Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

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Journal of Experimental Marine Biology and Ecology

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Grazing by sprat schools upon zooplankton within an enclosed marine lake

Anthony Hawkins a,⁎, Frank R. Knudsen b, John Davenport c, Rob McAllen c, Helen J. Bloomfield d,1,Carl Schilt e, Peter Johnson f

a Loughine Ltd, Kincraig, Blairs, Aberdeen, AB12 5YT, United Kingdomb Fisheries Research, Simrad, Kongsberg Maritime, P.O. Box 111, N-3191 Horten, Norwayc School of Biological, Earth and Environmental Sciences, University College Cork, Enterprise Centre, Distillery Fields, North Mall, Cork City, Irelandd School of Marine Science and Technology, Newcastle University, NE1 7RU, United Kingdome Bigleaf Science Services, P.O. Box 225, North Bonneville, WA 98639 USAf LGL Limited Northwest, P.O. Box 771, Stevenson, WA 98648 USA

⁎ Corresponding author. Tel.: +44 1224 868984.E-mail addresses: a.hawkins@btconnect.com (A. Haw

frank.reier.knudsen@simrad.com (F.R. Knudsen), j.davenr.mcallen@ucc.ie (R. McAllen), h.j.bloomfield@liv.ac.uk (bigleaf@gorge.net (C. Schilt), pjohnson@lgl.com (P. John

1 Current address: School of Environmental Science3GP, United Kingdom.

0022-0981/$ – see front matter © 2011 Elsevier B.V. Alldoi:10.1016/j.jembe.2011.11.002

a b s t r a c t

a r t i c l e i n f o

Article history:Received 8 March 2011Received in revised form 1 November 2011Accepted 2 November 2011Available online 29 November 2011

Keywords:Echo soundingFish abundanceGrazingSchoolingSprattus sprattusZooplankton

We have investigated grazing by sprat schools upon zooplankton within Lough Hyne (Ireland), a marine lakewith only a narrow and shallow connection to the sea. Acoustic surveys showed the presence of largenumbers of sprat (Sprattus sprattus), preyed upon by mackerel Scomber scombrus. The sprat formed denseschools during the day and dispersed at night. Zooplankton were widely distributed within the lough, al-though absent below the oxythermocline. However, echo traces showed clear volumes, indicating an absenceof zooplankton, surrounding the daytime sprat schools. Pumped sampling of the zooplankton at differentdepths, close to and away from the sprat schools, confirmed that those volumes of water that appearedacoustically clear were largely devoid of macro zooplankton (92.7% reduction overall). Comparison of clearareas with adjacent areas showed that almost all decapod larvae and calanoid copepods andmost bivalve larvaewere absent. The differences for cladocerans were also significant but for gastropod larvae they were not signif-icant. Large calanoid copepods were much less abundant in the clear areas and their size distribution hadchanged.We conclude that the sprat schools had rapidly depleted their surroundings of zooplankton, suggestingthat fish within the schools may be substantially food-limited. Dispersal at night, when visual predators are lessefficient, may enable the sprat to feedmore effectively. Thus, although schooling may confer benefits to individ-ual fish there are concomitant disadvantages in terms of food depletion. The reduction in zooplankton as a resultof heavy grazing by sprat within the enclosed lough may affect the phytoplankton, with significant effects uponthe ecology of Lough Hyne.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

Previous studies in 2008 at Lough Hyne (Ireland), a marine lakewith only a narrow and shallow connection to the sea, showed thepresence of large numbers of sprat (Sprattus sprattus) and mackerel(Scomber scombrus) (Knudsen et al., 2009). The sprat formed denseschools during the day, when they were under attack by mackerel,and dispersed at night. From daytime acoustic surveys of the spratschools it was noted that a volume of water around each schoolshowed especially low acoustic scattering, suggesting a depletion ofzooplankton in the water in and around the school. During September

kins),port@ucc.ie (J. Davenport),H.J. Bloomfield),son).s, University of Liverpool, L69

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2009 a further series of acoustic surveys were carried out within thelough to investigate this phenomenon. The surveys were complementedby pumped sampling of zooplankton in water close to and distant fromthe sprat schools to ascertain whether predation by sprat had a signifi-cant impact upon zooplankton densities and composition.

2. Materials and methods

2.1. Location

Lough Hyne is a small, sheltered, sea lough near the western endof southern Ireland (51° 30′ N, 9° 18′ W). It connects with the seathrough a narrow and shallow channel; the Rapids (Fig. 1). Withinthe lough, the tides are greatly modified by the narrow shelving en-trance, with a reduced tidal range (about 1 m at spring tides and0.75 m at neap tides). The lough is divided into north and south basinsby a ridge, and the two basins are connected west of the ridge by atrough dropping to a depth of almost 50 m. Salinity falls within the typ-ical range for coastalwaters and the fauna and flora are typicallymarine

Fig. 1. Lough Hyne, on the south coast of Ireland (51° 30′ N, 9° 18′W), is a small sheltered marine lough connecting with the sea through a narrow channel called the Rapids. Surfacearea of the lough is about 0.5 km2.

