Burst Response of Damselfish (Ontogeny)

Burst response of the Damselfish, Acanthochromis polyacanthus to visual

stimulus

ABSTRACT: Burst performance determines the ability of fish to avoid predators and capture prey,

especially in their larval or juvenile stages. Since most coral reef fishes are sedentary, burst

performance has the potential to determine survival and abundance of adult fish within a habitat.

Previous studies on burst performance of vertebrates focused on commercial freshwater and

marine fishes. This study focuses on the burst performance of a coral reef fish, Spiny chromis

(Acanthochromis polyacanthus), which is abundant common species on the Great Barrier Reef,

Australia. Furthermore, this species of damselfish has the unique characteristic that it does not

have a pelagic larvae stage, but rather hatches as a juvenile. This study examines the effect of

early ontogenetic development of juveniles and the effect caused by batch variation to burst

performance. This study was done by identifying the pattern of various variables such as

maximum burst speed, directionality and responsiveness in burst performance. Parameters of

burst performance examined included the maximum burst speed, mean burst speed, directionality

and response latency. Visual stimulus, a looming silhouette triggered by a pendulum was used to

imitate a predator attack to initiate a startle response from the juvenile. As predicted, larger and

older juveniles had higher maximum burst speed and mean burst speed. Both of these variables

were highly correlated. Generally, juveniles showed improvement of burst response variables

such as higher maximum burst speed, mean burst speed, directionality and responsiveness as

they grow. However, no parental effect was found on burst performance variables and there was

no ontogenetic effect on the response latency of juveniles. Interestingly, the response latency of

the juveniles was weakly correlated with their maximum burst speed. More research is needed to

clarify the relationship between the kinematic and sensory receptors during the burst performance

of this species. This study shows that the importance of burst performance behaviour during the

early life stage of a coral reef damselfish in predator avoidance.

KEY WORDS: Juvenile fish – Coral reef – Burst Performance – Growth and Development-Batch

effect

INTRODUCTION

Burst performance of fish is an important mechanism for predation avoidance and for

obtaining food in the early life stages of fish (Eaton and DiDomenico, 1986). Previous studies

have found that the food availability is less important source of mortality during the larval phase

than predation (Martin et al, 1985; Paradis et al., 1996). Hence, predator avoidance influences

fish survival and for this reason burst performance is a key mechanism in population dynamic

study. Burst performance is also often known as escape or fast-start response to external

stimulus or threats (Webb, 1976).

Body size and ontogenetic development of fish have been proposed as the major factors

that influence burst performance (Bailey, 1984; Bailey and Batty, 1984; Blaxter and Batty, 1985;

Margulies, 1989; Cowan et al, 1996). Body size of mackerel (Scomber scombus), white seabass

larvae (Atractoscion nobilis), and fish length northern Anchovy (Engraulis mordax) were found to

determine the burst swimming speed (Margulies, 1989; Wardle and He, 1988; Webb and Corolla,

1981). Age is correlated with size and ontogenetic development and these are also known to

influence escape performance. The development of sense organs (Blaxter, 1986, Blaxter, 1988;

Blaxter and Fuiman, 1990; Blaxter, 1991), visual neurological responses (Anderson, 1988) and

locomotor mechanics (Hale, 1996) all seem to improve the fast start performance of fish. Size

and age correlates with larval survival, such that smaller individuals often have a higher

probability of dying (the ‘bigger is better’ hypothesis, Miller et al. 1988). There is however,

considerable debate on the general applicability of this hypothesis (Litvak & Leggett 1992;

McCormick & Molony 1993).

Parental effects can be profound during the early life stage of teleosts fish (Kamler,

2006). Batches of juveniles from different parents or clutch effect showed different behavioural

performance for red drum (Sciaenops ocellatus) larvae on the burst performance (Fuiman et al.

2005) especially during their early life stage. However, previous field studies on batch effects on

larval quality in term of burst performance were highly confounded by environmental effects, such

as water temperature (marine temperate fish, Batty et al, 1993; freshwater fish, Lyon et al, 2008)

and timing of spawn within a breeding season ( Fuiman et al, 2005). In addition, nutrition levels in

the water or food supply after hatching also influence the success of a larval batch (Yin and

Blaxter, 1987). The present study investigates the effect of different parents on the larval burst

speed.

