Male Frogs Research Articles

Dynamic bimodal signal evokes fighting behavior in a dart-poison frog

As a neuroethologist, Bob Capranica strongly encouraged his students to study animals in their natural habitat in order to truly understand the behavioral rules underlying acoustic communication. This study was one of many inspired by those lessons. Male anuran vocalizations serve to attract conspecific females and to regulate male spacing through territorial interactions. In response to playback of a conspecific call, some male frogs have been reported to alternate their call with the perceived stimulus or shift their call-dominant frequency to avoid acoustic interference, or add call notes to signal an increased state of aggression. In some species, males orient toward the sound source followed by physically approaching the loudspeaker. Although natural fighting behavior between conspecific males has been observed in the field, it has not heretofore been possible to elicit with loudspeakers broadcasting sounds. In this playback study of the Brilliant-thighed dart-poison frog (Epipedobates femoralis) in French Guiana, we used an electromechanical model to provide realistic bimodal cues (acoustic and visual) to calling males. Our data suggest that agonistic behavior could be evoked in territorial males only when both acoustic and visual cues were presented simultaneously. [Work supported by grants from NIH (PMN) and Austrian Science Foundation (WH).]

More bang for your buck: the effect of caller position, habitat and chorus noise on the efficiency of calling in the spring peeper

Many animals use acoustic signals as a means of intra- and inter-specific communication. For example, male anuran amphibians produce advertisement calls to attract females for breeding, and as a territorial signal. The production of acoustic signals can be energetically costly, and the distance over which a signal is effective depends on a range of variables including the location of the caller and receiver, ambient conditions and the habitat through which the sound travels. This paper presents a spatially explicit model of the propagation of an anuran advertisement call across a landscape, using the example of the northern spring peeper Pseudacris crucifer crucifer. The model is used to investigate (a) the effect of habitat, caller position and chorus noise on the effective distance of a call with a frequency of approximately 3 kHz; and (b) the energetics and efficiency of calling at different intensities and from different locations in the landscape. Calling next to still water or from an elevated perch increases, while calling in a chorus decreases, the distance over which a female can distinguish an individual male's call. For a given call intensity and calling rate, a male spring peeper will get the greatest “bang for its energetic buck” if it calls next to still water in the absence of chorus noise. However, when a chorus of spring peepers is gathered at a pond, calling from an elevated position away from the pond (and the chorus noise) will maximise the effective distance of an individual call, although this may entail other costs. The model presented here is the first realistic, interactive mathematical model of the propagation of animal sounds across a landscape, and uses a gis interface to display the effect of habitat and caller position on animal communication. It has applications for both research and teaching, and a copy can be obtained free of charge by contacting the author.

G and C banding show structural differences between the Z and W chromosomes in the frog Buergeria buergeri.

G and C banding studies were made on cultured blood cells of matured male and female Buergeria (B.) buergeri frogs. The Z is subtelocentric and the W is submetacentric. There is a satellite near the end of the long arm of the Z. Constitutive heterochromatin is seen near the proximal and distal portions of the long arms of both Z and W. A single heavily stained G band is seen in the short arm of Z, while one or two heavily stained G bands are observed in the short arm of W. The Z may have originated through a process, in the course of which parts of W have been translocated to Z.

Sound duration as a perceptual cue influencing vocal behavior of male bullfrogs

Female frogs of several species use the temporal cue of sound duration to aid in mate choice. Little is known, however, about the sensitivity of male frogs to this cue. Male bullfrogs emit a complex advertisement call to attract females for mating, and to announce territory occupation to other males. In two experiments, the sensitivity of vocalizing male bullfrogs to field playbacks of advertisement calls differing in duration was examined. The number and latency of evoked vocal responses to the stimuli was used as a measure of perception. Males responded with fewer calls, at longer latencies, to stimuli shorter in duration than the standard signal (with a duration at the mean value for the species). Males preferred stimuli longer in duration than the standard signal, responding with more calls at shorter latencies. They did not, however, significantly lengthen their own calls in response to playbacks of long duration signals. This preference for ‘‘supernormal’’ stimuli may be an important factor mediating the evolution of communication signals. [Work supported by NIH.]

