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Biological controls to manage Acropora-eating flatworms in coral aquaculture

January 2019
Aquaculture Environment Interactions 12

DOI:10.3354/aei00347

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Authors:

Jonathan Barton

Australian Institute of Marine Science

Craig Humphrey

Australian Institute of Marine Science

Kate S Hutson

Cawthron Institute

Coral aquaculture is expanding to supply the marine ornamental trade and active coral reef restoration. A common pest of Acropora corals is the Acropora-eating flatworm Prosthiostomum acroporae, which can cause colonial mortality at high infestation densities on Acropora spp. We investigated the potential of 2 biological control organisms in marine aquaria for the control of P. acroporae infestations. A. millepora fragments infested with adult polyclad flatworms (5 flatworms fragment-1) or single egg clusters laid on Acropora skeleton were cohabited with either sixline wrasse Pseudocheilinus hexataenia or the peppermint shrimp Lysmata vittata and compared to a control (i.e. no predator) to assess their ability to consume P. acroporae at different life stages over 24 h. P. hexataenia consumed 100% of adult flatworms from A. millepora fragments (n = 9; 5 flatworms fragment-1), while L. vittata consumed 82.0 ± 26.76% of adult flatworms (mean ± SD; n = 20). Pseudocheilinus hexataenia did not consume any Prosthiostomum acroporae egg capsules, while L. vittata consumed 63.67 ± 43.48% (n = 20) of egg capsules on the Acropora skeletons. Mean handling losses in controls were 5.83% (shrimp system) and 7.50% (fish system) of flatworms and 2.39% (fish system) and 7.50% (shrimp system) of egg capsules. Encounters between L. vittata and P. hexataenia result in predation of P. acroporae on an Acropora coral host and represent viable biological controls for reducing infestations of P. acroporae in aquaculture systems.

Proportion of Acropora-eating flatworm individuals and egg capsules removed (error bars: ± SD) in the presence and absence of biocontrols. (A) Lysmata vittata and flatworm individuals (n = 24), (B) L. vittata and flatworm eggs (n = 20 egg clusters), (C) Pseudocheilinus hexataenia and flatworms (n = 9), and (D) P. hexataenia and flatworm eggs (n = 9 egg clusters). *: statistical significance between treatments and controls. Photos: = L. vittata and P. hexataenia. (P. hexataenia photo credit: creative commons license istockphoto.com user: marrio31 id#471448553)

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AQUACULTURE ENVIRONMENT INTERACTIONS

Aquacult Environ Interact

Vol. 12: 61–66, 2020

https://doi.org/10.3354/aei00347 Published February 13

1. INTRODUCTION

Biological control utilizes living organisms (control

agents) to suppress the population density and subse-

quent impact of a specific pest organism by leveraging

ecological interactions through predation, parasitism,

herbivory, or other natural mechanisms (Eilenberg et

al. 2001). Biological controls are used extensively in

agriculture, where the tactical release of parasites or

predators is used to reduce insect pest species of eco-

nomic importance (Smith & Basinger 1947, Simmonds

et al. 1976, Greathead 1994, Eilenberg et al. 2001). In

aquaculture, high stocking densities of cultured or-

ganisms can facilitate transmission of pathogens and

parasites, requiring analogous approaches for disease

management (Deady et al. 1995, Tully et al. 1996,

Maeda et al. 1997, Powell et al. 2018). In the northern

hemisphere, cleaner fishes (e.g. ballan wrasse Labrus

bergylta Ascanius, 1767 and, more recently, lumpfish

Cyclopterus lumpus Linnaeus, 1758) are bred in cap-

tivity and subsequently cohabited with farmed salmon

(primarily Salmo salar Linnaeus, 1758) to remove ec-

toparasitic copepods (e.g. Lepeophtheirus salmonis

[Krøyer, 1837]; Tully et al. 1996). This non-chemical

Attribution Licence. Use, distribution and reproduction are un -

restricted. Authors and original publication must be credited.

Publisher: Inter-Research · www.int-res.com

*Corresponding author: jonathan.barton1@my.jcu.edu.au

NOTE

Biological controls to manage Acropora-eating

flatworms in coral aquaculture

Jonathan A. Barton1, 2, 3,*, Craig Humphrey2, 3, David G. Bourne1, 2, Kate S. Hutson1, 4

1College of Science and Engineering, James Cook University, Douglas, QLD 4814, Australia

2Australian Institute of Marine Science, Cape Cleveland, QLD 4816, Australia

3AIMS@JCU, James Cook University, DB17-148, Townsville, QLD 4811, Australia

4Cawthron Institute, 98 Halifax Street East, Nelson 7010, New Zealand

ABSTRACT: Coral aquaculture is expanding to supply the marine ornamental trade and active

coral reef restoration. A common pest of Acropora corals is the Acropora-eating flatworm Prosthio -

stomum acroporae, which can cause colonial mortality at high infestation densities on Acropora

spp. We investigated the potential of 2 biological control organisms in marine aquaria for the con-

trol of P. acroporae infestations. A. millepora fragments infested with adult polyclad flatworms (5

flatworms fragment−1) or single egg clusters laid on Acropora skeleton were cohabited with either

sixline wrasse Pseudocheilinus hexataenia or the peppermint shrimp Lysmata vittata and com-

pared to a control (i.e. no predator) to assess their ability to consume P. acroporae at different life

stages over 24 h. P. hexataenia consumed 100% of adult flatworms from A. millepora fragments

(n = 9; 5 flatworms fragment−1), while L. vittata consumed 82.0 ± 26.76% of adult flatworms (mean

± SD; n = 20). Pseudocheilinus hexataenia did not consume any Prosthiostomum acroporae egg cap-

sules, while L. vittata consumed 63.67 ± 43.48% (n = 20) of egg capsules on the Acropora skeletons.

Mean handling losses in controls were 5.83 % (shrimp system) and 7.50% (fish system) of flatworms

and 2.39% (fish system) and 7.50 % (shrimp system) of egg capsules. Encounters be tween L. vittata

and P. hexataenia result in predation of P. acroporae on an Acro pora coral host and represent viable

biological controls for reducing infestations of P. acroporae in aquaculture systems.

KEY WORDS: Prosthiostomum acroporae · Acropora-eating flatworm · Lysmata vittata ·

Pseudocheilinus hexataenia · Biological control · Coral aquaculture

PEN

CCESS

Aquacult Environ Interact 12: 61– 66, 2020

approach to pest management is preferable to costly

treatments, which stress cultured fish and reduce ap-

petite (Skiftesvik et al. 2013, Powell et al. 2018).

