviewed 4.1.2. Sperm 662
599 by Izquierdo and co-workers (Izquierdo et al., 2001). The definition It is an obvious statement that nutrient requirements of the 663
RR
600 of reproductive performance is very broad and includes many broodstock are to be met in order to sustain reproductive perfor- 664
601 types of parameters including egg size, larval size, timing of repro- mance, and this includes the provision of essential fatty acids, 665
602 duction season, puberty, fecundity, plasma levels of reproductive mainly unsaturated ones, that the fish cannot synthesize. Gener- 666
603 hormones, and spawning frequency. In contrast, data on the spe- ally, fresh water species including Salmonidae, Cyprinidae, and 667
604 cific effects of broodstock diet on gamete quality are more limited, eel need both 18:2(n 6) and 18:3(n 3) fatty acids in the diet 668
and sometimes controversial. Indeed, Brooks and co-workers have while marine species need the more elongated and unsaturated 669
CO
605
606 previously indicated that the evidence that diet can directly affect fatty acids 20:5(n 3) and 22:6(n 3) (Takeuchi and Watanabe, 670
607 egg quality is very limited (Brooks et al., 1997). According to these 1982; Watanabe, 1982). It was shown that lipid composition of 671
608 authors, the different methods used to evaluate egg quality and the the diet affects sperm lipid composition even when the essential 672
609 different timings of provision of the studied diet during the fish’s nutritional requirements are met (Labbe et al., 1995; Bell et al., 673
610 life, make it difficult to identify any real improvements that are a 1996; Pustowka et al., 2000; Asturiano et al., 2001). Nevertheless, 674
UN
611 function of the diet alone. In the present section, we will focus preferential retention of some polyunsaturated fatty acids (namely 675
612 on the effects of broodstock nutrition on the developmental capac- 22:6(n 3)) was observed, as if the most important components 676
613 ities of the egg once fertilized, and on the fertilization ability of the were maintained at a specific level in sperm membranes (Labbe 677
614 sperm. et al., 1995). This stability of a basal fatty acid composition in sper- 678
matozoa may explain why lipid diet little affected spermatozoa 679
615 4.1.1. Eggs quality, as shown after cryopreservation of rainbow trout sperma- 680
616 While specific data on egg fertilization and/or developmental tozoa (Labbe et al., 1993; Pustowka et al., 2000). It should be noted 681
617 success are scarce, many studies have shown that food restriction however that in European sea bass (Asturiano et al., 2001), 682
618 can have major effects on spawning success, gametogenesis, egg although sperm motility and fertilization ability was not affected 683
619 and larvae size as previously reviewed (Izquierdo et al., 2001). Sim- by the male diet, survival of embryos and larvae was affected. This 684
620 ilarly, many studies have shown significant effects of diet compo- indicates a unique and striking long-term effect of diet-mediated 685
621 sition on fecundity, spawn quantity, spawn frequency, eicosanoid sperm quality. 686
622 production, steroid hormone levels, and gonadotropin-induced Vitamins are also components that the fish cannot synthesize 687
623 maturation. Other investigations (also reviewed in Izquierdo and which should be added to the diet. Ascorbic acid (vitamin C) 688
624 et al., 2001) have shown that some components of broodstock diet is one of these vitamins whose effect on sperm quality was ex- 689
625 were necessary to ensure a normal development of the embryo. For plored to some extent. Dabrowski and co-workers showed in rain- 690
ARTICLE IN PRESS
691 bow trout and in yellow perch (Perca flavescens) that seminal plas- 4.2.2. Photoperiod 755
692 ma concentration of ascorbic acid reflects vitamin C dietary sup- As discussed above, the effect of photoperiod on egg quality is 756
693 plementation. They further demonstrated that low ascorbic acid difficult to study, because manipulation of photoperiod often re- 757
694 levels in the seminal fluid impaired sperm concentration and sults in the modification of other parameters throughout oogene- 758
695 motility (Ciereszko and Dabrowski, 1995), sperm fertilization abil- sis, including during late oogenesis. For instance, age and body 759
696 ity (Dabrowski and Ciereszko, 1996) and the hatching rate of em- size of the broodfish, water temperature, and length of oogenesis 760
697 bryos sired by spermatozoa from the deficient males (Dabrowski can be different from the normal-photoperiod control. In many fish 761
698 and Ciereszko, 1996; Lee and Dabrowski, 2004). species, including salmonids, the decrease of egg quality observed 762
after out of season spawning has often been attributed to subopti- 763
699 4.2. Environmental factors: temperature, photoperiod, salinity mal temperature as discussed in the previous section (Breton et al., 764
1983; Devauchelle et al., 1988; Davies and Bromage, 2002; van der 765
700 4.2.1. Temperature Meeren and Ivannikov, 2006). Nevertheless, it was shown in rain- 766
F
701 Temperature is known to have a major impact on egg quality. bow trout that artificial photoperiod resulting in an advanced 767
702 This is especially true during the reproductive season and spawn- spawning in June–July resulted in a significant decrease of egg 768
OO
703 ing. Both high and low temperature can have a negative impact quality even if the water temperature was kept at 12 °C during 769
704 on egg quality, depending on the species. In rainbow trout, tem- the reproductive season (Bonnet et al., 2007a). Egg quality defects 770
705 peratures of 15 °C and above can significantly reduce egg quality were characterized by significantly lower survival of the progeny 771
706 (Pankhurst et al., 1996; Aegerter and Jalabert, 2004) and in brook at eyeing and yolk-sac resorption and a significantly increased inci- 772
707 trout (Salvelinus fontinalis) temperatures of 12 °C and above sig- dence of deformities, especially abnormal yolk-sac resorption. 773
708 nificantly reduced hatching rate (Hokanson et al., 1973). In those Some evidence also suggested that the timing of ovulation during 774
PR
709 salmonid species, high temperatures significantly increased the the first reproductive season had an impact on egg quality ob- 775
710 incidence of embryonic deformities (Hokanson et al., 1973; served after photoperiod-advanced spawning (Bonnet et al., 776
711 Aegerter and Jalabert, 2004) and triploid fry (Aegerter and Jala- 2007a). A study conducted in sea bass using 5 different artificial 777
712 bert, 2004). In contrast, the quality of Arctic charr (Salvelinus alpi- photoperiod regimes showed that egg quality (estimated by the 778
713 nus) eggs obtained from females held at 10 °C is significantly percentage of floating eggs), hatching rate and survival to first 779
714 reduced in comparison to eggs obtained from females held at feeding were affected by at least some photoperiod regimes (Car- 780
715
716
5 °C (Gillet et al., 1996). In the Atlantic halibut (Hippoglossus hip-
poglossus) high water temperature during the reproductive season
D rillo et al., 1989). Indeed, while mean hatching rate expressed as
a percentage of floating eggs was 84.8 ± 3.3 (mean ± SE) in the con-
781
782
717 resulted in significantly lower fertilization and hatching rates trol group, the 5 different photoperiod regimes resulted in 783
TE
718 (Brown et al., 1995). Similarly, the temperature experienced by 21.4 ± 2.8, 64.5 ± 9.7, 78.9 ± 7.5, 81.2 ± 6.3, and 83.2 ± 6.7 hatching 784
719 female Wolffish during the breeding season significantly influ- respectively. In addition, at least one spawn in which less than 5% 785
720 enced egg quality (Tveiten et al., 2001). It has also been shown of the eggs were floating (i.e. were of good quality) was found for 786
721 in Atlantic salmon (Salmo salar) that suboptimal temperatures each artificial photoperiod regime while that never happened in 787
722 during vitellogenesis can negatively impact egg quality (King the control group (Carrillo et al., 1989). In summary, available data 788
EC
723 et al., 2003). In addition to the negative impact on egg quality indicate that photoperiod-induced manipulation of spawning data 789
724 by itself, high temperatures also increase the drop of egg quality can negatively impact egg quality. The importance of this negative 790
725 resulting from the post-ovulatory ageing process. In several sal- effect on egg quality seems highly dependant on the type of photo- 791
726 monid species, high temperatures result in a much faster and period regime used. It seems also clear that suboptimal temperature 792
727 stronger decrease of egg quality in comparison to optimal tem- around spawning time will further increase any negative impact of 793
RR
728 perature (Gillet, 1991; Aegerter and Jalabert, 2004). Finally, out the photoperiod regime on the overall quality of the eggs. 794
729 of season spawning resulting in ovulation at suboptimal temper-
730 atures has led to the production of significantly reduced egg qual- 4.2.3. Salinity 795
731 ity in several species (Devauchelle et al., 1988; Davies and For species that spend a part of their life in sea water and mi- 796
732 Bromage, 2002; van der Meeren and Ivannikov, 2006). In these grate to fresh water for reproduction, water salinity during the 797
733 studies, it is however difficult to separate the specific effects of reproductive season can significantly affect reproductive success. 798
CO
734 temperature and photoperiod on egg quality. In Atlantic salmon, holding females in sea water during the repro- 799
735 There are little reports to our knowledge on sperm quality ductive season resulted in either delayed or blocked ovulation 800
736 changes in response to broodstock rearing temperature. The rear- (Haffray et al., 1995). However, eggs stripped from females held 801
737 ing temperature of the fish is known to modulate their metabo- in sea water and freshwater exhibited similar eyeing rates. In con- 802
738 lism, and some adaptive responses to abrupt temperature trast, when eggs were fertilized two weeks after ovulation, egg 803
UN
739 changes were described in organs bearing a key role for fish sur- quality was significantly reduced in eggs stripped from females 804
740 vival. Erythrocytes, brain, liver or muscle membranes respond to held in sea water. Earlier studies conducted in Coho salmon 805
741 temperature changes by changing lipid composition (see the re- (Oncorhynchus kisutch) produced in similar results (Sower et al., 806
742 view by Hazel and Williams, 1990). In rainbow trout, spermatozoa 1982). In contrast, another study showed that transferring Pink 807
743 from fish transferred to a temperature lower than their rearing and Coho salmon females captured in estuary or freshwater into 808
744 temperature (cold acclimation) displayed a lipid composition seawater resulted in a limited but significant decrease in the eye- 809
745 slightly different from that of warm-acclimated fish (Labbe and ing rate (Werthemer, 1984). 810
746 Maisse, 1996). Additionally, sperm quality after freeze–thawing It was reported that the spermatozoa of brown trout reared in 811
747 was better in cold-acclimated fish in comparison to warm-accli- sea water had a higher membrane permeability and/or a lower 812
748 mated fish. The effect of this temperature acclimation was no long- membrane resistance to hypo-osmotic stress than spermatozoa 813
749 er detected 2 months after the temperature change. However, of fish kept in freshwater (Labbe and Maisse, 2001). Interestingly, 814
750 these temperature effects were not tested on fresh spermatozoa. sperm motility just after collection was better in the fresh water 815
751 Whether the positive temperature effect was due to the lipid group whereas it was better in the sea water group after 3 days 816
752 changes, namely cholesterol content changes, was explored (Mul- of storage. The role of seminal fluid osmotic pressure is proposed 817
753 ler et al., 2008), but no straightforward role of cholesterol was as one parameter involved in the sperm response to the salinity 818
754 reported. in the male rearing environment. 819
ARTICLE IN PRESS
820 4.3. Husbandry practices including spawning induction, egg post- on Arctic charr where 30% of the population had naturally ovu- 885
821 ovulatory ageing, and gamete handling post-stripping lated, resulted in a limited advancement of ovulation and compa- 886
rable survival at the eyed stage in hormonally-stimulated and 887
822 4.3.1. Spawning induction control groups (Gillet et al., 1996). Finally, a study conducted on 888
823 Hormonal induction of spawning is widely used in aquaculture rainbow trout at 11.5 °C did not show any differences in fertiliza- 889
824 to induce ovulation in species that do not spontaneously ovulate in tion, eyeing and hatching percentages between the progenies of 890
825 captivity, or to synchronize ovulation for practical reasons in other control and hormonally-stimulated females (Arabaci et al., 2004). 891
826 species. A great deal of information is thus available on spawning- However, authors did not test differences between cumulative sur- 892
827 induction techniques and their efficiency in terms of ovulation vival rates at each stage, the maximum being observed in the con- 893
828 rate. In contrast, the impact of spawning-induction techniques on trol group. These results were confirmed by a recent study 894
829 gamete quality is less documented and sometimes limited to conducted at 12 °C in which the lower survival rates observed in 895
830 embryonic survival at early stages (up to eyed stage). During the the progeny of hormonally-stimulated females were significantly 896
F
831 final stages of oogenesis (also referred to as final oocyte matura- different from the control at yolk-sac resorption but not at the eyed 897
832 tion), the follicle-enclosed oocyte progressively acquires its ability stage (Bonnet et al., 2007a). Interestingly, in contrast to what has 898
OO
833 (i) to resume meiosis, and (ii) to subsequently develop into a nor- been seen for other factors known to impact egg quality, spawning 899
834 mal embryo after fertilization (Bobe et al., 2008). In vertebrates, induction does not seem to significantly increase the percentage of 900
835 these two partially overlapping processes are referred to as ‘‘oocyte malformed alevins (Bonnet et al., 2007a). Together, these studies 901
836 maturational competence acquisition” and ‘‘oocyte developmental indicate that spawning induction can induce egg quality defects 902
837 competence acquisition” respectively. It is thus possible to artifi- in salmonids, the strongest effects being observed when the hor- 903
838 cially induce meiosis in a meiotically competent oocyte that will monal stimulation protocol is applied early in the reproductive 904
PR
839 not necessarily result in a fully developmentally competent meta- season. The egg quality defects subsequently observed are charac- 905
840 phase II oocyte. Indeed, the ovarian stage at the time of spawning terized by lower embryonic survival up to yolk-sac resorption, but 906
841 induction will have a major effect of the developmental capacities with no specific embryonic malformation. Finally, as previously 907
842 of subsequently ovulated oocytes. A study in European sea bass hypothesized (Mylonas et al., 1992), existing data indicate that 908
843 showed that the quality of eggs obtained using 3 different types the physiological status or state of maturity of the female at the 909
844 of spawning-induction techniques was always lower (hatching rate D time of hormonal induction is critical for the quality of the subse- 910
845 below 50%) than for eggs obtained after natural ovulation (75% quently ovulated eggs. This physiological status probably corre- 911
846 hatching rate) (Fornies et al., 2001). Similarly, in Senegal sole (Solea sponds, at least in part, to the process of intrafollicular oocyte 912
847 senegalensis), the percentage of buoyant eggs used as an estimator developmental competence acquisition. 913
TE
848 of egg quality was lower (26–61%) in hormonally-stimulated fe- As recently reviewed by Alavi et al. (2008), spawning inductors 914
849 males than in saline-injected females (88.9–97.8%) (Agulleiro are very efficient at increasing sperm volume production and den- 915
850 et al., 2006). In yellowtail flounder, it was concluded that GnRHa- sity. Spawning inductors either maintain or increase sperm motil- 916
851 induction of ovulation tends to decrease egg quality (Avery et al., ity in all species tested, most likely because the hormonal 917
852 2004). These studies, along with previous work in other species, stimulation is favorable to sperm maturation in the testis and in 918
EC
853 clearly show that developmental capacities of the eggs obtained the sperm ducts. Improved fertilization ability was subsequently 919
854 after spawning induction can be extremely variable and range from observed after hormonal stimulation in both tench (Tinca tinca) 920
