Deconstructing a controversial local range expansion: conservation biogeography of the painted reed frog (Hyperolius marmoratus) in South Africa

Local range expansions might either be the response of populations to climate or landscape change, or be caused directly by human intervention. In the latter case the expansion would be considered the first in the steps leading to a biological invasion. In species typically not the subject of human commerce, distinguishing the causes of local range expansions is problematic. Range dynamic theory provides a basis for doing so, and, when used to assess phylogeographical information, can be a powerful conservation biogeographical approach. Here we adopt this approach to resolve the controversial case of the recent range expansion of the painted reed frog (Hyperolius marmoratus) in southern South Africa. Within the last decade, H. marmoratus has spread westward approximately 500 km from its historical range. This local range expansion could either represent human‐mediated jump dispersal, or a response to landscape or climate change. To date, the latter has been assumed, although not universally. Using a phylogeographic approach to investigate these competing hypotheses, a portion of the mitochondrial COI gene was sequenced for individuals from within the historical range (n = 178), and four putatively introduced populations in dams (n = 121). There was substantial geographical population structure within the historical range, and these populations were significantly different from the dam populations (Φ_ST = 0.817, P < 0.001). The presence of one or a few dissimilar haplotypes in the dams suggests that introductions are from a number of different sources. This, in conjunction with new survey data, supports the hypothesis that recent establishment of these populations is the result of human‐mediated jump dispersal. The impact of this range expansion on ecosystem functioning is unknown, but given the rapid spread of this species and its potential influence on ecosystems, safeguards should be put in place to control further introductions and to restrict the currently invasive populations.     

Success breeds success in mating male reed frogs (Hyperolius marmoratus).

Studies of the distribution of mating success among males in frog choruses typically seek to identify specific phenotypic attributes that confer a higher mating success on certain individual males. These attributes invariably relate to competition among males: either direct competition in the form of aggression, or competition to attract and be chosen by females. In this paper, we present evidence that an additional factor may operate in frog choruses. We show that individual males who mate on a given night enjoy a higher probability of being successful on the next night, and we suggest that this is because successful mating enables males to conserve energy.     

Adaptations of the reed frog Hyperolius viridiflavus (Amphibia,Anura, Hyperoliidae) to its arid environment

Summary After breeding African savanna dwelling reed-frogs of the superspecies Hyperolius viridiflavus face a severe dry season. The frogs withstand the adverse abiotic conditions in exposed positions, clinging to dry vegetation. Only juveniles (300–700 mg) are able to adjust water economy and metabolism to a prolonged dry season. Wet season frogs attain low levels of evaporative water loss (EWL) within 6–8 days after incipient water shortage. This time course is mainly determined by the animal's ability to lower metabolism and activity level to the minimum demands of a dry season. Barriers against diffusion of water which most probably are built up by the stratum corneum and/or the overlying film of dried mucus seem not to be essentially modified during adjustment to dry season conditions. Changeover to dry season physiology is greatly accelerated through preconditioning frogs to water shortage. AdultHyperoliusare unable to reduce activity and metabolism as fast and effectively as juveniles. Most probably these are the main reasons for their very restricted survival capability under dry season conditions; the generally poor energy reserves after the breeding period may further shorten their survival time. At the critical thermal maximum (CTM) Hyperolius uses skin gland secretions for evaporative cooling. Acclimation effects and regulation of evaporative cooling within some 1/10° C help to employ limited water reserves very economically. Dry adapted, dehydrated frogs take up water, whenever available, via specialized skin areas. Rate of uptake is high and is mainly determined by the actual stage of dehydration. The onset of the water-balance-response is also affected by preconditioning. Survival time of small (<500 mg) estivating Hyperolius is limited by their water reserves.Due to their unfavourable surface to volume ratio they loserelatively more water by evaporation than larger conspecifics. Therefore, smaller specimens should allocate energy preferably to growth, until reducing EWL so far to survive the average periods between the rare precipitations. In larger frogs (>500 mg) the amount of stored energy determines maximal survival time. When a critical size is reached in postmetamorphic growth, a change in energy allocation from body growth to energy storage would improve prospects of survival and should therefore be expected. Species specific differences in regard to EWL and CTM indicate a strong correlation between physiological properties and ecological demands.Abbreviations EWL evaporative water loss - CTM critical thermal maximum - WSF wet season frog - TSF transitional season frog - DSF dry season frog - SD saturation deficit     