Within coral aquaculture and the marine ornamental

trade, the peppermint shrimps Lysmata wurdemanni

(Gibbes, 1850), L. seti caudata (Risso, 1816), L. bog -

gessi, and L. ankeri Rhyne & Lin, 2005, as well as the

nudibranch Berghia sp. are used for biological control

of anemones Aiptasia spp. (Rhyne et al. 2004, Calado

et al. 2005, Rhyne & Lin 2006). The reef fishes Thalas-

soma duperrey (Quoy & Gaimard, 1824) and Chaeto -

don auriga Forsskål, 1775 are also potential candi-

dates to mitigate infestations of the corallivorous

nudibranch Phestilla sibogae Begh, 1905 in captivity

(Gochfeld & Aeby 1997).

Control of pests of Acropora spp. coral is highly

desired, given that it is the most represented genus

imported into many countries globally (Rhyne et al.

2014), and Acropora spp. are commonly used for reef

restoration efforts (Barton et al. 2017). A problematic

coral pest, Prosthiostomum acroporae (Rawlinson,

Gillis, Billings, & Borneman, 2011), commonly known

as the Acropora-eating flatworm, has plagued hob-

byist aquaria for many years (Delbeek & Sprung

2005). P. acroporae is an obligate associate of Acrop-

ora spp. and actively consumes coral tissue, which

results in characteristic ~1 mm circular pale feeding

scars, often resulting in coral tissue necrosis. Infesta-

tions are associated with colonial mortality at high

densities in captivity (Nosratpour 2008). P. acroporae

infestations are challenging to detect because of their

highly cryptic nature, which facilitates their spread

into new systems undetected. Infestations impact

coral health through reduction of host coral fluores-

cence over time and hinder the coral’s ability to photo-

acclimate to changes in lighting conditions (Hume et

al. 2014). Infestations are often not de tected until

compromised host health is observed through visual

signs, at which point flatworm population density is

high and colonial mortality of the coral may occur.

There is no current empirical evidence to support

effective treatment or prevention measures for P.

acroporae infestations, although Barton et al. (2019)

examined the life cycle under a range of temperature

conditions and suggested timed intervention to dis-

rupt the life cycle.

The aim of the present study was to evaluate the

potential of 2 biological controls to reduce infestation

by the Acropora-eating flatworm P. acroporae on

coral. Biocontrol candidates included the peppermint

shrimp L. vittata (Stimpson, 1860), which has been

previously reported to remove parasites on fish and

in the environment (Vaughan et al. 2017, 2018a,b),

and the wrasse Pseudocheilinus hexataenia (Bleeker,

1857), based on anecdotal evidence that it may

reduce P. acroporae populations in aquaria through

active foraging (Delbeek & Sprung 2005). This study

examined the efficacy of potential biocontrols on

adults and eggs of Prosthiostomum acroporae in

captive systems over a 24 h period in vivo.

2. MATERIALS AND METHODS

2.1. Species selection, husbandry, and culture

Twenty Lysmata vittata and 10 Pseudocheilinus

hexataenia were purchased from Cairns Marine,

Cairns, Australia, and maintained for 1 mo before

any experimentation. Because of space limitations,

shrimps were housed together in one 50 l flow-

through aquarium system (10 turnovers d−1) with

approximately 5 kg of ‘live’ rock for hiding and pro-

tection between molts. P. hexataenia were housed

individually in 50 l flow-through aquarium systems

(10 turnovers d−1) with a 60 mm PVC tee (3-way junc-

tion) each for shelter. Filtered seawater (0.04 µm

nominal pore size) at 27°C was used to supply the

system. Shrimps and fish were fed twice daily to sati-

ation with a mixture of thawed Tasmanian mysid

shrimp, Ocean Nutrition®Marine Fish Eggs, Ocean

Nutrition®Cyclopods, and Vitalis®Platinum formu-

lated feed. Animals were fed the morning prior to the

commencement of each experimental trial but not

during their trial period.

Adult Prosthiostomum acroporae were collected

from a culture of infested captive Acropora spp. colo -

nies. Flatworms were maintained in culture using

established methods (see Barton et al. 2019).

2.2. Coral fragment preparation, infestation, and

egg collection

To provide A. millepora for biological control trials,

96 A. millepora fragments (approximately 50 mm

height; 30 mm width) were generated from donor

colo nies harvested from 2 colonies sourced from

Davies Reef, Australia (harvested September 2017;

GBRMPA Permit: G12/35236.1), and 5 captive colo -

nies originating from Orpheus Island, Australia (har-

vested May 2016; G14/36802.1). A combination of

bone cutters and a band saw (Gyrphon®Aquasaw

XL) was used to prune A. millepora fragments, which

were then fixed onto aragonite coral plugs (32 mm

diameter) with cyanoacrylate glue.

Barton et al.: Biological control of Prosthiostomum acroporae

To infest A. millepora fragments with P. acroporae,

fragments were housed temporarily in individual 5 l

containers. Before the start of each experimental

trial, 5 P. acroporae individuals, approximately 3 mm

in size, were directly pipetted onto each A. millepora

fragment. After 60 s, each fragment was gently

shaken to ensure P. acroporae had laterally ap -

pressed themselves to the host coral’s tissue and

were not stuck in the coral mucus (flatworms can dis-

lodge if stuck in mucus). Any worms that detached

were attempted to be reattached once and then dis-

carded for another specimen if unsuccessful.

Egg capsules were naturally laid on Acropora

skeleton in the P. acroporae culture and then har-

vested using bone cutters to remove the section of

skeleton with these eggs. The underside of each sub-

sequent skeletal fragment was glued onto clean

aragonite disks or ‘frag plugs’ with cyanoacrylate

glue. The number of eggs per cluster was determined

by counting them under a dissecting microscope

(Leica EZ4, 10−40× magnification) while immersed in

seawater to prevent desiccation. Only fragments of

coral skeleton bearing unhatched and undamaged

egg capsules were selected for experimentation.

2.3. L. vittata experiments

Experiments with L. vittata were conducted on 4

separate trial days (i.e. 6 control and 6 treatment

replicates per trial; n = 24 control; 24 treatment). On

the day before each L. vittata trial, a random number

generator was used to designate treatments and con-

trols to aquaria. PVC blocks (80 × 80 × 25 mm; 32 mm

diameter depression with central 10 × 15 mm hole to

hold 32 mm diameter aragonite plugs in all repli-

cates) were placed in each aquarium (3.5 l) before

each trial. After their morning feeding, 6 L. vittata

were haphazardly caught from their holding system

using a 500 ml wide−mouth container and placed

into their respective experimental tanks. L. vittata

were given a minimum of 2 h to acclimate to their

surroundings in the replicate experimental flow-

through aquaria (5 l h−1) maintained at 27 ± 0.1°C. L.

vittata were considered acclimated once they settled

on the bottom of each aquarium.