Environmental Estrogens and Reproductive Biology in Amphibians

In this paper, the effects of an estrogenic compound, 4-nonyl-phenol (NP), on the amphibians Rana esculenta and Triturus carnifex are described together with those on sexual differentiation in Xenopus laevis. NP increased plasma vitellogenin in male frogs and newts in a dose-related manner; moreover, inhibitory effects on gonadotropin and prolactin (PRL) secretion by pituitary were found together with an elevation of plasma androgens. NP treatment also caused a remarkable increase in number of prolactin-immunolabeled cells, suggesting that xenoestrogen might induce, at least in the newt pituitary, a PRL accumulation possibly due to a reduction of the hormone release. In addition, both NP and bisphenol A caused feminization by increasing the percentage of female phenotypes in X. laevis, and the in vivo effects were more pronounced than those of estradiol-17β.

Socially Mediated Pitch Alteration by Territorial Male Bullfrogs, Rana catesbeiana

Acoustic communication signals play important roles in aggressive social interactions between male anuran amphibians (Wells, 1977). For example, a number of studies demonstrate that male frogs behaviorally discriminate between two conspecific signals that differ in size-related spectral properties during conflicts over mates, calling sites, or territories (Davies and Halliday, 1978; Arak, 1983; Ramer et al., 1983; Given, 1987). In anurans, spectral call properties, such as dominant or fundamental frequency, are usually negatively correlated with body size because of morphological constraints on the sound producing apparatus (Martin, 1972). Because larger male frogs typically win fights against smaller males (e.g., Howard, 1978; Arak, 1983; Given, 1988), spectral properties of frog calls are often cited as a classic example of an honest, unbluffable signal of fighting ability (Wiley, 1983; Alcock, 1998; Bradbury and Vehrencamp, 1998). In playback tests, male frogs are often more likely to persistently attack sources of the high-frequency calls of simulated small males, whereas they typically stop calling or abandon their calling sites in response to the low-frequency calls of a simulated large opponent (e.g., Davies and Halliday, 1978; Arak, 1983; Wagner, 1989). There is growing evidence, however, that spectral properties of frog calls may be plastic, especially during social interactions among competing males. Lopez et al. (1988) first demonstrated frequency alteration in white-lipped frogs (Leptodactylus albilabris), in which males increased or decreased the dominant frequency of their calls to match that of a nearby male. Wagner (1989, 1992) and Bee and Perrill (1996) demonstrated, respectively, that male cricket frogs (Acris crepitans) and green frogs (Rana clamitans) reliably decreased the dominant frequency of their calls during simulated aggressive interactions over calling sites. Males of the erspect. Plant Ecology and Evolutio ary System-

RESPONSE TO VARIATION IN CHUCK FREQUENCY BY MALE AND FEMALE TÚNGARA FROGS

We examined how male and female tungara frogs, Physalaemus pustulosus, respond to variation in the frequency spectrum of the chuck component of the advertisement call. We varied chuck frequency in two different ways. In the fixed frequency series, the sequence of calls within each series had chucks of the same dominant frequency. Different fixed-frequency series had chucks of different dominant frequencies designated as high, high–medium, medium, medium–low, or low frequency relative to variation in the test population. In the second varying frequency series, the sequence of calls varied in the chuck's dominant frequency such that the individual series had the same average frequencies as the high, high–medium, medium, medium–low, and low fixed-frequency experiments. Both males and females tended to respond more to lower-frequency chucks. The responses of both sexes to the same mean chuck frequency was similar to the fixed- and varying-frequency series of chucks.

