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9 Acoustic Communication in Fishes and Frogs

RANDY ZELICK, DAVID A. MANN, AND ARTHUR N. POPPER

1. Introduction

Many fish and amphibian species use sounds for communication in a wide range of behavioral and environmental contexts. The behaviors most often associated with acoustic communication in both groups include territorial behavior, mate finding, courtship, and aggression. Unlike most other communication channels (e.g., chemical, visual, touch), sound pro- vides a means for long-distance communication as well as for com- munication in areas where there is poor visibility. Both fishes and frogs tend to use fairly broad-band pulsed sounds, although in both groups there are species known to use narrow bands of noise or even relatively pure tones.

Although there are a number of similarities in the uses and features of sound in both fishes and amphibians, direct comparisons between the groups is difficult for several reasons. Of these, the most significant is the substantial difference in what we know about acoustic communication in the two groups. The basis for this difference arises not from the potential breadth of communications involving sounds in the two groups, but more from the difficulties in studying acoustic communication in an aquatic ver- sus a terrestrial environment. An appropriate analogy here might be that the difficulties in studying fish bioacoustics are only paralled by the difficul- ties in studying bioacoustics of marine mammals, while amphibian bioa- coustics parallels the study of bird communication.

The problems in studying fish bioacoustics arise from the difficulty of finding and seeing the subjects of study. While it has been known for some time that the marine environment is quite noisy (reviewed in Tavolga 1971; also see Section 2.1), it still requires a good deal of equipment to record from fishes, and divers or underwater video systems to observe behavior. Even if these problems can be overcome, hydrophones (underwater micro- phones) and underwater observers are poor at localizing sounds in water, and so it is not easy to tell exactly which animal in a group (or even spread over a reef) is a sound producer. Not until very recently, with the limited

363 R. R. Fay et al. (eds.), Comparative Hearing: Fish and Amphibians © Springer-Verlag New York Inc. 1999

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ling egg laying and other reproductive behaviors, and when circulating levels of A VT are high, corresponding with a female who is ready to mate, the release call is inhibited (Diakow 1978). The A VT may act indirectly because it causes release of both prolactin and at least one type of pro- staglandin (Diakow and Nemiroff 1981; Boyd 1992). Prolactin itself will inhibit release calling, and prostaglandin modifies activity in some nuclei that control vocalization. Interestingly, prostaglandin may also have a role in suppressing male advertisement vocalization (Schmidt and Kemnitz 1989).

The male advertisement call is given only during the appropriate season and depends on seasonal fluctuation in circulating androgens. Female frogs obviously have the ability to vocalize. Is the lack of advertisement calling in females due to the basic difference that females lack androgens at the appropriate time of year? Female Xenopus produce a click-train release call, which is modified when adult ovariectomized females are treated with androgens (Hannigan and Kelley 1986). This treatment does not lead to production of a male advertisement call, however. As is the case for many other neural systems, there is a critical developmental window when an- drogens are needed to masculinize the vocal system. If juvenile female Xenopus are implanted with testes (after gonadectomy), they produce upon maturity advertisement calls indistinguishable from males (Watson and Kelley 1992). One component of this ability is the induction of male-type laryngeal muscle, which is in turn controlled by a gene whose expression is androgen-dependent (Catz et al. 1992).

3.6 Plasticity, Diversity, and Information Content

There is no evidence the frogs learn any aspect of acoustic signaling, and it is common to associate such genetically programmed behavior with ex- treme stereotypy. Variations from the stereotyped call are thought to be due simply to unavoidable environmental factors such as temperature (see Section 3.1) or a lack of natural selection to maintain a particular vocaliza- tion parameter constant, perhaps because it is less important in conveying information. This view underestimates the flexibility to convey meaning, which may exist in many anuran vocal communication systems, and has been documented in several. For example, Taigen and Wells (1985) found that male Hyla versicolor produce advertisement calls of varying duration. A longer call is more attractive to females, but producing long calls over a prolonged breeding bout is very costly from an energetic standpoint. Thus males give long calls only when they are competing with other nearby males of the same species. Similar behavior has been seen in other species, and the important point is that to at least a certain extent frogs may adjust their "programmed" calls to particular circumstances. In addition to duration, call rate and call complexity may change according to context (Wells and

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Schwartz 1984). Even call dominant frequency may be modulated. Cricket frogs (Acris crepitans blanchardi) may lower their dominant frequency when they hear another nearby cricket frog. The lowering of frequency seems to signal the resident's ability or willingness to engage in a territorial fight (Wagner 1992). Indeed, although the advertisement call is the most conspicuous type of vocalization, most frogs produce a variety of other sounds that have different meanings and the most common type of nonadvertisement call is that given to maintain a territory (in many species the advertisement call plays the dual role of advertisement and territory maintenance/aggression). Acoustic defense of a resource is common in frogs, and like advertisement calls, specific aggressive vocalizations may be modulated according to context (Narins and Capranica 1978; Schwartz and Wells 1984; Wells and Bard 1987). Furthermore, a given frog may switch between advertisement and aggressive calls to suit the immediate situation. A review of the large variety of call types and their functions may be found in Wells (1977).

