Contrasting effects of functionally distinct tadpole species on nutrient cycling and litter breakdown in a tropical rainforest stream

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Wild justice and fair play: cooperation,forgiveness, and morality in animals

In this paper I argue that we can learn much about ‘wild justice’ and the evolutionary origins of social morality – behaving fairly – by studying social play behavior in group-living animals, and that interdisciplinary cooperation will help immensely. In our efforts to learn more about the evolution of morality we need to broaden our comparative research to include animals other than non-human primates. If one is a good Darwinian, it is premature to claim that only humans can be empathic and moral beings. By asking the question ‘What is it like to be another animal?’ we can discover rules of engagement that guide animals in their social encounters. When I study dogs, for example, I try to be a ‘dogocentrist’ and practice ‘dogomorphism.’ My major arguments center on the following ‘big’ questions: Can animals be moral beings or do they merely act as if they are? What are the evolutionary roots of cooperation, fairness, trust, forgiveness, and morality? What do animals do when they engage in social play? How do animals negotiate agreements to cooperate, to forgive, to behave fairly, to develop trust? Can animals forgive? Why cooperate and play fairly? Why did play evolve as it has? Does ‘being fair’ mean being more fit – do individual variations in play influence an individual's reproductive fitness, are more virtuous individuals more fit than less virtuous individuals? What is the taxonomic distribution of cognitive skills and emotional capacities necessary for individuals to be able to behave fairly, to empathize, to behave morally? Can we use information about moral behavior in animals to help us understand ourselves? I conclude that there is strong selection for cooperative fair play in which individuals establish and maintain a social contract to play because there are mutual benefits when individuals adopt this strategy and group stability may be also be fostered. Numerous mechanisms have evolved to facilitate the initiation and maintenance of social play to keep others engaged, so that agreeing to play fairly and the resulting benefits of doing so can be readily achieved. I also claim that the ability to make accurate predictions about what an individual is likely to do in a given social situation is a useful litmus test for explaining what might be happening in an individual's brain during social encounters, and that intentional or representational explanations are often important for making these predictions.     

Cyanosis by methemoglobinemia in tadpoles of Cochranella granulosa (Anura: Centrolenidae)

Tadpoles inhabit generally well oxygenated rivers and streams, nevertheless they were found in areas with limited oxygen availability inside the rivers. To assess this feature, I examined factors that influence centrolenid tadpole behaviour using Cochranella granulosa. The tadpoles were reared in well-oxygenated and hypoxic environments and their development, survivorship and growth were compared. The tadpoles in oxygenated water acquired a pale color, while tadpoles in hypoxic water grew faster and were bright red and more active. In the oxygenated water, the ammonium, which had its origin in the tadpoles' urine and feces, was oxidized to nitrate. In contrast, in the hypoxic treatment, the nitrogen compounds remained mainly as ammonium. Presumably, the nitrate in oxygenated water was secondarily reduced to nitrite inside the long intestine coils, because all symptoms in the tadpoles point to methemoglobinemia, which can occur when the nitrite passes through the intestine wall into the bloodstream, transforming the hemoglobin into methemoglobin. This could be checked by a blood test where the percentage of methemoglobin was 2.3% in the blood of tadpoles reared in hypoxic condition, while there was a 19.3% level of methemoglobin in the blood of tadpoles reared in oxygenated water. Together with the elevated content of methemoglobin, the growth of the tadpoles was delayed in oxygenated water, which had high nitrate content. The study about quantitative food-uptake showed that the tadpoles benefit more from the food in hypoxic water, although they spent there more energy moving around than the tadpoles living in oxygenated but nitrate-charged water.     

The Reproductive Biology and Larvae of the First Tadpole-Bearing Frog,Limnonectes larvaepartus

Most of the reproductive modes of frogs include an exotrophic tadpole, but a number of taxa have some form of endotrophic development that lacks a feeding tadpole stage. The dicroglossid frog genus Limnonectes ranges from China south into Indonesia. The breeding biologies of the approximately 60 described species display an unusual diversity that range from exotrophic tadpoles to endotrophic development in terrestrial nests. There have been mentions of oviductal production of typical, exotrophic tadpoles in an undescribed species of Limnonectes from Sulawesi, Indonesia. Here we examine newly collected specimens of this species, now described as L. larvaepartus and present the first substantial report on this unique breeding mode. Typical exotrophic tadpoles that are retained to an advanced developmental stage in the oviducts of a female frog are birthed into slow-flowing streams or small, non-flowing pools adjacent to the streams.     

