Allometry and selection in a novel predator–prey system: Australian snakes and the invading cane toad

Because many organismal traits vary with body size, interactions between species can be affected by the respective body sizes of the participants. We focus on a novel predator–prey system involving an introduced, highly toxic anuran (the cane toad, Bufo marinus ) and native Australian snakes. The chance of a snake dying after ingesting a toad depends on the size of the snake and the size of the toad, and ultimately reflects the effect of four allometries: (1) physiological tolerance (the rate that physiological tolerance to toad toxin changes with snake size); (2) swallowing ability (the rate that maximal ingestible toad size (i.e. snake head size) increases with snake body size); (3) prey size (the rate that prey size taken by snakes increases with snake head size) and (4) toad toxicity (the rate that toxicity increases with toad size). We measured these allometries, and combined them to estimate the rate at which a snake's resistance changes with toad toxicity. The parotoid glands (and thus, toxicity) of toads increased disproportionately with toad size (i.e. relative to body size, larger toads were more toxic) but simultaneously, head size relative to body size (and thus, maximal ingestible prey size relative to predator size) declined with increasing body size in snakes. Thus, these two allometries tended to cancel each other out. Physiological tolerance to toxins did not vary with snake body size. The end result was that across snake species, mean adult body size did not affect vulnerability. Within species, however, smaller predators were more vulnerable, because the intraspecific rate of decrease in relative head size of snakes was steeper than the rate of increase in toxicity of toads. Thus, toad invasion may cause disproportionate mortality of juvenile snakes, and adults of the sex with smaller mean adult body sizes.     

Vulnerability of an Australian anuran tadpole assemblage to the toxic eggs of the invasive cane toad (Bufo marinus)

The invasion of cane toads (Bufo marinus) across tropical Australia has fatally poisoned many native predators; the most frequent victims may be tadpoles of native frogs, which die when they consume the toxic eggs of the toads. Field studies have documented high and species‐specific mortality of tadpoles following toad spawning. To clarify the determinants of tadpole vulnerability, we conducted 1593 laboratory trials in which single tadpoles were exposed to 10 toad eggs, either with or without an alternative food source (lettuce). At least some tadpoles within all 15 species tested consumed toad eggs. Interspecific variance in survival rates (from 0 to >70%) was driven by feeding responses not by physiological tolerance to toxins: almost all native tadpoles that consumed eggs died rapidly. Tadpole mortality was decreased by the presence of an alternative food source in four species, increased in two species, and not affected in seven species. In three of four taxa where we tested both small (early‐stage) and large (late‐stage) tadpoles, both mean survival rates and the effects of alternative food on survival shifted with tadpole body size. Trials with one species (Limnodynastes convexiusculus) showed no significant inter‐clutch variation in feeding responses or tolerance to toxins. Overall, our data show that cane toad eggs are highly toxic to native anuran tadpoles, but that whether or not a tadpole is killed by encountering toad eggs depends upon a complex interaction between the native anuran's species, its body size, and whether or not alternative food was present. In nature, larval vulnerability also depends upon the seasonal timing and location of spawning events, and habitat selection and foraging patterns of the tadpoles. Our results highlight the complexity of vulnerability determinants, and identify ecological factors (rather than physiology or feeding behaviour) as the primary determinants of cane toad impact on native tadpoles.     

Effects of an invasive anuran [the cane toad (Bufo marinus)] on the invertebrate fauna of a tropical Australian floodplain

The ways in which invasive organisms influence native ecosystems remain poorly understood. For example, feral cane toads Bufo marinus have spread extensively through tropical Australia over the last 70 years, but assessments of their ecological impact remain largely anecdotal. We conducted experimental trials to examine the effect of cane toad presence on invertebrate fauna in relatively small (2.4 × 1.2 m) outdoor enclosures on a floodplain near Darwin in the wet–dry tropics. Toads significantly reduced invertebrate abundance and species richness, but only to about the same degree as did an equivalent biomass of native anurans. Thus, if toads simply replaced native anurans, the offtake of invertebrates might not be substantially different from that due to native anurans before toad invasion. However, our field surveys suggest that toads cause a massive (fourfold) increase in total amphibian biomass. The end result is that cane toads act as a massive nutrient sink in the floodplain ecosystem because they consume vast numbers of invertebrates but (unlike native frogs) are largely invulnerable to predation by frog-eating predators.     

