Behavioral responses to immune-system activation in an anuran (the cane toad, Bufo marinus): field and laboratory studies

The challenges posed by parasites and pathogens evoke behavioral as well as physiological responses. Such behavioral responses are poorly understood for most ectothermic species, including anuran amphibians. We quantified effects of simulated infection (via injection of bacterial lipopolysaccharide [LPS]) on feeding, activity, and thermoregulation of cane toads Bufo marinus within their invasive range in tropical Australia. LPS injection reduced feeding rates in laboratory trials. For toads in outdoor enclosures, LPS injection reduced activity and shifted body temperature profiles. Although previous research has attributed such thermal shifts to behavioral fever (elevated body temperatures may help fight infection), our laboratory studies suggest instead that LPS-injected toads stopped moving. In a thermal gradient, LPS-injected toads thus stayed close to whichever end of the gradient (hot or cold) they were first introduced; the introduction site (rather than behavioral thermoregulation) thus determined body temperature regimes. Shifts in thermal profiles of LPS-injected toads in outdoor enclosures also were a secondary consequence of inactivity. Thus, the primary behavioral effects of an immune response in cane toads are reduced rates of activity and feeding. Thermoregulatory modifications also occur but only as a secondary consequence of inactivity.     

Behavioural thermoregulation of the Andean toad (Bufo spinulosus) at high altitudes

Summary The body temperature of free-ranging Andean toadsBufo spinulosus was measured either directly or radiotelemetrically during two 15-day periods at 3200 m elevation in the Mantaro Valley, Central Perú. All toads attempted to maintain their diurnal sum of body temperature within a narrow range. Consequently thermoregulatory behaviour differed according to cloud cover and precipitation. If the sky was clear, toads emerged from their hiding place and exposed themselves to solar radiation during 3–5 h in the morning. Core temperature increased up to 15° C above the air temperature in shade and reached maximum values of about 32° C. At air temperatures (in sun) exceeding 29° C, toads maintained body temperatures below 32° C by evaporative cooling. Following heliothermic heating during the moring toads retreated to the shade, thereby decreasing body temperature below air temperature. Under overcast sky toads remained exposed during the whole day displaying body temperatures at or slightly above ambient levels. Quantitative models to predict the core temperature of toads under the different weather conditions demonstrated that the substrate temperature was the main energy source accounting for 64.6–77.9% of total variance whereas air temperature was of minor importance (1.5–4.4%). The unexplained variance was probably due to evaporative cooling. The volume of urine stored into the urinary bladder of toads varied diurnally; during basking in the morning hours most bladders contained large volumes of urine, whereas during the afternoon the bladders were mostly empty. The bladder contents probably serve as water reserves during basking when evaporative water loss was high. Toads preferred sites that provided shady hiding places as well as sun-exposed bare soil within a radius of 5 m. However, they frequently changed their centers of activity and moved to other sites in 20–70 m distance after periods of 2–5 days. The helio-and thigmothermic behaviour of the Andean toad permits the maintenance of high core temperature during morning which probably increases the digestion rate and accelerate growth. Evaporative cooling and preference of shady sites were employed to regulate body temperature below the morning levels in response to the constraints of water balance. Periodic changes between thigmothermic behaviour and locomotory activity during the night maintains body temperature above air temperature and prolongs the period of food uptake.Dedicated to Prof. Dr. H. Schneider on the occasion of his sixtieth birthday     

Body temperature in arboreal and nonarboreal anuran amphibians: Differential effects of a small change in water vapor density

1. 1.|Body temperatures (T_b) and contaneous evaporative water loss rates (CWL) were measured in tree frogs (Hyla cinerea) and toads (Bufo valliceps) exposed to cyclical ramp changes in water vapor density (WVD) between 7.5 and 9.8 gm⁻³ (1 cycle h⁻¹ at an air temperature of 27.0°C.

2. 2.|CWL was 3.3 times greater in toads than in tree frogs.

3. 3.|T_b in toads cycled directly with WVd; WVD accounted for 98% of the variation in toad T_b.