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Among the Amphibia, cannibalism is most commonly associated with tadpole species that exploit ephemeral systems. This behaviour may confer significant fitness benefits to those that cannibalise, given that these systems generally possess limited food resources, but will incur significant fitness costs to the cannibalised. Herein, we describe cannibalism of recently oviposited eggs of the sandpaper frog (Lechriodus fletcheri) by conspecific tadpoles as a likely adaptation to limited nutrient availability within highly ephemeral pools in which it is an obligate breeder. Field observations revealed L. fletcheri tadpoles actively preyed on conspecific eggs of recently oviposited spawn bodies, which were commonly consumed whole. When tadpoles were exposed to spawn for the first time in laboratory trials, they quickly engaged in extended periods of consumption, gorging themselves until they appeared to be full. We found this behaviour to be common in the field and suggest that conspecific eggs form a significant food resource for tadpoles of this species in the otherwise nutrient-poor systems in which they breed. This feeding strategy might be common among anurans exploiting temporary aquatic systems that are nutrient-poor and gives rise to many questions surrounding how individuals can utilise cannibalism to increase their fitness while simultaneously avoiding becoming victims of this behaviour themselves.     

Embryogenomics: developmental biology meets genomics

Fundamental questions in developmental biology are: what genes are expressed, where and when they are expressed, what is the level of expression and how are these programs changed by the functional and structural alteration of genes? These questions have been addressed by studying one gene at a time, but a new research field that handles many genes in parallel is emerging. The methodology is at the interface of large-scale genomics approaches and developmental biology. Genomics needs developmental biology because one of the goals of genomics – collection and analysis of all genes in an organism – cannot be completed without working on embryonic tissues in which many genes are uniquely expressed. However, developmental biology needs genomics – the high-throughput approaches of genomics generate information about genes and pathways that can give an integrated view of complex processes. This article discusses these new approaches and their applications to mammalian developmental biology.     

A Rapid,Non-invasive Method for Anatomical Observations of Tadpole Vertebrae in Vivo

The tadpole is a critical stage in the amphibian life cycle and plays an important role during the transition from the aquatic to the terrestrial stage.However,there is a large gap in tadpole research,which represents a vital component of our understanding of the diversity and complexity of the life history traits of amphibians,especially their developmental biology.Some aspects of this gap are due to limited research approaches.To date,X-ray microcomputed tomography(micro-CT)has been widely used to conduct osteology research in adult amphibians and reptiles,but little is known about whether this tool can be applied in tadpole studies.Thus,we compared the results of two methods(the bone-cartilage double-staining technique and micro-CT)to study vertebrae in tadpole specimens.The results revealed no significant difference between the two methods in determining the number of vertebrae,and micro-CT represents a rapid,non-invasive,reliable method of studying tadpole vertebrae.When scanning tadpoles,voltage is the most critical of the scanning parameters(voltage,current and scan time),and moderate scanning parameters are recommended.In addition,micro-CT performed better using specimens stored in 70% ethanol than those preserved in 10% formalin.Finally,we suggest that micro-CT should be more widely applied in herpetological research to increase specimen utilization.     

Trophic roles of tadpoles in tropical Australian streams

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Spatial and temporal distribution of tadpole assemblages (Amphibia,Anura) in a seasonal dry tropical forest of southeastern Brazil

We determined spatial and temporal distribution of tadpoles in 11 breeding habitats from Morro do Diabo State Park (MDSP), southeastern Brazil. Breeding habitats occupancy by tadpoles was tested to be different from a null model of random placement of species. We also tested whether tadpole occupancy in a given breeding habitat is organized according to different ecomorphological guilds, and we analyzed spatial partitioning of tadpoles among breeding habitats through similarity analysis. For temporal analysis we analyzed temporal partitioning of tadpole monthly occurrence also using similarity analysis, and assessed what climatic variable better predicts tadpole temporal occurrence in the MDSP, through regression analysis. Among tadpoles from 19 anuran species, distribution was different from a null model, but co-occurrence patterns among the breeding habitats did not differ among different guilds. However, breeding habitats with similar hydroperiods had similar species composition, which may be related to the reproduction patterns of species. Among the three climatic variables analyzed (rainfall, temperature, and photoperiod), temporal occurrence of monthly tadpole richness and abundance was correlated with temperature and rainfall. Most species were found only during the rainy season months, and overlap occurred within three groups of species. Thus, temporal distribution does not seem to be an important mechanism in species segregation at the MDSP, where the dry season is pronounced. In this case, spatial partitioning tends to be more important for species coexistence.     