Native Australian frogs avoid the scent of invasive cane toads

Invasive species can affect the ecosystems they colonize by modifying the behaviour of native taxa; for example, avoidance of chemical cues from the invader may modify habitat use (shelter site selection) by native species. In laboratory trials, we show that metamorphs of most (but not all) native frog species on a tropical Australian floodplain avoid the scent of invasive cane toads (Bufo marinus Linnaeus 1758). Cane toads also avoid conspecific scent. This response might reduce vulnerability of metamorph frogs and toads to larger predatory toads. However, similar avoidance of one type of pungency control (garlic), and the presence of this avoidance behaviour in frogs at the toad invasion front (and hence, with no prior exposure to toads), suggest that this may not be an evolved toad‐specific response. Instead, our data support the simpler hypothesis that the metamorph anurans tend to avoid shelter sites that contain strong and unfamiliar scents. Temporal and spatial differences in activity of frogs versus toads, plus the abundance of suitable retreat sites during the wet season (the primary time of frog activity), suggest that avoiding toad scent will have only a minor impact on the behaviour of native frogs. However, this behavioural impact may be important when environmental conditions bring toads and frogs into closer contact.     

The impact of transportation and translocation on dispersal behaviour in the invasive cane toad

Biological invasions transport organisms to novel environments; but how does the translocation process influence movement patterns of the invader? Plausibly, the stress of encountering a novel environment, or of the transport process, might induce rapid dispersal from the release site—potentially enhancing (or reducing) invader success and spread. We investigated the effect of transportation and release to novel environments on dispersal-relevant traits of one of the world’s most notorious invaders, the cane toad (Rhinella marina). We collected toads in northern New South Wales from heath and woodland habitats, manipulated the level of transport stress and either returned toads to their exact collection point (residents) or reciprocally translocated them to a novel site. Both translocation and the level of transport stress drastically altered toad dispersal rates for at least 5 days post-release. Translocated toads (depending on their level of transport stress and release habitat) moved on average two to five times further per day (mean range 67–148 m) than did residents (mean range 22–34 m). Translocated toads also moved on more days, and moved further from their release point than did resident toads, but did not move in straighter lines. A higher level of transport stress (simulating long-distance translocation) had no significant effect on movements of resident toads but amplified the dispersal of translocated toads only when released into woodland habitat. These behavioural shifts induced by translocation and transportation may affect an invader’s ability to colonise novel sites, and need to be incorporated into plans for invader control.     

入侵植物意大利苍耳种子萌发对环境因子的响应

室内受控条件下,研究了意大利苍耳种子萌发阶段对环境因子(外界温度、光照、土壤湿度、土壤盐分以及土壤酸碱度)的响应。结果表明:意大利苍耳对各环境因子都有较宽泛的耐受幅度,10—35℃条件下均有种子萌发,而最适宜温度为25℃。其种子萌发阶段对光照没有严格需求,光照和黑暗条件下的萌发率均超过了93%。意大利苍耳表现出了极强的土壤水分耐受性,在相对湿度为30%—100%的土壤环境中,均有超过70%的种子可以正常萌发。其种子萌发率随土壤盐分浓度的升高呈下降趋势,但在280mmol/L的土壤NaCl环境中,仍有1/3的种子可以萌发。其种子对土壤酸碱度表现出较强的耐受性,在pH值是4—10的土壤环境中,种子萌发率均高达90%以上。意大利苍耳在种子萌发阶段对温度、光照、土壤水分、盐分及土壤酸碱度均表现出了极强的耐受性,说明无论是温凉的高原山区,还是炎热的盆地沙漠;无论是开阔地,还是郁闭的林下、田间;无论是干旱的荒漠,还是湿润的河谷湿地;也无论是甜土,还是盐碱地都是意大利苍耳种子萌发的适宜生境。鉴于其宜生生境的广谱性和其生态危害的严重性,建议在所有的生境类型中对意大利苍耳进行全方位的严格监控,一经发现须立即铲除。     

