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Effect of darkness and water flow rate on survival, grazing and growth rates of abalone Haliotis rufescens postlarvae.

ABSTRACT The effect of two light conditions (light at 10-13-[micro]mol quanta/[m.sup.2]/s and darkness) in three water flow rates (0, 200, and 600 mL/min) on the survival, grazing grazing,
n See irregular feeding.


1. actions of herbivorous animals eating growing pasture or cereal crop.

2. area of pasture or cereal crop to be used as standing feed. See also pasture.
, and growth rates Growth Rates

The compounded annualized rate of growth of a company's revenues, earnings, dividends, or other figures.

Remember, historically high growth rates don't always mean a high rate of growth looking into the future.
 of 6-day-old Haliotis rufescens postlarvae (pl) was evaluated. A factorial experiment fac·to·ri·al experiment
An experimental design in which two or more series of treatments are tried in all combinations.

factorial experiment

see factorial experiment.
 with three replicates per treatment in blocks was conducted for 44 days in 2-L plastic containers with ca. 100 postlarvae each, inoculated every week with the cultured diatom diatom (dī`ətŏm', -tōm'), unicellular organism of the kingdom Protista, characterized by a silica shell of often intricate and beautiful sculpturing. Most diatoms exist singly, although some join to form colonies.  Navicula incerta. Survival was highest (80%) in the treatment without water flow and with light, whereas the lowest (52%) corresponded to the 600-mL/min flow rate under darkness, but these differences were not significant. Initial grazing rate was significantly higher in darkness Adv. 1. in darkness - without light; "the river was sliding darkly under the mist"
 than in light (37 cell/pl/hr, SE = 1.6, and 27 cell/pl/hr, SE = 2.8, respectively). Growth rate was not significantly affected by the light treatments. However, in static conditions growth was higher in darkness (38-[micro]m/day, SE = 2.0) than in light (34-[micro]m/day, SE = 1.0). Growth rates of postlarvae were significantly affected by flow conditions, with means of 36 (SE = 1.3), 33 (SE = 0.7) and 31 (SE = 0.7) [micro]m/day in flows of 0, 200, and 600 mL/min, respectively). These results suggest that the benefits of dark conditions on the growth rate of abalone abalone (ăbəlō`nē), popular name in the United States for a univalve gastropod mollusk of the genus Haliotis, members of which are also called ear shells, or sea ears, as their shape resembles the human ear.  postlarvae shown in previous experiments might not occur under flow conditions. However, the flow rates tested here were apparently too high to allow an optimal postlarval growth and slower flows should be tested in future experiments. On the other hand, flow allowed the development of high diatom densities under the light condition, which were difficult to maintain in darkness.

KEY WORDS: postlarvae, Haliotis rufescens, growth, darkness, flow


Abalone (Haliotis spp.) seed production includes the culture of postlarvae that feed mostly on biofilms dominated by benthic ben·thos  
1. The collection of organisms living on or in sea or lake bottoms.

2. The bottom of a sea or lake.

 diatoms diatoms

a series of unicellular algae, microscopic in size, with cell walls containing silica. Members of the family Diatomaceae. Their remains accumulate as geological deposits and are mined. See diatomaceous earth.
 (Hahn 1989, Leighton 2000). Growth of postlarvae in culture systems is affected by several factors, including diatom strain (Kawamura et al. 1998, Roberts et al. 1999, Daume et al. 2000, Sawatpeera et al. 2004, Carbajal-Miranda et al. 2005, Gordon et al. 2006) and biofilm Biofilm

An adhesive substance, the glycocalyx, and the bacterial community which it envelops at the interface of a liquid and a surface. When a liquid is in contact with an inert surface, any bacteria within the liquid are attracted to the surface and adhere
 density (Searcy-Bernal et al. 2001, Day et al. 2004, Gorrostieta-Hurtado & Searcy-Bernal 2004). Light intensity is a key abiotic a·bi·ot·ic  
Nonliving: The abiotic factors of the environment include light, temperature, and atmospheric gases.

 factor affecting postlarval growth of cultured abalone because it controls the growth of diatom films (Searcy-Bernal et al. 2003, Day et al. 2004, Watson et al. 2004, Watson et al. 2005).

