ORIGINAL PAPER

Lyngbya majuscula blooms and the diet of small subtropicalbenthivorous fishes

Ben L. Gilby • Dana D. Burfeind • Ian R. Tibbetts

Received: 19 April 2010 / Accepted: 27 September 2010 / Published online: 28 November 2010

� Springer-Verlag 2010

Abstract Increasing concerns about the ecological

impacts of ongoing and possibly worsening blooms of the

toxic, carcinogenic cyanobacteria Lyngbya majuscula in

Moreton Bay, Australia, led us to assess differences in

meiofaunal prey assemblages between bloom and non-

bloom substrates and the potential dietary impacts of dense

L. majuscula blooms on the omnivorous benthivore, the

Eastern Long-finned Goby, Favonigobius lentiginosus and

the obligate meiobenthivorous juveniles of Trumpeter

Whiting, Sillago maculata. Marked differences in inver-

tebrate communities were found between sandy and

L. majuscula bloom foraging substrates, with copepods

significantly more abundant (18.49% vs. 70.44% numerical

abundance) and nematodes significantly less abundant

(55.91% vs. 1.21% numerical abundance) within bloom

material. Gut analyses showed that bentho-planktivorous

fishes exposed to L. majuscula in captivity had consumed a

significantly greater quantity of prey by both total number

(P \ 0.0019) and volume (P \ 0.0006) than fish exposed

to sand treatments. Thus, it is likely for such fishes that

L. majuscula blooms increase rates of prey encounter and

consumption, with consequent changes in trophic rela-

tionships through shifts in predator–prey interactions

between small benthivorous fishes and their meiofaunal

prey.

Introduction

The incidence, density and frequency of harmful algal

blooms (HABs) have increased throughout the world in

recent years (Hallegraeff 1993; Anderson et al. 2002),

meaning that their related impacts have broadened. While

blooms mostly affect local ecosystems and the usability of

bloom areas for recreation, increasing HAB prevalence has

the potential to increase monitoring costs and impact

fisheries. Despite this, little is known about their impacts

on wildlife, especially at an individual species level

(Arthur et al. 2008). Lyngbya majuscula is a toxic, benthic

cyanobacterium that attaches to a variety of substrates,

including seagrasses, mussel and oyster colonies and sandy

substrates and can become a damaging HAB in tropical and

subtropic marine habitats (Albert et al. 2005). While it

grows naturally in shallow marine habitats along the east

coast of Australia, damaging blooms have been increasing

in frequency and intensity near some urban centres since

the mid-1990s (e.g. Moreton Bay, adjacent to Brisbane;

Dennison et al. 1999; Osborne et al. 2001; Pittman and

Pittman 2005; Watkinson et al. 2005; Garcia and Johnstone

2006; Roelfsema et al. 2006). In addition to the direct

effects of smothering of seagrasses, coral and other benthic

substrates, accumulation of L. majuscula secondary

metabolites has been found in organisms that consume

L. majuscula (Pennings and Paul 1993; Pennings et al.

1996; Capper et al. 2005); however, the effect of

L. majuscula blooms on more motile species, especially

fishes and crustaceans, remains poorly understood (Pittman

and Pittman 2005).

Communicated by U. Sommer.

B. L. Gilby � D. D. Burfeind � I. R. Tibbetts (&)

School of Biological Sciences,

The University of Queensland, St Lucia,

QLD 4072, Australia

e-mail: i.tibbetts@uq.edu.au

D. D. Burfeind

Australian Rivers Institute, Griffith University,

Gold Coast Campus, Southport, QLD 4222, Australia

123

Mar Biol (2011) 158:245–255

DOI 10.1007/s00227-010-1555-9

In Moreton Bay, L. majuscula bloom size and intensity

are strongly influenced by iron, phosphorus and organic

carbon (Elmetri and Bell 2004; Albert et al. 2005; Wat-

kinson et al. 2005; Ahern et al. 2006a, b, 2007a, b, 2008).

Inputs of anthropogenic pollutants and runoff from poorly

managed land-based development and land clearing are

thought to have increased annual L. majuscula blooms in

some parts of this large bay (Watkinson et al. 2005). While

bloom events can occur year round, the larger, most rapidly

expanding blooms occur late in the Austral summer from

December to April, when water temperatures ([22�C) and

ambient light levels are closest to the optimum for bloom

expansion (Watkinson et al. 2005). Blooms can expand

rapidly, especially in shallow areas (\30 m, Izumi and

Moore 1987) with elevated iron concentrations (Ahern

et al. 2008), reaching an average peak biomass of

210 gdw-1 m-2 (Watkinson et al. 2005).

