The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback

Acoustic signals produced by most anurans are accompanied by inflation of a conspicuous vocal sac. We presented female túngara frogs, Physalaemus pustulosus, with acoustic playback of the male advertisement call, synchronized with a video playback of vocal sac inflation. Females significantly preferred a stimulus combination including vocal sac inflation over an identical set of stimuli with the vocal sac inflation removed. Neither a moving rectangle bearing the gross contrast and spatiotemporal properties of the vocal sac inflation sequence, nor the image of a noncalling male significantly enhanced the attractiveness of the acoustic stimulus. Both the form and spatiotemporal properties of the vocal sac thus appear to be salient to females. The results indicate that the vocal sac can serve as a visual cue, which may account for the conspicuous pigmentation found on the vocal sacs of males in many species. Gular inflation in synchrony with a call may function to facilitate female localization of individual males in an aggregation.     

Sophisticated Communication in the Brazilian Torrent Frog Hylodes japi

Intraspecific communication in frogs plays an important role in the recognition of conspecifics in general and of potential rivals or mates in particular and therefore with relevant consequences for pre-zygotic reproductive isolation. We investigate intraspecific communication in Hylodes japi, an endemic Brazilian torrent frog with territorial males and an elaborate courtship behavior. We describe its repertoire of acoustic signals as well as one of the most complex repertoires of visual displays known in anurans, including five new visual displays. Previously unknown in frogs, we also describe a bimodal inter-sexual communication system where the female stimulates the male to emit a courtship call. As another novelty for frogs, we show that in addition to choosing which limb to signal with, males choose which of their two vocal sacs will be used for visual signaling. We explain how and why this is accomplished. Control of inflation also provides additional evidence that vocal sac movement and color must be important for visual communication, even while producing sound. Through the current knowledge on visual signaling in Neotropical torrent frogs (i.e. hylodids), we discuss and highlight the behavioral diversity in the family Hylodidae. Our findings indicate that communication in species of Hylodes is undoubtedly more sophisticated than we expected and that visual communication in anurans is more widespread than previously thought. This is especially true in tropical regions, most likely due to the higher number of species and phylogenetic groups and/or to ecological factors, such as higher microhabitat diversity.     

Take time to smell the frogs: vocal sac glands of reed frogs (Anura: Hyperoliidae) contain species‐specific chemical cocktails

Males of all reed frog species (Anura: Hyperoliidae) have a prominent, often colourful, gular patch on their vocal sac, which is particularly conspicuous once the vocal sac is inflated. Although the presence, shape, and form of the gular patch are well‐known diagnostic characters for these frogs, its function remains unknown. By integrating biochemical and histological methods, we found strong evidence that the gular patch is a gland producing volatile compounds, which might be emitted while calling. Volatile compounds were confirmed by gas chromatography–mass spectrometry in the gular glands in 11 species of the hyperoliid genera Afrixalus, Heterixalus, Hyperolius, and Phlyctimantis. Comparing the gular gland contents of 17 specimens of four sympatric Hyperolius species yielded a large variety of 65 compounds in species‐specific combinations. We suggest that reed frogs might use a complex combination of at least acoustic and chemical signals in species recognition and mate choice. © 2013 The Authors. Biological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 828–838.     

Facial and gill musculature of polynemid fishes,with notes on their possible relationships with sciaenids (Percomorphacea: Perciformes)

The Polynemidae is a family of primarily marine fishes with eight genera and 42 extant species. Many aspects of their morphology are largely unknown, with few reports about their osteology and barely any information on their myology. This paper describes and illustrates in detail all facial and branchial muscles of representative species of polynemids. Our analysis demonstrates the existence of several remarkable and previously unknown specializations in the polynemid musculature. The aponeurotic and completely independent origin of the pars promalaris of the adductor mandibulae is apparently unique among percomorphs. The differentiation of this section into lateral and medial subsections; the total separation of the promalaris from the retromalaris; the differentiation of the pars primordialis of the levator arcus palatini into external and internal subsections are also uncommon features of polynemids that are shared by sciaenids, thus supporting the hypothesis of a closer relationship between these families.     