Juvenile and adult abalone have nocturnal habits and display a photophobic pho·to·pho·bic
1. Exhibiting photophobia.

2. Avoiding light.

3. Growing best in the absence of light.
 behavior in the laboratory (Hahn 1989). The feeding and growth rates of H. discus discus /dis·cus/ (dis´kus) pl. dis´ci   [L.] disk.

n. pl. dis·ci
A flat circular surface; a disk.


pl. disci [L.]

 hannai juveniles (ca. 30 mm shell length) increased 20% and 160%, respectively when grown in complete darkness rather than in light conditions and similar effects were detected on H. discus and H. sieboldi (Kim et al. 1997). For H. rufescens (ca. 40 mm shell length) feeding and growth rates improved 24% and 260%, respectively when grown in the dark (Ebert & Houk 1984). Similar findings were reported for H. iris (Clarke & Creese 1998).

It is not known when nocturnal habits of abalone first develop and it is generally considered that these arise after postlarval stages, because postlarvae do not exhibit a cryptic behavior (McShane 1992) and graze on diatom films under illumination (e.g., Martinez-Ponce & Searcy-Bernal 1998). Culture systems for postlarvae provide natural or artificial illumination to promote diatom growth, avoiding excessive light intensity by shading, because this condition may create overdeveloped films and adverse ecological conditions (Ebert & Houk 1984, Hahn 1989, Searcy-Bernal 1996, Watson et al. 2004).

Recent research suggests that nocturnal habits of abalone may develop early in postlarval stages. In small-scale experiments (10-mL containers) under static conditions with newly-settled postlarvae (2-14 d) of H. rufescens, growth rate increased up to 300% in darkness compared with constant illumination (Gorrostieta-Hurtado & Searcy-Bernal 2004) and similar results were obtained with H. corrugata (Gorrostieta-Hurtado 2005). The main objective of this study is to determine whether these results would also be obtained under flow conditions.


Abalone, Haliotis rufescens, larvae Larvae, in Roman religion
Larvae: see lemures.
 were provided by a local commercial hatchery hatchery

a commercial establishment dedicated to the hatching of bird eggs to provide day old chicks and poults to the poultry industry.

hatchery liquid
the contents of unfertilized eggs. Used in petfood manufacture.
 (Abulones Cultivados, Erendira, B.C.) and settled with gamma-aminobutyric acid gamma-aminobutyric acid /gam·ma-ami·no·bu·tyr·ic ac·id/ (gam?ah-ah-me?no-bu-tir´ik) ?.

gam·ma-a·mi·no·bu·tyr·ic acid
n. Abbr.

gamma-aminobutyric acid

GABA (gamma-aminobutyric acid)
A neurotransmitter that slows down the activity of nerve cells in the brain.
, 1.5-[micro]M final concentration, Searcy-Bernal & Anguiano-Beltran 1998) at the Instituto de Investigaciones Oceanologicas (I.I.O.) facilities. Postlarvae were fed the cultured benthic diatom Navicula incerta before the experiment.

An experiment following a two-factor randomized ran·dom·ize  
tr.v. ran·dom·ized, ran·dom·iz·ing, ran·dom·iz·es
To make random in arrangement, especially in order to control the variables in an experiment.
 block design was conducted using 2-L plastic containers (bottom area = 196 [cm.sup.2]) with ca. 100 postlarvae (6 d, mean shell length = 332 [micro]m, SE = 2.1) as experimental units. Factors considered were water flow rate (0, 200 and 600 mL/min) and light condition (light and darkness). Three blocks were considered along the water table where the units were placed, because irradiance ir·ra·di·ant  
Sending forth radiant light.

[Latin irradi
 at the center was higher than at the edges (13- and 10-[micro]mol quanta/[m.sup.2]/s, respectively). One replicate per treatment was randomly assigned to each block (i.e., three replicates per treatment). In the darkness treatments, units were enclosed in black plastic bags. Seawater seawater

Water that makes up the oceans and seas. Seawater is a complex mixture of 96.5% water, 2.5% salts, and small amounts of other substances. Much of the world's magnesium is recovered from seawater, as are large quantities of bromine.
 was filtered to 1 [micro]m and UV-sterilized. Water from the static treatments was changed daily. Two days before introducing the postlarvae into the experimental vessels, these were inoculated with N. incerta (ca. 280 cells/[mm.sup.2]).