L. majuscula blooms can dramatically change the faunal

assemblages of the ecosystems in which they occur.

Affected areas typically exhibit decreased biodiversity

across all taxa, especially in response to decreased seagrass

abundance and lower oxygen availability (Cruz-Rivera and

Paul 2000; Pittman and Pittman 2005). However, species of

meiofauna that can withstand the typically detrimental

bloom impacts and/or feed on cyanobacteria thrive during

blooms (Pennings et al. 1996; Gamenick et al. 1997; Nagle

et al. 1998; Capper et al. 2005; Garcia and Johnstone 2006;

Ahern et al. 2008). Changes in faunal communities are

especially prevalent in the meiofauna of sediments below

L. majuscula blooms, in the infaunal communities of the

bloom itself and in surrounding seagrasses (Garcia and

Johnstone 2006). Anecdotal field observations suggest

significant increases in some nematode, amphipod, cope-

pod and polychaete species within areas affected by large

blooms (Pittman and Pittman 2005; Andersson et al. 2009).

Increases in these taxa within L. majuscula blooms may be

driven by increased habitat structural complexity enhanc-

ing predator avoidance, providing increased access to food

or a combination of the two (Pennings 1990; Pennings and

Paul 1993).

Many estuarine fish species pass through an obligatory

meiobenthic feeding stage in shallow coastal waters and

rely heavily on benthic copepods in their diet (Coull et al.

1995; Krueck et al. 2009). Therefore, meiofaunal com-

munity change is important when blooms occur in critical

fish feeding and nursery habitats, including seagrass beds,

and subtidal and intertidal sandy habitats (Beck et al. 2001;

Pittman and McAlpine 2003; Pittman and Pittman 2005).

Altered sediment conditions and associated changes in

meiofaunal communities during L. majuscula blooms have

the potential to disrupt the feeding regime of bentho-

planktivorous fishes and their roles in fisheries and local

ecosystems (Long and Ross 1999; Hua et al. 2006).

Changes in prey abundance and distribution may force

juvenile fish and the adults of small species to respond

behaviourally by avoiding L. majuscula-dominated habitat

(Eggleston et al. 1998; Lindholm et al. 2001; Thrush et al.

2003) or facilitate predation by concentrating preferred

meiofaunal prey species for some benthivorous fishes

(Pittman and Pittman 2005).

Evidence of changes in meiofaunal communities in the

habitats adjacent to L. majuscula blooms (Beck et al. 2001;

Pittman and McAlpine 2003; Pittman and Pittman 2005)

suggests that the results of experiments merely contrasting

meiofauna and fish feeding relationships between bloom

material and adjacent substrates could be misleading, par-

ticularly amongst the benthic copepods, many of which

undergo diurnal vertical migration and recruitment to

adjacent habitats (Jacoby and Greenwood 1989). Thus

we evaluated the potential ecological impacts of dense

L. majuscula blooms on meiobenthivorous fishes by com-

paring the meiofaunal community of a typical, sandy

intertidal substrate not influenced by L. majuscula blooms

with that of L. majuscula bloom matrix to gauge differ-

ences in potential prey between the two substrates. The

chosen substrates were used as a proxy for a benthic

ecology independent of L. majuscula blooms and secondly

as a proxy for dense blooms where access to underlying

sandy substrates is precluded either by bloom density or

depressed water quality near the sediment–water interface.

We then relate these findings to the affect of a simulated

L. majuscula bloom on the diet of two subtropical bentho-

planktivorous fishes in captivity. We hypothesize a sig-

nificant difference in both abundance and diversity of

meiofauna between the two substrates, with L. majuscula

blooms creating structure for taxa of micro-invertebrates

not available in sand interstices and that this will be

reflected in the diversity of prey captured by the fishes.

