Sum of fears among intraguild predators drives the survival of green sea turtle (Chelonia mydas) eggs.

Ecologists have long theorized that apex predators stabilize trophic systems by exerting a net protective effect on the basal resource of a food web. Although experimental and observational studies have borne this out, it is not always clear what behavioural mechanisms among the trophically connected species are responsible for this stability. Fear of intraguild predation is commonly identified as one such mechanism in models and mesocosm studies, but empirical evidence in natural systems remains limited, as the complexity of many trophic systems renders detailed behavioural studies of species interactions challenging. Here, we combine long-term field observations of a trophic system in nature with experimental behavioural studies of how all the species in this system interact, in both pairs and groups. The results demonstrate how an abundant, sessile and palatable prey item (sea turtle eggs, Chelonia mydas) survives when faced by three potential predators that all readily eat eggs: an apex predator (the stink ratsnake, Elaphe carinata) and two mesopredators (the brown rat, Rattus norvegicus, and kukri snake, Oligodon formosanus). Our results detail how fear of intraguild predation, conspecific cannibalism, habitat structure and territorial behaviour among these species interact in a complex fashion that results in high egg survival.

Too hard to swallow: a secret secondary defence of an aposematic insect.

Anti-predator strategies are significant components of adaptation in prey species. Aposematic prey are expected to possess effective defences that have evolved simultaneously with their warning colours. This study tested the hypothesis of the defensive function and ecological significance of the hard body in aposematic Pachyrhynchus weevils pioneered by Alfred Russel Wallace nearly 150 years ago. We used predation trials with Japalura tree lizards to assess the survivorship of 'hard' (mature) versus 'soft' (teneral) and 'clawed' (intact) versus 'clawless' (surgically removed) weevils. The ecological significance of the weevil's hard body was evaluated by assessing the hardness of the weevils, the local prey insects, and the bite forces of the lizard populations. The existence of toxins or deterrents in the weevil was examined by gas chromatography-mass spectrometry (GC-MS). All 'hard' weevils were instantly spat out after being bitten once and survived attacks by the lizards. In contrast, the 'soft' weevils were chewed and subsequently swallowed. The results were the same regardless of the presence or absence of the weevil's tarsal claws. The hardness of 'hard' Pachyrhynchus weevils was significantly higher than the average hardness of other prey insects in the same habitat and the mean bite forces of the local lizards. The four candidate compounds of the weevil identified by GC-MS had no known toxic or repellent functions against vertebrates. These results reveal that the hardness of aposematic prey functions as an effective secondary defence, and they provide a framework for understanding the spatio-temporal interactions between vertebrate predators and aposematic insect prey.

Rafting on floating fruit is effective for oceanic dispersal of flightless weevils.

Terrestrial species, especially non-vagile ones (those unable to fly or swim), cannot cross oceans without exploiting other animals or floating objects. However, the colonisation history of flightless Pachyrhynchus weevils, inferred from genetic data, reveals their ability to travel long distances to colonise remote islands. Here, we used captive-bred Pachyrhynchus jitanasaius to analyse (i) the physiological tolerance of weevils (egg, larva and adult stages) to different levels of salinity; (ii) the survival rate of larvae in a simulated ocean environment in the laboratory; and (iii) the survival rate of larvae in a field experiment in the ocean using fruit of the fish poison tree floating on the Kuroshio current in the Pacific Ocean. We found that the survival rate of larvae in seawater was lower than in fresh water, although if the larvae survived 7 days of immersion in seawater, some emerged as adults in the subsequent rearing process. No adults survived for more than 2 days, regardless of salinity level. After floating separately for 6 days in salt water in the laboratory and in the Kuroshio current, two of 18 larvae survived in the fruit. This study provides the first empirical evidence that P. jitanasaius larvae can survive 'rafting' on ocean currents and that the eggs and larvae of these weevils have the highest probability of crossing the oceanic barrier. This ability may facilitate over-the-sea dispersal of these flightless insects and further shape their distribution and speciation pattern in the Western Pacific islands.

