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Woolley and Partridge , 2016- The Effect of Different Rotifer Feeding Regimes on the Growth and Survival Of
Woolley and Partridge , 2016- The Effect of Different Rotifer Feeding Regimes on the Growth and Survival Of
Woolley and Partridge , 2016- The Effect of Different Rotifer Feeding Regimes on the Growth and Survival Of
12723
Correspondence: G J Partridge, Australian Centre for Applied Aquaculture Research, Challenger Institute of Technology, Fleet
Street, Fremantle, WA 6160, Australia. E-mail: .gavin.partridge@challenger.wa.edu.au
2724 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2723–2731
13652109, 2016, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/are.12723 by INIDEP-Instituto Nacional de Investigacion y Desarrollo Pesq, Wiley Online Library on [05/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Aquaculture Research, 2016, 47, 2723–2731 Rotifer feeding regimes for yellowtail kingfish larvae L D Woolley & G J Partridge
Table 1 Rotifer feeding treatments fed to yellowtail king- analysed for total bacterial counts and Vibrio sp.
fish larvae from 3 to 12 days post hatch (dph) counts by the Department of Agriculture and
Food, Western Australia according to standard
High Low methods described by Buller (2004). The trial was
Rotifer density density Hybrid
terminated on 13 dph, the end of the rotifer feed-
treatment/ (rotifers (rotifers (rotifers
Age (dph) mL 1) mL 1) mL 1) ing stage, and larvae from each tank were hand
counted to determine the survival.
3 10 5 10
4 10 5 10
5 15 5 15 Statistics
6 15 5 5
7 15 6 6 A repeated measures ANOVA was used to determine
8 20 6 6 the effect of larval age and rotifer feeding treat-
9 20 7 7
ment on the growth of larvae (i.e. length and dry
10 30 7 7
11 30 8 8
weight) and number of rotifers consumed (i.e.
12 30 8 8 mastaxes per larval gut converted to a rate per
hour). For all repeated measures ANOVA tests, larval
age (dph) was selected as the within-subject factor
and feeding treatment as the between-subject fac-
decreased to match the low density feeding regime tor and each tank was used as the replication unit.
from 6 to 12 dph. The three regimes were com- One-way ANOVA was used to determine difference
pared with four replicate rearing tanks. Rotifers between treatments and parameters of survival,
were enriched with Spresso (INVE Aquaculture, numbers of rotifers added to each tank and culture
Dendermonde, Belgium) at 1000 ind. mL 1 water bacteria counts. Data were arcsine trans-
according to the manufacturer’s ‘overnight long- formed where necessary to ensure homogeneity of
term enrichment’, in which a background of variance. Significance was set at P < 0.05 and val-
100 ppm of Spresso was initially dosed into the ues are presented as mean SD. All statistical
enrichment tank followed by an 18 h enrichment analyses were performed using PASW Statistics 18
period during which two doses of 250 ppm each (Release 18.0.2, Chicago, IL, USA).
were administered at 19:30 and 01:30. Larvae
were fed rotifers three times per day (08:30, 12:30
Results
and 15:30 hours). Rotifer residuals were counted
half an hour prior to each feed, i.e. at 12:00 and Larval survival to 13 dph was 28 7% in the
15:00 hours for the 12:30 and 15:30 hours feed hybrid treatment compared with 17 5% and
respectively. Three 5 mL, depth-integrated samples 17 9% in the low and high density treatments,
were collected and counted for rotifers from each respectively, however these differences were not
tank. Sufficient rotifers were then added to each significant (P = 0.08; Fig. 1).
tank to maintain their target density shown in Larval growth, measured as standard length
Table 1. Random checks of rotifer densities at and dry weight was not significantly affected by
08:00 hours confirmed that rotifer residuals were feeding regime (P = 0.85 and 0.71, respectively;
at zero prior to the 08:30 hours feed. Fig. 2), by 12 dph larvae had reached
6.08 0.17 mm and 280 49 mg (DW), pooled
average. The number of rotifers ingested by larvae
Sampling protocol
increased significantly with larval age (P < 0.01),
Larval standard length and dry weight were with larvae ingesting 59 1.6 rotifers lar-
assessed on 4, 6, 8 and 12 dph on 20 randomly vae 1 h 1 (pooled average) by 11 dph, an
selected larvae per tank. Individual rotifers were increase of 173% from first feeding, however, there
quantified in the larval guts (5 per tank) by count- was no affect by the feeding regime (P = 0.62;
ing undigested mastaxes under a stereomicroscope Fig. 3). The number of rotifers actually used (i.e.