The experiment was conducted for 44 days. During this period seawater temperature was 17[degrees]C [+ or -] [degrees]C. Survival was determined by counting live postlarvae in the containers weekly. Grazing rates were estimated 2-3 h after the introduction of postlarvae into vessels, by measuring the grazed graze 1  
v. grazed, graz·ing, graz·es

1. To feed on growing grasses and herbage.

2. Informal
a. To eat a variety of appetizers as a full meal.
 area (digital analysis of video-recorded images) and the diatom density (Martinez-Ponce & Searcy-Bernal 1998, Searcy-Bernal et al. 2001). This method provides only an estimation of initial grazing rates. Feeding activity is hard to quantify after this period because of the movement of diatoms into grazed areas.

Growth rates Were determined based on the weekly measurements of the shell length of 15-20 postlarvae per unit, also by the digital analysis of images (Scion sci·on  
1. A descendant or heir.

2. also ci·on A detached shoot or twig containing buds from a woody plant, used in grafting.
 Image 4.0.2) recorded directly from the bottom of containers (nondestructive non·de·struc·tive  
Of, relating to, or being a process that does not result in damage to the material under investigation or testing.

 method) on an inverted microscope An inverted microscope is a microscope with its light source and condenser on the top above the stage pointing down, and the objectives and turret are below the stage pointing up.  using a high-resolution camera (Sony SSC-C374).

The density of the diatom N. incerta was determined periodically by counting three ungrazed microscopic fields (x400 final magnification Magnification

A measure of the effectiveness of an optical system in enlarging or reducing an image. For an optical system that forms a real image, such a measure is the lateral magnification m
). These measurements reflect the highest diatom density achieved in each treatment and may be used to compare, at least qualitatively, the food supply for postlarvae among treatments. The actual food availability is difficult to estimate because of the patchiness patch·y  
adj. patch·i·er, patch·i·est
1. Made up of or marked by patches: patchy trousers.

 of the distribution of diatoms and abalone postlarvae. However, these usually concentrate at the edges of ungrazed films for feeding.

Re-inoculations of diatoms were performed in those containers with low densities, trying to reach adequate levels suggested by previous experience. During the first four weeks, diatom densities were attempted to be kept around 3,000 cells/ [mm.sup.2] and during the last two weeks around 8,000 cells/[mm.sup.2]. In previous trials these densities promoted optimal postlarval growth of this abalone species (see Gorrostieta-Hurtado & Searcy-Bernal 2004). The new density after reinoculation was also determined. This procedure was required especially in the static and dark treatments (Table 1).

Data were analyzed by two-factor ANOVAs for block designs (Steel at al. 1997). Percent survival data were subjected to the arcsine square root transformation before the analyses.

Block effects were never significant and are not reported here. In all tests the error degrees of freedom were 10.


Survival at the end of the experiment was 70% to 80% in all treatments except for the dark-600 mL/min treatment where the lowest survival (52%) was observed. These differences were not significant for light condition (F = 3.07, P=0.11), flow rate (F = 2.40, P = 0.14) or interaction (F = 0.32, P = 0.72).

Grazing rates were significantly higher in darkness than in light (37.0 cell/pl/hr, SE = 1.6 and 27.1 cell/pl/hr, SE = 2.8, respectively; F = 13.74, P = 0.004). There was no significant effect of flow rate (F = 2.66, P = 0.11) but a strong interaction was detected (F = 3.62, P = 0.06) (Fig. 1).

Shell length data are presented in Figure 2. By the end of the experiment the largest postlarvae corresponded to the static treatments. Figure 3 shows postlarval growth rates in different periods during the experiment. During the first 12 days there was an increased growth at moderate flow rates (200 mL/min) (Fig. 3a) but after this period growth decreased in flow conditions. The highest final growth rates were obtained in static conditions (34.4 [micro]m/d, SE = 1.0, and 37.9 [micro]m/d, SE = 2.0, in light and dark conditions, respectively) and the lowest in the 600 mL/min flow rate (30.9 [micro]m/d, SE = 0.9 and 30 [micro]m/d, SE = 1.0, in light and dark conditions, respectively) (Fig. 3d). Flow effects on final growth rates were significant, but light effects and interactions terms were not significant at any time period tested (Table 2).

