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Light intensity can trigger differentagonistic responses in juveniles ofthree cichlid speciesThaís B. Carvalho a , James C. Ha b & Eliane Gonçalves-de-Freitasc

a Departamento de Ciências Fisiológicas, Universidade Federal doAmazonas (UFAM), Manaus, AM, Brazilb Psychology Department, University of ‘Washington, Seattle, WA,USAc Departamento de Zoologia e Botânica e Centro de Aquiculturada UNESP, Universidade Estadual Paulista (UNESP), São José do RioPreto, SP, BrazilVersion of record first published: 28 May 2012.

To cite this article: Thaís B. Carvalho , James C. Ha & Eliane Gonçalves-de-Freitas (2012): Lightintensity can trigger different agonistic responses in juveniles of three cichlid species, Marine andFreshwater Behaviour and Physiology, 45:2, 91-100

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Marine and Freshwater Behaviour and PhysiologyVol. 45, No. 2, March 2012, 91–100

Light intensity can trigger different agonistic responses in juveniles of

three cichlid species

Thaıs B. Carvalhoa*, James C. Hab and Eliane Goncalves-de-Freitasc

aDepartamento de Ciencias Fisiologicas, Universidade Federal do Amazonas (UFAM),Manaus, AM, Brazil; bPsychology Department, University of ‘Washington, Seattle,WA, USA; cDepartamento de Zoologia e Botanica e Centro de Aquicultura da UNESP,Universidade Estadual Paulista (UNESP), Sao Jose do Rio Preto, SP, Brazil

(Received 28 January 2012; final version received 28 January 2012)

Light intensity affects aggressive behavior in fish because this variableinfluences physiological processes. Such effects could, however, varyaccording to the species and the ontogenetic stage of life because differentlife history can modulate behavior. Thus, we compared the effect of lightintensity on the agonistic behavior of juvenile cichlids acara tingaGeophagus proximus, Nile tilapia Oreochromis niloticus, and the angelfishPterophyllum scalare under low and high light intensity conditions. Fishwere isolated in 36 l-aquaria for 96 h and paired (resident-intruder) untilhierarchy settlement, while agonistic interactions were recorded. High lightintensity increased latency to fighting in G. proximus and O. niloticus, butdid not affect it in P. scalare. High light intensity also affected theoccurrence of several other agonistic behaviors (chase, circling, lateral fight,frontal display, and mouth fight) but in different ways across the threespecies. We conclude that mechanisms underlying these data reflectdifferences in the natural history of the cichlid species.

Keywords: aggressiveness; rank order; environmental disturbance; lifehistory

Introduction

Changes in the aquatic environment can emerge from global climate perturbations,destruction of riparian vegetation, changes in dynamic of plant community (Barkoet al. 1986; Sand-Jensen 1989), human disturbance, and also from artificialenvironment found in aquaculture systems (Barrella et al. 2000). In such conditions,organisms can adjust their physiology and behavior in response to short- or long-term changes (Wingfield 2003), such as aggressiveness that is one trait that could beaffected by environmental perturbations (Sloman et al. 2001; Sneddon et al. 2006).Besides several studies related to the effect of environmental changes on physiologyand behavior, one that is still poorly explored is the effects of light intensity on fishaggressive interactions as well the mechanisms that modulate these relationships.

Increased light intensity can reduce aggressiveness in some fish species (Sakakuraand Tsukamoto 1997; Castro and Caballero 2004). In fact, the reduction of

*Corresponding author. Emails: thaisbillalba@ufam.edu.br; thaisbillalba@yahoo.com.br

ISSN 1023–6244 print/ISSN 1029–0362 online

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aggressiveness in high light intensity is a more profitable strategy to reduceconspicuousness (Castro and Caballero 2004). In this way, we predicted that anincrease in light intensity would decrease aggressive interactions among individualsas an adaptive mechanism to reduce the predation risk. Additionally, the effect ofthis abiotic factor on the aggressiveness can be species specific and related to sexualmaturity and living conditions of the fish.

