No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Vocal Behavior During Territorial Intrusions in the Lusitanian Toadfish: Boatwhistles Also Function as Territorial ‘Keep‐Out’ Signals
Abstract
Male signals are frequently studied in a single behavioral context, but in some cases they may assist multiple functions, namely for both male–male competition and female mate choice. Boatwhistles are known as the mate attraction calls of toadfishes typically produced during the breeding season. However, recent observations with the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae) indicate that the emission of boatwhistles is not restricted to this period, which suggests a function in other behavioral contexts such as agonistic territorial interactions. We experimentally manipulated the social context of toadfish males to investigate whether boatwhistles are produced during territorial defense, by introducing ‘intruders’ in an experimental tank containing nesting ‘resident’ males. Furthermore, we examined whether parental care (eggs in the nest) affected the behavioral responses of resident males during territorial defense. Resident males defended their shelters producing sounds, mostly boatwhistles, towards intruders. Parental males revealed higher aggression levels, exhibiting additional threatening and attack behaviors. Boatwhistles registered during agonistic events were compared with the mate advertising boatwhistles recorded from small aggregations of nesting males in a natural breeding intertidal area. Agonistic boatwhistles were produced in lower and variable calling rates comparing with the advertising ones that were typically emitted in long series of calls. Agonistic boatwhistles were similar in duration and frequency harmonic structure (with a middle tonal phase) to the advertising calls, but presented less amplitude modulation, and lower dominant and fundamental frequencies. These acoustic differences were probably related to differences in calling rates and broadcast demands associated to the distance to the intended receiver. We provide first evidence that, apart from attracting mates, the toadfish boatwhistles also function as active ‘keep-out’ signals during territorial defense.
... Individuals can also face trade-offs related to a single behaviour, such as when choosing between different modes of foraging [6]. In many species, individuals use signals in more than one sensory modality to communicate [7][8][9][10][11]. Multimodal components may signal different information [12] but can also provide the same information and thus be used flexibly depending on circumstances [13,14]; the latter represents a within-behaviour trade-off. ...
... For instance, parrotfish (Scaridae) and surgeonfish (Acanthuridae) shift their prioritization of behaviours, such as foraging or predator avoidance, depending on the time of day and the predator type to which they are exposed [21]. In addition, laboratory-housed Lusitanian toadfish (Halobatrachus didactylus) altered their aggressive visual displays and defensive acoustic signals under changing social contexts, demonstrating multimodal flexibility [10]. However, this capacity for individuals to shift between sensory modalities has rarely been documented in wild aquatic systems [19]. ...
... Vocalizations, therefore, offer an effective form of nest-defence signalling under predation risk. Vocal fish often respond acoustically to predators [41] and can use acoustic signals for dual purposes [10]. The multi-pulse knock vocalizations of the Ambon damselfish, which increased in the presence of a conspecific intruder and predator, could potentially deter the predator as well as the conspecific intruder. ...
Animals are expected to respond flexibly to changing circumstances, with multimodal signalling providing potential plasticity in social interactions. While numerous studies have documented context-dependent behavioural trade-offs in terrestrial species, far less work has considered such decision-making in fish, especially in natural conditions. Coral reef ecosystems host 25% of all known marine species, making them hotbeds of competition and predation. We conducted experiments with wild Ambon damselfish (Pomacentrus amboinensis) to investigate context-dependent responses to a conspecific intruder; specifically, how nest defence is influenced by an elevated predation risk. We found that nest-defending male Ambon damselfish responded aggressively to a conspecific intruder, spending less time sheltering and more time interacting, as well as signalling both visually and acoustically. In the presence of a model predator compared to a model herbivore, males spent less time interacting with the intruder, with a tendency towards reduced investment in visual displays compensated for by an increase in acoustic signalling instead. We therefore provide ecologically valid evidence that the context experienced by an individual can affect its behavioural responses and multimodal displays towards conspecific threats.
... Four species are particularly well-studied: the plainfin midshipman (P. notatus) (for example Woods et al., 2022), the oyster toadfish (Opsanus tau) (Fine, 1977), the Lusitanian toadfish (Halobatrachus didactylus) (Vasconcelos et al., 2010), and the bocon toadfish (Amphyichtys cryptocentrus) and gulf toadfish (O. beta) (Salas et al., 2018;Staaterman et al., 2018). ...
... Breeding males of this family migrate to the intertidal area and nest or burrow under rocks, boards, pipework, and rocky outcrops (McIver et al., 2014;Salas et al., 2018). Artificial nests can be easily created in the laboratory or the field using concrete tiles or roof tiles (Amorim et al., 2015;Vasconcelos et al., 2010;Woods et al., 2022). Focal males are sedentary and thus easy to identify (Salas et al., 2018). ...
... Once inside the nest, the male produces two types of sounds: the grunt/growl in agonistic interactions, and the boatwhistle/hum during courtship (Brantley and Bass, 1994;Bass and McKibben, 2003;Maruska and Mensinger, 2009;Salas et al., 2018), depending on the species. For example, the most frequent sounds of the Lusitanian toadfish are the boatwhistle and grunt trains (Vasconcelos et al., 2010) with calling rate and effort related to the condition of the sonic muscles . The three-spined toadfish (Batrachomoeus trispinosus) produces acoustic beats and other non-linear vocalizations, thought to be produced via a highly specialized sonic muscle/swimbladder structure (Rice and Bass, 2009;Rice et al., 2011). ...
Substrate-borne communication via mechanical waves is widespread throughout the animal kingdom but has not been intensively studied in fishes. Families such as the salmonids and sculpins have been documented to produce vibratory signals. However, it is likely that fish taxa on or close to the substrate that produce acoustic signals will also have a vibratory component to their signal due to their proximity to substrates and energy transfer between media. Fishes present an intriguing opportunity to study vibrational communication, particularly in the context of signal production and detection, detection range, and how vibratory signals may complement or replace acoustic signals. It is highly likely that the vibrational landscape, the vibroscape, is an important component of their sensory world, which certainly includes and overlaps with the soundscape. With the wide range of anthropogenic activities modifying underwater substrates, vibrational noise presents similar risks as acoustic noise pollution for fishes that depend on vibrational communication. However, in order to understand vibrational noise, more empirical studies are required to investigate the role of vibrations in the fish environment.
... The Lusitanian toadfish, H. didactylus, is a gregarious vocal species with an unusually rich repertoire for a fish (Amorim et al., 2008) that relies on acoustic communication for mate finding and attraction (Vasconcelos et al., 2012) and for the spacing out of territorial males (Vasconcelos et al., 2010;Conti et al., 2015). The more commonly produced soundthe boatwhistle (BW)is used both to attract females and repel possible intruders (Vasconcelos et al., 2010(Vasconcelos et al., , 2012Conti et al., 2015). ...
... The Lusitanian toadfish, H. didactylus, is a gregarious vocal species with an unusually rich repertoire for a fish (Amorim et al., 2008) that relies on acoustic communication for mate finding and attraction (Vasconcelos et al., 2012) and for the spacing out of territorial males (Vasconcelos et al., 2010;Conti et al., 2015). The more commonly produced soundthe boatwhistle (BW)is used both to attract females and repel possible intruders (Vasconcelos et al., 2010(Vasconcelos et al., , 2012Conti et al., 2015). A reduction in BW active space will likely affect mate detection distance and vocal interactions amongst neighbouring territorial males, with implications for fitness. ...
... Our results indicate that boat noise lowers communication distance, interferes with male-male vocal interactions and provokes a significant decrease in the males' calling rate during boat noise playback. In this species, females are attracted to the breeding sites and to the nests by advertisement BWs (Amorim and Vasconcelos, 2008) and this vocalization is also used as a territorial 'keep-out' signal (Vasconcelos et al., 2010). The BW pulse period, amplitude modulation and calling rate are correlated with male quality (Amorim et al., 2010b) and these acoustic signals have potential for individual recognition (Amorim and Vasconcelos, 2008;Vieira et al., 2015). ...
... The Lusitanian toadfish, H. didactylus, is a gregarious vocal species with an unusually rich repertoire for a fish (Amorim et al., 2008) that relies on acoustic communication for mate finding and attraction (Vasconcelos et al., 2012) and for the spacing out of territorial males (Vasconcelos et al., 2010;Conti et al., 2015). The more commonly produced soundthe boatwhistle (BW)is used both to attract females and repel possible intruders (Vasconcelos et al., 2010(Vasconcelos et al., , 2012Conti et al., 2015). ...
... The Lusitanian toadfish, H. didactylus, is a gregarious vocal species with an unusually rich repertoire for a fish (Amorim et al., 2008) that relies on acoustic communication for mate finding and attraction (Vasconcelos et al., 2012) and for the spacing out of territorial males (Vasconcelos et al., 2010;Conti et al., 2015). The more commonly produced soundthe boatwhistle (BW)is used both to attract females and repel possible intruders (Vasconcelos et al., 2010(Vasconcelos et al., , 2012Conti et al., 2015). A reduction in BW active space will likely affect mate detection distance and vocal interactions amongst neighbouring territorial males, with implications for fitness. ...
... Our results indicate that boat noise lowers communication distance, interferes with male-male vocal interactions and provokes a significant decrease in the males' calling rate during boat noise playback. In this species, females are attracted to the breeding sites and to the nests by advertisement BWs (Amorim and Vasconcelos, 2008) and this vocalization is also used as a territorial 'keep-out' signal (Vasconcelos et al., 2010). The BW pulse period, amplitude modulation and calling rate are correlated with male quality (Amorim et al., 2010b) and these acoustic signals have potential for individual recognition (Amorim and Vasconcelos, 2008;Vieira et al., 2015). ...
Anthropogenic noise is considered a major underwater pollutant as increasing ocean background noise due to human activities is impacting aquatic organisms. One of the most prevalent anthropogenic sounds is boat noise. Although motorboat traffic has increased in the past few decades, its impact on the communication of fish is still poorly known. The highly vocal Lusitanian toadfish (Halobatrachus didactylus) is an excellent model to test the impact of this anthropogenic stressor as it relies on acoustic communication to attract mates. Here, we performed two experiments to test the impact of boat noise on the acoustic communication of the Lusitanian toadfish. Using the auditory evoked potential (AEP) technique, we first compared the maximum distance a fish can perceive a boatwhistle (BW), the mate attraction acoustic signal, before and after embedding it in boat noise. Noises from a small motorboat and from a ferryboat reduced the active space from a control value of 6.4–10.4 m to 1.7–2.5 m and 6.3–6.7 m, respectively. In the second experiment we monitored the acoustic behaviour of breeding males exposed to boat noise playbacks and we observed an increase in the inter-onset interval of BWs and a disruption of the usual vocal interactions between singing males. These results demonstrate that boat noise can severely reduce the acoustic active space and affect the chorusing behaviour in this species, which may have consequences in breeding success for individuals and could thus affect fitness.
... The Lusitanian toadfish, Halobatrachus didactylus, is a benthic species with an unusually rich vocal repertoire that produces sounds in both reproductive and agonistic contexts (dos Santos et al., 2000;Vasconcelos et al., 2010). However, the boatwhistle (BW) dominates its vocal activity (Amorim et al., 2006(Amorim et al., , 2010b and is produced in both contexts (Vasconcelos et al., 2010). ...
... The Lusitanian toadfish, Halobatrachus didactylus, is a benthic species with an unusually rich vocal repertoire that produces sounds in both reproductive and agonistic contexts (dos Santos et al., 2000;Vasconcelos et al., 2010). However, the boatwhistle (BW) dominates its vocal activity (Amorim et al., 2006(Amorim et al., , 2010b and is produced in both contexts (Vasconcelos et al., 2010). Like other Batrachoididae species, Lusitanian toadfish territorial males usually nest under rocks and vocalize to attract mates Vasconcelos et al., 2012). ...
... 60 Hz., with the dominant frequency usually being the second or fourth harmonic (Amorim et al., 2006). The fundamental frequency of the boatwhistle can also be the one with most energy as reported by Vasconcelos et al. (2010) for agonistic interactions. ...
Males of several fish species aggregate and vocalize together, increasing the detection range of the sounds and their chances of mating. In the Lusitanian toadfish (Halobatrachus didactylus), breeding males build nests under rocks in close proximity and produce hundreds of boatwhistles (BW) an hour to attract females to lay their demersal eggs on their nest. Chorusing behaviour includes fine-scale interactions between individuals, a behavioural dynamic worth investigating in this highly vocal fish. Here we present a study to further investigate this species' vocal temporal patterns on a fine (individual rhythms and male-male interactions) and large (chorus daily patterns) scales. Several datasets recorded in the Tagus estuary were labelled with the support of an automatic recognition system based on hidden Markov models. Fine-scale vocal temporal patterns exhibit high variability between and within individuals, varying from an almost isochronous to an apparent aperiodic pattern. When in a chorus, males exhibited alternation or synchrony calling patterns, possibly depending on motivation and social context (mating or male-male competition). When engaged in sustained calling, males usually alternated vocalizations with their close neighbours thus avoiding superposition of calls. Synchrony was observed mostly in fish with lower mean calling rate. Interaction patterns were less obvious in more distanced males. Daily choruses showed periods with several active calling males and periods of low activity with no significant diel patterns in shallower intertidal waters. Here, chorusing activity was mainly affected by tide level. In contrast, at a deeper location, tide level did not significantly influence calling and there was a higher calling rate at night. These data show that photoperiod and tide levels can influence broad patterns of Lusitanian toadfish calling activity as in other shallow-water fishes, but fine temporal patterns in acoustic interactions among nesting males is more complex than previously known for fishes.