Materials and methods

Collection sites

Moreton Bay is a large (3,400 km2), mostly shallow, sandy

embayment in southeast Queensland, Australia (Fig. 1). To

the west, the bay is bordered by its catchment area,

including the extensive urban development of Brisbane

(total catchment population 2.73 million; EHMP 2008) and

to the east by three large sand islands (Moreton, North and

South Stradbroke). Lyngbya majuscula was collected by

hand at two sites; Eastern Banks (27�270 S, 153�230 E), a

series of sand banks and shallow seagrass beds in clear

oceanic water in eastern Moreton Bay, adjacent to North

Stradbroke Island (27�510 S, 153�410 E) and on the west

coast of North Stradbroke Island on One Mile Beach, south

246 Mar Biol (2011) 158:245–255

123

of One Mile Harbour, Dunwich (Fig. 1). These sites are

well known for L. majuscula blooms, having exhibited

blooms in excess of 8 km2 since 1999 and are monitored

for L. majuscula by the Queensland Department of Envi-

ronment and Resource Management throughout the year

(Queensland DERM 2010).

Comparison of meiofaunal communities

L. majuscula was collected by carefully placing clumps

into Ziploc bags immediately upon collection and whilst

still underwater to avoid loss of meiofauna. This was

repeated twice on three separate sampling days approxi-

mately 3 weeks apart for a total of six samples, providing a

good representation of the bloom’s highest density period

when the associated meiofaunal community is likely to be

well developed. Sediment cores were taken from One Mile

Beach, on the sandy intertidal flats adjacent to a seagrass

bed and at least 600 m from existing L. majuscula blooms.

Cores were collected using a modified 50-ml syringe,

yielding an overall sample of 30 ml. Cores were collected

whilst gathering sand for each day’s feeding trials (see next

section) and took place over a period of approximately

2 months (for a total of n = 9). Cores were fixed in 10%

neutral buffered formalin/seawater.

The combination of marked differences in the physical

characteristics of the two substrates (i.e. unlike sand,

L. majuscula matrix cannot be sorted using sieves) and the

delicate bodies of copepod meiofauna (i.e. damage caused

by teasing apart the L. majuscula matrix) required different

approaches to surveying their respective meiofaunal com-

munities. Meiofauna were extracted from L. majuscula by

placing a 15 g (wet weight) subsample into a shallow Petri

dish of seawater and shining a cold light source to one side

of the clump in a darkened room. Many vagile meiofauna

are positively phototactic and congregate around the light

source, facilitating collection via pipette. Other meiofauna,

still within the clump and/or those not attracted to light,

were collected by teasing open the remaining L. majuscula

filaments under a dissecting microscope with a probe and

removing individuals with a pipette. Meiofauna were then

preserved in 70% ethanol/seawater solution before being

counted under an Olympus SZX9 dissection microscope

with a Graticules LTD Sedgwick-Rafter counting cell. For

sand samples, meiofauna were removed via decanting with

a 63-lm sieve and counted under an Olympus SZX9

microscope in a glass sorting chamber marked with 1-mm

grid squares. Identification was based on the procedure

described by Giere (2009), and preliminary surveys indi-

cated that the meiofauna in sand and L. majuscula could be

most effectively surveyed using the following categories;

Metis holothuriae (a large, red harpacticoid copepod,

which was included as a separate category due to their

dominance in L. majuscula bloom material), Other

Copepoda, Nematoda, Polychaeta, Amphipoda, Ostracoda,

Bivalvia, Gastropoda, Penaeidae, Other Crustacea and

Other. Although larger macrograzers [e.g. small sea hares

(20–40 mm total length) and top snails (to 25 mm)] were

common throughout L. majuscula blooms, these are

unlikely to be targeted by the small, gape-limited

Fig. 1 Map of Moreton Bay,

Queensland, Australia, showing

the Eastern Banks and Dunwich

Lyngbya majuscula collection

sites

Mar Biol (2011) 158:245–255 247

123

bentho-planktivorous fishes that are the focus of this study

and were therefore excluded from consideration.

Feeding experiment

Adults and juveniles of the locally abundant Eastern Long-

finned Goby, Favonigobius lentiginosus [11–45 mm total

length (TL)] and juveniles (\45 mm TL) of the commer-

cially important Trumpeter Whiting, Sillago maculata,

were collected as representatives of second-level consum-

ers present near L. majuscula blooms. F. lentiginosus are

primarily meiobenthic but also consume smaller juvenile

Sillago spp. and detrital material (C. Chargulaf and I.