Aggressiveness is frequently investigated in adult fish because agonistic contest isusually related to territorial defense for reproductive purposes (Baerends andBaerends-Van Roon 1950). But, some juvenile fish show aggressive behavior (e.g.,Alvarenga and Volpato 1995; Goncalves-de-Freitas and Mariguela 2006), probablytoward competition for space or food, but the factors affecting this behavior are littleknown. Thus, our goal was to test the effect of light intensity on agonistic behaviorof juvenile cichlids acara tinga Geophagus proximus (Castelnau 1855), Nile tilapiaOreochromis niloticus (L. 1758) and the angelfish Pterophyllum scalare (Schultze1823). These cichlid species were chosen because this fish family exhibits significantaggressive interactions (Baerends and Baerends-Van Roon 1950; Barlow 2000) andthey have been used to understand effects of environmental changes on behavior(e.g., Kotrschal and Taborsky 2010). We also chose species that are important forornamental fisheries and aquaculture (Popma and Lovshin 1995; IBAMA 2008),which is another condition in which fish may be exposed to constant changes in lightintensity. Also, they are found in different habitats. Geophagus proximus andP. scalare are Amazonian cichlids, but acara tinga live in mud and sand-bottomedchannels and angelfish inhabit swamps or flooded grounds where the aquaticvegetation is dense and the water is clear (http://www.fishbase.org/search.php). Onthe other hand, O. niloticus is an African cichlid fish that occurs in a wide variety ofhabitats (Axelrold 1996) and this species is subjected to high predation risk than theneotropical cichlids. Moreover, it was important to examine these effects in morethan one species because the diversity of tropical fish and the extent of theirbehavioral generalizations are not well documented.

Material and methods

We tested the influence of light intensity on aggressiveness in pairs of juvenile cichlidsG. proximus, O. niloticus, and P. scalare. The agonistic behavior of pairs wascompared between low and high light intensity environments.

Animals and rearing conditions

We used G. proximus and O. niloticus held in outdoor ponds at Sao Paulo StateUniversity (UNESP)/Aquaculture Center of UNESP (CAUNESP), Sao Jose do RioPreto, SP, Brazil. Pterophyllum scalare were provided by the Laboratory ofOrnamental Fish/Aquaculture Center of UNESP (CAUNESP), Jaboticabal, SP,Brazil. Thus, captive-bred fish were used for the three cichlid species.

Before the experiments, the fish were acclimated to laboratory conditions in500L indoor tanks (ca1 fish 5L�1; 27�C and 12 h light/dark cycles) for at least15 days. Biological filters and constant aeration ensured water quality. Fish were fedto satiation with commercial ration for tropical fish (G. proximus: Alcon Bottomfish�; O. niloticus: 32% protein; Guabi/Pira�; P. scalare: Alcon Basic�) twice a day.

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Experimental design

We compared aggressive interactions in juvenile pairs under two light intensity

treatments showed as mean� S.D.: low � 253.56� 58.14 l� (n¼ 10 for each species)

and high � 1446.53� 640.68 l� (n¼ 10; exception in high intensity in G. proximus

where n¼ 8). Fish were sized, weighed, and isolated for 96 h (to avoid the

interference of prior residence effect), and paired by using a resident–intruder

paradigm (Figler and Einhorn 1983) with sufficient time for hierarchical settlement:

G. proximus �30min (Teresa and Goncalves-de-Freitas 2003); O. niloticus �40min

(Carvalho and Goncalves-de-Freitas 2008) and P. scalare �20min (T.B.Carvalho

personal communication). Hierarchical settlement in cichlid can be easily identified

by behavior (dominant fish chase subordinates, which in turn do not attack back

dominant), as described by Baerends and Baerends van Rom (1950). Furthermore,

social rank was also checked by the frequency of aggressive acts directed to the

opponent fish (e.g., Boscolo et al. 2011 for Nile tilapia). Agonistic interactions were

recorded in that period for each species and observations were made at the same time

of day (14 : 00–16 : 00 h).