... The Lusitanian toadfish Halobatrachus didactylus (Bloch and Schneider 1801) is a member of the family Batrachoididae that inhabits coastal waters and estuaries (Roux, 1986). It is a benthic species with an unusually rich vocal repertoire (Amorim et al., 2008) that produces sounds in both reproductive and agonistic contexts (dos Santos et al., 2000;Vasconcelos et al., 2010). During the breeding season, males aggregate in nesting areas close to the substrate and produce advertisement callsthe boatwhistle (BW)to attract mates (Jordão et al., 2012;Vasconcelos et al., 2012). ...
... Halobatrachus didactylus has been used in both behavioural (e.g. Vasconcelos et al., 2010;Ramos et al., 2012;Conti et al., 2015) and physiological (e.g. Vasconcelos and Ladich, 2008;Vasconcelos et al., 2011a,b) studies, making it an excellent model species for the assessment of active space of acoustic signals in fish. ...
... We only considered data with coherence values above 0.9. Hence, we selected 120, 240 and 540 Hz as these are multiples of 60 Hz, a common fundamental frequency in this species (Vasconcelos et al., 2010). Notice that we excluded 120 Hz at 2 m depth and 16 m distance, and 540 Hz at 5 m depth and 16 m distance because they did not meet the coherence value criterion. ...
The active space of a signal is an important concept in acoustic communication as it has implications on the function and evolution of acoustic signals. However, it remains mostly unknown for fish since it has been measured in only a restricted number of species. We combined physiological and sound propagation approaches to estimate the communication range of the Lusitanian toadfish's (Halobatrachus didactylus) advertisement sound, the boatwhistle (BW). We recorded BWs at different distances from vocalizing fish in a natural nesting site at circa 2-3 m depth. We measured the representation of these increasingly attenuated BWs in the auditory pathway through the auditory evoked potentials technique (AEP). These measurements point to a communication range ranging between 6 to 13 m, depending on the spectral characteristics of the BW. A similar communication range (circa 8 m) was derived from comparing sound attenuation at selected frequencies with auditory sensitivity. This is one of the few studies that combines auditory measurements with sound propagation to estimate the active space of acoustic signals in fish. We emphasize the need for studies to consider that active space estimates should take informational masking into account.
... This marine teleost relies on acoustic communication to mediate social interactions early in development. The Lusitanian toadfish exhibits an unusually large vocal repertoire that consists of about five different vocalisations used in various social contexts, including long tonal sounds (Amorim et al., 2008;Vasconcelos et al., 2010). Vasconcelos and Ladich (2008) using the auditory evoked potential (AEP) recording technique showed that the Lusitanian toadfish exhibits an ontogenetic increase in auditory sensitivity at the lowest (100 Hz) and highest tested frequencies (800-1000 Hz). ...
... Behavioural observations of fry and juveniles suggested that the different vocalisations are produced during specific social contexts. Single grunts and grunt trains were typically emitted during agonistic interactions while competing for either food or territory, as observed by Vasconcelos and Ladich (2008) and Vasconcelos et al. (2010). Long grunt trains and double-croaks, which had so far been recorded only in adults in semi-natural conditions (Amorim et al., 2008), were also produced by juveniles inside their shelters but without any obvious social interaction or visual display, possibly to signal shelter occupancy. ...
... Finally, one of the most surprising results was that large juveniles of Lusitanian toadfish were capable of producing long harmonic boatwhistles. This signal was produced while the resident was facing an intruder, similar to agonistic boatwhistles previously recorded in territorial male adults (Vasconcelos et al., 2010). Such findings strongly suggest that similar to P. notatus (Knapp et al., 1999), the CPG must be fully developed at this developmental stage long before sexual maturity, which occurs around 30-35 cm total length for all morphotypes in this species (Pereira et al., 2011). ...
Vocal differentiation is widely documented in birds and mammals but has been poorly investigated in other vertebrates, including fish, which represent the oldest extant vertebrate group. Neural circuitry controlling vocal behaviour is thought to have evolved from conserved brain areas that originated in fish, making this taxon key to understanding the evolution and development of the vertebrate vocal-auditory systems. This study examines ontogenetic changes in the vocal repertoire and whether vocal differentiation parallels auditory development in the Lusitanian toadfish Halobatrachus didactylus (Batrachoididae). This species exhibits a complex acoustic repertoire and is vocally active during early development. Vocalisations were recorded during social interactions for four size groups (fry: <2 cm; small juveniles: 2-4 cm; large juveniles: 5-7 cm; adults >25 cm, standard length). Auditory sensitivity of juveniles and adults was determined based on evoked potentials recorded from the inner ear saccule in response to pure tones of 75-945 Hz. We show an ontogenetic increment in the vocal repertoire from simple broadband-pulsed 'grunts' that later differentiate into four distinct vocalisations, including low-frequency amplitude-modulated 'boatwhistles'. Whereas fry emitted mostly single grunts, large juveniles exhibited vocalisations similar to the adult vocal repertoire. Saccular sensitivity revealed a three-fold enhancement at most frequencies tested from small to large juveniles; however, large juveniles were similar in sensitivity to adults. We provide the first clear evidence of ontogenetic vocal differentiation in fish, as previously described for higher vertebrates. Our results suggest a parallel development between the vocal motor pathway and the peripheral auditory system for acoustic social communication in fish.
... Fishes from the Batrachoididae family have become a key neuroethological model for studying acoustic communication in vertebrates because mate attraction and territorial defence in theses fishes rely heavily on acoustic signalling [15][16][17]. While mating advertisement calls (boatwhistles and hums) produced by batrachoidid nest-holders have been also implied in signalling territorial ownership and in spacing out individuals [9,16,18], grunts are considered the main agonistic call [8,15]. ...
... Fishes from the Batrachoididae family have become a key neuroethological model for studying acoustic communication in vertebrates because mate attraction and territorial defence in theses fishes rely heavily on acoustic signalling [15][16][17]. While mating advertisement calls (boatwhistles and hums) produced by batrachoidid nest-holders have been also implied in signalling territorial ownership and in spacing out individuals [9,16,18], grunts are considered the main agonistic call [8,15]. Within this family, Lusitanian toadfish (Halobatrachus didactylus) males mainly defend their nests with agonistic boatwhistles (BW) that are similar to mating advertisement BW except for presenting lower dominant frequencies and weaker amplitude modulation [16]. ...
... While mating advertisement calls (boatwhistles and hums) produced by batrachoidid nest-holders have been also implied in signalling territorial ownership and in spacing out individuals [9,16,18], grunts are considered the main agonistic call [8,15]. Within this family, Lusitanian toadfish (Halobatrachus didactylus) males mainly defend their nests with agonistic boatwhistles (BW) that are similar to mating advertisement BW except for presenting lower dominant frequencies and weaker amplitude modulation [16]. As BW have shown to be rather complex signals [8] they render the opportunity to assess the salience of relevant sound features for territorial defence in teleosts. ...
... Females deposit their eggs under the roof of the nest and males guard the eggs of multiple females until the offspring is able to swim away Roux, 1986). During this period competition for nests is high (Amorim et al., 2010b) and males actively defend the nest from intruders with visual and acoustic behaviour (Vasconcelos et al., 2010;Ramos et al., 2012). Recently, Vasconcelos and colleagues (Vasconcelos et al., 2010) have proposed that the boatwhistle functions as a 'keep-out' signal and suggested that vocalising may be an effective means to avoid territorial intrusions and escalated levels of fighting in the Lusitanian toadfish. ...
... During this period competition for nests is high (Amorim et al., 2010b) and males actively defend the nest from intruders with visual and acoustic behaviour (Vasconcelos et al., 2010;Ramos et al., 2012). Recently, Vasconcelos and colleagues (Vasconcelos et al., 2010) have proposed that the boatwhistle functions as a 'keep-out' signal and suggested that vocalising may be an effective means to avoid territorial intrusions and escalated levels of fighting in the Lusitanian toadfish. However, the study of Vasconcelos et al. (2010) cannot exclude the possibility that chemical or other cues could also be at play. ...
... Recently, Vasconcelos and colleagues (Vasconcelos et al., 2010) have proposed that the boatwhistle functions as a 'keep-out' signal and suggested that vocalising may be an effective means to avoid territorial intrusions and escalated levels of fighting in the Lusitanian toadfish. However, the study of Vasconcelos et al. (2010) cannot exclude the possibility that chemical or other cues could also be at play. In the Lusitanian toadfish, vocalisations are generated by vibration of the swimbladder caused by the contraction of intrinsic sonic muscles (dos Santos et al., 2000); muting can therefore be easily achieved by making a cut and deflating the swimbladder under anaesthesia. ...
The function of fish sounds in territorial defence, in particular its influence on the intruder's behaviour during territorial invasions, is poorly known. Breeding Lusitanian toadfish males (Halobatrachus didactylus) use sounds (boatwhistles) to defend nests from intruders. Results from a previous study suggest that boatwhistles function as a 'keep-out signal' during territorial defence. To test this hypothesis we performed territorial intrusion experiments with muted Lusitanian toadfish. Subject males were assigned to three groups: muted, sham and unmanipulated. Males were muted by making a cut and deflating the swimbladder (the sound producing apparatus) under anaesthesia. Sham males suffered the same surgical procedure except the swimbladder cut and deflation. Toadfish nest-holder males reacted to intruders mainly by emitting sounds (sham and unmanipulated) and less frequently with escalated fights. When the nest-holder produced a boatwhistle, the intruder fled more frequently than expected by chance alone. Muted males experienced a higher number of intrusions than the remaining groups probably due to their inability to vocalise. Together, our results show that fish acoustic signals are effective deterrents in nest/territorial intrusions, similar to bird song.
... Boatwhistle characteristics were consistent with previous descriptions (e.g. Vasconcelos et al., 2010) and showed a large between-individual variation (Table2). ...
... Consequently, females benefit from choosing good fathers, and more so if they are single spawners such as batrachoidids (Brantley and Bass, 1994;Modesto and Canário, 2003a). Parental care in the Lusitanian toadfish is costly because type I males experience reduced feeding, fan the eggs and defend their nest vigorously for at least 30 days (till the fry becomes free swimming) (Modesto and Canário, 2003a;Vasconcelos et al., 2010), consistent with the marked decrease in the male's condition (hepatossomatic index and the Fulton's condition factor, K) during the spawning season (Modesto and Canário, 2003a). Our results suggest that Lusitanian toadfish females should favour males that call at a higher rate and for prolonged periods, as they would be in better condition and could provide better parental care. ...
... Amplitude modulation is an important characteristic to distinguish boatwhistle emitted by nesting males in different motivational contexts. Vasconcelos et al. (Vasconcelos et al., 2010) have shown that the Lusitanian toadfish also emits boatwhistles during territorial intrusions by other males but these lack amplitude modulation, which seems characteristic of a mating context. Consequently, it is possible that males can also advertise their quality and motivation by increasing the amplitude modulation of the mating boatwhistle, although this suggestion needs to be tested. ...
... Phylogenetic analysis indicated that Lusitanian toadfish represents a basal lineage in the Batrachoididae, providing an excellent model for understanding integrated mechanisms underlying the evolution of acoustic communication in fishes (Rice and Bass 2009). Moreover, the Lusitanian toadfish is highly tolerant to experimental manipulations, displays the full acoustic repertoire, and mates in seminatural situations Vasconcelos et al. 2010). ...
... Besides boatwhistles, Lusitanian toadfish also produces other pulsed sounds, such as grunt trains, long grunt trains, croaks, double croaks, and associations between some of these calls . Some of these sounds are known to be used during agonistic interactions, such as territorial defense (e.g., grunt train, Vasconcelos and Ladich 2008;Vasconcelos et al. 2010), but the function of such vocal plasticity remains unclear. Females deposit the eggs on the roof of the nest, which are guarded by the male until the offspring are free swimming (dos Santos et al. 2000). ...
... Nests were surrounded with a plastic net to prevent vocal type I males from escaping and to ensure individual identity throughout the recordings (see Vasconcelos et al. 2010; Figure 1). A small opening (10 cm wide, 5 cm high) was created at the entrance of each of these nests to allow females and, eventually, small type I or type II males to enter. ...
The relation between acoustic signaling and reproductive success is important to understand the evolution of vocal communi-cation systems and has been well studied in several taxa but never clearly shown in fish. This study aims to investigate whether vocal behavior affects the reproductive success in the Lusitanian toadfish (Halobatrachus didactylus) that relies on acoustic communication to attract mates. We recorded 56 nest-holding (type I) males during the breeding season and analyzed the calling performance and acoustic features of the mate advertising sounds (boatwhistles) exhibited over circa 2 weeks. Hormonal levels of the subjects and the number of eggs (reproductive success) present in the respective nests were quantified. Nesting males attracted both females and other males, namely smaller type I males with significantly lower total length (TL), body condition, sonic muscle mass, gonad mass, and accessory glands mass. Calling rate (CR), calling effort (CE) (% time spent calling), and sound dominant frequency were significantly higher in nesting males with clutches than in those without clutches. Sex steroids (11-ketotestosterone and testosterone) were not correlated with vocal parameters or number of eggs. Maximum CR and CE were the best predictors of the number of eggs. In addition, these vocal variables were best explained by male's TL, condition, and sonic muscle mass. We provide first evidence that vocal behavior significantly determines reproductive success in a vocal fish and show that acoustic signaling at higher and constant rates can operate as an indicator of the male's size and body condition and probably of elevated motivation for reproduction. Key words: acoustic communication, Batrachoididae, mate attraction, reproductive success, toadfish. [Behav Ecol 23:375–383 (2012)] INTRODUCTION
... During this period (c. 30 days), the competition for shelters in shallow waters increases and shelter owner substitutions occur, including in nests with eggs (Vasconcelos et al., 2010). Nest-holding males defend their nests with the emission of agonistic boatwhistles, frequently resulting in the expulsion of the intruder, or with chases and bites when fights escalate (Vasconcelos et al., 2010). ...
