Anfipodos

aqua-online Caprellid amphipods: An overlooked marine finfish aquaculture resource? Chris M. C. Woods * National Institute of Water and Atmospheric Research, PO Box 8602, Riccarton 8011, Christchurch, New Zealand article PACE 1 orq to View nut*ge info abstract The present review examines aspects of the known biology and ecology of caprellid amphipods and their potential suitability as a novel marine finfish feed. Caprellids are widely distributed globally and are an important secondary trophic link in many marine ecosystems.

They form an important natural dietary component in a variety of coastal marine finfish and appear o contain relatively high levels of beneficial polyunsaturated fatty acids, particularly docosahexaenoic acid (DHA), 22:6n—3 and eicosapentaenoic acid (EPA), although their overall nutritional value is poorly known. Relatively sedentary, caprellids are common members of epibiotic communities on a variety of natural substrata. They readily colonize artificial structures, and under appropriate conditions can attain high biomass, particularly in environments with a higher organic loading, such as around species can be quite broad.

There is a paucity of Information available on culture techniques for caprellids, with most accounts elating to small-scale experimental or laboratory culture, although many of these do Indicate the potential suitabllity of caprellids to larger scale culture. Overall, these characteristics indicate that caprellids are worthy of consideration for application in marine finfish aquaculture. 0 2009 Elsevier 3. V. All rights reserved. Article history: Received 9 November 2008 Received in revised form 1 g January 2009 Accepted 20 January 2009 Keywords: Amphipod Aquaculture Caprellid Marine Finfish contents 1. . 3. 4. 5. 6. 7. 8. g. Introduction . Do finfish consume caprellids in the natural environment? . Caprellid nutritional value . . Caprellid ecology and life history feeding.. . Environmental tolerances , . Diseases, toxins and allergenicity associated with caprellids . Caprellid culture methodology Discussion 9. 1 Simple caprellid culture and harvest . 9. 2. Caprellids in integrated co-culture and intensive culture Acknowledgments References .. 2 OF . . 201 202 203204 205 205 206 206 207 207 208 208 1 .

Introduction To meet increasing demand for marine finfish for varied human use in the face of generally static or declining capture fisheries, aquaculture Will have to increase current production levels to meet Tel. : +64 3 3488987; fax: +64 3 3485548. E-mail address: c. woods@niwa. co. nz. 0044-8486/$ – see front matter C 2009 Elsevier B. V. All rights reserved. doi:10. 101 6/j. aquaculture. 2009. 01. 018 this demand (Brugàre and Ridler, 2004; Bell and WaagbE, 2008; Pitcher, 2008).

Commensurately, there is also a growing focus on improving finfish aquaculture efficiency, as well as its environmental and financial sustainability (Boyd et al. , 2007; Bell and Waagba, 2008). In aquaculture, the provision of feed is often the most costly production input, and can have important downstream ecological effe eed is often the most costly production input, and can have important downstream ecological effects. At present, many marine finfish aquaculture efforts in developed nations are directed at high trophic level carnivorous fish that are often reliant upon on-growing aquafeeds derived from 200 C. M. C.

Woods / Aquaculture 289 (2009) 199-211 catches of Iower trophic level fish. However, these resources are often themselves the subject of static or declining capture fisheries, with increasing associated capture costs and biodiversity/ecosystem impacts (Tacon and Metian, 2008). Although terrestrial plant-based and animal by-product eeds Offer alternative nutrient sources, their substitution into formulated diets is considerably easier for herbivorous/ omnivorous species (Tacon and Metian, 2008), and they are themselves subject to increasing production costs, competition from urban expansion and other cropping/land use demands.

In addition, feeds based on terrestrial plants and animal by-products are stlll recommended to include a marine dietary component in order to maintain desirable fatty acid levels and other necessary nutrient inputs (Gatlin et al_, 2007; Bell and Waagbe, 2008). Many marine finfish aquaculture efforts, particularly for larval or juvenile infish stages, utilise a limited range of live food organisms, such as: Artemia, rotifers, copepods and mysid shrimp (e. g.

Domingues et ala, 2001; Dhont and Van Stappen, 2003; Lubzens and Zmora, 2003; Stattrup, 2006). Whilst the majority ofthese live foods have been successfully developed into viable culture feeds, they represent a limited dietary range that may not be nutritionally optimal for the increasing diversity of finfis a limited dietary range that may not be nutritionally optimal for the increasng diversity of finfish species beng cultured or life stages that utilise them (Ostrowski and Laidley, 2001).

In addition, orne ofthe larger live food organisms may be dificult to culture economically and reliably at high biomass. Consequently, there is a plangent need to explore the potential of hitherto neglected natural aquatic organisms as live feeds, and as components of aquafeeds, toward increasing levels of sustainable marine finfish aquaculture. Here I report on the suitability of caprellid amphipods (Amphipoda: Caprellidea) to fulfil these requirements in marine finfish aquaculture as a natural feed organism.