Table 1Acoustical surveys of Lough Hyne during September 2009.

No. Date Start Finish Description

1 3rd 15:28 17:21 South and north basin, N/S transects2 4th 15:24 17:45 North basin, N/S transects3 5th 10:15 12:08 South and north basin, N/S transects4 6th 20:26 21:44 South and north basin, N/S transects5 7th 09:52 12:45 North basin and western trough,

with plankton sampling6 7th 14:15 16:01 North basin, E/W transects

60 A. Hawkins et al. / Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

(Bassindale et al., 1948). Lough Hyne has been a marine nature reservesince June 1981.

During tidal inflow a powerful current enters the lough, and isdeflected in a western direction across the south basin, with a weakermovement into the north basin above the western trough. Duringoutflow, surface water moves towards the Rapids from all parts of thesouth basin. Tidal replacement of water in the south basin is muchmore rapid than replacement of water in the north basin (Bassindaleet al., 1957). Johnson et al. (1995) report a 41 day total flushing timefor the lough.

2.2. Temperature and oxygen profiles

A seasonal thermocline forms annually within the western troughof Lough Hyne at depths of between 20 and 30 m and lasts from Aprilto November (Kitching et al., 1976; McAllen et al., 2009). The waterbeneath the thermocline becomes anoxic as summer progresses(Kitching et al., 1976). The water above the thermocline is subjectto renewal by the currents from the Rapids and remains oxygenated.

Vertical gradients of oxygen and temperature were measured on7th of September 2009 with a conductivity, temperature, and depth(CTD)meter lowered from the surface in the deepest part of the west-ern trough. The temperature decreased from 15 °C at the surface to10.3 °C on the seabed at a depth of 48 m. A thermocline was evidentat a depth of 28 m. The oxygen concentration varied between8.63 mg L−1 at the lough surface and 0.0 mg L−1 at the seabed, with asharp decline in oxygen below 28 m. In the shallower parts of thelough, including the main parts of the south and north basins, neithera thermocline nor oxycline was present.

2.3. Echo sounding

As previously described (Knudsen et al., 2009), acoustic surveys ofthe lough for pelagic fish were performed along a series of transectlines across the main basins of Lough Hyne. Stationary recordingswere also made during zooplankton sampling. Surveys were con-ducted by means of an echosounder (Simrad EY60) operating at200 kHz as described by Knudsen et al. (2009). The echosounder

was calibrated by recommended methods (Foote et al., 1987) usinga standard copper sphere with a diameter of 13.7 mm and nominaltarget strength of −45 dB re 1 m2. The echosounder was run from alaptop computer interfaced with a GPS to provide accurate positionand speed.

2.4. Echo sounding procedure

Hydroacoustic data were collected during the period 3rd–7th ofSeptember 2009 using the methods described by Knudsen et al.(2009). The surveys were conducted at slow speeds (approximately1.5 ms−1). Six surveys of the lough were conducted as shown inTable 1. The degree of coverage (CV; Aglen, 1983, 1989) was >15 forthe two full surveys conducted on the 3rd and 5th of September. Con-tinuous echosounding also took place throughout the zooplanktonsampling.

2.5. Biological sampling

Zooplankton populations were sampled by means of an electricalpump at the surface, connected to a long hose. Water samples werestrained through plankton netting (mesh size 200 μm), washed intosample jars and preserved in 10% seawater formalin. Pumping tookplace from three different depths in the north basin (8, 12 and15 m) and each sample had a volume of 257 l. Six pairs of sampleswere collected from neighbouring bodies of water in proximity tosprat schools in the eastern part of the north basin (Table 2). Each

Table 2Collection of zooplankton samples on the 7th of September 2009.