General procedures

During all isolation and pairing period, the animals were held under light intensities

according to their assigned treatment. The average light intensity in each treatment

was taken from 36 points shown in the aquarium, by means of a portable digital

luximetre (model LD 240). The high light intensity was emitted from two 9W

fluorescent light bulbs placed 55mm above the water surface. The low intensity was

obtained from the conventional illumination of the laboratory. The light intensities

used corresponded to those observed in outdoor ponds and under laboratory

conditions.Pairs were formed by size-matched fish in the two light intensity treatments

(Table 1) and the individual recognition of G. proximus and O. niloticus was provided

by small cuts in its caudal fin (as used in Fernandes and Volpato 1993 and Hoglund

et al. 2005). Pterophyllum scalare was identified by natural differences in body

coloration. Sexual dimorphism has not been observed in juveniles; thus, we did not

match pairs by sex. Sexual immaturity was confirmed at the end of the experiment by

macroscopic analysis of gonads.

Table 1. Standard length (LS) and mass (M) (mean� SE) of resident and intruder fish in thethree cichlid species.

Geophagus proximus(n¼ 16)

Oreochromis niloticus(n¼ 20)

Pterophyllum scalare(n¼ 20)

Resident Intruder pa Resident Intruder pa Resident Intruder pa

LS (mm) 72.9� 0.6 72.2� 0.7 0.52 60.6� 0.7 60.5� 0.7 0.94 31.1� 0.4 30.3� 0.4 0.22M (g) 10.25� 0.32 9.96� 0.39 0.57 8.69� 0.44 7.80� 0.28 0.92 1.12� 0.06 0.98� 0.05 0.9

Notes: aStudent’s t independent test.

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Aquaria and animal manipulation

All fish (intruder and resident) were isolated in 36L glass aquaria(300� 300� 400mm) with three walls covered with an opaque blue plastic toprevent visual contact among other isolated fish. Blue color was chosen due to itseffect on reducing cortisol levels after stress experience in O. niloticus (Volpato andBarreto 2001). Water temperature was regulated to 25.80�C� 1.30�C and photope-riod to 12 h light/dark cycles. The animals were fed with commercial ration (seerearing conditions) corresponding to 2% of biomass offered twice a day.

Biometry and isolation were preceded by anesthesia with benzocaine(12.8mg l�1). Anesthesia was not used to transfer intruder fish to resident aquarium,though they were carefully manipulated to avoid stress.

Agonistic behavior

Aggressive interaction was quantified in terms of frequency of different agonisticevents (Table 2). The ethogram was based on previous descriptions forG. surinamensis (G. proximus) (Teresa and Goncalves-de-Freitas 2003), O. niloticus(Falter 1983; Alvarenga and Volpato 1995), and P. scalare (Yamamoto et al. 1999).The time elapsed between fish introduction in the resident’s aquarium until the first

Table 2. Aggressive behavior in the three cichlid species.

Agonistic event

Species

G. proximus O. niloticus P. scalare

Chase: one fish follows the opponent thatswims in opposite direction.

X X X

Circling: two fish with erected dorsal fin swimfollowing each other, describing a circle, likea very slow chasing.

0 X 0

Frontal display: both fish approach frontallyeach other with head-up posture (around45�), but without physical contact.

0 0 X

Lateral fight: the fish remain alongside eachother facing the same or opposite directionand beat their tails sideways.

X X 0

Lateral threat: one fish with their fins spreadand mouth opened approaches laterally tothe opponent, which keeps away.

X X X

Mouth fight: both fish approach frontally eachother with their mouths opened and bite theopponent’s mouth. Their mouths are kepttightly together while one fish displaces theopponent backwards.

X X X

Nipping: the aggressor swims toward theopponent and bites its body.

X X X

Undulation: only one fish beats its tail side-ways (undulating the body), withoutspreading its fins.

X X X

Notes: X – agonistic event is observed for species; 0 – agonistic event is not observed forspecies.

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aggressive interaction (latency to perform the aggressive behavior) was recorded foreach species. The dominance settlement was defined as loser animal exhibitedsubmissive behaviors, such as changes in body color and escape from anotherindividual (dominant), as observed by Falter (1983).