Drastic population fluctuations explain the rapid extinction of the passenger pigeon.

To assess the role of human disturbances in species' extinction requires an understanding of the species population history before human impact. The passenger pigeon was once the most abundant bird in the world, with a population size estimated at 3-5 billion in the 1800s; its abrupt extinction in 1914 raises the question of how such an abundant bird could have been driven to extinction in mere decades. Although human exploitation is often blamed, the role of natural population dynamics in the passenger pigeon's extinction remains unexplored. Applying high-throughput sequencing technologies to obtain sequences from most of the genome, we calculated that the passenger pigeon's effective population size throughout the last million years was persistently about 1/10,000 of the 1800's estimated number of individuals, a ratio 1,000-times lower than typically found. This result suggests that the passenger pigeon was not always super abundant but experienced dramatic population fluctuations, resembling those of an "outbreak" species. Ecological niche models supported inference of drastic changes in the extent of its breeding range over the last glacial-interglacial cycle. An estimate of acorn-based carrying capacity during the past 21,000 y showed great year-to-year variations. Based on our results, we hypothesize that ecological conditions that dramatically reduced population size under natural conditions could have interacted with human exploitation in causing the passenger pigeon's rapid demise. Our study illustrates that even species as abundant as the passenger pigeon can be vulnerable to human threats if they are subject to dramatic population fluctuations, and provides a new perspective on the greatest human-caused extinction in recorded history.

Metabolic effects of parasitization by the barnacle Polyascus plana (Cirripedia: Rhizocephala: Sacculinidae) on a grapsid host, Metopograpsus thukuhar.

Pathophysiological studies of rhizocephalan infections are rare. We describe differences in the levels of tissue and hemolymph metabolites between Polyascus plana-parasitized and unparasitized individuals of Metopograpsus thukuhar. Crabs were assigned to either a parasitized (carrying at least 1 externa, i.e. a protruding reproductive body) or an unparasitized (not carrying externae and determined to be rootlet-free by a barnacle 18S rRNA-based polymerase chain reaction) group. Quantification of metabolites showed that muscle glycogen levels were significantly lower and hepatopancreas levels were significantly higher in parasitized crabs compared to unparasitized crabs; hepatopancreas triacylglycerol levels were significantly higher and hemolymph levels significantly lower in parasitized hosts, and there was no significant difference in muscle triacylglycerol levels between unparasitized and parasitized animals. Glucose levels in the hepatopancreas, muscle, and hemolymph were all significantly higher in parasitized hosts. Significant levels of glucose, triacylglycerol, and glycogen were present in the barnacle externae. In addition, levels of crustacean hyperglycemic hormone in the sinus glands were not significantly different between unparasitized and parasitized animals. Glucose mobilized from the muscle is likely converted to glycogen and triacylglycerol in the rootlet-infiltrated hepatopancreas of parasitized hosts, and the eyestalk neuroendocrine system appears not to be significantly impaired, in terms of hormone production and storage, by parasitization.

Territorial behavior in Taiwanese kukrisnakes (Oligodon formosanus).

The independent evolutionary origin of a complex trait, within a lineage otherwise lacking it, provides a powerful opportunity to test hypotheses on selective forces. Territorial defense of an area containing resources (such as food or shelter) is widespread in lizards but not snakes. Our studies on an insular population of Taiwanese kukrisnakes (Oligodon formosanus) show that females of this species actively defend sea turtle nests by repelling conspecifics for long periods (weeks) until the turtle eggs hatch or are consumed. A clutch of turtle eggs comprises a large, long-lasting food resource, unlike the prey types exploited by other types of snakes. Snakes of this species have formidable weaponry (massively enlarged teeth that are used for slitting eggshells), and when threatened, these snakes wave their tails toward the aggressor (an apparent case of head-tail mimicry). Bites to the tail during intraspecific combat bouts thus can have high fitness costs for males (because the hemipenes are housed in the tail). In combination, unusual features of the species (ability to inflict severe damage to male conspecifics) and the local environment (a persistent prey resource, large relative to the snakes consuming it) render resource defense both feasible and advantageous for female kukrisnakes. The (apparently unique) evolution of territorial behavior in this snake species thus provides strong support for the hypothesis that resource defensibility is critical to the evolution of territoriality.