Other factors, such as previous experience, phenotypic plasticity and rearing condition,

influence the burst performance of larvae. A previous study showed that the reactive distance of

the zebra danio increased as a function of past experiences (Dill, 1974a). It showed repetitive

stimulus to a single subject will cause uncertainty or noise in burst performance. Phenotypic

plasticity is another noise factor in behavioural study (Wiedenmayer, 2009). The rearing condition

variation such as temperature (Batty et al, 1993) and food (Yin and Blaxter, 1987) can cause

developmental change of larval. Herring larval, Clupea herengus had higher burst speed in higher

post-hatching environment temperature (Batty et al, 1993). Well fed marine fish larvae such as

Clyde and Baltic-herring, cod and flounder had higher burst speed than others (Yin and Blaxter,

1987).

A fast-start burst has three kinematic stages (Anderson, 1988). In stage one, the fish

bend their body, orienting themselves away from the stimulus and making a profound tailed flip,

but the center of mass of the fish remain stationary (Foreman and Eaton, 1993; Hale, 2000). In

the second stage, the fish display a reflexive tail flip resulting in the rapid propulsion of the center

of mass (Foreman and Eaton, 1993; Hale, 2000). In the third and final stage, the fish burst and

cruise alternatively away from the stimulus. Other fast start performance variables have included

the burst distance, speed and acceleration, latency of response to the stimulus, the duration of

each kinematic stage, and the change of directionality (Domenici and Blake, 1997). Generally,

smaller fish larvae had shorter duration of the kinematic stages compared to larger fish (Domenici

and Blake, 1997; Hale, 2000). The directionality of fish during burst performance includes the

turning angle and turning radius. The turning angle of fish during escape can span about 180° to

either side of the fish (Domenici and Blake, 1991; Foreman and Eaton, 1993). On the other hand,

the turning radius is important in predator prey interaction and it is always in circular path around

the centre of mass of the fish (Webb, 1976; Domenici and Blake, 1991).The turning radius was

found to be highly related to fish body length (Webb, 1976; Domenici and Blake, 1991).

A variety of methods have been used to study the burst performance of larval fish. The

earliest methods consisted of using the presence of a real predator to feed on the fish larvae.

This is a ‘black box’ experiment, where the gut content of the predator determines the success of

prey during the predator-prey encounter. However, this method had the disadvantage because

the actual acceleration or burst performance of the fish larvae is not measured. However, it was

not until the development of high-speed cinematology in recording the kinematic of fish burst

performance when scientists were able to measure the burst response of fish. Then, the visual

stimulus and acoustic stimulus had been used to trigger the burst performance largely due to it

high repeatability (Dill, 1974b). The most recent developed method is the used of water flow to

trigger the predator strike (McHenry et al, 2009). A previous study was done to compare

response from visual stimuli and acoustic stimuli for red drum (Fuiman et al, 1999).The used of

pendulum with the silhouette that represent the cross section of the fish had most promising

result.

Most studies on burst performance of fish have focused on temperate freshwater species

and pelagic marine species with commercial value (Leis et al, 2006). Early studies include

flounder, plaice, herring and cod larvae (Bailey, 1984), northern anchovy (Webb and Corolla,

1981), salmon, red drum (Fuiman et al, 1999) and zebra Danio (Dill, 1974a,b). There has been

little research tropical reef species despite reef fish being different from temperate fish in many

aspects. For example, similar length reef fish larvae swim faster compared to temperate fish (Leis

and McCormick, 2006). In physiological aspect, fish are able to swim better in warmer tropic (25-

29°C) than in temperate condition (10-20°C) (Fuiman and Batty, 1997). The present study

collected some of the first information for the burst performance of a coral reef fish.

The overall objective of this project was to study the burst performance of a common reef

fish, the spiny Chromis (Acanthochromis polyacanthus). This objective will be achieved by: 1)

comparing the mean and maximum swimming speed during the startle response through the

early development stage of juvenile fish; 2) examining the effect of clutch identity on burst

performance; 3) examining the effect of growth and development on the response latency of

juvenile fish to visual stimulus.; and 4) identifying the change of direction juvenile fish during the

burst performance.