4. 4.|T_b in tree frogs was independent of WVD, probably due to changes in skin resistance to water loss.

Daily rhythmic behaviors and thermoregulatory patterns are disrupted in adult female MeCP2-deficient mice

Mutations in the X-linked gene encoding Methyl-CpG-binding protein 2 (MECP2) have been associated with neurodevelopmental and neuropsychiatric disorders including Rett Syndrome, X-linked mental retardation syndrome, severe neonatal encephalopathy, and Angelman syndrome. Although alterations in the performance of MeCP2-deficient mice in specific behavioral tasks have been documented, it remains unclear whether or not MeCP2 dysfunction affects patterns of periodic behavioral and electroencephalographic (EEG) activity. The aim of the current study was therefore to determine whether a deficiency in MeCP2 is sufficient to alter the normal daily rhythmic patterns of core body temperature, gross motor activity and cortical delta power. To address this, we monitored individual wild-type and MeCP2-deficient mice in their home cage environment via telemetric recording over 24 hour cycles. Our results show that the normal daily rhythmic behavioral patterning of cortical delta wave activity, core body temperature and mobility are disrupted in one-year old female MeCP2-deficient mice. Moreover, female MeCP2-deficient mice display diminished overall motor activity, lower average core body temperature, and significantly greater body temperature fluctuation than wild-type mice in their home-cage environment. Finally, we show that the epileptiform discharge activity in female MeCP2-deficient mice is more predominant during times of behavioral activity compared to inactivity. Collectively, these results indicate that MeCP2 deficiency is sufficient to disrupt the normal patterning of daily biological rhythmic activities.     

Circadian change of heat loss in response to change in core temperature in rats

1. 1.|Circadian changes in heat production (M), heat loss (H), core temperature (T_c) and feeding activity (FA) of ad-lib fed rats were observed by direct and indirect calorimetry.

2. 2.|M, H and T_c showed a clear nocturnal increase associated with several discrete increases.

3. 3.|Whereas the slope of M vs T_c relation did not change appreciably within a day, the slope of H vs T_c or thermal conductance vs T_c relation tended to decrease at night, implying that the correlation between heat loss and body temperature is also a function of time of day in rats.

Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads

Prevalence of the pathogen Batrachochytrium dendrobatidis (Bd), implicated in amphibian population declines worldwide, is associated with habitat moisture and temperature, but few studies have varied these factors and measured the response to infection in amphibian hosts. We evaluated how varying humidity, contact with water, and temperature affected the manifestation of chytridiomycosis in boreal toads Anaxyrus (Bufo) boreas boreas and how prior exposure to Bd affects the likelihood of survival after re-exposure, such as may occur seasonally in long-lived species. Humidity did not affect survival or the degree of Bd infection, but a longer time in contact with water increased the likelihood of mortality. After exposure to approximately 10(6) Bd zoospores, all toads in continuous contact with water died within 30 d. Moreover, Bd-exposed toads that were disease-free after 64 d under dry conditions, developed lethal chytridiomycosis within 70 d of transfer to wet conditions. Toads in unheated aquaria (mean = 15 degrees C) survived less than 48 d, while those in moderately heated aquaria (mean = 18 degrees C) survived 115 d post-exposure and exhibited behavioral fever, selecting warmer sites across a temperature gradient. We also found benefits of prior Bd infection: previously exposed toads survived 3 times longer than Bd-na?ve toads after re-exposure to 106 zoospores (89 vs. 30 d), but only when dry microenvironments were available. This study illustrates how the outcome of Bd infection in boreal toads is environmentally dependent: when continuously wet, high reinfection rates may overwhelm defenses, but periodic drying, moderate warming, and previous infection may allow infected toads to extend their survival.     

Survival of the feces: Does a nematode lungworm adaptively manipulate the behavior of its cane toad host?