... 30 days), the competition for shelters in shallow waters increases and shelter owner substitutions occur, including in nests with eggs (Vasconcelos et al., 2010). Nest-holding males defend their nests with the emission of agonistic boatwhistles, frequently resulting in the expulsion of the intruder, or with chases and bites when fights escalate (Vasconcelos et al., 2010). ...
... We used an experimental procedure similar to that conducted by Vasconcelos et al. (2010). Concrete nests (internal dimensions: 50 cm long, 30 cm wide and 20 cm height) with a hemicylinder shape capped at one end were placed in the Tagus River estuary (Military Air Force Base 6, Montijo, Portugal; 38°42′ N; 8°58′ W). ...
In many fish species in which males guard nests with their eggs, parental care directed to genetically unrelated offspring may arise for example from nest takeovers or cuckoldry. Lusitanian toadfish (Halobatrachus didactylus) has exclusive male parental care and face intensive nest competition during the breeding season that may lead to care of foster eggs. Males of this species use visual displays and sounds when defending their nests frequently resulting in expulsion of the intruder without escalated confrontation. In this study we intended to investigate the existence of alloparental care in Lusitanian toadfish, a behavior whose adaptive significance is still poorly understood. Fish were randomly assigned to three different treatments: parental males in nests with their eggs, parental males with foster eggs and parental males without eggs. Nests with eggs with no nest holder or with females were used as controls. We performed three territorial intrusions over periods of 15 days and observed the acoustic and visual behaviors of residents and intruders. Egg survival was tallied from nests' photographs in all groups. Circulating steroid levels were measured in the three test groups and in another set of non-manipulated males. There were no differences in acoustic and visual territorial defense behaviors among treatments. Egg survival was similar between males (parental and alloparental) and significantly higher than in nests with no nest-tender. Females presented intermediate egg survival. All groups presented similar levels of testosterone and alloparental males showed higher 11-ketotestosterone levels but within the range of levels observed in non-manipulated males. Cortisol levels were similar in all male groups suggesting that experiments did not increase fish stress. The present results suggest the existence of alloparental care in this species.
... For example, Pollymirus isidori, the Elephant Fish, has vocalizations for distinct functions; Grunts, Moans, and Growls are associated with courtship, but Hoots and Pops are associated with territory defense, all with varying intensity depending on the male-male or male-female interaction (Crawford et al. 1986). Additionally, in Hypoplectrus unicolor (Butter Hamlet) sounds are produced just prior to or simultaneously with gamete release, which may facilitate synchronous gamete release (Lobel 1992), while in Padogobius martensii (Common Goby) and Knipowitschia punctatissima (Panzarolo Goby) spawning vocalizations have been shown to be modified before and during oviposition (Lugli et al. 1995).In Lusitanian Toadfish (Halobatrachus didactylus) call rate and effort strongly represented male size and condition (Amorim et al. 2010). ...
... In the field, both RH2 and Pulse trains were not evenly distributed across the diel cycle, despite a general increase in density. This random pattern could be explained by the fact that RH2 can be accompanied by Pulse trains making it a call with more than one purpose (e.g., territory defense and/or courtship display), as has been shown to be the case for 'boatwhistles' of the Lusitanian Toadfish (Vasconcelos et al. 2010) and for the spawning vocalizations of Common Goby (Lugli et al. 1995). In the case of the Pulse train, a random pattern could result when fish produce quieter sounds as they move through the territories to set up at the aggregation site prior to spawning (Shapiro et al. 1993b, Nemeth et al. 2007). ...
Passive acoustic monitoring provides a method for studying grouper courtship associated sounds (CAS). For Red Hind (Epinephelus guttatus), this approach has documented spatio—temporal patterns in their spawning aggregations. This study described vocalizations produced by E. guttatus and their respective behavioral contexts in field and laboratory studies. Five sound types were identified, which included 4 calls recorded in captivity and one sound recorded in the wild, labeled as Chorus. Additionally, the Grunt call type recorded was presumed to be produced by a female. Call types consisted of variations and combinations of low frequency (50—450 Hz) pulses, grunts and tonal sounds in different combinations. Common call types exhibited diel and lunar oscillations during the spawning season, with both field and captive recordings peaking daily at 1800 AST and at 8 days after the full moon.
... Apart from the muted, two intact males did not produce advertisement BW. One was silent and the other made a total of 5 BW with a Max CR of 3 BW, likely being agonistic [48]. All sham-muted and sham males vocalized. ...
... Also, it could have been caused by an erroneous attribution of vocal activity to subject males in the open-nest experiment. As competition for nests is high in this breeding area [2,11], nest takeovers may occur [48] leading to the possibility of attributing the vocal behaviour of a succession of males to the last nest-holder. In addition, it is also likely that females are attracted by high calling rates but assess other male attributes while in the nest. ...
... For example, the calling rate of oyster toadfish males increases when females approach the male's nest (Fish 1972). On the other hand, Lusitanian toadfish males defend their nests from other male intruders with single to short sequences of boatwhistles, contrasting with the long sequences of advertising boatwhistles emitted to attract females (Vasconcelos et al. 2010). ...
... However, how different anthropogenic noise sources present in nowadays aquatic environments affect fish behaviour, including social and mating activities, and its evolutionary consequences, is still poorly investigated and far from understood. Some studies suggest that in addition to the impact of noise on female detection of mates, masked hearing may also increase escalated aggressiveness as acoustic assessment is impaired (Vasconcelos et al. 2007(Vasconcelos et al. , 2010. ...
Fish acoustic signals associated with mating behaviour are typically low-frequency sounds produced by males when in close proximity to females. However, some species make sounds that serve the function and follow the design of advertisement calls, well known in insects, anurans, and birds. Close-range courtship acoustic signals may be used by females in mate assessment as they contain information of male quality such as size and condition. For example, sound-dominant frequency, amplitude, and fatigue resistance may signal body size whereas pulse period (i.e. muscle contraction rate) and calling activity are related with body condition in some species. Some signal features, such as sound pulse number, may carry multiple messages including size and condition. Playback experiments on mate choice of a restricted number of species suggest that females prefer vocal to silent males and may use sound frequency, amplitude, and mainly calling rate
when assessing males. The assessment of males by females becomes more challenging when males engage in choruses or when sounds are otherwise masked by anthropogenic noise but almost nothing is known about how these aspects affect mating decisions and fish reproductive success.
... Differences in the number of nest openings or of nest shape did not seem to exert an influence in nest occupation. A nest with two openings allow the entrance of intruders from both sides but territorial intrusion experiments carried out in seminatural conditions with either tiles (nest 1) or nests 2-5 did not put into evidence any difference in the likelihood of nest intrusions from conspecifics Vasconcelos et al., 2010). The wider section at the closedend of nests 3 and 5 was also unlikely to have affected nest defence and egg fanning costs as the nest opening and most of the nest internal space remained similar to nests 2 and 4. A logistic regression further showed that nest size did not influence the probability of nest occupation suggesting that males choose their nests independent of nest-size availability. ...
... Although appropriate egg-laying substrate can be limiting for male reproductive success (DeMartini, 1988), the accrued cost of offspring care, such as egg fanning and defence from egg predators, and the increased risk of a nest take-over by a larger/good condition male, have to be traded-off with possible fitness gains granted by a larger breeding territory (Björk and Kvarnemo, 2012;Candolin and Voigt, 2001). Indeed nest take-overs are frequent in the Lusitanian toadfish Vasconcelos et al., 2010) and could impose a too large toll on occupying an inadequate nest size. Larger nests have a larger volume of water to set in motion in order to oxygenate the eggs, which means increased energy costs (Björk and Kvarnemo, 2012;Kvarnemo, 1995). ...
Male reproductive success often depends on male attributes and resource quality. Here, we examined male preference for nest size in the Lusitanian toadfish, a nest-guarding fish with parental care. We also investigated the combined effect of male length and nest size in male breeding success. Approximately 80 shelters with five different sizes were placed on an intertidal zone of the Tagus estuary. Nests were checked every fortnight at spring low tides for occupation, nest-holder length, and number of eggs. Males did not select for the larger nests despite their availability but showed size assortative nest choice. Only nest size was a significant predictor of clutch size in occupied nests and it explained 60% of the variability in the number of obtained eggs. Male length and the interaction of male length and nest size did not have a significant effect on male reproductive success. These results suggest that although nest size is key to male's reproductive success, the choice for nest size results from a trade-off between accrued costs of offspring care or risk of a nest take-over and possible benefits of increased fitness.
... Sounds produced by fishes during territorial defence usually function as a complement to visual behaviour such as colour alterations or aggressive visual displays, including fin erection or quivering (Ladich & Myrberg 2006). Though sound seems to play an important role in fish communication there is little experimental evidence demonstrating the function of acoustic signals in fish territorial defence (Ladich & Myrberg 2006; Vasconcelos et al. 2010). Experiments with muted specimens and with sound playback suggest that in an agonistic context acoustic signals can reveal valuable information about the sender and may help avoid overt confrontation and thus energy depletion or even injury and death (Valinsky & Rigley 1981; Riggio 1981; Ladich et al. 1992; Ladich 1998; Raffinger & Ladich 2009; Bertucci et al. 2010; for a review see Ladich & Myrberg 2006). ...
... Valinsky & Rigley (1981) muted juveniles of skunk loaches Yasuhikotakia horae and showed that muted individuals had fewer chances to chase intruders from their shelters. Consistent with our results, Ladich & Myrberg (2006) and Vasconcelos et al. (2010) suggest that fish agonistic sounds can act as a 'keep-out' signal towards intruders. For example, nest-holding Lusitanian toadfish (Halobatrachus didactylus) males defend their territories with loud sounds (boatwhistles), which often elicits fleeing behaviour from the intruder, thus decreasing the chances of escalated fights and nest takeovers (Vasconcelos et al. 2010). ...
Animals often vocalize during territorial challenges as acoustic signals may indicate motivation and fighting ability and contribute to reduce aggressive escalation. Here, we tested the function of agonistic sounds in territorial defence in the painted goby. Pomatoschistus pictus, a small vocal marine fish that defends nests during the breeding season. We first measured the number of times a male approached, avoided, explored, entered and exited two unattended nests associated with either conspecific agonistic sounds or a control: silence or white noise. Acoustic stimuli were played back when the male approached a nest. In a second experimental set, we added visual stimuli, consisting of a conspecific male in a small confinement aquarium near each nest. Even though we found no effect of the visual stimuli, the sound playbacks induced similar effects in both experimental conditions. In the sound vs. silence treatment, we found that when males approached a nest, the playback of conspecific sounds usually triggered avoidance. However, this behaviour did not last as in longer periods males visited nests associated with agonistic sounds more often than silent ones. When the control was white noise, we found no significant effect of the playback treatment in male behaviour. Although we cannot exclude the possibility that other sounds may dissuade nest occupation, our results suggest that agonistic sounds act as territorial intrusion deterrents but are insufficient to prevent nest intrusion on their own. Further studies are needed to test the significance of sound production rate, spectral content and temporal patterns to deter territorial intrusion in fish.
... The BW, the most frequent sound of this species, is a highly stereotyped low-frequency signal that is mostly used as an advertisement call but can also be used in agonistic situations (Amorim and Vasconcelos 2008;Vasconcelos et al. 2010). This sound type presents significant differences between males that allow to distinguish different singing males based on the features of their sounds. ...
... It is benthic, solitary, and relatively sedentary, being more active from dusk to dawn (Pereira et al., 2021). During the reproductive season (May-July in the Iberian Peninsula), large territorial males (type I) nest under rocks or other hard substrates and produce long advertisement calls (boat whistles) to attract ripe females, and agonistic boat whistles to defend their nest from conspecific nest intruders through the contraction of paired sonic muscles attached to the swim bladder (Modesto & Canário, 2003a;Vasconcelos et al., 2010Vasconcelos et al., , 2011. This sophisticated sound repertoire, which includes individual rhythms and distinct chorus patterns (Vieira et al., 2021), is essential for breeding success and is used as an indicator of male condition (Vasconcelos et al., 2012). ...
The current study investigated the structure and function of the olfactory system of the Lusitanian toadfish, Halobatrachus didactylus, using histology and electrophysiology (electro‐olfactogram [EOG]), respectively. The olfactory system consists of a digitated anterior peduncle, of unknown function, containing the inhalant nostril. This then leads to a U‐shaped olfactory chamber with the olfactory epithelium—identified by Gαolf‐immunoreactivity—on the ventral surface. A large lacrimal sac is connected to this tube and is likely involved in generating water movement through the olfactory chamber (this species is largely sedentary). The exhalent nostril lies by the eye and is preceded by a bicuspid valve to ensure one‐way flow of water. As do other teleosts, H. didactylus had olfactory sensitivity to amino acids and bile acids. Large‐amplitude EOG responses were evoked by fluid from the anterior and posterior testicular accessory glands, and bile and intestinal fluids. Anterior gland and intestinal fluids from reproductive males were significantly more potent than those from non‐reproductive males. Male urine and skin mucus proved to be the least potent body fluids tested. These results suggest that chemical communication—as well as acoustic communication—may be important in the reproduction of this species and that this may be mediated by the accessory glands and intestinal fluid.
