carpio: an Endemic Salmonid of , Northern Italy Fernando Lunelli*1, Filippo Faccenda1, Ivano Confortini2, Cristina Cappelletti1 and Francesca Ciutti1

a. b.

FIGURE 1. Figure 1. Male (a) and female (b) carpione during the spawning period.

The carpione Salmo carpio is The body shape of the carpione is Gratton and Gandolfi 2011). a strictly endemic salmonid of the characterized by a relatively small head. The carpione differs from largest lake in Italy, Lake Garda The background body color is silvery other indigenous salmonids in (volume = 49 km3, surface area = grey, with small blackish dots on the Italy, such as the marble 368 km2, maximum depth = 350 dorsal area. The species is thought Salmo (trutta) marmoratus, on the m). Salmo carpio is a medium- to be gregarious, particularly during basis of the temporal and spatial sized trout, attaining a maximum seasonal migration between spawning peculiarities of reproductive total length of 35 to 40 cm and a and foraging areas. The diet of the behavior. Eggs of the carpione are maximum weight of approximately carpione is mostly zooplankton. deposited during two spawning 500 g in the natural environment. seasons, peaking in December- Record trophy specimens might exceptionally reach 50 cm and January and July-August, in deep (50-200 m) lakebeds with one kilogram. The body shape of the carpione is characterized abundant oxygen. Many authors suggest that each specimen by a relatively small head. The background body color is reproduces either in winter or in summer, although the silvery grey, with small blackish dots on the dorsal area. During hypothesis of a unique, long spawning period has never been spawning seasons, some sexual dimorphism can be observed, verified in the species’ natural environment. with males showing a dark bronze background and blackish fins (Fig. 1). Full sexual maturity of the carpione occurs at three A Critically Endangered Species years of age in males and at four years in most females, although Carpione is considered critically endangered according some spawning may occur one year earlier (Melotto and Alessio to the Red List of Threatened Species (IUCN 2010), with 1990). The species is thought to be gregarious, particularly most important threats being overfishing, habitat deterioration during seasonal migration between spawning and foraging areas. and introduction of exotic competitor species. In detail, the The diet of the carpione is mostly zooplankton (Alessio et al. introduction of planktivorous whitefish spp. in 1918 is 1990). generally thought to have promoted the demographic decline of Genetic diversity of the carpione was investigated by the carpione. sequence analysis of the complete mitochondrial DNA control Historically carpione were caught intensively during region (mtDNA D-loop) on a relatively high number of S. spawning periods. The commercial catch was more than 20 t per carpio and S. trutta samples from Lake Garda, prompting year during the 1950s, but the population of S. carpio has been us to reconsider the proposed hypotheses on the origin and reduced drastically during the last decades (Fig. 2). Currently phylogeny of the taxon (Gandolfi et al. 2006). From a genetic the only conservation actions concerning the carpione are the viewpoint, extensive molecular screening, including sequencing prohibition of fishing during spawning periods (15 November of the complete mitochondrial DNA control region (mtDNA — 31 January and 20 June — 20 August), establishment of a D-loop) and genotyping of highly-variable microsatellite loci, minimum harvest size (30 cm), and the regulation of net size provide novel insights into phylogeny, population structure and used by fishermen (Ciutti et al. 2010). conservation status of a taxon of interest (Gandolfi et al. 2006, Conservation also goes through ex situ multiplication. In