METHODS AND MATERIALS

Study species and maintenance: This study was done in February 2010 using laboratory

reared spiny damselfish, Acanthochromis polyacanthus, a fish lacking a larval dispersal phase

(Doherty et al, 1994; Miller-sims et al, 2008). The reason for choosing this species was to

compare the immediate response of the juvenile to previous studies on larvae. Juveniles of this

species have significant morphological differences from other Pomacentrid larvae (Murphy et al.,

2007), hence the burst performance of the juvenile may be unique. To obtain juveniles, the adult

fish were captured from a few locations within the Northern and Southern regions of the Great

Barrier Reef, because a previous study found that this species had genetically differentiated

subspecies within the Great Barrier Reef (Doherty et al, 1994). Hence, the subjects of this study

represent the whole breed stock of this species. Adult breeding pairs were kept in different tanks

at MARFU (JCU). The tanks were equipped with continuous flow of filtered salt water. Three

bricks were arranged like an arch in the tanks to allow the adult fish to attach the eggs.

Laboratory protocol: Juveniles were separated from the adult fish on the day they

hatched and reared in an air-conditioned environment maintained at constant temperature of 25

°C. The study was conducted in the laboratory and daily observations were taken before juveniles

were fed. A juvenile fish was randomly selected from a batch of fish and left in an aquarium

(10x10x10cm) that had been covered with black and dull fabric on 3 sides for 30 minutes to

acclimate. After the acclimation, an electro-magnetised pendulum was triggered to release a

transparent plate with darken oval, which acted as the burst stimulus. The shape of the oval was

chosen to represent the cross section silhouette of a common predator, the dottyback

Pseudochromis fuscus. A previous study showed that predation was maximal highest when fish

larvae were 10% of the length of the predator (Paradis et al, 1996). Hence, the size of the oval

was approximately the cross section of a dottyback that had 10 times the length of the average

body length of juvenile Acanthochromis. The burst performance of the juvenile before and after

the visual stimulus was video recorded (Fuiman & Cowan, 2003). A soft sponge was used to stop

the swinging stimulus and minimising the noise and vibration from the pendulum to avoid

triggering acoustic and tactile responses from the juvenile.

Video recording and analysis: The entire burst response of juvenile fish was recorded

with a high speed camera at 300fps. The camera was placed parallel to a (30cmx30cm) mirror

with a 45° to the experimental aquarium (Fuiman and Cowan, 2003; Fuiman et al., 2006). The

video was replayed, trimmed and transformed to image sequence (60Hz) using a Quicktime Pro.

Measurements including the burst speed and response latency were made using Image-J with

MtrackJ software. The maximum burst speed of a juvenile is the highest speed performed by it for

3 trials. The mean burst speed of a juvenile is the average of the highest speed performed by it

for 3 trials. Another high resolution digital stills camera was used to record the standard and total

length of the fish and the morphological differences (caudal fin grows) during its development

were noted by observation.

Data analysis: The responsiveness of juvenile fish to the pendulum image was recorded

as a binary variable, 0 as no response and 1 as positive response (Fuiman, 1989; Fuiman et al.,

1999). The response latency was defined as the t ime after the stimulus was triggered until the

first detectable movement observed from the juvenile fish (Domenici and Batty, 1997). The

directionality of the juvenile fish during the escape response was recorded as binary data. “Away

response” and “towards response” each comprised of 180° where the axis line is perpendicular to

the stimulus. One-factorANOVAs were used to examine the effect of size and age on the burst

speed to size and age respectively. Regression line was drawn to illustrate the response latency

to the age (day) and body size of the juvenile fish. Two-factor ANOVA was done on the size and

the batch effect to the maximum burst speed.

RESULTS

The overall mean of burst performance variables, such as the response latency (ms),

Square maximum , maximum burst speed (mm s-1), mean burst speed (mm s-1 )of all 177

juveniles is recorded in Table 1. The descriptive data such as the minimum, maximum and

mean of the variables is recorded.

Ontogenetic trends of maximum burst speed: The maximum burst speed (mm/s)

increased linearly with the length of the fish. The correlation both total length and standard length

of the fish to the maximum burst speed were statistically significantly (Fig. 1). However, the

standard length (r2 =0.149, p<0.001) of the fish showed a stronger burst response compared to

the total length (r2 =0.131, p<0.001).

