Hyperolius Marmoratus Research Articles

ILLUSTRATED TYPE CATALOGUE OF THE “LOST” HERPETOLOGICAL COLLECTIONS OF MUSEU DO DUNDO, ANGOLA

The herpetological collections of the Museu do Dundo in Lunda Norte Province, northeast Angola, are among the most important in southern Africa and represent one of the largest collections of Angolan amphibians and reptiles in the world. The collection comprises more than 2,750 preserved specimens, including type specimens of taxa described by Raymond F. Laurent during the 1950s and 1960s, when he was affiliated with the Musée royal de l'Afrique centrale (RMCA) in Tervuren, Belgium, and the Museum of Comparative Zoology (MCZ) at Harvard University, Cambridge, Massachusetts, where portions of these type series were also deposited. We provide details for all type specimens and summarize the history and taxonomy for each species represented in the type collection. The collections contain type specimens of 28 amphibian and reptile species, including seven snakes: Typhlops praeocularis lundensis, Dispholidus typus punctatus, Lycodonomorphus subtaeniatus, Lycophidion hellmichi, Gonionotophis brussauxi prigoginei, Prosymna ambígua brevis, and Elapsoidea decosteri huilensis; 13 lizards: Rhoptropus boultoni montanus, Rhoptropus taeniostictus, Hemidactylus nzingae, Lygodactylus tchokwe, Cordylus vittifer machadoi, Chamaesaura anguina oligopholis, Gerrhosaurus bulsi, Nucras scalaris, Ichnotropis bivittata pallida, Mabuya bayonii huilensis, Mabuya ivensii septemlineata, Trachylepis raymondlaurenti, and Eumecia anchietae major; one amphisbaenian: Monopeltis vanderysti vilhenai; and seven frogs: Hyperolius machadoi, Hyperolius marmoratus alborufus, Hyperolius vilhenai, Ptychadena grandisonae, Ptychadena loveridgei, Ptychadena perplicata, and Ptychadena upembae machadoi. The type specimens of the snake Xenocalamus bicolor machadoi were not found in the collections. A brief history of the museum and remarks on the overall herpetological collections are also provided. We also note additional information about the related type material of these taxa at the MCZ.

Monophyly of the species of Hepatozoon (Adeleorina: Hepatozoidae) parasitizing (African) anurans, with the description of three new species from hyperoliid frogs in South Africa.

Haemogregarines (Apicomplexa: Adeleiorina) are a diverse group of haemoparasites reported from almost all vertebrate classes. The most commonly recorded haemogregarines to parasitize anurans are species of Hepatozoon Miller, 1908. To date 16 Hepatozoon species have been described from anurans in Africa, with only a single species, Hepatozoon hyperolli (Hoare, 1932), infecting a member of the Hyperoliidae. Furthermore, only two Hepatozoon species are known from South African anurans, namely Hepatozoon theileri (Laveran, 1905) and Hepatozoon ixoxo Netherlands, Cook and Smit, 2014, from Amietia delalandii (syn. Amietia quecketti) and three Sclerophrys species, respectively. Blood samples were collected from a total of 225 individuals representing nine hyperoliid species from several localities throughout northern KwaZulu-Natal, South Africa. Twenty frogs from three species were found positive for haemogregarines, namely Afrixalus fornasinii (6/14), Hyperolius argus (2/39), and Hyperolius marmoratus (12/74). Based on morphological characteristics, morphometrics and molecular findings three new haemogregarine species, Hepatozoon involucrum Netherlands, Cook and Smit n. sp., Hepatozoon tenuis Netherlands, Cook and Smit n. sp. and Hepatozoon thori Netherlands, Cook and Smit n. sp., are described from hyperoliid hosts. Furthermore, molecular analyses show anuran Hepatozoon species to be a separate monophyletic group, with species isolated from African hosts forming a monophyletic clade within this cluster.

Does restricted access limit management of invasive urban frogs?