To be considered as a replacement or supplement for traditional feeds, a natural feed organlsm should ideally he: 1) A natural ood, or similar to other natural foods, of the target organism; 2) Of appropriate morphology, palatability and size for the target organism to ingest, and exhibit «attractive» behaviour, if presented as live prey; 3) Of relatively high nutritional value to the target organism, or capable of being «enriched» to a high nutritional value; 4) Capable of reaching high population densities, rapid growth and attainment of reproductive maturity, with short duration between reproductive events to maximise collection from the WIId and/or culture productivity; 5) Easily and cheaply fed, and also preferably adaptable in feeding mode if being ultured; 6) Reasonably robust and tolerant of some degree of environmental fluctuation in order to avoid culture «crashes» should environmental conditions Vary; and 7) Locally available for harvesting or initial seed stock sourcing – and i s OF environmental conditions Vary; and 7) Locally available for harvesting or initial seed stock sourcing – and in such abundance that such sourcing does not impact upan the natural population – to minimise biosecurity/financial risks and transport costs associated with sourcing from out-of-region or country. Caprellids, also known as skeleton shrimp, are relatively Small (i. b5 cm length) marine amphipods that are common in many littoral habitats, where they form an important trophic link between primary producers and higher trophic levels. Like other amphipods, the head has two pairs of antennae and the body comprises multiple segments, most with a pair of limbs (Fig. 1). Unlike the more typical Fig. 1 . A) Mature male Caprella equilibra (upper) and C. mutica (Iower). Scale rule is in centimetres; B) Mature male C. equilibra amongst hydroids fouling the underside of a mussel longline float, and; C) Mature brooding female C. mutica amongst macroalgae fouling a string line. 201 mphipod, however, caprellids have a peculiar morphology of long, thin bodies, greatly reduced abdomens and pleopods, and the pereopods (legs) and gills on some thoracic segments may be reduced or absent.

Whilst there is an increasing global knowledge of caprellid taxonomy, ecology and biology, the application of caprellids as an aquaculture feed resource has received scant attention to date, and they may represent an overlooked marine aquaculture resource that could be utilised to help enable the development of increased sustainable marine finfish aquaculture production. This review examines aspects ofthe biology and cology of caprellid 6 OF ecology of caprellid amphipods in View of their potential suitability as a natural live finfish food, and as a possible component in marine aquafeeds. 2. Do finfish consume caprellids in the natural environment?

For some finfish species (including some commercially exploited food and ornamental aquarium species), caprellids are an important, and in some instances the dominant, natural dietary component (see Table 1). The majo ity offinfish species that prey on caprellids tend to be either relatively Small (i. e. b30 cm standard length (SL)) species (e. g. Hastings and Bortone, 1980; Demetropoulos et al. , 1990; Holbrook and Schmitt, 1992; Teixeira and Musick, 1995; Labropoulou et al. , 1998; Labai et al. , 2002), or the smaller ontogenetic stages of larger species (e. g_ juvenile chinook salmon (Fisher and pearcy, 1997; Fresh et al. , 2006) and yellowtail (Anraku and Azeta, 1967)).

Caprellid consumption by finflsh may Vary seasonally in reflection of caprellid population cycles and availability of other dietary components (e. g. Collie, 1987; Ryer and orth, 1987; caine, 1979a,b, 1991; Hinz et al. , 2005; Kwaket al. , 2005), or even differential access to caprellid-rich habitats ue to social hierarchles (Holbrook and Schmitt, 1992; Yamaoka et al. , 2003). For example, when shiner perch (Cymatogaster aggregata) move into seagrass beds in Padilla Bay National Estuarine Sanctuary (Washington, USA) during spring, they may feed exclusively on caprellids and then shift to other crustaceans as caprellid populations decline (Caine, 1991).

Similarly, Hinz et al. (2005) found that dab (Limanda limanda) consumed more caprellids (Pariambus Hinz et al. (2005) found that dab (Limanda limanda) consumed more caprellids (Pariambus typicus) in summer (- 55% of stomach contents) compared to in winter 10% of stomach contents). For other finfish species, deliberate consumption of caprellids may be relatively Iow where caprellids are present (e. g. Simenstad et al. , 1979; López-Jamar et al. , 1984; Lechanteur and Griffiths, 2003; Kwak et al. , 2004), or the probable result of incidental ingestion along with target food such as macroalgae (e. g. Lechanteur and Griffiths, 2003; Silvano and Güth, 2006).

