Determinants of dietary specialization: a comparison of two sympatric species of sea snakes

Why do some predator species specialize on only a single type of prey whereas others take a broad range? One critical determinant may be the ontogenetic range of body sizes of the predator compared to that of its prey. If any single prey taxon spans only part of the range of prey sizes ingestible by the predator, then the predator will be more likely to take multiple prey taxa. We exploit a model system that provides a robust opportunity to test this hypothesis. We studied two sympatric species of predatory sea snakes, similar in size and general ecology that feed on anguilliform fishes from different habitats in the Great Lagoon of New Caledonia. Eel species from soft‐bottom habitats must construct their own burrows, and thus tend to be more slender‐bodied and less variable in body size than eel species that inhabit variable‐sized crevices among hard coral. As a result, a laticaudine sea snake species (Laticauda saintgironsi) that feeds on hard‐coral‐dwelling eels relies primarily on a single prey species: juveniles take young eels whereas adults consume adult eels of the same species. In contrast, a laticaudine species (L. laticaudata) that forages on soft‐bottom eels switches its prey ontogenetically: juveniles take small eel species whereas adults consume large eel species. Thus, habitat‐imposed constraints on the range of body sizes within each prey taxon generate a striking difference in the degree of dietary specialization of two closely related, sympatric predator species.     

Sexual divergence in diets and morphology in Fijian sea snakes Laticauda colubrina (Laticaudinae)

In the Fiji Islands, female yellow‐lipped sea kraits (Laticauda colubrina) grow much larger than males, and have longer and wider heads than do conspecific males of the same body length. This morphological divergence is accompanied by (and may be adaptive to) a marked sex divergence in dietary habits. Adult female sea kraits feed primarily on large conger eels, and take only a single prey item per foraging bout. In contrast, adult males feed upon smaller moray eels, and frequently take multiple prey items. Prey size increases with snake body size in both males and females, but the sexes follow different trajectories in this respect. Female sea kraits consume larger eels relative to predator head size and body length than do males. Thus, the larger relative head size of female sea kraits is interpreted as an adaptation to consuming larger prey items. Our results are similar to those of previous studies on American water snakes (natricines) and Australian file snakes (acrochordids), indicating that similar patterns of sex divergence in dietary habits and feeding structures have evolved convergently in at least three separate lineages of aquatic snakes.     

Conflicts between feeding and reproduction in amphibious snakes (sea kraits,Laticauda spp.)

If reproduction impairs an organism's ability to perform other fitness‐related activities, natural selection may favour behavioural adjustments to minimize these conflicts. This is presumably the reason why many animals are anorexic during the breeding season. We studied amphibious sea snakes, a group whose ecology facilitates teasing apart the causal links between reproduction and feeding. In both Laticauda laticaudata and L. saintgironsi in New Caledonia, adult females cease feeding as their eggs develop. The advantages of foregoing feeding do not relate to thermoregulation (because foraging does not entail lower body temperatures), nor are they attributable to physical constraints on abdominal volume (because in a snake's linear body, there is little overlap between the stomach and the oviducts). Instead, female sea kraits appear to cease feeding because their bodily distension impedes locomotor ability, rendering them less effective at foraging and more vulnerable to aquatic predators.     

Plasticity matches phenotype to local conditions despite genetic homogeneity across 13 snake populations

In a widespread species, a matching of phenotypic traits to local environmental optima is generally attributed to site-specific adaptation. However, the same matching can occur via adaptive plasticity, without requiring genetic differences among populations. Adult sea kraits (Laticauda saintgironsi) are highly philopatric to small islands, but the entire population within the Neo-Caledonian Lagoon is genetically homogeneous because females migrate to the mainland to lay their eggs at communal sites; recruits disperse before settling, mixing up alleles. Consequently, any matching between local environments (e.g. prey sizes) and snake phenotypes (e.g. body sizes and relative jaw sizes (RJSs)) must be achieved via phenotypic plasticity rather than spatial heterogeneity in gene frequencies. We sampled 13 snake colonies spread along an approximately 200 km northwest–southeast gradient (n > 4500 individuals) to measure two morphological features that affect maximum ingestible prey size in gape-limited predators: body size and RJS. As proxies of habitat quality (HQ), we used protection status, fishing pressure and lagoon characteristics (lagoon width and distance of islands to the barrier reef). In both sexes, spatial variation in body sizes and RJSs was linked to HQ; albeit in different ways, consistent with sex-based divergences in foraging ecology. Strong spatial divergence in morphology among snake colonies, despite genetic homogeneity, supports the idea that phenotypic plasticity can facilitate speciation by creating multiple phenotypically distinct subpopulations shaped by their environment.     

