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Controlled reproduction in the wild European eel (Anguilla anguilla): two populations compared

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Abstract

This study aimed to describe the response variability of female silver eels in terms of gonad development and eggs production to a standardized gonadotropic treatment (Carp pituitary extracts—CPE), and to relate this variability to population characteristics. For this purpose, sexual maturation, ovulation, and fertilization were induced in two eel populations coming from different locations in Adriatic Sea (Comacchio—CM and Marano-Grado—MG lagoons), and after that, their reproductive capacity was valuated. External (Silver index—SI, Eye index—EI, Pectoral fin length index—PFLI, Condition factor—K) and hormonal (17β-estradiol—E2, testosterone—T) parameters were measured, and some subject/group were killed for histological and lipid analysis and age determination. Morphometric parameters showed the CM-Group to have highest values of Body weight (BW), Body length (BL), and K, while MG-Group presented highest PFLI and Gonadosomatic index (GSI) values. Regarding hormonal analysis, the CM-Group showed significantly higher T and E2 levels than the MG-Group, both groups showed considerably rapid increase at T5 (5th injection). A positive trend in gonadal development was found through histological evaluation; a more regular maturation was observed in the MG-Group, whereas the CM-Group presented an exponential oocytes development starting from T10 (10th week), which led to an anticipated spawning. Lipid content showed significant differences in T0 (start study), post-ovulation, and Control (30th week) between CM and MG eels. As to zootechnical performances, while MG eels released spontaneously into the water, the CMs were stripped in order to check ovulation. The MG eels were statistically the most productive with 40.1 ± 6.33 % BW of eggs released. Furthermore, CM females ovulated mainly between the 19th and 22nd week (77.8 % spawned eels) instead in the MG’s ovulation goes from the 24th to the 28th week (100 % spawned eels). As fertilization is of concern, in both groups fertilized eggs were obtained with no difference in larvae production. These results seem to indicate that bigger dimensions, higher K, and larger lipid content (Comacchio eels) could fasten gonadic maturation without positively influencing reproductive performance of animals, both in term of quantity and quality of produced eggs. Smaller females with a highest SI (Marano-Grado eels) presented a more regular gonadic development, leading the animals to spontaneous spawning.

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Abbreviations

BL:

Body length

BW:

Body weight

BWI:

Body weight index

Control-Group:

Control eels

CM-Group:

Comacchio eels

CPE:

Carp pituitary extracts

DHP:

17α,20β-dihydroxy-4-pregnen-3-one

E2:

17β-estradiol

EDh:

Eye diameter horizontal

EDv:

Eye diameter vertical

EI:

Eye index

GSI:

Gonadosomatic index

H&E:

Hematoxylin and eosin

hCG:

Human chorionic gonadotropin

IBW:

Initial body weight

K:

Condition factor

MG-Group:

Marano-Grado eels

PFL:

Pectoral fin length

PFLI:

Pectoral fin length index

RIA:

Radio-immuno assay

SI:

Silver index

SPE:

Salmon pituitary extracts

T:

Testosterone

References

  • Aarestrup K, Okland F, Hansen MM, Righton D, Gargan P, Castonguay M, Benrnatchez L, Howey P, Sparholt H, Pedersen MI, McKinley RS (2009) Oceanic spawning migration of the European Eel (Anguilla anguilla). Science 325:1660

    Article  PubMed  CAS  Google Scholar 

  • Aroua S, Schmitz M, Baloche S, Vidal B, Rousseau K, Dufour S (2005) Endocrine evidence that silvering, a secondary metamorphosis in the eel, is a pubertal rather than a metamorphic event. Neuroendocrinology 82:221–232

    Article  PubMed  CAS  Google Scholar 

  • Boetius I, Boetius J (1985) Lipid and protein content in Anguilla anguilla during growth and starvation. Dana 4:1–17

    Google Scholar 

  • Bono G, Cairoli F, Tamanini C, Abrate L (1983) Progesterone, estrogen, LH, FSH and PRL concentrations in plasma during estrous cycle in goat. Reprod Nutr Dev 23:217–222