Where the Tadpole Meets the World--Observations and Speculations on Biomechanical and Biochemical Factors that Influence Metamorphosis in Anurans

SYNOPSIS. A diversity of issues related to metamorphosis arediscussed in this paper, ranging from biomechanical constraintson behavior in premetamorphic anurans, to environmental factorsthat regulate metamorphosis. I begin by reviewing key behavioralfeatures of tadpoles that have implications to their form andlocomotion. Tadpoles lack all visceral behaviors, such as emesis, coughing,and egg-laying, that require major elevations of pressure inthe pleuroperitoneal cavity. I suggest that the inability toforcefully elevate pleuroperitoneal pressure is a consequenceof the tadpoles' short and inflexible spine. Although postmetamorphicfrogs have a similarly short vertebral column, they can compressviscera by movement at sacroiliac joints, which are absent intadpoles. I argue that the short torso of tadpoles is a necessaryconsequence of the need to innervate the frog's limbs earlyin development so that they can be fully functional by the endof metamorphosis. The short torso is a good mechanical design for the saltatoryfrog, but afflicts the tadpoles with a distinctly globous shapethat intuitively appears inefficient for aquatic locomotion.Computational fluid dynamics (CFD) models, however, reveal thattadpoles are, in fact, efficient undulatory swimmers comparedto subcarangiform fishes and that their swimming kinematicswork in concert with their shape to help generate thrust. Furthermorethe CFD models show that the crease in the dorsal profile oftadpoles, where the body abruptly meets the tail, produces a"dead water" zone immediately behind the body of the tadpole.As a result, tadpoles can grow hindlimbs in this region withoutthose limbs seriously impeding flow. Thus the shape of tadpolesnicely matches their need to transform into limbed tetrapods. In the latter half of this paper I review ideas on how environmentalfactors could influence metamorphosis in anurans. One speculationis that tadpoles may secrete a metamorphic inhibitor in theiroral mucus, which they then ingest with their food, with theresult that metamorphosis is delayed when food is abundant.An epidermal growth factor-like peptide has been suggested asa possible metamorphic inhibitor along the pathway just proposed.Strengths and weaknesses of this hypothesized agent and pathwayare reviewed. An experiment to test the hypothesis that orallyingested EGF inhibits metamorphosis yielded inconclusive results.Orally secreted EGF-like peptide may not inhibit metamorphosisof the tadpole gut, but other yet-to-be-identified factors intadpole oral mucus could still play a role in regulating metamorphosisof the alimentary tract in anurans. The essay ends with some broad speculations on the role thatpeptides in frogs' skin may play in the metamorphic processas well as several unanswered questions about how other organismsand the physical environment influence tadpole metamorphosis.     

Does Biology Need an Organism Concept?

Among biologists, there is no general agreement on exactly what entities qualify as ‘organisms’. Instead, there are multiple competing organism concepts and definitions. While some authors think this is a problem that should be corrected, others have suggested that biology does not actually need an organism concept. We argue that the organism concept is central to biology and should not be abandoned. Both organism concepts and operational definitions are useful. We review criteria used for recognizing organisms and conclude that they are not categorical but rather continuously variable. Different organism concepts are useful for addressing different questions, and it is important to be explicit about which is being used. Finally, we examine the origins of the derived state of organismality, and suggest that it may result from positive feedback between natural selection and functional integration in biological entities.     

Phenotypic plasticity in complex environments: effects of structural complexity on predator‐ and competitor‐induced phenotypes of tadpoles of the wood frog,Rana sylvatica

Theoretical and empirical research has demonstrated that phenotypically plastic responses to one environment are dependent on other environmental attributes. Such research is critical considering the complexity of natural habitats, yet few studies have examined how multiple environments affect patterns of plasticity and the adaptiveness of the resulting phenotypes within complex habitats. The present study examines how wood frog (Rana sylvatica) tadpoles alter their behavioural and morphological phenotypes in response to predation risk from larval diving beetles (Dytiscus spp.), competition from conspecifics, and physical structural complexity. It also tests whether structure affects selection intensities by Dytiscus larvae on tadpole morphological traits. Predation risk and competition induced typical changes to tadpole behaviour and morphology. Structure did not induce changes to any phenotype, nor did it interact with predation risk or competition in affecting phenotypes. Furthermore, structure did not affect the predator selection intensities on any morphological trait. Dytiscus larvae selected for shallow, short tailfins, and large tail muscles, yet tadpoles only developed deep tail muscles when raised in the presence of predator cues. These apparently maladaptive responses may have been a result of correlations between phenotypes. The present study expands plasticity research by examining the adaptiveness of plastic responses in complex environments. Additionally, the present study demonstrates that not all environments induce plastic responses. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 853–863.     