Effects of season, sex and body size on the feeding ecology of turtle-headed sea snakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs

In terrestrial snakes, many cases of intraspecific shifts in dietary habits as a function of predator sex and body size are driven by gape limitation and hence are most common in species that feed on relatively large prey and exhibit a wide body-size range. Our data on sea snakes reveal an alternative mechanism for intraspecific niche partitioning, based on sex-specific seasonal anorexia induced by reproductive activities. Turtle-headed sea snakes (Emydocephalus annulatus) on coral reefs in the New Caledonian Lagoon feed entirely on the eggs of demersal-spawning fishes. DNA sequence data (cytochrome b gene) on eggs that we palpated from stomachs of 37 snakes showed that despite this ontogenetic stage specialization, the prey comes from a taxonomically diverse array of species including damselfish (41 % of samples, at least 5 species), blennies (41 %, 4 species) and gobies (19 %, 5 species). The composition of snake diets shifted seasonally (with damselfish dominating in winter but not summer), presumably reflecting seasonality of fish reproduction. That seasonal shift affects male and female snakes differently, because reproduction is incompatible with foraging. Adult female sea snakes ceased feeding when they became heavily distended with developing embryos in late summer, and males ceased feeding while they were mate searching in winter. The sex divergence in foraging habits may be amplified by sexual size dimorphism; females grow larger than males, and larger snakes (of both sexes) feed more on damselfish (which often lay their eggs in exposed sites) than on blennies and gobies (whose eggs are hidden within narrow crevices). Specific features of reproductive biology of coral reef fish (seasonality and nest type) have generated intraspecific niche partitioning in these sea snakes, by mechanisms different from those that apply to terrestrial snakes.     

When seasnake meets seabird: Ecosystem engineering,facilitation and competition

Ecosystem engineers such as burrowing seabirds can increase habitat availability for sympatric taxa – but only if the burrow's owner allows other species to use the newly created shelter site. Our studies on a small Pacific island suggest that an avian burrower (the wedge‐tailed shearwater Puffinus pacificus) is both a facilitator and a competitor for amphibious seasnakes. Video camera inspection of 102 burrows revealed frequent usage of these burrows as retreat sites by the snakes, with Laticauda laticaudata restricted to burrows <4 m from the water's edge, whereas Laticauda saintgironsi often used burrows further inland. Snakes never occupied burrows that contained adult shearwaters, suggesting active burrow defence by the birds. Model snakes that we inserted into burrows were attacked, especially on the head and upper body, and we found one snake pecked to death outside a burrow. Wedge‐tailed shearwaters act as facilitators, creating a thermally favourable microhabitat and substantially enhancing habitat suitability for snakes; but they are also competitors, aggressively competing with snakes for occupancy of the resource that has been created.     

Moving in two worlds: aquatic and terrestrial locomotion in sea snakes (Laticauda colubrina,Laticaudidae)

Yellow‐lipped sea kraits (Laticauda colubrina) are amphibious in their habits. We measured their locomotor speeds in water and on land to investigate two topics: (1) to what degree have adaptations to increase swimming speed (paddle‐like tail etc.) reduced terrestrial locomotor ability in sea kraits?; and (2) do a sea krait’s sex and body size influence its locomotor ability in these two habitats, as might be expected from the fact that different age and sex classes of sea kraits use the marine and terrestrial environments in different ways? To estimate ancestral states for locomotor performance, we measured speeds of three species of Australian terrestrial elapids that spend part of their time foraging in water. The evolutionary modifications of Laticauda for marine life have enhanced their swimming speeds by about 60%, but decreased their terrestrial locomotor speed by about 80%. Larger snakes moved faster than smaller individuals in absolute terms but were slower in terms of body lengths travelled per second, especially on land. Male sea kraits were faster than females (independent of the body‐size effect), especially on land. Prey items in the gut reduced locomotor speeds both on land and in water. Proteroglyphous snakes may offer exceptional opportunities to study phylogenetic shifts in locomotor ability, because (1) they display multiple independent evolutionary shifts from terrestrial to aquatic habits, and (2) one proteroglyph lineage (the laticaudids) displays considerable intraspecific and interspecific diversity in terms of the degree to which they use terrestrial vs. aquatic habitats.     