Adaptations of the reed frog Hyperolius viridiflavus (Amphibia,Anura, Hyperoliidae) to its arid environment

Summary Hyperolius viridiflavus nitidulus inhabits parts of the seasonally very hot and dry West African savanna. During the long lasting dry season, the small frog is sitting unhidden on mostly dry plants and has to deal with high solar radiation load (SRL), evaporative water loss (EWL) and small energy reserves. It seems to be very badly equipped to survive such harsh climatic conditions (unfavorable surface to volume ratio, very limited capacity to store energy and water). Therefore, it must have developed extraordinary efficient mechanisms to solve the mentioned problems. Some of these mechanisms are to be looked for within the skin of the animal (e.g. protection against fast desiccation, deleterious effects of UV radiation and overheating). The morphology of the wet season skin is, in most aspects, that of a normal anuran skin. It differs in the organization of the processes of the melanophores and in the arrangement of the chromatophores in the stratum spongiosum, forming no Dermal Chromatophore Unit. During the adaptation to dry season conditions the number of iridophores in dorsal and ventral skin is increased 4–6 times compared to wet season skin. This increase is accompanied by a very conspicuous change of the wet season color pattern. Now, at air temperatures below 35° C the color becomes brownish white or grey and changes to a brilliant white at air temperatures near and over 40° C. Thus, in dry season state the frog retains its ability for rapid color change. In wet season state the platelets of the iridophores are irregularly distributed. In dry season state many platelets become arranged almost parallel to the surface. These purine crystals probably act as quarter-wave-length interference reflectors, reducing SRL by reflecting a considerable amount of the radiated energy input.EWL is as low as that of much larger xeric reptilians. The impermeability of the skin seems to be the result of several mechanisms (ground substance, iridophores, lipids, mucus) supplementing each other.The light red skin at the pelvic region and inner sides of the limbs is specialized for rapid uptake of water allowing the frog to replenish the unavoidable EWL by using single drops of dew or rain, available for only very short periods.     

Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment

Summary Hyperolius viridiflavus possesses one complete layer of iridophores in the stratum spongiosum of its skin at about 8 days after metamorphosis. The high reflectance of this thin layer is almost certainly the result of multilayer interference reflection. In order to reflect a mean of about 35% of the incident radiation across a spectrum of 300–2900 nm only 30 layers of well-arranged crystals are required, resulting in a layer 10.5 m thick. These theoretical values are in good agreement with the actual mean diameter of single iridophores (15.0±3.0 m), the number of stacked platelets (40–100) and the measured reflectance of one complete layer of these cells (32.2±2.3%). Iridescence colours typical of multilayer interference reflectors were seen after severe dehydration. The skin colour turned from white (0–10% weight loss) through a copper-like iridescence (10–25% weight loss) to green iridescence (25–42%). In dry season state, H. viridiflavus needs a much higher reflectance to cope with the problems of high solar radiation load during long periods with severe dehydration stress. Dry-adapted skin contains about 4–6 layers of iridophores. The measured reflectance (up to 60% across the solar spectrum) of this thick layer (over 60 m) is not in keeping with the results obtained by applying the multilayer interference theory. Light, scattered independently of wavelength from disordered crystals, superimposes on the multilayer-induced spectral reflectance. The initial parallel shift of the multilayer curves with increasing thickness and the almost constant (white) reflectance of layers exceeding 60 m clearly point to a changing physical basis with increasing layer thickness.     

Regeneration of digits and forelimbs in the Kenyan reed frog Hyperolius viridiflavus ferniquei.

Newly metamorphosed individuals of the Kenyan reed frog, Hyperolius viridiflavus ferniquei, are able completely to regenerate amputated digits, including the morphologically complex digital pad. The sequence of morphological events is very similar to that seen in the typical epimorphic regeneration of amphibian extremities. Amputated forearms typically produce hypomorphic spike regenerates. Despite the lack of underlying hand and digital structures, an apical "digital" pad commonly differentiates.     