Parasites can enhance their fitness by modifying the behavior of their hosts in ways that increase rates of production and transmission of parasite larvae. We used an antihelminthic drug to experimentally alter infections of lungworms (Rhabdias pseudosphaerocephala) in cane toads (Rhinella marina). We then compared subsequent behaviors of dewormed toads versus toads that retained infections. Both in the laboratory and in the field, the presence of parasites induced hosts to select higher body temperatures (thereby increasing rates of lungworm egg production), to defecate in moister sites, and to produce feces with higher moisture content (thereby enhancing survival of larvae shed in feces). Because those behavioral modifications enhance rather than decrease parasite fitness, they are likely to have arisen as adaptive manipulations of host behavior rather than as host adaptations to combat infection or as nonadaptive consequences of infection on host physiology. However, the mechanisms by which lungworms alter cane toad thermal preference and defecation are not known. Although many examples of host manipulation by parasites involve intermediate hosts facilitating their own demise, our findings indicate that manipulation of definitive hosts can be as subtle as when and where to defecate.     

Behaviour and body temperature of hibernating common toads Bufo bufo

Hibernation behaviour of six common toads Bufo bufo was studied. Transmitters, generating pulses with a temperature dependent repetition rate, implanted in the toad's abdominal cavity, were used to measure the body temperature. Measurements of body temperature and soil temperature at various depths were used to establish the hibernating depth. All toads moved vertically between a few preferred depths and hibernating depth appeared to vary for individual toads. Upward movements mostly were apparent reactions on changes of the soil temperature gradient at the depth of the toad.     

阿尔泰山前荒漠两种沙蜥体况指数特征及其与生态因子的关系

为明确奇台沙蜥(Phrynocephalus grumgrzimailoi)和旱地沙蜥(P. helioscopus)体况指数的年龄性别特征, 及其与海拔、年均温、年降水量、平均日较差之间的关系, 我们测量了阿勒泰地区84只奇台沙蜥与176只旱地沙蜥的体况数据, 用log体重/log头体长表示体况指数。结果显示: (1)旱地沙蜥与奇台沙蜥间体况指数差异显著。(2)旱地沙蜥体况指数雌雄两性差异不显著, 奇台沙蜥体况指数雌雄两性差异显著。(3)两种蜥蜴成体与亚成体间体况指数均差异明显。(4)以月份为单位, 奇台沙蜥体况指数月份差异明显, 旱地沙蜥体况指数月份差异不明显。(5)年均温对奇台沙蜥体况指数有重要影响, 而年降水量为补充因子, 主要通过与其他生态因子组合发挥作用, 海拔对旱地沙蜥体况指数有影响。这些结果表明两种沙蜥对不同环境因子的反应不同, 在不同环境的适应度也不同。     

The Ability of Three Species of Tadpoles to Differentiate among Potential Fish Predators

The ability of prey to respond to novel predator cues may depend on the generality or specificity of the response to predator cues. We used laboratory behavioral experiments to examine the ability of tadpoles of three species of anurans (American toad, Bufo americanus ; bullfrog, Rana catesbeiana ; and green frog, R. clamitans ) to respond to the presence of two native potential predators (bluegill, Lepomis macrochirus ; and largemouth bass, Micropterus salmoides ) and one non-native potential predator (goldfish, Carassius auratus ). We also examined the effect of tadpole size on the behavioral responses of American toads and green frogs to predator cues. All three species of tadpoles responded to the presence of predator cues, although the specific responses varied among species. American toads and green frogs reduced activity in the presence of at least some fish cues, but bullfrog tadpoles did not change their activity. Bullfrogs decreased use of vegetation in the presence of some predator cues, whereas American toads and green frogs did not. American toads only responded to the presence of bluegill cues but not the other fish predator cues, whereas bullfrogs and green frogs responded more generally to the fish predators. In both American toads and green frogs, tadpole size affected behavior. For American toads, activity increased, as did the use of the vegetated side of the aquarium, in larger tadpoles. Not only did size affect American toad behavior, but it also influenced the responses of the tadpoles to predator cues. For green frogs, activity decreased in larger tadpoles. Our results suggest that behavioral responses of tadpoles to predator cues can be influenced by both the identity of the predator and the prey, as well as the size of the potential prey.     