2 hours after the first feed on 4, 5, 7, 9 and taking into account residual values) in the low
11 dph in squash-mounted larvae (Ma et al. density and hybrid feeding method was signifi-
2012). The culture water from each tank was cantly less than the high density feeding regime,
sampled for total bacterial counts on 12 dph and 65 2% and 53 2% respectively (P < 0.001).
© 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2723–2731 2725
13652109, 2016, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/are.12723 by INIDEP-Instituto Nacional de Investigacion y Desarrollo Pesq, Wiley Online Library on [05/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Rotifer feeding regimes for yellowtail kingfish larvae L D Woolley & G J Partridge Aquaculture Research, 2016, 47, 2723–2731
2726 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2723–2731
13652109, 2016, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/are.12723 by INIDEP-Instituto Nacional de Investigacion y Desarrollo Pesq, Wiley Online Library on [05/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Aquaculture Research, 2016, 47, 2723–2731 Rotifer feeding regimes for yellowtail kingfish larvae L D Woolley & G J Partridge
The mean total Vibrio spp. top-up, only 59% of rotifers in the high density
(5452 3989 CFU mL 1) and total bacterial tanks on 4 dph would be fresh rotifers compared
(53 9 104 24 9 104 CFU mL 1) counts on with 75% in the low density feeding regime. On
12 dph were not significantly affected by treat- 9 dph, these values were calculated to be 53%
ment (P = 0.11 and 0.95 respectively). and 72% respectively.
Using the exchange rate of new water of 18%
h 1 and the rotifer consumption rates presented in
Discussion
Fig. 3, we have calculated the theoretical decline
in rotifer numbers under the high and low density The results of this study demonstrate that yellow-
feeding regimes for larvae of 4 and 9 dph in addi- tail kingfish larvae are efficient predators and can
tion to showing the actual rotifer residuals mea- feed effectively across a wide range of prey densi-
sured in each of these treatments (Fig. 4). These ties, regardless of age and that low prey densities
figures assume a survival rate of 100% and 40% do not negatively impact on growth or survival
of larvae at 4 and 9 dph, respectively and demon- under the conditions of this study. While optimiz-
strate that the actual rotifer residual values ing prey density and feeding regimes is of great
obtained were similar to those expected based on importance to optimising survival and growth of
the flushing rates and rotifer consumption rates. marine fish larvae in general, such optimization is
On the basis of the theoretical residual values and of particular importance at first feeding, as inade-
target densities, we have calculated that following quate regimes at this critical transition from
(a)
(b)
© 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2723–2731 2727
13652109, 2016, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/are.12723 by INIDEP-Instituto Nacional de Investigacion y Desarrollo Pesq, Wiley Online Library on [05/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Rotifer feeding regimes for yellowtail kingfish larvae L D Woolley & G J Partridge Aquaculture Research, 2016, 47, 2723–2731
endogenous to exogenous feeding can result in a the day of first feeding, i.e. 3 dph. Previous studies
failure to commence feeding and subsequently lead on snapper Lutjanus analis and grouper Epinephelus
to high rates of mortality (Cox & Pankhurst 2000; suillus larvae also suggest a much higher critical
Fushimi 2001; Chen, Qin, Caragher, Clarke, Ku- threshold compared to yellowtail kingfish larvae of
mar & Hutchinson 2007). Like most marine fish 20 and 18 ind. mL 1, respectively (Duray, Estudil-
larvae, yellowtail kingfish are visual predators lo & Alpasan 1996; Watanabe, Ellis, Ellis, Chaves
whose visual acuity and effective search volume & Manfredi 1998). The lower critical threshold
increase with age (Carton 2005; Georgalas, Malav- demonstrated in this study suggest yellowtail king-
asi, Franzoi & Torricelli 2007). To be appropriate, fish are more efficient predators and have a
prey density must be maintained at or above a quicker learning process and/or feeding ability at
critical threshold; a level which appears to be spe- the start of exogenous feeding (Y ufera & Darias
cies and age specific and dependent upon abiotic 2007).