Batch or clutch effects on juvenile performance: No systematic effect of clutch identity

was observed, where each batch of the juvenile spread within the range of maximum burst speed

within a range of body size (Fig 2).

Juveniles’ responsiveness and response latency: The responsiveness of the juvenile

fish increased as their body size increased and juveniles grew older. Of a total of 228 trials, 177

juveniles (77.6%) responded positively (Table 2 and 3). Juveniles one week after hatching (1wph)

had the lowest positive response (59.5%), followed by two-week post-hatching fish (2wph)

(74.8%), 3wph (82.4%) and 4wph juveniles which had 100% positive response (χ²= 17.705

p<0.001, df =3, Table 2). Juveniles with small standard body length had the lowest positive

response (59.02%), followed by the medium length (76.67%), large (91.94%) and extra large

(100%) juveniles which had 100% positive response (χ²= 23.848 p<0.001, df =3, Table 3). Chi-

squared test was done on the standard body length of the juvenile fish and age of the juvenile

fish. Both body size and age of the juvenile had a significant effect on the response score of the

fish (P<0.001, Chi-squared test).

The response latency had no relationship with the age of the juveniles and their body

size. Latency did not decrease for older juvenile for either total length or standard length of the

fish. However, fish standard length better represented the response time of the fish compared to

total length (r2 =0.10, p<0.001; r2 =0.08, p<0.001 respectively) . There was a negative correlation

between the maximum burst speed and the response latency of juvenile spiny Chromis (r=-0.396,

with 95% CI, Figure 3).

Directionality of the fish: From all the positive response, the initial startle directionality

was showed by binary angular variables. The Away or Towards (A/T) response which each

constitute 180° (Blaxter and Batty, 1985) depend on the change of directionality of fish during the

first stage of burst performance. Hence, the result was as expected where most of the juveniles

(99%) turned away from the stimuli with a few exceptions.

DICUSSION

Development of a startle response : Four of the five variables measured as part of the

burst response variables improved ontogenetically as expected. Maximum escape speed and

mean burst speed both significantly increased as juveniles grew. This result agrees with those of

previous studies on temperate species such as cod, flounder plaice and herring larval (Bailey and

Batty, 1984). However, contrary to previous study showing that the larvae required a shorter time

to respond as they grew larger (Fuiman et al, 1999), our study did not show an ontogenetic effect

on response latency. The 100 % away response showed by A. polyacanthus indicates a good

directionality in the predator prey interaction.

Ontogenetic trends of performance in A. polyacanthus :The maximum swimming

speed of juvenile Acanthochromis was highly dependent on the total length and standard length

of the juvenile fish. This result agrees with a previous study, which derived an equation for

average routine swimming speed as a function of larval total length for 9 species of fish (Miller et

al., 1988). The slope of our function in Figure 1 is slightly steeper than other studies which focus

on Northern anchovy larvae (Webb and Corolla, 1981; { max (cm/s)=1.95+20.8(length(mm)} and

temperate marine fish such as Atlantic Cod (Gadus morhua), Atlantic herring (Clupea harengus),

radiated shanny (Ulvaria subbifurcata) , capelin (Mallotus villosus) and winter flounder

(Pleuronectes americanus) William et al, 1996) {log (max speed) = 0.054 (length) +0.826. The

slope for Acanthochromis was much higher compared to both previous generalisations. This may

be due to a more advanced developmental stage of Acanthochromis, where the juvenile can

swim and feed immediately after they hatch.

Mean burst speed of juvenile Acanthochromis was also highly dependent on the standard

length of the juvenile indicating the importance of body length in predator avoidance. The slope of

the relationship of the mean burst speed against the standard size was smaller than for the

maximum burst speed, but still had a steeper slope compared to a previous studies (William et al,

1996) {log (mean speed) = 0.059 (length) +0.562}. This indicates that comparing the swimming

speed of different species based on length alone is not appropriate because fish undergo

developmental stages at different size. Generally, species which had similar body form perform

similarly.

As expected mean burst speed was highly correlated with the maximum burst speed.