长爪沙鼠与黑线仓鼠的温度选择比较

本文使用自制的陆生动物温度选择仪,对长爪沙鼠和黑线仓鼠的温度选择进行了比较,结果表明,长爪沙鼠的选择温度(29.06±0.62℃)较黑线仓鼠(26.65±0.64℃)高。这种差异可能与两种鼠的栖息环境及昼夜节律的不同有关。     

Ecdysterone induced sexual reproduction in Opalina sudafricana parasitic in Bufo regularis

Ecdysterone induced sexual reproduction in Opalina sudafricana parasitic in Bufo regularis. International Journal for Parasitology 3: 863–868. Ecdysterone injections (0·5 mg/ml) induced sexual reproduction in Opalina sudafricana parasitic in male or female Bufo regularis after 12 days. Hypophysectomy or gonadectomy did not prevent the hormone from producing its effect on the parasites. Ecdysterone did not induce sexual reproduction in the parasites in vitro. Urine of toads injected with ecdysterone induced the opalinids to encyst in vitro.     

Habitat Selection and Movement of Pond-Breeding Amphibians in Experimentally Fragmented Pine Forests

ABSTRACT Population-level responses of amphibians to forest management regimes are partly dictated by individual behavioral responses to habitat alteration. We examined the short-term (i.e., 24-hr) habitat choices and movement patterns of 3 amphibian species—southern leopard frogs (Rana sphenocephala), marbled salamanders (Ambystoma opacum), and southern toads (Bufo terrestris)—released on edges between forest habitats and recent clear-cuts in the Upper Coastal Plain of South Carolina, USA. We predicted that adult frogs and salamanders would preferentially select forest using environmental cues as indicators of habitat suitability. We also predicted that movement patterns would differ in clear-cuts relative to forests, resulting in lower habitat permeability of clear-cuts for some or all of the species. Using fluorescent powder tracking, we determined that marbled salamanders selected habitat at random, southern toads preferred clear-cuts, and southern leopard frogs initially selected clear-cuts but ultimately preferred forests. Frogs exhibited long-distance, directional movement with few turns. In contrast, toads exhibited wandering behavior and salamanders moved relatively short distances before locating cover. Southern toads and southern leopard frogs moved farther in forests, and all 3 species made more turns in clear-cuts than in forests. Habitat selection by southern toads did not vary according to body size, sex, or the environmental cues we measured. However, marbled salamanders were more likely to enter clear-cuts when soil moisture was high, and southern leopard frogs were more likely to enter clear-cuts when relative humidity and air temperature were higher in the clear-cut than in adjacent forest. Although we found evidence of reduced habitat permeability of clear-cuts for southern leopard frogs and southern toads, none of the species exhibited strong behavioral avoidance of the small (4-ha) clear-cuts in our study. Further studies of long-term habitat use and the potential physiological and other costs to individuals in altered forests are needed to understand the effects of forest management on population persistence. To reduce potentially detrimental effects of clear-cutting on amphibians in the Southeast, wildlife managers should consider the vagility and behavior of species of concern, especially in relation to the size of planned harvests adjacent to breeding sites.     

On the fringe of the invasion: the ecology of cane toads in marginally-suitable habitats

Understanding how invasive species flourish under climatic conditions outside those found within their native range can inform management. In southeastern Australia, cane toads (Rhinella marina) are spreading into montane areas cooler than have been predicted to be suitable. We monitored the presence of active toads in two high-elevation sites (750–1010 m above sea level [asl]) and two adjacent low-elevation sites (150–210 m asl) in northeastern New South Wales over spring and summer. We radio-tracked 28 field-collected adult toads (n = 5–9 toads per site) and quantified their thermoregulatory opportunities and body temperatures. Toads were active at low-elevation sites in spring, but were not seen in high-elevation sites until late summer. At low elevations, toads had access to a wide range of temperatures and selected cool diurnal refugia. In montane sites, toads had less control over their temperatures, because thermal differentials between exposed and sheltered microhabitats were smaller. Overall though, body temperatures of toads at high-elevation sites in summer were not different to those of conspecifics at lower elevations in spring. As a result, toads at high elevations moved as far (mean daily displacement around 50 m) as did low-elevation conspecifics. Toads in high elevations spent the day in superficial shelter, often partly exposed. Thus, although toads only appear in high-elevation sites seasonally, their behaviour at those sites (spending the day exposed; moving extensively at night) likely exacerbates their ecological impact by bringing them to the attention of vulnerable native predators.     