Plant—herbivore interactions in streams near Mount St Helens

1. In four separate field experiments near Mount St Helens (Washington, U.S.A.) during 1986, the grazing effects of two large benthic herbivores, tadpoles of the tailed frog Ascaphus truei and larvae of the caddisfly Dicosmoecus gilvipes, were investigated using streamside channels and in-stream manipulations. In the experimental channels, abundances of periphyton and small benthic invertebrates declined significantly with increasing density of these larger herbivores. 2. In eleven small, high-gradient streams affected to varying degrees by the May 1980 eruption, in-stream platforms were used to reduce grazing by A, truei tadpoles on tile substrates. Single platforms erected in each tributary and compared to grazed controls revealed only minor grazing effects, and no significant differences among streams varying in disturbance intensity (and, consequently, tadpole density). However, results probably were confounded by high variability among streams in factors other than tadpole abundance. 3. Grazing effects were further examined in two unshaded streams with different tadpole densities, using five platforms per stream. In the stream with five tadpoles m^?2, grazing reduced periphyton biomass by 98% and chlorophyll a by 82%. In the stream lacking tadpoles, no significant grazing effects were revealed. Low algal abundance on both platforms and controls, and high invertebrate density in that stream (c. 30000m^?2) suggests that grazing by small, vagile invertebrates was approximately equivalent to that of tadpoles. 4. The influence of large benthic herbivores on algal and invertebrate communities in streams of Mount St Helens can be important, but reponses vary spatially in relation to stream disturbance history, local environmental factors, and herbivore distributional patterns and abundance.     

The thermal environment of arboreal pools and its effects on the metabolism of the arboreal, oophagous tadpoles of a Taiwanese tree frog, Chirixalus eiffingeri (Anura: Rhacophoridae).

We have studied seasonal and diurnal fluctuations of water temperature in bamboo stumps and the effect of temperature on the energy metabolism of arboreal, oophagous tadpoles of Chirixalus eiffingeri. We collected tadpoles (Gosner stage 28-29) in February and August from Chitou, Taiwan and acclimated them to 12 and 22 degrees C. Using a closed system, we measured tadpole oxygen consumption (V.O(2)) at 12, 17 and 22 degrees C. The water temperature was lowest in February (11-13 degrees C), increased rapidly during March and April and was highest from May to August (20-24 degrees C). Diel fluctuations in the temperature of the pools of water in bamboo stumps mirrored fluctuations in air temperature. Tadpoles collected in February and August exhibited metabolic compensation in that tadpoles acclimated at 12 degrees C had significantly higher V.O(2) than those acclimated at 22 degrees C. There are at least two possible explanations for the presence of metabolic compensation in C. eiffingeri tadpoles. Firstly, the larval period of C. eiffingeri ranges from 40 to 78 days, a tadpole could experience relatively large fluctuations in body temperature (up to 10 degrees C) during the development. As a result, C. eiffingeri tadpoles most likely evolved metabolic compensation to maintain activity levels under different thermal environments. Secondly, because arboreal pools are small, thermally unstratified, aquatic microhabitats, tadpoles are unable to behaviorally select preferred temperatures. As a result, metabolic compensation allows tadpoles to regulate their physiological functions.     

Art,Culture and Ambiguity in Wilcannia,New South Wales

The claim of most town whites that Aboriginal people of Wilcannia make art but have no culture and the claim by Aboriginal people of the town that their art work and art designs demonstrate their culture and cultural traditions opens up the powerful and productive dimensions of art and culture for closer scrutiny. In so doing, the ambivalence and ambiguity which saturates these categories is ethnographically revealed. How can the presence and production of artworks in Wilcannia and the white denial of culture be considered? Why indeed do these questions matter, in what ways do they matter, and to whom do they matter? How do the categories of traditional/remote, urban/settled and their avatars intersect with black and white notions of Aboriginal art and Aboriginal culture discursively and experientially?     