A. millepora fragments (1 per aquarium) infested

with 5 P. acroporae each were introduced to each of

the 3.5 l aquaria (treatment and control) for 24 h to

determine if the presence of L. vittata (treatment)

influenced the number of remaining flatworms on

each coral fragment. The number of flatworms

remaining was determined using a seawater screen-

ing method (Barton et al. 2019). In addition, the PVC

blocks and clear tanks were inspected for flatworms

with the naked eye after each trial, with any flat-

worms found added to the remaining total of flat-

worms. Experiments examining the influence of L.

vittata on P. acroporae egg capsules were conducted

using the same approach, with the exception of egg

capsules being counted before and after the trial

under a stereo microscope (Leica EZ4, 10−40× mag-

nification). Skeletal fragments (n = 48) were divided

equally across treatments and controls (i.e. n = 24

control, 24 treatment) in L. vittata trials with 47.27 ±

19.09 (mean ± SD) egg capsules per fragment. L. vit-

tata do not forage immediately before or after molt-

ing (D. Vaughan pers. comm.), therefore any shrimps

that molted during the 24 h trial were excluded (i.e.

4 replicates were removed due to molting; n = 20).

2.4. P. hexataenia experiments

P. hexataenia (n = 9) were acclimated for approxi-

mately 2 wk to their randomly allocated flow-through

aquaria at 27 ± 0.1°C with PVC blocks in place. The

50 l aquaria (n = 9 with wrasse, 9 without) were sep-

arated by black plastic because of the acute eyesight

and territorial behavior of P. hexataenia. After accli-

mation, each fish regularly accepted food and did not

exhibit signs of physical or behavioral stress.

Following morning feeding of P. hexataenia, in -

fested A. millepora fragments (5 flatworms each) were

introduced to each 50 l aquarium and left for a dura-

tion of 24 h to assess if the presence of the wrasse in-

fluenced the number of flatworms remaining on each

coral fragment. Flatworms were recovered using an

established screening method (Barton et al. 2019).

The surfaces of the aquaria and the PVC blocks hold-

ing the fragment plugs were inspected visually for

any remaining worms, which were added to the total

remaining flatworms if present. Experiments examin-

ing the influence of P. hexataenia on P. acroporae egg

capsules were conducted similarly, but egg capsules

were counted before and after in spection with a

stereo microscope (Leica EZ4, 10−40× magnification).

The 18 skeletal fragments used in P. hexataenia trials

(n = 9 treatment, 9 controls) had 42.33 ± 16.95 (mean ±

SD) egg capsules per skeletal fragment.

2.5. Statistical analysis

Binomial generalized linear mixed models (GLMMs)

and generalized linear models (GLMs) were gener-

Aquacult Environ Interact 12: 61– 66, 2020

ated in RStudio (Version 1.0.143; R packages ‘car,’

Fox & Weisberg 2019, and ‘lme4,’ Bates et al. 2015) to

assess the effect of L. vittata treatments on P. acropo-

rae egg capsules and individual flatworms. Treat-

ment was considered a random effect and trial iden-

tity a fixed effect in the model to ensure that there

were no effects that changed the results significantly

(p < 0.05) between L. vittata trials. Lacking any sig-

nificant effects from trial identity in both experiments

testing L. vittata egg and individual consumption, the

GLM with pooled data denoted any significant

effects (p < 0.05) of treatment on consumption for

each experiment. Four replicates were removed from

statistical analysis of the L. vittata vs. egg capsule

experiment because these replicates molted during

the experimental trial. Kruskal-Wallis tests were

used to assess the results of P. hexataenia experi-

ments with a significance threshold of α= 0.05.

3. RESULTS AND DISCUSSION

The peppermint shrimp Lysmata vittata consumed

both settled flatworm individuals and egg capsules

laid on coral skeleton. The presence of L. vittata

significantly reduced (GLM; p < 0.001) Prosthiosto-

mum acroporae infestations over 24 h, with 82.0 ±

26.76% of the flatworms consumed (mean ± SD; n =

20; Fig. 1). Control tanks (n = 24)

showed a loss of 5.83 ± 10.77% (n =

24; Fig. 1). This indicates that approx-

imately 94% of flatworms were re-

covered using the screening method,

which is consistent with previous use

(Barton et al. 2019). L. vittata also sig-

nificantly reduced P. acroporae egg

capsules (GLM; p < 0.05), with 63.7 ±

43.48% (n = 20) of the egg capsules

removed compared to only 1.0 ±

2.99% (n = 24) in the control (Fig. 1).

Lysmata shrimps use their setae-

covered antennules to detect chemi-

cal cues (via cuti cular sensilla) from

their environment and locate suitable

prey items (Zhu et al. 2011, Caves et

al. 2016). Because they do not use vi-

sual mechanisms to locate and cap-

ture prey, L. vittata predation on P.

acroporae is not hindered by the

camouflage of these flatworms. How-

ever, L. vittata must physically en -

counter P. acroporae eggs or individ-

uals while foraging to consume them,

thus potentially limiting their ability to control P. ac r o -

porae populations in larger aquaria (aquaria >3.5 l

were not tested in this study), where the probability of

a direct encounter would be limited by proximity and

the availability of alternate food sources (L. vittata

were not fed during the trials). Despite this possible

limitation, L. vittata remain useful as a potential treat-

ment of P. acroporae infestations because intimate co-

habitation with Acropora enables shrimp to scavenge

among coral branches and consume P. acroporae indi-

viduals and egg capsules. L. vittata are also an aggre-

gating species and can be kept in high numbers when

provided with sufficient food and shelter (Vaughan et

al. 2018b). Future research could examine diet prefer-

ences of L. vittata, which may contribute to their effi-

cacy in removing flatworms from Acropora colonies

(e.g. Grutter & Bshary 2004).

Experimental trials with Pseudocheilinus hexa -

taenia demonstrated that these fish are effective at

reducing the P. acroporae population, with their pres-

ence having a significant effect on flatworm abun -

dance remaining on A. millepora fragments (Kruskal-

Wallis; p < 0.001). All P. acroporae exposed to P.

hexataenia were removed over 24 h (100%; n = 9),

compared to a loss of 7.5 ± 13.92% of flatworms (mean

± SD; n = 9) in controls. In contrast, all egg capsules

were recovered intact in the experimental treatments

(100%; n = 9) when cohabited with P. hexataenia. In

Fig. 1. Proportion of Acropora-eating flatworm individuals and egg capsules

removed (error bars: ± SD) in the presence and absence of biocontrols. (A)

Lysmata vittata and flatworm individuals (n = 24), (B) L. vittata and flatworm

eggs (n = 20 egg clusters), (C) Pseudocheilinus hexataenia and flatworms (n =

9), and (D) P. hexataenia and flatworm eggs (n = 9 egg clusters). *: statistical

significance between treatments and controls. Photos: = L. vittata and P. hexa-

taenia. (P. hexataenia photo credit: creative commons license istockphoto.com

user: marrio31 id#471448553)

Barton et al.: Biological control of Prosthiostomum acroporae

the control, 2.39 ± 3.84% egg capsules (mean ± SD;

n = 9) were not recovered, resulting in significant dif-

ferences between treatment and control (Kruskal-

Wallis; p < 0.05), likely from incidental mechanical

damage to egg capsules through handling.