Diatom density increased rapidly in the light treatments under flow, reaching values above 6,000 cells/[mm.sup.2] after the first week (Fig. 4) but in static conditions reinoculations were required to keep densities above 3,000 cells/[mm.sup.2] (Table 1). In dark conditions diatom densities were low during most of the experiment, despite reinoculation efforts (Fig. 4, Table 1). During the experimental period no other diatom species were detected in containers.




Effect of Darkness (Evidence of Nocturnal Habits in Abalone postlarvae?)

Overall, darkness stimulated postlarval growth of H. rufescens under static conditions (Figs. 2, 3), which is consistent with other small-scale trials on this species (Gorrostieta-Hurtado & Searcy-Bernal 2004) and H. corrugata (Gorrostieta-Hurtado 2005). This effect was detected despite the fact that food supply was generally lower in the dark treatment even after periodic reinoculation effort (Fig. 4, Table 1).


The most obvious explanation of this pattern is a difference in feeding activity. Grazing rates were also higher in dark conditions (Fig. 1) and this result is consistent with small-scale trials with H. corrugata (Gorrostieta-Hurtado 2005). Although these studies measure grazing rates only during the first 2-3 h of the experimental period, they support the hypothesis of an early development of nocturnal feeding habits even though, during the first weeks after settlement, abalone postlarvae do not display photophobic behavior and show feeding activity even under constant illumination (e.g., Martinez-Ponce & Searcy-Bernal 1998, Searcy-Bernal et al. 2001). This is also partially supported by a preliminary trial by Ve1ez-Espino (1999) on grazing rates of H. fulgens during a 24-h cycle. He reported a significant increase in feeding activity of early postlarvae (15- and 30-day-old) about an hour before sunset but in older postlarvae no significant differences between day and night hours The Night Hours are the fixed times of prayer in the Divine Office of the Roman Catholic Church, that take place after sunset and before sunrise. In the Latin Rite, the main Office is traditionally Matins, said in the early hours of the morning, and which is joined to the office of  were detected.

The only other paper available to the authors, comparing abalone postlarval growth in dark and light conditions is that by Stott et al. (2004), using plates coated with artificial feeds. They reported no differences in growth rate of Haliotis diversicolor supertexta postlarvae between light and darkness (four weeks after settlement) and explained this result by considering that microalgae that may have grown on illuminated plates provided postlarvae no advantages in terms of growth. However, an alternative hypothesis alternative hypothesis Epidemiology A hypothesis to be adopted if a null hypothesis proves implausible, where exposure is linked to disease. See Hypothesis testing. Cf Null hypothesis.  would be that postlarvae in the dark grew as well as those in light despite the absence of microalgae, probably because of an increased feeding activity.

Evidence on photophobic habits in abalone postlarvae can also be extracted from studies comparing different light intensities by shading procedures. For instance, postlarvae of H. fulgens grew better in low irradiances of 6 [micro]mol quanta/[m.sup.2]/s than in higher light intensities (24-75 [micro]mol quanta/[m.sup.2]/s) (Searcy-Bernal et al. 2003).

In a commercial-scale trial with H. rubra, Huchette (2003) reported a higher growth rate of postlarvae (ca. 1 mm shell length) in shaded tanks than in unshaded tanks (13.3 and 11.5 [micro]m/d, respectively) during the first weeks of the trial (although growth in unshaded tanks was higher thereafter).

Watson et al. (2004) conducted an experiment with early juveniles (ca. 3.5 mm) of H. laevigata, fed two diatoms in shaded and unshaded aquaria a·quar·i·a  
A plural of aquarium.
 (77 and 270 lux in the bottom, respectively). When fed Cocconeis sp. postlarvae grew better in shaded aquaria, despite a lower food supply. Moreover, these authors documented a negative phototactic behavior of juveniles, positioning themselves under airlines, under plate racks or in corners of the aquaria during the day, especially in the unshaded aquaria, although grazing during the night was evident (cleared areas over plates).