855 0% hatching rate for some females to hatching rates close to 90% for and goldfish (Zheng et al., 1997; Caille et al., 2006). 921
856 other females subjected to similar hormonal induction protocols
857 (Marino et al., 2003). This high variability is probably linked to 4.3.2. Egg post-ovulatory ageing 922
RR
858 existing differences between females in terms of oogenetic stages Post-ovulatory ageing occurs between the release of the meta- 923
859 at the time of stimulation and the lack of an accurate morpholog- phase II oocyte from the follicle at ovulation, and fertilization. Dur- 924
860 ical estimator that could be used to identify the best timing for ing this time period, the oocyte undergoes an overall decrease in its 925
861 hormonal stimulation. ability to be fertilized and to subsequently develop into a normal 926
862 In contrast to what was observed in some marine fishes (see embryo. Excessive post-ovulatory ageing can lead to major mor- 927
863 above), the impact of spawning induction seems to have a milder phological and biochemical changes of the egg. This process has 928
CO
864 effect on egg quality in salmonids. In rainbow trout, a study con- been referred to as ‘‘over-ripening”. However, in many cases, 929
865 ducted at 14 °C showed that hormonal induction of ovulation using post-ovulatory ageing can induce a significant decrease in egg 930
866 GnRH analogs resulted in rather low fertilization rates (Breton developmental capacities without any noticeable morphological 931
867 et al., 1990). Even though the differences were not significant, fer- changes in the appearance of the egg. This decrease in egg quality 932
868 tilization rates were lower in hormonally-stimulated fish (24–40%) occurs more or less rapidly depending on the species and is also 933
UN
869 than in control females (53%). It is however noteworthy that the highly dependent on external factors (e.g. temperature) and sub- 934
870 experimentation was conducted at the beginning of reproductive ject to high inter-female variability. In most fish species, the drop 935
871 the season at a time when females are still far from having com- in egg quality occurs very rapidly after ovulation. In goldfish, fertil- 936
872 pleted oocyte developmental competence acquisition. Similarly, ization and hatching rates are dramatically reduced within a few 937
873 another study carried out before the onset of the spawning season hours after ovulation and after 10 h hatching rate is 0% (Formacion 938
874 showed that treatments that could most efficiently advance rain- et al., 1995). In turbot, freshly ovulated eggs showed fertilization 939
875 bow trout ovulation resulted in low embryonic survival at eyed rates above 90%, while eggs retained in the lumen for 24 h exhib- 940
876 stage (around 55%) while the progeny of control females and fe- ited 0% survival at hatching (McEvoy, 1984). In Japanese flounder 941
877 males subjected to a less efficient treatment resulted in higher sur- (Paralichthys olivaceus), hatching rate reached a significant maxi- 942
878 vival rates (79–85%) (Billard et al., 1984). In total agreement with mum for eggs fertilized 24 h after ovulation and subsequently de- 943
879 these results, a study carried out in brown trout using several creased for ageing times greater than 24 h (Hirose et al., 1979). A 944
880 doses of GnRHa showed that the highest GnRHa (10 lg/kg bw) that rapid decrease in egg quality was also observed in other species 945
881 could significantly advance ovulation resulted in significantly low- such as bighead catfish (Clarias macrocephalus), cod, Ayu (Plecoglos- 946
882 er embryonic survival at both eyeing and hatching whilst lower sus altivelus), Oriental weatherfish (Misgurnus anguillicaudatus), 947
883 concentrations had no significant effects on ovulation and survival and striped bass (Roccus saxatilis) as previously reviewed (Kjörsvik 948
884 rates (Mylonas et al., 1992). In contrast, an experiment conducted et al., 1990; Bromage et al., 1994). By contrast, it has been known 949
ARTICLE IN PRESS
950 for a long time that salmonids are able to hold their eggs for several eggs at 13 °C or below resulted in significantly lower fertilization 1014
951 days without losing their developmental capacities (Sakai et al., rates. Similarly, eggs held in coelomic fluid for 19 h exhibited fer- 1015
952 1975; Escaffre et al., 1976, 1977; Escaffre and Billard, 1979). In tilizations rates below 35%, the maximum being obtained at 20– 1016
953 rainbow trout, eggs can be held in the body cavity for 2–4 weeks, 22 °C. In common carp, short-term (5, 30 and 60 min) exposure 1017
954 but maximum egg quality is reached around 5 days after ovulation of non-activated eggs to low temperatures induced a marked de- 1018
955 at 10–12 °C (Sakai et al., 1975; Escaffre et al., 1977; Bromage et al., crease of embryonic survival at hatching (Dinnyes et al., 1998). 1019
956 1994; Aegerter and Jalabert, 2004; Bonnet et al., 2007a). In this In another study carried out using koi carps, storage of pre-acti- 1020
957 species a slight but significance increase in egg quality is observed vated eggs at 7 °C resulted in a clear decrease in embryonic sur- 1021
958 within a few days after ovulation. At 10 °C, maximum fry survival vival at hatching for holding times greater that 2 h (Rothbard 1022
959 was observed from eggs stripped 4–6 days after ovulation (Sprin- et al., 1996). In European catfish (Silurus glanis), in vitro holding 1023
960 gate et al., 1984; Bromage et al., 1994) while a significant increase of ovulated eggs at 8, 19 and 25 °C for 3.5, 8.5 or 12 h resulted in 1024
961 in egg quality was observed from eggs stripped 5 days after ovula- a dramatic decrease in hatching rates. No survival was observed 1025
F
962 tion, in comparison to eggs stripped at ovulation, from females at 8 °C whilst at both 19 and 25 °C holding temperatures resulted 1026
963 held at 12 °C (Aegerter et al., 2005). At this temperature, a limited in low embryonic survival and an increased occurrence of mal- 1027
OO
964 but significant increase in malformed embryos was observed when formed larvae at hatching (Linhart and Billard, 1995). 1028
965 eggs were stripped 7 days after ovulation. For longer holding times, The issue of sperm handling and chilled storage after stripping 1029
966 post-ovulatory ageing induces not only a dramatic drop in survival was recently reviewed (Bobe and Labbe, 2008). It is generally ob- 1030
967 at the eyed stage, hatching, and yolk-sac resorption stages, but also served that whatever the fish rearing temperature, sperm handling 1031
968 a dramatic increase in malformed embryos (Aegerter and Jalabert, at 0–4 °C is preferred in order to reduce cell metabolism. Besides, 1032
969 2004; Aegerter et al., 2005; Bonnet et al., 2007a). Indeed, the age- most fish spermatozoa are not sensitive to chilling injury (Labbe 1033
PR
970 ing process specifically induces an increase in the frequency of the et al., 1997), in contrast to mammalian spermatozoa, and they 1034
971 ‘‘Cyclops” malformation (Bonnet et al., 2007a). Finally, long-term can therefore be stored at sub-zero temperatures without protec- 1035
972 post-ovulatory ageing is also associated with a significant increase tive agents. Dilution of spermatozoa is not always necessary for 1036
973 in ploidy anomalies of the developing embryo, including an in- short-term storage, but addition of antibiotics will always improve 1037
974 creased frequency of triploids (Aegerter and Jalabert, 2004). sperm quality during storage lasting for 1 day or more. Sperm from 1038
most species can be diluted in an appropriate medium which will 1039
975
976
4.3.3. Time of sperm stripping during the breeding season and
stripping frequency
D satisfy the required pH and osmolality. The ionic composition of
these media is usually based on the seminal plasma characteristics.
1040
1041
977 In species exhibiting an annual rhythm of reproduction such as For species whose motility duration is short, the dilution medium 1042
TE
978 rainbow trout or turbot, sperm production starts earlier and ends is also formulated to maximize the inhibition of motility activation. 1043
979 later, during reproductive season, than egg production (Büyükha-
980 tipoglu and Holtz, 1984; Baynes and Scott, 1985; Suquet et al., 4.4. Stress 1044
981 1998). Most studies have reported a lower total sperm production
982 at both the beginning and the end of the reproductive season, in Data on the effect of broodstock stress on subsequent gamete 1045
EC
983 contrast to the steady sperm production observed in the middle quality are scare and different conclusions have been reached 1046
984 of the season. A limited loss in sperm motility at the beginning depending on the type and intensity of stressor, the species, 1047
985 and at the end of the spermiation period was sometimes reported. and the period when the stressor was applied. In rainbow trout, 1048
986 Besides, a reduction in sperm fertilizing ability was reported at the repeated acute stress induced by exposure to emersion during 1049
987 end of the season in sea bass (Dicentrarchus labrax) (Dreanno et al., the 9 month period prior to spawning resulted in lower egg vol- 1050
RR
988 1999c). In contrast, no influence of stripping frequency on sperm ume, lower sperm density in milt and lower survival at the eyed 1051
989 quality was reported, apart from variations in total sperm produc- stage, hatching and swim-up (Campbell et al., 1992). Similar re- 1052
990 tion (Büyükhatipoglu and Holtz, 1984). Nevertheless, it should be sults on egg weight, egg volume and progeny survival were ob- 1053
991 kept in mind that frequent stripping could stress the males and tained in brown trout and rainbow trout males and females 1054
992 subsequently induce sperm production and/or quality problems. subjected to one or two episodes of confinement stress in the 1055
months immediately prior to ovulation (Campbell et al., 1994). 1056
CO
993 4.3.4. Gamete handling post-stripping In contrast, sperm counts did not significantly vary between 1057
994 After ovulation, eggs can be collected from the females by strip- stressed and control groups. Finally, significantly reduced circu- 1058
995 ping for the purpose of artificial fertilization. The ability of the egg lating vitellogenin plasma levels were observed in females. In a 1059
996 to be fertilized and subsequently develop into a normal embryo later study conducted on female Coho salmon during the final 1060
997 after ex-vivo holding is highly variable depending on the species two weeks of oogenesis, a stress induced by net chasing resulted 1061
UN
998 (see ‘‘post-ovulatory ageing” section above). Within a fish species, in a higher number of ovulating females in comparison to the 1062
999 the success of egg holding procedures will be highly dependant on control group and higher cortisol levels in eggs from the stressed 1063
1000 several parameters such as temperature, oxygenation, and charac- group (Stratholt et al., 1997). In rainbow trout, stress applied dur- 1064
1001 teristics of the medium used. In chum salmon (Oncorhynchus keta) ing early vitellogenesis resulted in smaller eggs while stress ap- 1065
1002 and Sockeye salmon (Oncorhynchus gorbuscha), unfertilized eggs plied during late vitellogenesis-final maturation resulted in 1066
1003 could be successfully stored for a few days at approximately 3 °C advanced ovulation. However, no effect on progeny survival was 1067
1004 (Withler and Morley, 1968; Jensen and Alderdice, 1984). In both observed (Contreras-Sanchez et al., 1998). Together, these data 1068
1005 rainbow and brown trout, unfertilized eggs could be held in vitro suggest that stress applied during oocyte growth can result in sig- 1069
1006 in coelomic fluid at 0–2 °C for at least 5–7 days (Carpentier and Bil- nificantly smaller egg size, while stress applied during the final 1070
1007 lard, 1978; Billard and Gillet, 1981; Babiak and Dabrowski, 2003). oogenesis stages can result in advanced ovulation. In addition, a 1071
1008 At a higher temperature (12 °C) comparable egg qualities were ob- severe stress (Campbell et al., 1992, 1994) can induce signifi- 1072
1009 served when eggs were held for 3 days in vivo, for the broodfish, or cantly lower embryonic survival while no or little effect is in- 1073
1010 in vitro in coelomic fluid (Bonnet et al., 2003). For warm-water spe- duced by a milder stress (Contreras-Sanchez et al., 1998). 1074
1011 cies such as tilapia (Sarotherodon mossambicus) unfertilized eggs The acute stress applied to mature wild fish during capture 1075
1012 can successfully be held in coelomic fluid for 1.5 h at temperatures and transportation may be responsible for the decrease in sperm 1076
1013 above 16 °C (Harvey and Kelley, 1984). In contrast, holding tilapia motility observed in white bass (Morone chrysops) (Allyn et al., 1077
ARTICLE IN PRESS
1078 2001). In rainbow trout, we also observed that males confined species. Within each species, the domestication level of broodfish 1108
1079 alone in small tanks had cortisol levels 4 times higher than the (i.e. captured form the wild or originating from captive reproduc- 1109
1080 controls, and sperm motility decreased to less than 10% of the tion) is also likely to have an impact on reproductive success in re- 1110
1081 control values. sponse to specific rearing conditions. 1111
1082 4.5. Other factors 5. Conclusions and future directions 1112
1083 Many other factors are susceptible to affect gamete quality, Egg quality can be defined as the ability of the egg to be fertil- 1113
1084 including exposure to xenobiotics and pollutants, or physiochemi- ized and to subsequently develop into a normal embryo. Similarly, 1114
1085 cal properties of the water (reviewed in Brooks et al., 1997). In sperm quality can be defined as its ability to successfully fertilize 1115
1086 addition, it has been shown in mammals that parental genotypes an egg and subsequently allow the development of a normal em- 1116
1087 can strongly influence fertility, fecundity and oocyte quality. By bryo. The identification of predictive estimators or markers of gam- 1117
F
1088 contrast, the effects of broodfish genetics on gamete quality remain ete quality would have major applications in the field or in the 1118
1089 poorly documented. Existing fertility differences in rainbow trout industry. For eggs, it would help prevent the risk of mixing, for 1119
OO
1090 female broodfish have been attributed to genetic differences (Stod- practical reasons, egg batches of poor and good quality. For sperm, 1120
1091 dard et al., 2005). Further investigations are however required to it would prevent the risk of poor fertilization rates resulting in the 1121
1092 evaluate the heritability of fertility observed during the first repro- loss of whole egg batches. However, to date, it seems clear that no 1122
1093 duction. In addition, the genetic influence of parental genomes on effective predictive marker or estimator of gamete quality exists 1123
1094 egg quality is difficult to study as the onset of zygotic transcription even though non-viable gametes can sometimes be identified in 1124
1095 does not occur until mid-blastula transition. Indeed, the very early some species, through the assessment of simple parameters such 1125
PR
1096 steps of embryonic development rely on gene products (maternal as buoyancy, appearance or motility. Thus, apart from markers of 1126
1097 mRNAs and proteins) supplied to the embryo by the mother. How- extremely low quality, it is still very difficult to accurately estimate 1127
1098 ever, the abundance and processing of maternal mRNAs and pro- the quality of the gametes prior to fertilization. For instance, nor- 1128
1099 teins in the female gamete are susceptible to be impacted on by mal eggs that do no show any sign of non viability could in fact 1129
1100 non-genetic factors such as environmental variables (e.g. photope- have low developmental capacities. Hence, the only biologically 1130
1101 riod) (Bonnet et al., 2007b). relevant way to accurately estimate gamete quality is to perform
D 1131
1102 Finally, in many fish species, social factors or inter-individual fertilization and/or monitor embryonic and larval survival. Fur- 1132
1103 interactions are highly susceptible to influence reproductive suc- thermore, monitoring embryonic malformation or larval deformi- 1133
1104 cess. In general, rearing conditions can strongly influence gameto- ties will further help characterize gamete quality. Specific 1134
TE
1105 genesis and gamete quality. The overall impact of broodstock malformations are associated with specific gamete quality prob- 1135
1106 breeding conditions is probably different in species that have been lems induced by specific factors (Bonnet et al., 2007a). It is thus 1136
1107 domesticated for a long time in comparison to new aquaculture important not only to record survival throughout development 1137
EC
Factors that can influence gamete quality How to estimate gamete quality?
stress
spawning induction
RR
temperature
Egg
photoperiod post-ovulatory ageing
egg handling
Ovulation
buoyancy Malformations
CO
Oocyte maturation Early cleavage