Burrowing in frogs

More than 95% of burrowing Anura dig hindfeet first into the soil, a pattern unique to frogs among terrestrial vertebrates. The postero-laterally placed hindlimbs and associated musculature of frogs are preadaptations for hindfeet digging. One fossorial, backwards burrower, Glyphoglossus molossus (Microhylidae), has morphological modifications of the hindlimb for positioning the spade-like metatarsal tubercle and for increasing the force of the lower leg during digging. In contrast, in the headfirst burrower Hemisus marmoratus (Ranidae) there is extensive reorganization of the pectoral-cranial morphology compared to that: of a non-burrowing confamilial species. A model links the shifts in the pectoral morphology in Hemisus marmoratus to specific action patterns of headfirst: burrowing. Finally, data on stomach contents, natural history and energy utilization of frog species are presented to demonstrate the interrelationships of distinct loco. motor patterns with specific feeding strategies.     

Ultrastructure of the anal sacs in <Emphasis Type="Italic">Thalassema</Emphasis><Emphasis Type="Italic">thalassemum</Emphasis> (Annelida,Echiura)

The anal sacs of Thalassema thalassemum consist of an elongate tubular invagination (end sac) that is uniformly covered with numerous sessile ciliated funnels. While the funnels are composed of multi-ciliated, non-muscular cells and possess a ciliated neck-like constriction, the end sacs are lined by a simple epithelium of large, irregularly formed and sparsely ciliated cells that include masses of secretory granules. Podocytes are incorporated in the peritoneum that surrounds the anal sacs. A muscle grid consisting of inner longitudinal, outer circular and additional diagonal fibres that branch off of the circular fibres is embedded in the matrix between the end sac epithelium and peritoneum. Major structural differences between the hindgut and anal sacs support the hypothesis that the anal sacs are not gut derivatives but are instead part of a modified metanephridial system. Comparison of the anal sac morphology in Echiura reveals that T. thalassemum shares a tubular end sac with all known members of Thalassematinae and Ikedaidae, as well as with some members of Bonelliidae and Echiurinae, while the sessile funnels are apomorphic for the Thalassematinae.     

From uni- to multimodality: towards an integrative view on anuran communication

Undeniably, acoustic signals are the predominant mode of communication in frogs and toads. Acoustically active species are found throughout the vast diversity of anuran families. However, additional or alternative signal modalities have gained increasing attention. In several anurans, seismic, visual and chemical communications have convergently evolved due to ecological constraints such as noisy environments. The production of a visual cue, like the inevitably moving vocal sac of acoustically advertising males, is emphasized by conspicuously coloured throats. Limb movements accompanied by dynamic displays of bright colours are additional examples of striking visual signals independent of vocalizations. In some multimodal anuran communication systems, the acoustic component acts as an alert signal, which alters the receiver attention to the following visual display. Recent findings of colourful glands on vocal sacs, producing volatile species-specific scent bouquets suggest the possibility of integration of acoustic, visual and chemical cues in species recognition and mate choice. The combination of signal components facilitates a broadened display repertoire in challenging environmental conditions. Thus, the complexity of the communication systems of frogs and toads may have been underestimated.     

Female germ unit in Genlisea and Utricularia, with remarks about the evolution of the extra-ovular female gametophyte in members of Lentibulariaceae

Lentibulariaceae is the largest family among carnivorous plants which displays not only an unusual morphology and anatomy but also the special evolution of its embryological characteristics. It has previously been reported by authors that Utricularia species lack a filiform apparatus in the synergids. The main purposes of this study were to determine whether a filiform apparatus occurs in the synergids of Utricularia and its sister genus Genlisea, and to compare the female germ unit in these genera. The present studies clearly show that synergids in both genera possess a filiform apparatus; however, it seems that Utricularia quelchii synergids have a simpler structure compared to Genlisea aurea and other typical angiosperms. The synergids are located at the terminal position in the embryo sacs of Pinguicula, Genlisea and were probably also located in that position in common Utricularia ancestor. This ancestral characteristic still occurs in some species from the Bivalvaria subgenus. An embryo sac, which grows out beyond the limit of the integument and has contact with nutritive tissue, appeared independently in different Utricularia lineages and as a consequence of this, the egg apparatus changes position from apical to lateral.     