The absence of species and sex recognition during mate search by male common toads, Bufo bufo

During mate search male Bufo bufo do not discriminate between green frogs and conspecifics, between sexes or between gravid females that differ in body size. We studied mate recognition and the mating behaviour of male European common toads, B. bufo using field-based choice experiments. When given a simultaneous choice between R. perezi and B. bufo both matched in size, male toads did not discriminate between species and amplected a frog or a toad with equal frequency. When a male toad amplected a frog, the frog uttered a release call but the toad did not release the frog and the amplexus lasted from several seconds to a few minutes. Usually frogs fought to release the male toad but test toads were tenacious and usually attempted several times to clasp the frog when the frog slipped away from toad. When given a simultaneous choice between a male and a female of equal size, males did not discriminate between the sexes and attempted to amplex a male or a female with equal frequency. When a test male clasped a stimulus male, the stimulus male uttered a specific release call that caused the test male to release the stimulus male. Male-male amplexus never lasted more than 3 sec, and consequently, the search cost associated with mating with the wrong sex was relatively low. Males did not discriminate between gravid females that differed in body size. Moreover, there was no assortative mating by size. Male-female amplexus was tenacious and prolonged in the three experiments.

Spatial Relationships of Male Green Frogs (Rana clamitans) throughout the Activity Season

Abstract The spatial relationships exhibited by individuals in a population may indicate their social organization. In territorial species interactions between individuals should lead to maximal spacing in a uniform pattern. Using nearest neighbor distances (NND), I tested for territoriality in the green frog (Rana clamitans) by determining if males were uniformly dispersed within breeding choruses. Observed dispersion patterns were not consistent with territoriality. Males were randomly dispersed on all seven nights during the breeding period, four of five nights during the nonbreeding period and uniformly dispersed on one night during the nonbreeding period. Dispersion did not differ between periods although density was higher and NND was smaller during the breeding period. There was also no correlation between male size and NND. The disparity of my results might be explained by differences in male density and resource distribution and its effect on habitat quality since these factors influence behavior...

Responses to synthetic advertisement calls by lake frogs from western Anatolia

Bioacoustic and morphological measurements suggest that the lake frog, Rana ridibunda, may represent different species or subspecies over its wide geographic range. Vocal responses from male lake frogs from western Turkey were analyzed in response to laboratory playbacks of synthetic advertisement calls of lake frogs from Turkey, Israel, and Greece. Lake frogs in Israel (Rana bedriagae) and Greece (R. balcanica) are thought to represent different species. Stimuli varied in the number of pulse groups in each call. Males responded most vigorously to playbacks of the R. bedriagae call. In contrast, males rarely responded to the calls of R. balcanica, and never responded to the calls of Hyla cinerea. Males preferred stimuli with more rather than fewer pulse groups. These observations may be used in the classification of Turkish R. ridibunda populations.

Bidder's organ of Bufo ictericus: a light and electron microscopy analysis

Male toads of the Bufonidae Family have rudimentary ovaries designated Bidder's organs, and if the testes are removed this organ develops into a functional ovary, representing a morphological strategy for the reproduction of the species. The Bidder's organ of Bufo ictericus was examined using routine and histochemical techniques by light microscopy and transmission electron microscopy. Each Bidder's organ presented a typical ovarian morphology, being composed of a cortex and a medulla. Bidderian follicles in different stages of development were visualized in the cortex, where they are better developed. The germ cells exhibit a large oocyte with a round-shaped nucleus. The Bidderian follicles are supported by a loose net of reticular fibers. In the medullar region, collagen fibers were immersed in the matrix rich in blood vessels that also contained a small quantity of neutral glycoproteins rich in hexose and/or sialic acid and carboxylated polymers with a characteristic distribution of glycosaminoglycans. The oocyte and the follicular cells were separated by a narrow space containing microvilli. The oocyte exhibit a well developed smooth endoplasmic reticulum, a poorly developed Golgi apparatus, and occasional lysosomes. Concentric cisternal complexes are often visualized; however, their morphological significance remains unclear. The peroxisomes display a fine granular matrix without a crystalline core, with a weak 3,3′-diaminobenzidine-reaction. Intimate association between peroxisomes, peroxisomes and lipid inclusions was observed in the oocyte, suggesting its participation in yolk metabolism.