Oogenesis patterns
Egg
Fertilization
Development
Eyeing Hatching Yolk-sac
resorption
UN
Spermatogenesis
Fertilization success
Spermatozoa
Survival
stress Motility
Membrane integrity
Sperm nutrition
time in the Energy metabolism
reproductive season
DNA compaction
sperm handling
Fig. 2. Main factors that can influence gamete quality in fish and main parameters than can be recorded to fully characterize gamete quality. The time period during when
factors can influence gamete quality is indicated by dotted lines.
ARTICLE IN PRESS
1138 but also to monitor embryonic and larval deformities to completely receptor Ib, and p53 in the rainbow trout oocyte in relation with developmental 1201
competence. Mol. Reprod. Dev. 67, 127–135. 1202
1139 assess gamete quality. 1203
Aegerter, S., Jalabert, B., Bobe, J., 2005. Large scale real-time PCR analysis of mRNA
1140 Many investigations have successfully led to the identification abundance in rainbow trout eggs in relationship with egg quality and post- 1204
1141 of external, experimental or rearing factors that can significantly ovulatory ageing. Mol. Reprod. Dev. 72, 377–385. 1205
Agulleiro, M.J., Anguis, V., Canavate, J.P., Martinez-Rodriguez, G., Mylonas, C.C., 1206
1142 impact gamete quality. Despite these efforts, the environmental 1207
Cerda, J., 2006. Induction of spawning of captive-reared Senegal sole (Solea
1143 control of gamete quality is far from being fully understood and senegalensis) using different administration methods for gonadotropin- 1208
1144 existing research efforts dedicated to a better characterization releasing hormone agonist. Aquaculture 257, 511–524. 1209
Alavi, S.M.H., Linhart, O., Coward, K., Rodina, M., 2008. Fish spermatology: 1210
1145 and understanding of the effect of external factors and broodstock
Implications for Aquacultureculture management. In: Alavi, S.M.H., Cosson, 1211
1146 management conditions on gamete quality should be pursued. In J.J., Coward, K., Rafiee, G. (Eds.), Fish Spermatology Alpha Science International 1212
1147 order to be fully informative, such studies have to thoroughly as- Ltd., Oxford, U.K., pp. 397–460. 1213
1148 sess gamete quality in order to avoid the drawing of biased conclu- Allyn, M.L., Sheehan, R.J., Kohler, C.C., 2001. The effects of capture and 1214
transportation stress on white bass semen osmolality and their alleviation via 1215
1149 sions based on a partial evaluation of gamete quality. It should also
F
sodium chloride. Trans. Am. Fish. Soc. 130, 706–711. 1216
1150 be stressed that not only species-specific characteristics but also Arabaci, M., Diler, I., Sari, M., 2004. Induction and synchronisation of ovulation in 1217
1151 domestication level and adequacy of rearing systems and brood- rainbow trout, Oncorhynchus mykiss, by administration of emulsified buserelin 1218
OO
(GnRHa) and its effects on egg quality. Aquaculture 237, 475–484. 1219
1152 stock management conditions have to be taken into account when Asturiano, J.F., Sorbera, L.A., Carillo, M., Zanuy, S., Ramos, J., Navarro, J.C., Bromage, 1220
1153 drawing conclusions on the effect of a specific factor on gamete N., 2001. Reproductive performance in male European sea bass (Dicentrarchus 1221
1154 quality. Ideally, a control resulting in almost 100% viable and nor- labrax, L.) fed two PUFA-enriched experimental diets: a comparison with males 1222
fed a wet diet. Aquaculture 194, 173–190. 1223
1155 mal individuals will be a good indicator of the full adequacy of the 1224
Avery, T.S., Boyce, D., Brown, J.A., 2004. Mortality of yellowtail flounder, Limanda
1156 experimental system used to test the effect of a specific factor on ferruginea (Storer), eggs: Effects of temperature and hormone-induced 1225
1157 gamete quality. This is especially true for factors that have a mild ovulation. Aquaculture 230, 297–311. 1226
PR
Avery, T.S., Brown, J.A., 2005. Investigating the relationship among abnormal 1227
1158 effect on gamete quality. In suboptimal systems, in which gamete 1228
patterns of cell cleavage, egg mortality and early larval condition in Limanda
1159 quality is intermediate and/or variable, only major effects will be ferruginea. J. Fish Biol. 67, 890–896. 1229
1160 detected. Existing work conducted on the main aquaculture spe- Avery, T.S., Killen, S.S., Hollinger, T.R., in press. The relationship of embryonic 1230
development, mortality, hatching success, and larval quality to normal or 1231
1161 cies on the influence of external factors and husbandry practices
abnormal early embryonic cleavage in Atlantic cod, Gadus morhua. 1232
1162 on gamete quality (mostly eggs) has led to the identification of Aquaculture. Q2 1233
1163 key factors that should be controlled in order to obtain good qual- Avramova, Z., Uschewa, A., Stephanova, E., Tsanev, R., 1983. Trout sperm chromatin. 1234
1164 ity gametes (Fig. 2). Some specific factors (e.g. post-ovulatory age-
D I. Biochemical and immunological study of the protein composition. Eur. J. Cell 1235
Biol. 31, 137–142. 1236
1165 ing) probably have general effects that can be extended to other Babiak, I., Dabrowski, K., 2003. Refrigeration of rainbow trout gametes and embryos. 1237
1166 species. For other factors, or for less documented species, the J. Exp. Zoolog. A Comp Exp. Biol 300, 140–151. 1238
TE
1167 amount of available data is scarce and specific efforts should be Bally-Cuif, L., Schatz, W.J., Ho, R.K., 1998. Characterization of the zebrafish Orb/ 1239
CPEB-related RNA binding protein and localization of maternal components in 1240
1168 made to address these questions. This is especially true for newly the zebrafish oocyte. Mech. Dev. 77, 31–47. 1241
1169 domesticated species or for future aquaculture species. For these Baynes, S.M., Scott, A.P., 1985. Seasonal variations in parameters of milt production 1242
1170 new species, significant efforts should also be dedicated to the and in plasma concentration of sex steroids of male rainbow trout (Salmo 1243
gairdneri). Gen. Comp. Endocrinol. 57, 150–160. 1244
1171 determination of appropriate gamete handling procedures after 1245
EC
Beck, J.C., Fulcher, K.D., Beck, C.F., Cloud, J.G., 1992. Sperm surface antigen required
1172 collection. The procedures include storage conditions (medium, for fertility: identification on spermatozoa of rainbow trout by use of 1246
1173 temperature, and duration), in vitro fertilization methods, and em- monoclonal antibodies. Trans. Am. Fish. Soc. 121, 333–339. 1247
Bell, M.V., Dick, J.R., Thrush, M., Navarro, J.C., 1996. Decreased 20:4n 6/20:5n 3 1248
1174 bryo rearing conditions. 1249
ratio in sperm from cultured sea bass, Dicentrarchus labrax, broodstock
1175 In the past few years, several studies have aimed at identifying compared with wild fish. Aquaculture 144, 189–199. 1250
1176 cellular and molecular mechanisms that could play important roles Billard, R., 1983. Ultrastructure of trout spermatozoa: changes after dilution and 1251
RR
deep-freezing. Cell Tissue Res. 228, 205–218. 1252