Table 1 Examples of recorded fish predation on caprellid amphpods Teleost family Fish species Caprellid species consumed Caprella cicur, C. penantis, C. longicollls Not described Eight species including: Duetella venenosa, C. ilidigitata, C. equilibra C. laeviuscula C. laeviuscula Nine species including: C. californica, C. verrucosa, C. penantis C. laeviuscula C. kroeyeri, C. tsugarensis Not described C. scaura Relative dietary importance source 17. 7% pv, 57. 9% FO 16. 2% PV 11. 2% pv, FO 31. 8% PV 66. 1% PV 17. 2% pv, FO O 100% PV DW, 41% FO 0. 08 to 0. 82 PN 47. 1% PI prochazka (1998) Demetropoulos et al. (1990) Hobson and Chess (2001 ) Caine (1979a,b) Caine (1 979a,b) Hobson and Chess (2001 ) Caine (1991 ) Kwak et al. 2004) Holbrook and Schmitt (1992) Dubiaski-Silva and Masunari (2008) Kwak et al. (2005) page et al. 2007) Fjasne and Gjaseter (1996) Hobson and Chess (2001) Dubiaski-snva and Masunari (2008) caine (1979a,b) Hinz et al. (2005) Dubiaski-Silva and Masunari (2008) Brawley and Fei (1987) H0bson and Chess (2001 ) yamaoka et al. (2003) Lechanteur and Griffiths (2003) Woods (2002) Kendrick and Hyndes (2005) Kendri Yamaoka et al. (2003) Lechanteur and Griffiths (2003) Woods (2002) Kendrick and Hyndes (2005) Kendrick and Hyndes (2005) Kendrick and Hyndes (2005) Horinouchi and Sano (2000) Horinouchi and Sano (2000) prochazka (1998) Horinouchi and sano (2000) Cheilodactylidae Redfingers Cheilodactylus fasciatus Cottidae

Scalyhead sculpin Artedius harringtoni Snubnose sculpin Orthonopias triacis Rhamphocottus richardsonii Spiny lumpsucker Eumicrotremus orbis Kelp perch Brachyistius frenatus Shiner perch Cymatogaster aggregata Ditremma temmincki Surfperch Embiotica lateralis Chere-chere grunt Haemulon steindachneri Cyclopteridae Embiotocidae Haemulidae Hexagrammidae Greenling Hexagrammos agrammus Painted greenling Oxylebius pictus Labridae Goldsinny wrasse Ctenolabrus rupestris Labrisomidae Monacanthidae Pholidae Pleuronectidae Sciaenidae Scorpaenidae Serranidae Sparidae Syngnathidae Island kelpfish Alloclinus holderi planehead ilefish Stephanolepis hispidus Penpoint gunnel Apodichthys flavidus Dab Limanda limanda High-hat Pareques acuminatus Rockfish Sebastes thompsoni Kelp bass Paralabrax clathratus Crimson sea bream (solitary) Ewynnis japonica Steentje seabream Spondyliosoma emarginatum Large-bellied seahorse Hippocampus abdominalis Short-snouted seahorse H. breviceps Macleay’s crested ppefish Histiogamphelus cristatus Spotted pipefish Stigmatopora argus Redfin velvetfish Hypodytes rubripinnis Panther pufferfish Takifugu pardalis Cape triplefin Cremnochochorites capensis Kazunagi Zoarchias veneficus C. kroeyeri, C. sugarensis, C. scaura Mainly C. mutica C. sepentrionalis, C. linearis, ina Six+ species including: C. californica, Aciconula ac . pilidieita C. sca Phthisica marina Six+ species including: C. californica, Aciconula acanthosoma, C. pilidigita C. scaura C. Iaeviuscula Pariambus typicus C. scaura C. irregularis Five species including: C. pilidigita, C. alifornica, Deutella venenosa Not described Not described C. equilibra Not described Not described Not described Not described Not described Unidentified Not described 15. 3% DW, 60. 4% FO – 15 to BN 15. 3% pv, FO 19. 5% pv, FO 40. 2% PI 749% PV- 10 to PV 69. % PI PV 11. 2% pv, FO 2. 6 to 18. 2% pv, 20 to 78. 6% FO 32. 9% pv, FO pv, 26% FO 13. 5% pv, 44. 8% FO 21. 8% pv, 60. 3% FO 13. 6% pv, 36. 4% FO PV 11. 3% pv, 81. 5% FO PV Terarogidae Tetraodontidae Tripterygidae Zoarcidae Relative dietary importance of caprellids in fish gut contents indicated by: DW % doy weight (mass) of gut contents; PV % volume of gut contents; FO = % frequency of occurrence in gut contents (i. e. % of fish guts examined of all those examined that contained caprellids); PN = Proportion of gut contents by number; BN = % of gut contents by number; Pl Preponderance ndex (relative index of frequency of occurrence and volumetric content). Where multiple caprellid species are described for each fish species in Source references, only the three most important (i. e. according to % volume, % frequency of occurrence etc. ) caprellid species are presented for brevity. 202 C. M. C. Woods / Aquaculture 289 (2009) 199-211 -rabie 2 Mean ± 1 SE percentage (%) fatty acid composition of nine caprellid species (Caprella acanthifera, C. grandimana, C. danilevskii, C. equilibra, C. liparotensis, C. penantis, C. santosrosai, Phtisica marina, and Pseudoprotella phasma) fr