Predation drives interpopulation differences in parental care expression.

Expressing parental care after oviposition or parturition is usually an obligate (evolved) trait within a species, despite evolutionary theory predicting that widespread species should vary in whether or not they express parental care according to local selection pressures. The lizard Eutropis longicaudata expresses maternal care only in a single population throughout its large geographical range, but why this pattern occurs is unknown. We used reciprocal translocation and predator exclusion experiments to test whether this intraspecific variation is a fixed trait within populations and whether predator abundance explains this perplexing pattern. Wild-caught female lizards that were reciprocally translocated consistently guarded or abandoned eggs in line with their population of origin. By contrast, most lizards raised in a common garden environment and subsequently released as adults adopted the maternal care strategy of the recipient population, even when the parents originated from a population lacking maternal care. Egg predation represents a significant fitness cost in the populations where females display egg-guarding behaviour, but guarding eggs outweighs this potential cost by increasing hatching success. These results imply that predators can be a driving force in the expression of parental care in instances where it is normally absent and that local selection pressure is sufficient to cause behavioural divergence in whether or not parental care is expressed.

Tail loss compromises immunity in the many-lined skink, Eutropis multifasciata.

Tail autotomy incurs energetic costs, and thus, a trade-off in resource allocation may lead to compromised immunity in lizards. We tested the hypothesis that tailless lizards will favor constitutive innate immunity responses over an energetically costly inflammatory response. The influence of fasting and colorful ornamentation was also investigated. We experimentally induced tail autotomy in the lizard Eutropis multifasciata and found that inflammation was suppressed by tail loss, but not further affected by fasting; the suppressive effect of colorful ornamentation was manifested only in males, but not in females. Constitutive innate immunity was not affected by any of these factors. As expected, only costly inflammation was compromised, and a less expensive constitutive innate immunity might be favored as a competent first-line defense during energetically demanding periods. After considering conventional trade-offs among tail regeneration and reproduction, further extending these studies to incorporate disease risk and how this influences escape responses to predators and future reproduction would make worthwhile studies.

Loss of sea turtle eggs drives the collapse of an insular reptile community.

Marine subsidies are vital for terrestrial ecosystems, especially low-productivity islands. However, the impact of losing these subsidies on the terrestrial food web can be difficult to predict. We analyzed 23 years of survey data from Orchid Island to assess the consequences of the abrupt loss of an important marine subsidy. After climate-driven beach erosion and predator exclusion efforts resulted in the abrupt loss of sea turtle eggs from the terrestrial food web, predatory snakes altered their foraging habitats. This increased predation on other reptile species in inland areas, resulting in population declines in most terrestrial reptile species. Comparisons with sea turtle-free locations where lizard populations remained stable supported these findings. Our study emphasizes the cascading effects of generalist predators and the unintended consequences of single-species conservation, highlighting the importance of understanding species interconnectedness and considering potential ripple effects in marine-dependent insular ecosystems.

Effects of intraguild predators on nest-site selection by prey.