Data analyses

The Shapiro–Wilk test was used to test data normality (Zar 1999) and the Fmax testwas used to check homocedasticity (Ha JC and Ha RR 2011). As the time of pairingwas not the same for each species, we used the percentage of time to compare latencyamong the three species. No transformations of the rate data were required. The rateof behaviors (frequency min�1), and latency to fighting were compared betweentreatments using multiple general linear modeling (multiple ANOVA; Tabachnikand Fidell 1989) and univariate tests when indicated (results of the univariate testsare reported). Light condition, species and the potential interaction of the twofactors was tested using multiple MGLM techniques (multiple two-way ANOVA;Tabachnik and Fidell 1989), followed by univariate tests (reported) and Bonferroni-corrected post-hoc comparisons. All statistics were conducted using Systat(Wilkinson et al. 1996). Statistical significance was set to �¼ 0.05.

Ethics

This study was conducted according to the ethical principles adopted by theBrazilian College of Animal Experimentation (COBEA) and was approved by theEthical Commission of Animal Experimentation of the Sao Paulo State University(UNESP), Botucatu, SP, Brazil (protocol 052/06).

Results

High light intensity showed higher latency to fighting in G. proximus (df¼ 1.16,p< 0.05) and O. niloticus (df¼ 1.18, p< 0.01), but did not affect P. scalare (Figure 1).

0

20

40

60

80

low light intensity high light intensity

late

ncy

to f

ight

ing

(%)

b* b

b

b

a* a

Figure 1. Mean (�SE) latency to fighting for Geophagus proximus (h), Oreochromis niloticus(#) and Pterophyllum scalare (#) in the two light intensity conditions. Asterisks indicatesignificant differences between light intensities for each species (p< 0.005). Different lettersindicate significant differences between the three species to each light intensity (p< 0.0001).Data are show as percentage of the total time of paring.

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High light intensity provided less chase, circling and lateral fight in O. niloticus(df¼ 1.18, p< 0.05) more frontal display and mouth fight in P. scalare (d.f.¼ 1.18,p< 0.01) and did not affect agonistic interactions in G. proximus (Figure 2).

There were some differences among the species of agonistic behavior for bothlight intensity conditions. Circling and frontal display were observed, respectively,only in O. niloticus and P. scalare. Lateral fight was shown in O. niloticus andG. proximus (Table 2). Latency to fighting in O. niloticus was lower than G. proximusand P. scalare (d.f.¼ 2.52, p< 0.001; Figure 1). Moreover, P. scalare showed lowerundulation frequency than the other two species (df¼ 2.52, p< 0.001). The rates oflateral threat were different among species, with P. scalare and O. niloticus exhibitinglower rates than G. proximus (df¼ 2.52, p< 0.01; Figure 2). The rates of mouth fightalso varied by species, with P. scalare exhibiting a higher rate and G. proximusexhibiting a lower rate than O. niloticus (df¼ 2.52, p< 0.01; Figure 2).

Discussion

Some studies have shown that light intensity affects aggressive behavior in fish, butseveral of these results are contradictory. In fact, high light intensity can reduce thefrequency of agonistic interaction (Sakakura and Tsukamoto 1997; Castro andCaballero 2004), but high light condition increases aggressiveness in other species(Valdimarsson and Metcalfe 2001; Almazan-Rueda et al. 2004). In the same way, ourresults show that light intensity affected the agonistic behavior of different species ofjuvenile cichlids in different ways. This suggests that responses could be speciesspecific.

Latency to perform aggressive behaviors was higher in G. proximus andO. niloticus to low light intensity treatment. However, this abiotic factor does notaffect the aggressive levels in P. scalare. Changes in aggressiveness are a function of atheoretical concave-down-shaped curve across increased light intensity conditions(Sakakura and Tsukamoto 1997; Castro and Caballero 2004). This curve has anintensity threshold following which aggressive behavior decreases rapidly. Thus, thelow rate of agonistic interactions in high light intensity in the O. niloticus wouldindicate that this aggressive suppression threshold was exceeded. Nevertheless, inangelfish, the threshold cannot have been reached, because aggressiveness was higherin high light levels. In G. proximus, effects of light intensity on the frequency ofagonistic interactions was not observed, indicating that our high light intensity levelwas not enough to affect the regulating mechanisms of the aggressive behavior in thisspecies. Thus, our results indicate that aggressive levels in different cichlid speciescould be engendered from different levels of sensitivity to light intensity.