46 DECEMBER 2012 • WORLD AQUACULTURE • WWW.WAS.ORG 2008, the CARPIOGARDA Environmental factors were project was started, funded monitored and simulated by the Autonomous Province using a multi-parameter of Trento. The project aims smart probe with remote to define rearing protocols to sensing technology. produce hatchery strains used Improvements of for rehabilitation, assess the adult feeding and rearing status of spawning areas, and conditions led to a high detect the best reintroduction production of eggs and techniques for the species. juveniles. Hatching rates were greater than 60 percent, Rearing Trials compared to early artificial A fish quarantine breeding (30 percent). There facility was specifically were problems similar to created near Lake Garda the reproductive disorder to evaluate the sanitary FIGURE 2, ABOVE. Commercial catch of wild carpione in Lake Garda, Italy. in salmon called the M74 state of wild specimens FIGURE 3, BELOW. The ZEFiRe module. syndrome. In carpione, the regarding Viral Hemorrhagic syndrome was manifest as Septicemia (VHS) and offspring mortality during Infectious Hematopoietic the yolk-sac fry phase, Necrosis (IHN), following but mortality has been European health laws reduced by adding dietary (European Parliament and supplements. the Council of the European For carpione held Union 2006). Although in captivity, anticipated there are similarities sexual maturity was 16- between carpione and other 18 months for males and salmonids, specific hatching 24 months for females. and rearing temperatures and Fish reared in captivity artificial diets were evaluated can spawn twice per year. in the quarantine facility. This is undoubtedly an Rearing tests started exceptional occurrence when from artificial breeding of compared to wild specimens, wild specimens caught in representing a peculiarity 2006. Previous attempts to in the reproductive biology catch spawners in the lake of salmonids. On the other were not successful. A light- hand, gregarious behavior dark cycle for spawners has also been observed also was tested in a modular in rearing tanks, where fish production system called tend to move in shoals. ZEFiRe — an acronym for Reared carpione Innovative Zero Energy are susceptible to some Fish Farming Research. common bacterial diseases, The ZEFiRe is an energy such as furunculosis efficient, modular system (Aeromonas salmonicida, for aquaculture that aims to Aeromonas hydrophila) and improve energy efficiency, flavobacteriosis (cold water use renewable energy, and disease, Flavobacterium have low environmental psychrophilum); water impact. Water in the system mold infections, such as can be reused repeatedly Saprolegnia spp.; and after a treatment process that uses bioremediation and parasites (Icthyobodo necator, Gyrodactylus spp.). Preliminary phytoremediation techniques (Fig. 3). A prototype system was results of experimental infection of carpione revealed high constructed to raise fish for commercial purposes. Carpione resistance to VHS, while tests for sensitivity to IHN and were reared in the ZEFiRe module in tanks where water Infectious Pancreatic necrosis (IPN) will be conducted in the temperature and light were set, simulating daily and seasonal near future. natural variations of temperature and light in Lake Garda. (CONTINUED ON PAGE 46)

WWW.WAS.ORG • WORLD AQUACULTURE • DECEMBER 2012 47 At present we in the lake, as observed have achieved a good during underwater production of eggs, fry surveys. and juveniles, with an increasing number of The Future of broodstock (Table 1). Carpione The production Study of of elevated quantities Reproductive of eggs, fry and Sites juveniles indicate the Spawning areas promise of future ex of carpione are situ multiplication characterized by the and reintroduction of presence of gravel carpione. This represents and cobbles free of an encouraging result, mud, mainly located considering this is in proximity to river the first attempt to estuaries or recent rear carpione. We are landslides from aware, however, that a mountains. Historical viable hatchery strain maps show the of S. carpio should be distribution of spawning reinforced repeatedly areas, mainly located in by wild spawners. This the northwestern part of will be a major challenge the lake for the winter in the future, given the reproductive period and scarcity of wild carpione. in the southern part for We observed good the summer one (Fig. 4). reproductive sites in The functionality our study and lake and conservation status monitoring surveys of reproductive sites FIGURE 4. A map from 1725 of reproductive sites in Lake Garda, Italy. showed a trophic was assessed during condition ranging from spring 2010 by direct and indirect measurements. Transects of oligotrophy to mesotrophy (Salmaso et al. 2009). Accordingly, the lake coast (24.5 km) were made with an underwater robotic these data allow us to hypothesize that the most severe threat camera operated at depths between 50 and 250 m. Sonar sensor factors, which led to the drastic decline of the carpione, are not measurements were conducted to investigate the geologic and related to environmental degradation but primarily to overfishing stratigraphic profile of the lake floor. during spawning periods and competition of the carpione with Gravel stratification was connected with weak streams, introduced exotic fish species. Furthermore, the occurrence of which might indicate functional reproductive sites. Indirect wild fish prone to reproduction outside the fishing prohibition measurements were able to distinguish two morphological period highlights the inefficiency of fishing period restrictions. classes of spawning areas: submerged alluvial fans and coastal Finally the available information regarding the biology of S. cliffs (Fig. 5) (Lunelli 2010). carpio are based on only a few studies, in which few individuals were analyzed. As a consequence, many aspects have not yet Reintroduction Techniques been investigated. Traditional and innovative methodologies Stocking of high numbers of alevins in past decades did not should be combined, such as radio tracking to study migration lead to an effective increase in commercial harvest of carpione. behavior, stomach content analysis to investigate food competition In deep reproductive areas, between the carpione and reintroduction will be exotic fishes, and histological conducted by positioning TABLE 1. Available carpione at present. analysis of gonads to reveal Vibert boxes containing eyed details of reproductive biology. eggs. Thereby, eggs also will Stage Number of individuals Unfortunately the small be protected from predation number of individuals caught by burbot Lota lota, a species Eggs/Fry 2012 100,000 in recent years has constrained introduced to Lake Garda Juveniles 2011 15,000 new research endeavors. around 1858. The species is Broodstock 2008-2010 400 Hopefully our research efforts a voracious predator on eggs are not too late! and can reach great depths

