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ACOUSTIC BEHAVIOUR IN MALAWIAN
CICHLIDS (PSEUDOTROPHEUS, CICHLIDAE):
POTENTIAL CUES FOR SPECIES RECOGNITION
AND INTRASPECIFIC COMMUNICATION
AKUSTIŒNO VEDENJE MALAVIJSKIH CIKLIDOV
(PSEUDOTROPHEUS, CICHLIDAE):
MOÆNA VLOGA PRI PREPOZNAVANJU VRST
IN PRI INTRASPECIFIŒNI KOMUNIKACIJI
JOSE MIGUEL SIMÕES, INES DUARTE, PAULO JORGE FONSECA, G.
F. TURNER & M. CLARA P. AMORIM
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RAZPRAVE IV. RAZREDA SAZU XLVII-3 229–236 LJUBLJANA 2006
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ABSTRACT
Acoustic behaviour in Malawian Cichlids (Pseudotropheus, Cichlidae): Potential cues for species recognition
and intraspecific communication
Acoustic communication may play an important role in mate recognition systems among African cichlids and
may contribute to the evolutionary processes involved in their rapid speciation. Sounds produced in early courtship
(during quivering) by males of three closely related Malawi species of the Pseudotropheus zebra complex
(Pseudotropheus zebra, P. callainos and P. ‘zebra gold’)were recorded and compared among species. In one species
(P. zebra), sounds emitted during quivering were compared to sounds produced during later courtship behaviour, such
as circle and lead-swim, and with sounds emitted during male-male and female-female interactions. The following
acoustic parameters were measured: sound duration (ms), number of pulses per sound, initial and mean pulse periods
(ms), and peak frequency of sounds (Hz). Differences in male courtship sounds were found among species. P. ‘zebra
gold’ produced longer sounds with a higher number of pulses than P. callainos, and P. zebra males showed longer ini-
tial and mean pulse periods than the other two species. In P. zebra, male courtship, male agonistic and female ago-
nistic sounds also differed significantly in some parameters. These results suggest that in the studied species acoustic
signals could be used in species-specific recognition and potentially promote reproductive isolation, and in intraspe-
cific communication.
Key words: Acoustic communication, speciation, sound production, Pseudotropheus, Cichlidae.
IZVLEŒEK
Akustiœno vedenje malavijskih ciklidov (Pseudotropheus, Cichlidae): moæna vloga pri prepoznavanju vrst in pri
intraspecifiœni komunikaciji.
Zvoœna komunikacija je verjetno pomembna pri prepoznavanju spolnih partnerjev afriøkih ciklidov in pri evolu-
cijskih procesih, ki so udeleæeni pri njihovi hitri speciaciji. Zvoki, ki jih samci rib oddajajo v zgodnji fazi dvorjenja
(med drgetom) pri treh ozko sorodnih vrstah kompleksa Pseudotropheus zebra (P. zebra, P. calainos in P. 'zebra gold')
so avtorji snemali in primerjali med seboj. Pri eni vrsti (P. zebra) so primerjali tudi glasove, oddane med drgetom, z
glasovi ki jih ribe oddajajo med poznejøimi fazami dvorjenja in sicer med kroæenjem in vodenim plavanjem kot tudi
z oglaøanjem med interakcijami samcev ali samic. Merili so naslednje zvoœne parametre: trajanje zvoka, øtevilo pul-
zov v zvoœnem signalu, trajanje zaœetnega in povpreœnega cikla pulza (ms) in frekvenœni vrh zvoka. Ugotovili so med-
vrstne razlike pri glasovih dvorjenja. P. ‘zebra gold’ je oddajala daljøe zvoœne signale z viøjim øtevilom pulzov od
vrste P. callainos, pri samcih vrste P. zebra pa sta trajanje zaœetnih pulzov in povpreœno trajanje daljøi kot pri drugih
dveh vrstah. Pri slednji vrsti se vsaj v nekaterih parametrih signifikantno razlikujejo glasovi dvorjenja, agonistiœni sig-
nali samcev ter samic. Ti rezultati kaæejo, da pri raziskovanih vrstah zvoœni signali omogoœajo vrstno prepoznavanje
in morda pospeøujejo reproduktivno izolacijo in omogoœajo komunikacijo znotraj vrst.
Kljuœne besede: zvoœna komunikacija, speciacija, produkcija zvoka, Pseudotropheus, Cichlidae.