The differential response to light intensity observed among the three species canbe associated to environmental parameters, because species with different ecologicalpreferences can show distinct adaptations to environmental conditions (Burlesonet al. 2001). On the other hand, the differences in life history do not necessarilyinvalidate the effect of the environment on aggressiveness in relation to lightintensity. Moreover, the lack of natural history information about these species(especially G. proximus) makes it difficult to make more precise predictions regardingaggressiveness in different light conditions.

Besides evolutionary characters related to environment, the effects of high lightintensity on the aggressive interactions in the three cichlid species can also be derived

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threatmouth fight

nipping undulation lateralfight display

chase lateral circling frontal total flight

freq

uenc

y.m

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freq

uenc

y.m

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chase lateral circling frontal display

total flight

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(c)

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nipping undulation lateral

nipping undulation lateral fight display

circling frontal total flight

(b)

b

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ac

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* *

**

bXXX XXX

XXX

XXX XXX

*

Figure 2. Mean frequency (�SE) of aggressive interaction for Geophagus proximus (a),Oreochromis niloticus (b) and Pterophyllum scalare (c) in low (h) and high (#) light intensityconditions. Behavior unit absent for species is denoted by triple x. Asterisks indicatesignificant differences between light intensities in each species (p< 0.005). Letters indicatedifferences among species to each light intensity (p< 0.001).

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from different mechanisms. If changes in abiotic factors may be a stressor (e.g.,Sneddon and Yerbury 2004) then the low aggressive behavior may be a strategy toavoid high-energy expenditure in high light condition. Moreover, this effect of lightintensity on the agonistic interaction can reduce animal conspicuousness (Castro andCaballero 2004) and vulnerability to predators (Britz and Pienaar 1992). Forexample, juvenile pike-perch Sander lucioperca (L. 1758) and tench Tinca tinca(L. 1758) showed preference for the lowest available light intensity (Gallardo et al.2006; Luchiari et al. 2006; respectively). Moreover, adult nonbreeding long-ear sunfish Lepomis megalotis (Rafinesque 1820) preferred to occupy low light intensity andsubmerged cover because this condition may be a refuge from predation (Goddardand Mathis 1997). This could also be the main point regulating aggressiveness duringthe juvenile phase of life, because juvenile fish need to be hidden to reduce predationrisk, instead of defending territory to attract females.

Oreochromis niloticus originate from habitats with high predation risk, thereforethey appear to diminish such risks by reducing interactions. Predation risk should beless intense for neotropical cichlids, thus latency to fighting is reduced forG. proximus. In P. scalare, an increase in agonistic interactions in high lightintensities can be mediated by the reduction of plasma melatonin levels, a hormonereleased in low light intensity (Ekstrom and Meissl 1997; Bayarri et al. 2002) and thatcan reduce the aggressiveness in fish (Munro 1986). Although the total fightfrequency of P. scalare did not increase, some energetically costing behaviors doincrease (e.g., Alvarenga and Volpato 1995), suggesting light levels can increaseaggressiveness in such species over longer periods.

We observed that the three cichlid species showed some differences inaggressiveness (frequency and agonistic events). In fact, different levels of aggressivebehavior can be affected in distinct ways by external factors, such as light regimes(e.g., Benus et al. 1988). Thus, our results could emerge from different strategiesassociated with the aggression profiles of each species.

In this study, the light intensity triggered behavioral strategies in cichlid fish, whichcorresponds to emergency life-history stage (‘take-it-or-leave-it’) which emergenceallow organisms to adjust to predictable or unpredictable environmental perturba-tions (Wingfield 2003). Furthermore, the light intensity is an environmental factor thatcan be controlled in rearing systems to reduce the harmful effect of aggressiveness onthe health and welfare of farmed fish. Finally, this study highlights the importance ofcomparative behavior studies at other-than-adult life history stages.

Acknowledgments

The authors thank J.B.K. Fernandes (Aquaculture Centre of UNESP) for donating P. scalare;R.S. Costa-Ferreira and C.E. Souza for the technical support. This study was sponsored byFundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP), proc. 2006/05013-0.

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