Nest-site selection involves tradeoffs between the risk of predation (on females and/or nests) and nest-site quality (microenvironment), and consequently suitable nesting sites are often in limited supply. Interactions with "classical" predators (e.g., those not competing for shared resources) can strongly influence nest-site selection, but whether intraguild predation also influences this behavior is unknown. We tested whether risk of predation from an intraguild predator [the diurnal scincid lizard Eutropis (Mabuya) longicaudata] influences nest-site selection by its prey (the nocturnal gecko Gekko hokouensis) on Orchid Island, Taiwan. These two species putatively compete for shared resources, including invertebrate prey and nesting microhabitat, but the larger E. longicaudata also predates G. hokouensis (but not its hard-shelled eggs). Both species nested within a concrete wall containing a series of drainage holes that have either one ("closed-in") or two openings ("open"). In allopatry, E. longicaudata preferred to nest within holes that were plugged by debris (thereby protecting eggs from water intrusion), whereas G. hokouensis selected holes that were open at both ends (facilitating escape from predators). When we experimentally excluded E. longicaudata from its preferred nesting area, G. hokouensis not only nested in higher abundances, but also modified its nest-site selection, such that communal nesting was more prevalent and both open and closed-in holes were used equally. Egg viability was unaffected by the choice of hole type, but was reduced slightly (by 7%) in the predator exclusion area (presumably due to higher local incubation temperatures). Our field experiment demonstrates that intraguild predators can directly influence the nest density of prey by altering maternal nest-site selection behavior, even when the predator and prey are active at different times of day and the eggs are not at risk of predation.

Trans-marine dispersal inferred from the saltwater tolerance of lizards from Taiwan.

Dehydration and hypersalinity challenge non-marine organisms crossing the ocean. The rate of water loss and saltwater tolerance thus determine the ability to disperse over sea and further influence species distribution. Surprisingly, this association between physiology and ecology is rarely investigated in terrestrial vertebrates. Here we conducted immersion experiments to individuals and eggs of six lizard species differently distributed across Taiwan and the adjacent islands to understand if the physiological responses reflect the geographical distribution. We found that Plestiodon elegans had the highest rate of water loss and the lowest saltwater tolerance, whereas Eutropis longicaudata and E. multifasciata showed the lowest rate of water loss and the highest saltwater tolerance. Diploderma swinhonis, Hemidactylus frenatus, and Anolis sagrei had medium measurements. For the eggs, only the rigid-shelled eggs of H. frenatus were incubated successfully after treatments. While, the parchment-shelled eggs of E. longicaudata and D. swinhonis lost or gained water dramatically in the immersions without any successful incubation. Combined with the historical geology of the islands and the origin areas of each species, the inferences of the results largely explain the current distribution of these lizards across Taiwan and the adjacent islands, pioneerly showing the association between physiological capability and species distribution.

When males live longer: Resource-driven territorial behavior drives sex-specific survival in snakes.

Phylogenetic analysis has shown that males' propensity to engage in aggressive encounters is associated with females having greater longevity. Here, we confirm the causal link between aggression and reduced longevity by looking at an egg-eating snake (Oligodon formosanus) in which females defend territories in the presence of sea turtle eggs. We monitored aggressiveness and survival at two sites: a control site with a stable supply of turtle eggs, and a second site where we collected data before and after a storm that eroded the beach on which turtles nested, thus leading to a loss of territoriality. We show that territoriality was the driver behind higher injury rates in females. Territorial females also had lower survival and decreased longevity compared with the nonterritorial males, but these differences disappeared when females were not territorial. Our study demonstrates how resource availability can influence the evolution of sex-specific patterns of survival across vertebrates.

Ecology and reproductive patterns of the agamid lizard Japalura swinhonis on an east Asian island, with comments on the small clutch sizes of island lizards.

I describe the habitat use, diet, and the male and female reproductive cycles of Japalura swinhonis, an oviparous agamid lizard inhabiting Orchid Island, a tropical island off the southeastern coast of Taiwan. Ninety percent of lizards (n=126) were observed on tree trunks or at the forest edge. The diet of J. swinhonis on Orchid Island consisted mostly of hymenopterans (53.33%) and orthopterans (16.67%). The mean snout-vent length (SVL) of adult males was 74.58 (n=89) and that of females was 69.31 (n=37) mm. Females exhibited a long vitellogenic period from November to February, with parturition occurring from March to October. The onset of vitellogenesis did not correlate with the mass of the female fat bodies. Females produced two to five eggs per clutch, and clutch size was not correlated with SVL. Two clutches were recorded during a single year in some individuals. Clutch size in J. swinhonis was compared with that in other Japalura species. Clutch sizes of Japalura species are larger in mainland China than on insular Taiwan. Clutch size is also mainly affected by environmental constraints, and smaller clutch sizes are probably affected by predators on Orchid Island.