1177 in controlling the developing potential of the oocyte and early em-
Billard, R., Gillet, C., 1981. Ageing of eggs and temperature potentialization of 1253
1178 bryo (Aegerter et al., 2005; Bonnet et al., 2007b; Ziv et al., 2008; micropolluant effects of the Aquaculturetic medium on trout gametes. Cahier 1254
1179 Crespel et al., 2008). These studies have successfully identified can- du Laboratoire de Montereau 12, 35–42. 1255
1180 didate mRNAs and proteins that could participate in the regulation Billard, R., Reinaud, P., Hollebecq, M.G., Breton, B., 1984. Advancement and 1256
synchronisation of spawning in Salmo gairdneri and S. Trutta following 1257
1181 and/or control of egg quality. However, the intracellular picture of administration of LRH-A combined or not with pimozide. Aquaculture 43, 57–66. 1258
1182 a developmentally competent egg or early embryo is far from being 1259
CO
Billard, R., Cosson, J., Crim, L.W., Suquet, M., 1995. Sperm physiology and quality. In:
1183 complete and additional genomic and functional investigations are Bromage, N.R., Roberts, R.J. (Eds.), Broodstock Management and Egg and Larval 1260
Quality. Cambridge University Press, Cambridge, pp. 53–76. 1261
1184 required to address this question. Blom, J.H., Dabrowski, K., 1995. Reproductive success of female rainbow trout 1262
1185 Similarly, it should be stressed that very little is known about (Oncorhynchus mykiss) in response to graded dietary ascorbyl monophosphate 1263
1186 the effect of ongoing genetic selection on the quality of the ga- levels. Biol. Reprod. 52, 1073–1080. 1264
Bobe, J., Jalabert, B., Fostier, A., 2008. Oogenesis: post-vitellogenic events leading to 1265
1187 metes. In many farmed animals (e.g. dairy cows) a decrease in fer- 1266
a fertilizable oocyte. In: Rocha, M.J., Arukwe, A., Kapoor, B.G. (Eds.), Fish
UN
1188 tility is often associated with the genetic selection for non- Reproduction. Science Publishers, Enfield, pp. 1–36. 1267
1189 reproductive phenotypes (Weigel, 2006). This is also a possible is- Bobe, J., Labbe, C., 2008. Chilled storage of sperm and eggs. In: Cabrita, E., Robles, V., 1268
Herraez, P. (Eds.), Methos in reproductive aquaculture: Marine and freshwater 1269
1190 sue for aquaculture that will require specific investigations in the 1270
species Taylor and Francis, London (UK).
1191 future. Boitano, S., Omoto, C.K., 1992. Trout sperm swimming patterns and role of 1271
intracellular Ca2+. Cell Motil. Cytoskel. 21, 74–82. 1272
Bonnet, E., Fostier, A., Bobe, J., 2007a. Characterization of rainbow trout egg quality: 1273
1192 Acknowledgment
a case study using four different breeding protocols, with emphasis on the 1274
incidence of embryonic malformations. Theriogenology 67, 786–794. 1275
1193 The authors thank Miranda Maybank for critical reading of the Bonnet, E., Fostier, A., Bobe, J., 2007b. Microarray-based analysis of fish egg quality 1276
1194 manuscript. after natural or controlled ovulation. BMC Genomics 8, 55. 1277
Bonnet, E., Jalabert, B., Bobe, J., 2003. A 3-day in vitro storage of rainbow trout 1278
(Oncorhynchus mykiss) unfertilised eggs in coelomic fluid at 12 degrees C does 1279
1195 References not affect developmental success. Cybium 27, 47–51. 1280
Breton, B., Maisse, G., Le Menn, F., 1983. Contrôle photopériodique de la saison de 1281
1196 Aegerter, S., Jalabert, B., 2004. Effects of post-ovulatory oocyte ageing and reproduction en salmoniculture: une expérience pilote en Bretagne. Bull. Fr. 1282
1197 temperature on egg quality and on the occurrence of triploid fry in rainbow Peche Piscic. 288, 35–45. 1283
1198 trout, Oncorhynchus mykiss. Aquaculture 231, 59–71. Breton, B., Weil, C., Sambroni, E., Zohar, Y., 1990. Effects of acute versus sustained 1284
1199 Aegerter, S., Jalabert, B., Bobe, J., 2004. Messenger RNA stockpile of cyclin B, insulin- administration of GnRHa on GtH release and ovulation in the rainbow trout, 1285
1200 like growth factor I, insulin-like growth factor II, insulin-like growth factor Oncorhynchus mykiss. Aquaculture 373–383. 1286
ARTICLE IN PRESS
1287 Bromage, N., Bruce, M., Basavaraja, N., Rana, K., Shields, R., Young, C., Dye, J., Smith, Dreanno, C., Cosson, J., Suquet, M., Seguin, F., Dorange, G., Billard, R., 1999b. 1373
1288 P., Gillespie, M., Gamble, J., 1994. Egg quality determinants in finfish: the role of Nucleotide content, oxidative phosphorylation, morphology, and fertilizing 1374
1289 overripening with special reference to the timing of stripping in the Atlantic capacity of turbot (Psetta maxima) spermatozoa during the motility period. Mol. 1375
1290 halibut Hippoglossus hippoglossus. J. World Aquacult. Soc. 25, 13–21. Reprod. Dev. 53, 230–243. 1376
1291 Bromage, N., Jones, J., Randall, C., Thrush, M., Davies, B., Springate, J.R.C., Duston, J., Dreanno, C., Suquet, M., Fauvel, C., Le Coz, J.-R., Dorange, G., Quemener, L., Billard, R., 1377
1292 Barker, G., 1992. Broodstock management, fecundity, egg quality and the timing 1999c. Effect of the aging process on the quality of sea bass (Dicentrarchus 1378
1293 of egg production in the rainbow trout (Oncorhynchus mykiss). Aquaculture 100, labrax) semen. J. Appl. Ichthyol. 15, 176–180. 1379
1294 141–166. Dreanno, C., Seguin, F., Cosson, J., Suquet, M., Billard, R., 2000. 1H-NMR and (31)P- 1380
1295 Brooks, S., Tyler, C.R., Sumpter, J.P., 1997. Egg quality in fish: what makes a good NMR analysis of energy metabolism of quiescent and motile turbot (Psetta 1381
1296 egg? Revi. Fish Biol. Fish. 7, 387–416. maxima) spermatozoa. J. Exp. Zool. 286, 513–522. 1382
1297 Brown, N.P., Shields, R.J., Bromage, N.R., 1995. The effect of spawning temperature Escaffre, A.M., Billard, R., 1979. Evolution de la fécondabilité des ovules de truite 1383
1298 on egg viability in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture arc-en-ciel Salmo gairdneri laissés dans la cavité abdominale au cours de la 1384
1299 261, 993–1002. période post-ovulatoire. Bull. Fr. Piscic. 272, 56–70. 1385
1300 Burns, K.H., Viveiros, M.M., Ren, Y., Wang, P., DeMayo, F.J., Frail, D.E., Eppig, J.J., Escaffre, A.M., Petit, J., Billard, R., 1976. Evolution de la fécondabilité des ovules de 1386
1301 Matzuk, M.M., 2003. Roles of NPM2 in chromatin and nucleolar organization in truite arc en ciel laissés dans la cavité coelomique après ovulation. Rev. Trav. 1387
F
1302 oocytes and embryos. Science 300, 633–636. Inst. Pêches. Marit. 40, 561–562. 1388
1303 Büyükhatipoglu, S., Holtz, W., 1984. Sperm output in rainbow trout (Salmo Escaffre, A.M., Petit, J., Billard, R., 1977. Evolution de la quantité d’ovules récoltés et 1389
1304 gairdneri)—effect of age, timing and frequency of stripping and presence of conservation de leur aptitude à être fécondés au cours de la période post 1390
OO
1305 females. Aquaculture 37, 63–71. ovulatoire chez la truite arc-en-ciel. Bull. Fr. Piscic. 265, 134–142. 1391
1306 Caille, N., Rodina, M., Kocour, M., Gela, D., Flajshans, M., Linhart, O., 2006. Quantity, Fauvel, C., Omnès, M.-H., Suquet, M., Normant, Y., 1993. Reliable assessment of 1392
1307 motility and fertility of tench Tinca tinca (L.) sperm in relation to LHRH analogue overripening in turbot (Scophthalmus maximus) by a simple pH measurement. 1393
1308 and carp pituitary treatments. Aquacult. Int. 14, 75–87. Aquaculture 117, 107–113. 1394
1309 Campbell, P.M., Pottinger, T.G., Sumpter, J.P., 1992. Stress reduces the quality of Feist, G., Schreck, C.B., Fitzpatrick, M.S., Redding, J.M., 1990. Sex steroid profiles of 1395
1310 gametes produced by rainbow trout. Biol. Reprod. 47, 1140–1150. coho salmon (Oncorhynchus kisutch) during early development and sexual 1396
1311 Campbell, P.M., Pottinger, T.G., Sumpter, J.P., 1994. Preliminary evidence that differentiation. Gen. Comp. Endocrinol. 80, 299–313. 1397
1312 chronic confinement stress reduces the quality of gametes produced by brown Formacion, M.J., Venkatesh, B., C.H., T., T.J., L., 1995. Overripening of ovulated eggs in 1398
PR
1313 and rainbow trout. Aquaculture 120, 151–169. goldfish, Carassius auratus: II. Possible involvement of postovulatory follicles 1399
1314 Carpentier, P., Billard, R., 1978. Conservation à court terme des gamètes de and steroids. Fish Physiol. Biochem. 14, 237–246. 1400
1315 Salmonidés à des températures voisines de 0°C. Ann. Biol. Anim. Biochim. Fornies, M.A., Mananos, E., Carrillo, M., Rocha, A., Laureau, S., Mylonas, C.C., Zohar, 1401
1316 Biophys. 18, 1083–1088. Y., Zanuy, S., 2001. Spawning induction of individual European sea bass females 1402
1317 Carrillo, M., Bromage, N., Zanuy, S., Serrano, R., Prat, F., 1989. The effect of (Dicentrarchus labrax) using different GnRHa-delivery systems. Aquaculture 1403
1318 modifications in photoperiod on spawning time, ovarian development and egg 202, 221–234. 1404
1319 quality in the sea bass (Dicentrarchus labrax L.). Aquaculture 81, 351–365. Gardiner, D.M., 1978. Utilisation of extracellular glucose by spermatozoa of two 1405
1320 Christen, R., Gatti, J.-L., Billard, R., 1987. Trout sperm motility. The transient viviparous fishes. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 59, 165– 1406
1321 movement of trout sperm is related to changes in the concentration of ATP 168. 1407
1322 following the activation of the flagellar movement. Eur. J. Biochem. 166, 667–
D
Geffen, A.J., Frayer, O., 1993. Retention of sperm motility in turbot Scophthalmus 1408
1323 671. maximus L.: the effects of time from activation, thermal shock and adenosine 1409
1324 Christensen, M.E., Rattner, J.B., Dixon, G.H., 1984. Hyperacetylation of histone H4 triphosphate levels. Aquacult. Fish. Manag. 24, 203–209. 1410
TE
1325 promotes chromatin decondensation prior to histone replacement by Gibbons, B.H., Gibbons, I.R., Baccetti, B., 1983. Structure and motility of the 9 + 0 1411
1326 protamines during spermatogenesis in rainbow trout. Nucleic Acids Res. 12, flagellum of eel spermatozoa. J. Submicrosc. Cytol. 15, 15–20. 1412
1327 4575–4592. Gillet, C., 1991. Egg production in an Artic charr (Salvelinus alpinus L.) brood stock: 1413
1328 Ciereszko, A., Dabrowski, K., 1994. Relationship between biochemical constituents effects of temperature on the timing of spawning and the quality of eggs. Aquat. 1414
1329 of fish semen and fertility: the effect of short-term storage. Fish Physiol. Living Resour. 4, 109–116. 1415
1330 Biochem. 12, 357–367. Gillet, C., Breton, B., Mikolajczyk, T., 1996. Effects of GnRHa and pimozide 1416
1331 1417
EC
Ciereszko, A., Dabrowski, K., 1995. Sperm quality and ascorbic acid concentration in treatments on the timing of ovulation and egg quality in Arctic charr
1332 rainbow trout semen are affected by dietary vitamin C: an across-season study. (Salvelinus fontinalis) at 5 and 10 °C. Aquat. Living Resour. 9, 257–263. 1418
1333 Biol. Reprod. 52, 982–988. Giraldez, A.J., Mishima, Y., Rihel, J., Grocock, R.J., Van Dongen, S., Inoue, K., Enright, 1419
1334 Ciereszko, A., Wojtczak, M., Dietrich, G.J., Kuzminski, H., Dobosz, S., in press. A lack A.J., Schier, A.F., 2006. Zebrafish MiR-430 promotes deadenylation and clearance 1420
1335 of consistent relationship between distribution of lipid droplets and egg quality of maternal mRNAs. Science 312, 75–79. 1421
1336 Q1 in hatchery-raised rainbow trout, Oncorhynchus mykiss. Aquaculture. Haffray, P., Fostier, A., Normant, Y., Fauré, A., Loir, M., Jalabert, B., Maisse, G., Le Gac, 1422
1337 Ciereszko, A., Wolfe, T.D., Dabrowski, K., 2005. Analysis of DNA damage in sea F., 1995. Influence du maintien en mer ou de la période du transfer en eau douce 1423
RR
1338 lamprey (Petromyzon marinus) spermatozoa by UV, hydrogen peroxide, and the des reproducteurs de saumon atlantique Salmo salar sur la maturation sexuelle 1424
1339 toxicant bisazir. Aquat. Toxicol. 73, 128–138. et la qualité des gamètes. Aquat. Living Resour. 8, 135–145. 1425
1340 Contreras-Sanchez, W.M., Schreck, C.B., Fitzpatrick, M.S., Pereira, C.B., 1998. Effects Harvey, B., Kelley, R.N., 1984. Short-term storage of Sarotherodon mossambicus ova. 1426
1341 of stress on the reproductive performance of rainbow trout (Oncorhynchus Aquaculture 37, 391–395. 1427
1342 mykiss). Biol. Reprod. 58, 439–447. Hayashi, H., Yamamoto, K., Yonekawa, H., Morisawa, M., 1987. Involvement of 1428
1343 Cosson, J., 2008a. The motility apparatus of fish spermatozoa. In: Alavi, S.M.H., tyrosine protein kinase in the initiation of flagellar movement in rainbow trout 1429