In general, it is male frogs who make conspicuous advertisement calls, but this is not strictly true. Female carpenter frogs (Rana virgatipes) pro- duce a vocal response to the acoustic advertisement of male carpenter frogs (Given 1993a). The relatively stealthful existence of most female frogs has surely led to an underestimate of the number of species in which females make vocalizations of communicative significance.

3.7 Radiation Pattern and Habitat Effects

Despite several theoretical studies of environmental influences on sound propagation (for a recent review see Forrest 1994), only a few investigations have focused on specific problems relative to anuran acoustic communica- tion. There are two issues here. First, has natural selection operated on advertisement calls of frogs that are adapted to particular microenviron- ments? Acoustic production could, in principle, be optimized for that particular microenvironment. For different subspecies of the frog Acris crepitans, different call structures characteristic of the subspecies do propa- gate farther in their relative preferred habitats (open vs. forest), leading to the suggestion that selection has· indeed adapted the calls for maximum transmission (Ryan and Wilczynski 1991; Ryan et al. 1991).

Ryan and Sullivan (1989) found that the temporal structures ofthe adver- tisement calls of two toads (Bufo valliceps and Bufo woodhousii) were affected differently by environmental propagation in their natural habitat. If there are reflective surfaces in the environment, the receiver will en- counter an acoustic signal that is temporally degraded due to multipath distortion. The most sensitive parameter of the advertisement call to this distortion is amplitude modulation percent. Depending on the modulation rate and pulse duration, calls of different species may differentially drop

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below the frog's detection threshold for amplitude modulation, and poten- tially then for species recognition, even though they are audible signals.

The second issue is whether a given calling frog selects a location to improve its broadcast. The radiation pattern of the advertisement call must depend, to some extent, on the physical features of the immediate calling site, but in fact there is little evidence that frogs choose a site for its acoustic qualities. Field measurements of calling frogs show that individuals of some species produce a uniform sound field, whereas individuals of other species produce directional fields, with major lobes 5 to 8 dB greater than the minor lobes (Gerhardt 1975). More information on radiation pattern and anuran acoustic active space would be welcome.

3.8 Ecological and Evolutionary Aspects

3.8.1 Species Isolation

The use of frogs to examine principles of evolutionary biology was begun rigorously in the 1950s starting with the work of W. Frank Blair and C.M. Bogert (see, for example, Blair 1958; Bogert 1960). The main focus was to look at frog calls as devices of speciation. Here is the idea: Different species of frogs have different advertisement calls. Indeed, each is referred to as "the species-specific advertisement call." It is inefficient, for several obvious reasons, to mate with the wrong species. Thus natural selection should favor female frogs who can discriminate one species call from that of another, especially if there is a chance of encountering, during the mating season or a time of day, a particular wrong species. Also, there is variation in the advertisement calls of individuals in a given species, and for some related species many spectral or temporal parameters of the call may overlap. Thus ecological theory would predict that in zones of sympatry, where popula- tions of similar species interact, the calls would diverge, and selection would favor those male frogs from both populations with the most different calls and the females best able to discriminate the difference. This divergence is called character displacement. Conversely, where two populations are not likely to encounter each other, there is little selection pressure to have divergence of call parameters. Indeed, when many different species of frogs were analyzed, character displacement in call structure was observed in sympatric zones (Duellman 1967) and, in general, the advertisement call is more attractive to conspecifics than heterospecifics.