... The BW, the most frequent sound of this species, is a highly stereotyped low-frequency signal that is mostly used as an advertisement call but can also be used in agonistic situations (Amorim and Vasconcelos 2008;Vasconcelos et al. 2010). This sound type presents significant differences between males that allow to distinguish different singing males based on the features of their sounds. ...
Most marine soundscapes have changed due to the massive presence of anthropogenic noise. Lusitanian toadfish (Halobatrachus didactylus) is a vocal fish species that has been recurrently used as a model in both behavioral and physiological studies, making it an excellent species also to understand the effects of aquatic noise. This chapter aims to review what is known about the effects of boat noise on this species and its possible implications. Vocal behavior, hearing, reproduction, and early stages development of the Lusitanian toadfish are summarized, including several studies that observed effects of boat noise on this species in these different topics. Boat noise can disrupt and decrease calling activity, mask environmental and conspecific signals, reduce reproduction success, induce stress, affect parental care, and even affect larvae development. These results warn of the possible severe effects of noise pollution on fish and warrant the need of further studies addressing the consequences of noise at the population level.
... evolved to attract females and were later co-opted to deter aggression from competitor males (Morris, Tudor & Dubois, 2007). The boatwhistles in the Lusitanian toadfish Halobatrachus didactylus are mainly used as an ornament but also signal territorial ownership (Vasconcelos et al., 2010). The courtship display is another type of sexual trait expressed as body movements or dances, which often also serves to highlight other ornaments, such as sizes, colours and vocalizations (e.g., Oliveira & Custodio, 1998;Kodric-Brown & Nicoletto, 2001;Borgia & Coleman, 2000;respectively). ...
Background
Evidence of male-male courtship display is widespread across the animal kingdom. Yet, its function and evolutionary origin remain unclear. Here, we hypothesise that male-male courtship display evolved in response to selection pressure exerted by intrasexual competition during male-female courtship interactions. Intrasexual competition can be caused by bystander male pressure through eavesdropping and exploiting on displayer male’s courtship interactions with females. This bystander pressure can lead to an audience effect by the displayer, who will change their courtship behaviour in the presence of bystanders and display directly towards them, even in the absence of females, as an intimidation strategy. In species where this selection pressure has taken place, we predict that the male courtship display will have a dual function: attract females and deter competitors. Therefore, we expected to find more evidence of bystander-related behaviours in species for which male-male courtship display is linked to intrasexual competition compared to species for which other explanatory hypotheses are more plausible ( e.g ., mistaken identity or courtship practice).
Methodology
We conducted two systematic reviews to test this hypothesis. First, we conducted a search for studies of species with courtship display between males and of the hypotheses provided to explain this behaviour. Our goal was to identify the species with male-male courtship display and evidence of intrasexual competition. Second, among the species with male-male courtship display, we searched for evidence of bystander-related behaviours, i.e ., articles referring to eavesdropping, exploitation, and audience effect during male-female courtship interactions. Our goal was to test whether species with intrasexual competition are also more likely to show bystander-related behaviours.
Results
Although most studies reporting male courtship display towards other males do not suggest any explanatory hypothesis for this behaviour, the intrasexual competition hypothesis was largely mentioned and supported by some studies reviewed. Additionally, there is more evidence of eavesdropping and of all three bystander-related behaviours combined in species for which the intrasexual competition hypothesis was suggested.
Conclusions
Overall, our review supports the hypothesis that intrasexual competition can play a key role in male courtship display evolution, namely that male-male courtship display may have evolved as a secondary function of male-female courtship interactions via bystander male pressure. However, our review also shows that despite the increasing interest in same-sex sexual behaviours, and male-male courtship display in particular, most studies were found to be merely descriptive, and the hypotheses they suggested to explain courtship display between males mostly speculative. This highlights an important gap in the literature. To clarify both the evolution and the function of male-male courtship display, this behaviour needs to be empirically studied more often. Our review can help advancing this research area, as it makes the 20 species with male-male courtship display for which the intrasexual competition hypothesis was suggested excellent candidates for empirical research.
... Species with specific home ranges, like reef fish, are more easily observed (e.g., Wardle et al., 2001), an approach used on land to monitor animal behavior during playbacks at specific locations such as watering holes (O'Connell-Rodwell et al. 2006, 2007, within burrows (Hill and Shadley 2001), or upon single plants (Morales et al. 2008;Caldwell et al. 2010a). The sessile lifestyle of many invertebrates, and the territorial nature of some benthic fish, e.g., the sound-producing Lusitanian toadfish (Vasconcelos et al. 2010), in aquatic systems means that this monitoring approach may be feasible in some cases. ...
Here we provide an overview of work related to anthropogenically produced substrate-borne vibrational noise. We review the marine and terrestrial vibrational noise literature base, focusing upon the species studied, the increasing research attention, and the findings of latest papers. We highlight the key sources of vibrational noise, how noise may be measured and mitigated (both by humans and by animal receivers), and how we can test for the potential impacts of noise sources. We present two case studies of previously untested species, the first relating to vibrational sensitivity of barnacles, and the second relating to activity patterns of the Madagascar hissing cockroach under vibrational noise. Currently it is difficult to draw firm conclusions on the effects of vibrational noise, given the few studies in both environments. However, effects seen to date include interference with signaling, pair formation and parental care, in addition to activity changes, and an increase of stress-related behaviors. Notably the aquatic research base lags behind the terrestrial, with the vibrational sensing capabilities of most benthic organisms largely unknown currently. We highlight vibrational noise as an area that requires more research attention both on the land and in the sea.
... In some cases, the signaller may employ entirely different signals for different receivers, or in different contexts (Andersson et al., 2002;Balakrishnan & Pollack, 1996;Baptista, 1978;Byers & Kroodsma, 2009;Centeno et al., 2021;Karubian et al., 2009;Leo, 1959;Rosenthal et al., 2018;Vanderbilt et al., 2015;Zambre & Thaker, 2017). Alternatively, signallers with limited repertoires may modify the sequence in which notes are emitted, such that similar signals may convey different messages to different receivers (Berglund et al., 1996;Dalziell & Cockburn, 2008;Mosk at & Hauber, 2019;Myberg Jr, 1997;Vasconcelos et al., 2010). Studies have modelled vocal sequences as first-order Markov chains, or used Shannon entropy to characterize sequence variability (Kershenbaum et al., 2016). ...
Acoustic signals in animals serve to convey context-dependent information to receivers. Birds and mammals combine diverse sounds into complex sequences to communicate, but the role of temporal sequencing of signals remains understudied in other taxa. Anuran vocalizations are a prominent feature of their life history, and function in defence of territories and to attract mates. However, there are few data on whether anurans pattern their calls into sequences, and whether temporal sequences convey information about context. Here, we investigated the context-dependent vocal repertoire and the use of vocal sequences by two anuran species belonging to different lineages, comparing frogs vocalizing alone and in the presence of a territorial rival. Using a robust analytical framework, we present evidence that both species modify their vocal sequence structure according to context. Specifically, one species (with a smaller repertoire, from a more basal lineage) appends notes to generate more complex sequences, whereas the other (more recently diverged and with a larger repertoire) shifts to different note types, resulting in different sequences for different contexts. Thus, despite differences in repertoire size, both frog species are capable of adjusting the temporal sequence of vocalizations to communicate in different contexts. Vocal sequences and context-dependent ‘syntax’ may be more common in anurans than previously thought, and our methodology presents a paradigm to study the evolution and function of these complex vocal patterns.
... Using a custom LabVIEW script, particle motion amplitude measurements (V pk-pk ) for each axis ( x-, y-and z-axis) were corrected for the gain (sensitivity) of the accelerometer. The V pk-pk measurements for each axis ( x-, y-and z-axis) were then used to calculate the combined magnitude vector of particle acceleration in dB scale ( Eq. (1) ) ( Bhandiwad et al., 2017 ;Vasconcelos et al., 2010 ;Wysocki et al., 2009 ) as follows: ...
Age-related hearing loss (ARHL), also known as presbycusis, is a widespread and debilitating condition impacting many older adults. Conventionally, researchers utilize mammalian model systems or human cadaveric tissue to study ARHL pathology. Recently, the zebrafish has become an effective and tractable model system for a wide variety of genetic and environmental auditory insults, but little is known about the incidence or extent of ARHL in zebrafish and other non-mammalian models. Here, we evaluated whether zebrafish exhibit age-related loss in auditory sensitivity. The auditory sensitivity of adult wild-type zebrafish (AB/WIK strain) from three adult age subgroups (13-month, 20-month, and 37-month) was characterized using the auditory evoked potential (AEP) recording technique. AEPs were elicited using pure tone stimuli (115-4500 Hz) presented via an underwater loudspeaker and recorded using shielded subdermal metal electrodes. Based on measures of sound pressure and particle acceleration, the mean AEP thresholds of 37-month-old fish [mean sound pressure level (SPL) = 122.2 dB ± 2.2 dB SE re: 1 μPa; mean particle acceleration level (PAL) = -27.5 ± 2.3 dB SE re: 1 ms⁻²] were approximately 9 dB higher than that of 20-month-old fish [(mean SPL = 113.1 ± 2.7 dB SE re: 1 μPa; mean PAL = -37.2 ± 2.8 dB re: 1 ms⁻²; p = 0.007)] and 6 dB higher than that of 13-month-old fish [(mean SPL = 116.3 ± 2.5 dB SE re: 1 μPa; mean PAL = -34.1 ± 2.6 dB SE re: 1 ms⁻²; p = 0.052)]. Lowest AEP thresholds for all three age groups were generally between 800 Hz and 1850 Hz, with no evidence for frequency-specific age-related loss. Our results suggest that zebrafish undergo age-related loss in auditory sensitivity, but the form and magnitude of loss is markedly different than in mammals, including humans. Future work is needed to further describe the incidence and extent of ARHL across vertebrate groups and to determine which, if any, ARHL mechanisms may be conserved across vertebrates to support meaningful comparative/translational studies.
... The inter-call interval (from the end of one call to the start of the next call), single-call duration, and the number of pulses per bout were observed to be 4.97 6 1.05 s, 0.45 6 0.05 s, and 17.80 6 3.17, respectively [ Table I], indicating a toadfish sound (Vasconcelos, 2010;Mensinger, 2014). The spectrogram [ Fig. 6(c)] of a single call from location 1 confirms that the sounds were from Batrachoididae [Figs. ...
In this study, an analysis of the passive acoustic data is carried out for the quantitative characterization of shallow-water acoustic environments from three major estuarine systems of Goa during the months of March and April. The identification of fish sounds was carried out using waveform and peak power spectral densities (PSDs) of the individual fish calls. Fish sound data showed that the toadfish of the Batrachoididae family (Colletteichthys dussumieri species) produced a spectral level 112.27 ± 4.48 dB re 1 μPa² /Hz at 448.96 ± 40.30 Hz frequency from the mangrove-dominated tidally influenced Mandovi estuary. Similarly, in a coral reef area near Grande Island in the Zuari estuary, Tiger Perch fish from the Terapontidae family (Terapon threaps species) were identified, having spectral levels 106.91 ± 3.08 dB re 1 μPa² /Hz at 1791.56 ± 106.55 Hz frequency. From the Sal estuary, PSD levels were found to be around 98.24 ± 2.98 dB re 1 μPa²/Hz at 1796.95 ± 72.76 Hz frequency for Tiger Perch of the Terapontidae family (T. threaps species). To characterize the contributions of biophony (fish), geophony (wind and flow, etc.), and anthrophony (boats, etc.), cluster analysis is employed. In the Mandovi estuary, the root-mean-square sound pressure level (SPLrms) of broadband toadfish was a function of the water flow and temperature. In the Zuari estuary, SPLrms was a function of the water temperature and wind, whereas in the Sal estuary, wind mainly influenced the SPLrms.
... Thus, our findings corroborate previous studies that have assumed changes in rates of detected sounds relate to changes in rates of fish sound production Bertucci et al., 2015) and support previous assumptions that levels of recorded sounds are indicative of reproductive activity (Locascio and Mann, 2011a;Montie et al., 2016Montie et al., , 2017 and the relative abundances of both sexes Rowell et al., 2012;Rowell et al., 2017), when environmental effects on detection and variability among sound producers are considered and understood. In addition, as some species produce sounds within multiple behaviours, the behavioural contexts of sounds need to be fully understood before making such inferences (Mann and Lobel, 1998;Vasconcelos et al., 2010;Tricas and Boyle, 2014). For example, some species, such as haddock Melanogrammus aeglefinus, produce the same types of sounds during and outside of the spawning season (Casaretto et al., 2015). ...
While monitoring fish sounds has enhanced our understanding of spatio-temporal patterns of spawning and acoustic communication, data interpretation often fails to account for environmental effects on acoustic recordings, resulting in uncertainty of whether measures of detected fish sounds correspond to rates of sound production, specific behaviours, and abundance. In this study, we applied acoustic propagation modelling and detection theory to estimate rates of sound production of territorial, male Gulf grouper (Mycteroperca jordani) from passive acoustic recordings and evaluate effective communication distances. To assess behavioural drivers, environmentally calibrated, hourly estimates of sound production rates were compared to diver observations of courtship, spawning, and numbers of females encountered within male territories. Rates of sound production increased before sunset and were correlated to observed rates of spawning and females encountered, indicating that sound production is largely driven by female presence and increased opportunities to spawn. The mean effective communication distance was estimated to be <21 m, supporting the importance of short-range communication within the observed behaviours. Our findings corroborate that fish sounds can be used to infer measures of reproductive activity and the relative abundance of both sexes during spawning periods once properly calibrated for environmental effects and detection capabilities.