1344 Cosson, J.J., Coward, K., Rafiee, G. (Eds.), Fish Spermatology, Alpha Science spermatozoa. J. Biol. Chem. 262, 16692–16698. 1430
1345 International Ltd., Oxford, pp. 281–316. 1431
CO
Hazel, J.R., Williams, E.E., 1990. The role of alterations in membrane lipid
1346 Cosson, J.J., 2008b. Methods to analyse the movements of fish spermatozoa composition in enabling physiological adaptation of organisms to their 1432
1347 and their flagella. In: Alavi, S.M.H., Cosson, J.J., Coward, K., Rafiee, G. physical environment. Prog. Lipid Res. 29, 167–227. 1433
1348 (Eds.), Fish Spermatology, Alpha Science International Ltd., Oxford, U.K., Hirose, K., Machida, Y., Donaldson, E.M., 1979. Induced ovulation of Japanes 1434
1349 pp. 63–102. flounder (Limanda yokohoma) with HCG and salmon gonadotropin, with special 1435
1350 Cosson, M.-P., Billard, R., Gatti, J.-L., Christen, R., 1985. Rapid and quantitative references to changes in the quality of eggs retained in the ovarian cavity after 1436
1351 assessment of trout spermatozoa motility using stroboscopy. Aquaculture 46, ovulation. Bull. Jap. Soc. Fish. 45, 31–36. 1437
1352 71–75. Hokanson, K.E., McCormick, J.H., Jones, B.R., Tucker, J.H., 1973. Thermal 1438
UN
1353 Crespel, A., Rime, H., Fraboulet, E., Bobe, J., Fauvel, C., 2008. Egg quality in requirements for maturation, spawning, and embryo survival of the brook 1439
1354 domesticated and wild seabass (Dicentrarchus labrax): a proteomic analysis. trout, Salvelinus fontinalis. J. Fish. Res. Board Can. 30, 975–984. 1440
1355 Cybium 32, 205. Horvath, A., Urbanyi, B., 2000. The effect of cryoprotectants on the motility and 1441
1356 Dabrowski, K., Ciereszko, A., 1996. Ascorbic acid protects against male infertility in a fertilizing capacity of cryopreserved African catfish Clarias gariepinus (Burchell 1442
1357 teleost fish. Experientia 52, 97–100. 1822) sperm. Aquacult. Res. 2000. 31, 317–324. 1443
1358 Davies, B., Bromage, N., 2002. The effects of fluctuating seasonal and constant water Howley, C., Ho, R.K., 2000. MRNA localization patterns in zebrafish oocytes. Mech. 1444
1359 temperatures on the photoperiodic advancement of reproduction in female Dev. 92, 305–309. 1445
1360 rainbow trout, Oncorhynchus mykiss. Aquaculture 205, 183–200. Hwang, P.P., Wu, S.M., Lin, J.H., Wu, L.S., 1992. Cortisol content of eggs and larvae of 1446
1361 Devauchelle, N., Alexandre, J., Corre, N., Letty, Y., 1988. Spawning of turbot teleosts. Gen. Comp. Endocrinol. 86, 189–196. 1447
1362 (Scophthalmus maximus) in captivity. Aquaculture 69, 159–184. Inaba, K., 2008. Molecular mechanisms of the activation of flagellar 1448
1363 Dietrich, G.J., Wojtczak, M., ska, M., Dobosz, S., ski, H., Ciereszko, A., 2007. Broken motility in sperm. In: Alavi, S.M.H., Cosson, J.J., Coward, K., Rafiee, G. 1449
1364 eggs decrease pH of rainbow trout (Oncorhynchus mykiss) ovarian fluid. (Eds.), Fish spermatology, Alpha Science International Ltd., Oxford, pp. 1450
1365 Aquaculture 273, 748–751. 267–279. 1451
1366 Dinnyes, A., Urbanyi, B., Baranyai, B., Magyary, I., 1998. Chilling sensitivity of carp Inaba, K., Akazome, Y., Morisawa, M., 1993. Purification of proteasomes from 1452
1367 (Cyprinus carpio) embryos at different developmental stages in the presence or salmonid fish sperm and their localization along sperm flagella. J. Cell Sci. 104, 1453
1368 absence of cryoprotectants: work in progress. Theriogenology 50, 1–13. 907–915. 1454
1369 Dreanno, C., Cosson, J., Suquet, M., Cibert, C., Fauvel, C., Dorange, G., Billard, R., Inaba, K., Kagami, O., Ogawa, K., 1999. Tctex2-related outer arm dynein light chain 1455
1370 1999a. Effects of osmolality, morphology perturbations and intracellular is phosphorylated at activation of sperm motility. [erratum appears in Biochem 1456
1371 nucleotide content during the movement of sea bass (Dicentrarchus labrax) Biophys Res Commun 2000 Feb 24;268(3):952.]. Biochem Biophys Res Commun 1457
1372 spermatozoa. J. Reprod. Fertil. 116, 113–125. 256, 177–183. 1458
ARTICLE IN PRESS
1459 Inaba, K., Morisawa, S., Morisawa, M., 1998. Proteasomes regulate the motility of Lahnsteiner, F., Berger, B., Weismann, T., Patzner, R.A., 1998. Determination of 1545
1460 salmonid fish sperm through modulation of cAMP-dependent phosphorylation semen quality of the rainbow trout, Oncorhynchus mykiss, by sperm motility, 1546
1461 of an outer arm dynein light chain. J. Cell Sci. 111, 1105–1115. seminal plasma parameters, and spermatozoal metabolism. Aquaculture 163, 1547
1462 Ingermann, R.L., 2008. Energy metabolism and respiration in fish spermatozoa. In: 163–181. 1548
1463 Alavi, S.M.H., Cosson, J.J., Coward, K., Rafiee, G. (Eds.), Fish spermatology. Alpha Lahnsteiner, F., Patzner, R.A., Weismann, T., 1993. Energy resources of spermatozoa 1549
1464 Science International Ltd, Oxford, UK, pp. 241–266. of the rainbow trout Oncorhynchus mykiss (Piisces, Teleostei). Reprod. Nutr. Dev. 1550
1465 Itoh, A., Inaba, K., Ohtake, H., Fujinoki, M., Morisawa, M., 2003. Characterization of a 33, 349–360. 1551
1466 cAMP-dependent protein kinase catalytic subunit from rainbow trout Lee, K.-J., Dabrowski, K., 2004. Long-term effects and interactions of dietary 1552
1467 spermatozoa. Biochem. Biophys. Res. Commun. 305, 855–861. vitamins C and E on growth and reproduction of yellow perch, Perca flavescens. 1553
1468 Izquierdo, M.S., ndez-Palacios, H., Tacon, A.G.J., 2001. Effect of broodstock nutrition Aquaculture 230, 377–389. 1554
1469 on reproductive performance of fish. Aquaculture 197, 25–42. Leray, C., Nonnote, G., Roubaud, D., Leger, C., 1985. Incidence of (n 3) essential 1555
1470 Jensen, J.O., Alderdice, D.F., 1984. Effect of temperature on short-term storage of fatty acid deficiency on trout reproductive processes. Reprod. Nutr. Dev. 25, 1556
1471 eggs and sperm of chum salmon. Aquaculture 37, 251–265. 567–581. 1557
1472 Jin, Z.X., Inaba, K., Manaka, K., Morisawa, M., Hayashi, H., 1994a. Monoclonal Linhart, O., Billard, R., 1995. Survival of ovulated oocyte of the European catfish 1558
1473 antibodies against the protein complex that contains the flagellar movement- (Silurus glanis) after in vivo and in vitro storage or exposure to saline solutions 1559
F
1474 initiating phosphoprotein of oncorhynchus keta. J. Biochem. (Tokyo). 115, 885– and urine. Aquat. Living Resour. 8, 317–322. 1560
1475 890. Mansour, N., Lahnsteiner, F., Patzer, R.A., 2007. Distribution of lipid droplets is an 1561
1476 Jin, Z.X., Nakajima, T., Morisawa, M., Hayashi, H., 1994b. Isolation and properties of a indicator of egg quality in brown trout, Salmo trutta fario. Aquaculture 273, 1562
OO
1477 protein complex containing flagellar movement-initiating phosphoprotein from 744–747. 1563
1478 testes of a white salmon. J. Biochem. (Tokyo). 115, 552–556. Marian, T., Krasznai, Z., Balkay, L., Balazs, M., Emri, M., Bene, L., Tron, L., 1993. Hypo- 1564
1479 Kane, D.A., Kimmel, C.B., 1993. The zebrafish midblastula transition. Development osmotic shock induces an osmolality-dependent permeabilization and 1565
1480 119, 447–456. structural changes in the membrane of carp sperm. J. Histochem. Cytochem. 1566
1481 Kho, K.H., Tanimoto, S., Inaba, K., Oka, Y., Morisawa, M., 2001. Transmembrane cell 41, 291–297. 1567
1482 signaling for the initiation of trout sperm motility: roles of ion channels and Marino, G., Panini, E., Longobardi, A., Mandich, A., Finoia, M.G., Zohar, Y., Mylonas, 1568
1483 membrane hyperpolarization for cyclic AMP synthesis. Zoolog. Sci. 18, 919–928. C.C., 2003. Induction of ovulation in captive-reared dusky grouper, Epinephelus 1569
1484 Kime, D.E., Ebrahimi, M., Nysten, K., Roelants, I., Rurangwa, E., Moore, H.D.M., marginatus (Lowe, 1834), with a sustained-release GnRHa implant. Aquaculture 1570
PR
1485 Ollevier, F., 1996. Use of computer assisted sperm analysis (CASA) for 219, 841–858. 1571
1486 monitoring the effects of pollution on sperm quality of fish; application to the Martinez-Pastor, F., Cabrita, E., Soares, F., Anel, L., Dinis, M.T., 2008. Multivariate 1572
1487 effect of heavy metals. Aquat. Toxicol. 36, 223–237. cluster analysis to study motility activation of Solea senegalensis spermatozoa: a 1573
1488 King, H.R., Pankhurst, N.W., Watts, M., Pankhurst, P.M., 2003. Effect of elevated model for marine teleosts. Reproduction 135, 449–459. 1574
1489 summer temperatures on gonadal steroid production, vitellogenesis and egg McEvoy, L.-A., 1984. Ovulatory rythms and over-ripening of eggs in cultivated 1575
1490 quality in female Atlantic salmon. J. Fish Biol. 63, 153–167. turbot, Scophtalmus maximus L. J. Fish Biol. 24, 437–448. 1576
1491 Kjørsvik, E., Hoehne-Reitan, K., Reitan, K.I., 2003. Egg and larval quality criteria as McLay, D.W., Clarke, H.J., 2003. Remodelling the paternal chromatin at fertilization 1577
1492 predictive measures for juvenile production in turbot (Scophthalmus maximus in mammals. Reproduction 125, 625–633. 1578
1493 L.). Aquaculture 227, 9–20. Mishra, S., Murphy, L.C., Murphy, L.J., 2006. The prohibitins: emerging roles in
D 1579
1494 Kjörsvik, E., Mangor-jensen, A., Homefjord, I., 1990. Egg quality in marine fishes. diverse functions. J. Cell Mol. Med. 10, 353–363. 1580
1495 Adv. Marine Biol. 26, 71–113. Miura, T., Yamauchi, K., Takahashi, H., Nagahama, Y., 1992. The role of hormones in 1581
1496 Knoll-Gellida, A., Andre, M., Gattegno, T., Forgue, J., Admon, A., Babin, P.J., 2006. the acquisition of sperm motility in salmonid fish. J. Exp. Zool. 261, 359–363. 1582
TE
1497 Molecular phenotype of zebrafish ovarian follicle by serial analysis of gene Mommsen, T., Korsgaard, B., 2008. Vitellogenesis. In: Rocha, M.J., Arukwe, A., 1583
1498 expression and proteomic profiling, and comparison with the transcriptomes of Kapoor, B.G. (Eds.), Fish Reproduction Science Publishers, Enfield, pp. 1–36. 1584
1499 other animals. BMC Genomics 7, 46. Morisawa, M., Hayashi, H., 1985. Phosphorylation of a 15 K axonemal protein is the 1585
1500 Koldras, M., Loir, M., Maisse, G., Le Gac, F., 1996. Study of the composition of seminal trigger initiating trou sperm motility. Biomed. Res. 6, 181–184. 1586
1501 fluid and of sperm motility along the genital tract, during a spawning season, in Morisawa, M., Okuno, M., 1982. Cyclic AMP induces maturation of trout sperm 1587
1502 the rainbow trout (Oncorhynchus mykiss). Aquat. Living Resour. 9, 337–345. axoneme to initiate motility. Nature 295, 703–704. 1588
1503 1589
EC
Kopeika, J., Kopeika, E., Zhang, T., Rawson, D.M., Holt, W.V., 2003. Detrimental Morisawa, M., 1994. Cell signaling mechanisms for sperm motility. Zoolog. Sci. 11,
1504 effects of cryopreservation of loach (Misgurnus fossilis) sperm on subsequent 647–662. 1590
1505 embryo development are reversed by incubating fertilised eggs in caffeine. Morisawa, M., Ishida, K., 1987. Short-term changes in levels of cyclic AMP, 1591
1506 Cryobiology 46, 43–52. adenylate cyclase, and phosphodiesterase during the initiation of sperm 1592
1507 Kopeika, J., Kopeika, E., Zhang, T., Rawson, D.M., Holt, W.V., 2004. Effect of DNA motility in rainbow trout. J. Exp. Zool. 242, 199–204. 1593
1508 repair inhibitor (3-aminobenzamide) on genetic stability of loach (Misgurnus Morisawa, M., Suzuki, K., 1980. Osmolality and potassium ion: their roles in 1594
1509 fossilis) embryos derived from cryopreserved sperm. Theriogenology 61, 1661– initiation of sperm motility in teleosts. Science 210, 1145–1147. 1595
RR
1510 1673. Morisawa, M., Tanimoto, S., Ohtake, H., 1992. Characterization and partial 1596
1511 Krasznai, Z., Marian, T., Izumi, H., Damjanovich, S., Balkay, L., Tron, L., Morisawa, M., purification of sperm-activating substance from eggs of the herring, Clupea 1597
1512 2000. Membrane hyperpolarization removes inactivation of Ca2+ channels, palasii. J. Exp. Zool. 264, 225–230. 1598
1513 leading to Ca2+ influx and subsequent initiation of sperm motility in the Morisawa, S., Ishida, K., Okuno, M., Morisawa, M., 1993. Roles of pH and cyclic 1599
1514 common carp. Proc. Natl. Acad. Sci. USA 97, 2052–2057. adenosine monophosphate in the acquisition of potential for sperm motility 1600
1515 Labbe, C., Crowe, L.M., Crowe, J.H., 1997. Stability of the lipid component of trout during migration from the sea to the river in chum salmon. Mol. Reprod. Dev. 1601