This result agrees to that of a previous study, which also examined the effect of development on

the escape response in marine fishes (William et al, 1996). Since both variables are highly

correlated with body size, hence our study supports the ‘bigger –better hypothesis’ indirectly. This

is based on the hypothesis that higher burst speed enhances survival probability in the predator-

prey encounter. However, the linear increase found in the present study is contra to a previous

study, which included the encounter probability and searching effort as determining factors

(Bailey and Houde, 1989 in Paradis et al., 1996). These studies found that the vulnerability of fish

larvae to invertebrates’ predation and predatory fish is dome shape, where the fish seem to have

its optimum escaping size then the ability decrease through time (Bailey and Houde, 1989 in

Paradis et al., 1996). However, our study only involved the immediate post hatched juvenile,

which is the earliest life stage, hence survival of fish in different stages needs to be examine in

further research.

The response latency of juveniles did not reduce as age and/or body size increased.

These results differ from a previous study, which showed that red drum larvae had a shorter

response time as the larvae grew bigger levelling off as they reached 8 mm total length (Fuiman

et al, 1999). There may be other factors besides age and body size affecting response latency.

One factor may be eye development of the fish (Jones and Blaxter, 1967), where the rod

formations in the retina determine the response latency . Previous study had showed that the size

of eye is one of the determining factors in response time. Besides sensory organ, mechanical

factors, such as muscle constriction that has negative relationship with body length, also may

affect the response latency in this study (Wardle, 1967). The actual distance of the fish from the

stimulus might also affect the response latency. A study showed that the fish responded earlier

when they were nearer to the source of stimulus. The depth of the juvenile when the stimulus is

triggered was founds to be influential in response latency. This was due to the velocity of the

looming silhouette from the pendulum, known as the approaching speed of the dark oval, to the

juvenile. Since the stimulus is a two-dimensional image, due to the refraction of light the visual

image viewed by the juvenile is different at different depths in the aquarium.

However, our study found that the response latency of juveniles showed an interesting

negative relationship with maximum burst speed. Juveniles that reacted faster also responded

with a higher speed, or they had a faster burst response. This indicates that the magnitude of the

innate response by the juvenile is highly related to the effect of stimulus but, more research is

needed to understand the relationship of these two burst performance variables. A correlation

between these two variables, as showed in this study, would have important implications in our

understanding of the predator-prey encounter process.

Ontogenetic trends in juvenile responsiveness: The responsiveness of the juvenile fish

to the stimulus also increased as the size of the fish increased. This finding agrees with those of

previous studies on red drum larvae (Fuiman et al, 1999) and herring larvae (Blaxter and Fuiman,

1990). The increasing trend in this study was significant for larvae less than 6mm in body length,

but then the probability of responsiveness levelled off. Acanthochromis had a better

developmental stage compared to red drum larval and herring larvae, which each levelled off

after reaching 8mm (Fuiman et al., 1999) and 26 mm (Blaxter and Fuiman, 1990) respectively.

Hence, reef fish juvenile had better responsiveness compared to marine temperate fishes with

respect to body size.

An increase in the probability that a fish would respond to a visual stimulus indicates the

increase of active predator avoidance mechanism in these fish. They utilised more active

mechanisms for predator avoidance as their size increased. The newly hatched juvenile might

utilise other forms of predator avoidance mechanism, such as remain static and sink ing to the

bottom to camouflage themselves from the predator. Since they are small and less efficient

swimmers, their only mechanism to survive is to hide from the predator. This might indicate a shift

of mechanism from early to late juvenile stage from stationary camouflage to active escape.

Since their burst speed increases with body size, they can use more effective mechanism in

predator-prey encounter with increasing size.

Batch or clutch effects on juvenile performance: The maximum burst speed of juvenile

fish varied over a similar range with growth and development. This study showed no batch or

clutch effect on the burst performance, hence it support the risk spreading reproductive strategy

indirectly. This theory states that females try to vary the condition their offspring to maximise the

chance of batch survival. In other words, the individual survival is not as important as batch

survival in this reproductive resource allocation strategy. Although the Spiny Chromis lacks a

pelagic larvae stage, females may still practise this way of maximising the success of a

population through its evolution.

Kinematics of the burst performance: The usual swimming burst speed and the

stimulated burst speed were found to be highly correlated to one another (Holmes and

McCormick, 2009). This suggests that the improvement of propulsive surface area as the fins and

caudal tail grow helps the fish to burst in both circumstances. We observed that the surface area

of the caudal tail in the present study increased as the size of the juvenile reached 9 mm. This

result agrees with those of previous studies on many species of fish larvae (Fuiman, 1983;

Fuiman et al, 1988). Red drum larvae start to grow their caudal fin rays at a size of 4.5mm and

finish the process before they reach 6.0 mm, after which the burst speed increment reduces

(Fuiman et al., 1998). Hence, swim-related morphological features do influence on burst

performance kinetically.