... The sounds described in this study proportionally were observed most often during interactions with females that often resulted in spawning. However, considering that visual observations were only made for short periods of time during the month of May each year and males were also observed to generate sounds in the absence of females when patrolling territories, the sounds described may also be produced within additional behavioural contexts, such as defence of non-spawning territories or agonism (Mann & Lobel, 1998;Tricas & Boyle, 2014;Vasconcelos et al., 2010). ...
The reproductive and acoustic behaviours of Gulf grouper Mycteroperca jordani were studied at a spawning aggregation site in the southern Gulf of California, México. In May 2015–2017, divers located and surveyed a spawning aggregation site within Cabo Pulmo National Park. Adult M. jordani conformed to a lek mating system in which large males formed territories over sand adjacent to a rocky reef that were spatially segregated from smaller females outside of courtship and spawning periods. Females moved into male territories during evening hours to spawn. Male courtship behaviours targeted a single female, included head shakes and burst rises and preceded pair spawning prior to sunset. Males and females displayed three shared colour phases, but four phases were sex‐specific. During evening hours, courtship and spawning, both sexes exhibited sexual dichromatism concurrent with reproductive behaviours. The pair‐spawning mating system and observations of bimodal size distributions by sex support previous claims of protogyny in the species. Males produced sounds during territorial patrols, courtship and spawning rushes, which corroborated the importance of acoustic communication within the behavioural repertoire associated with spawning. Long‐term acoustic monitoring revealed increases in total sounds detected day⁻¹ from March through June with diel increases (e.g., evenings) that may be indicative of the spawning season. Observations of spawning on 12 consecutive evenings in May 2017 coupled with extended periods of sound production suggest that spawning does not follow a lunar rhythm. This first description of the mating system and sounds of the endangered M. jordani facilitates future development of seasonal and areal protections to restore and manage the species.
... and is exhibited across a range of taxa, including mammals (Erlinge 1968;Rosell et al. 1998), birds (Gill & Wolf 1975), reptiles (Marler et al. 1995), fish (Craig 1996), insects (Davies 1978) and amphibians (Wells 1978). Behaviours used to defend territories can include visual signals (e.g., foot-flagging in frogs, Preininger et al. 2009), auditory signals (e.g., vocalizations of green frogs, Wells 1978; boatwhistles in the Lusitanian toadfish, Vasconcelos et al. 2010) and chemical signals (e.g., latrines of swift foxes, Darden et al. 2008; scent marking in Eurasian beavers, Rosell et al. 1998). ...
I investigated territorial defence behaviour and tested the mechanism of kin recognition in red squirrels (Tamiasciurus hudsonicus) using playbacks of territorial calls. Red squirrels did not discriminate between the calls of kin and non-kin despite previous evidence that they are capable of recognizing kin through territorial vocalizations. I suggest that changes in environmental conditions might have altered the costs and benefits of differential treatment of kin, resulting in a lack of discrimination. Also, red squirrels were no more aggressive in response to playback calls from non-neighbours than from neighbours. Additional playback trials with territorial calls where the frequency was altered suggested that fundamental frequency is the important acoustic component for kin recognition. Variation in territorial defence was evident in red squirrels and call rates increased as the number of surrounding conspecifics increased, indicating that red squirrels adjust territorial defence in response to intruder pressure.
... The plainfin midshipman has two male reproductive morphs, types I and II, that diverge in courtship and spawning behaviors as well as a range of morphological and hormonal characters (Section 2.04.2.2; Figure 1, Table 1; Bass, 1996). Comparable tactics and morphs have been described in at least one other species of toadfish, the Lusita- nian toadfish, Halobatrachus didactylus (e.g., Modesto and Can?rio, 2003;Vasconcelos et al., 2010). Type I males were those already known in the literature to build nests under rocky shelters in the intertidal and sub- tidal environments where they fertilize the eggs of females that are deposited on the roof of the nest (Figure 1(a) and 1(b)) (e.g., Greene, 1924;Arora, 1948). ...
... In general, sound types in this family consist of growls and hums (Bass and McKibben 2003), croaks (dos Santos et al. 2000), short, broadband grunts (Thorson and Fine 2002a;Fine and Waybright 2015), and the harmonic Bboatwhistleĉ all used primarily for mate attraction (Bass and McKibben 2003). Calls have also been observed to be produced in the defense of the nest by males of Halobatrachus didactylus (Vasconcelos et al. 2010;Conti et al. 2015). Grunts are produced right before calls (Talvoga 1958) or as stand-alone utterances, singly or in combination, in agonistic and distress situations by both males and females (Gray and Winn 1961;dos Santos et al. 2000;Amorim et al. 2006;Maruska and Mensinger 2009;Fine and Waybright 2015). ...
The soundscapes of many coastal habitats include vocalizations produced by species of the family Batrachoididae (toadfish and midshipman). We describe the calling and grunting behavior of male Amphichthys cryptocentrus, a tropical toadfish, and predict how these vocalizations are influenced by conspecifics. We recorded individual males, which produced broadband grunts and multi-note, harmonic “boatwhistle” calls. Grunts were either in combination with calls or stand-alone. We used a null model to test if these latter grunts were produced at random or in response to calls from conspecifics. The model supports the hypothesis that grunts were in response to calls from neighboring males, suggesting acoustic competition. Using the most conservative estimate of hearing abilities we predict that males responded to the second harmonic of neighbor’s calls (230 Hz) at amplitudes of approximately 100–125 dB re 1μPa2/Hz. We also observed that call and grunt rates increased when males were exposed to higher rates of acoustic activity from neighboring fish. Fish used grunts to respond to background calls that occurred at different amplitudes, suggesting they responded to the calls of multiple neighboring fish and not just the highest amplitude neighbor. This communication with multiple fish within hearing range suggests a communication network in which the spatial distribution of individual toadfish relative to one another will impact their vocal behavior. Thus, the density and distribution, and not just abundance, of these toadfish at a given site will influence the characteristics of the chorus and the role of this species in the local soundscape.
... While the fishing boat noise, with more energy at the BW spectral range, had a severe impact (over 60%) on communication range, ferry boat noise had a smaller impact due to its lower energy in the BWs range thus causing less masking. As the BW is key for reproduction success (Vasconcelos et al. 2012 and territorial defense (Vasconcelos et al. 2010, Conti et al. 2015 the reduction in BW active space of BWs reported here, mainly for small boat noise, will likely incur fitness costs for the species. Indeed boat noise is known to affect the rate of breeding vocalizations in the oyster toadfish Opsanus tau (Luczkovich et al. 2016) and in sciaenids (Picciulin et al. 2012) likely having a detrimental impact on the reproductive outcome of these species. ...
Anthropogenic noise is considered of global concern since increasing ocean background noise due to human activities is impacting aquatic lifeforms. One of the most prevalent anthropogenic noise sources are boat engines. Although motorboat traffic has increased in the last decades, the impact of boat noise on the communication of aquatic animals is still poorly known. Impact of boat noise on the communication active space of a vocal teleost, the Lusitanian toadfish (Halobatrachus dydactilus), was tested. To achieve this goal a comparison between the maximum distance a fish can perceive the conspecific advertisement signal – the boatwhistle, before and after embedding the acoustic signal in boat noise, using the AEP technique, was made. Noise from two different types of boat, a small motorboat and a ferryboat, was used. At about 2 m water depth, active space ranged between 6 and 13 m, depending on boatwhistle spectral characteristics.Noise from the small motorboat and from the ferry boat reduced the communication range to 2.5-4 m and 7-8.5 m, respectively. These results demonstrate that boat noise can severely reduce the acoustic active space of this fish and, with heavy boat traffic, it may influence mate finding, depending on the boat noisecharacteristics.
... The plainfin midshipman has two male reproductive morphs, types I and II, that diverge in courtship and spawning behaviors as well as a range of morphological and hormonal characters (Section 2.04.2.2; Figure 1, Table 1; Bass, 1996). Comparable tactics and morphs have been described in at least one other species of toadfish, the Lusitanian toadfish, Halobatrachus didactylus (e.g., Modesto and Canário, 2003;Vasconcelos et al., 2010). Type I males were those already known in the literature to build nests under rocky shelters in the intertidal and subtidal environments where they fertilize the eggs of females that are deposited on the roof of the nest (Figure 1(a) and 1(b)) (e.g., Greene, 1924;Arora, 1948). ...
Teleost fish exhibit a diversity of reproductive phenotypes, including alternative reproductive tactics used by male morphs that differ in a suite of behavioral, somatic, neural, and endocrine traits. The hormonal and neurophysiological underpinnings of intrasexual divergence in reproductive-related behaviors are well studied in species that depend on acoustic communication for reproduction. Toadfishes are ‘vocal champions’ of acoustic communication among fishes, the largest group of living vertebrates, and include species exhibiting alternative reproductive strategies. Studies in toadfishes have elucidated neural, hormonal, and genetic mechanisms underlying sensory (auditory) and motor (vocal) control of acoustic communication that diverge between and within the sexes.
... As far as we know, fish are also likely to be susceptible to the human-induced rise in underwater sound, as they are well known to hear and use sounds for many aspects of their underwater life (Fay, 2009;Ladich, 2004;Slabbekoorn et al., 2010). Like in air, underwater masking effects are determined by the spectral overlap of ambient noise with biologically relevant sounds (Codarin, Wysocki, Ladich, & Picciulin, 2009;Gutscher, Wysocki, & Ladich, 2011;Vasconcelos, Simões, Almada, Fonseca, & Amorim, 2010). Independent of masking, several studies have also reported behavioural changes in response to artificial tones or wideband sounds. ...
... Besides boatwhistles, Lusitanian toadfish also produces other pulsed sounds, such as grunt trains, long grunt trains, croaks, double croaks, and associations between some of these calls (). Some of these sounds are known to be used during agonistic interactions, such as territorial defense (e.g., grunt train, Vasconcelos and Ladich 2008; Vasconcelos et al. 2010), but the function of such vocal plasticity remains unclear. Females deposit the eggs on the roof of the nest, which are guarded by the male until the offspring are free swimming (dos Santos et al. 2000). ...
... Here the usefulness of HMM-based automatic recognition systems to extensively analyse toadfish sound recordings is demonstrated. Future work using this system will allow assessing subtleties of the Lusitanian toadfish vocal behaviour in its natural habitat, which requires very long round-the-clock sound recordings, such as vocal rhythms, vocal interactions among fish, etc. Adjustments on this system to allow more subtle discriminations of sounds could, for example, permit to infer the dynamics of agonistic interactions throughout the breeding season by sorting advertisement from agonistic boatwhistles, which differ in dominant frequency and amplitude modulation (Vasconcelos et al., 2010). Also the ability to recognize the less frequent sounds may improve by increasing data sets, which can be relevant to study this species communication. ...
The study of acoustic communication in animals often requires not only the recognition of species specific acoustic signals but also the identification of individual subjects, all in a complex acoustic background. Moreover, when very long recordings are to be analyzed, automatic recognition and identification processes are invaluable tools to extract the relevant biological information. A pattern recognition methodology based on hidden Markov models is presented inspired by successful results obtained in the most widely known and complex acoustical communication signal: human speech. This methodology was applied here for the first time to the detection and recognition of fish acoustic signals, specifically in a stream of round-the-clock recordings of Lusitanian toadfish (Halobatrachus didactylus) in their natural estuarine habitat. The results show that this methodology is able not only to detect the mating sounds (boatwhistles) but also to identify individual male toadfish, reaching an identification rate of ca. 95%. Moreover this method also proved to be a powerful tool to assess signal durations in large data sets. However, the system failed in recognizing other sound types.
... These leave the nests shortly after laying the eggs, while the male continues to vocalize to attract more females to spawn with until the nest is filled with multiple clutches (Carriço et al., 2014). The males provide parental care to the offspring (cleaning, promoting water renewal and egg aeration and protection from predators) for several weeks until juveniles are free-swimming (Modesto & Canário, 2003;Barimo et al., 2007;Vasconcelos et al., 2010;Ramos et al., 2012), a behaviour that may limit the males' feeding opportunities. Type II males, the alternative morphotype, have a satellite-spawning behaviour and never provide parental care to sired eggs (Modesto & Canário, 2003;Costa, 2004). ...
The Lusitanian toadfish,
Halobatrachus didactylus
, like other batrachoidids, is a benthic fish species with nesting behaviour during the breeding season. During this prolonged period it engages in mating activities and remains in the nest providing parental care. It is not known whether males feed while providing parental care but it is likely that their limited mobility may restrict their diet and influence their fitness. As a consequence, egg cannibalism could occur as a life-history strategy. The aim of the present study is to ascertain the feeding behaviour of nesting males, in comparison to mature non-nesting males, and to identify potential life-history traits related to egg cannibalism. Nest-holders were sampled from artificial nests placed in an intertidal area of the Tagus estuary, only exposed during spring low tides. The diet of nest-holders was compared with that of non-nesting mature males from the same area, captured by otter trawl. The present study demonstrates that despite their constrained mobility nest-holders feed during the breeding season, although in a more opportunistic fashion than non-nesting males. Nest-holders showed a generalist feeding behaviour, with a more heterogeneous diet. Egg cannibalism was not related to male condition, paternity or brood size but showed a higher incidence early in the season when water temperatures were lower. The results suggest a possible seasonal trade-off strategy between care and energy recovery, triggered by environmental factors, where under unfavourable conditions to sustain viable eggs the male may recover energy by eating eggs, thus benefiting future reproductive success, later in the season.