R. Tibbetts, unpublished data), while juvenile S. maculata,

of the size range under consideration, are obligate meio-

benthivores (Coull et al. 1995; Krueck et al. 2009). Fishes

were collected from One Mile Beach, Dunwich, North

Stradbroke Island by either seine net or hand held dip net

and placed directly into aerated aquaria at the Moreton Bay

Research Station (ca. 150 m from collection site). Fish

were acclimated for at least 18 h to minimize impacts of

stress and to purge their guts in preparation for experi-

mentation (Coull et al. 1995).

Aquarium-based trials were used to determine the

feeding regime of the fishes in simulated dense L. ma-

juscula blooms and over subtidal sand collected from One

Mile Beach. Plastic aquaria (30 9 20 9 20 cm) were

filled with 4 L of seawater and aerated. In twenty separate

tanks we created replicates of each of two treatments with

similar volumes of foraging substrate; one with 60 g

(saturated wet weight) of freshly collected L. majuscula

bloom material (collected on same date and location as

meiofauna survey blooms) and the other with 150 g of

unwashed saturated subtidal sand from One Mile Beach.

Foraging substrates were left saturated as blotting to

remove water either damages or removes meiofauna (pers

obs IT). One fish was added to each treatment tank and

allowed to forage for 6 h (as per Coull et al. 1995). Fish

were euthanized with an overdose of clove oil in seawater

and frozen for subsequent gut content analysis. We con-

ducted three trials (n = 30 for each species and treat-

ment); however, fish with empty guts were excluded from

analyses for two reasons: (1) fish that had not fed were

not informative in terms of our chosen statistical methods

and (2) such fish may have been reacting adversely to the

experimental conditions or collection and not behaving

normally.

Gut content analysis was used to determine whether: (1)

fish fed during trials; (2) any L. majuscula was ingested;

and (3) the key prey categories targeted. Gut contents were

analysed as per Linke et al. (2001), using the same 11

categories as the previously described L. majuscula meio-

faunal surveys, with the inclusion of the Trematoda (which

are gut parasites of these species). In instances where parts

of whole organisms were found, only intact head sections

were counted. Fish total length, number of empty guts, prey

category volume (via the points method, as described in

Hynes 1980), total gut contents volume (sum of all prey

category volumes) and gut fullness (ratio of fish total

length to total gut contents volume) were also recorded.

Individuals with empty guts were not included in estimates

of prey item proportion; thus, the final number of fishes

included in statistical analyses is less than the total number

of individuals dissected.

Proportion by volume of a prey item in a species diet

was calculated as per Zaret and Rand (1971);

Pij ¼PN

X¼1 Pix

Njð1Þ

where Pix is the volumetric proportion of food category i in

the gut of individual x, and Nj is the number of individuals

examined in species j. Each individual fish that contained

prey was assigned equal weight irrespective of gut fullness

or total length.

An electivity index (Ivlev’s E) was used to compare

proportions of prey items in the diet with their proportions

in the substrate;

Ei ¼ri � pi

ri þ pið2Þ

where ri is proportion of food i in the diet of an individual

species (as per Eq. 1) and pi is the proportion of food i in

the environment. Ivlev’s E gives a value of between plus

and minus one for selectivity and avoidance, respectively,

and a value of zero for random, non-specific feeding (see

Chesson 1978 for details).

Student’s t tests (a = 0.05) were used to detect any

differences in gut fullness and total prey consumption

between treatments. Multidimensional scaling (MDS)

ordination plots were used to assess community differ-

ences and to elucidate differences in community com-

position, both in natural abundance and in gut content

data. Data for MDS ordinations were fourth root trans-

formed in Primer v5 (PrimerE) to reduce the influence of

highly abundant prey groups, and the Bray-Curtis index

of similarity was used to eliminate the influence of

shared absences. One-way analysis of similarity (ANO-

SIM) was conducted for community composition data to

test the significance of the community differences rep-

resented in MDS ordinations. ANOSIM is a multivariate

test of significance that works under the principle that if

the chosen factors are meaningful, samples from within

groups should be different from samples from other

groups; thus, the null hypothesis is that there is no dif-

ference between groups (for further detail, see Clarke

and Warwick 1994).