On the contrary, Day et al. (2004) reported that postlarval growth of H. rubra was higher in unshaded than in shaded containers, during the first five weeks after settlement. This experiment was conducted with water flow, but, apparently without reinoculation of food. Therefore, food limitation in shaded containers might help to explain differences in growth rates. Watson et al. (2005) reported that grazing rates of H. laevigata juveniles feeding on Navicula jeffreyi were higher in unshaded (22 [micro]mol quanta/[m.sup.2]/s) than in shaded (4.7 [micro]mol quanta/[m.sup.2]/s) containers. However, biofilms were denser in unshaded conditions and that result might reflect a positive relationship between grazing rates and diatom density as reported for H. fulgens postlarvae (Searcy-Bernal et al. 2001).


Other hypotheses may also help to explain the higher postlarval growth in the dark (or shade) than in the light, or the similar growth despite reduced food supply. High light intensities may result in high oxygen supersaturation supersaturation,
n the addition to or presence of an ingredient in a solution in greater quantity than the solvent can permanently take up.
 levels in the boundary layer boundary layer

In fluid mechanics, a thin layer of flowing gas or liquid in contact with a surface (e.g., of an airplane wing or the inside of a pipe). The fluid in the boundary layer is subjected to shear forces.
, which might affect postlarval fitness (Searcy-Bernal 1996). These levels can be more extreme than the subsaturation concentrations found under darkness (Roberts et al. 2006). Although there is some evidence that abalone postlarvae can survive in up to 150% oxygen saturation oxygen saturation sO2 The O2 concentration of blood expressed as a ratio of its total O2-carrying capacity; the OS is a measure of the utilization of O2 transport capacity; sO2  (Loipersberger 1996), information on potential sublethal sublethal /sub·le·thal/ (-le´thal) insufficient to cause death.

Not sufficient to cause death.
 effects is lacking.

On the other hand, the nutritional value of diatoms for abalone postlarvae might change in different light regimes. For instance, it has been reported that the benthic diatom Navicula perminuta produces mucus mucus /mu·cus/ (mu´kus) the free slime of the mucous membranes, composed of secretion of the glands, various salts, desquamated cells, and leukocytes.

 at a higher rate in darkness than under light conditions (Smith & Underwood 2000) and diatom mucus plays an important role in early postlarval nutrition of abalone (Kawamura et al. 1998). In a recent study, Watson et al. (2005) reported higher protein and lower fat contents of the benthic diatom Navicula jeffrey in shaded (4.7 [micro]mol quanta/[m.sup.2]/s) than in unshaded (22 [micro]mol quanta/[m.sup.2]/s) culture conditions.

Effect of Water Flow Rate

The pattern of postlarval growth observed in static conditions (higher growth in darkness than in light) was not maintained under flow conditions. Overall, growth rates were similar in dark and light under flow conditions (Fig. 3). This is consistent with results from a preliminary trial testing the effects of darkness and diatom density on the growth of H. rufescens postlarvae, at a similar flow rate than the highest in this experiment (Gorrostieta-Hurtado 2005).

Diatom densities increased rapidly with flow only under light conditions (Fig. 4) and food supply remained low in the dark treatments during most of the experimental period, despite reinoculation efforts (Table 1). Growth rates of postlarvae in the dark (under flow) were similar to those in the light, despite the reduced food availability.

Although the flow rates tested here had been used in previous trials in our laboratory (Gorrostieta-Hurtado 2005), these were probably too high for optimal postlarval development, probably because of reduced feeding and the energetic costs of staying in place or move against the water flow (Donovan & Carefoot 1997). This is supported by the observation that grazing rate decreased in dark conditions under flow, falling to levels similar to those observed in light. (Fig. 1).

Water flow stimulated diatom growth under light but not in the dark (Fig. 4) and denser diatom films probably provided some protection for postlarvae against water flow. This would explain the lowest survival (52%) and lowest growth rate (30 [micro]m/day. Fig. 3) in the highest flow rate (600 mL/min) under the dark condition.