Management recommendations that target urban invaders should consider environmental and socio-economic aspects peculiar to the urban landscape. Urbanization often leads to the fragmentation of the invaded landscape into subunits inaccessible to managers (restricted access) or for which detailed information is lacking. Using models to explore impact of these limitations on management success provides a useful approach to propose effective countermeasures. Here we deploy a spatially explicit age-structured model applied to a pond network to investigate how restricted access and lack of detailed information may affect management of three invasive anuran species across a peri-urban landscape. The target species, the guttural toad Sclerophrys gutturalis, the African clawed frog Xenopus laevis and the painted reed frog Hyperolius marmoratus, belong to different ecotypes (terrestrial, aquatic and arboreal, respectively) and have different life history traits. We show that restricted property access significantly constrains management success in two of the three species (the guttural toad and the painted reed frog), while lack of detailed information around the invaded landscape impedes successful management in only one species (the guttural toad). The species-dependent response we detected is due to contrasting demographic and spatial invasion dynamics linked to the different anuran ecotypes. Our work highlights the necessity to adopt a context-dependent approach when proposing management recommendations in urban environment.

Invasive amphibians in southern Africa: A review of invasion pathways

Background: Globally, invasive amphibians are known for their environmental and social impacts that range from poisoning of local fauna and human populations to direct predation on other amphibians. Although several countries on most continents have had multiple introductions of many species, southern Africa appears to have escaped allochthonous introductions. Instead, it has a small number of domestic exotic species that have rapidly expanded their ranges and established invasive populations within South Africa. Objectives methods: We used the literature to provide a historical overview of dispersal by some of the world’s major invasive amphibians, give examples of species that are commonly moved as stowaways and discuss historical and current amphibian trade in the region. In addition, we give an overview of new South African legislation and how this is applied to amphibian invasions, as well as providing updates on the introduced populations of three domestic exotics: Hyperolius marmoratus, Sclerophrys gutturalis and Xenopus laevis. Results: We show that frogs are mainly moved around southern Africa through ‘jump’ dispersal, although there are a number of records of ‘cultivation’, ‘leading-edge’ and ‘extreme long-distance’ dispersal types. Important pathways include trade in fruit and vegetables, horticultural products and shipping containers. Conclusion: We suggest that southern Africa is becoming more vulnerable to amphibian invasions because of an increase in trade, agricultural and domestic impoundments as well as global climate change. Increasing propagule pressure suggests that preventing new introductions will become a key challenge for the future. Currently, trade in amphibians in the region is practically non-existent, suggesting potential for best practice to prevent importation of species with high invasion potential and to stop the spread of disease.

Mycobacterial Arthritis and Synovitis in Painted Reed Frogs (Hyperolius marmoratus)

Several species of atypical mycobacteria have been isolated from wild and captive amphibians. In captive anurans, cutaneous and visceral mycobacteriosis are common and can result in significant mortality, particularly when animals are immunocompromised. Mycobacterial arthritis and synovitis are reported rarely in amphibians. We describe 20 cases in painted reed frogs (Hyperolius marmoratus), which presented with cachexia, limb paresis or paralysis or 'spindly leg syndrome'. Histopathology revealed multifocal histiocytic to granulomatous synovitis affecting appendicular, rib or spinal intervertebral joints. Periarticular granulomata, granulomatous cellulitis and skeletal muscle atrophy, necrosis and degeneration were also present. In one case, granulomatous spinal osteomyelitis was recorded. Ziehl-Neelsen stains showed large numbers of acid-fast bacteria in macrophages and histiocytes. The mycobacterial isolates obtained from culture were identified as members of the Mycobacterium chelonae complex (either M. chelonae or Mycobacterium abscessus). This was confirmed by 5'-16S ribosomal ribonucleic acid (rRNA) sequencing. In 17 cases mycobacterial lesions were present only in the joints and skeleton, highlighting the importance of not ruling out mycobacterial infection on the basis of absence of cutaneous or visceral lesions.