248 Mar Biol (2011) 158:245–255

123

Results

Meiofaunal communities

Copepods dominated the meiofaunal communities of the

sampled Lyngbya majuscula blooms with 70.40% of the

total count (Fig. 2). Metis holothuriae was the most

abundant copepod, comprising 29.51% of the total

numerical abundance and 20.10% of the total meiofaunal

biomass within the L. majuscula (Table 1). Amphipods

were the second most abundant group (12.96% numeri-

cally) followed by ostracods (9.71%). The numbers of

nematodes found during L. majuscula meiofauna surveys

were very low (1.21%) in comparison with their relative

dominance in sandy habitats (55.91%). Members of the

‘Other’ category contributed 5.67% of total individuals and

were mostly bivalves and gastropods but also included

some isopods, polychaetes, tanaids and oligochaetes. The

meiofaunal communities of sand substrates were domi-

nated by copepods and nematodes with remaining taxa

together comprising only 25.91% of total numerical

abundance and 19.54% of biomass (Table 1). Polychaetes,

ostracods and bivalves were the next most common taxa;

however, each contributed a maximum of only 3.80%

to the total numerical abundance of potential prey.

M. holothuriae were relatively uncommon in sand substrate

samples (0.32%). Significant differences in the natural

abundance of meiofaunal communities between bloom and

sandy habitats are reflected in the clear separation of the

two habitats in community structure MDS ordinations

(ANOSIM, P = 0.002; Fig. 3). No effect of sampling day

was found on meiofaunal abundance (ANOVA, F(2,36) =

0.60246, P = 0.55289).

Feeding trials

We examined gut contents from 30 individuals in each

treatment; however, only 28 S. maculata and 20 F. lentigi-

nosus from L. majuscula treatments and 29 S. maculata and

16 F. lentiginosus from sand treatments actually contained

prey. Diets were dominated numerically by copepods in both

L. majuscula (63.16% in F. lentiginosus and 76.75% in

S. maculata) and sand treatments (28.69% in F. lentiginosus

and 50.51% in S. maculata), and while nematodes and

ostracods were secondarily preferred in the sand treatment,

amphipods were second most dominant during L. majuscula

trials (Fig. 4). Examination of gut contents using the dis-

secting microscope failed to reveal any visible L. majuscula

material or other plant fragments in any gut of either species.

Ivlev’s E electivity values indicate a positive selection

(E C 0.18) for copepods by both species in both treatments

(Table 2). Nematodes were positively selected for in

L. majuscula treatments (E C 0.545), yet avoided in sand

treatments (E B -0.264), where they were the most com-

mon meiofaunal taxa. M. holothuriae was avoided by both

species in L. majuscula treatments, with strongly negative

E values of -0.864 and -0.761 for S. maculata and

F. lentiginosus, respectively. Amphipods also gave

Fig. 2 Average percentage

abundance (±SE) of meiofauna

within Lyngbya majusculablooms and sand cores from

Moreton Bay. The category

‘Other’ contained mostly

bivalves, small gastropods,

tanaids, isopods and other

annelids, including oligochaetes

Table 1 Average percentage numerical abundance and biomass (calculated by via the points method, as described in Hynes 1980) for

meiofaunal categories found in within Lyngbya majuscula blooms and on a subtidal sand flat in Moreton Bay, Queensland, Australia

Measurement Other Copepoda Metis holothuriae Nematoda Amphipoda Ostracoda Other

Lyngbya majuscula numerical percentages 40.90 (2,089) 29.54 (1,509) 1.21 (69) 12.96 (661) 9.71 (496) 5.68 (290)

Lyngbya majuscula biomass percentages 27.78 20.07 1.65 35.21 4.62 10.68

Sand numerical percentages 18.17 (169) 0.32 (3) 55.91 (520) 0.65 (6) 3.76 (35) 21.18 (197)

Sand biomass percentages 11.25 0.20 69.22 1.60 1.63 16.11

Total number for each category of meiofauna is given in parenthesis

Mar Biol (2011) 158:245–255 249

123

negative electivity values in both treatments by both spe-

cies. Ostracods were strongly favoured by F. lentiginosus

in sand but negatively selected for in all other treatments.