These results indicate that P. hexataenia is highly

efficient at eating flatworms using well-developed

eyesight (Gerlach et al. 2016) but does not interact

with the hard shell of flatworm egg capsules. The

implementation of P. hexataenia as biological con-

trols must consider their ecology and husbandry

requirements. In the wild, these fish actively forage

in their established territory (Geange & Stier 2009,

Geange 2010), generally only coming together for

mating purposes (Kuwamura 1981). While their for-

aging behavior appears similar in captivity, the soli-

tary and territorial nature of P. hexataenia renders

keeping more than 1 individual in smaller aquaria

(e.g. <1000 l) problematic. More than 1 individual

could be kept in aquaculture systems large enough

to avoid territorial confrontation, but the ‘patrol’

range of this territory may remain relatively constant.

It is for this reason, combined with the fact that this

fish does not interact with flatworm egg capsules,

that they may not be as suitable for treating acute

infestations of P. acroporae compared to L. vittata.

However, their performance in our trials suggests

that this colorful labrid is a useful tool for consuming

adult flatworms, thus mitigating the chronic impacts

of a given P. acroporae infestation by removing or

reducing the P. acroporae density to non-lethal levels

for the Acropora host.

P. hexataenia and L. vittata identify prey items in

different ways while foraging, which has implica-

tions for how they are used in the captive environ-

ment and their ecological roles in native ecosystems.

Little is understood about the dynamics of wild P.

acroporae populations, although our results may pro-

vide further understanding of the trophic relation-

ships between P. acroporae and natural predators in

reef ecosystems. P. acroporae are cryptic and there

are no documented infestations causing colonial mor-

tality of Acropora colonies in the wild. It does remain

likely that some proportion of wild mortality of Acro-

pora colonies attributed to other causes (e.g. sedi-

mentation and algal competition) is instead experi-

encing negative secondary effects on coral health

from P. acroporae infestation. However, the presence

of natural predators of P. acroporae (e.g. P. hexatae-

nia and L. vittata) may reduce incidences of mortality

in wild Acropora colonies.

In captive systems, pairing both of these biologi-

cal control organisms with the manual removal of

P. acroporae egg clusters is likely to be highly effec-

tive in reducing the overall infestation within a given

aquarium system. However, consideration must be

given to the sustainable supply of the organisms if

used as biological controls. L. vittata are available

through the ornamental trade and can be bred in

captivity. Although peppermint shrimp species from

other regions (e.g. L. wurdmenii, L. boggessi, Rhyne

& Lin 2006) were not investigated in the present

study, they could also be examined for their ability to

interact analogously with P. acroporae and could be

supplied sustainably for biocontrol of flatworm infes-

tations. Although P. hexataenia is categorized as

Least Concern (Bertoncini 2010; IUCN Red List

2010), overharvesting for use as biological controls in

the ornamental trade could impact local populations.

Lessons should be taken from the Scandinavian

salmonid industry, where harvesting of wrasse

broodstock used for biological control of sea lice par-

asites has exerted considerable pressures upon wild

populations (Brooker et al. 2018, Powell et al. 2018).

In summary, this study provides the first empirical

evidence of potential biological control organisms for

P. acroporae in captivity. The ability of both L. vittata

and P. hexataenia to consume P. acroporae renders

them useful preventative measures of infestation in

addition to potentially being used to treat colonies

infested with adult flatworms and thereby drastically

reducing the impact of this pest on captive colonies.

While P. hexataenia had no apparent interest in P.

acroporae egg capsules, L. vittata displayed the

added benefit of consuming egg capsules through

their foraging activities, with encounters with the

egg clusters likely to further control the flatworm

populations in captive systems. The addition of sus-

tainable biological control organisms adds a valuable

tool for flatworm control, which is suitable for both

aquarium hobbyists and large-scale coral aquacul-

ture facilities.

Acknowledgements. We thank Brett Bolte and Rachel Neil

for help in maintaining the P. acroporae culture. We also

thank Kate Rawlinson for constructive comments on the

manuscript. This project was funded through an AIMS@JCU

pilot grant. Experiments were conducted in the National Sea

Simulator, at the Australian Institute of Marine Science,

under James Cook University Animal Ethics approval

(A2466).

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66
Editorial responsibility: Tim Dempster,
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Submitted: September 26, 2019; Accepted: December 9, 2019
Proofs received from author(s): Februar y 3, 2020

Unresolved taxonomy confounds invasive species identification: the Lysmata vittata Stimpson, 1860 (Decapoda: Caridea: Lysmatidae) species complex and recent introduction of Lysmata vittata sensu stricto in the western Atlantic

Article

Full-text available

Jan 2022

Peppermint shrimp resembling Lysmata vittata Stimpson, 1860, a species native to the Indo-West Pacific, were found in the lower Chesapeake Bay and adjacent coastal embayments in 2013, representing the first recorded introduction of this species in the northwestern Atlantic. Conflicting morphological descriptions, inconsistent morphological terminology, and limited molecular data (i.e., unresolved taxonomy), as well as the destruction of the type material of L. vittata, created uncertainty regarding proper identification. We provide the first phylogeny incorporating individuals from across the presumed native and introduced range of L. vittata. Morphological and phylogenetic analyses clearly indicate L. vittata represents a species complex of two widely divergent groups: 1) "Bruce Type" with a uniramous dorsal antennule that agrees with A.J. Bruce's 1990 redescription of L. vittata, and 2) "Rauli Type" with a one-article accessory branch on the dorsal antennule that agrees most closely with the junior synonym L. rauli Laubenheimer & Rhyne, 2010. Given the taxonomic ambiguity surrounding L. vittata, we designate the individual used by A.J. Bruce to redescribe L. vittata and incorporated in our analyses as a neotype to fix the identity of this species. We therefore identify introduced North American and New Zealand populations as L. vittata sensu stricto and postulate that the native range spans temperate/subtropical East Asia. These data suggest that L. rauli is a valid species, which includes a possible undescribed sister species. We confirm the presence of L. californica Stimpson, 1866 in New Zealand, the first non-native record for this species. We also provide data suggesting L. dispar Hayashi, 2007 may be more widespread in the Indo-West Pacific than currently known and consider L. lipkei Okuno & Fiedler, 2010 to be a likely junior synonym.