    Article  PubMed  CAS  Google Scholar 

  • Burgerhout E, Brittijn SA, Kurwie T, Decker P, Dirks RP, Palstra AP, Spaink HP, van den Thillart GEEJM (2011) First artificial hybrid of the eel species Anguilla australis and Anguilla Anguilla. BMC Dev Biol 11:16

    Article  PubMed  CAS  Google Scholar 

  • Burzawa-Gerard E, Dumas-Vidal A (1991) Effects of 17β-estradiol and carp gonadotropin on vitellogenesis in normal hypophysectomized European silver female eel (Anguilla anguilla L.) employing a homologous radioimmunoassay for vitellogenin. Gen Comp Endocrinol 84:264–276

    Article  PubMed  CAS  Google Scholar 

  • Chiba H, Iwatsuki K, Hayami K, Hara A, Yamuchi K (1994) Changes in serum steroid hormones and vitellogenin levels in cultured female European eel Anguilla anguilla during artificially induced ovarian development. J World Aquac Soc 25(4):553–560

    Article  Google Scholar 

  • Cosolo M, Utmar P, Roppa F, Sponza S (2009) Interactions between fish resources and cormorants Phalacrocorax carbo in the Grado and Marano Lagoon (NE Italy). Acrocephalus 30(149):17–23

    Google Scholar 

  • Cottril RA, McKinley RS, Van der Kraak G, Dutil JD, Reid KB, McGrath KJ (2001) Plasma non-esterified fatty acid profiles and 17β-oestradiol levels of juvenile immature and maturing adult America eels in the St Lawrence River. J Fish Biol 50:364–379

    Article  Google Scholar 

  • De Leo GA, Gatto M (1996) Trends in Vital rates of the European eel: evidence for density dependence? Ecol Appl 6(4):1281–1294

    Article  Google Scholar 

  • Dufour S, van den Thillart G (2009) Reproduction capacity of European Eels. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning Migration of the European Eel. Reproduction index, a useful tool for conservation management, vol 30. Springer, New York, USA, pp 465–473

  • Durif C, Gosset C, Rives J, Travade F, Elie P (2003) Behavioral study of downstream migrating eels by radio-telemetry at a small hydroelectric power plant. In: Dixon DA (ed) Biology, management and protection of catadromous eels. American Fisheries Society, Symposium, Bethesda, pp 343–356

    Google Scholar 

  • Durif C, Dufour S, Elie P (2005) The silvering process of the Anguilla anguilla: a new classification from the yellow resident to the silver migrating stage. J Fish Biol 66:1025–1043

    Article  Google Scholar 

  • Durif CMF, Dufour S, Elie P (2006) Impact of silvering stage, age, body size and condition on the reproductive potential of the European eel. Mar Ecol Prog Ser 327:171–181

    Article  Google Scholar 

  • Durif CMF, van Ginneken V, Dufour S, Muller T, Elie P 2009 Seasonal Evolution and Differences in Silvering Eels from Different Locations. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning Migration of the European Eel. Reproduction index, a useful tool for conservation management, vol 30. Springer, New York, USA, pp 13–38

  • EELREP (2006) Estimation of the reproduction capacity of European eel. Final report, EU Project, EELREP, Q5RS-2001-01836. Leiden University

  • Folch BJ, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Fontaine YA (1994) L’argenture de l’anguille: metamorphose, anticipation, adaptation. Bull Fr Peche Piscic 335:171–185

    Article  Google Scholar 

  • Gaiani R, Chiesa F, Mattioli M, Nannetti G, Galeati G (1984) Androsteneidione and T testosterone concentrations in plasma and milk of the cow throughout pregnancy. J Reprod Fertil 70:55

    Article  PubMed  CAS  Google Scholar 

  • Gelli F (2011) Per uno studio di fattibilità della produzione di anguilla marinata delle valli del Friuli Venezia Giulia. In: Prime ricerche svolte su anguilla europea (Anguilla anguilla), Centro Stampa Regione Emilia-Romagna, Bologna (Italy) pp 50–75