factors such as light intensity and turbidity Larvae need to consume more live prey as they
(Puvanendran & Brown 1999). The light and grow in order to meet their increasing energy
algal-induced turbidity levels used in this trial demands (Puvanendran, Burt & Brown 2006). In
were above and below the levels that limit prey this study, the number of rotifers consumed
ingestion by yellowtail kingfish larvae increased with larval growth regardless of the
(<8 lmol s 1 m 2 and >16 9 104 cells mL 1, rotifer feeding regime. This is similar to results by
respectively) (Carton 2005; Stuart & Drawbridge Hamasaki, Tsuruoka, Teruya, Hashimoto, Hamad-
2011). a and Hotta (2009), who described an increase
The results from this study demonstrating an in the number of rotifers ingested by Japanese
equal ingestion rate of rotifers and equal growth yellowtail Seriola dumerili with an increase in
and survival rates across treatments suggest that body length. Although rotifer ingestion rates
the lowest first feeding rotifer density of 5 ind. increased significantly with time, this does not
mL 1 is above the threshold density. Working imply that the number of rotifers offered also
with the same species, Ma et al. (2012) found that needs to increase at the same rate. This is due to
5 dph larvae offered 1 rotifer mL 1 ate signifi- the fact that as larvae grow and develop they
cantly fewer rotifers during the first meal of the become more efficient predators as a result of
day compared to those offered ≥10 ind. mL 1, but improved visual acuity, increased search volume
by 8 dph rotifer ingestion was equal across all (Rabe & Brown 2000) and swimming ability
rotifer densities. The early feed limitation resulted (Fisher, Bellwood & Job 2000; Hunt von Herbing,
in significantly lower growth of the former larvae. Gallager & Halteman 2001). Our observation of
Combined, these data suggest that the threshold equal rotifer ingestion rates across the different
rotifer density for early feeding of yellowtail king- feeding regimes with time and equal larval
fish under non-limiting light and turbidity condi- growth rates demonstrates that our rate of
tions is >1 but ≤5 ind. mL 1. While Shaw, increase in rotifer density in the low density
Pankhurst and Battaglene (2006) suggested that regime was sufficient to keep pace with the lar-
larvae may spend more time searching out prey at vae’s increasing energetic demands. While we
lower densities, which may lead to slower growth, cannot rule out that further reductions in rotifer
the fact that we observed equal growth across all use may be possible by either maintaining the
regimes suggest that any additional energy same low density or reducing the rate of increase
expended by yellowtail kingfish larvae on search- with time, our loss modelling does suggest that
ing for prey at the lowest densities did not impact had survival remained high, that rotifer numbers
on their growth. may have become limiting by 7 dph or, con-
Sawada, Miyashita, Aoyama, Kurata, Mukai, versely, that such a limitation may have caused
Okada, Murata and Kumai (2000) determined that lower survival. We believe however, that the lat-
rotifer densities considered optimal for first feeding ter is unlikely and if rotifers did become limiting
in Pacific northern bluefin tuna Thynnus thynnus that a reduction in larval growth would be the
were within a wide range between 10 and 30 ind. more likely outcome, as the same ration of roti-
mL 1. These authors demonstrated that the fers is shared among a greater number of fish.