Just what is the extent of genetic hybridization in any two frog popula- tions, and what is the effectiveness of one or more mating call parameters in preventing hybridization? Gerhardt has examined this issue extensively in North American hylid frogs. Females of different species are not always very selective about the species of male with which they will breed (Fig. 9.8). For example, H. andersonii and H. cinerea will hybridize, and in fact

388 Randy Zelick, David A. Mann, and Arthur N. Popper

Hy/8 gratiosa Hy/8 gratiosa X Hy/8 cInerrJa Hy/8~ 8

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FIGURE 9.8. Sound spectrograms (sonograms) of two North American Hylids and the spectrogram of a hybrid individual. Note the rich harmonic structure in this call, which, interestingly, extends well beyond the hearing range of either species. For approximately 40 years the spectrograph, which produces this output of frequency composition vs. time and with darkness proportional to intensity, was the standard tool for analyzing animal vocalizations. (From Bogert 1960. © 1960 American Institute of Biological Sciences.)

female H. andersonii will respond to the calls of H. cinerea (Gerhardt 1974). On the other hand H. crucifer and Pseudacris ornata also can hybridize, but reject each other's advertisement calls, and thus appear to have more robust acoustically mediated behavioral isolation. Naturally occurring viable hy- brids of H. chrysoscelis and H. versicolor can be found, but they are quite rare (probably much less than 0.5%) even though mismatings may occur about 7% to 10% of the time (SchIefer et a1. 1986; Gerhardt et a1. 1994a). The interpretation of these results is that hybrids are not particularly fit, genetically, and there should be strong natural selection against mismatings. Why then is the acoustic isolating mechanism not better? Fe- male frogs may not be given a choice insofar as male frogs often attempt to mate with any small animal that moves nearby. Thus while females may be phonotactically attracted only to the species-specific mating call, in a mixed- species chorus encountering a male of the wrong species could result in unavoidable mismating. If this is common, females could in theory avoid heterospecific males by diverting their trajectory when they hear a conspe-

9. Acoustic Communication 389

cific nearby. This notion has recently been tested (Gerhardt et al. 1994a) with three sympatric species of North American hylids. The female hylids did not, in fact, avoid the heterospecific vocalizations. Perhaps the limit of auditory selectivity for the relevant call features has been reached, and these hylids must accept a certain amount of gametic wastage.

3.8.2 Sexual Selection

Despite the imperfect ability of some frogs to select the calls of their own species, much attention has been paid to investigating if female frogs can perform the more subtle task of acoustically judging the quality of a mate of her own species.

Males of nearly all species of frogs fertilize eggs externally, and parental care is certainly not the rule in amphibians. Compared with birds or mam- mals, this makes it difficult to judge mating success. Persistent, careful field work has been successful, however, in showing that indeed some males in a population are more successful at mating than their neighbors (Whitney and Krebs 1975; Licht 1976; Wells 1977). Assuming there is female choice, what male characteristics might a female frog be interested in? Size of the calling male is one obvious feature, because a large male has presumably been able to acquire more food resources, live longer, or both, and thus such a male has desirable genes. A number of studies have examined the notion that males of a larger size are more successful at mating (e.g., Howard 1978; Davies and Halliday 1979), and from these studies we con- clude that indeed size is a factor. Is body size something that a male frog can communicate acoustically to a prospective mate? In both Bufonids (Gerhardt 1975) and Hylids (Fellers 1979) females choose the louder of two otherwise equal advertisement calls and it is the larger males that produce the louder calls. Furthermore, in many species the dominant frequency of the advertisement call is related to body size such that larger males produce lower frequency calls (Loftus-Hills and Littlejohn 1971; Morris 1991) and females can select larger males on the basis of dominant frequency (Ryan 1983b; Morris 1991). On the bases of call intensity or dominant frequency, then, females could assess male size.

In other anuran species, however, size is not correlated with mating success (Sullivan 1982; Passmore et al. 1992; Cherry 1993). In Woodhouse's toad (Bufo woodhousei), painted reed frogs (Hyperolius marmoratus), and the raucous toad (Bufo rangeri) , females are instead interested in the rate at which calls are given, but call rate in these species is not correlated with male size. Indeed, raucous toad males that consistently call at higher rates lose weight faster than other males and are thus unlikely be the largest specimens! What other desirable characteristic might a male communicate with increased call rate?

It has recently been hypothesized that male frogs are selected to have traits that take advantage of female preferences regardless of whether the

390 Randy Zelick, David A. Mann, and Arthur N. Popper

traits convey any accurate information about the male (Ryan and Keddy- Hector 1992; Ryan and Rand 1993). This idea comes from studies that show that females prefer an extreme variant on a relevant call parameter. For example, the North American cricket frog Acris crepitans prefers artificial calls lower in dominant frequency than any natural call (Ryan et al. 1992). Alternatively, females may prefer calling that demonstrates extreme prow- ess (i.e., the highest rate or longest duration).