Fantastic Flatworms and Where to Find Them: Insights into Intertidal Polyclad Flatworm Distribution in Southeastern Australian Boulder Beaches

Article

Full-text available

Mar 2023
Diversity

There is a rapid and extensive decline of our marine biodiversity due to human impacts. However, our ability to understand the extent of these effects is hindered by our lack of knowledge of the occurrence and ecology of some species groups. One such group of understudied organisms are marine flatworms of the order Polycladida, a conspicuous component of southeastern Australia’s marine ecosystems that has received little attention over the years. Intertidal boulder beaches support a diverse range of polyclad flatworms in other countries, but the role of these environments in maintaining biodiversity is not well understood. In this study, we identified hotspots of flatworm occurrence by assessing the diversity and overall abundance of flatworms at boulder beaches along the southeast Australian coast. Bottle and Glass, Sydney Harbour, was found to be the most diverse site for flatworms. We also identified a higher occurrence of flatworms under large boulders and less exposed beaches and noted an increased presence of flatworms at higher latitudes. Probable influences on these patterns such as the requirement for shelter and protection are discussed. This study contributes to our knowledge of Australia’s coastal biodiversity and can be used to assist in the management and conservation of our marine environments.

Mitigation of substrate biofouling to increase post-settlement coral survival

Thesis

Full-text available

Dec 2021

Denise Hassinger

Biofouling is a major concern in coral aquaculture and hinders the upscaling of coral reef restoration efforts as it leads to increased juvenile coral mortality through smothering. This study proposed using platinum-cured liquid silicone rubber (PC-LSR), also known as “food-grade” or “food-safe” silicone, as an antifouling substrate for coral larvae to settle onto and for corals to grow on. To determine if algae grow on the silicone, silicone squares and ceramic tiles were kept in four different tanks (with different algal communities) for one month. Scanning electron microscope (SEM) analysis was used to determine if algae can attach to silicone. The suitability of silicone squares (PC-LSR) as settlement substrate was tested using larvae from five stony coral species (Montastraea. cavernosa, Pseudodiploria. strigosa, Pseudodiploria. clivosa, Colpophyllia natans, and Orbicella faveolata); ceramic tiles were tested as a control. To assess if corals can grow on the silicone, a silicone ‘skirt’ was placed around two corals. In all tanks except one, algal growth was observed on silicone squares; algal growth was observed on all ceramic tiles. There was no algal attachment to silicone squares in tanks R, H, and 3, and minimal attachment in tank 4. Larval settlement of M. cavernosa, P. strigosa, and O. faveolata was not significantly different between substrates, but P. clivosa and C. natans larvae settled significantly more on ceramic tiles. New tissue growth was observed after a 3-month period on both silicone ‘skirts.’ One M. cavernosa colony grew eight new polyps with a total tissue growth area of 0.792 cm2, but experienced a disturbance, losing three polyps (0.353 cm2). A second M. cavernosa colony grew at a slower rate, producing two new polyps with a total tissue growth of 0.245 cm2. This study suggests PC-LSR can prevent or minimize algal attachment, resulting in lower algal growth in tanks, especially turf algae. While PC-LSR can be used as a larval settlement substrate for some coral species, the survival and growth of newly settled corals on this substrate seems vulnerable due to adhesion issues. Consequently, PC-LSR appears to be an effective way to prevent algal overgrowth around corals, especially when deployed as a skirt around corals that are already attached to a substrate, and thus should be the subject of further study.

Delimiting species within the Lysmata vittata (Stimpson, 1860) (Decapoda: Lysmatidae) species complex in a world full of invaders

Article

Jun 2022

Historically, Lysmata vittata has been reported with a near global non-polar distribution. Early studies reported a wide morphological variation in this species, which served as a basis for further synonymization of at least four species. Herein, we investigated the species diversity within L. vittata complex and tested whether L. rauli and L. durbanensis are valid species instead of junior synonyms of L. vittata. Our integrated morphological and molecular data strongly supports the validity of at least six taxonomic entities within the broader L. vittata complex, including L. rauli and L. durbanensis and three undescribed species. Multivariate analyses highlighted prominent morphological differences in accessory branch structure of dorsolateral antennular flagellum, number of carpal and meral segments of the second pereopod, and color pattern which segregated shrimps into distinct morpho-groups. Phylogenetic analyses supported morphological groupings and recovered five widely divergent lineages, which corresponded to the morphological groupings: L. vittata sensu stricto; L. rauli sensu stricto; L. sp. CHINA; L. sp. AUS1; and L. sp. AUS2. Therefore, we formally resurrect L. rauli to valid species status and posit it is native to the subtropical and tropical Indo West-Pacific. Although data were limited, we also formally resurrect L. durbanensis to valid species status from southern Africa. Our results imply L. vittata and L. rauli are exotic species in the western Atlantic, New Zealand, and the Mediterranean. This study provides a solid framework to continue untangling the historic L. vittata species complex, which is likely to include additional species to the ones included in the present study.

Natural Products in Polyclad Flatworms

Article

Full-text available

Jan 2021
MAR DRUGS

Marine invertebrates are promising sources of novel bioactive secondary metabolites, and organisms like sponges, ascidians and nudibranchs are characterised by possessing potent defensive chemicals. Animals that possess chemical defences often advertise this fact with aposematic colouration that potential predators learn to avoid. One seemingly defenceless group that can present bright colouration patterns are flatworms of the order Polycladida. Although members of this group have typically been overlooked due to their solitary and benthic nature, recent studies have isolated the neurotoxin tetrodotoxin from these mesopredators. This review considers the potential of polyclads as potential sources of natural products and reviews what is known of the activity of the molecules found in these animals. Considering the ecology and diversity of polyclads, only a small number of species from both suborders of Polycladida, Acotylea and Cotylea have been investigated for natural products. As such, confirming assumptions as to which species are in any sense toxic or if the compounds they use are biosynthesised, accumulated from food or the product of symbiotic bacteria is difficult. However, further research into the group is suggested as these animals often display aposematic colouration and are known to prey on invertebrates rich in bioactive secondary metabolites.

Refining southwestern Atlantic peppermint shrimp biodiversity: description of a new species of Lysmata (Decapoda: Lysmatidae) using an integrative systematic approach

Article

Jun 2023
J MAR BIOL ASSOC UK

Currently, 14 of the 50 species of Lysmata are known to possess a long accessory branch with more than two articles. Historically, Lysmata intermedia and Lysmata moorei were the only two 'long-branch' species inhabiting the southwestern Atlantic. Here we describe, based on morphological, molecular and colour pattern data, a new species of Lysmata possessing a long accessory branch from Pernambuco, northeastern Brazil. Our maximum-likelihood analysis recovered Lysmata elisa sp. n. as a sister species to Lysmata jundalini. Both species are closely related to Lysmata holthuisi and L. intermedia. The four aforementioned species comprise the L. intermedia species complex. The new species may be morphologically distinguished from the other closely related species by different sets of characters, which include details of the dorsolateral antennular flagellum, armature of ischium of the second pair of per-eiopods, intraorbital process shape and relative proportions of pereiopods. Our results reinforce the importance of refining biodiversity data through the application of integrative taxonomic approaches to expand the knowledge of local and global biodiversity. The biodiversity of Lysmata deserves special attention, as they are intensively exploited in the aquarium trade.