Sample Depth Start Time Finish Time Latitude Longitude

Sprat 1 12 m 10.01 10.03 51°30.248 N 9°17.990 WSprat 2 12 m 10.07 10.09 51°30.220 N 9°17.989 WSprat 3 15 m 10.11 10.13 51°30.225 N 9°17.997 WSprat 4 15 m 10.20 10.22 51°30.287 N 9°17.978 WSprat 5 8 m 10.24 10.26 51°30.232 N 9°18.000 WSprat 6 8 m 10.29 10.31 51°30.224 N 9°17.985 WNo sprat 1 12 m 10.37 10.39 51°30.146 N 9°18.132 WNo sprat 2 12 m 10.43 10.45 51°30.138 N 9°18.180 WNo sprat 3 15 m 10.50 10.52 51°30.166 N 9°18.150 WNo sprat 4 15 m 10.56 10.58 51°30.173 N 9°18.109 WNo sprat 5 8 m 11.02 11.04 51°30.179 N 9°18.105 WNo sprat 6 8 m 11.08 11.10 51°30.177 N 9°18.163 WW. trough 1 5 m 12.22 12.25 51°30.047 N 9°18.241 WW. trough 2 5 m 12.27 12.29 51°30.047 N 9°18.241 WW. trough 3 15 m 12.35 12.39 51°30.047 N 9°18.241 WW. trough 4 15 m 12.44 12.49 51°30.047 N 9°18.241 WW. trough 5 25 m 12.53 13.01 51°30.047 N 9°18.241 WW. trough 6 25 m 13.05 13.12 51°30.047 N 9°18.241 WW. trough 7 35 m 13.17 13.27 51°30.047 N 9°18.241 WW. trough 8 35 m 13.36 13.47 51°30.047 N 9°18.241 W

Fig. 2. Day time echograms from the eastern part of the north basin of Lough Hyne,showing well defined, dense sprat schools with a characteristic plume shape andoften with bottom contact. The schools are predominantly red, yellow and green.Zooplankton is predominantly blue. Note that the areas around the schools are clear,indicating reduced zooplankton densities. In the presented echograms, the numbers tothe left show depth in metres. The arrow in A indicates individual fish (green), probablymackerel.

61A. Hawkins et al. / Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

pair consisted of one sample collected from a volume of water identi-fied as an acoustically clear area surrounding a compact school ofsprat (‘sprat’), and one sample collected from an adjacent area,away from the schools and where sprat were absent (‘no sprat’). Sub-sequently, the boat was moored over the western trough, and sam-ples taken at 4 different depths (5, 15, 25 and 35 m). The positionsfrom which the samples were taken are shown in Table 2.

2.6. Analysis of acoustic data

Acoustic data were analysed using Sonar5 (Balk and Lindem,2007) post-processing software as described by Knudsen et al.(2009). Complete daytime surveys of the whole of the lough wereconducted on the 3rd and the 5th of September. One evening surveywas conducted on the 6th of September. Zooplankton quantities wereassessed by first removing all fish schools from the data sets and thenestablishing a whole water column zooplankton spherical scatteringcross section for the basin or whole lough (sA, m2). See MacLennanet al. (2002) for an explanation of the terms and metrics.

The zooplankton scattering cross section was subtracted from theanalysis for fish in cases where fish and zooplankton were clearly sep-arable. Where fish and zooplankton were mixed, it was not possibleto assign a value of sA to one or the other. For every fish school en-countered a line backscattering coefficient (sL) with unit mwas calcu-lated. The sL is the integral of sV over the 2D cross section area of theschools (MacLennan et al., 2002). Target strength (TS) was analysedas described by Knudsen et al. (2009).

Zooplankton sampling was performed on the 7th of September.Acoustic data were collected during the zooplankton sampling andanalysed by establishing the volume backscattering strength Sv (dB re1 m−1) for the period of the sampling corresponding to ±0.5 m ofthe sampling depth.

3. Results

3.1. Hydroacoustic measurements

During daytime echosounder surveys in both September 2008 and2009 schools of pelagic fish were found in the eastern part of thenorth basin. A few smaller schools were found close to the northend of the lough. In contrast, very few pelagic acoustic targets largeenough to be fish were observed in the south basin and in the westerntrough above the oxythermocline. Echograms from the eastern side ofthe north basin showed well defined, dense schools (shown in red,

yellow and green in the echograms) with a characteristic plumeshape, sometimes in contact with the seabed (Fig. 2). Some isolatedacoustic targets, attributed to larger individual fish, were encounteredin the vicinity of the plumes (Fig. 2). Weaker and more diffuse scatter-ing, assigned to zooplankton (shown as blue traces on the echograms),was found above the oxythermocline across the whole lough, but wasabsent in a zone surrounding the sprat schools (Fig. 2).

No pelagic fish schools were found deeper than 25 m. Locations ofthe school positions during surveys on the 3rd and 5th of September2009 are shown in Fig. 3 with biomass values shown as line backscat-tering coefficient (sL×10−3) for each school.

The fish schools dispersed at night (Fig. 4), breaking up at dusk toform a uniform layer throughout the north basin with somemovementinto the western trough. There was some indication of vertical migra-tion of zooplankton from the seabed intomid-water during the evening.

In the western trough, large numbers of small acoustic targets, at-tributed to zooplankton, were evenly distributed in the whole watercolumn above the oxythermocline, during both day (Fig. 5) andnight. Few acoustic targets were detected below the oxythermocline.