Surf and turf: predation by egg-eating snakes has led to the evolution of parental care in a terrestrial lizard.

Animals display a great diversity of parental care tactics that ultimately enhance offspring survival, but how such behaviors evolve remains unknown for most systems. Here, we studied the evolution of maternal care, in the form of nest guarding, in a single population of long-tailed sun skink (Eutropis longicaudata) living on Orchid Island (Taiwan). This species typically does not provide protection to its offspring. Using a common garden experiment, we show that maternal care is genetically determined in this population. Through field manipulations, we demonstrate that care provides a significant increase in egg survival on Orchid Island by reducing predation from egg-eating snakes (Oligodon formosanus); this predator is not abundant in other populations of the lizard, which do not display parental care. Finally, using extensive field surveys, we show that the seasonal availability of green sea turtle (Chelonia mydas) nests is the cause for the high abundance of snake predators on Orchid Island, with the snakes consuming lizard eggs when green turtle eggs are not available. Together, these lines of evidence provide the first full demonstration of how predation can trigger the evolution of parental care in a species derived from a non-caring ancestor.

Reproductive characteristics of Bufo bankorensis at two elevations in Taiwan.

We compared the reproductive characteristics of two populations of Bufo bankorensis in central Taiwan, one inhabiting a temperate climate (Meifong, 2100 m), the other inhabiting a subtropical climate (Wushe, 1100 m). We determined ovary status, spermatogenetic activity, fat body and liver mass cycles, and plasma 17-betaestradiol and androgen levels over a 14 month period. B. bankorensis from both populations are prolonged breeders but the temperate population exhibits breeding activity throughout the year, while the subtropical population only breeds from September to March. Their spermatogenic cycles are continuous, and their spermatogenetic activities are invariably at stage 6, in which spermatozoa are predominant in the seminiferous tubule. Both populations show monthly variations in plasma androgen and 17-betaestradiol levels, but follow different patterns. Ovary mass is larger in the temperate than in the subtropical population. The reproduction differences of two elevation toads could be reflected by adaptations to the local environmental regimes of its habitat. The reproductive patterns of these populations of Bufo bankorensis are also compared to those of sympatric and allopatric populations of five anurans studied from sites throughout Taiwan.

Functional Assessment of Residues in the Amino- and Carboxyl-Termini of Crustacean Hyperglycemic Hormone (CHH) in the Mud Crab Scylla olivacea Using Point-Mutated Peptides.

To assess functional importance of the residues in the amino- and carboxyl-termini of crustacean hyperglycemic hormone in the mud crab Scylla olivacea (Sco-CHH), both wild-type and point-mutated CHH peptides were produced with an amidated C-terminal end. Spectral analyses of circular dichroism, chromatographic retention time, and mass spectrometric analysis of the recombinant peptides indicate that they were close in conformation to native CHH and were produced with the intended substitutions. The recombinant peptides were subsequently used for an in vivo hyperglycemic assay. Two mutants (R13A and I69A rSco-CHH) completely lacked hyperglycemic activity, with temporal profiles similar to that of vehicle control. Temporal profiles of hyperglycemic responses elicited by 4 mutants (I2A, F3A, D12A, and D60A Sco-CHH) were different from that elicited by wild-type Sco-CHH; I2A was unique in that it exhibited significantly higher hyperglycemic activity, whereas the remaining 3 mutants showed lower activity. Four mutants (D4A, Q51A, E54A, and V72A rSco-CHH) elicited hyperglycemic responses with temporal profiles similar to those evoked by wild-type Sco-CHH. In contrast, the glycine-extended version of V72A rSco-CHH (V72A rSco-CHH-Gly) completely lost hyperglycemic activity. By comparing our study with previous ones of ion-transport peptide (ITP) and molt-inhibiting hormone (MIH) using deleted or point-mutated mutants, detail discussion is made regarding functionally important residues that are shared by both CHH and ITP (members of Group I of the CHH family), and those that discriminate CHH from ITP, and Group-I from Group-II peptides. Conclusions summarized in the present study provide insights into understanding of how functional diversification occurred within a peptide family of multifunctional members.