48 DECEMBER 2012 • WORLD AQUACULTURE • WWW.WAS.ORG Notes a. all’Adige (TN): Istituto 1 Fondazione Edmund agrario di San Michele Mach–Istituto Agrario di all’Adige. 85-86. ISSN: San Michele all’Adige. 2037-7541. www.iasma.it/ Via Edmund Mach, 1 UploadDocs/7651_FEM_ I- 38010 San Michele CTT_Rapporto_2010_03_11_ all’Adige (TN), Italy web.pdf 2 Provincia di Verona, Melotto, S. and G. Alessio. Servizio tutela faunistico 1990. Biology of carpione, ambientale, Verona, Italy Salmo carpio L., an endemic Corresponding author: species of Lake Garda (Italy). [email protected] Journal of Fish Biology 37:687-698. Gandolfi, A., S. Fantini, References F. Ciutti and M.S. Grando. Alessio, G., S. Melotto and b. 2006. Il carpione del Garda E. Oppi. 1990. Indagini (Salmo carpio): variabilità fondamentali sulla biologia genetica e relazioni del carpione, Salmo carpio filogenetiche rispetto al L., del Lago di Garda. complesso Salmo trutta. Rivista di Idrobiologia Biologia Ambientale 20:7-12. 29:51-68. Gratton, P., and A. Gandolfi. Ciutti, F., F. Lunelli, N. 2011. Composing the Merlo, I. Confortini, F. evolutionary puzzle of the Gatti and A. Gandolfi. last remains of trout (Salmo 2010. Problematiche trutta complex) diversity di conservazione del in Italy. In Advances in Carpione del Garda (Salmo Biogeography: Early Career carpio L.). Studi Trentini Conference, 23-25 September di Scienze Naturali 87:175- 2011, Oxford, UK. 177. IUCN (International Union European Parliament and the c. for Conservation of Nature) Council if the European 2010. Red List of Threatened Union. 2006. Directive Species. www.iucnredlist.org. 2006/88/EC of 24 Accessed 1 September 2010. October 2006 on animal Salmaso, N., A. Boscaini, C. health requirements for Cappelletti and F. Ciutti. aquaculture and 2009. Le condizioni di products thereof, and on salute del Lago di Garda: the prevention and control aggiornamento dello stato of certain diseases in delle conoscenze su carichi aquatic animals. Official di nutrienti algali e sulle Journal of the European componenti biologiche della Community 328:14-56. zona pelagica e litorale. Lunelli, F. 2010. The FIGURE 5. Suitable (a) and unsuitable (b) substrate for spawning and sonar Pages 49-88 In: F. Bertin reproductive sites of Garda sensor profile of the lake bottom (c). and A. Bortoli, editors. Lake ‘carpione’ (Salmo Problematiche ambientali carpio): monitoring and conservation status. In: Centro del Lago di Garda. Approfondimenti e proposte di risanamento. Trasferimento Tecnologico Rapporto 2010. San Michele Libro degli Atti: Torri del Benaco.

Traditional and innovative methodologies should be combined, such as radio tracking to study migration behavior, stomach content analysis to investigate food competition between the carpione and exotic fishes, and histological analysis of gonads to reveal details of reproductive biology. Unfortunately the small number of individuals caught in recent years has constrained new research endeavors.

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