The daytime scattering coefficient (sA) values for the westerntrough and south basin, where fish schools were absent, were notvery different for the surveys on the 3rd and 5th of September(Table 3) and the majority of the targets were small (TSb−65 dB re1 m2) and distributed throughout the water column. In the eveningof the 6th of September, larger targets were found near the surface(b15 m) in the western trough giving a mean TS of −53 dB re 1 m2

within the 0–15 m layer. These targets were equivalent acoustically

Fig. 3. Locations of sprat schools during surveys on the 3rd and 5th of September 2009,withtotal-echo strength shown (as line backscattering coefficient (sL×10−3) with unit m).

Fig. 5. Daytime transect across the western trough from North to South, commencingat 11:26 h on the 5th of September, showing that the area below the oxythermoclineis devoid of zooplankton (blue) and fish.

62 A. Hawkins et al. / Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

to a 10 cm sprat (see Knudsen et al., 2009). The sA was also higher inthe evening in the western trough (Table 3). In the north basin sAwas lower in the evening (Table 3) indicating horizontal movement

Fig. 4. Evening echograms from the north basin on the 6th of September, showing spratschools (red, yellow and green) breaking up to form a layer at around 10 m depth.Zooplankton is predominantly blue. The numbers to the left show depth in metres. TransectA commenced at 20:52 h. Transect B commenced at 21:25 h.

of fish from the north basin into the western trough. This finding dif-fers from those in 2008 where no horizontal movement of fish be-tween basins was found (Knudsen et al., 2009). The sA values fromthe south basin did not vary much between day and evening, indicat-ing a constant biomass (Table 3)

3.2. Interpretation of the acoustic observations

The species responsible for the dense plumes were identified asschooling sprat (S. sprattus), and the surrounding individual acoustictargets were identified as mackerel (S. scombrus). The stomachs of themajority of mackerel caught by rod and line fishing contained one ormore sprat varying in length between 7.5 and 12 cm, confirming pre-dation by the mackerel upon the sprats.

During the evening the sprat plumes broke up into smaller schoolswith the acoustic targets subsequently dispersing into thewater column.Vertical distributions of fish from the echograms showed that at nightfish targets weremostly present at water depths of between 3 and 15 m.

In the north basin, during daytime, the region surrounding thedense sprat schools showed little evidence of the weak and diffusescattering normally associated with zooplankton.

Whole water column sA values were higher in the north basin, butvaried between 51 and 86.3 m2 on the 3rd of September and the 5thof September, respectively. In the evening on the 6th of Septemberthe sA was lower than during the day in the north basin, and had risenover the western trough indicating horizontal movement of the sprat.

The total-echo strengths from the fish schools were predominantlyhighest in the north basin. However, the corresponding zooplanktonsA values were low in the north basin (b0.6 m2) with higher values inboth the western trough and the south basin (Table 3). Diffuse scatter-ing, assigned to zooplankton, was found above the oxythermocline

Table 3Assessment of whole water column biomass as sA (m2 per basin area or total lougharea) for each of the basins and in total for the whole lough. The estimates in thenorth basin are for fish during daytime. The estimates in the western trough andsouth basin are for zooplankton. By removing all fish schools from the north basinthe remaining sA, assigned to zooplankton, was less than 0.6 m2. In the evening thehigher sA value in the western trough was likely to have resulted from horizontalmovement of fish from the north basin.

Date North basin Western trough South basin Total for Lough

3rd September(day)

51 12.5 3.7 62.2

5th September(day)

86.3 11.4 2.9 100.6

6th September(evening)

14.4 41 3.2 58.6

63A. Hawkins et al. / Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

across the whole lough, but was absent in a zone of several tens of me-tres diameter surrounding the sprat schools (Fig. 2). The much lower sAvalues for zooplankton in the north basin compared to the westerntrough and south basin may result from a reduction of zooplankton bythe foraging planktivorous sprat.

From stationary sampling it was evident that there were strong dif-ferences in the scattering coefficient for zooplankton between theacoustically clear ‘sprat’ areas and the adjacent ‘no sprat’ areas (Table 4).

3.3. Pumped sampling of zooplankton abundance and composition

Table 5 shows the numbers of animals present in plankton samplescollected by pumping from the north basin of Lough Hyne on the 7th ofSeptember 2009. Sampling positions are shown in Fig. 6. From these re-sults it is evident that there are major differences between ‘sprat’ and‘no sprat’ samples. Table 6 shows the percentage change in numbersof animals between ‘no sprat’ and ‘sprat’ sample volumes. Extremelysignificant differences are shown between ‘sprat’ and ‘no sprat’ samplesin the case of calanoid copepods, decapod larvae and bivalve larvae, andfor total animals. In the case of cladocerans there is also a significant dif-ference. Only in the case of gastropod larvae (the smallest animals pre-sent) are the differences not significant.