Territorial male bullfrogs (Rana catesbeiana) do not assess fighting ability based on size-related variation in acoustic signals

Some animals use communication signals to assess their opponent’s size and fighting ability during aggressive conflicts. Male frogs assess their opponent’s size based on the fundamental frequency (pitch) of advertisement calls, which is negatively correlated with body size, an important determinant of fighting ability in frogs. I conducted a field playback experiment to investigate whether territorial male bullfrogs assess the size of opponents based solely on size-related variation in fundamental frequency. I repeatedly broadcast synthetic bullfrog advertisement calls to three groups of males. Playback stimuli simulated a large male (n 24), a small male (n 24), or an acoustically size-matched male (n 34). Neither the simulated size of the opponent, the subject’s own size, nor the degree of size asymmetry between the subject and simulated intruder had significant effects on the magnitude of responses during the playback test or on the rate of habituation that occurred with repeated stimulation. Post-hoc analyses of effect sizes and statistical power indicated that the effects in this study were quite small compared to previous studies in other frogs. More important, power analyses indicated that this study had high power (1 0.90) to detect the magnitude of effect sizes observed in previous studies. Thus, territorial male bullfrogs do not appear to assess an opponent’s fighting ability based solely on the fundamental frequency of acoustic signals. These results contrast starkly with theoretical predictions and previous empirical work with frogs. Key words: bullfrogs, communication, fighting ability, Rana catesbeiana, size assessment, territoriality. [Behav Ecol 13:109–124 (2002)]

Non‐random pairing with respect to past breeding experience in the common toad (Bufo bufo)

AbstractA 20‐year study of a common toad Bufo bufo population in south Dorset, U.K. was carried out between 1980 and 1999. On average, c. 33% of all experienced males and females arriving each year did so during the first quarter of each breeding season with only 18% arriving during the last quarter. Conversely, a slightly higher proportion (27%) of all inexperienced (first‐time breeders) males and females arrived during the last quarter season than during the first quarter (22%). In 18 of the 20 years, the proportion of inexperienced females found paired with inexperienced males was significantly higher than could be expected from the proportion of inexperienced males in the pond, suggesting that selective pairing was occurring. One potential effect of pairings between inexperienced male and female toads, coupled with the sex difference in the age of attaining sexual maturity, might be a reduction in the incidence of sibling matings (inbreeding) in the common toad. This is particularly relevant in a species that is both highly philopatric and which congregates in large numbers every spring to breed in very localized areas.

Chorus participation by male bullfrogs, Rana catesbeiana: a test of the energetic constraint hypothesis

Chorus tenure is the number of nights that a male anuran spends attending choruses, and dominant tenure is the number of nights that a male adopts a dominant (i.e. territorial) mating tactic. While male bullfrogs that have longer tenure (chorus tenure and dominant tenure) acquire more mates, tenure is believed to be energetically costly. During the summer of 1998, we tested the hypothesis that tenure of bullfrogs is energy constrained, by conducting a feeding experiment to manipulate energetic condition, and by measuring each male's body condition on every night of his chorus tenure. The energetic constraint hypothesis did not adequately predict variation in male chorus tenure. However, male bullfrogs with longer dominant tenures, other things being equal, were in better initial condition, poorer final condition and lost condition more slowly than males with shorter dominant tenures. Feeding had no significant effect on either chorus tenure or dominant tenure. We found evidence that direct selection through endurance rivalry favoured traits in male bullfrogs that increased tenure.