Individuals from both species in the L. majuscula

treatments consumed more prey by both volume (two-

sample t-test: S. maculata, t26 = 1.67, P = 0.00003;

F. lentiginosus, t21 = 1.69, P = 0.00082) and number

(two-sample t-test: S. maculata, t26 = 1.67, P = 0.00006;

F. lentiginosus, t19 = 1.69 P = 0.00627) than in sandy

environments (Fig. 5). Both fish species also consumed a

greater diversity of prey groups in L. majuscula treatments

than in sand treatments (Table 3). Indeed, during L. ma-

juscula treatments, 66.67% of S. maculata and 15.00% of

F. lentiginosus exhibited a gut fullness ratio of above one,

whereas no individuals of either species demonstrated

ratios greater than one during sand treatments. Gut para-

sites, primarily trematodes, occurred in 63.81% of F. len-

tiginosus stomachs and contributed 13.90% of total gut

contents in the L. majuscula treatments and 70.50% in the

sand treatments. Despite this, there was no significant

effect of treatment (two-sample t-test, t25 = 1.70,

P = 0.05335) on abundance of trematodes. As a result, the

presence of trematodes was deemed to be independent of

treatment, and their gut contents category, Trematodes, was

excluded from gut content analysis.

Multidimensional scaling ordinations of gut contents

following exposure to L. majuscula and sand showed a

distinct separation in the feeding habitats between treat-

ments. In Figs. 6 and 7, L. majuscula samples were mostly

distributed in the centre of the ordination plot with sand

samples distributed peripherally, demonstrating greater

similarities amongst L. majuscula replicates than amongst

sand replicates. This was also found to be the case in

Fig. 3, where L. majuscula points clustered closely,

whereas sand samples showed a looser yet clearly defined

grouping. ANOSIM confirmed these differences with both

S. maculata (P = 0.002) and F. lentiginosus (P = 0.002)

exhibiting significant differences in gut contents between

the two treatments.

Discussion

Meiofaunal survey results indicate dramatic differences in

faunal assemblages between sandy substrates and Lyngbya

Fig. 3 Non-parametric MDS ordination (fourth root transformed,

Bray-Curtis similarity) comparing meiofaunal community composi-

tion of Lyngbya majuscula blooms and sandy environments. Each

point represents one sample from each habitat. These data indicate a

significant difference in community composition (ANOSIM, global

R = 1.0, P = 0.002)

Fig. 4 Average proportions, by

number (±SE) of the four major

prey categories present in the

guts of each species and

treatment

250 Mar Biol (2011) 158:245–255

123

majuscula bloom material. Although large numbers of

copepods were present in both treatments, there was an

order of magnitude difference in the abundance of nema-

todes between L. majuscula (just over 1%) and sand (ca.

50%). Some meiofauna that were less abundant in sandy

habitats were more abundant during blooms, especially

amphipods, ostracods and copepods. Detritivores and

bacterivores (Rieper 1978; Campbell 1995; dos Santos

et al. 2009) are likely to benefit considerably from the

propensity of the L. majuscula matrix to collect detrital

material and promote bacterial growth (Pittman and Pitt-

man 2005). Some species may also have greater physio-

logical tolerance to bloom-related impacts, especially

anoxic conditions (Pittman and Pittman 2005; Watkinson

et al. 2005) and potential toxicity (Osborne et al. 2001;

Capper et al. 2005, 2006a; Gyedu-Ababio and Baird 2006).

Sillago maculata and Favonigobius lentiginosus con-

sume a greater range of prey taxa during simulated

L. majuscula bloom conditions. This results from highly

Table 2 Ivlev’s E electivity values for each prey category from Sillago maculata and Favonigobius lentiginosus during Lyngbya majuscula and

sand microcosm treatments

Species/treatment Other Copepoda Metis holothuriae Nematoda Amphipoda Ostracoda Other

Sillago maculata versus Lyngbya majuscula 0.291 -0.864 0.547 -0.136 -0.189 -1

Sillago maculata versus Sand 0.452 0.649 -0.264 -0.330 -0.247 0.843

Favonigobius lentiginosus versus Lyngbya majuscula 0.180 -0.761 0.545 -0.123 -0.029 -1

Favonigobius lentiginosus versus Sand 0.218 -1 -0.741 -1 0.797 -1

Positive numbers indicate positive prey selection

Fig. 5 Mean gut fullness ratios (±SE) for Sillago maculata and

Favonigobius lentiginosus after sand and Lyngbya majuscula foraging

treatments

Table 3 Number of prey categories consumed by Sillago maculataand Favonigobius lentiginosus during Lyngbya majuscula and sand

microcosm treatments

Sillago maculata Favonigobius lentiginosus

Sand 8 5

Lyngbya majuscula 11 9

P value 0.0997

(t = 6.33)

0.1772

(t = 3.5)

Student’s t tests were used to find P values

Fig. 6 MDS ordinations comparing gut composition in Sillagomaculata between Lyngbya majuscula bloom conditions and sandy

environments. Each point represents an individual dissected fish.