Thus those volumes of water that appeared to be clear acousticallywere largely (92.7% reduction overall) devoid of macro zooplankton(Table 6). Decapod larvae, calanoid copepods and bivalve larvaewere almost completely absent in comparison with adjacent waters.

Table 7 shows size differences in calanoid copepods between the‘sprat’ and ‘no sprat areas’. Large calanoid copepods had been re-moved from the area close to the sprat schools, changing and skewingthe size distribution.

Zooplankton sampling conducted above and below the oxythermo-cline in the western trough showed a general decline in zooplanktondensity with depth (Fig. 7), with appreciable numbers of molluscan lar-vae only being recorded from the sample taken at 5 m. However, therewere still large numbers of calanoid copepods present in the samples ata depth of 25 m (just above the oxythermocline). The two samplestaken below the oxythermocline (at 35 m) were almost devoid of zoo-plankton (containing only 175 and 83 animals respectively).

4. Discussion

In the autumn of both 2008 and 2009, the north basin of LoughHyne contained large numbers of sprat. During daytime the spratformed dense schools with predatory mackerel close by. The spratthemselves were consuming zooplankton; samples taken in 2008showed the presence of copepods and decapod larvae in their sto-machs. Sprat were found in those parts of the lough where water ex-change is minimal. Few sprat were found in the south basin, wheretidal replacement of water is highest (Bassindale et al., 1957).

Acoustically clear water volumes were found around the spratschools during daytime and these volumes were almost devoid of thelarger zooplankton (92.7% reduction overall). The sprat had grazedthese volumes of water heavily and had removed almost all decapod

Table 4Acoustic volume backscattering strengths corresponding to zooplankton samplings atdifferent water depths in ‘sprat’ areas and ‘no sprat’ areas.

Zooplankton Sv (dB re m−1)

Site Depth A. ‘sprat’ B. ‘no sprat’

1. 12 m −77.7 −68.72. 12 m −78.9 −67.43. 15 m −78.0 −67.84. 15 m −77.5 −66.75. 8 m −80.5 −66.86. 8 m −85.9 −66.1

larvae and calanoid copepods, and most bivalve larvae. The spratschools had less impact on cladocerans and their impact on gastropodlarvae was not significant. It is evident that the presence of spratchanges and skews the size distribution of calanoid copepods withinthe north basin, removing larger individuals.

Grünbaum (1998) suggested that schoolingmight facilitate a searchfor resources such as food. By contrast, we have shown that sprat gath-ered together in dense compact schools deplete their surroundings ofzooplankton andmay become food-limited. This limitationmaybecomemore pronounced as the day goes on. At night, dispersal of the sprattakes place over a wider area of the north basin and perhaps also overthe western trough. The individual fish are more widely spaced andthey extend over a wider area, increasing their ability to forage.

Williams (1966) pointed out that schooling is particularly evidentin fish inhabiting open waters and that it allows individual fish to re-duce their exposure to predation. The aggregation of sprats intoschools during daytime provides a defence against visual predatorslike mackerel. However, the formation of large schools reduces feedingopportunities. Within such a school the food will be used up and onlythose fish on the periphery will have an opportunity to encounter andconsume food items. Hamner and Hamner (2000) have emphasisedthat schoolingmay create an internal microenvironment of accumulatedwaste products, reduced oxygen, parasites and diseases — to which wecan now add food depletion. At night, when visual predators like mack-erel are least effective and schooling is no longer required as a defenceagainst predation, the schools break up.

Thus, our findings confirm that although schooling may conferbenefits to individual fish, such as protection from predators, school-ing has concomitant disadvantages, in particular in terms of competi-tion for food. Although in daytime the school is a safer place to be, atnight it offers few advantages, while the breakup of the school allowsmore freedom of movement for foraging and feeding.

It was evident that zooplankton echo strength was lower in thenorth basin compared with the western trough and the south basin,reflecting the impact of higher grazing levels by sprat in the northbasin. In shallow freshwater lakes it is known that the presence ofplanktivorous fish populations affects the zooplankton community,with additional impact upon phytoplankton. Predation by fish leadsto a shift from a community dominated by Daphnia to one dominatedby Bosmina and cyclopoid copepods, and, at high fish predation, toone dominated by rotifers and cyclopoid copepods (Gulati, 1990;Jeppesen et al., 1992). There is a shift towards dominance by small-bodied zooplankton as a result of fish predation, which changes thegrazing pressure upon phytoplankton. A negative correlation betweenfish and zooplankton abundance has been observed acoustically in afreshwater reservoir (Swierzowskia et al., 2000).