3.9 Chorusing Behavior

3.9.1 Leks and Satellite Behavior

Female frogs are often not assessing isolated vocalizations. Rather it is a conspicuous feature, especially of temperate zone frogs, to find male frogs calling in a dense temporary assemblage called a chorus (Fig. 9.9). In some cases frog choruses may be considered leks (Ryan 1991; Bourne 1992), a particular type of mating system in which (1) there is an arena (lek) to which females are attracted, (2) the females choose males at the lek, but (3) the males control no resources of interest to the female at the lek (Bradbury 1981). A fourth criterion is the absence of male parental care. Indeed, in most frog species the only contribution males make to reproductive success is to provide gametes, and the other conditions for lekking are probably satisfied in many frog choruses as well. The significance of lekking in frogs is not clear, except that it is now known to occur in all vertebrate classes, but only sporadically. If frogs are found to satisfy the criteria for lekking on a widespread basis, more information as to the value of this mating system will accrue. Frog acoustic behavior as a model system to investigate the evolutionary significance of leks has already yielded rewards, as it has been shown that female choice can be based on a "direct" or immediate improve- ment rather than a genetic improvement of fitness (Bourne 1993).

It is clear that one of the main determinants of male reproductive success is the amount of time a male frog spends calling in a chorus (Ritke and Semlitsch 1991; Murphy 1994a,b; Townsend and Stewart 1994). For a male frog, probability favors attracting a mate if the male has a greater presence in the chorus. Thus we can define a supermale frog as having the lowest dominant frequency (see above), the highest call rate, the longest call duration, the loudest call, and the greatest persistence over days in the chorus. All of this effort comes at a great energetic cost, however, as will see below. It is interesting that for the last feature, persistence would work to a male's benefit if females arrive at the chorus at unpredictable, infrequent intervals. This advantage accrues because the probabilistic nature of en- countering females simply favors males who are more commonly adver- tising. It is also possible that a female could instead make an assessment over a relatively prolonged period (days). There is a small amount of data

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FIGURE 9.9. A variety of different frogs species may aggregate to form a mixed- chorus. Each has a preferred calling perch. Clockwise from upper right: Hyla femoralis, Hyla squirella, Hyla cinerea, Bufo quercicus, Microhyla carolinensis, Acris gryllus, Bufo terrestris, Rana pipiens, Hyla gratiosa. (From Bogert 1960. © 1960 American Institute of Biological Sciences.)

suggesting this is true (Sullivan 1990; Dyson et al. 1994) and more data on this topic would be welcome.

Not all the males in a chorus give advertisement calls. Most often, it is smaller males that do not call, yet they will still attempt to mate with females moving toward calling males. This sort of sexual parasitism is termed satellite behavior (Miyamoto and Cane 1980; Perrill et al. 1982). Both satellite and regular calling males are successful at mating (Forester and Lykens 1986; Ovaska and Hunte 1992). Driving satellite behavior is the advantage of not competing for calling sites, and/or reducing energetic costs associated with calling. Although the energetic argument is sensible, as yet there is no evidence that satellite males are physiologically weaker than other males who do call (Lance and Wells 1993). Lucas and colleagues (1996) have modeled the advantage to becoming a satellite male using the following hypothetical calling pattern: In their first year males do not call, in

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the second year they participate in the chorus, and in their third year die of old age. For first-year males, with less energy reserve, the optimum strategy is to call initially then switch to satellite behavior. Second-year males should continue to call and not become satellites. An interesting further effect that emerges from the mathematical model is alternating nights of calling, such that the chorus may be present one night and not a subsequent night, without prolonging the entire seasonal length of the chorus. It is interesting that the results of the model fit well the observed dynamic behavior of many temperate frog choruses.

3.9.2 Temporal Aspects of Chorus Life

When motivated, a male frog in isolation commonly produces advertise- ment calls at a more or less regular rate. Typical values range from one call per second to one call per several minutes. This nominal rate is controlled by a midbrain neuronal oscillator (Schmidt 1992). When two calling frogs can hear each other, however, very particular changes in the timing of calls may occur such that there is synchronization or alternation of calls. There have been numerous studies of these temporal interactions addressing the three basic issues: the extent to which frogs alternate or synchronize, the reason this might be important, and the mechanism of alternation or synchrony.

In at least some species, the timing of this oscillator is rapidly adjusted based on nearby acoustic events, such as the calls of neighbors (Zelick and Narins 1985; Schwartz 1991). The adjustments allow entrainment, which yields two observed outcomes: synchronization in which calls partially over- lap, or alternation causing the perception by a human observer of dueting or antiphonal calling. In some cases the synchronization is fast enough that the calls of one individual almost completely overlap with those of a neigh- bor (Tuttle and Ryan 1982; Ryan 1986).