A Common Marking Technique Affects Tadpole Behavior and Risk of Predation

In many studies, it is necessary for researchers to mark individual animals for later identification. It is often assumed in the interpretation of these studies that marks have no effects on the biology of the animals. This assumption is insufficiently tested, and, when it is, coarse assessments of negative effects are often used, such as survival and growth under simplified laboratory conditions. We examined the consequences of a common larval amphibian marking technique (staining with methylene blue) for wood frog tadpole behavior and survival in an ecologically realistic scenario (predation). We measured a number of tadpole behavioral variables, under baseline conditions and in the presence of olfactory cues of a predator, for marked and unmarked tadpoles. We then exposed pairs of tadpoles (one marked and one unmarked) to one of two predators and tested for the effects of marking on the susceptibility of tadpoles to predation. We found that marking suppressed the increase in movement rate that typically occurred in (unmarked) tadpoles in the presence of predator cues. Marked tadpoles were significantly more likely to be captured by predators, an effect that could not be attributed to this difference in movement rate. These results raise concern about the use of this staining method and highlight the need for studies involving marked animals to thoroughly address any relevant effects the marks may have on the biology of the subjects.     

Divergent responses of exposed and naive Pacific tree frog tadpoles to invasive predatory crayfish

Invasive predators can devastate native species and ecosystems. However, native species may be able to coexist with invasive predators through a variety of mechanisms, such as changes in morphology or behavior due to a plastic response or selection on fixed anti-predator traits. We examined whether exposed and naive populations of Pacific tree frog tadpoles (Pseudacris regilla) display divergent morphological and behavioral traits in response to the invasive predatory red swamp crayfish (Procambarus clarkii). Tadpoles were collected from three study streams with and three without crayfish, in the Santa Monica Mountains of Southern California. We analyzed tadpole morphology and tested anti-predator behavior and survival in the laboratory. Tadpoles from streams with crayfish had shallower, narrower tails than tadpoles from streams without crayfish. Tadpoles from streams with and without crayfish were less active after exposure to crayfish chemical cues. The divergent morphology of naive and exposed tadpoles is consistent with tadpoles exhibiting a plastic response to crayfish or undergoing selection from crayfish predation. In laboratory predation experiments, we found no difference in survival between tadpoles from streams with and without crayfish but tadpoles that survived predation had deeper tail muscles than those that were killed or injured. Our results suggest that deeper tails are advantageous in the presence of crayfish, yet tadpoles from crayfish streams had shallower tails than those from crayfish-free streams. Shallower tails may have an alternative unmeasured advantage or there may be a physiological constraint to developing deeper tails in the wild. These results highlight the ability of a native frog to respond to an invasive predatory crayfish, potentially allowing for coexistence.     

Spatial dependence of phenotype-environment associations for tadpoles in natural ponds

Within natural habitats, phenotypes are shaped by many environmental factors. Consequently, heterogeneity of these factors can promote phenotypic divergence. However, because environments exhibit heterogeneity at different spatial scales, phenotypic divergence should also exhibit such scale-dependence. Using hierarchical linear models, I determined how multiple environmental factors at two spatial scales affected the morphology of wood frog (Rana (Lithobates) sylvatica) tadpoles collected from natural ponds. Among ponds, predation risk intensity and tadpole density were strong predictors of tadpole morphology, while within ponds, other environmental variables such as water depth and leaf litter were more important. Spatial analyses revealed that water depth and leaf litter, but not predation risk intensity or tadpole density, exhibited heterogeneous spatial distributions within ponds, suggesting that spatial properties of environmental variables influenced the scale at which they shaped phenotypes. Furthermore, patterns of phenotypic variation with respect to predation risk intensity and tadpole density among ponds largely matched observations from previous laboratory studies. These results emphasize the importance of considering phenotype-environment associations across multiple spatial scales.     

Companion-Animal Caregiver Knowledge,Attitudes, and Beliefs Regarding End-of-Life Care

Although awareness of end-of-life care is growing within the veterinary field and there appears to be consumer demand for these services, it is unclear exactly what caregivers know about end-of-life options for their companion animals. Are companion-animal caregivers aware of the range of options for their nonhuman animals? What do they value most highly for their nonhuman animals at the end of life? Answers to these and other related questions about caregiver perceptions are important because what they know about end-of-life care and how they approach decision-making for their companion animals will shape the kind of care an animal receives. This article presents the results of a large survey exploring companion-animal caregivers’ knowledge, attitudes, and beliefs about end-of-life care, including in-home euthanasia, hospice and palliative care, financial commitment to end-of-life care, insurance usage, and level of comfort in providing care (e.g., subcutaneous fluids) in the home.