Within Lough Hyne, although areas depleted of zooplankton wereonly detected around the sprat schools during daytime, it is likely thatgrazing by the sprat increases at night as a result of thewider separationbetween individual fish. There is some evidence from the echograms ofa vertical migration of zooplankton from just above the seabed intomid-water at dusk that may increase food availability for the sprat atnight.

The zooplanktonic community of Lough Hyne has been extensivelystudied in recent years, notably by Rawlinson et al. (2004, 2005a,2005b). Vertical migration by dominant zooplankters (copepods, mol-luscan larvae) is complex, with some species showing negligible verticalmigration and others showing diel migrations, the amplitude of which isaffected by site within the Lough, turbulence and tidal cycle (Rawlinsonet al., 2004). However, most species showed ‘normal’ vertical migration(i.e. movement towards the surface at night). Nocturnal migration ofzooplankton into surface waters was confirmed by neustonic sampling(Rawlinson et al., 2005a). It is possible that some of the observed upwardmovement of echoes might represent benthonic forms, but typicallybenthonic groups such as harpacticoid copepodswere rare in the studiesof Rawlinson et al. (2004, 2005a,b) andmost of the seabed in the Lough is

Table 5Plankton sample results collected from the north basin of Lough Hyne on the 7th of September 2009.

Calanoid copepods Cladocerans Decapod larvae Gastropod larvae Bivalve larvae All animalsa

Site pair A. sprat B. no sprat A. sprat B. no sprat A. sprat B. no sprat A. sprat B. no sprat A. sprat B. no sprat A. sprat B. no sprat

1. 15 m 29 1537 8 12 0 6 12 93 6 345 94 20232. 12 m 81 3394 9 23 0 15 102 181 50 431 279 40853. 15 m 57 4645 4 5 0 10 66 189 26 229 181 50914. 15 m 263 1630 5 5 0 10 47 75 74 141 425 16305. 8 m 209 3691 0 18 2 12 93 200 74 439 394 44146. 8 m 73 5005 0 25 0 22 117 370 110 529 319 5999Mean 118.7 3317 4.3 14.7 0.33 12.50 72.8 184.7 56.7 352.3 282 3874Median 77 3543 4.5 15 0 11 79.5 185 62 388 299 4250pb 0.0051 0.0435 0.0036 0.0542 — NS 0.0050 0.0051

p Valuesb0.05 indicate significant differences. NS = not significant.a ‘All animals’ includes taxa where numbers were too low, or spatial distribution too patchy, to permit statistical analysis.b Indicates p values derived from Mann–Whitney U tests of the medians recorded from ‘sprat’ and ‘no sprat’ volumes.

Table 6Proportional reduction in the number of animals between sample volumes with andwithout sprat (percentage differences in terms of means).

Taxa % reduction produced by sprat schools

1. Calanoid copepods 96.42. Cladocerans 70.53. Decapod larvae 97.44. Gastropod larvae 60.6 NS5. Bivalve larvae 83.9

All animals 92.7

NS = not significant.

64 A. Hawkins et al. / Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

of a soft-bottom nature and inherently lower in benthonic diversity thanvegetated substrates.

The heavy grazing of sprat upon the larger zooplankters withinLough Hyne, as indicated by our plankton sampling, may significantlyreduce the overall abundance of zooplankton, as shown by the re-duced echo strengths within the north basin. Reduced grazing bythe zooplankton may in turn result in changes to the phytoplankton,affecting the overall ecology of the lough.

Marked differences in plankton abundance between Lough Hyneand outside coastal waters have been observed (Jessopp and McAllen,2008; Johnson and Costello, 2002). Dinoflagellates, diatoms, tintinnids,copepods, and nauplii were more abundant in samples fromwithin thelough (Johnson and Costello, 2002). A similar pattern was observed forcnidarian zooplankton (Ballard andMyers, 1997). It is not clear to whatextent these differences in zooplankton reflect different conditions orsimply retention within the lough. Rawlinson et al. (2005a,b) havereported a net import of zooplankters to the lough during somemonthsof the year. However, Jessopp and McAllen (2008) concluded that

Fig. 6. Location of plankton samples collected by pumping from Lough Hyne on the 7thof September 2009. Closed circles are ‘sprat’ samples; open circles are ‘no sprat’samples. Grey circle is the western trough sampling area.

Lough Hyne was not acting as an overall importer or exporter of larvalabundance, although over short temporal scales there was scope forhigh levels of import and export of some zooplankton. They suggestedthat limited water exchange at Lough Hyne, shown by the long flushingtime of c 41 days (Johnson et al., 1995),might be limiting larval dispersal,creating an isolated, self-seeding area.