... As far as we know, fish are also likely to be susceptible to the human-induced rise in underwater sound, as they are well known to hear and use sounds for many aspects of their underwater life (Fay, 2009;Ladich, 2004;Slabbekoorn et al., 2010). Like in air, underwater masking effects are determined by the spectral overlap of ambient noise with biologically relevant sounds (Codarin, Wysocki, Ladich, & Picciulin, 2009;Gutscher, Wysocki, & Ladich, 2011;Vasconcelos, Simões, Almada, Fonseca, & Amorim, 2010). Independent of masking, several studies have also reported behavioural changes in response to artificial tones or wideband sounds. ...
... As far as we know, fish are also likely to be susceptible to the human-induced rise in underwater sound, as they are well known to hear and use sounds for many aspects of their underwater life (Fay, 2009;Ladich, 2004;Slabbekoorn et al., 2010). Like in air, underwater masking effects are determined by the spectral overlap of ambient noise with biologically relevant sounds (Codarin, Wysocki, Ladich, & Picciulin, 2009;Gutscher, Wysocki, & Ladich, 2011;Vasconcelos, Simões, Almada, Fonseca, & Amorim, 2010). Independent of masking, several studies have also reported behavioural changes in response to artificial tones or wideband sounds. ...
Anthropogenic noise of variable temporal patterns is increasing in both marine and freshwater systems. Aquatic animals often rely on sounds for communication and orientation, which may therefore become more difficult. Predator–prey interactions may be affected by masking of auditory cues, sound-related disturbance or attentional interference. Here, we investigated the impact on both predator and prey for zebrafish, Danio rerio, preying on water fleas, Daphnia magna. We experimentally raised ambient sound levels in an aquarium and tested four sound conditions that varied in temporal pattern: continuous, fast and slow regular intermittent and irregular intermittent, which we compared with ambient sound levels with no extra exposure. We found no effects on water flea swimming speed or depth but there was an increasing number of individual zebrafish with an increased number of startle responses, especially to the intermittent sound treatments, which was also reflected in a significant increase in zebrafish swimming speed, but not in any change in zebrafish swimming depth. Discrimination in attacking edible water fleas or inedible duckweed particles was low for the zebrafish and unaffected by sound exposure, but foraging was affected in two ways: intermittent sounds delayed the initial acceleration response and all treatments caused a rise in handling error. These insights confirm that elevated sound levels, and especially intermittent conditions, may affect predator–prey interactions. Our results apply to laboratory conditions but call for outdoor studies that go beyond single-species effects. If acoustic impact of human activities extends to multiple species and their interactions, natural sound conditions may turn out to be important for the stability and dynamics of aquatic ecosystems.
... Fish emit sounds in a variety of ways and the sounds are often associated with distinct behaviours (Amorim, 2006). Sounds can be expressed during agonistic interactions (Amorim & Neves, 2008;Raffinger & Ladich, 2009;Vasconcelos et al., 2010), in the presence of predators (e.g., Winn et al., 1964;Myrberg, 1981;Smith, 1992), when feeding (e.g., Phillips, 1989;Lagardère & Mallekh, 2000;Amorim et al., 2004), and during courtship (e.g., Lobel & Kerr, 1999;Lugli et al., 2004;Malavasi et al., 2009). One of the most well-studied purposes of auditory communication is for mate attraction (Kasumyan, 2009), with males calling not only to indicate their location (Tavolga, 1958;Lugli et al., 1996a, b), but also to advertise male quality to females (Amorim, 2006). ...
Acoustic communication is of fundamental importance in many fish species but it is often unclear what information is present in different calls and how responsiveness varies with reproductive state and the sex of the receiver. The current study investigates reproductive flexibility in acoustic responsiveness through differential attraction between reproductive morphs of the round goby (Neogobius melanostomus) to conspecific calls. Parental male (PM) round gobies emit calls and females respond to these calls with high specificity. We used playback experiments to determine the response of gobies to recordings of two conspecific calls, a grunt and a drum. For the grunt, reproductive females (RF) displayed a significantly higher response for first approach than nonreproductive males (NRM), but RFs never responded to the drum call. Upon examining within-morph responses for time spent at a playing speaker, RFs were found to spend the longest time at the grunt call compared to other sound types. In contrast to the female responses, NRMs and sneaker males (SM) displayed a strong preference to the drum call. Overall these results support that the grunt could be for mate attraction while NRMs and SMs may be eavesdropping on the drum call. By determining the relationship between reproductive state and responses to conspecific calls, we show that reproductive state is a critical factor in understanding behavioural responses in fish.
... Afterwards, we discarded all tests where the average RMS amplitude of the PBK was less than one-third of the RMS amplitude of the subjects' call; thus, we only used PBKs that mimicked the amplitude of a conspecific neighbour calling from no further than about 1.5 m away. The speakers used for stimuli playbacks may alter the amplitude modulation of the stimuli boatwhistles and do not respond well to frequencies below about 100 Hz, cutting off the fundamental frequency, but maintained the second harmonic as the dominant frequency (Fig. 1), which is the typical main frequency of mating boatwhistles (Amorim & Vasconcelos 2008; Vasconcelos et al. 2010). ...
Choruses have been described mostly in birds, anurans and insects but have been poorly studied in fish. Research in batrachoidid (toadfishes) species suggest vocal facilitation among neighbouring males, but whether chorusing fish present more complex interactions is unknown. In this study, we test the hypothesis that chorusing fish males compete actively to increase attractiveness to females. We first describe vocal interactions in natural choruses of Lusitanian toadfish males. Our analysis found positive correlations between the calling rates of neighbouring males in several occasions. However, we also found that males that showed an overall low vocal activity throughout the observation period exhibited peaks of increased calling activity when neighbours decreased their calling rate, suggesting an opportunistic maximisation of attractiveness. We further test with playback experiments how toadfish males adjust calling activity relative to their neighbours'. We observed that males silent at the time of the playbacks but who had an overall high vocal performance tended to start calling when exposed to playbacks in contrast to low‐activity males. Playback experiments further showed that males initially calling at a high rate adjust their calling rate according to the neighbour's vocal activity level, that is, they increased calling rate when exposed to a high calling rate and decreased it when confronted with a low calling rate. However, males calling at a low rate did not significantly alter their calling rate when presented with a low (similar) or higher calling rate, probably due to temporary physiological and/or ecological constraints. We argue that Lusitanian toadfish males tend to optimise calling effort in relation to their neighbours when they are actively advertising. Further studies are necessary to better understand vocal behaviour with increased chorus size.
... Numerous species of fishes emit sounds in early phases of agonistic interactions and it has been demonstrated that acoustic signals can be key to the fight outcome in some fish species (Ladich & Myberg, 2006). For example, in Halobatrachus didactylus sounds (boatwhistles) function as active 'keep-out' signals during territorial defence (Vasconcelos et al., 2010) and in the cichlid fish Metriaclima zebra the association between visual and acoustic signals lowers the level of aggressiveness between opponents (Bertucci et al., 2010). In the painted goby, sound duration (drum and 'drum sequence' duration) has been suggested to give information about male size and perhaps motivation (Amorim & Neves, 2008). ...
Communication signals provide key information for conspecific recognition, mate choice and rival assessment. The painted goby Pomatoschistus pictus and the common goby P. microps are two closely-related sand goby species, often sympatric and with an overlapping breeding season. In this study we staged male–male and male–female interactions and compared visual, tactile and acoustic behaviour in both species. Sound production in the common goby is here accounted for the first time. We observed some differences in visual behaviour and a striking divergence in the use of tactile and acoustic communication during courtship and agonistic interactions. We further describe differences in drumming signals with social context in the painted goby. This study suggests a divergence in communication in two closely-related sand goby species and emphasizes the importance of further research concerning the role of multimodal communication in closely-related species.
Contests are an important aspect of the lives of diverse animals, from sea anemones competing for space on a rocky shore to fallow deer stags contending for access to females. Why do animals fight? What determines when fights stop and which contestant wins? Addressing fundamental questions on contest behaviour, this volume presents theoretical and empirical perspectives across a range of species. The historical development of contest research, the evolutionary theory of both dyadic and multiparty contests, and approaches to experimental design and data analysis are discussed in the first chapters. This is followed by reviews of research in key animal taxa, from the use of aerial displays and assessment rules in butterflies and the developmental biology of weapons in beetles, through to interstate warfare in humans. The final chapter considers future directions and applications of contest research, making this a comprehensive resource for both graduate students and researchers in the field.
Contests are an important aspect of the lives of diverse animals, from sea anemones competing for space on a rocky shore to fallow deer stags contending for access to females. Why do animals fight? What determines when fights stop and which contestant wins? Addressing fundamental questions on contest behaviour, this volume presents theoretical and empirical perspectives across a range of species. The historical development of contest research, the evolutionary theory of both dyadic and multiparty contests, and approaches to experimental design and data analysis are discussed in the first chapters. This is followed by reviews of research in key animal taxa, from the use of aerial displays and assessment rules in butterflies and the developmental biology of weapons in beetles, through to interstate warfare in humans. The final chapter considers future directions and applications of contest research, making this a comprehensive resource for both graduate students and researchers in the field.
North Pacific minke whale (Balaenoptera acutorostrata) boing calls are commonly detected in Hawaiian waters. When producing boing vocalizations, minke whales seem to be in one of two calling behavioral states. Most often minke whales produce boings with inter-call intervals of several minutes, but sometimes minke whales call rapidly with inter-call intervals of less than a minute. Since minke whales are difficult to detect visually, cue-rate-based density estimation using passive acoustic monitoring has been proposed. However, the variables that influence cue rate or calling rate are poorly understood in most whales, including minke whales. We collected passive acoustic recordings from 47 bottom-mounted hydrophones at the Pacific Missile Range Facility’s instrumented range off the coast of Kauaʻi, Hawaiʻi to test the hypothesis that minke whales call more rapidly when closer in proximity to other calling conspecifics. A total of 599 days of data were recorded between August 2012 and July 2017 and were automatically post-processed to detect, classify, and localize calls. Localized calls were grouped into tracks and manually validated, resulting in 509 individual tracks composed of 36,033 calls within a 16 x 39 km focal study area. Tracked minke whales exhibited a strong bimodal call rate with means of one call every 6.85 min (σ= 2.54 min) and 0.63 min (σ= 0.36 min). We ran hidden Markov models to quantify the relationship between call rate and the distance to the nearest calling conspecific. Overall, the probability of the higher call rate occurring increased as the distance to the nearest conspecific decreased, and the probability of the lower call rate occurring increased as the distance to the nearest conspecific increased. We also examined individual track data and found that minke whales may also exhibit other responses (i.e. increased speed, changes in heading, and cessation of calling) when calling conspecifics are nearby. These findings provide new information about minke whale calling behavior in what is likely a breeding area.
Males of widow spiders courting on the web of females engage in web-reduction behavior which entails excising a section of the web, bundling it up, and wrapping it with their silk. Males of the false black widow spider, Steatoda grossa, in European populations also produce stridulatory courtship sound which has not yet been studied in their invaded North American range. Working with a North American population of S. grossa, we tested the hypotheses that (1) web reduction by males renders webs less attractive to rival males; (2) deposition of silk by courting males has an inter-sexual (male-female) signal function that enhances their likelihood of copulation; and (3) stridulatory sound is a courtship signal of males. Testing anemotactic attraction of males in Y-tube olfactometer experiments revealed that reduced webs (indicative of a mated female) and intact webs (indicative of a virgin female) were equally attractive to males. Recording courtship behavior of males with either functional (silk-releasing) spinnerets or spinnerets experimentally occluded on the web of virgin females showed that males with functional spinnerets were more likely to copulate with the female they courted. Although males possess the stridulatory apparatus to produce courtship sound, they did not stridulate when courting or copulating on the web of females. Our data support the conclusion that web-reduction behavior of S. grossa males in their invaded North American range has no long-range effect on mate seeking males. Instead, web-reduction behavior has an inter-sexual signaling function that seems to be linked to functional spinnerets of the courting male. The signal produced by a male likely entails a volatile silk-borne pheromone, but may also embody a gauge of his endurance (the amount of time he engages in web reduction causing web vibrations).
Papers on sexual selection often highlight the incredible diversity of sexually selected traits across animals. Yet, few studies have tried to explain why this diversity evolved. Animals use many different types of traits to attract mates and outcompete rivals, including colours, songs, and horns, but it remains unclear why, for example, some taxa have songs, others have colours, and others horns. Here, we first conduct a systematic survey of the basic diversity and distribution of different types of sexually selected signals and weapons across the animal Tree of Life. Based on this survey, we describe seven major patterns in trait diversity and distributions. We then discuss 10 unanswered questions raised by these patterns, and how they might be addressed. One major pattern is that most types of sexually selected signals and weapons are apparently absent from most animal phyla (88%), in contrast to the conventional wisdom that a diversity of sexually selected traits is present across animals. Furthermore, most trait diversity is clustered in Arthropoda and Chordata, but only within certain clades. Within these clades, many different types of traits have evolved, and many types appear to have evolved repeatedly. By contrast, other major arthropod and chordate clades appear to lack all or most trait types, and similar patterns are repeated at smaller phylogenetic scales (e.g. within insects). Although most research on sexual selection focuses on female choice, we find similar numbers of traits (among sampled species) are involved in male contests (44%) and female choice (55%). Overall, these patterns are largely unexplained and unexplored, as are many other fundamental questions about the evolution of these traits. We suggest that understanding the diversity of sexually selected traits may require a shift towards macroevolutionary studies at relatively deep timescales (e.g. tens to hundreds of millions of years ago).