Directionality during the first stage of the burst response (‘away response’): Only the

newly-hatched juvenile fish did not show a positive away response in Acanthochromis. This

suggests that that their visual sensory organ had not developed yet (at the body length of ~6mm).

For temperate fish, proliferation of rod in the peripheral retina occurred at a threshold of 25-30mm

body length (Blaxter and Jones, 1967). The result of the present study agrees with previous

studies where larger larvae showed a better away response to the stimulus with increasing age

(Yin and Blaxter, 1987; Domenici and Batty, 1997). An improvement in visual acuity might be the

cause of these directionality changes in escape response.

Limitations of the study : There were some limitations in recording the fish movement

such as the container volume, temperature and the duration of the experiment (Paradis et al.,

1996). The size of the container limits the distance travelled by the juvenile, because they reach

the side of the aquaria within a second forcing it to change direction. However, a previous study

on herring larvae showed that the response distance is no associated with sensory capability

(Blaxter and Fuiman, 1990). A second limitation of this study is the burst performance variables

only included the two dimension analysis (horizontal image only), hence the vertical movement of

the juvenile was ignored. To include this it is necessary to develop a new image analysing

software and a recording method to measure the change in depth by juvenile fish in burst

response. Since two out of the five variables measured depend on the distance travelled, it will be

more accurate if we included the vertical distance travel during the burst.

CONCLUSION

This study examined the burst performance variables for a common coral reef fish,

Acanthochromis polyacanthus. Measurements of burst performance, including mean and

maximum burst speed, directionality and response latency represent the first dataset for a coral

reef fish. These data can be used as reference for further studies on reef fish in survival during

the post-hatching stage. The present study found that the burst performance of very young

juveniles was less active compared to older juveniles. Their transparent body and static reaction

upon hatching may be due to underdeveloped sense organs or an innate response. On the other

hand, the older juveniles (more than 7 days after hatching) actively burst away from the stimulus

source. Future studies should examine the impact of parental condition in influencing the

development of burst performance in this interesting coral reef fish species.

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Appendix

Table 1. Summary statistics for routine swimming, escape performance and morphological traits for Acanthochromis polyacanthus juvenile. Data from all positive response trials are included (N=177). Variables Minimum Maximum Mean

Standard Length (mm) 5.30 11.80 7.86

Response latency (ms) 0.083 0.433 0.231

Square maximum (mm s-1)2 8999.4 363932.3 90452.3

Maximum response speed (mm s -1) 94.87 603.27 280.29

Mean response speed (mm s -1) 69.79 531.44 215.46

Table 2 Responsiveness of the juvenile at each week (χ²= 17.705 p<0.001, df =3)

Total number of juveniles is 228.

Responsiveness N Number of positive

response Percentage of

positive response

First week juveniles, N1 37 22 59.46%

Second week juveniles, N2 107 80 74.77%

Third week juveniles, N3 51 42 82.35%

Forth week juveniles, N4 33 33 100.00%

Table 3 Responsiveness of the juvenile at different group of body size during it early life stage

(χ²= 23.848 p<0.001, df =3). The body size ranges of different group of juveniles were as below:

Small (0.53-0.64cm), Medium (0.65=0.79cm), Large (0.80-1.04cm), Extra large (1.05-

1.18cm).Total number of juveniles is 228.

Responsiveness N Number of positive

response Percentage of

positive response

Small juveniles, N1 61 36 59.02%

Medium juveniles, N2 90 69 76.67%

Large juveniles, N3 62 57 91.94%

Extra Large, N4 15 15 100.00%

Figure 1 Relationship between standard length and maximum burst speed for Acanthochromis

polyacanthus juveniles of varying sizes. Burst responses of the fish were stimulated by a

pendulum. n=228

Figure 2 Relationship between standard length and maximum burst speed for Acanthochromis

polyacanthus juveniles of different batch or clutch, n=177.

Figure 3. Relationship between maximum burst speed and response time N=177.