Egg predation and predator-induced hatching plasticity in the African reed frog, Hyperolius spinigularis

Density regulation is assumed to be common, but is very rarely tested experimentally. Using annual plant communities, we tested the hypotheses that 1) regulation of abundance in plants occurs at the level of entire communities, not just within species, and 2) such regulation is strongest when resources are most limiting. We transplanted different amounts of seeds from two diverse source communities in Israel to an experimental garden and monitored plant densities and cover for two years under different irrigation regimes. Both total density and total plant cover showed strong evidence of community-level regulation; plots sown at higher than average natural density declined or stayed the same in total abundance over time, while plots sown at lower than average natural density increased in abundance over time. This convergence of community abundance was strongest with the lowest irrigation in both source communities, consistent with the hypothesis of stronger regulation when all resources are more limiting (light levels were high, regardless of irrigation level). The main mechanism of regulation was strong density dependent recruitment, while survival was either density independent or inversely density dependent. Thus, the results also emphasize the need for direct experimental studies of the population dynamic consequences of interactions, as well as of individual level consequences.     

Graded Aggressive Calls in the African Painted Reed Frog Hyperolius marmoratus (Hyperoliidae)

The African painted reed frog, Hyperolius marmoratus, has a potentially complex communication system. Advertisement calls and aggressive calls, although distinct from each other, are in fact two ends of a continuum of graded calls. Playback experiments using standard advertisement calls showed that males increased the proportion of aggressive calls as the stimulus intensity was increased. In addition, three characteristics of the aggressive calls changed in response to higher playback levels. Males increased the number of pulses/call, increased call duration, and decreased dominant frequency. Aggressive calling occurred primarily during the early hours of the night, with considerable overlap with times when females were searching for mates in the chorus. Females tested in two-choice arena trials discriminated against aggressive calls in favor of advertisement calls. It is suggested that aggressive calls reduce a male's ability to attract a female and that a graded signalling system may enable males to escalate agonistic encounters with other males without rendering calls completely unattractive to females.     

DDT congener effects on secondary sex coloration in the reed frog Hyperolius argus: a partial evaluation of the Hyperolius argus endocrine screen

Organochlorine compounds such as o,p'DDT can mimic estrogen effects. We compared the effects of o,p'DDT and six other DDT congeners to the effects of estradiol by comparing in vivo color changes in the reed frog (Hyperolius argus). Premature female color pattern induction in H. argus is specific to estrogens and the current study suggests that this assay has potential for use in discriminating between xenobiotic estrogens and non-estrogens. Animals were treated at forelimb emergence and maintained in treated solution until final evaluation. Estradiol, o,p.DDT (0.1 microg/ml), o,p'DDE (1 microg/ml) and o,p'DDD (1 microg/ml) prematurely induced adult female coloration patterns in juvenile animals, whereas p,p'DDT, p, p'DDE and p,p'DDD did not.     

Alternative life cycle strategies in the West African reed frog Hyperolius nitidulus: the answer to an unpredictable environment?

The West African reed frog Hyperolius nitidulus, mainly known for its extraordinary aestivation behaviour and physiology, is able to vary its reproductive strategy in response to environmental conditions. We found indirect as well as direct evidence for individuals not following the generally assumed one year-one generation life cycle including an extended aestivation phase during the dry season, but leading very short lives for only a part of that rainy season in which the frogs were born. Second-generation frogs (males and females that reproduced in the season in which they were born) were significantly smaller than all other adults and their egg diameter was reduced. As the pattern and amount of rainfall and thus the span of time suitable for reproduction in H. nitidulus varies strongly between years in this savannah region, a flexible reproductive strategy may be highly adaptive for risk spreading. Alternative reproduction strategies probably contribute to the great success of H. nitidulus in terms of the extension of its geographical range and its often very high local abundance.     

Two-choice phonotaxis in Hyperolius marmoratus (Anura: Hyperoliidae): the effect of temporal variation in presented stimuli

Female painted reed frogs, Hyperolius marmoratus, were subjected to two-choide discrimination experiments to determine whether temporal overlap in the presented stimuli affects frequency preferences. The results showed that females preferred low frequency calls when the stimuli were presented alternately. Simultaneous presentation of stimuli resulted in a random response by females. When presented stimuli partially overlapped or abutted each other, the females responded significantly more often to the leading call irrespective of its frequency. These findings provide some insight into the possible effects of male vocal interactions on the ability of females actively to choose mates based on call frequency in natural breeding assemblages.     