Toadfishes (family Batrachoididae) are a well-studied family of soniferous fishes, yet only a fraction of species within the family have been recorded, and only few detailed descriptions of calls exist. Here, we present the first description of the acoustic ecology of Amphyichtys cryptocentrus, a new-world toadfish species, distributed across the southern Caribbean Sea. We recorded fourteen individuals in a seagrass habitat over six nights in the Bocas del Toro Archipelago. Like other toadfishes, A. cryptocentrus produces compound calls with broadband and tonal components; a typical call contains 1–2 grunts, followed by 1–2 boops (average fundamental frequency = 112 Hz, average source level = 138 dB re:1 μPa RMS). While we observed relatively low between-individual variation in frequency components, our results show that individuals can be readily identified based on their call composition and call rate. This suggests that each toadfish has an individual “voice,” which may transmit selection-linked information to females about body condition, status, or motivation to mate. We also observed that toadfish produced grunts during neighbors’ calls, a previously-described aggressive behavior called “acoustic tagging”, which can intercept a potential rival’s mating advertisement. Our findings suggest that A. cryptocentrus (and its population in Bocas del Toro, in particular) represents a useful system for the study of fish bioacoustics and behavioral ecology, and we demonstrate that acoustic communication represents a major aspect of social behavior in coral reef fishes.
Of the three, paired otolithic endorgans in the ear of teleost fishes, the saccule is the one most often demonstrated to have a major role in encoding frequencies of biologically relevant sounds. The toadfish saccule also encodes sound level and sound source direction in the phase-locked activity conveyed via auditory afferents to nuclei of the ipsilateral octaval column in the medulla. Although paired auditory receptors are present in teleost fishes, binaural processes were believed to be unimportant due to the speed of sound in water and the acoustic transparency of the tissues in water. In contrast, there are behavioral and anatomical data that support binaural processing in fishes. Studies in the toadfish combined anatomical tract-tracing and physiological recordings from identified sites along the ascending auditory pathway to document response characteristics at each level. Binaural computations in the medulla and midbrain sharpen the directional information provided by the saccule. Furthermore, physiological studies in the central nervous system indicated that encoding frequency, sound level, temporal pattern, and sound source direction are important components of what the toadfish ear tells the toadfish brain about sound.
Choruses have been described mostly in birds, anurans and insects but have been poorly studied in fish. Research in batrachoidid (toadfishes) species suggest vocal facilitation among neighbouring males, but whether chorusing fish present more complex interactions is unknown. In this study, we test the hypothesis that chorusing fish males compete actively to increase attractiveness to females. We first describe vocal interactions in natural choruses of Lusitanian toadfish males. Our analysis found positive correlations between the calling rates of neighbouring males in several occasions. However, we also found that males that showed an overall low vocal activity throughout the observation period exhibited peaks of increased calling activity when neighbours decreased their calling rate, suggesting an opportunistic maximisation of attractiveness. We further test with playback experiments how toadfish males adjust calling activity relative to their neighbours'. We observed that males silent at the time of the playbacks but who had an overall high vocal performance tended to start calling when exposed to playbacks in contrast to low-activity males. Playback experiments further showed that males initially calling at a high rate adjust their calling rate according to the neighbour's vocal activity level, that is, they increased calling rate when exposed to a high calling rate and decreased it when confronted with a low calling rate. However, males calling at a low rate did not significantly alter their calling rate when presented with a low (similar) or higher calling rate, probably due to temporary physiological and/or ecological constraints. We argue that Lusitanian toadfish males tend to optimise calling effort in relation to their neighbours when they are actively advertising. Further studies are necessary to better understand vocal behaviour with increased chorus size.
Fishes have been central to our understanding of many of the major aspects of contest behaviour, extending from Tinbergen's early work on social releasers to some of the initial tests of assessment models and now to the neuroendocrine and genomic regulation of aggression and dominance. In this chapter, we focus on some exciting areas of research in fish contest behaviour that promise to shed light on the mul-tidimensionality of resource holding potential, sex-and size-related differences in decision-making during contests, whole-organism performance and fight outcomes, selection and potential constraints on contest behaviour; and the role of developmental plasticity in driving RHP-related phenotypic variation. We have developed this chapter more as a prospectus than a review, using the concrete foundation laid down by numerous researchers to highlight areas that could be of great import in the years to come. This approach, of course, leaves us with many unanswered questions that we hope will serve as a springboard for rigorous hypothesis testing using an integrative framework for fish contest behaviour.
A previously unreported kind of fish sound, which was produced spontaneously by nesting male Porichthys notatus, was recorded in the field and laboratory. Unlike other fish sounds, this monotonous ‘hum’ continues uninterrupted from a few seconds to over 60 min with a mean length of about 11 min. It has a fundamental frequency between 98–108 Hz. The hum was produced only at night. The hum stimulates male-searching behavior in gravid females and serves as an underwater acoustic beacon for mate localization in this nocturnally active species. Gravid females responded in identical manner to pure tones as to the hum and became most highly excited at ~95 Hz, but also responed actively to pure tones over a range of 85–115 Hz. Spent females, juveniles and ripe males showed little, if any, response to the same pure tones. Gravid females tracked in an 8 m diameter concrete tank oriented to the 95 Hz pure tone by swimming directly 2–3 m to the suspended speaker, or by swimming in a circuitous path to the source, then pausing, turning or stopping under the speaker or swimming up to and butting and nipping the speaker.
Fish sound characteristics are associated with different sound-generating mechanisms. Sounds produced by swimbladder-related mechanisms usually comprise low-frequency pulses produced at different rates. Fishes emit one to five sound types that do not show such outstanding variability as found in other taxa. However, closely related species show consistent differences in their sounds and in some species even individuality is found. Of particular interest are differences in courtship sounds made by closely related sympatric species that may promote reproductive isolation. Differences between individuals of the same species may in turn play a role in sexual selection through male-male competition and female mate choice. Other known sources of variability are related to context, including motivation and recent social status, season, time of day, ontogenetic changes and sexual dimorphism. Fish sound variability is mainly based on temporal patterning of sounds or pulses within a sound and on frequency variation (sometimes modulation). Such variability has been found to play a role in the social life of fishes.
Boatwhistles produced by the toadfish Halobatrachus didactylus seem to function as mate attraction calls during the breeding season. Recent observations, however, indicate that their emission is not restricted to this period, suggesting that boatwhistles may have other functions. The possible dual function of boatwhistles was tested by eliciting sound production from reproductive males in advertisement and territorial defence contexts. These were simulated by creating aggregations of confined nesting males in an intertidal area and by conducting territorial intrusion experiments in tanks, respectively. Furthermore, we investigated whether parental care (eggs in the nest) affected the behavioral responses of territorial males. Nesting males kept in aggregations emitted boatwhistles spontaneously for several days. The relation between calling rate and number of eggs in the nest is under analysis. During territorial intrusions, resident males prevented the entrance of intruders in their shelters by producing mostly boatwhistles. Parental males revealed higher aggression levels, exhibiting additional threatening and attack behaviors. Agonistic boatwhistles differed from the mating calls by presenting less amplitude modulation and lower dominant and fundamental frequencies. These results suggest that, apart from attracting mates, the boatwhistles of batrachoidids may also function as an active keep‐out signal during territorial defence.
Female and male preferences for various features of the male's vibratory courtship signals are described for the wandering spider Cupiennius getazi (Ctenidae). Preferences were determined by replaying synthetic and natural, but altered, conspecific male signals to the spiders. Although the number of females responding varied between the different test situations, the number of responses per replayed signal were not significantly different. The latency of the first female response was not correlated with the number of females responding, that is, with the quality of the male's signal. Females responded on average around the third replayed signal. Thus females appeared to follow an all-or-none response rule. They were only broadly tuned to the average properties of the male's releaser (e.g. they tolerated large variations of amplitudes, durations and repetition rates). Moreover, they did not prefer high to low amplitudes, long to short signals, or frequently repeated to rarely displayed signals or syllables. It thus seems unlikely that they differentiated between conspecific males during the vibratory communication phase of courtship. In contrast, females exhibited clear preferences for syllables longer than 240 ms and consisting of two 'subsyllables'. These patterns are typical for conspecific signals, but atypical for heterospecific signals. This strongly suggests that female preferences serve species recognition. Theory predicts that when male investment is small relative to that of females, males will be less selective in responding to cues indicating the presence of a potential mate. In C. getazi, displaying males are such a cue for both sexes. In response to male vibrations, males had few preferences and were either as selective as females or less so (in two and five of the seven tested parameters, respectively).
Several batrachoidids have been known to produce sounds associated with courtship and agonistic interactions, and their repertoires have been studied acoustically and behaviourally. In contrast, sound production of the Lusitanian toadfish Halobatrachus didactylus, although often noted, has not been acoustically studied.This sedentary predator of Northeastern Atlantic coastal waters is usually found in sandy and muddy substrates, under rocks or crevices. Sound recordings were made in Ria Formosa, a lagoon complex in southern Portugal. The sound producing apparatus was studied in adult individuals of both sexes captured by local fishermen.It is shown that this species produces acoustic emissions similar to other batrachoidids. It produces a long, rhythmical, tonal sound, often in choruses, which is comparable to the boatwhistle or hum signals of Opsanus and Porichthys, and a complex of signals that were classified as grunts, croaks, double croaks and mixed calls (‘grunt-croak’). As in other toadfishes, H. didactylus presents sonic muscles connected to a bi-lobed swimbladder. Asynchronous contractions of the sonic muscles were detected when massaging the ventral surface of the fish.
Most passive acoustics studies focus on daily and seasonal timing and location of choruses of calling fish, particularly sciaenids. Because male toadfish Opsanus spp. are stationary for extended periods, it is possible to extract detailed information about their calls and interactions, making them a powerful model for passive acoustics studies on commercially important species. Toadfishes of both sexes produce a short, pulsatile agonistic grunt, and males produce a “boatwhistle” advertisement call for male-male competition and to attract females. We identify unseen vocal individuals (oyster toadfish O. tau and Gulf toadfish O. beta) near a stationary hydrophone and describe call variability and changes over short- and long-term periods, source levels, call propagation, and directionality. Calls exhibit a directional pattern related to the heart-shaped swim bladder morphology, generating a maximal level behind the fish; grunt frequency spectra allow differentiation of individual callers over multiweek periods. Boatwhistle parameters of oyster toadfish calls change geographically, seasonally, and with temperature, and males call day and night. The Gulf toadfish call rate increases during twilight, when individuals produce shorter and simpler calls. Finally, nearby calling males compete acoustically by increasing their calling rates or producing a grunt (an acoustic tag) during another male's boatwhistle. Toadfishes have been successful models for addressing numerous questions in unseen fish by means of passive acoustics.
Agonistic behaviour and sound production were described for captive Gaidropsarus mediterraneus, a shore-dwelling gadoid. Thump-like sounds were produced during agonistic interactions, which involved disputes over access to shelter sites.
The energetics of mate calling has been studied in insects, frogs, birds, and mammals, but not in fishes. The oyster toadfish, Opsanus tau, produces a boatwhistle advertisement call using one of the fastest muscles known in vertebrates. Because toadfish will not boatwhistle in a respirometer, we measured oxygen consumption after eliciting sound production by electrically stimulating the sonic swim bladder muscle nerve. Induced sounds were similar to a male calling at a rapid rate. Stimulation of the sonic nerve increased the respiration rate by 4060% in males, but they became agitated. Repeating the experiment decreased agitation, and in most fish respiration rates approximated control levels by the second or third replication. Elicited sounds and therefore sonic-muscle performance were similar in all repetitions, hence it appears that the increased oxygen consumption in the first trial was caused by the fish's agitation. Controls indicated that electrode implantation and electrical stimulation of the body cavity did not affect the respiration rate. We suggest that allocation of a small amount of the total energy budget to sound production is reasonable in toadfish, and probably most other fish species, because of the small amount of time that the sonic muscles actually contract and their small size (about 1% of body mass).
The Lusitanian toadfish Halobatrachus didactylus (Bloch & Schneider) (Batrachoididae) is a well-known sound producer that has an unusual large acoustic repertoire for fish. This repertoire consists so far of five distinct sound categories: boatwhistles, grunt trains, croaks, double croaks and a mixed grunt–croak call. Sixteen males that spontaneously occupied artificial concrete nests placed in the intertidal zone of the Tagus estuary (Portugal) were recorded over 8 days in June/July 2006. During the analysis of the recordings new sound emissions were found. Long grunt trains that sounded to the human ear like a running engine were heard. These sounds differ from the normal grunt trains by having a lower amplitude, a much longer duration (tens of seconds versus <1 second) and more grunts per call. Other new sound emissions (e.g. triple croaks) were also registered but were heard less frequently. The incidence of the various sound types is given.