Feeding causes thermophily in the woodhouse's toad (Bufo woodhousii)

(1) We placed 12 toads (Bufo woodhousii) in linear thermal gradients with floor temperatures ranging from 10 to 40 degrees C and monitored body temperatures (T(b)'s) with chromega-alomega thermocouples interfaced with a datalogger. (2) We measured T(b)'s at 10min intervals over a 24h period in toads that had eaten an equivalent of 5% of their body mass or had fasted for 5 days. (3) The mean 24h T(b) did not differ significantly between the fed and fasted groups. (4) Hourly mean T(b)'s of fed toads differed significantly over the 24h, but those of fasted toads did not. Fed toads selected highest T(b)'s during late afternoon and evening.     

The ecological impact of commercial beehives on invasive cane toads (<Emphasis Type="Italic">Rhinella marina</Emphasis>) in eastern Australia

Understanding the factors that affect an invasive species’ viability and distribution has vital implications for biocontrol. In Australia, invasive cane toads (Rhinella marina) are anecdotally reported to utilise commercial beehives as a prey resource, but that interaction has never been studied in detail. We investigated the impact of apiaries on cane toads in northern New South Wales via mark-recapture surveys, dissections, and camera-trap observations. Cane toads were the most frequent visitors to apiaries, followed by bandicoots and corvid birds. Cane toads at apiaries were more abundant and in better body condition (i.e., larger mass relative to snout-urostyle length) than were toads at nearby control sites. Toads at beehives contained more prey items per stomach (mostly bees, which were never recorded in the stomachs of toads from other sites), and adult female toads at beehives had larger livers and ovaries relative to body size. We conclude that commercial apiaries attract cane toads, influence their diets, and increase their feeding rates and reproductive capacity. Like other habitat modifications wrought by agricultural activities, honey bee colonies provide resources that facilitate the spread of cane toads through an otherwise harsh landscape matrix. Minor modifications to beehives could exclude toads, thereby eliminating their positive impact on the invader.     

Activity metabolism of the toad (Bufo americanus): Ecological consequences of ontogenetic change

Summary Following metamorphosis, juvenile toads form dense, heliothermic aggregations on the margins of the ponds from which they emerge. After a period of growth and development, during which body mass increases ten-fold, the juveniles disperse from the pond and assume the solitary, nocturnal habits that characterize adult toads.The dispersal of the toads coincides with the culmination of ontogenetic changes in activity metabolism. Unlike adults, juvenile toads exhaust rapidly when exercised and exhibit a low aerobic component of total metabolic scope. Values of aerobic scope for sustained activity ranged from 0.5 ml O₂/(g·h) for the smallest juveniles to 1.0 ml O₂/(g·h) for adults. The capacity of juveniles for oxygen consumption increases rapidly with growth, reaching the level of mature animals immediately prior to dispersal.In contrast to aerobic metabolism, anaerobic scope was independent of body size. Whole body lactate content after a 1 min bout of vigorous activity was elevated above the resting level by 0.14 mg lactate/g for both juvenile and adult animals.The elevated body temperatures that are achieved by basking juvenile toads probably hasten their physiological development and increase their capacity for aerobic metabolism.     