Morphology of the gas bladder in bumblebee catfishes (Siluriformes,Pseudopimelodidae)

The gross morphology of the gas bladder is described and compared for representatives of all valid genera of Pseudopimelodidae (Siluriformes). Cephalosilurus albomarginatus and species of Batrochoglanis, and Microglanis have the most basic form: a large, cordiform gas bladder with a simple internal T‐shaped septum. Cephalosilurus apurensis, C. fowleri, and C. nigricauda also have a large, cordiform gas bladder, but they have well‐developed trabeculae associated with the internal T‐shaped septum, and a pair of well‐developed constrictor muscles inserted on the external wall; the latter feature is present in most species of Pimelodidae, but absent in all other catfishes. The monotypic Lophiosilurus alexandri also has well‐developed constrictor muscles, and its gas bladder is moderately sized. The species of Pseudopimelodus and Cruciglanis have a diminutive gas bladder partially divided into two lateral sacs without internal communication, and lack constrictor muscles. The parapophysis of the fourth vertebra is a wide and long shelf connected to the dorsal surface of the gas bladder in most pseudopimelodid genera. However, in the species of Pseudopimelodus and Cruciglanis the parapophysis of the fourth vertebra is shorter and has its anterior ramus folded back, partially covering the gas bladder anteroventrally; and the tympanic opening is smaller than in species of the other genera. Five phylogenetic characters are proposed based on the morphology of the gas bladder and associated structures in species of Pseudopimelodidae, and the evolution of those characters in the family is discussed. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Loss of air sacs improved hominin speech abilities

In this paper, the acoustic-perceptual effects of air sacs are investigated. Using an adaptive hearing experiment, it is shown that air sacs reduce the perceptual effect of vowel-like articulations. Air sacs are a feature of the vocal tract of all great apes, except humans. Because the presence or absence of air sacs is correlated with the anatomy of the hyoid bone, a probable minimum and maximum date of the loss of air sacs can be estimated from fossil hyoid bones. Australopithecus afarensis still had air sacs about 3.3 Ma, while Homo heidelbergensis, some 600 000 years ago and Homo neandethalensis some 60 000 years ago, did no longer. The reduced distinctiveness of articulations produced with an air sac is in line with the hypothesis that air sacs were selected against because of the evolution of complex vocal communication. This relation between complex vocal communication and fossil evidence may help to get a firmer estimate of when speech first evolved.     

The corystosperm pollen organ Pteruchus from the Triassic of antarctica

The permineralized corystosperm pollen organ Pteruchus is described from the early Middle Triassic of Antarctica. Pteruchus fremouwensis consists of an axis bearing numerous, helically arranged microsporophylls, each of which terminates in a distal flattened head. The axis is 1–2 mm in diameter and eustelic. Spherical to elliptical secretory cavities are present in the ground tissue of the axis, microsporophyll, and pollen sac wall. The basal stalk of the microsporophyll is vascularized by a C-shaped strand that gives rise to a midvein and numerous lateral veins in the distal head. At least 38 pollen sacs are borne on the abaxial surface of the microsporophyll head. These are arranged in pairs on either side of lateral veins. Each pollen sac is sessile, elongated, and uniloculate. The pollen sac wall is several cell layers thick early in ontogeny, but reduced to a single layer in thickness when mature. Dehiscence is longitudinal along the inner surface. Pollen is monosulcate and bisaccate, and of the Alisporites-type. The Triassic specimens are the first structurally preserved pollen organs of the Pteruchus-type and can be related to the associated corystosperm stem and leaf genera based on the presence of unique secretory cavities. The morphology of Pteruchus and the relationship of this pollen organ with other Mesozoic and Paleozoic pollen organs is discussed.     