1516 sperm plasma membrane during freeze–thawing. Cryobiology 34, 176–182. 34, 420–426. 1602
1517 Labbe, C., Loir, M., Kaushik, S., Maisse, G., 1993. The influence of both rearing 1603
CO
Morisawa, S., Morisawa, M., 1986. Acquisition of potential for sperm motility in
1518 temperature and dietary lipid origin on fatty acid composition of rainbow trout and chum salmon. J. Exp. Biol. 126, 89–96. 1604
1519 spermatozoan polar lipids in rainbow trout (Oncorhynchus mykiss). Effect on Morisawa, S., Morisawa, M., 1988. Induction of potential for sperm motility by 1605
1520 sperm cryopreservation tolerance. Fish Nutrition in Practice INRA, Paris, pp. bicarbonate and pH in rainbow trout and chum salmon. J. Exp. Biol. 136, 13–22. 1606
1521 49–59. Mounib, M.S., 1967. Metabolism of pyruvate, acetate and glyoxylate by fish sperm. 1607
1522 Labbe, C., Maisse, G., 1996. Influence of rainbow trout thermal acclimation on sperm Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 20, 987–992. 1608
1523 cryopreservation: relation to change in the lipid composition of the plasma Muller, K., Labbe, C., Zachowski, A., 1994. Phospholipid transverse asymmetry 1609
1524 membrane. Aquaculture 145, 281–294. in trout spermatozoa plasma membrane. Biochim. Biophys. Acta 1192, 21– 1610
UN
1525 Labbe, C., Maisse, G., 2001. Characteristics and freezing tolerance of brown trout 26. 1611
1526 spermatozoa according to rearing water salinity. Aquaculture 201, 287–299. Muller, K., Muller, P., Pincemy, G., Kurz, A., Labbe, C., 2008. Characterization of 1612
1527 Labbe, C., Maisse, G., Muller, K., Zachowski, A., Kaushik, S., Loir, M., 1995. Thermal sperm plasma membrane properties after cholesterol modification: 1613
1528 acclimation and dietary lipids alter the composition, but not fluidity, of trout consequences for cryopreservation of rainbow trout spermatozoa. Biol. 1614
1529 sperm plasma membrane. Lipids 30, 23–33. Reprod. 78, 390–399. 1615
1530 Labbe, C., Martoriati, A., Devaux, A., Maisse, G., 2001. Effect of sperm Munoz-Guerra, S., Azorin, F., Casas, T., Marcet, X., Maristany, M.A., Roca, J., Subirana, 1616
1531 cryopreservation on sperm DNA stability and progeny development in J.A., 1982. Structural organization of sperm chromatin from the fish Carassius 1617
1532 rainbow trout. Mol. Reprod. Dev. 60, 397–404. auratus. Exp. Cell Res. 137, 47–53. 1618
1533 Lahnsteiner, F., Patzner, R., Weismann, T., 1992. Monosaccharides as energy Mylonas, C.C., Hinshaw, J.M., Sullivan, C.V., 1992. GnRHa-induced ovulation of 1619
1534 resources during motility of spermatozoa in Leuciscus cephalus (Cyprinidae, brown trout (Salmo trutta) and its effect on egg quality. Aquaculture 106, 379– 1620
1535 Teleostei). Fish Physiol. Biochem. 10, 283–289. 392. 1621
1536 Lahnsteiner, F., Patzner, R.A., 1998. Sperm motility of the marine teleosts Boops Nagler, J.J., 2000. In vivo treatment with cycloheximide or actinomycin D inhibits 1622
1537 boops, Diplodus sargus, Mullus barbatus and Trachurus mediterraneus. J. Fish Biol. early embryonic development in rainbow trout (Oncorhynchus mykiss). Fish 1623
1538 52, 726–742. Physiol. Biochem. 22, 61–66. 1624
1539 Lahnsteiner, F., Patzner, R.A., 2008. Sperm morphology and ultrastructure in fish. In: Oda, S., Igarashi, Y., Manaka, K., Koibuchi, N., SakaiSawada, M., Sakai, K., Morisawa, 1625
1540 Alavi, S.M.H., Cosson, J.J., Coward, K., Rafiee, G. (Eds.), Fish spermatology Alpha M., Ohtake, H., Shimizu, N., 1998. Sperm-activating proteins obtained from the 1626
1541 Science International Ltd., Oxford, pp. 2–61. herring eggs are homologous to trypsin inhibitors and synthesized in follicle 1627
1542 Lahnsteiner, F., 2000. Morphological, physiological and biochemical parameters cells. Dev. Biol. 204, 55–63. 1628
1543 characterizing the over-ripening of rainbow trout eggs. Fish Physiol. Biochem. Ogier de Baulny, B., Labbe, C., Maisse, G., 1999. Membrane integrity, mitochondrial 1629
1544 23, 107–118. activity, ATP content, and motility of the European catfish (Silurus glanis) 1630
ARTICLE IN PRESS
1631 testicular spermatozoa after freezing with different cryoprotectants. Stoddard, J.W., Parsons, J.E., Nagler, J.J., 2005. Early onset of embryonic mortality in 1700
1632 Cryobiology 39, 177–184. sub-fertile families of rainbow trout (Oncorhynchus mykiss). Reprod. Fertil. Dev. 1701
1633 Ogier de Baulny, B., Le Vern, Y., Kerboeuf, D., Maisse, G., 1995. ATP content and flow 17, 785–790. 1702
1634 cytometric evaluation of mitochondrial activity and membrane integrity in Stratholt, M.L., Donaldson, E.M., Liley, N.R., 1997. Stress induced elevation of plasma 1703
1635 fresh and cryopreserved trout spermatozoa: effect of different cryoprotectants. cortisol in adult female coho salmon (Oncorhynchus kisutch), is reflected in egg 1704
1636 Cryobiology 32, 581. cortisol content, but does not appear to affect early development. Aquaculture 1705
1637 Ogier de Baulny, B., Le Vern, Y., Labbe, C., Maisse, G., 1997. Cryopreservation of fish 158, 141–153. 1706
1638 semen: why does the most effective cryoprotectant differ from one species to Suquet, M., Dreanno, C., Dorange, G., Normant, Y., Quemener, L., Gaignon, J.L., 1707
1639 another. Cryobiology 35, 342. Billard, R., 1998. The ageing phenomenon of turbot spermatozoa: effects on 1708
1640 Ohkawa, K., Inaba, K., Morisawa, M., 1997. Purification and characterization of 26S morphology, motility and concentration, intracellular ATP content, fertilization, 1709
1641 proteasome from sperm flagella of chum salmon and its roles in the regulation and storage capacities. J. Fish Biol. 52, 31–41. 1710
1642 of sperm motility. Biomed. Res.—Tokyo 18, 353–363. Tagawa, M., Hirano, T., 1987. Presence of thyroxine in eggs and changes in its 1711
1643 Ohta, T., Kato, K.H., Abe, T., Takeuchi, T., 1993. Sperm morphology and distribution content during early development of chum salmon, Oncorhynchus keta. Gen. 1712
1644 of intramembranous particles in the sperm heads of selected freshwater Comp Endocrinol. 68, 129–135. 1713
1645 teleosts. Tissue Cell 25, 725–735. Takeuchi, T., Watanabe, T., 1982. Effects of various polyunsaturated fatty acids on 1714
F
1646 Palace, V.P., Werner, J., 2006. Vitamins A and E in the maternal diet influence egg growth and fatty acid compositions of rainbow trout Salmo gairdneri, coho 1715
1647 quality and early life stage development in fish: a review. Scientia Marina 70, salmon Onchorhynchus kisutch, and chum salmon Onchorhynchus keta. Bull. Jpn. 1716
1648 41–57. Soc. Sci. Fish. 48, 1745–1752. 1717
OO
1649 Pankhurst, N.W., Purser, G.J., Van der Kraak, G., Thomas, P.M., Forteath, G.N.R., 1996. Tata, J.R., 1986. Coordinated assembly of the developing egg. Bioessays 4, 197–201. 1718
1650 Effect of holding temperature on ovulation, egg fertility, plasma levels of Terner, C., 1962. Oxidative and biosynthetic reactions in spermatozoa. In: Bishop 1719
1651 reproductive hormones and in vitro ovarian steroidogenesis in the rainbow D.W. (Ed.), Spermatozoan Motility, American asociation for the Advancement of 1720
1652 trout Oncorhynchus mykiss. Aquaculture 146, 227–290. Science, Washington D.C., pp. 89–98. 1721
1653 Patino, R., Sullivan, C.V., 2002. Ovarian follicle growth, maturation, and ovulation in Terner, C., Korsh, G., 1963a. The biosynthesis os fatty acids of glycerides and 1722
1654 teleost fish. Fish Physiol. Biochem. 26, 57–70. phosphatides by isolated spermatozoa of the rainbow trout. J. Cell Comp. 1723
1655 Pelegri, F., 2003. Maternal factors in zebrafish development. Dev. Dyn. 228, 535– Physiol. 62, 251–256. 1724
1656 554. Terner, C., Korsh, G., 1963b. The oxydative metabolism of pyruvate, acetate and 1725
PR
1657 Perchec, G., Jeulin, C., Cosson, J., André, F., Billard, R., 1995. Relationship between glucose in isolated fish spermatozoa. J. Cell Comp. Physiol. 62, 243–249. 1726
1658 sperm ATP content and motility of carp spermatozoa. J. Cell Sci. 108, 747– Tubbs, C., Thomas, P., 2008. Functional characteristics of membrane progestin 1727
1659 753. receptor alpha (mPR[alpha]) subtypes: a review with new data showing 1728
1660 Pustowka, C., McNiven, M.A., Richardson, G.F., Lall, S.P., 2000. Source of dietary lipid mPR[alpha] expression in seatrout sperm and its association with sperm 1729
1661 affects sperm plasma membrane integrity and fertility in rainbow trout motility. Steroids 73, 935–941. 1730
1662 Oncorhynchus mykiss (Walbaum) after cryopreservation. Aquacult. Res. 31, Tveiten, H., Solevag, S., Johnsen, H., 2001. Holding temperature during the breeding 1731
1663 297–305. season influences final maturation and egg quality in common wolffish. J. Fish 1732
1664 Rime, H., Guitton, N., Pineau, C., Bonnet, E., Bobe, J., Jalabert, B., 2004. Post-ovulatory Biol. 58. 1733
1665 ageing and egg quality: a proteomic analysis of rainbow trout coelomic fluid. van der Meeren, T., Ivannikov, V.P., 2006. Seasonal shift in spawning of Atlantic cod 1734
1666 Reprod. Biol. Endocrinol. 2, 26.
D (Gadus morhua L.) by photoperiod manipulation: egg quality in relation to 1735
1667 Robitaille, P.-M.L., Mumford, K.G., Brown, G.G., 1987. 31P nuclear magnetic temperature and intensive larval rearing. Aquac. Res. 37, 898–913. 1736
1668 resonance study of trout spermatozoa at rest, after motility, and during short Wallace, R., Selman, K., 1981. Cellular and dynamic aspects of oocyte growth in 1737
TE
1669 term storage. Biochem. Cell Biol. 65, 474–485. teleosts. Am. Zool. 21, 325–343. 1738
1670 Rothbard, S., Rubinshtein, I., Gelman, E., 1996. Storage of common carp. Cyprinus Wallace, R.A., Selman, K., 1985. Major protein changes during vitellogenesis and 1739
1671 carpio L., eggs for short durations.. Aquac. Res. 27, 175–181. maturation of Fundulus oocytes. Dev. Biol. 110, 492–498. 1740
1672 Rurangwa, E., Volckaert, F.A., Huyskens, G., Kime, D.E., Ollevier, F., 2001. Quality Watanabe, T., 1982. Lipid nutrition in fish. Comp. Biochem. Physiol. B 73, 3–15. 1741
1673 control of refrigerated and cryopreserved semen using computer-assisted Weigel, K.A., 2006. Prospects for improving reproductive performance through 1742
1674 sperm analysis (CASA), viable staining and standardized fertilization in genetic selection. Anim. Reprod. Sci. 96, 323–330. 1743
1675 1744
EC
African catfish (Clarias gariepinus). Theriogenology 55, 751–769. Werthemer, A.C., 1984. Maturation success of Pink salmon (Oncorhynchus
1676 Sakai, K., Nomura, M., Oto, H., 1975. The over-ripening phenomenon of rainbow gorbuscha) and Coho salmon (O. kisutch) held under three salinity regimes. 1745
1677 trout II, Changes in the percentage of eyed eggs, hatching rate and incidence of Aquaculture 43, 195–212. 1746
1678 abnormal alevins during the process of over-ripening. Bull. Jap. Sci. Fish. 41, Withler, F.C., Morley, R.B., 1968. Effects of chilled storage on viability of stored ova 1747
1679 855–860. and sperm of sockeye and pink salmon. J. Fish. Res. Board Can. 25, 2695–2699. 1748
1680 Sakai, K., Nomura, M., Takashima, F., 1985. Characteristics of naturally spawned Yu, S., Kojima, N., Hakomori, S.I., Kudo, S., Inoue, S., Inoue, Y., 2002. Binding of 1749
1681 eggs of red sea bream. Bull. Jpn. Soc. Sci. Fish 51, 1395–1399. rainbow trout sperm to egg is mediated by strong carbohydrate-to- 1750
RR
1682 Saperas, N., Lloris, D., Chiva, M., 1993a. Sporadic appearance of histonesn histone- carbohydrate interaction between (KDN)GM3 (deaminated neuraminyl 1751
1683 like proteins, and protamines in sperm chromatin of bony fish. J. Exp. Zool. 265, ganglioside) and Gg3-like epitope. Proc. Natl. Acad. Sci. USA 99, 2854–2859. 1752
1684 575–586. Zheng, W., Strobeck, C., Stacey, N., 1997. The steroid pheromone 4-pregnen-17, 1753
1685 Saperas, N., Ribes, E., Buesa, C., Garcia Hegart, F., Chiva, M., 1993b. Differences in 20ss-diol-3-one increases fertility and paternity in goldfish. J. Exp. Biol. 200, 1754
1686 chromatin condensation during spermiogenesis in two species of fish with 2833–2840. 1755
1687 distinct protamines. J. Exp. Zool. 265, 185–194. Zietara, M.S., Slominska, E., Swierczynski, J., Rurangwa, E., Ollevier, F., Skorkowski, 1756
1688 Saudrais, C., Fierville, F., Loir, M., Le Rumeur, E., Cibert, C., Cosson, J., 1998. The use of E.F., 2004. ATP content and adenine nucleotide catabolism in african catfish 1757
1689 phosphocreatine plus ADP as energy source for motility of membrane-deprived 1758
CO
spermatozoa stored in various energetic substrates. Fish Physiol. Biochem. 30,