Adaptations of the reed frog Hyperolius viridiflavus (Amphibia,Anura, Hyperoliidae) to its arid environment. VII. The heat budget of Hyperolius viridiflavus nitidulus and the evolution of an optimized body shape

Estivating reed frogs of the superspecies Hyperolius viridiflavus are extraordinarily resistant to the highly adverse climatic conditions prevailing in their African savanna habitats during dry season (air temperature up to 45°C, solar radiation load up to 1000 W·m^-2, no water replenishment possible for up to 3 months). They are able to withstand such climatic stress at their exposed estivation sites on dry plants without evaporative cooling. We developed a heat budget model to understand the mechanisms of how an anuran can achieve this unique tolerance, and which allows us to predict the anuran's core and surface temperature for a given set of environmental parameters, to within 4% of the measured values. The model makes it possible to quantify some of the adaptive mechanisms for survival in semiarid habitats by comparing H. viridiflavus with anurans (H. tuberilinguis and Rana pipiens) of less stressful habitats. To minimize heat gain and maximize heat loss from the frog, the following points were important with regard to avoiding lethal heat stress during estivation: 1) solar heat load is reduced by an extraordinarily high skin reflectivity for solar radiation of up to 0.65 under laboratory and even higher in the field under dry season conditions. 2) The half-cylindrical body shape of H. viridiflavus seems to be optimized for estivation compared to the hemispheroidal shape usually found for anurans in moist habitats. A half-cylinder can be positioned relative to the sun so that large surface areas for conductive and convective heat loss are shielded by a small area exposed to direct solar radiation. 3) Another important contribution of body shape is a high body surface area to body mass ratio, as found in the estivating subadult H. viridiflavus (snout-vent lengths of 14–20 mm and body weights of 350–750 mg) compared to adult frogs (24–30 mm, 1000–2500 mg) which have never been observed to survive a dry season. 4) These mechanisms strongly couple core temperature to air temperature. The time constant of the core temperature is 29±10 s. Since air temperature can be 43–45°C, H. viridiflavus must have a very unusual tolerance to transient core temperatures of 43–45°C. 5) If air temperature rises above this lethal limit, the estivating frog would die despite all its optimizations, but moving from an unsuited to a more favorable site during estivation can be extremely costly in terms of unavoidably high evaporative water loss. Therefore, H. viridiflavus must have developed behavioral strategies for reliably choosing estivation sites with air temperature staying on average within the vital range during the whole dry season.Abbreviations a absorption coefficient - a absorption coefficient of a T _OE model - A area - A _A light absorbing area - A _C theoretical body core area surrounding a constant core temperature - A _D dorsal skin area - A _E thermal (far infrared radiation) emitting area - A _EM A _E of a T _OE model - A _S silhouette area - A _SM A _S of a T _OE model - A _T total surface area - A _v ventral area - b body breadth just behind the forelimbs - bw body weight - bl body length - C _S specific heat capacity - C _D conductive energy flow - C _v convective energy flow - f _(z) silhouette function - h _C heat transfer coefficient - h _CM heat transfer coefficient of a T _OE model     

A new species of Polystoma (Monogenea: Polystomatidae) parasitic in Hyperolius marmoratus (Anura: Hyperoliidae) in South Africa

Polystoma marmorati n. sp. is described as a new polystomatid species parasitic in the urinary bladder of the painted reed frog Hyperolius marmoratus marmoratus collected in southern Natal, South Africa. Parasite prevalence varied from 14.5 to 47.4% and the mean intensity from 1.0 to 1.1. The hamuli of the new species have a characteristic, partly fragmented appearance, a feature also seen in Polystoma batchvarivi, the only other polystome described from a species of the genus Hyperolius. The similarity between the two species, in spite of their geographical separation, is commented upon.     