It is likely that both alternation and synchrony are two extremes of a single continuum and both share the same mechanism. Evoked calling is common in frogs, and the finer ability to rapidly adjust the neural call oscillator, allowing tracking of even randomly placed acoustic events (Zelick and N arins 1985), could grow out of this simple behavior. A particu- lar delay relative to the acoustic trigger will yield the appearance of either synchrony or alternation. Interestingly, the original selective pressure to allow rapid adjustments in call oscillator timing may have been a female's inability to localize or judge overlapping or massed calls (Greenfield 1994). If the female prefers the leading call, simply on grounds of ease of localiza- tion or feature detection, then every frog would want to lead. One strategy to be a leader is to abort a call that is scheduled to coincide with your neighbor, and try again after an interval. This sort of communication strat- egy is not unlike modern packet transmission protocols of computer networks.

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Call alternation or at least avoidance of temporal overlap has been seen in many frog species (Lemon 1971; Loftus-Hills 1974; Rosen and Lemon 1974; Awbrey 1978; Lemon and Struger 1980; Narins 1982; Schwartz and Wells 1983; Given 1993b), and one might assume a common obvious signifi- cance to the behavior. A reasonable presumption is that alternation avoids the deleterious alternative, namely jamming your neighbor's calls. Is there evidence that female frogs have difficulty localizing male frogs when their calls overlap? While this is widely assumed to be true, in at least one case females were found to accurately localize calls played from speakers even if there was complete overlap (Passmore and Telford 1981). Rather, it may be that call alternation is more important for (1) detection of fine-temporal structure within the call and (2) male-male spacing and territory maintenance. Calls that overlap in time and have particular pulses or trills within them will have those temporal patterns obscured by overlap (Schwartz 1987; Sullivan and Leek 1987; Given 1993b). Relative to acoustic territory maintenance, if a male frog is less able to hear another male's calls during, and for a short period after he vocalizes, it would be advanta- geous for neighbors to call following this refractory period . In this way the nearest neighbors maximize their own detectability (Schwartz 1987; Given 1993b ).

Call alternation also occurs in mixed-species choruses. The Central American frog Hyla ebraccata calls in dense choruses with other H. ebraccata males but also with Hyla microcephala males. Female H. ebraccata are less attracted to male H. ebraccata calls when the male H. ebraccata calls overlap H. microcephala calls (Schwartz and Wells 1984, 1985). H. ebraccata males normally alternate calls with H. microcephala and presumably increase their chance of mating.

The issue of male-male spacing in a chorus is an interesting one. Male frogs are often aggressive toward con specific males; thus, a balance must be struck between the tendency to be aggressive and the need to participate in the chorus. This is particularly true when the density of calling males and their vocal activity is high. As the number of frogs in a chorus increases, one would expect that if male-spacing and aggression are regulated by acoustic cues, then the chorus boundary should grow so that chorus density would stay the same. In fact, the density of the chorus increases (Fellers 1979; Gerhardt et al. 1989; Dyson and Passmore 1992). What happens in choruses when the density of males increases? If the chorus has males which alternate calls, then only the nearest neighbors will alternate and further neighbors are ignored (Brush and Narins 1989; Schwartz 1993, 1994). In addition, the tolerance threshold for aggressive behavior increases. This is a compromise because time spent in aggressive interactions lessens the time available for advertisement calling (Wells 1988). In such choruses density can only in- crease to a point (Narins 1982). In the case of H. marmorata choruses, in which males do not alternate calls, the regular spacing of calling frogs at low densities becomes random at high densities (Dyson and Passmore 1992). In

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these densest of choruses females can still find males because they seem to attend to a local set of males. While females prefer spaced males, they can still localize and evaluate more crowded calling frogs (Telford 1985; Gerhard and Klump 1988; Brush and Narins 1989).

It is clear that there are advantages to alternation of calls, but what is the advantage of synchrony? There is one case where it appears to be adaptive to synchronize calls: The tropical frog Smilisca sila produces advertisement calls spaced widely in time (about one call every minute) and there is no obvious rhythm in the calling. Due to the ability of Smilisca to rapidly track acoustic signals (with an evoked call delay as short as 55ms!), the calls of neighbors sometimes overlap almost completely. This behavior makes a given frog more difficult to localize by a predatory bat, which uses the frog's call as a homing signal (Tuttle and Ryan 1982; Ryan 1986). Antiphonal calling can also depend on very short latencies of around 60ms (Walkowiak 1992), and more work should be done on the neuronal bases of these fast non-reflex behaviors.