From the current study it seems that grazing upon the largerzooplankters by sprat schools plays an important role in determiningthe composition of the plankton within the lough, especially within thenorth basin. The presence of several tonnes of sprat within the lough(Knudsen et al., 2009) may greatly affect the richness and turnover ofzooplankton andmay therefore influence the overall ecological character-istics of this enclosedmarine reserve. Cassini et al. (2008) have remarkedthat in the Baltic Sea increases in sprat populations have resulted in adecline in zooplankton and an increase in phytoplankton. Above a certainthreshold, sprat abundance becomes the main forcing function forzooplankton variation. In LoughHyne, the abundance of fish at the highertrophic levels, especially mackerel and sprat, probably results in top-down regulation of the zooplankton composition and abundance. Aknock-on ecological effect is likely to be a reduction in the extent of

Table 7Size selection of calanoid copepods by sprat schools. Size measurements (overalllength) made upon randomly chosen copepods measured beneath binocular micro-scope (accuracy 20 μ). Normality test indicates result of Anderson Darling test; * indi-cates non-normality. Analysis of size selection was only feasible in the case ofsamples 4 and 5 where several hundred copepods were present in the ‘sprat’ sample.In the case of other samples there were too few calanoid copepods remaining in‘sprat’ samples for statistically safe random selection of copepods for measurement.

Meanlength (μ)

Medianlength (μ)

Normalitytest result

Mood mediancomparison

Station 4 (15 m depth)No sprat sample (n=60) 636 640 p=0.278 pb0.0005Sprat sample (n=60) 542 540 p=0.043*Station 5 (8 m depth)No sprat sample (n=60) 716 710 p=0.523 pb0.0005Sprat sample (n=60) 519 500 pb0.0005*

Fig. 7. Composition of zooplankton samples collected from the Western Trough on the7th of September 2009. Open symbols are duplicate samples, closed symbols aremeans. Circles indicate total zooplankton numbers per 257 l sample; squares indicatenumbers of calanoid copepods; diamonds indicate numbers of molluscan larvae(sums of gastropod and bivalve larval numbers). Note that the oxythermocline waspresent at a depth of about 28 m.

65A. Hawkins et al. / Journal of Experimental Marine Biology and Ecology 411 (2012) 59–65

browsing upon phytoplankton, enhancing the intensity and duration ofphytoplankton blooms within the Lough.

Acoustic images of the western trough showed zooplankton-freevolumes beneath the oxythermocline. Pumped samples from beneaththe thermocline showed a very low incidence of zooplankters, con-firming earlier findings by Rawlinson et al. (2004). These observa-tions provide strong evidence that zooplankters avoid the hypoxicpart of the water column, though this part of the water column isalso rich in sulphide, so the cue for avoidance is uncertain.

5. Conclusions

During daytime sprat gather in dense schools in the eastern part ofthe north basin of Lough Hyne, and we have suggested that formationof these schools is a defence against predation by mackerel. However,these schools rapidly deplete their surroundings of larger zooplanktersand extensive volumes of water around them are largely devoid of zoo-plankton. The absence of food organisms in the vicinity of the spratplumes suggests that fish within the schools may be substantiallyfood-limited during the day. At night the schools break up, perhapsallowing the individual sprat to forage more effectively. Overall thereis a general depletion of zooplankton within the north basin of LoughHyne as a result of predation by sprat.

This is apparently the first study in which acoustically clear volumesofwater have been validated as almost devoid of zooplankton; it is there-fore the first study that has unequivocally demonstrated that schoolingsprat may remove almost all food from the water around them. It isalso a particularly good demonstration of prey size selection by a filter-feeding fish. Although schooling may confer benefits to individual fishin terms of protection from predation, there are concomitant disadvan-tages in terms of a depletion of food within and adjacent to the school.

Heavy grazing by sprat upon zooplankton both during the day andnight may in turn have a significant impact upon grazing by thezooplankton on the phytoplankton and may affect the overall ecologyof the enclosed lough significantly.

The absence of zooplankton below the oxythermocline in thewestern trough of Lough Hyne strongly suggests that the planktersavoid the hypoxic part of the water column.

Acknowledgements

The studies at Lough Hyne during 2009 were carried out under Re-search Permit Number R30 - 35/08 from the Irish Dept of Environment,Heritage and Local Government. The Royal Society of Edinburgh provideda Travel Assistance Grant to Professor Hawkins. The authors are gratefulto Alistair Thomson and Susan Hawkins for their invaluable assistancewith the fieldwork. [SS]

References

Aglen, A., 1983. Random errors of the acoustic fish abundance estimate in relation tothe survey grid density applied. FAO Fish. Rep. 300, 293–298.

Aglen, A., 1989. Empirical results on precision–effort relationships for acoustic surveys.ICES CM 1989/B, 30. (28 pp.).