  • Han YS, Liao IC, Tzeng WN, Huang YS, Yu JYL (2003a) Serum estradiol-17β and testosterone levels during silvering in wild Japanese eel Anguilla japonica. Comp Biochem Physiol 136:913–920

    Article  Google Scholar 

  • Han YS, Liao IC, Huang YS, He JT, Chang CW, Tzeng WN (2003b) Synchronous changes of morphology and gonadal development of silvering Japanese eel Anguilla japonica. Aquaculture 219:783–796

    Article  Google Scholar 

  • Holthaus KB, Savorelli F, Gelli F, Modugno S, Trentini PL, Tasselli A (2011) Il comprensorio vallivo di Comacchio e l’indice di maturità sessuale su campioni di anguille. In: Tasselli A, Gelli F, Mordenti O (eds) Prime ricerche svolte su anguilla europea (Anguilla anguilla). Centro Stampa Regione Emilia-Romagna, Bologna (Italy), pp 19–28

  • Huang YS, Sbaihi M, Le Belle N, Dufour S (2001) Combination of testosterone with cortisol stimulates the silvering of female European eel (Anguilla anguilla. L). In: Yu JYT (ed) Proceedings of 4th Congress of the Asian and Oceania society for comparative endocrinology. Institute of Zoology, Academia Sinica, Taipei, pp 215–222

  • Ijiri S, Kazeto Y, Takeda N, Chiba H, Adachi S, Yamauchi K (1995) Changes in serum steroid hormones and steroidogenic ability of ovarian follicles during artificial maturation of cultivated Japanese eel, Anguilla japonica. Aquaculture 135:3–16

    Article  Google Scholar 

  • Ijiri S, Kayaba T, Takeda N, Tachiki H, Adachi S, Yamauchi K (1998) Pretreatment reproductive stage and oocyte development induced by salmon pituitary homogenate in the Japanese eel Anguilla japonica. Fish Sci 64:531–537

    CAS  Google Scholar 

  • Ijiri S, Tsukamoto K, Chow S, Kurogi H, Adachi S, Tanaka H (2011) Controlled reproduction in the Japanese eel (Anguilla japonica), past and present. Aquac Eur 36(2):13–17

    Google Scholar 

  • Kagawa H (2005) Estimation of gonadal status of Japanese female eel Anguilla japonica by a single injection of salmon pituitary extract. Fish Sci 71:1084–1090

    Article  CAS  Google Scholar 

  • Kamei H, Kaneko T, Aida K (2006) Steroidogenic activities of follicle-stimulating hormone in the ovary of Japanese eel, Anguilla japonica. Gen Comp Endocrinol 146:83–90

    Article  PubMed  CAS  Google Scholar 

  • Larsson P, Hamrin S, Okla A (1990) Fat content as a factor inducing migratory behavior in the eel (Anguilla anguilla L.) to the Sargasso Sea. Naturwissenschaften 77:488–490

    Article  Google Scholar 

  • Matsubara H, Lokman PM, Kazeto Y, Adachi S, Yamauchi K (2005) Serum steroid profiles in artificially maturing female Japanese eel, Anguilla japonica. Aquaculture 243:393–402

    Article  CAS  Google Scholar 

  • Melia P, Bevacqua D, Crivelli AJ, Panfili J, De Leo GA, Gatto M (2006) Sex differentiation of the European eel in brackish and freshwater environments: a comparative analysis. J Fish Biol 69:1228–1235

    Article  Google Scholar 

  • Messaouri H, Baloche S, Leloup-Hatey J, Burzawa-Gerard E (1991) Hepatic 17β-estradiol receptors and vitellogenesis in Anguilla anguilla L. after treatment by 17β-estradiol alone associated with bovine growth hormone. Gen Comp Endocrinol 82:238