1690 trout spermatozoa. Cell Motil. Cytoskeleton 41, 91–106. 119–127. 1759
1691 Shields, R.J., Brown, N.P., Bromage, N.R., 1997. Blastomere morphology as a Zilli, L., Schiavone, R., Zonno, V., Storelli, C., Vilella, S., 2003. Evaluation of DNA 1760
1692 predictive measure of fish egg viability. Aquaculture 155, 1–12. damage in Dicentrarchus labrax sperm following cryopreservation. Cryobiology 1761
1693 Sower, S.A., Schreck, C.B., Donaldson, E.M., 1982. Hormone-induced ovulation of 47, 227–235. 1762
1694 Coho salmon (Oncorhynchus kisutch) held in seawater and fresh water. Can. J. Zilli, L., Schiavone, R., Zonno, V., Storelli, C., Vilella, S., 2004. Adenosine triphosphate 1763
1695 Fish. Aquat. Sci. 39, 627–632. concentration and beta-D-glucuronidase activity as indicators of sea bass semen 1764
1696 Springate, J.R.C., Bromage, N.R., Elliott, J.A.K., Hudson, D.L., 1984. The timing of quality. Biol. Reprod. 70, 1679–1684. 1765
UN
1697 ovulation and stripping and their effects on the rates of fertilization and Ziv, T., Gattegno, T., Chapovetsky, V., Wolf, H., Barnea, E., Lubzens, E., Admon, A., 1766
1698 survival to eying, hatch and swim-up in the rainbow trout (Salmo gairdneri R.). 2008. Comparative proteomics of the developing fish (zebrafish and gilthead 1767
1699 Aquaculture 43, 313–322. seabream) oocytes. Comp. Biochem. Physiol. D: Genomics Proteomics 3, 12–35. 1768
1769
View publication stats