Although acoustically very different, the songs of birds, frogs and insects have many functional similarities, affecting both female choice of mate and male contests. Probable functions of female response to song in certain species are reproductive isolation, enhancement of material benefits or fertility, and improvement of offspring fitness. Ensuring species identity is a likely function of male response to song; estimation of aggressive intentions or resource holding power are other possibilities. -from Authors
Gobies emit sounds during different stages of reproduction, including courtship, pre-spawning events (in the nest) and spawning. The breeding sounds of the painted goby Pomatoschistus
pictus and associated courtship behaviour were recorded in captivity and described for the first time. Males emitted thump-like sounds mainly when displaying alone in the nest and produced drumming sounds outside the nest. Thumps have never been reported for other species of the genus Pomatoschistus. Thumps were short (~80 ms) very-low frequency (below 100 Hz) non-pulsed sounds, whereas drums were longer (hundreds of ms) and consisted of low frequency (~300 Hz) pulse trains. Thump characteristics varied significantly among males but also showed high within-male variability. The frequency of thump emissions and courtship behaviour (total number of courtship displays, lead and nest display) were positively correlated with male size but not with male somatic condition. Thump bursts emitted during nest displays were significantly longer than when emitted with other behaviours. These results suggest that larger males courted females more intensively, both with visual and acoustic displays, than smaller ones.
The mating sounds (boatwhistles) of nesting batrachoidid Halobatrachus didactylus males were recorded in the Tagus Estuary from piers. Thirteen males with 16 boatwhistles per fish were analysed for 20 acoustic features. All variables showed larger between-male than within-male variation and differed significantly among individuals. Discriminant function analyses (DFA) considering seven of these variables assigned 90–100% of boatwhistles to the correct individual, depending on the number of males and number of sounds per male included in the model. The acoustic features that consistently best discriminated individuals were the dominant frequency of the middle tonal segment of the boatwhistle (P2) and dominant frequency modulation, followed by P2 pulse period, amplitude modulation and sound duration. These results suggest the possibility of individual recognition based on acoustic cues.
Secondary sexual characters in many species function both in male-male competition and as cues for female choice. Based on a literature compilation of existing knowledge of traits with this dual function, we propose that they commonly arise through intrasexual selection processes and serve as honest signals to other males regarding fighting ability or dominance. Faking these traits, here called armaments, (i.e. weapons and status badges) is difficult, as they are constantly put to trial in male-male contests. Females that subsequently utilize them as indicators of male phenotypic quality when selecting a partner will benefit by acquiring males of higher quality to father their offspring. Thus, evolution of armaments through male-male competition is seen as a usually initiating process, whereas female choice later may assume a role as an additional selective factor. The reverse, that males use information from traits evolved through female choice, is, however, also possible. The traditional view of independently evolved and temporarily unordered intra-and intersexual selection processes fails to explain dual trait functions. Moreover, our model may more satisfyingly than traditional ones explain how trait honesty and trait genetic variance are maintained: theoretical and empirical evidence suggests that such honesty and variation are more easily maintained under male-male competition than under female choice.
Male courtship acoustic signals from five Lake Malawi cichlid fish species of the Pseudotropheus zebra complex were recorded and compared. Sounds made by males of P. zebra, Pseudotropheus callainos and the undescribed species known as Pseudotropheus ‘zebra gold’ from Nkhata Bay, and Pseudotropheus emmiltos and Pseudotropheus faizilberi from Mphanga Rocks, differed significantly in the number of pulses and in pulse period. The largest differences in acoustic variables were found among the sympatric Mphanga Rocks species that, in contrast to the other three species, show relatively minor differences in male colour and pattern. These findings suggest that interspecific mate recognition is mediated by multimodal signals and that the mass of different sensory channels varies among sympatric species groups. This study also showed that sound peak frequency was significantly negatively correlated with male size and that sound production rate increased significantly with courtship rate.
Male signaling behaviors are often studied in a single context but may serve multiple functions (e.g., in male–male competition
and female mate choice). We examined the issue of dual function male signals in a wolf spider species Schizocosa ocreata (Hentz) that displays the same species-specific signaling behaviors in both male–male and male–female contexts. These signaling
behaviors have been described as either aggression or courtship according to the context observed. We tested the possibility
of dual functions by comparing the relationship between behaviors and outcome of male–male contests (winner/loser) and male–female
mating encounters (mating success). Frequency, rate, and mean duration of signaling behaviors did not vary with outcome of
male–male contests, which appears instead to be based upon relative size and body mass. Winners of contests had significantly
greater body mass than losers, and greater mass relative to opponents was significantly associated with probability of winning.
Overall, signaling rates were much higher in male–female interactions than in male–male contests and were higher for males
that successfully mated than for those that did not mate. Mean duration of some male displays was also greater for males that
successfully mated. However, male size was not associated with probability of mating. Taken together, results suggest an intersexual
selection context for the current function of male signals in these wolf spiders and that increased display vigor is associated
with male mating success.
Many territorial advertisement signals are thought to be dual-function signals, directed to both rival male and receptive
female conspecifics. However, few studies have tested this assumption by examining whether in fact both sexes are likely to
elicit signaling behavior from territorial males. In this study, I experimentally manipulated the social context of male sand
fiddler crabs (Uca pugilator) to investigate the effect of different audiences on the performance of the claw-waving display, a territorial signal that
is often presumed to be directed to both males and females. To test whether males perform this signal to both audiences, I
measured the frequency of waving behavior by focal males when housed in field enclosures alone, with only males, with only
females, or with both males and females. Focal males waved at a low frequency when alone, and the presence of males had no
effect on their level of waving. However, in the presence of females, focal males showed a significantly higher level of waving,
whether or not males were also present. In addition, there was no association between fighting and waving behavior. This experiment
provides evidence that from the perspective of the signaling male, the claw-waving display of U. pugilator is not a dual-function signal but rather is primarily directed to receptive females.
In the Puerto Rican frog Eleutherodactylus coqui, parental care is performed exclusively by males, and consists of attending the eggs and hatchlings at a terrestrial oviposition site. The two major behavioural components of parental care are egg brooding and nest defence against conspecific egg cannibals. Defence behaviour includes aggressive calling, biting, sustained biting, wrestling, and blocking directed against nest intruders. Parental care lasts from oviposition to hatching (17–26 days) and often for several days after hatching. During pre-hatching development, males are present in their nests 97.4% of the time during the day and 75.8% of the time at night. A large portion of this time is spent brooding eggs. In a field experiment, males were removed from their nests and the fate of clutches was monitored. Compared to control clutches (males not removed), experimental clutches had significantly lower hatching success and suffered significantly greater mortality from desiccation and cannibalism. Hence, parental care yields significant benefits to male fitness via increased offspring survival.
Infanticide is an important mortality factor for juveniles in a wide variety of taxa, and is thought to be an important influence on the evolution of pair bonding and parental care of offspring. Many parents, in response to conspecific infanticide, may alter their behavioural aggressiveness towards conspecifics in an adaptive manner to favour their offsprings' fitness. Research on conspecific aggression as an infanticidal counter-strategy by parents, however, has largely focused on mammals and birds. Owing to the almost ubiquitous occurrence of altricial young/parental provisioning of offspring in these taxa, our ability to test comparative hypotheses regarding the initial evolution of parental care is limited. Recent evidence of highly variable social systems within a monophyletic social lizard clade (Egernia spp.) provides an opportunity to further our knowledge in this regard. We examined patterns of aggressiveness towards a conspecific model by females from a wild population of social lizards (White's skink, Egernia whitii), while also documenting the first-year growth and survival of their offspring in the field. Female aggression increased during pregnancy and was maintained at a high level during postpartum periods, relative to aggressiveness during mating periods. We also observed consistent interindividual expression of aggressiveness in females, and offspring from more aggressive female behavioural phenotypes had higher rates of survival, but not growth, over their first year of life. These results suggest that relatively ‘simple’ forms of parental care (i.e. territoriality combined with kin tolerance) may favour offspring fitness and therefore parental care, without necessarily entailing the costs of full parental provisioning of offspring.
Many sonic fishes appear to produce advertisement calls at a lower rate than insects, frogs and birds (song). Fish sonic muscles in many species rank among the fastest in vertebrates, suggesting that acoustic signalling is a costly activity. Surprisingly however, sound production in the oyster toadfish Opsanus tau requires negligible oxygen consumption. Male toadfish produce a long-duration tonal advertisement call, the boatwhistle, and both sexes produce short-duration agonistic grunt calls. The question of what limits the calling activity in fishes has not been addressed. We tested the hypothesis that calling in the oyster toadfish is limited by fatigue of the sonic muscles by stimulating them intermittently at the most rapid rate evoked by playbacks of the courtship boatwhistle call (100 ms every 4 s at 200 Hz = 1.5 s stimulation/min) for 5 min and measured swimbladder movement, sound production and glycogen use. Muscles in both sexes showed almost complete fatigue by 5 min (7.5 s of stimulation), although rested control muscles contained over twice as much glycogen in males as in females. Glycogen use was similar in both sexes, but males used 10.8% of their glycogen and females used 23.2%. Glycogen would support muscle contraction at this rate for 15 min in males during mating call production. It appears that sound production in the oyster toadfish is fatigue limited, which dictates a low rate of spontaneous calling that can be elevated for brief bursts of activity.
A functional analysis of the striated swim-bladder muscles engaged in the sound production of the toadfish has been performed by simultaneous recording of muscle action potentials, mechanical effects, and sound. Experiments with electrical nerve stimulation were made on excised bladder, while decerebrate preparations were used for studies of reflex activation of bladders in situ. The muscle twitch in response to a single maximal nerve volley was found to be very fast. The average contraction time was 5 msec. with a range from 3 to 8 msec., the relaxation being somewhat slower. The analysis of muscle action potentials with surface electrodes showed that the activity of the muscle fibers running transversely to the long axis of the muscle was well synchronized both during artificial and reflex activation. With inserted metal microelectrodes monophasic potentials of 0.4 msec. rise time and 1.2 to 1.5 msec. total duration were recorded. The interval between peak of action potential and onset of contraction was only 0.5 msec. Microphonic recordings of the characteristic sound effect accompanying each contraction showed a high amplitude diphasic deflection during the early part of the contraction. During relaxation a similar but smaller deflection of opposite phase could sometimes be distinguished above the noise level. The output from the microphone was interpreted as a higher order derivative function of the muscle displacement. This interpretation was supported by complementary experiments on muscle sound in mammalian muscle. The dependence of the sound effects on the rate of muscle contraction was demonstrated by changing the temperature of the preparation and, in addition, by a special series of experiments with repeated stimulation at short intervals. Results obtained by varying the pressure within the bladder provided further evidence for the view that the sound initiated in the muscle is reinforced by bladder resonance. Analysis of spontaneous grunts confirmed the finding of a predominant sound frequency of about 100 per second, which was also found in reflexly evoked grunts. During these, muscle action potentials of the same rate as the dominant sound frequency were recorded, the activity being synchronous in the muscles on both sides. Some factors possibly contributing to rapid contraction are discussed.
Guidelines for submitting commentsPolicy: Comments that contribute to the discussion of the article will be posted within approximately three business days. We do not accept anonymous comments. Please include your email address; the address will not be displayed in the posted comment. Cell Press Editors will screen the comments to ensure that they are relevant and appropriate but comments will not be edited. The ultimate decision on publication of an online comment is at the Editors' discretion. Formatting: Please include a title for the comment and your affiliation. Note that symbols (e.g. Greek letters) may not transmit properly in this form due to potential software compatibility issues. Please spell out the words in place of the symbols (e.g. replace “α” with “alpha”). Comments should be no more than 8,000 characters (including spaces ) in length. References may be included when necessary but should be kept to a minimum. Be careful if copying and pasting from a Word document. Smart quotes can cause problems in the form. If you experience difficulties, please convert to a plain text file and then copy and paste into the form.
Attraction of reproductively active, notch tongue females requires both the visual stimulus of a conspecific male and courtship sounds. Neither a silent male nor the sounds, alone, are sufficient to attract females consistently to the nest. These findings are essentially the same as reported by Tavolga (1956) for females of the congeneric, frillfin goby. However, female frillfins responded essentially the same to conspecific sounds and those of a non-familial species (a blenny), suggesting that sound discrimination was not a capability of females. This study demonstrated that female notchtongues discriminated between sounds of their own species and sounds of the related frillfin and those of the distantly related damselfish. This was the sole, important difference existing between the two studies. Recognition of conspecific sounds is likely due to the stutters in the repertoire of courting males. REFERENCES Tavolga, W.N. (1956) Visual, chemical and sound stimuli as cues in the sex discriminatory behaviour of the gobiid fish Bathygobius soporator. Zoologica 41, 49-64.
The plainfin midshipman Porichthys notatus has two male reproductive morphs, ‘Type I’ and ‘Type II’, which are distinguishable by their physical traits alone. Type I males are eight times larger in body mass than Type II males and have a six-fold larger relative sonic (vocal) muscle mass than Type II males. In contrast, the testicles of Type II males are seven times larger than those of Type I males. This study demonstrates morph-specific patterns of reproduction, including acoustic signals, for Type I and II males. Field censuses of nests showed that only Type 1 males maintained nests. Type II males and females transiently appeared in these nests in association with each other. Infra-red video and hydrophone recordings in aquaria showed that Type I males maintained nests and readily vocalized. Long-duration ‘hums’ and sequences of short-duration ‘grunts’ were produced during advertisement and agonistic contexts, respectively. Humming Type I males attracted females to their nests, pair-spawned, and then guarded egg clutches alone. By contrast, Type II males neither acoustically courted females nor maintained available nest sites, but rather ‘sneak-’ or ‘satellite-spawned’ at the nests of Type I males. Type II males infrequently produced low amplitude, short duration grunts that were similar in spectral, temporal and amplitude characteristics to the grunts of females. Type II males appear to be obligate sexual parasites of the nest-building, mate-calling, and egg-guarding Type I males. The dimorphic body and vocal muscle traits of the two male morphs in the plainfin midshipman are thus paralleled by a divergence in their reproductive tactics and the properties of their acoustic signals.