Limited cross-species virus transmission in a spatially restricted coral reef fish community

Article

Full-text available

Feb 2023

The Great Barrier Reef (GBR)—the largest coral reef ecosystem in the world—supports over 1,200 fish species with some of the highest population densities and diversities observed in vertebrates, offering a high potential for virus transmission among species. As such, the GBR represents an exceptional natural ecosystem to determine the impact of host community diversity on virus evolution and emergence. In recent decades, the GBR has also experienced significant threats of extinction, making it one of the most vulnerable ecosystems on the planet. Despite the global importance of the GBR, our understanding of virus diversity and connectivity in tropical reef fishes remains poor. Here, we employed metatranscriptomic sequencing to reveal the viromes of sixty-one reef fish species. This identified transcripts representing 132 putative viral sequences, 38 of which exhibited strong phylogenetic relationships with known vertebrate-associated viral genera, including a novel Santee-Cooper ranavirus (Iridoviridae). We found little evidence for virus transmission between fish species living within a very restricted geographical space—a 100-m2 coral reef ecosystem—suggesting that there might be important host barriers to successful cross-species transmission despite regular exposure. We also identified differences in virome composition among reef fish families, such that cryptobenthic reef fishes—characterized by small body sizes and short life spans—exhibited greater virome richness compared to large reef fishes. This study suggests that there are important barriers to cross-species virus transmission and that successful emergence in a reef fish community likely requires active host adaptation, even among closely related host species.

New perspectives on the role of cleaning symbiosis in the possible transmission of fish diseases

Article

Full-text available

Jun 2021
REV FISH BIOL FISHER

For the last seven decades, cleaning sym-biosis in the marine environment has been a research field of intrigue. There is substantial evidence that, by removing undesired items from their client fishes, cleaner organisms have positive ecosystem effects. These include increased fish recruitment, abundance and enhanced fish growth. However, the intimate association and high frequency of interactions between cleaners and clients potentially facilitates pathogen transmission and disease spread. In this review, we identify knowledge gaps and develop novel hypotheses on the interrelationship between parasites, hosts and the environment (disease triangle concept), with a particular emphasis on the potential role of cleaner organisms as hosts and/or transmitters of parasites. Despite evidence supporting the positive effects of cleaner organisms, we propose the cleaners as transmitters hypothesis; that some parasites may benefit from facilitated transmission to cleaners during cleaning interactions, or may use cleaner organisms as transmitters to infect a wider diversity and number of hosts. This cost of cleaning interactions has not been previously accounted for in cleaning theory. We also propose the parasite hotspot hypothesis; that parasite infection pressure may be higher around cleaning stations, thus presenting a conundrum for the infected client with respect to cleaning frequency and duration. The impact of a changing environment, particularly climate stressors on cleaners' performance and clients' cleaning demand are only beginning to be explored. It can be expected that cleaners, hosts/cli-ents, and parasites will be impacted in different ways by anthropogenic changes which may disrupt the long-term stability of cleaning symbiosis.

Is predation of juvenile crown-of-thorns seastars (Acanthaster cf. solaris) by peppermint shrimp (Lysmata vittata) dependent on age, size, or diet?

Article

Full-text available

Apr 2021
CORAL REEFS

Outbreaks of crown-of-thorns seastars (CoTS) are one of the leading causes of coral decline on Indo-Pacific coral reefs. Predator removal has been proposed to be a possible mechanism contributing to CoTS outbreaks in this region. Although some data exist on predation of adults, little work has been conducted on predators of juvenile CoTS. The aim of this study was therefore to establish whether predation of juvenile CoTS (1–9 months old after settlement) by peppermint shrimp (L. vittata) is affected by the age, size, or diet of juvenile CoTS. Through a set of ten predation experiments and statistical modeling, this study demonstrated that both age and size of juvenile CoTS are important factors affecting partial and lethal predation. Age was, however, found to be a better predictor of changes in probability (P) of lethal and partial predation (based on smaller AICc). Up to the age of ~ 4 months post-settlement, the probability of lethal predation over a span of 3 d of the experiment was nearly 1. Juvenile CoTS > 4 months old were rarely consumed entirely (P lethal predation = 0) yet showed increased partial predation (such as arm removal or damage to the center of the body) with probabilities increasing after 6 months post-settlement. A subset of CoTS over the age of 4 months was offered either coral or crustose coralline algae (CCA) as food to test for the effect of diet on predation. Diet did not significantly impact either partial or lethal predation. Thus, peppermint shrimp were identified as predators of juvenile CoTS up to an age of 4 months post-settlement, yet partial predation past this age still occurs, which may have consequences on population dynamics. The present study and future research on other juvenile predators fill important gaps in understanding CoTS population outbreaks.

OCTOCORALLIA, HEXACORALLIA, SCLERACTINIA, AND OTHER CORALS

Chapter

Mar 2022

This chapter focuses on the corals of the class Anthozoa. The Anthozoa are routinely divided into various subclasses, though the number of subclasses and spelling are highly variable. The elegant three-volume Corals of the World provides some valuable keys for the reef-forming corals and remains a good taxonomy over all. It divides the Anthozoa into three subclasses: Octocorallia, Hexacorallia, and Ceriantipatharia. The octocorals are traditionally divided into five or six orders (Telestacea, Alcyonacea, Gorgonacea, Pennatulacea, Helioporacea, and sometimes Stolonifera). In captive management of corals, health care focuses nearly entirely on environmental management. All corals need sufficient water motion for oxygenation of tissues and for flushing away of debris. Nutritional diseases of corals are probably more common than is currently documented, though the complex relationship between micronutrition and water quality complicates their assessment. The chapter presents several infectious diseases such as bacterial diseases, fungal diseases, protozoal diseases, dinoflagellate diseases, and metazoan diseases.