Ability of predatory native Australian fishes to learn to avoid toxic larvae of the introduced toad Bufo marinus

Of two native Australian fishes naïve to the introduced toad Bufo marinus most barramundi Lates calcarifer rapidly learned to avoid B. marinus tadpoles, while sooty grunter Hephaestus fuliginosus exhibited considerable intraspecific variation in their learning ability. Some sooty grunter learned to avoid tadpoles after only a few attacks, while other individuals continued to attack and reject tadpoles throughout the entire laboratory trials. Individuals of both species recognized and avoided tadpoles 1 day after their previous encounter. None of the fishes died during the trials. The observed variation in behavioural responses of fishes to B. marinus may be due to differences in (1) learning ability, (2) fish hunger levels, and or (3) tadpole palatability and toxicity. The results demonstrate that most barramundi and sooty grunter learn to avoid B. marinus tadpoles with minimal trauma. Consequently, it is anticipated that the toads are unlikely to have a significant negative impact on wild populations of these fishes through direct toxic effects.     

Foraging responses of predators to novel toxic prey: effects of predator learning and relative prey abundance

Learning to avoid toxic prey items may aid native predators to survive the invasion of highly toxic species, such as cane toads Bufo marinus in tropical Australia. If the predators’ initial aversion is generalized, native prey that resemble the toxic invader may receive a benefit through accidental mimicry. What ecological factors influence the acquisition of learned avoidance (and hence, the impact of invasion on both predators and native prey)? We conducted laboratory experiments to evaluate how the relative abundance of toad tadpoles compared to palatable native tadpoles (Litoria caerulea and L. rubella) affected the ability of native aquatic predators to discriminate between these two prey types. Both fish (northern trout gudgeon, Mogurnda mogurnda) and frogs (Dahl's aquatic frog, Litoria dahlii) learned to discriminate between toads and frogs within an eight‐day period. Higher abundance of toad tadpoles relative to frog tadpoles enhanced rates of predator learning, and thus reduced predation on toads and increased predation on native tadpoles. In the field, spatial and temporal variation in the relative abundance of cane toads compared to native frogs may influence the rates at which these novel toxic items are deleted from predator diets, and the duration of predator protection afforded to natives that resemble the invader.     

Responses of the mangroves Avicennia marina and Bruguiera gymnorrhiza to oil contamination

The effects of bunker fuel oil on morphological and physiological responses of Avicennia marina and Bruguiera gymnorrhiza were investigated in glasshouse and field experiments. In the glasshouse study, 15-month-old seedlings of A. marina were subjected to oiling or debarking treatments for 6 months. Oiling or debarking of a 5 cm ring of the basal portion of the stem, alone and in combination, reduced leaf CO₂ exchange by over 50% and resulted in the production of adventitious roots immediately above the debarked and/or oiled stem 8–12 weeks after the commencement of treatments. In the field study, sediment oiling at a single dose of 5 l m⁻² of A. marina and B. gymnorrhiza trees reduced electron transport rate (ETR) through Photosystem II (PSII) and PSII quantum yield. Oiling also reduced the photochemical efficiency of PSII (F_v/i_m) in B. gymnorrhiza, but not in A. marina. After 15 weeks of oiling, adventitious roots developed at the base of the stem in A. marina, but not in B. gymnorrhiza. Naturally occurring A. marina seedlings with adventitious roots exhibited lower leaf CO₂ exchange rates, photochemical efficiency of PSII and leaf chlorophyll content than similar seedlings without these roots. These results indicate that bunker fuel oil adversely affects photosynthetic performance of A. marina and B. gymnorrhiza mangroves. A. marina responds to oiling by producing adventitious roots at the base of the stem. Adventitious root production at the base of the stem may be a useful biological indicator of oil or other toxic pollutants in A. marina.     