Aspects of the ecology and energetics of the egg sac parasites of the wolf spider Pardosa lugubris (Walckenaer)

Summary The egg sacs of the wolf spider Pardosa lugubris are parasitised by two ichneumonid wasps, namely Gelis micrurus and Hidryta sordidus. The parasites are bivoltine, the first generation parasitising the summer egg sac of P. lugubris and the second generation parasitising, and overwintering in, the autumn egg sac. Parasitised egg sacs have a characteristic appearance.The degree of egg sac parasitism was 9.8% and 6.9% for the two egg sac batches in 1965 and 2.9% and 34.8% for those of 1966. The degree of parasitism varies from area to area as does the percentage parasitism attributable to the two species.The gross growth efficiency for Hidryta from the first egg sac is 31.2% and from the second 16.2%. 3.0% in 1965 and 4.3% in 1966, of the annual yield from P. lugubris to predators and parasites, goes to the egg sac parasites. This represents reductions in recruitment of 9.1% in 1965 and 10.9% in 1966.     

Superficial mandibular musculature and vocal sac structure in hemiphractine hylid frogs

Three patterns of superficial mandibular musculature are described in hemiphractine hylid frogs. One of these is unique to the morphologically bizarre Hemiphractus. A second pattern is found in Flectonotus and also occurs in some species of Gastrotheca and Stefania. A third pattern involves a differentiated apical element of the m. intermandibularis and is found in Cryptobatrachus, many species of Gastrotheca, and one species of Stefania. Evidence supports the plesiomorphic state of an undifferentiated m. intermandibularis and two derived states of differentiation of that muscle. One of these is the development of supplementary posterolateral elements characteristic of the Phyllomedusinae, whereas the diferentiation of an apical element has occurred in at least six independent lineages—the entire Pelodryadinae, three unrelated genera of Hylinae, and two genera of Hemiphractinae. Gastrotheca and Stefania are the only anuran genera known to include species possessing, and others lacking, differentiation of the m. intermandibularis. Vocal sacs and apertures are absent in Cryptobatrachus, Hemiphractus, Stefania, and six species of Gastrotheca. © 1995 Wiley-Liss, Inc.     

The musculature of Squatinella rostrum (Milne, 1886) (Rotifera: Lepadellidae) as revealed by confocal laser scanning microscopy with additional new data on its trophi and overall morphology

Wilts, E.F., Wulfken, D., Ahlrichs, W.H. and Martínez Arbizu, P. 2012. The musculature of Squatinella rostrum (Milne, 1886) (Rotifera: Lepadellidae) as revealed by confocal laser scanning microscopy with additional new data on its trophi and overall morphology.—Acta Zoologica (Stockholm) 93 : 14–27. The monogonont rotifer Squatinella rostrum was investigated with light, scanning electron and confocal laser scanning microscopy to reveal new morphological data on its inner and outer anatomy. In total, the visualized somatic musculature displays five paired longitudinal muscles (musculi longitudinales I–V) and nine circular muscles (musculi circulares I–IX). Compared to other species, S. rostrum is characterized by the absence of several longitudinal and circular muscles (e.g. musculus longitudinalis capitis, corona sphincter and pars coronalis). A reconstruction of the mastax musculature revealed a total number of seven paired and two unpaired mastax muscles. Possibly homologous somatic and mastax muscles in other, thus far investigated rotifers are discussed. Moreover, we provide a phylogenetic evaluation of the revealed morphological characters and suggest possible autapomorphic characters supporting Squatinella and Lepadellidae. Finally, we refer to some striking similarities in the morphology, ecology and way of movement of Squatinella and Bryceella that may indicate a closer relationship of both taxa.     

Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free‐living cheilostomes

Numerous gross morphological attributes are shared among unrelated free‐living bryozoans revealing convergent evolution associated with functional demands of living on soft sediments. Here, we show that the reproductive structures across free‐living groups evolved convergently. The most prominent convergent traits are the collective reduction of external brood chambers (ovicells) and the acquisition of internal brooding. Anatomical studies of four species from the cheilostome genera Cupuladria and Discoporella (Cupuladriidae) show that these species incubate their embryos in internal brooding sacs located in the coelom of the maternal nonpolymorphic autozooids. This sac consists of a main chamber and a narrow neck communicating to the vestibulum. The distal wall of the vestibulum possesses a cuticular thickening, which may further isolate the brood cavity. The presence of this character in all four species strongly supports grouping Cupuladria and Discoporella in one taxon. Further evidence suggests that the Cupuladriidae may be nested within the Calloporidae. Based on the structure of brooding organs, two scenarios are proposed to explain the evolution of the internal brooding in cupuladriids. The evolution of brood chambers and their origin in other free‐living cheilostomes is discussed. Unlike the vast majority of Neocheilostomina, almost all free‐living cheilostomes possess nonprominent chambers for embryonic incubation, either endozooidal and immersed ovicells or internal brooding sacs, supporting the idea that internal embryonic incubation is derived. We speculate that prominent skeletal brood chambers are disadvantageous to a free‐living mode of life that demands easy movement through sediment in instable sea‐floor settings. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Egg sac damage and previous egg sac production influence truncated parental investment in the wolf spider,Pardosa milvina

Life history theory predicts that iteroparous animals adaptively partition reproductive effort between current and future reproduction. When rearing costs of current offspring exceed the potential benefits, parental care should be terminated and deferred toward future reproduction. We tested two related predictions that follow from life history theory: (a) parents should be sensitive to offspring viability and withhold parental care if offspring survival probability drops and future reproductive opportunities are likely, and (b) parents should be less sensitive to offspring survival probability when future reproduction is unlikely and maximize parental care late in life. The wolf spider, Pardosa milvina, demonstrates extensive parental care; however, they may also abandon or cannibalize their egg sacs. We tested the effects of egg sac damage and production of a previous egg sac on egg sac abandonment and cannibalism decisions. Among four egg sac groups (1st egg sac intact, 1st egg sac damaged, 2nd egg sac intact, 2nd egg sac damaged), we daily monitored egg sac abandonment and cannibalism and measured differences in egg sac searching, protection, and grooming among removed and damaged egg sacs (N = 116 with 1st egg sac and 88 with 2nd egg sac). Females with first egg sacs abandoned and cannibalized damaged egg sacs significantly more compared to unmanipulated egg sacs; however, females with second egg sacs were insensitive to egg sac damage. Females also spent significantly more time protecting second egg sacs compared to first egg sacs and groomed damaged egg sacs significantly more than undamaged. These results support the general predictions of life history theory that indicate that abandonment and cannibalism should decrease with diminished future reproductive potential and that parents should be less sensitive to indicators of offspring survival probability late in life.     

Vocal Strategies in Confronting Interfering Sounds by a Frog from the Southern Temperate Forest,Batrachyla antartandica

Animals are communicating by sound face interference from biotic and abiotic sources. Contrasting strategies have been reported in different taxa in the presence of prolonged noises, but in particular, interactions among acoustically active species have been studied to a very limited extent. In addition, reactions of a single species to interferences having contrasting structural patterns have not been explored systematically. The vocal responses of 16 male frogs Batrachyla antartandica from the temperate austral forest in Chile were tested with conspecific calls and with the calls of two sympatric species: B. taeniata and B. leptopus, broadcast at amplitudes of 73, 79, 85, 91, and 97 dB peak sound pressure level (SPL). Also, the vocal activity of the subjects during exposure to a 3‐min continuous broadband noise presented at 67 dB root mean square (RMS) SPL was monitored. The subjects gave significantly higher responses to the conspecific relative to the heterospecific calls but increased their vocal output in the presence of continuous noise. The preference of vocal responses for the conspecific relative to heterospecific signals bears a general resemblance to those exhibited by B. taeniata in a previous study and potentially contributes to the typical segregation in conspecific choruses observed in areas where these frogs breed in sympatry. Such lack of vocal responses to heterospecific stimuli contrasts with the increase in vocal activity during exposure to continuous noise lacking a temporal fine structure and points to identify different strategies in confronting interferences of diverse origin.     