The Life Cycle of the Acropora Coral-Eating Flatworm (AEFW), Prosthiostomum acroporae; The Influence of Temperature and Management Guidelines

Article

Full-text available

Sep 2019

As coral aquaculture is increasing around the world for reef restoration and trade, mitigating the impact of coral predators, pathogens and parasites is necessary for optimal growth. The Acropora coral-eating flatworm (AEFW), Prosthiostomum acroporae (Platyhelminthes: Polycladida: Prosthiostomidae) feeds on wild and cultivated Acropora species and its inadvertent introduction into reef tanks can lead to the rapid death of coral colonies. To guide the treatment of infested corals we investigated the flatworm’s life cycle parameters at a range of temperatures that represent those found in reef tanks, coral aquaculture facilities and seasonal fluctuations in the wild. We utilized P. acroporae from a long-term in vivo culture on Acropora species to examine the effects of temperature (3°C increments from 21 to 30°C) on flatworm embryonation period, hatching success, hatchling longevity, and time to sexual maturity. Our findings show that warmer seawater shortened generation times; at 27°C it took, on average, 11 days for eggs to hatch, and 35 days for flatworms to reach sexual maturity, giving a minimum generation time of 38 days, whereas at 24°C the generation time was 64 days. Warmer seawater (24–30°C) also increased egg hatching success compared to cooler conditions (21°C). These results indicate that warmer temperatures lead to higher population densities of P. acroporae. Temperature significantly increased the growth rate of P. acroporae, with individuals reaching a larger size at sexual maturity in warmer temperatures, but it did not influence hatchling longevity. Hatchlings, which can swim as well as crawl, can survive between 0.25 and 9 days in the absence of Acropora, and could therefore disperse between coral colonies and inter-connected aquaria. We used our data to predict embryonation duration and time to sexual maturity at 21–30°C, and discuss how to optimize current treatments to disrupt the flatworm’s life cycle in captivity.

Cleaner shrimp are a sustainable option to treat parasitic disease in farmed fish

Article

Full-text available

Sep 2018

Chemical use is widespread in aquaculture to treat parasitic diseases in farmed fish. Cleaner fish biocontrols are increasingly used in fish farming as an alternative to medicines. However, cleaner fish are susceptible to some of their clients' parasites and their supply is largely dependent on wild harvest. In comparison, cleaner shrimp are not susceptible to fish ectoparasites and they can be reliably bred in captivity. The effectiveness of shrimp in reducing parasites on farmed fish remained unexplored until now. We tested four cleaner shrimp species for their ability to reduce three harmful parasites (a monogenean fluke, a ciliate protozoan, and a leech) on a farmed grouper. All shrimp reduced parasites on fish and most reduced the free-living early-life environmental stages-a function not provided by cleaner fish. Cleaner shrimp are sustainable biocontrol candidates against parasites of farmed fish, with the peppermint cleaner shrimp reducing parasites by up to 98%.

Cleaner shrimp remove parasite eggs on fish cages

Article

Full-text available

Sep 2018

Benthic stages of cultured fishes’ ectoparasites are a major contributor to persistent reinfections in aquaculture. These stages are resistant to chemical therapies and are costly to manage in terms of time and labour. Cleaner shrimp, unlike cleaner fishes, prey on benthic stages, suggesting they have the potential to reduce parasite reinfection pressure without having to be in direct contact with the client fish. Cleaner shrimp have never been used as biocontrols in commercial aquaculture, but offer an advantage over cleaner fishes in that they are not susceptible to the ectoparasites of their clients. We present the first investigation of a cultured cleaner shrimp, Lysmata vittata, as a biocontrol agent against the eggs of the economically important cosmopolitan ectoparasite Neobenedenia girellae infecting cultured juvenile grouper, Epinephelus lanceolatus, under simulated recirculating aquaculture conditions. L. vittata removed the eggs of N. girellae entangled on the mesh of the culture cages and significantly reduced N. girellae recruitment to fish by ~87%. Our results demonstrate the value of cleaner shrimp in addressing ectoparasite problems and highlight the importance of investigating novel biocontrol strategies in aquaculture.

Use of lumpfish for sea-lice control in salmon farming: Challenges and opportunities

Article

Full-text available

Mar 2017

OPEN ACCESS: http://onlinelibrary.wiley.com/doi/10.1111/raq.12194/full Efficient sea-lice control remains one of the most important challenges for the salmon farming industry. The use of wrasse (Labridae) as cleaner fish offers an alternative to medicines for sea-lice control, but wrasse tend to become inactive in winter. Lumpfish (Cyclopterus lumpus) continue to feed on sea-lice at low temperatures, and commercial production has escalated from thousands of fish in 2010 to well over 30 million juveniles deployed in 2016. However, production still relies on the capture of wild broodstock, which may not be sustainable. To meet global industry needs, lumpfish production needs to increase to reach c. 50 million fish annually and this can only come from aquaculture. We review current production methods and the use of lumpfish in sea cages and identify some of the main challenges and bottlenecks facing lumpfish intensification. Our gap analysis indicates that the areas in most need of research include better control of maturation for year-round production; formulation of appropriate diets; artificial selection of elite lines with desirable traits; and development of vaccines for certified, disease-free juvenile production. The welfare of farmed lumpfish also needs to be better quantified, and more information is needed on optimal densities and tank design. Finally, the risk of farmed lumpfish escaping from net pens needs to be critically assessed, and we argue that it might be beneficial to recover cleaner fish from salmon cages after the production cycle, perhaps using them as broodstock, for export to the Asian food markets or for the production of animal feeds.

Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses

Article

Full-text available

Dec 2016
FISH FISH

Cleaning symbiosis has been documented extensively in the marine environment over the past 50 years. We estimate global cleaner diversity comprises 208 fish species from 106 genera representing 36 families and 51 shrimp species from 11 genera representing 6 families. Cleaning symbiosis as originally defined, is amended to highlight communication between client and cleaner as the catalyst for cooperation, and to separate cleaning symbiosis from incidental cleaning, which is a separate mutualism preceded by no communication. Moreover, we propose the term “dedicated” to replace “obligate” to describe a committed cleaning lifestyle. Marine cleaner fishes have dominated the cleaning symbiosis literature, with comparatively little focus given to shrimp. The engagement of shrimp in cleaning activities has been considered contentious because there is little empirical evidence. Plasticity exists in the use of “cleaner shrimp” in the current literature, with the potential to cause significant confusion. Indeed, this term has been used incorrectly for the shrimp Infraorder Stenopodidea, involving three families, Stenopodidae, Palaemonidae, and Hippolytidae, and to represent all members of Lysmata and Stenopus. Caution is expressed in the use of grey literature and anecdotal observations to generate data on cleaning interactions, due to the presence of species complexes. Interest in cleaning organisms as biological controls in aquaculture is increasing due to their value as an alternative to various chemical ectoparasite controls. Reports of the importance of cleaner organisms in maintaining a healthy reef ecosystem has also been increasing and we review the current biological knowledge on cleaner-organisms, highlighting areas that are understudied.

Fluorescence characterisation and visual ecology of pseudocheilinid wrasses

Article

Full-text available

Mar 2016
Front Zool

Background: Wrasses represent the second largest family of marine fishes and display a high diversity of complex colours linked to ecological functions. Recently, red autofluorescent body colouration has been reported in some of these fishes. However, little is known about the distribution of such fluorescent body patterns in wrasses or the animals' ability to perceive such colours. Results: Against this background, we (1) investigated long-wavelength emission autofluorescence in thirteen species of pseudocheilinid wrasses and (2) characterised the spectral absorbance of visual pigments in one of the examined species, the fairy wrasse Cirrhilabrus solorensis. Spectrophotometric analysis revealed that fluorescent body colouration is widespread and diverse within this clade, with considerable variation in both fluorescent pattern and maximum emission wavelength between species. Characterisation of visual pigments in retinal photoreceptors showed a single class of rod and three spectrally distinct cone photoreceptors, suggesting possible trichromacy. Conclusion: Combining the emission characteristics of fluorescence body colouration and the spectral sensitivity data of retinal cells suggests that the visual system of C. solorensis is sensitive to pseudocheilinid fluorescence.