Besides stimulating diatom growth, water flow replaces nutrients and gases, washes wastes away and reduces boundary layer problems (Roberts et al. 2006), so there should be slower flow rates than those tested here, that would provide these benefits without interfering with postlarval locomotion locomotion

Any of various animal movements that result in progression from one place to another. Locomotion is classified as either appendicular (accomplished by special appendages) or axial (achieved by changing the body shape).
 and grazing, and thus resulting in increased growth. Water flow can also increase feeding rates and growth in larger juveniles of H. laevigata (Fleming et al. 1997, Higham et al. 1998).

It is difficult to compare the flow rates tested here with those used in hatcheries or other experiments. Water exchange rates were probably higher in this study but the water velocity over culture surfaces may be more important to compare and this is usually not available.

In conclusion, this study confirms previous trials showing increased grazing and growth rates of abalone postlarvae when grown in the dark without water flow, and these results support the hypothesis of the development of nocturnal habits earlier in the life history of abalone than previously considered. This pattern was not observed in flow conditions probably because flow rates were too high, and more research with slower flows is required. The potential benefits of culturing postlarval abalone in the dark (or very low light intensities) would depend on the practicability of maintaining an adequate food supply, which may be a difficult task. Possible approaches to maintain biofilms, whereas benefiting from the photophobic behavior of postlarvae, besides intensive diatom cultivation, would include to either alternate periods of light and darkness or to increase the duration of nocturnal periods.


The authors thank the farm Abulones Cultivados for the donation of larvae. The diatom Navicula incerta was provided by the Microalgae Laboratory of the I.I.O. The authors also thank two anonymous reviewers whose comments improved the quality of this manuscript. This study was partially funded by the UABC UABC Universidad Autónoma de Baja California (Mexico)
UABC United Aircraft Building Corporation (Russia) 
 grant 4403 and the Mexican Government (CONACyT grant 37461-B and SNI (1) (Subscriber Network Interface) The point of interface between the customer's equipment (CPE) and a communications service from a common carrier.

(2) (SNA Network I
 scholarship 5532). This paper is part of the doctoral dissertation of E. Gorrostieta-Hurtado supported by CONACyT scholarships.


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Located or occurring outside a cell or cells.
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1. Of, relating to, or found in an estuary.

2. Geology Formed or deposited in an estuary.

Adj. 1. estuarine - of or relating to or found in estuaries
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Of or relating to the mollusks.

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 Res. 25:1-8.


(1) Instituto de Investigaciones Oceanologicas. Universidad Autonoma de Baja California, Ensenada, Baja California
For other uses see Ensenada (disambiguation)

Ensenada is the third-largest city in the Mexican state of Baja California. It is located 116 km (about 70 miles) south of Tijuana, at .
, Mexico; (2) Centro de Investigacion Cientifica y Educacion Superior de Ensenada, Ensenada, Baja California, Mexico

* Corresponding author. E-mail:
Inoculation scheme of Navicula incerta in experimental
treatments. Those with an asterisk were reinoculated
in the specified day after the start of the experiment,
because of low diatom densities.

               Light                      Darkness

        0       200      600       0       200      600
Day   mL/min   mL/min   mL/min   mL/min   mL/min   mL/min

 2                                 *        *        *
 6                                 *        *        *
12                                 *        *        *
19      *                          *        *        *
26      *                          *        *        *
29      *                          *        *        *
37      *        *        *        *        *        *

Result of ANOVAs for growth rates in different periods after
the start of the experiment. Initial age of postlarvae was 6 days.
Block effects were not significant (error df = 10).

                    Light         Water Flow
                  Condition          Rate       Interaction

Period (days)     F       P       F       P       F       P

0-12            1.43    0.26    0.81    0.47    1.24    0.33
12-29           0.17    0.68    2.17    0.17    0.56    0.59
29-44           0.58    0.46    2.05    0.18    0.89    0.44
0-44            0.65    0.44    8.30    0.008   0.92    0.43
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Author:Searcy-Bernal, Ricardo; Gorrostieta-Hurtado, Erendira
Publication:Journal of Shellfish Research
Date:Sep 1, 2007
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