Finally, there is the case of H. microcephala males, which permit gross temporal overlap of calls with neighbors but in a very specific way (Schwartz and Wells 1985). Each call is composed of a series of pulses and the overlapping calls are temporally positioned so that individual pulses of one call and those of the neighbor's call interdigitate. Again such behavior requires remarkably precise triggered oscillator timing.

3.10 Costs of Communication

3. 10.1 · Energetic Costs

Displays used for mating advertisement can be essentially free. For ex- ample, the colorful plumage of birds and other animals does not represent a significant energetic cost to make or maintain. Acoustic displays are another matter, however. The long-term acoustic output of a frog is propor- tional to the power in each note of the call, the duration of the notes, and the rate at which notes are given. In most cases frogs do not modulate the intensity of their calls, and from a theoretical standpoint they should call at the highest rate sustainable if calling effort is correlated with mating success (Ryan 1988).

Interestingly, the first study to examine the energetic cost of calling in frogs was done on the same species for which another very interesting cost of display has been studied. Bucher and colleagues (1982) placed calling male Physalaemus pustulosus, a small (2g) Central American frog, in respirometer chambers and measured the oxygen consumption during rest- ing and calling periods. They found that the mean energy expenditure of calling males is twice the expenditure during resting. In other words, adver- tisement calling is costly! Interestingly, at higher call rates, the energetic

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cost per call goes down, possibly because air is shuttled more efficiently between the lungs and vocal sac.

Frogs that give more intense calls spend even more energy on advertise- ment. The gray treefrog (Hyla crucifer) produces extraordinarily intense calls of around 1l0dB (re: 20IlPa) at 50 cm, and makes over 1200 such calls per hour. This is sustained for 2 to 3 hours each night (Gerhardt 1973; Rosen and Lemon 1974). A 10-g gray treefrog may, just by calling, increase its energy expenditure from a resting value of 13 joules/hour to near 300 joules/hour (Taigen and Wells 1985; Wells and Taigen 1986). Thus it is not surprising that male frogs, but not female frogs, lose considerable body mass over a breeding season (Grafe et al. 1992) and that the number of hours during which a particular frog chorus is active declines throughout the breeding season (Runkle et al. 1994).

The high metabolic cost of sound production implies further that calling is not very efficient, and indeed this seems to be true. Prestwich (1994) estimates an efficiency (acoustic power/net metabolic power) of between 0.05% and 6.0%, considerably less than the efficiency of locomotion, which has an efficiency between 10% and 20%, and for which the frog uses less total energy. Finally, the number of calls given per unit time is also temperature dependent and varies linearly with oxygen consumption (Wells et al. 1996). Thus the metabolic cost of calling increases with ambient temperature.

3.10.2 Predation Costs

Predators use all sensory means available to them to locate potential prey items. Thus in many cases organisms have become extremely stealthful, using such techniques as cryptic coloration, to avoid becoming a meal. This poses a problem for intra-specific communication, because it is at the same time impossible to be entirely cryptic yet broadcast information about yourself. One of the most elegant studies of the evolutionary consequences of incidental communication to a predator involves the same Central American frog described above, Physalaemus pustulosus (Ryan 1985). This frog gives an advertisement call of variable complexity. The first part is a frequency modulated "whine" and is always produced. The second part is one to six harmonically rich "chucks." Females are attracted to the whine, but are more attracted to the whine plus chucks. Thus natural selection should favor males who append lots of chucks onto their whines. Unfortu- nately for Physalaemus, the bat Trachops cirrosus is a predator who finds the calling males by listening to their advertisement calls. Presumably be- cause of the broad frequency spectrum of the chucks, the bats more easily localize frogs producing chucks compared with those that produce only whines. Thus there is competing selection pressure on the frogs to produce no chucks. The compromise is that when males do not detect conspecifics calling, they produce only whines. Without competition from other

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Physalaemus, they will be attractive enough to females. In the presence of other calling males, however, the males begin adding chucks, balancing the need to be more attractive than their neighbors with the increased likeli- hood that they will be eaten by a bat.