Coral propagation: a review of techniques for ornamental trade and reef restoration

Article

Full-text available

Dec 2015

Aquaculture of coral offers an alternative to wild harvest for the ornamental trade and shows considerable promise for restoring reefs and preserving biodiversity. Here, we compare advantages and disadvantages of asexually derived fragments versus sexually derived propagules and in situ versus ex situ nursery phases for the ornamental trade and reef restoration. Asexual propagules, sourced from a donor coral colony that is cut into smaller parts and attached to artificial substrate, are most commonly used. The most suitable corals are typically branching species, although fragments from species with other growth forms can be successful, albeit slower growing. Sexually derived propagules are collected from the wild or from colonies in aquaria during spawning, with an artificial substrate provided for settlement. The timing of spawning is known for many broadcast spawning corals, but opportunities for collection of gametes are generally limited to only once or a few times per year. Brooding species with multiple periods of larval release provide better options for culture of sexually derived propagules. Propagation techniques have developed considerably over the past 20 years, yielding faster growth rates, reduced mortality and reduced detachment from substrates. Simple and cost–effective propagation techniques can be used to restore denuded reefs, preserve endangered species, provide live corals to the international ornamental trade, enable livelihood diversification for coastal communities and provide experimental materials for marine research. This review provides a comprehensive synthesis of recent developments in aquaculture propagation techniques for the purpose of ornamental trade and coral reef restoration, including asexual and sexual propagation, nursery and transplantation stages.

Sustainable production and use of cleaner fish for the biological control of sea lice: Recent advances and current challenges

Article

Jul 2018

Currently, cleaner fish are one of the most widely used sea lice control strategies in Atlantic salmon aquaculture. Two species are currently being farmed in North Atlantic countries, ballan wrasse (Labrus bergylta) and lumpfish (Cyclopterus lumpus), and the sector in most countries is rapidly expanding towards self-sufficiency. The species are very different both in terms of their biology and life histories and, consequently, production and husbandry methods must be tailored to each species. There are numerous health challenges currently experienced in both species, with bacterial and parasitic diseases being the most prevalent, and cohabitation with salmon may increase the risk of disease. Good husbandry and routine health monitoring are essential, although treatment is often required when disease outbreaks occur. Ballan wrasse and lumpfish are both proven to be effective salmon delousers, although delousing efficacy can be variable in farmed fish; the provision of suitable habitat and acclimation to net-pen conditions may encourage natural behaviours, including delousing, and the use of operational welfare indicators can highlight potential welfare issues. Cleaner fish research is progressing rapidly, although much of the basic knowledge regarding the species’ biology remains unknown. The simultaneous domestication of two new marine aquaculture species is a significant challenge demanding sustained effort and funding over a prolonged period of time. Research must focus on enhancing the robustness of the farmed stocks and increasing hatchery outputs to meet the urgent demands from the salmon sector and protect wild stocks from overfishing.

The Reef Aquarium, Vol. 3: Science, Art, and Technology

Book

Nov 2005

I am sorry, but this book is out-of-print and no reprints or copies have ever been available to send out, so please do not request these. Copies _can_ be obtained via a library, interlibrary loan, purchased online as an ebook from Amazon.com, or as a printed version from various online book resellers. The Reef Aquarium Volume Three: Science, Art, and Technology Reefkeeping science involves the interplay of biology, chemistry, and physics. However, a reef aquarium is not simply a product of scientific knowledge. The application of engineering and its product technology, makes it possible to duplicate the specific biological, chemical, and physical requirements of a coral reef in a relatively small volume of water. This third volume in The Reef Aquarium series, provides the most thorough description of the science behind the creation of a captive reef, and critically reviews and explains the different philosophical approaches to reef aquarium design. It also describes and illustrates the existing as well as emerging technology for building reef aquariums, to help guide the selection of equipment, its proper use, and installation. While science and technology afford the blank canvas and tools to build a suitable life support system, the plants, animals, and of course the aquarist provide the final ingredient that we call art. This art also involves the system design as it relates to the living space, the aesthetic appearance of the display, and its ease of maintenance, safety, and functionality. To this end, this book provides a wealth of information regarding aquascaping techniques, which combine art, biology, and physics; and invaluable information regarding plumbing, electrical, and other aspects of the aquarium design that combine art and engineering. Lastly, this book discusses the benefits and potential environmental impacts of the marine aquarium hobby, the challenges for its future, and possible new directions. The Reef Aquarium volume three is the essential manual for all reef aquarium hobbyists, professional aquarists, and coral reef researchers who study, create, and enjoy coral reef ecosystems in the confines of an aquarium.

Spectral sensitivity, spatial resolution, and temporal resolution and their implications for conspecific signalling in cleaner shrimp

Article

Jan 2016

Cleaner shrimp (Decapoda) regularly interact with conspecifics and client reef fish, both of which appear colourful and finely-patterned to human observers. However, whether cleaner shrimp can perceive the colour patterns of conspecifics and clients is unknown, because cleaner shrimp visual capabilities are unstudied. We quantified spectral sensitivity and temporal resolution using electroretinography (ERG), and spatial resolution using both morphological (inter-ommatidial angle) and behavioural (optomotor) methods in three cleaner shrimp species: Lysmata amboinensis, Ancylomenes pedersoni, and Urocaridella antonbruunii. In all three species, we found strong evidence for only a single spectral sensitivity peak of (mean±s.e.m.) 518±5 nm, 518±2 nm, and 533±3 nm, respectively. Temporal resolution in dark-adapted eyes was 39±1.3 Hz, 36±0.6 Hz, and 34± 1.3 Hz. Spatial resolution was 9.9±0.3°, 8.3±0.1°, and 11±0.5°, respectively, which is low compared with other compound eyes of similar size. Assuming monochromacy, we present approximations of cleaner shrimp perception of both conspecifics and clients, and show that cleaner shrimp visual capabilities are sufficient to detect the outlines of large stimuli, but not to detect the colour patterns of conspecifics or clients, even over short distances. Thus, conspecific viewers have likely not played a role in the evolution of cleaner shrimp appearance; rather, further studies should investigate whether cleaner shrimp colour patterns have evolved to be viewed by client reef fish, many of which possess tri- and tetra-chromatic colour vision and relatively high spatial acuity.