Addresses – Naslovi
230
Razprave IV. razreda SAZU, XLVII-3 (2006)
Jose Miguel SIMÕES (Corresponding author)
Departamento de Biologia
Animal e Centro de Biologia Ambiental
Faculdade de Ciências da Universidade de Lisboa
Bloco C2 Campo Grande
1749-016 Lisboa
Portugal
E-mail: josemiguelsimoes@gmail.com
Ines DUARTE
Departamento de Biologia
Animal e Centro de Biologia Ambiental
Faculdade de Ciências da Universidade de Lisboa
Bloco C2 Campo Grande
1749-016 Lisboa
Portugal
E-mail: i.duarte@netcabo.pt
Paulo Jorge FONSECA
Departamento de Biologia
Animal e Centro de Biologia Ambiental
Faculdade de Ciências da Universidade de Lisboa
Bloco C2 Campo Grande
1749-016 Lisboa
Portugal
E-mail: pjfonseca@fc.ul.pt
G. F. TURNER
Department of Biological SciencesUniversity of Hull
HU6 7RX
U.K.
M. Clara P. AMORIM (Corresponding author)
Unidade de Investigação em Eco-Etologia
I.S.P.A.
Rua Jardim do Tabaco 34
1149-041 Lisboa
Portugal
E-mail: amorim@ispa.pt
18 IBAC knjiga 10:01:2007 16:58 Page 230
INTRODUCTION
The cichlids from the Great African Lakes represent one of the fastest known case of
adaptive radiation among vertebrates (e.g. LANDE et al. 2001, ALBERTSON et al. 2003). It
is thought that in Lake Malawi alone there are at least 295 endemic species of cichlids and
at least 300 remain undescribed (GENNER & TURNER 2005). Most of these species may
have arisen in the Pleistocene, 700.000 years ago (KNIGHT & TURNER 1999, COULDRIDGE
2002). Sexual selection by females, based on chromatic patterns of males seems to be the
foremost mechanism responsible for the rapid speciation in these cichlids (e.g. DOMINEY
1984, MCKAYE 1991, COULDRIDGE & ALEXANDER 2002, GENNER & TURNER 2005). Visual
cues are very important for inter and intraspecific recognition and can act as a sexual bar-
rier between different species (KNIGHT & TURNER 1999, COULDRIDGE & ALEXANDER
2002). However, other channels of communication can also be important in sexual selec-
tion, such as the acoustic and chemical ones. Males of African cichlids, including
Pseudotropheus spp., are known to produce sounds during courtship (LOBEL 1998,
AMORIM et al. 2003, AMORIM et al. 2004). A preliminary study with three sisters species
(AMORIM et al. 2004), showed the existence of significant differences in some of the para-
meters measured, suggesting that acoustic communication may have an important role in
the reproductive isolation among these animals and consequently on their impressive rate
of speciation.
Three species of the Pseudotropheus complex (Pseudotropheus zebra, P. ‘zebra gold’
and P. callainos) are sympatric, reproductively isolated in nature (VAN OPPEN et al. 1998)
and mate assortatively in the laboratory, indicating that reproductive isolation can be
maintained by direct mate choice alone (KNIGHT et al. 1998). Sounds made during the ini-
tial stages of courtship by males of these species were recorded and compared to check for
differences in the acoustic signals that could potentially be used in species recognition. In
addition, sounds made during late courtship stages and during agonistic interactions
(male-male and female-female) were also registered for P. zebra to study the variability
in the acoustic signals within one species.
METHODS
Trials were conducted in two aquaria (120 x 45 x 60 cm; Lx Wx D) placed on top
of a concrete plate supported by two rock-wool blocks (100 x 40 x 30 cm). This setup
proved to be effective to minimize external noise and building’s vibration, also improving
noise to signal ratio considerably. Tanks were fitted with an external power filter and
maintained at 25-27°C, pH 7-9, with a 12h light/dark cycle. Each aquarium was divided
into three compartments, one of 50 cm, in the middle, and two of 35 cm. Each smaller
compartment had a terracotta pot and held a single male, while females were kept in the
larger compartment. Males were identified by their natural marks, such as eggspots, fin
length and body and fin blots.
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Courtship sounds were recorded between January and September 2005. Sounds were
recorded with two High Tech 94 SSQ hydrophones (sensitivity of -165 dB re 1VmPa-1, flat
frequency response up to 6 kHz±1 dB) and with a Pioneer DVD Recorder DVR-3100.
Before the recording period, both heaters and filters were switched off. One of the opaque
partitions, that separated a male from the females was removed before the start of the
courtship experiments which allowed the subject male free access to the females. Sounds
from females were recorded from female-female interactions that naturally occurred when
they were in the middle compartment isolated from the males. Sounds from male-male
interactions were recorded by placing another male the middle compartment (instead of
the females), and following a similar procedure to the courtship sound recordings. Fights
were stopped before escalation to avoid physical injuries in the males. Recording session
durations were of 10 minutes for female-female, 15 minutes for male-male and 20 minutes
for male-female interactions.