Plasticity of thermal tolerance and metabolism but not water loss in an invasive reed frog

Phenotypic plasticity may buffer the selection pressures on organisms that inhabit novel or rapidly-changing environments. We investigated plasticity of thermal tolerance, energetic and water loss traits and their interaction with behaviour in a small-bodied, arboreal anuran (Hyperolius marmoratus Rapp, Hyperoliidae) undergoing rapid range expansion into the winter rainfall region of South Africa. After short-term exposure to three temperatures (acclimation treatments) commonly encountered in their historical and novel ranges, frogs exhibited a broad thermal tolerance range (mean±s.d.: 42.1±2.9°C) and higher plasticity in CTmax than in CTmin. Resting metabolic rate was lowest in cold-acclimated animals, while active metabolic rates were lowest in warm-acclimated frogs, likely reflecting compensation towards energy conservation. Evaporative water loss was not significantly altered by the acclimation treatments in either resting or active animals, indicating limited plasticity in this trait compared to metabolism. Our results suggest that plasticity of temperature limits and metabolism may benefit this species in variable environments such as those encountered in its expanded range. Lack of plasticity in water loss during resting and activity suggests that these frogs rely on their high cutaneous resistance and behavioural means to buffer climate variation. This study highlights the importance of synergistic interactions between physiology and behaviour in determining amphibian responses to temperature variation.

Existing and emerging high impact invasive species are characterized by higher functional responses than natives

Predicting ecological impacts of invasive species and identifying potentially damaging future invaders are research priorities. Since damage by invaders is characterized by their depletion of resources, comparisons of the 'functional response' (FR; resource uptake rate as a function of resource density) of invaders and natives might predict invader impact. We tested this by comparing FRs of the ecologically damaging 'world's worst' invasive fish, the largemouth bass (Micropterus salmoides), with a native equivalent, the Cape kurper (Sandelia capensis), and an emerging invader, the sharptooth catfish (Clarias gariepinus), with the native river goby (Glossogobius callidus), in South Africa, a global invasion hotspot. Using tadpoles (Hyperolius marmoratus) as prey, we found that the invaders consumed significantly more than natives. Attack rates at low prey densities within invader/native comparisons reflected similarities in predatory strategies; however, both invasive species displayed significantly higher Type II FRs than the native comparators. This was driven by significantly lower prey handling times by invaders, resulting in significantly higher maximum feeding rates. The higher FRs of these invaders are thus congruent with, and can predict, their impacts on native communities. Comparative FRs may be a rapid and reliable method for predicting ecological impacts of emerging and future invasive species.

Effects of Different Fire Regimes on Amphibian Communities in the Nyika National Park, Malawi

Fire is a frequent feature of African grasslands because agriculture is often used as a management tool in conservation areas. Richness, diversity, and abundance of amphibians were compared in four areas of montane grassland subjected to different fire regimes in Nyika National Park (Malawi, southeastern Africa). The surveys were performed using drift fences and pitfall traps randomly set in four areas (12 sites) subjected to the following fire regimes: (A) no fire for at least 15 years; (B) no fire for at least 10 years; (C) no fire for at least 6 years; and (D) annually burned. We also measured the vegetation cover and vegetation height. We collected 370 amphibians from 17 species and six families during 50 days sampling period. The lowest value of abundance was found in areas C and D. The amphibian species Hyperolius marmoratus and H. nasutus were most abundant in the control area A. Arthroleptis xenodactyloides, Amietophrynus gutturalis and Am. maculatus were found in all areas. There was a strong correlation between vegetation height and species richness. Vegetation structure, which is affected by fire, appears to be a key factor impacting amphibian assemblages in montane grasslands.