These data indicate a significant difference in community composi-

tion (ANOSIM, global R = 0.234, P = 0.001)

Fig. 7 MDS ordinations comparing gut composition in Favonigo-bius lentiginosus between Lyngbya majuscula bloom conditions and

sandy environments. Each point represents an individual fish. These

data indicate a significant difference in community composition

(ANOSIM, global R = 0.426, P = 0.001)

Mar Biol (2011) 158:245–255 251

123

favoured prey items becoming more available within

blooms than within sandy environments. Although elec-

tivity indices indicate an avoidance of amphipods during

exposure to L. majuscula conditions, their consumption

increased from almost negligible values in sand treatments

to just over 10% numerically when foraging amongst

L. majuscula material. Specifically, 20.5% of overall

stomach contents in bloom-exposed F. lentiginosus by

volume were amphipods. This reflects the marked increase

in amphipod biomass during blooms (Fig. 2). In addition,

the filamentous matrix structure of L. majuscula material

may increase fishes’ ability to successfully capture prey,

especially through the contrast of colouration between the

darker cyanobacterial matrix and the lighter colouration of

the meiofauna. The increased proportions of preferred

meiofauna prey present during blooms, combined with

increased prey capture success creates an environment for

bentho-planktivores that provides a more consistent supply

of preferred prey items; however, this supply would be

restricted by bloom occurrence and density. Curiously, the

large red harpacticoid Metis holothuriae, which is strongly

contrasted against both L. majuscula and sand, was avoided

in both substrates by both species (E = -0.864 for

S. maculata and E = -0.761 for F. lentiginosus). While

gape limitation might be argued to explain this avoidance

in very small S. maculata, F. lentiginosus can ingest

juvenile Sillago spp (C. Chargulaf, personal communica-

tion), suggesting that this behaviour is unlikely to be due to

a physical constraint and is worthy of further investigation.

Copepods are important in the diets of both S. maculata

and F. lentiginosus (Coull et al. 1995; Krueck et al. 2009;

C. Chargulaf, unpublished data). In substrates where

copepods were less prevalent, the fishes consumed fewer

prey rather than alter their feeding regime, as is demon-

strated by the lower proportion of copepods found within

sandy substrates (Fig. 2), coupled with significantly

decreased gut fullness values in fishes feeding on this

substrate (Fig. 5). However, for nematodes, a greater

abundance was found in guts of fish from the sand treat-

ment than from those exposed to the L. majuscula. This is

reflected in the sand meiofauna community where nema-

todes were numerically dominant. For copepods, a strongly

positive electivity value highlights their importance in the

diets of these meiobenthic fishes. For nematodes, a strongly

positive electivity value, coupled with a very low avail-

ability, also indicates that nematodes are a highly favoured

food item (Fig. 4), likely due to their high abundance in

sandy substrates. This results in increased nematode elec-

tivity values despite their much lower abundance in

L. majuscula. In sandy treatments, the high abundance of

nematodes results in a strongly negative electivity value,

even though the actual number of nematodes consumed

remains relatively static.

Changes in prey availability between the two environ-

ments are indicated by the significant changes in the diets

of these species between the two treatments. This is

reflected by tightly clustered MDS ordinations and signif-

icant ANOSIM results (Fig. 3). The tighter grouping of

L. majuscula communities in MDS ordinations reflects a

lower variability in the presence and abundance of pre-

ferred prey. This also suggests a more patchy distribution

of meiofauna within sandy habitats. With an abundant

supply of preferred prey in bloom material, fishes are no

longer inhibited in their prey choice and most commonly

consume prey until their guts are full on a diet that varies

little among individuals.

No L. majuscula fragments were observed during sur-

veys of gut contents using a dissecting microscope. Pre-

vious studies have suggested that the consumption of

L. majuscula by fish and crustaceans must be elucidated

(Osborne et al. 2001; Pittman and Pittman 2005). Our study

demonstrates that even the omnivorous species F. lentigi-

nosus consumes no visible L. majuscula under simulated

bloom conditions. This eliminates one potential pathway

for the entrance of L. majuscula secondary metabolites into

the food web and is probably due to active avoidance of

the bloom fragments by fish. Surveys using compound

microscopes would be required to confirm this; however,

L. majuscula ingestion by benthivorous fishes is not likely

to be either trophically or ecologically significant.