consumption of rotifers was lower at 5 ind. mL 1 Rotifers metabolize the nutrients they acquire
than at densities of 10 ind. mL 1 and above on during enrichment, resulting in a deterioration in
2728 © 2015 John Wiley & Sons Ltd, Aquaculture Research, 47, 2723–2731
13652109, 2016, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/are.12723 by INIDEP-Instituto Nacional de Investigacion y Desarrollo Pesq, Wiley Online Library on [05/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Aquaculture Research, 2016, 47, 2723–2731 Rotifer feeding regimes for yellowtail kingfish larvae L D Woolley & G J Partridge
their nutritional quality over time (Yamamoto, platforms for early weaning. The direct early wean-
Teruya, Hara, Hokazono, Kai, Hashimoto, Furuita, ing from rotifers to artificial diets has been achieved
Matsunari & Mushiake 2009). Although our loss for barramundi Lates calcarifer Bloch (Curnow, King,
modelling demonstrates the greater potential for Bosmans, & Kolkovski 2006; Curnow, King, Par-
nutritional depletion of enriched rotifers in the tridge et al. 2006) and more recently in several
high density treatment, we witnessed no difference commercial hatcheries for sea bass Dicentrarchus
in growth or survival between treatments. This labrax (O’Brien 2013) and sea bream Sparus aurata
suggests that nutritional depletion was not a sig- (King et al. 2011). Reducing the reliance on Artemia
nificant determinant in the larvae’s performance, has many economic and technical benefits and has
or that the Nannochloropsis sp. and Isochrysis sp. been a goal of commercial hatcheries for many
added to the rearing tanks were sufficient to main- years (Callan, Jordaan & Kling 2003). The success
tain the nutritional value of the rotifers. of such early weaning in the aforementioned species
There was a significant reduction in the num- is believed to be attributable (at least in part) to the
bers of rotifers used in the low density and hybrid use of a low density rotifer feeding strategy,
feeding techniques compared to the high density whereby rotifer densities drop below the critical
feeding regime. With live feed production costs threshold level for a significant period of time
being a major component of the cost of producing between live prey feeds. This approach results in
juvenile marine fish (Ballagh, Fielder & Pankhurst periods of time when the larvae are not fully sati-
2010), such reductions translate into significant ated on rotifers and subsequently more willing to
savings in production and also ease production accept the artificial diet (Rosenlund, Stoss & Talbo
demands on the live feed cultures. The reductions 1997). This is supported by a previous study on tur-
in rotifer usage of 65% and 53% in the low den- bot Scophthalmus maximus L. larvae which demon-
sity and hybrid feeding treatments, respectively, strated that larvae offered live prey at higher rations
would directly translate into the same percentage during weaning preferentially feed on the live prey,
reduction in the costs of production consumables, thereby delaying weaning (Bromley 1978). Further
such as culture and enrichment diets. Mass pro- studies will be required to confirm whether the
duction of rotifers is prone to higher bacterial lower density rotifer feeding strategies investigated
infestation and the accumulation and transfer to in this study do indeed facilitate early weaning in
larval fish is detrimental (Dhert et al. 2001), yellowtail kingfish.
although bacterial colonies were detected in the This study demonstrated that optimal rotifer
larval tank at the end of the trial, there were no densities thresholds are lower for yellowtail king-
significant differences between the feeding treat- fish than previously described species. Yellowtail
ments. kingfish are efficient at capturing prey at low den-
Previous studies have indicated that many mar- sities and have a rapid learning process and/or
ine finfish larvae do not display constant ingestion feeding ability at the start of exogenous feeding,
but have diel feeding patterns (Kotani & Fushimi requiring feeding densities of >1 but ≤5 rotifers per
2011) and a pulse feeding strategy fits with this nat- millilitre.
ural behaviour. Yellowtail kingfish larvae are
‘cruise searchers’, spending most of their time swim-
Acknowledgments
ming and foraging for food, however their swim-
ming efforts decrease as they become satiated, This study was funded by the Australian Seafood
similar to the behaviour observed in yellowtail Cooperative Research Centre (Project No. 2011/
flounder Pleuronectes ferrugineus by Rabe and Brown 754). The authors wish to thank Clean Seas Tuna
(2000). Yellowtail kingfish slow down their preda- Ltd. for providing the eggs. The authors also thank
tory behaviour once they are satiated, so there is no the Australian Centre for Applied Aquaculture
benefit in providing constant excess numbers of roti- Research for use of facilities and support through
fers within the rearing tanks. This is supported by the larval rearing.
our finding that the residual rotifer numbers in each
tank were generally higher at 3 pm than at 12 pm;
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