2009 Bobeand Labbe GCEonline

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

2009 Bobeand Labbe GCEonline

Uploaded by

Copyright:

Available Formats

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

Egg and sperm quality in ﬁsh

Article in General and Comparative Endocrinology · January 2012

CRIOBIV View project

Reproduction biotechnology View project

The user has requested enhancement of the downloaded file.

General and Comparative Endocrinology xxx (2009) xxx–xxx

Contents lists available at ScienceDirect

General and Comparative Endocrinology

2 Egg and sperm quality in ﬁsh

39 1. Introduction The present review is therefore aiming at (i) brieﬂy presenting 60

46 2. Molecular and cellular characteristics of ﬁsh gametes 67

0016-6480/$ - see front matter Ó 2009 Published by Elsevier Inc.

2 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 3

262 iable depending on the species. Salmonidae spermatozoa possess a 327

4 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 5

6 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 7

8 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 9

10 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

1082 4.5. Other factors 5. Conclusions and future directions 1112

Oocyte maturation Early cleavage

J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 11

deep-freezing. Cell Tissue Res. 228, 205–218. 1252

12 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx 13

14 J. Bobe, C. Labbé / General and Comparative Endocrinology xxx (2009) xxx–xxx

spermatozoa stored in various energetic substrates. Fish Physiol. Biochem. 30,

You might also like