The functional significance of aposematic signals: geographic variation in the responses of widespread lizard predators to colourful invertebrate prey.

Conspicuous colouration can evolve as a primary defence mechanism that advertises unprofitability and discourages predatory attacks. Geographic overlap is a primary determinant of whether individual predators encounter, and thus learn to avoid, such aposematic prey. We experimentally tested whether the conspicuous colouration displayed by Old World pachyrhynchid weevils (Pachyrhynchus tobafolius and Kashotonus multipunctatus) deters predation by visual predators (Swinhoe's tree lizard; Agamidae, Japalura swinhonis). During staged encounters, sympatric lizards attacked weevils without conspicuous patterns at higher rates than weevils with intact conspicuous patterns, whereas allopatric lizards attacked weevils with intact patterns at higher rates than sympatric lizards. Sympatric lizards also attacked masked weevils at lower rates, suggesting that other attributes of the weevils (size/shape/smell) also facilitate recognition. Allopatric lizards rapidly learned to avoid weevils after only a single encounter, and maintained aversive behaviours for more than three weeks. The imperfect ability of visual predators to recognize potential prey as unpalatable, both in the presence and absence of the aposematic signal, may help explain how diverse forms of mimicry exploit the predator's visual system to deter predation.

Testing cost-benefit models of parental care evolution using lizard populations differing in the expression of maternal care.

Parents are expected to evolve tactics to care for eggs or offspring when providing such care increases fitness above the costs incurred by this behavior. Costs to the parent include the energetic demands of protecting offspring, delaying future fecundity, and increased risk of predation. We used cost-benefit models to test the ecological conditions favoring the evolution of parental care, using lizard populations that differ in whether or not they express maternal care. We found that predators play an important role in the evolution of maternal care because: (1) evolving maternal care is unlikely when care increases predation pressure on the parents; (2) maternal care cannot evolve under low levels of predation pressure on both parents and offspring; and (3) maternal care evolves only when parents are able to successfully defend offspring from predators without increasing predation risk to themselves. Our studies of one of the only known vertebrate species to exhibit interpopulation differences in the expression of maternal care provide clear support for some of the hypothesized circumstances under which maternal care should evolve (e.g., when nests are in exposed locations, parents are able to defend the eggs from predators, and egg incubation periods are brief), but do not support others (e.g., when nest-sites are scarce, life history strategies are "risky", reproductive frequency is low, and environmental conditions are harsh). We conclude that multiple pathways can lead to the evolution of parental care from a non-caring state, even in a single population of a widespread species.

Foraging behaviors of two sympatric ant species in response to lizard eggs.

The trade-off between behavioral dominance and resource discovery ability represents a mechanism which could facilitate the coexistence of species, but evidence of the existence of this trade-off is limited and is often derived from experiments using artificial bait. In this study, I performed a field experiment to investigate the outcome of potential food competition between an encounter species (Paratrechina longicornis) and an exploitative one (Pheidole taivanensis) and to examine the factors that may explain the behavior of P. taivanensis when obtaining food (lizard eggs) without being attacked by P. longicornis. When P. longicornis was experimentally introduced to eggs occupied by P. taivanensis for 1 day, it displaced P. taivanensis. However, P. longicornis ignored lizard eggs which had been occupied by P. taivanensis for 2 or more days, and did not displace P. taivanensis, because by that time the eggshells had been damaged by P. taivanensis so they could no longer be used by P. longicornis. Eggshells were damaged more quickly by P. taivanensis at Santimen, southwestern Taiwan, than at four other study sites where there were lower intensities of food competition between P. taivanensis and P. longicornis. The displacement percentage was higher at Santimen which had higher ant population densities. The present study shows that lizard eggs may constitute a natural, ephemeral resource for which ants compete in space and time. Comparisons between study sites with and without ants suggest the existence of a trade-off between resource discovery and territorial defense.