Osmoregulation of the cane toad, Bufo marinus, in salt water

Adult cane toads, B. marinus, survived in salinities up to 40% sea-water (SW). Pre-exposure to 30, then 40% SW, increased the survival time of toads in 50% SW. Plasma from toads acclimated to salt water is hyperosmotic to the environment--a result of increased plasma sodium, chloride and urea concentrations. When toads were placed in tap-water and 20% SW, all significant changes to plasma sodium, chloride, urea and osmotic pressure occurred within the first 2 days of exposure. When toads were placed in 30 and 40% SW environments, the increases in plasma sodium and chloride concentrations occurred within the first 2 days of exposure while urea and total osmotic pressure continued to rise until some time between 2 and 7 days exposure.     

Impact of the invasive cane toad (Bufo marinus) on an Australian frog (Opisthodon ornatus) depends on minor variation in reproductive timing

Invasive species are widely viewed as unmitigated ecological catastrophes, but the reality is more complex. Theoretically, invasive species could have negligible or even positive effects if they sufficiently reduce the intensity of processes regulating native populations. Understanding such mechanisms is crucial to predicting ultimate ecological impacts. We used a mesocosm experiment to quantify the impact of eggs and larvae of the introduced cane toad (Bufo marinus) on fitness-related traits (number, size and time of emergence of metamorphs) of a native Australian frog species (Opisthodon ornatus). The results depended upon the timing of oviposition of the two taxa, and hence the life-history stages that came into contact. Growth and survival of O. ornatus tadpoles were enhanced when they preceded B. marinus tadpoles into ponds, and reduced when they followed B. marinus tadpoles into ponds, relative to when tadpoles of both species were added to ponds simultaneously. The dominant tadpole-tadpole interaction is competition, and the results are consistent with competitive priority effects. However, these priority effects were reduced or reversed when O. ornatus tadpoles encountered B. marinus eggs. Predation on toxic toad eggs reduced the survival of O. ornatus and B. marinus. The consequent reduction in tadpole densities allowed the remaining O. ornatus tadpoles to grow more rapidly and to metamorphose at larger body sizes (>60% disparity in mean mass). Thus, exposure to B. marinus eggs reduced the number of O. ornatus metamorphs, but increased their body sizes. If the increased size at metamorphosis more than compensates for the reduced survival, the effective reproductive output of native anurans may be increased rather than decreased by the invasive toad. Minor interspecific differences in the seasonal timing of oviposition thus have the potential to massively alter the impact of invasive cane toads on native anurans.     

Infection dynamics of the lungworm Rhabdias pseudosphaerocephala in its natural host, the cane toad (Bufo marinus), and in novel hosts (native Australian frogs)

Host-parasite systems have often evolved over time, such that infection dynamics may become greatly modified from the time of initial contact of the host with the parasite. Biological invasions may be useful to clarify processes in the initial contact of hosts with parasites, and allow us to compare parasite uptake between the ancestral (coevolved) host and novel (noncoevolved) hosts. Cane toads (Bufo marinus) are spreading rapidly through tropical Australia, carrying with them a nematode lungworm (Rhabdias pseudosphaerocephala) congeneric with those found in Australian frogs. We investigated the dynamics of infections of the toad parasite by conducting histologic examinations of cane toads and three native Australian frogs (Litoria dahlii, Litoria nasuta, and Opisthodon ornatus) at 2, 6, and 10 days after experimental exposure to the toad lungworm. More worms were found in toads than in frogs, especially at longer periods postexposure. In toads, the infective larvae entered the skin and muscles within 2 days postexposure, passed into the coelom in 6 days, and reached the lungs at 10 days. In frogs, larvae were found in many organs rather than migrating to consistent target tissues; a few larvae reached the lungs of L. dahlii. Migratory larvae caused increasing inflammation (primarily granulomatous admixed with granulocytes then lymphocytes) through time, especially in frogs. Evolution has resulted in an enhanced ability of the lungworm to locate the target organ (the lungs) of the toad, and an increase in rates of parasite survival within this host.     