Terrestrial Habitat Preferences of Adult Arroyo Southwestern Toads

Using an external belt attachment system, we attached 1.8-g radiotransmitters to arroyo southwestern toads (Bufo microscaphus californicus). We tracked 83 arroyo southwestern toads over an average period of 30.9 days (SD = 29.0) in 1998. Male calling activity began at the study site on 6 March and ended on 29 July. We observed arroyo toad activity in upland habitats throughout the study. We examined the habitat preferences of arroyo toads by comparing land cover within a minimum convex polygon estimate home range for each animal to the study site subarea where each toad occurred. We also compared substrate, vegetation, and vegetation structure use to availability within each minimum convex polygon area. We found significant between-sex differences in land use and vegetation-type preferences during the study, but not for substrate or vegetation-structure preferences. Female arroyo southwestern toads preferred terrace and channel habitats to campground, agricultural, or upland habitats.During the breeding season, male arroyo southwestern toad preference for channel habitats was significantly greater than for all other habitat types. Toads preferred sands for burrowing substrate, but no substrate type was preferred for surface activity. Differences in preference rank for vegetation type were weak. Male use of agricultural lands adjacent to breeding sites increased after the breeding season. Dense, tall vegetation structures were least preferred by arroyo southwestern toads for burrows. Arroyo southwestern toads may forage and disperse through many vegetation types that are common in riparian and upland habitats of southern California.

Do Male White-Lipped Frogs Use Seismic Signals for Intraspecific Communication?

Abstract Modern frogs and toads possess a structurally unique saccule, endowing them with seismic sensitivity greater than that observed so far in any other group of terrestrial vertebrates. In synchrony with their advertisement calls, approximately half of the calling males of one frog species, the Puerto-Rican white-lipped frog (Leptodactylus albilabris), produce impulsive seismic signals (thumps). The spectral distribution of power in these seismic signals matches precisely the spectral sensitivity of the frog's saccule. The signals have sufficient amplitude to be sensed easily by the frog's saccule up to several meters from the source—well beyond the typical spacing when these frogs are calling in a group. This circumstantial evidence suggests that white-lipped frogs may use the seismic channel in intraspecific communication, possibly as an alternative to the airborne channel, which often is cluttered with noise and interference. Using the frog's vocalizations as our assay, we set out to test that pro...

Vocal behaviors are related to nonrandom structure of anuran breeding assemblages in Guyana

An important problem in community ecology is that of identifying patterns of structure in data by employing null models. Null models use reiterative methods to generate large numbers of virtual communities that are compared with empirical assemblages. These allow detection of nonrandom structure of organization attributable to biotic and abiotic factors. We tested the hypothesis that vocal behaviors are related to nonrandom structure in frog breeding assemblages. Male frogs of many species gather at ephemeral bodies of water, and produce advertisement calls that primarily attract conspecific females who are ready to mate. We determined whether null models and multivariate techniques could test for nonrandom patterns in pond breeding assemblages comprised of 16 and 14 species in Guyana, South America. Comparisons of empirical data against two null models indicated that observed patterns of temporal, spatial, and spectral acoustic variables, and calling site use by heterospecific frogs were significantly nonrandom patterns. Observed patterns of spatial and calling site usage appeared to contribute to high species richness of these Neotropical frog breeding assemblages. Principal component analysis of advertisement calling variables of sympatric treefrogs (Hylidae) suggested that species differed in dominant frequency, fundamental frequency, pulse rate, note duration, call duration, and call rate. Discriminant function analysis of these same call variables in the numerically three most common treefrog species of the genus Scinax indicated that fundamental frequency and pulse rate alone separated the three species. Overall, the null models and multivariate statistical techniques suggested that nonrandom patterns of spatial and calling site usage were implicated in the apparent nonrandom structure of these Neotropical pond breeding anuran assemblages.

Female reciprocal calling in the Iberian midwife toad (Alytes cisternasii) varies with male call rate and dominant frequency: implications for sexual selection.

Male midwife toads (Alytes cisternasii) responded differently depending on the call frequency and call rate of other males. I tested female Iberian midwife toads with the same set of stimuli used earlier with males. Females responded faster to high call rates, and female vocal activity was greater in response to low-frequency male calls. Thus, in both sexes, the vocal response differs in the same direction according to signal frequency variation, but the magnitude of the response is greater in males than in females. In the light of these results, I discuss the implications for sexual selection of this reciprocal calling.

Determination of age, longevity and age at reproduction of the frog Microhyla ornata by skeletochronology.