Farm dams facilitate amphibian invasion: Extra‐limital range expansion of the painted reed frog in South Africa

AbstractDriven by the mobility of organisms and novel habitats created by anthropogenic changes of landscape structure and climate, range expansion can modify the functioning of recipient ecosystems by altering ecosystem processes such as intra‐ and cross‐trophic biotic interactions. We explain the spatial and temporal dynamics of the recent range expansion of painted reed frogs (Hyperolius marmoratus Rapp) in the Western Cape Province of South Africa. We identify the geographical and temporal origin of expansion, quantify extent of occurrence, internal range structure and habitat characteristics of occupied sites. The painted reed frog was introduced into its novel range during 1997 or early 1998, and is now widespread. Highly variable annual spread rates suggest both diffusion‐based and human‐mediated jump dispersal as drivers of the range expansion. Spatial structure is evident at the scale of the entire novel range, with two distinct populations separated by at least 100 km of unoccupied terrain. Models show that occupancy is limited by summer aridity, low winter temperatures and the absence of fringing vegetation around water bodies. The range structure and the presence of breeding populations in 26% of water bodies surveyed imply that there are further opportunities for range expansion across the network of artificial water bodies available. We infer that, facilitated by human‐mediated jump dispersal and the dense distribution of perennial farm dams, painted reed frogs have colonized the winter rainfall region of south‐western South Africa and fit the description of ‘urban exploiters’. Unspecialized habitat requirements, rapid spread and high local population sizes further suggest that they could compete with co‐occurring endemic frogs and hamper the conservation of these range‐restricted amphibians.

Afrobatrachian mitochondrial genomes: genome reorganization, gene rearrangement mechanisms, and evolutionary trends of duplicated and rearranged genes.

BackgroundMitochondrial genomic (mitogenomic) reorganizations are rarely found in closely-related animals, yet drastic reorganizations have been found in the Ranoides frogs. The phylogenetic relationships of the three major ranoid taxa (Natatanura, Microhylidae, and Afrobatrachia) have been problematic, and mitogenomic information for afrobatrachians has not been available. Several molecular models for mitochondrial (mt) gene rearrangements have been proposed, but observational evidence has been insufficient to evaluate them. Furthermore, evolutionary trends in rearranged mt genes have not been well understood. To gain molecular and phylogenetic insights into these issues, we analyzed the mt genomes of four afrobatrachian species (Breviceps adspersus, Hemisus marmoratus, Hyperolius marmoratus, and Trichobatrachus robustus) and performed molecular phylogenetic analyses. Furthermore we searched for two evolutionary patterns expected in the rearranged mt genes of ranoids.ResultsExtensively reorganized mt genomes having many duplicated and rearranged genes were found in three of the four afrobatrachians analyzed. In fact, Breviceps has the largest known mt genome among vertebrates. Although the kinds of duplicated and rearranged genes differed among these species, a remarkable gene rearrangement pattern of non-tandemly copied genes situated within tandemly-copied regions was commonly found. Furthermore, the existence of concerted evolution was observed between non-neighboring copies of triplicated 12S and 16S ribosomal RNA regions.ConclusionsPhylogenetic analyses based on mitogenomic data support a close relationship between Afrobatrachia and Microhylidae, with their estimated divergence 100 million years ago consistent with present-day endemism of afrobatrachians on the African continent. The afrobatrachian mt data supported the first tandem and second non-tandem duplication model for mt gene rearrangements and the recombination-based model for concerted evolution of duplicated mt regions. We also showed that specific nucleotide substitution and compositional patterns expected in duplicated and rearranged mt genes did not occur, suggesting no disadvantage in employing these genes for phylogenetic inference.

Effect of land use on anuran species composition in north-eastern KwaZulu-Natal, South Africa