Some factors influencing the sensitivity of body temperature to activity in neonates

In adult humans, core temperature is influenced by activity; the sensitivity of core temperature to such effects shows a phase dependence and is also influenced by the environment and whether the individual is asleep or awake. We have investigated if similar effects are evident in neonates, in whom thermoregulation and the circadian rhythm of core temperature are not fully developed. Eleven full-term, healthy babies were studied singly (light 07:00-19:00) at 2 days of age and again 4 weeks after birth; between these times, they were tended routinely on a communal ward. On study days, 10-minute recordings were made of rectal and skin (abdominal) temperature, heart rate (HR), and behavioral state. Sensitivities of the temperatures to activity (“arousal”) were assessed throughout the 24h by measuring the gradient of (temperature/HR). Sensitivities measured at 01:00, 05:00, 09:00, 13:00,17:00, and 21:00 were used as dependent variables in stepwise regression and linear regression analyses, with “subjects” “light versus dark”, “behavioral state”, and “difference between time of measurement and the acrophase of the endogenous component of the temperature rhythm” (ignoring sign) as possible predictors. (Acrophases of the temperature rhythms had been estimated from 24h data purified using the behavioral state record.) Light versus dark acted as a significant predictor of the sensitivity of rectal temperature to arousal on day 2 and week 4, the sensitivity increasing in the light, and there was limited evidence for behavioral state acting as a predictor on day 2. Neither factor was a significant predictor when the sensitivity of the babies' skin temperatures to arousal was investigated. There was also some evidence that the difference between the time of measurement and the temperature acrophase acted as a predictor of sensitivity to arousal in both rectal (day 2) and skin (week 4) temperature, with larger differences decreasing the sensitivity. These results indicate that there are masking effects on body temperature due to arousal in neonates, the size of which depends on both internal and external factors. However, this sensitivity of temperature to arousal shows differences from the sensitivity of temperature to physical activity in both adult humans and adult mice. One possible explanation of this result is that temperature regulation and the circadian system are not fully developed in humans at this age. (Chronobiology International, 17(5), 679-692, 2000)     

The ecological impact of invasive cane toads (Bufo marinus) in Australia

Although invasive species are viewed as major threats to ecosystems worldwide, few such species have been studied in enough detail to identify the pathways, magnitudes, and timescales of their impact on native fauna. One of the most intensively studied invasive taxa in this respect is the cane toad (Bufo marinus), which was introduced to Australia in 1935. A review of these studies suggests that a single pathway-lethal toxic ingestion of toads by frog-eating predators-is the major mechanism of impact, but that the magnitude of impact varies dramatically among predator taxa, as well as through space and time. Populations of large predators (e.g., varanid and scincid lizards, elapid snakes, freshwater crocodiles, and dasyurid marsupials) may be imperilled by toad invasion, but impacts vary spatially even within the same predator species. Some of the taxa severely impacted by toad invasion recover within a few decades, via aversion learning and longer-term adaptive changes. No native species have gone extinct as a result of toad invasion, and many native taxa widely imagined to be at risk are not affected, largely as a result of their physiological ability to tolerate toad toxins (e.g., as found in many birds and rodents), as well as the reluctance of many native anuran-eating predators to consume toads, either innately or as a learned response. Indirect effects of cane toads as mediated through trophic webs are likely as important as direct effects, but they are more difficult to study. Overall, some Australian native species (mostly large predators) have declined due to cane toads; others, especially species formerly consumed by those predators, have benefited. For yet others, effects have been minor or have been mediated indirectly rather than through direct interactions with the invasive toads. Factors that increase a predator's vulnerability to toad invasion include habitat overlap with toads, anurophagy, large body size, inability to develop rapid behavioral aversion to toads as prey items, and physiological vulnerability to bufotoxins as a result of a lack of coevolutionary history of exposure to other bufonid taxa.     

6-Hydroxydopamine produces a weight increase in toads

A large increase in body weight occurred after injection of 6-hydroxydopamine (6-OHDA, 100 mg kg-1) into the iliac lymph sac of toads. The body weight increase was apparently due to retention of fluid and only occurred when toads could not avoid contact of their ventral skin with water. Lower doses of 6-OHDA (25 or 50 mg kg-1) did not cause a weight increase although they were sufficient to eliminate fluorescence from peripheral adrenergic nerves. A peripheral injection of 6-OHDA did not affect the appearance of central aminergic nerves. Removal of the pituitary and median eminence did not affect the weight increase. Although the primary action of 6-OHDA in upsetting water balance in toads has not been revealed by this study, it is clearly not related to the chemical sympathectomy of adrenergic nerves.