Sounds were analysed with Cool Edit Pro 2.0 and Raven 2.0. Only sounds that
showed a clear structure and were recorded at a distance of 1-2 BL (body length) of the
male were considered. The acoustic parameters analysed were: sound duration (ms), num-
ber of pulses in a sound, initial and mean pulse period (ms) and peak frequency 1 and 2
(Hz) (for a description of the acoustic parameters see AMORIM et al. 2004). These were the
two frequency components with the highest energy in the entire sound. All parameters
were analysed separately using the non-parametic Kruskal-Wallis test.
RESULTS
Sounds emitted by Pseudotropheus were typically pulsed short signals (500 to 800
ms), with most energy below 1 kHz. Most sounds were emitted in the initial stages of
courtship, during quiver, so comparisons among species only considered ‘quiver sounds’.
There were significant differences between species in the following acoustic parameters:
sound duration and number of pulses per sound were higher in P. ‘zebra gold’ and, the ini-
tial and mean pulse periods were longer in P. zebra than in the other two species (Kruskal-
Wallis, P. zebra (N=12), P. ‘zebra gold’ (N=12), P. callainos (N=13), H=6.4-15.6,
P<0.05). Sounds produced by P. zebra males during quiver differed significantly from
sounds of later stages of courtship (lead swim and circle). ‘Quiver sounds’ (Q) were
longer, with higher number of pulses, shorter mean pulse periods and higher peak fre-
quency 1 than circle (C) and lead swim (LS) sounds (Kruskal-Wallis, Q (N=36), C
(N=10), LS (N=12), H=8.5-29.1, P<0.05). Males and females of P. zebra also emitted
sounds during agonistic interactions (male-male and female-female interactions). Male
courtship and agonistic sounds, had longer sound duration and higher number of pulses
per sound than female sounds and both male and female agonistic sounds had shorter ini-
tial and mean pulse periods than male courtship ones. Females produced shorter sounds
and with a lower number of pulses but otherwise very similar to males’ agonistic sounds
(Kruskal-Wallis, M-F (N=48), M-M (N=36), F-F (N=27), H=11.7-17.5, P<0.05).
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DISCUSSION
The three studied sympatric sister Pseudotropheus species emitted low frequency
sounds during different stages of courtship. Male courtship sounds emitted during quiver
showed differences among species in the sound duration, the number of pulses and in the
initial and mean pulse period. In a preliminary study using males of the same
Pseudotropheus species, AMORIM et al. (2004) also reported significant inter-specific dif-
ferences for the number of pulses but only marginally non-significant differences for
sound duration, probably due to the smaller sample size.
In one species, P. zebra, sound emission was also observed in agonistic interactions
and both males and females were able to emit sounds. In this species, sounds differed
between initial and late stages of courtship, and between social contexts (courtship – male-
female interactions, and agonism – female-female and male-male interactions), in sound
duration, number of pulses, pulse period and in peak frequency 1.
The interspecific differences in courtship sounds found in this study suggest that
acoustic communication could potentially promote species isolation and play a role in the
amazingly rapid speciation found in these cichlids. Temporal and pulse grouping patterns
are believed to play a fundamental role in species recognition in fish (e.g. SPANIER 1979).
For example, playback experiments of courtship sounds (chirps) carried out with sym-
patric damselfishes (Stegastes spp.) showed that males could distinguish conspecific from
heterospecific chirps based on the number of pulses and pulse rate (MYRBERG et al. 1978,
SPANIER 1979). In cichlids, LOBEL (1998) showed statistically significant differences in
pulse rates and durations in the courtship sounds of two other sympatric Malawian cich-
lids and proposed that acoustic communication could play a role in mate choice and
species recognition.
Likewise, differences found in P. zebra for the number of pulses, temporal and fre-
quency parameters, for sounds emitted in different contexts (courtship vs. agonistic inte-
ractions) could be used in mate choice. For example, females could be able to extract
information on the motivation and spawning readiness of males, as suggested for other
fishes (e.g. AMORIM et al. 2003).
Evolution questions have driven attention to cichlids of the Great African Lakes lea-
ding to the hypothesis that speciation has been driven by mate choice based on male
colour. The present and other recent studies (PLENDERLEITH et al. 2005) suggest that dif-
ferent channels of communication can be acting together in species isolation, inviting for
future research on the role of different modalities in cichlid mate choice.
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Figure 1: Oscillogram (A) and sonagram (B) of a courtship sound produced by a
Pseudotropheus zebra male. Oscillogram was filtered with a 60 Hz high-pass filter and the
sonogram used a Hamming window and a filter bandwidth of 200 Hz.
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