Human induced landscape change is a major driver of biodiversity of loss and landscape homogeneity. North-eastern KwaZulu-Natal, South Africa, is an area of high biodiversity as well as increased human urban development and changing land use. We assessed the effects of various agricultural land uses on anuran species composition within this area. Anuran species composition was examined over three strata namely: land use, season and habitat. Land use types surveyed were eucalyptus (Eucalyptus sp.) plantations (n = 4), sugar cane (Saccharum officinarum) farms (n = 4) and conservation areas (n = 5). Sampling was split into three sampling periods: early (Oct–Nov), mid (Dec–Jan) and late (Feb–Apr). Each property was sampled once during each of these periods, and three habitat types were sampled: open water bodies, wetland areas and grassland/woodland complexes. Pit-fall traps with drift-net fences and vocalizations were used to identify anuran species. Mean number of anuran species found on conservation, sugar and eucalyptus sites were 13 ± 6.6; 4 ± 1.3; and 3 ± 1.4 respectively. Correspondence Analysis (CA) produced eigen values of 0.526, 0.485, 0.435 and 0.363 for the first four axes respectively. These axes accounted for 41.5% of the total inertia. Sites within the CA were classified according to land use, season and habitat. Sugar and eucalyptus plantations had lower variation between sites, and low variation in habitat type. Low anuran species richness in the eucalyptus and sugar cane areas is most likely lack of suitable habitat for species that are either totally dependent or totally not dependent on water bodies. Absence of Hyperolius marmoratus and Amietophrynus gutturalis was the factor defining the first division (eigen value 0.498) produced by the TWINSPAN analysis. The two groups produced were significantly different in terms of land use, habitat and season. Land use, particularly sugar cane and agroforestry plantations, had an impact on anuran species presence and composition, and needs to be considered in management for their conservation.

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.

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

ABSTRACTLocal 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 (ΦST = 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.

Phonotaxis and chorus organization in African frogs

Detailed studies of the phonotactic behavior and chorus organization of several species of African amphibians were conducted from 1982–1992. A range of phonotactic experiments conducted in two- and three-dimensional arenas, using between one and four loudspeakers and a variety of different stimuli were carried out on the painted reed frog (Hyperolius marmoratus). These experiments revealed the remarkable ability of very small anurans (<30 mm, SVL) to accurately localize a sound source, in both the horizontal and vertical planes. Furthermore, females were able to discriminate between two sound sources that differed in intensity by only 5 dB and their ability was significantly impaired by the introduction of further sound sources. The confounding effect of multiple sound sources on female choice may explain the presence of nonrandom mating with respect to size in this species. The chorus organization of five species of African anurans was investigated by using playback experiments. These experiments revealed four distinct categories of chorus organization which can be plotted on a continuum, from random calling to very precise triggered responses. The type of chorus organization was found to be directly related to the length of the call and the delay in response to the playback stimulus.

Consistency of calling performance in male Hyperolius marmoratus marmoratus: implications for male mating success

The calling behaviour of male Hyperolius marmoratus marmoratus was monitored continuously over a 21 day period in the laboratory. These data were then compared to the results of a study of calling behaviour and mating success in a natural population of these frogs. Males were classified as callers, intermittent callers or noncallers depending on their level of calling performance. We propose that intermittent calling behaviour allows a male to extend chorus attendance when levels of male-male competition are low. The frogs classified as callers in the captive population showed a high degree of repeatability in call rate (0.464) between nights. In accordance with this, there was no significant difference between a male's calling behaviour on the first and last nights of calling. These results have important implications for male mating success. The consistency of a caller's behaviour facilitates female choice based on male call rate which is evident on a nightly basis, as males that are going to mate call at faster rates than their unmated competitors. Additionally, time spent calling and total number of calls produced showed more within male variation than was found for call rate with repeatabilities of 0.233 and 0.208, respectively. This result is not surprising as males that mate do so early in the evening and thus produce fewer calls and spend less time calling than those that do not mate.

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.

The relative importance of bladder versus neotenic stages of Polystoma marmorati and P. umthakathi in natural frog populations in South Africa

AbstractInfection levels of Polystoma marmorati (Polystomatidae: Monogenea) in the painted reed frog, Hyperolius marmoratus, and P. umthakathi in the kloof frog, Natalobatrachus bonebergi, were studied under natural conditions. The recorded prevalence for P. marmorati was generally high in adult frogs and low in tadpoles. In the case of P. umthakathi, the opposite was found with a low prevalence in adult frogs and a very high prevalence in tadpoles. Based on these findings, the hypothesis is presented that for P. marmorati the neotenic stage does not play a determining role and the population is maintained by bladder parasites. For P. umthakathi the neotenic stage appears to be more important than the bladder parasite and the population can probably survive without any significant contribution from bladder parasites.