Balk, H., Lindem, T., 2007. Sonar4 and Sonar5-Pro post processing systems. OperatorManual, Version 5.9.7. Balk and Lindem Data Acquisition, Oslo, Norway.

Ballard, L., Myers, A., 1997. Vertical distribution, morphology and diet of Proboscidactylastellata (cnidaria: limnomedusae) in Lough Hyne marine nature reserve, Co. Cork,Ireland. J. Mar. Biol. Assoc. UK 77, 999–1009.

Bassindale, R., Ebling, F.J., Kitching, J.A., Purchon, R.D., 1948. The ecology of the LoughIne Rapids with special reference to water currents. I. Introduction and hydrogra-phy. J. Ecol. 36, 305–322.

Bassindale, R., Davenport, E., Ebling, F.J., Kitching, J.A., Sleigh, M.E., Sloane, J.F., 1957.The ecology of the Lough Ine Rapids with special reference to water currents. VI.Effects of the Rapids on the hydrography of the South Basin. J. Ecol. 45, 879–900.

Cassini, M., Lovgren, J., Hjelm, J., Cardinale, M., Molinero, J.-C., Kornilovs, G., 2008.Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proc.R. Soc. B 275, 1793–1801.

Foote, K.G., Knudsen, H.P., Vestnes, G., MacLennan, D.N., Simmonds, E.J., 1987. Calibrationof acoustic instruments for fish density estimation: a practical guide. ICES CooperativeResearch Report, p. 144 (69 pp.).

Grünbaum, D., 1998. Schooling as a strategy for taxis in a noisy environment. Evol. Ecol.12, 503–522.

Gulati, R.D., 1990. Structural and grazing responses of zooplankton community to bio-manipulation of some Dutch water bodies. Hydrobiologia 200 (201), 99–118.

Hamner, W.M., Hamner, P.P., 2000. Behavior of Antarctic krill (Euphausia superba):schooling, foraging, and antipredatory behaviour. Can. Bull. Fish. Aquat. Sci. 57,192–202.

Jeppesen, J.E., Sortkjzr, O., Sondergaan, L.M., Erlandsen, M., 1992. Impact of a trophiccascade on heterotrophic bacterioplankton production in two shallow fish-manipulated lakes. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37, 219–231.

Jessopp, M.J., McAllen, R., 2008. Go with the flow: tidal import and export of larvaefrom semi-enclosed bays. Hydrobiologia 606, 81–92.

Johnson, M.P., Costello, M.J., 2002. Local and external components of the summertimeplankton community in Lough Hyne, Ireland a stratified marine inlet. J. PlanktonRes. 24, 1305–1315.

Johnson, M.P., Costello, M.J., O'Donnell, D., 1995. The nutrient economy of a marineinlet Lough Hyne, south–west Ireland. Ophelia 41, 137–151.

Kitching, J.A., Ebling, F.J., Gamble, J.C., Hoare, R., McLeod, A.A.Q.R., Norton, T.A., 1976.The ecology of Lough Hyne. XIX. Seasonal changes in the western trough. J.Anim. Ecol. 45, 731–758.

Knudsen, F.R., Hawkins, A.D., McAllen, R., Sand, O., 2009. Diel interactions betweensprat and mackerel in a marine lough and their effects upon acoustic measure-ments of fish abundance. Fish. Res. 100, 140–147.

MacLennan, D.N., Fernandes, P.G., Dahlen, J., 2002. A consistent approach to definitionsand symbols in fisheries acoustics. ICES J. Mar. Sci. 59, 365–369.

McAllen, R., Davenport, J., Bredendieck, K., Dunne, D., 2009. Seasonal structuring of abenthic community exposed to regular hypoxic events. J. Exp. Mar. Biol. Ecol.368, 67–74.

Rawlinson, K.A., Davenport, J., Barnes, D.K.A., 2004. Vertical migration strategies withrespect to advection and stratification in a semi-enclosed lough: a comparison ofmero- and holozooplankton. Mar. Biol. 144, 935–946.

Rawlinson, K.A., Davenport, J., Barnes, D.K.A., 2005a. Temporal variation in diversityand community structure of a semi-isolated neuston community. Biol. Environ.105B, 107–122.

Rawlinson, K.A., Davenport, J., Barnes, D.K.A., 2005b. Tidal exchange of zooplanktonbetween Lough Hyne and the adjacent coast. Estuar. Coast. Shelf Sci. 62, 205–215.

Swierzowskia, A., Godlewska, M., Póltorak, T., 2000. The relationship between thespatial distribution of fish, zooplankton and other environmental parameters inthe Solina reservoir, Poland. Aquat. Living Resour. 13, 373–377.

Williams, G.C., 1966. Adaptation and Natural Selection. Princeton University Press,Princeton NJ.