    Google Scholar 

  • Mordenti O, Di Biase A, Sirri R, Modugno S, Tasselli A (2012) Induction of sexual maturation in wild female European eel (Anguilla anguilla) in darkness and light conditions. The Israeli Journal of Aquaculture—Bamidgeh (in press)

  • Ohta H, Kagawa H, Tanaka H, Okuzawa K, Hirose K (1996) Changes in fertilization and hatching rates with time after ovulation induced by 17, 20β-dihydroxy-4- pregnen-3-one in the Japanese eel, Anguilla japonica. Aquaculture 139:291–301

    Article  CAS  Google Scholar 

  • Ohta H, Kagawa H, Tanaka H, Okuzawa K, Iinuma N (1997) Artificial induction of maturation and fertilization in the Japanese eel, Anguilla japonica. Fish Physiol Biochem 17:163–169

    Article  CAS  Google Scholar 

  • Okamura A, Yamada Y, Yokouchi K, Horie N, Mikawa N, Utoh T, Tanaka S, Tsukamoto K (2007) A silver index for the Japaese eel (Anguilla japonica). Environ Biol Fish 80:77–89

    Article  Google Scholar 

  • Okamura A, Yamada Y, Horie N, Utoh T, Mikawa N, Tanaka S, Tsukamoto K (2008) Effects of silvering state on induced maturation and spawning in wild female Japanese eel Anguilla japonica. Fish Sci 74:642–648

    Article  CAS  Google Scholar 

  • Okamura A, Yamada Y, Mikawa N, Horie N, Utoh T, Kaneko T, Tanaka S, Tsukamoto K (2009) Growth and survival of leptocephali (Anguilla japonica) in low-salinity water. Aquaculture 296:367–372

    Article  CAS  Google Scholar 

  • Oliveira K, Hable WE (2010) Artificial maturation, fertilization, and early development of the American eel (Anguilla rostrata). Can J Zool 88:1121–1128

    Article  Google Scholar 

  • Ozaki Y, Koga H, Takahashi T, Adachi S, Yamauchi K (2008) Lipid content and fatty acid composition of muscle, liver, ovary and eggs of captive-reared and wild silver Japanese eel Anguilla japonica during artificial maturation. Fish Sci 74:362–371

    Article  CAS  Google Scholar 

  • Palstra AP, van den Thillart GEEJM (2009) Artificial maturation and reproduction of the European eel. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European Eel. Reproduction index, a useful tool for conservation management, vol 30. Springer, New York, pp 309–331

    Chapter  Google Scholar 

  • Palstra A, van den Thillart GEEJM (2010) Swimming physiology of European eels (Anguilla anguilla L.): energetic costs and effects on sexual maturation and reproduction. Fish Physiol Biochem 36:297–322

    Article  PubMed  CAS  Google Scholar 

  • Palstra AP, Cohen EGH, Niemantsverdriet PRW, van Ginneken VJT, van den Thillart GEEJM (2005) Artificial maturation and reproduction of European silver eel: development of oocytes during final maturation. Aquaculture 249:533–547

    Article  Google Scholar 

  • Palstra AP, van Ginneken VJT, van den Thillart GEEJM (2009) Effect of swimming on silvering and maturation of the European eel, Anguilla Anguilla L. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European Eel. Reproduction index, a useful tool for conservation management, vol 30. Springer, New York, pp 229–251

    Chapter  Google Scholar 

  • Pedersen BH (2003) Induced sexual maturation of the European eel Anguilla anguilla and fertilisation of the eggs. Aquaculture 224:323–338

    Article  Google Scholar 

  • Pedersen BH (2004) Fertilisation of eggs, rate of embryonic development and hatching following induced maturation of the European eel Anguilla anguilla. Aquaculture 237:461–473

    Article  Google Scholar 

  • Perez L, Penaranda DS, Dufour S, Baloche S, Palstra AP, van den Thillart GEEJM, Asturiano JF (2011) Influence of temperature regime on endocrine parameters and vitellogenesis during experimental maturation of European eel (Anguilla anguilla) females. Gen Comp Endocrinol 174:51–59