A preliminary biochemical genetic survey of four South African painted reed frog (Hyperolius marmoratus) populations

Allozyme electrophoresis was used to evaluate genetic variability in painted reed frog (Hyperolius marmoratus) populations from the Northern Province and the Eastern Cape. Sixteen protein-encoding loci were resolved, of which seven displayed allelic polymorphism. Average heterozygosity (H) values in two permanent H. m. taeniatus populations from the Northern Province (7.9% and 6.3%) did not differ substantially from each other nor from the geographically distant Eastern Cape H. m. verrucosus (9.1%). An isolated Northern Province H. m. taeniatus population displayed more polymorphism than any other group with H=14.1%, which can probably be attributed to the periodic influx of reed frogs following dry periods. Genetic distances and gene diversity (FST) values conformed with expected values for conspecific populations. The results attained concur with the hypothesis of increased genetic heterogeneity among populations of small and relatively sedentary animals

Regulation of body water balance in reedfrogs (superspecies Hyperolius viridiflavus and Hyperolius marmoratus: Amphibia, anura, hyperoliidae) living in unpredictably varying savannah environments

The regulation of body water balance was examined in the reedfrogs Hyperolius marmoratus taeniatus and Hyperolius viridiflavus ommatostictus. Temperature and stage of post-metamorphic development significantly affected the rate of water uptake. Hydrated reedfrogs prevented hyperhydration by voiding diluted urine when obtaining water. Within 48 hr after rehydration, body fluid osmolality remained at low levels, which may be supportive to counter excessive cutaneous water influx in hydrated frogs. Once evaporative water loss exceeded 10–12% total body mass, reedfrogs became anuric. The rate of water uptake strongly increased with increasing body water deficit. Both the anuric response and the increased rate of water uptake are assumed to strongly enhance the efficacy of using very briefly available water sources during dry-period conditions. Dry-adapted and estivating reedfrogs survived evaporative water losses between 40 and 55% total body mass. Bladder fluid stores contributed substantially to this desiccation tolerance. During a 16-day period of desiccation, H. v. ommatostictus could replace approximately 25% of evaporative water loss from the bladder fluid store. During desiccation, the level of free amino acids selectively increased in the gastrocnemius muscle tissue, which may support cell volume regulation and/or protect cellular structures from osmotic stresses. Even strongly dehydrated reedfrogs rehydrated quickly with no obvious osmoregulatory problem. Rehydration was associated with a higher than expected decrease of free amino acids in the gastrocnemius muscle tissue, a response that may help to protect cells from bursting during fast rehydration.

Costs and benefits of mate choice in the lek-breeding reed frog,Hyperolius marmoratus

Direct benefits to females of choosing mates have recently been suggested to play a role in the evolution of female preferences even in non-resource-based mating systems. Direct benefits affect the fecundity or survival of females whereas females gain indirectly from being choosy by passing on good genes to offspring or by producing sons that are themselves more attractive to females. I investigated two potential direct benefits that females gain from being choosy in the lek-breeding painted reed frog, Hyperolius marmoratus broadleyi: assurance of fertilization and reduction in search costs. Males did not differ in their fertilization rates, indicating that choosy females did not benefit by gaining higher rates of fertilization. However, costs of mate searching were high due to predation risk by brown water snakes, Lycodonomorphus rufulus, at the breeding site. Small natural choruses were monitored using an acoustic localization technique based on the measurement of arrival time differences of a male's signal at an array of microphones. Females preferred males that were near to their release site and that called at high rates. These preferences were corroborated experimentally in two-choice arena trials and are consistent with the notion that females should reduce search time under high predatory pressure. Because sampling costs are high, females are selected to reduce search time and males are predicted to call so that females can locate them easily. High sampling costs also make direct selection on female preferences a plausible solution to the lek paradox.