The common occurrence of incompletely developed pollen of Eupatorium (Compositae: Eupatorieae)

Mature anthers of Eupatorium serotinum Michx., E. coelestinum L. and E. purpureum L. (Compositae: Eupatorieae) contain both loose mature pollen grains and acetolysis-resistant extratapetal sacs enclosing clusters of immature pollen. Many sacs contain incompletely developed pollen grains that differ in size diameter, with spines of varying lengths and degrees of acuity and with colpal areas having narrow to markedly protracted margins. We presume that all nutrients for pollen development within sacs come from plasmodial tapetum included therein. Thus, pollen in portions of the sac or in isolated sacs with inadequate plasmodial tapetum may be incompletely developed. Such partial development may result from stress, e.g. insufficient nutrients and water. While our data are from three species of Eupatorium, we have long noted the syndrome in other Eupatorieae and other tribes in the Compositae. Curtailing supplies for development of some portions of an anther could be an evolutionary strategy for survival of the species through periods of stress.     

Sexual Dimorphism of the Larynx of the Mongolian Gazelle (Procapra gutturosa Pallas, 1777) (Mammalia, Artiodactyla, Bovidae)

The larynges (except for the epiglottis) of two adult Mongolian gazelles, one male and one female, were dissected. This species is characterized by a pronounced sexual dimorphism of the larynx. Dimorphism with regard to the size of the entire larynx and of the thyroid cartilage is about 2:1 whereas the difference of mean body mass is about 1.3:1 between males and females. Unexpectedly, and in contrast to other bovids, the larynx of the male Mongolian gazelle has a paired lateral laryngeal ventricle. However, in contrast to horse, dog, pig and many primate species also possessing such a paired ventricle, its rostral opening in the Mongolian gazelle is situated lateral to the corniculate process of the arytenoid cartilage. The neck of the laryngeal ventricle is embraced by the bifurcated cuneiform process of the epiglottis. Despite the enlarged laryngeal cartilages, the vocal process of the male arytenoid cartilage is relatively shorter than that of the female. The male thyroarytenoid muscle is clearly separated into a rostral ventricular muscle and a caudal vocal muscle whereas the female's, as in other bovids, is almost uniform. The lateral sac of the two-chambered laryngeal ventricle in the male projects laterally between the ventricular and the vocal muscle. As in the domestic bovids and in many other artiodactyls the larynx of the male Mongolian gazelle is lacking any rostrally directed membraneous portion of the vocal fold. Instead, the thick and tough bow-like vocal fold projects caudally into the infraglottic cavity and is supported by a peculiar pan-like fibroelastic pad. This resilient element, situated medial to the bipartite thyroarytenoid muscle, might be a homologue of the vocal ligament, eventually including lateral portions of the elastic cone. A fibroelastic pad is absent in the female. The resilient floor of the laryngeal vestibulum, ventral to the fibroelastic pad, is rostrally and caudally subducted by tube-like spaces. Evolutionary enlargement of the male larynx, including the vocal folds, and of the caudal portions of the vocal tract may have shifted the fundamental and formant frequencies to a lower register. The paired lateral laryngeal ventricle might produce an amplitude increase of the vocalizations assisted by differential action of the bipartite thyroarytenoid muscle. In addition, the peculiar shape, size and tough consistency of the male vocal folds may, as in roaring felids, assist in producing high amplitude and low frequency vocalizations. Perhaps the biological role of the enlarged male larynx of Procapra gutturosa has evolved in relation to its mating system. In the rutting season, dominant males establish individual territories and maintain harems. During prolonged courtship prior to mating, these males perform an acoustic display uttering loud and guttural bellows. In addition, the bulging ventral neck region of males may serve as an optical attractant for the females. Thus, the evolution of the enlarged larynx of the male Mongolian gazelle may have been favoured by sexual selection.