Skeletochronological estimation of age, longevity, age at sexual maturity and breeding of Microhyla ornata was done. Frogs (n=62) were collected locally in August (rainy season) 1997 and brought to the laboratory. Body mass and snout-vent-length (SVL) of each frog was recorded; the 4th toe of both the hind limbs was clipped under anaesthesia, fixed in 10% formalin, demineralized in 5% nitric acid and processed for histology. Limb bones (femur, humerus, tibiofibula and radioulna) of 6 large sized frogs were also processed for skeletochronology in order to study the rate of resorption. Gonads of 25 frogs (belonging to different body size ranges) were processed for histology in order to ascertain the gametogenic status of individual frogs. One to four growth rings consisting of growth zones and lines of arrested growth (LAGs) were noticed in frogs of different body sizes; the number of LAGs remained identical in all the limb bones and phalanges in 5 out of 6 frogs. Back calculation indicated that the resorption rate is very low in this frog. Male frogs possessed sperm bundles in seminiferous tubules in the 1st year, while females showed yolky follicles in the ovary in the 2nd year. Frogs found in amplexus were 3 5 years old. The results suggest that this frog may live for a maximum of 5 years in the natural population.

Ultrastructural design of anuran muscles used for call production in relation to the thermal environment of a species

I examined the aerobic trunk muscles, which are used for call production, of male frogs from species that breed in different thermal environments to test the hypothesis that cold-adapted frogs should have fewer capillaries per unit mitochondrial volume in oxidative muscles than warm-adapted frogs because of reduced mitochondrial function at low temperatures. The species of interest were the cold-temperate Pseudacris crucifer and the warm-tropical Hyla microcephala in the family Hylidae, and the cold-temperate Rana sylvatica and the warm-temperate Rana clamitans in the family Ranidae. Trunk-muscle mitochondrial volume, V(V)(mt,f), was proportionally higher in species with higher mean calling rates (number of notes per hour), irrespective of the familial affinity of a species and the thermal environment in which it vocalized. Trunk-muscle capillary length density, J(V)(c,f), was significantly lower in P. crucifer than in H. microcephala because of significantly higher mean fiber area, a macro (f). Conversely, trunk-muscle J(V)(c,f) was similar in the two ranid species. Using total capillary length, J(c), and total mitochondrial volume, V(mt,m), as a measure of maximal oxygen supply and demand, respectively, in trunk muscles, J(c)-to-V(mt,m) ratios were significantly lower in cold-adapted P. crucifer (4.3 km cm(-3)) and R. sylvatica (4.8 km cm(-3)) than in warm-adapted H. microcephala (7.1 km cm(-3)) and R. clamitans (6.4 km cm(-3)). In contrast, J(c)-to-V(mt,m) ratios in the more anaerobic gastrocnemius muscle of these species was not related to the thermal environment of a species, which may reflect capillaries conforming to microcirculatory functions, e.g. lactate removal, that take precedence over oxygen delivery. Mitochondrial cristae surface area, S(V)(im,mt), in P. crucifer trunk and gastrocnemius muscles (37.7+/-1.6 and 35.9+/-1.5 m(2 )cm(-3) respectively) was, on average, similar to mammalian values, suggesting equivalent structural capacities of muscle mitochondria in these two taxa. Taken together, the present data suggest that trunk-muscle respiratory design may reflect a capillary supply commensurate with maximal levels of oxygen delivery set by mitochondria operating at different environmental temperatures. P. crucifer and H. microcephala trunk muscles were also characterized by a high lipid content, which contrasted with a near absence of trunk-muscle lipids in R. sylvatica and R. clamitans. The extraordinarily high lipid content of P. crucifer trunk muscles (26 % of muscle volume) may serve as an auxiliary oxygen pathway to mitochondria and thus compensate in part for this tissue's reduced capillary/fiber interface. The effect of potentially high depletion rates of trunk-muscle lipid stores on metabolic rates of male frogs while calling is discussed.