3.11 Physical Environmental Factors

Amphibians find themselves in a special situation with regard to their environmental physiology. Amphibians are ectothermic, thus they have only behavioral means to regulate their body temperature. In practice the body temperature of most terrestrial frogs is not well controlled and this has consequences for acoustic communication. In addition, while nearly all species of frogs and toads are terrestrial as adults, they have no skin barriers to water loss and indeed lose water at the same rate as a free surface of water of the same surface area (Shoemaker et al. 1992). Terrestrial amphib- ians must thus contend with both temperature and serious dehydrational stress.

3.11.1 Temperature Effects

Reptiles are well known for behaviors such as basking and making postural changes to regulate their body temperature (Avery 1972). On theoretical grounds it should be less advantageous for amphibians to bask because they, unlike reptiles, cannot use basking to maintain a body temperature much higher than the ambient air temperature: as the amphibian warms up, evaporative cooling compensates for the thermal radiation. As a conse- quence frogs are best considered eurythermal, that is, operating as well as possible over a wide range of temperatures (Putnam and Bennett 1981; Renaud and Stevens 1983). This strategy can work because, compared with most reptiles, frogs tend not to be active foraging predators, instead using a sit-and-wait strategy for obtaining food.

Although not as useful as for reptiles, there are nevertheless some frogs that do seem to behaviorally thermoregulate by basking in the sun. Mem- bers of three families of anurans (Ranidae, Hylidae, and Bufonidae) have been observed to bask in the wild and in some cases shuttle between a sunlit bank and the water during the day to maintain a high temperature (Lillywhite 1970; Valdiviesio and Tamsitt 1974; Carey 1978; Bradford 1984). Compared to the small number of field observations, there are nu- merous lab studies showing that both larval (tadpoles) and adult amphib- ians select preferred body temperatures (for review see Hutchison and Dupre 1992). The difference between the field and laboratory data may be explained by a cost-benefit analysis. In the wild, behavioral means of body temperature regulation only seems to occur when it is not very costly. Thus a lizard might move from shade to sun if this is a relatively short distance,

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but the lizard will not climb a 10-m tree to find sun (Withers and Campbell 1985).

For acoustic communication the expected consequence of these tempera- ture effects is for one or more call features to vary with temperature, and sometimes in the range of temperatures within which the frog must defend a territory or advertise for a mate. Clearly such temperature variation in call parameters could create problems for female frogs attempting to find a male of the correct species when the localization is based on that male's call!

As a rule the spectral parameters of frog calls do not change greatly with temperature (Blair 1958; Lorcher 1969; Heinzmann 1970; Schneider and Eichelberg 1974). The temperature 010 for the spectral features of a num- ber of frogs and toads is approximately 0.2, which suggests remarkably good stability. For comparison, a typical value for the change in vertebrate nerve conduction velocity with temperature is 1.8, or nine times larger (Schmidt- Nielsen 1993).

Despite the small changes in vocalization carrier frequency with temperature, several studies have examined this effect in relation to the frequency tuning of the peripheral auditory system. Ideally, any temperature-dependent change in the male's call carrier frequency should be matched by an equal change in female preference, given two important assumptions. First, it must be the case that both females and the males they are trying to find are at the same temperature. If there are micro environ- mental differences between male calling sites and the paths females take to find the males, the usefulness of temperature matching is questionable. Second, we assume that a given temperature-dependent feature of the male's call is important for the female in terms of localization and/or judg- ment of quality. Perhaps the most labile call parameter will respect to temperature is pulse or trill modulation rate. For this parameter the female's preference for the species-specific advertisement call shows a matched temperature dependence: Colder female gray tree frogs (Byla versicolor), for example, prefer male calls that have a modulation pulse rate expected from a cold male, and warmer females prefer the pulse rate associated with a warmer male (Gerhardt 1978; Gerhardt and Mudry 1980).

3.12 Genetic Coupling of Sound Production and Generation

The temperature coupling experiments described above suggest a close association between the vocal control system and the sound detection sys- tems of anurans. Such an association has been more directly demonstrated in experiments where hybrids of two different frog species (Byla chrysoscelis and H. femoralis) were made by artificial crossing (Doherty

398 Randy Zelick, David A. Mann, and Arthur N. Popper

and Gerhardt 1984). Such hybrid males produce a call that is intermediate in temporal modulation properties, and it is this hybrid call that female hybrids find more attractive, when given the choice between it and either of the parental-type calls. Figure 9.8 shows a similar situation from one of the first documented records of hybridization effects on vocalization. Thus there is a genetic linkage between the sound generating portions of the frogs brain, and those involved in recognizing important features of another frog's vocalizations. This is similar to the situation described for insects with acoustic communication such as crickets (Hoy et al. 1977). Interestingly, the fact that hybrids reveal themselves as acoustic intermediates has also been used as a tool to verify the occurrence of natural hybrids (Gerhardt et al. 1994b).