In sand treatments, a greater proportion of nematodes

were consumed than in L. majuscula trials, especially by

S. maculata. This reflects the relative paucity of nematode

populations in L. majuscula blooms as opposed to sand.

Garcia and Johnstone (2006) showed that in response to

L. majuscula blooms, the majority of nematodes remain in

the sediment and move deeper into the sand as opposed to

moving out of the sediment and into the bloom material

itself. Bloom specialists (amphipods, ostracods, M. holo-

thuriae and other large harpacticoids) that become more

common during blooms may simply have the capacity to

withstand the adverse conditions created by the bloom (e.g.

hypoxia, increased salinity and exposure to toxins and

secondary metabolites from the bloom itself; Sellner 1997;

Watkinson et al. 2005), thus enabling populations of non-

nematodes to thrive (Samson et al. 2008). However, this

strategy may increase susceptibility to predation as

meiofauna are driven closer to the surface of the sandy

substrate (Sutherland et al. 2000; Danovaro et al. 2007) by

a reduction in the depth of the redox discontinuity layer.

Lyngbya majuscula blooms may not be as damaging to

faunal communities over the short term as was initially

suspected (Pittman and Pittman 2005). For example, larger

penaeid prawns exhibited significantly greater biomass in

response to increased prey availability, and L. majuscula

blooms increased food availability for herbivorous

252 Mar Biol (2011) 158:245–255

123

organisms, especially fish and molluscs, during blooms

(Paul et al. 1990; Pennings et al. 1996; Nagle et al. 1998;

Capper et al. 2005, 2006a, b). It has also been suggested

that the increased sediment load and detrital accumulation

that occur during blooms could lead to some positive

effects in coastal systems for detritivores and other meio-

fauna (Meyer and Bell 1989). However, if some benefits

accrue in the short term, perhaps through increased growth

rates in response to increased food availability, long-term,

sublethal effects could be significantly more damaging.

Nevertheless, L. majuscula blooms do damage local ecol-

ogies, especially through the destruction of marine habitats

(Pittman and Pittman 2005), long-term alterations in water

quality and chemistry (Watkinson et al. 2005), increased

prevalence of cancers, including fibropapillomatosis in sea

turtles (Fujiki et al. 1993; Osborne et al. 2001; Arthur et al.

2008) and the potential for biomagnification of toxins in

higher trophic levels over long periods (Capper et al. 2005,

2006a, b). The ongoing effects and likelihood of toxicity in

meiofauna and the channelling of L. majuscula toxins and

secondary metabolites through benthivorous fishes, espe-

cially in commercially important species for human con-

sumption, including the commercially Sillago spp., should

be assessed.

Blooms of L. majuscula have significant detrimental

effects on local ecosystems and dramatically change the

suitability of the soft sediment habitats in which they tend

to occur in Moreton Bay (Pittman and Pittman 2005;

Garcia and Johnstone 2006; Skilleter et al. 2006). Associ-

ated with these changes, we have determined cascade

effects to at least the second consumer level. Differing

ratios and densities of prey confront benthivorous fishes

when they inhabit L. majuscula blooms. Therefore, their

rates and range of prey consumption are different to what

would be found in a sandy, bloom-free environment. This

results in a shift in trophic relationships and predator–prey

interactions between benthivorous fishes and the inhabiting

meiofauna of blooms and sandy substrates. The effects that

these changes have on fishes are yet to be quantified;

however, increased gut fullness in both species within

bloom treatments suggests that predation is not effected by

the targeted meiofauna inhabiting a potentially toxic sub-

strate. Conversely, increased gut fullness within blooms

suggests some beneficial aspects of foraging bloom areas

due to increased access to preferred prey. Overall, further

studies should focus on the effects of chronic exposure of

L. majuscula toxins and secondary metabolites on these

fishes, especially when consuming vast quantities of toxin-

exposed meiofauna.

Acknowledgments We thank Craig Chargulaf, Angela Capper and

two anonymous reviewers for their constructive and helpful com-

ments. This project was partially funded by the Moreton Bay

Research Station Community Scholarship. The authors would like to

thank the brilliant staff at MBRS for their exemplary support

throughout the project. The described experiments were conducted

under the University of Queensland’s Animal Ethics Committee’s

approval number CMS/816/08 and Marine Parks Permits QS2005/

CVL319. The authors declare that they have no conflict of interest.

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