Sperm-egg interaction in the painted frog (Discoglossus pictus): An ultrastructural study

The ultrastructure of sperm changes and penetration in the egg was studied in the anuran Discoglossus pictus, whose sperm have an acrosome cap with a typical tip, the apical rod. The first stage of the sperm apical rod and acrosome reaction (AR) consists in vesiculation between the plasma membrane and the outer acrosome membrane. The two components of the acrosome cap are released in sequence. The innermost component (component B) is dispersed first. The next acrosome change is the dispersal of the outermost acrosome content (component A). At 30 sec postinsemination, when the loss of component B is first observed, holes are seen in the innermost jelly coat (J1), surrounding the penetrating sperm. Therefore, this acrosome constituent might be related to penetration through the innermost egg investments. At 1 min postinsemination, during sperm penetration into the egg, a halo of finely granular material is observed around the inner acrosome membrane of the spermatozoon, suggesting a role for component A at this stage of penetration. Gamete-binding and fusion take place between D1 (the egg-specific site for sperm interaction) and the perpendicularly oriented sperm. Spermatozoa visualized at their initial interaction (15 sec postinsemination) with the oolemma are undergoing vesiculation. The first interaction is likely to occur between the D1 glycocalyx and the plasma membrane of the hybrid vesicles surrounding the apical rod. As fusion is observed between the internal acrosome membrane and the oolemma, it can be postulated that gametic interaction might be followed by fusion of the latter with the apical rod internal membrane that extends posteriorly into the inner acrosome membrane. Insemination of the outermost jelly layer (J3) dissected out of the egg, and observations of the ultrastructural changes of spermatozoa in this coat, indicate that J3 rather than the vitelline coat (VC) induces the AR. Interestingly, at the late postinsemination stage, VC fibrils are seen crosslinking the inner acrosome membrane. The role of this binding is here discussed. Mol. Reprod. Dev. 47:323–333, 1997. © 1997 Wiley-Liss, Inc.     

Inter-male Spacing and Aggression in African Painted Reed Frogs,Hyperolius marmoratus

Inter-male spacing and the role of aggression in the maintenance of spatial organization was examined in choruses of Hyperolius marmoratus males housed in a semi-natural enclosure. The effects of chorus size on spacing patterns, nearest neighbour distances and male aggressive behaviour were examined. Males were found to reduce nearest neighbour distances as chorus size increased. This was accompanied by a shift in spacing pattern from even in small choruses (5–9 males) to random in choruses of 10 to 13 males. In choruses of 14, spacing patterns were once again even. The reason for these shifts is unclear but may reflect a sudden, rather than gradual increased tolerance by individuals to high neighbour call intensity as space to call from becomes more limited. The level of male aggression was influenced by chorus size and the time of night. In general, more aggressive interactions occurred in high density choruses. However, this did not translate into higher levels of individual male aggression as density increased. Individual male aggression was high in early evening choruses and declined to a minimum at peak chorusing time. High levels of aggression during early evening may reflect the establishment of calling sites by males, while the drop in aggression at peak chorusing time may occur in response to the presence of females in the chorus at this time or as a consequence of masking of neighbours calls.     

A scanning electron microscopic study of differentiation of the digital pad in regenerating digits of the kenyan reed frog,Hyperolius viridiflavus ferniquei

Newly metamorphosed Kenyan reed frogs, Hyperolius viridiflavus ferniquei, are able to regenerate amputated digits. The terminal digital pad is also completely reformed. Differentiation of the regenerating digital pad was studied by scanning electron microscopy. External differentiation of the digital pad began late in the second postamputational week with the appearance of small patches of specialized epidermal cells on the ventral surface of the regenerating digit. The differentiation of the pad spread out radially until late in the fourth week, when its overall shape approximated that of the normal digital pad. The appearance of patches of digital pad epidermis on the ends of spike regenerates arising from the forearm was also confirmed.     

Calling Behaviour Influences Mating Success in Male Painted Reed Frogs,Hyperolius marmoratus

A detailed study was made of the natural calling behaviour of male painted reed frogs in the wild. Comprehensive minute by minute records of the vocal activity of males calling simultaneously in the breeding chorus were generated over a 19-night period using a multi-channel event recorder. With few exceptions, the period over which males called either spanned or extended beyond the time window when females sought mates in the chorus. Males varied little in calling persistence and the majority produced advertisement calls during each minute of the calling period. Aggressive interactions between males curtailed advertisement call production but fights were short-lived, seldom repeated and limited to a small proportion (12.6%) of males. Call rate was independent of body size and varied widely among males active in the chorus at the same time and under the same environmental conditions. The relative call rate ranks of individuals were sustained over time. The call rates of mated males were high in relation to the rates of other males monitored in the chorus at, and prior to, the time of mating. Females usually preferred the higher of two call rate alternatives presented in a range of two-choice phonotaxis experiments.