    Article  PubMed  CAS  Google Scholar 

  • Peyon P, Baloche S, Burzawa-Gerard E (1996) Potentiating effect of growth hormone on vitellogenin synthesis induced by 17β-estradiol in primary culture of female eel (Anguilla anguilla L.) hepatocytes. Gen Comp Endocrinol 102:263–273

    Article  PubMed  CAS  Google Scholar 

  • Roncarati A, Gelli F, Brunelli F, Cavallini G, Forlini L, Pignata S, Melotti P (2008) Quality traits of Comacchio Valli eels before, during and after the pickling process. In: Cakli S, Celik U, Altinelataman C (eds) 1st International congress of seafood technology, 18–21 May 2008, Izmir Turkey, pp 295–299

  • Stearns SC, Koella JC (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reactionnorms for age and size at maturity. Evolution 40(5):893–913

    Article  Google Scholar 

  • Svedäng H, Wickström H (1997) Low fat contents in female silver eels: indications of insufficient energetic stores for migration and gonadal development. J Fish Biol 50:475–486

    Article  Google Scholar 

  • Svedäng H, Neuman E, Wickström H (1996) Maturation patterns in female European eels: age and size at the silver stage. J Fish Biol 48:342–351

    Article  Google Scholar 

  • Tanaka H, Kagawa H, Ohta H (2001) Production of leptocephali of Japanese eel (Anguilla japonica) in captivity. Aquaculture 201:51–60

    Article  Google Scholar 

  • Tanaka H, Kagawa H, Ohta H, Unuma K, Nomura N (2003) The first production of glass eel in captivity: fish reproductive physiology facilitates great progress in aquaculture. Fish Physiol Biochem 28:493–497

    Article  Google Scholar 

  • van den Thillart G, Dufour S (2009) How to estimate the reproductive success of European Silver Eels. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning migration of the European Eel. Reproduction index, a useful tool for conservation management, vol 30. Springer, New York, pp 1–9

    Chapter  Google Scholar 

  • van den Thillart G, Palstra A, van Ginneken V (2009) Energy requirements of European eel for trans Atlantic spawning migration. In: van den Thillart G, Dufour S, Rankin JC (eds) Spawning Migration of the European Eel. Reproduction index, a useful tool for conservation management, vol 30. Springer, New York, pp 179–199

    Chapter  Google Scholar 

  • van Ginneken V, Maes GE (2005) The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fish 15:367–398

    Article  Google Scholar 

  • van Ginneken V, van den Thillart G (2000) Eel fat stores are enough to reach the Sargasso. Nature 403:156–157

    Article  PubMed  Google Scholar 

  • van Ginneken V, Durif C, Balm SP, Boot R, Verstegen MWA, Antonissen E, van den Thillart G (2007) Silvering of European eel (Anguilla anguilla L): seasonal changes of morphological and metabolic parameters. Anim Biol 57(1):63–77

    Article  Google Scholar 

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Acknowledgments

This study was supported by Emilia-Romagna Region, Italy. The authors are very grateful to Dr. Aldo Tasselli for his help and for supplying the female eels and for sharing his experience on wild population of the European eel. They also thank Dr. Michaela Mandelli for critical reading of the manuscript and language revision.

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  1. Department of Veterinary Medical Sciences, Bologna University, Viale Vespucci 2, 47042, Cesenatico, FC, Italy

    Oliviero Mordenti, Andrea Di Biase, Giuseppe Bastone, Rubina Sirri, Annalisa Zaccaroni & Albamaria Parmeggiani

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  1. Oliviero Mordenti
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  2. Andrea Di Biase
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  3. Giuseppe Bastone
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  4. Rubina Sirri
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Correspondence to Oliviero Mordenti.

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Mordenti, O., Biase, A.D., Bastone, G. et al. Controlled reproduction in the wild European eel (Anguilla anguilla): two populations compared. Aquacult Int 21, 1045–1063 (2013). https://doi.org/10.1007/s10499-012-9611-8

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