Impacts of the invasive cane toad on aquatic reptiles in a highly modified ecosystem: the importance of replicating impact studies

Invasive species can have dramatic and detrimental effects on native species, and the magnitude of these effects can be mediated by a plethora of factors. One way to identify mediating factors is by comparing attributes of natural systems in species with heterogeneity of responses to the invasive species. This method first requires quantifying impacts in different habitats, ecosystems or geographic locations. We used a long-term, before-and-after study to quantify the impacts of the invasive and toxic cane toad (Rhinella marina) on two predators in a highly modified ecosystem: an irrigation channel in an agricultural landscape. Survey counts spanning 8 years indicated a severe population-level decline of 84 % in Merten’s Water Monitor (Varanus mertensi) that was coincident with the arrival of cane toads. The impact of cane toads on V. mertensi was similar to that found in other studies in other habitats, suggesting that cane toads severely impact V. mertensi populations, regardless of habitat type or geographic location. In contrast, a decline was not detected in the Freshwater Crocodile (Crocodylus johnstoni). There is now clear evidence that some C. johnstoni populations are vulnerable to cane toads, while others are not. Our results reinforce the need for the replication of impact studies within and among species; predicting impacts based on single studies could lead to overgeneralizations and potential mismanagement.     

Attempts to model the bloom dynamics of Pyrodinium, a tropical toxic dinoflagellate

For the first time, several models have been used to aid in the understanding of the bloom dynamics of Pyrodinium bahamense var. compressum, the major causal organism of toxic algal blooms in Manila Bay and several areas in the tropical world. The complex life cycle of Pyrodinium includes the formation of cysts that settle at the sediments, which can serve as the inoculum for the next bloom.The seasonal variation of temperature and salinity reflects the combined effects of convection and water column stability, which can control vertical movement of plankton and other parameters essential to its growth. The significance of wind forcing appears to be related to the potential to resuspend cysts. In the absence of wind, tidal currents in the inner part of the bay may be too weak to induce resuspension. The addition of wind results in a significant increase in bottom current velocity. Off Cavite at the southeast, bottom velocity is enhanced by orbital motion due to waves, one of the reasons why sediments off this area are dominated by sandy material. The strong vertical mixing of the water column at depths of less than 10 m may influence nutrient and consequently, plankton populations.The wave field during the southwest monsoon indicates that its contribution to the bottom velocity dominates in this area of the bay.Bloom simulations using combined bio-physical parameters show that direction of advection is almost always along wind direction. The dispersal distances increases if the Pyrodinium cells are found higher in the water column. For cells originating from southeastern (Cavite) sources, the direction of transport is slightly towards the north. In either case, the formation of cysts after a bloom is adjacent to the northern area (Pampanga) for blooms originating from the western side (Bataan) and along the eastern side (Parañaque–Manila) for blooms originating from the southeastern side (Cavite). Comparison with a few records of bloom occurrences in Manila Bay shows some consistent features. Reports of these blooms also showed that they occurred almost always during spring tides. There appears to be two main systems for bloom formation: one fed by cyst beds in the west (Bataan) which is advected along the west–northwest coast (Bataan–Bulacan) while the other one is fed by the southeast (Cavite) cyst beds that dominates in the east-southeast (Parañaque–Cavite) area.     