It is interesting that some of the coupling between the sender and receiver comes about because of mechanical morphometric factors. Wilczynski and colleagues (1993) found that in three related species of hylids both the temporal and spectral features of the advertisement call change with head and laryngeal muscle size, the latter being characteristi- cally different in the three species. Head size, as it relates to outer and middle ear structure size, also defines the preferred transmission of sound to the inner ear. Thus a female of a larger species will prefer sound gener- ated by a male of the larger species, etc.

3.13 Conclusions

There is now quite a large amount of behavioral data on frog acoustic communication. Studies of the underlying neural substrates is lagging. For example, frogs would be ideal for examination of the neuronal processes involved in making context-dependent judgments, as is . done when call types are switched following detection of a particular acoustic cue. In the area of ecology and evolution of signaling and mating systems, again we know much but there are interesting issues to be resolved. For instance, sometimes variation in call parameters is linked to female choice and mat- ing success, but in other cases there is no link. Why should this be so? Furthermore, in some cases female frogs are interested in extreme variants of the advertisement call, but in other cases females are both behaviorally and neurophysiologically "tuned" to a particular value of a parameter (such as trill rate). Finally, more work would be welcome providing field data on hormonal variation during such social activities as aggression, mating, and advertisement calling with the notion of learning the interplay between endocrine modulation and the operation of a frog's acoustic communica- tion paradigm. Recent work on a voiceless frog with male parental care (Emerson et al. 1992) is a good example as are the very nice studies of Walkowiak (e.g., Walkowiak and Luksch 1994).

9. Acoustic Communication 399

4. Summary

This chapter has presented overviews of what is known about sound communication by two of the major vertebrate groups, bony fishes (there are no indications that cartilaginous or jawless fishes produce sounds) and frogs. It is apparent from this overview that considerably more is known about sound communication in frogs than in fishes, and much of the explanation for these differences result from the problems associated with studying acoustic behavior underwater. Moreover, the investigators work- ing on frogs can benefit not only from the relative ease of studying their species, but also from the methodology developed for parallel studies in birds.

For the most part, investigators interested in fish communication would like to be able to ask many of the same questions that have already been asked about frogs. Important questions concerning intraspecific and inter- specific variation in calls, effects of selective pressure on sound content, and detailed analyzes of male-female interactions and the use of sounds that have been so elegantly answered for frogs need to be investigated for fishes. While it is improbable that the sounds produced by fishes are learned, there have been no hybridization studies on fishes, as there have been for frogs. Finally, while much is known about the energetics offrog sound production, nothing is known about fishes. How much energy does it take for a midship- man to contract its sonic muscles and produce sound for hours?

Perhaps the one area in which fish acoustics investigations lead those for frogs is in the understanding of sound detection (see Fay and Megala Simmons, Chapter 7) . Since fishes are far more amenable to conditioned behavioral investigations of hearing capabilities than frogs, we have a good sense of the kinds of sounds fish can detect and discriminate. Although we still need more data for sound-producing fishes, far fewer data are available for frogs due to the inherent difficulty of training frogs to respond behavior- ally in the presence of sounds. This does not mean, of course, that we don't know a good deal about frog hearing. Indeed, as described by Fay and Megala Simmons (Chapter 7) and Lewis and Narins (Chapter 4), we know a good deal about what frogs hear, and both peripheral and central (McCormick, Chapter 5) mechanisms and structures associated with sound detection. Research on the neurophysiological bases of alternative mating tactics in fishes is one area in which studies on fish communication can provide a guide for future studies in frog communication.

At this point, investigations of fish acoustic communication lags behind that of frog acoustic communication. With the advent of new techniques, one would hope that more extensive and sophisticated data will become available for fishes. Indeed, with fishes being by far the largest of all verte- brate groups (e.g., 25,000-30,000 extant species), it would be a wonder if fishes did not only parallel many of the behaviors seen in frogs, but

400 Randy Zelick, David A. Mann, and Arthur N. Popper

also demonstrate a range of behaviors and uses of sound that are vastly different.

Acknowledgments. R.Z. expresses thanks to C. Cookus for library assis- tance. The authors thank Drs. Richard R. Pay and William N. Tavolga for reading and commenting on a draft of the manuscript. Preparation of this chapter was supported in part by National Institutes of Health (NIH) training grant DC-00046-02 from the National Institute of Deafness and Other Communicative Disorders to D.M.

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