Sex‐specific prey partitioning in breeding piscivorous birds examined via a novel,noninvasive approach

Piscivorous birds frequently display sex‐specific differences in their hunting and feeding behavior, which lead to diverging impacts on prey populations. Cormorants (Phalacrocoracidae), for example, were previously studied to examine dietary differences between the sexes and males were found to consume larger fish in coastal areas during autumn and winter. However, information on prey partitioning during breeding and generally on sex‐specific foraging in inland waters is missing. Here, we assess sex‐specific prey choice of Great Cormorants (Phalacrocorax carbo) during two subsequent breeding seasons in the Central European Alpine foreland, an area characterized by numerous stagnant and flowing waters in close proximity to each other. We developed a unique, noninvasive approach and applied it to regurgitated pellets: molecular cormorant sexing combined with molecular fish identification and fish‐length regression analysis performed on prey hard parts. Altogether, 364 pellets delivered information on both, bird sex, and consumed prey. The sexes differed significantly in their overall prey composition, even though Perca fluviatilis, Rutilus rutilus, and Coregonus spp. represented the main food source for both. Albeit prey composition did not indicate the use of different water bodies by the sexes, male diet was characterized by higher prey diversity within a pellet and the consumption of larger fish. The current findings show that female and male cormorants to some extent target the available prey spectrum at different levels. Finally, the comprehensive and noninvasive approach has great potential for application in studies of other piscivorous bird species.     

Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus)

The arrival of a toxic invasive species may impose selection on local predators to avoid consuming it. Feeding responses may be modified via evolutionary changes to behaviour, or via phenotypic plasticity (e.g. learning, taste aversion). The recent arrival of cane toads (Bufo marinus) in the Northern Territory of Australia induced rapid aversion learning in a predatory marsupial (the common planigale, Planigale maculata). Here, we examine the responses of planigales to cane toads in north‐eastern Queensland, where they have been sympatric for over 60 years, to investigate whether planigale responses to cane toads have been modified by long‐term exposure. Responses to toads were broadly similar to those documented for toad‐naïve predators. Most Queensland planigales seized (21 of 22) and partially consumed (11 of 22) the first toad they were offered, but were likely to ignore toads in subsequent trials. However, unlike their toad‐naïve conspecifics from the Northern Territory, the Queensland planigales all survived ingestion of toad tissue without overt ill effects and continued to attack toads in a substantial proportion of subsequent trials. Our data suggest that (i) learning by these small predators is sufficiently rapid and effective that selection on behaviour has been weak; and (ii) physiological tolerance to toad toxins may be higher in planigales after 60 years (approximately 60 generations) of exposure to this toxic prey.     

Responses of wild type and abscisic acid mutants ofArabidopsis thaliana to cadmium

Heavy metal-induced inhibitory effects are reported to be concomitant with an increase in endogenous abscisic acid (ABA) levels in plant tissues indicating the possibility of this phytohormone mediating a part of the metal-imposed phytotoxicity. We examined this possibility by comparing the seed germination and seedling growth responses of ABA-deficient (aba-1, aba-3 and aba-4) and ABA-insensitive (abi2-1 and abi3-1) mutants of Arabidopsis thaliana to Cd with those of the wild type (Landsberg erecta, Ler). Assuming that Cd imposed a part of its toxic influence via affecting a rise in endogenous ABA level, all ABA mutants studied could be predicted to exhibit reduced responsiveness to Cd exposure in comparison to the wild type. However, the data obtained both in germination and growth assays were not consistent with this prediction. In germination assays, all ABA mutants proved consistently more sensitive than the wild type to Cd. In case of growth (root length and seedling fresh weight), the magnitude of Cd-induced inhibition in ABA mutants (aba-1, abi2-1 and abi3-1) was generally comparable to that in the wild type. Based on these observations a direct mediatory role of ABA in Cd-imposed phytotoxic effects on early growth could be excluded. The possible significance of heavy metal-dependent increase in endogenous ABA levels in plant tissues is discussed.