Dehydration and drinking responses in a pelagic sea snake

Recent investigations of water balance in sea snakes demonstrated that amphibious sea kraits (Laticauda spp.) dehydrate in seawater and require fresh water to restore deficits in body water. Here, we report similar findings for Pelamis platurus, a viviparous, pelagic, entirely marine species of hydrophiine ("true") sea snake. We sampled snakes at Golfo de Papagayo, Guanacaste, Costa Rica and demonstrated they do not drink seawater but fresh water at variable deficits of body water incurred by dehydration. The threshold dehydration at which snakes first drink fresh water is -18.3 ± 1.1 % (mean ± SE) loss of body mass, which is roughly twice the magnitude of mass deficit at which sea kraits drink fresh water. Compared to sea kraits, Pelamis drink relatively larger volumes of water and make up a larger percentage of the dehydration deficit. Some dehydrated Pelamis also were shown to drink brackish water up to 50% seawater, but most drank at lower brackish values and 20% of the snakes tested did not drink at all. Like sea kraits, Pelamis dehydrate when kept in seawater in the laboratory. Moreover, some individuals drank fresh water immediately following capture, providing preliminary evidence that Pelamis dehydrate at sea. Thus, this widely distributed pelagic species remains subject to dehydration in marine environments where it retains a capacity to sense and to drink fresh water. In comparison with sea kraits, however, Pelamis represents a more advanced stage in the evolutionary transition to a fully marine life and appears to be less dependent on fresh water.     

Does body size influence thermal biology and diet of a python (Morelia spilota imbricata)?

Current theory predicts that larger‐bodied snakes not only consume larger prey (compared with smaller individuals), but may also have a different range of prey available to them due to their thermal biology. It has been argued that smaller individuals, with lower thermal inertia (i.e. faster cooling rates at nightfall when air temperature falls and basking opportunities are limited), may be thermally restricted to foraging and hunting during the day on diurnally active prey, and have reduced capacity to hunt crepuscular and nocturnal prey species. This predictive theory was investigated by way of dietary analysis, assessment of thermal biology and thermoregulation behaviour in an ambush forager, the south‐west carpet python (Morelia spilota imbricata, Pythonidae). Eighty‐seven scats were collected from 34 individual pythons over a 3‐year radiotelemetry monitoring study. As predicted by gape size limitation, larger pythons took larger prey; however, 65% of prey items of small pythons were represented by nocturnally active, small mammals, a larger proportion than present in larger snakes. Several measures of thermal biology (absolute body temperature, thermal differential of body temperature to air temperature, maximum hourly heating and cooling rates) were not strongly affected by python body mass. Additionally, body temperature was only influenced by the behavioural choice of microhabitat selection and was not affected by python body size or position, suggesting that these behavioural choices do not allow smaller pythons to vastly increase their temporal foraging window. By coupling dietary analysis, measures of body temperature and behavioural observations of free‐ranging animals, we conclude that, contrary to theoretical predictions, a small body size does not thermally restrict the temporal window for ambush foraging in M. s. imbricata. An ontogenetic or size‐determined switch from ambush feeding to actively foraging on slower prey would account for the differences in prey taken by these animals. The concept of altered foraging behaviour warrants further investigation in this species.     

Morphology,Reproduction and Diet in Australian and Papuan Death Adders (Acanthophis,Elapidae)

Death adders (genus Acanthophis) differ from most other elapid snakes, and resemble many viperid snakes, in their thickset morphology and ambush foraging mode. Although these snakes are widely distributed through Australia and Papua New Guinea, their basic biology remains poorly known. We report morphological and ecological data based upon dissection of >750 museum specimens drawn from most of the range of the genus. Female death adders grow larger than conspecific males, to about the same extent in all taxa (20% in mean adult snout-vent length,  =  SVL). Most museum specimens were adult rather than juvenile animals, and adult males outnumbered females in all taxa except A. pyrrhus. Females have shorter tails (relative to SVL) than males, and longer narrower heads (relative to head length) in some but not all species. The southern A. antarcticus is wider-bodied (relative to SVL) than the other Australian species. Fecundity of these viviparous snakes was similar among taxa (mean litter sizes 8 to 14). Death adders encompass a broad range of ecological attributes, taking a wide variety of vertebrate prey, mostly lizards (55%), frogs and mammals (each 21%; based on 217 records). Dietary composition differed among species (e.g. frogs were more common in tropical than temperate-zone species), and shifted with snake body size (endotherms were taken by larger snakes) and sex (male death adders took more lizards than did females). Overall, death adders take a broader array of prey types, including active fast-moving taxa such as endotherms and large diurnal skinks, than do most other Australian elapids of similar body sizes. Ambush foraging is the key to capturing such elusive prey.     

The diets of Hispaniolan colubrid snakes

Summary Approximately 1590 Hispaniolan colubrid snakes representing six genera and eight species were examined for prey remains (Alsophis cantherigerus, Antillophis parvifrons, Darlingtonia haetiana, Hypsirhynchus ferox, Ialtris dorsalis, Uromacer catesbyi, U. frenatus, and U. oxyrhynchus). The snakes were collected at many localities over a span of 80 years.Of 426 prey items, 77.9% were lizards (of which 69.6% were anoles), 19% frogs, 2.6% birds and mammals, and 0.5% other snakes. Darlingtonia was the only snake that did not exploit lizards; it fed exclusively on Eleutherodactylus frogs, including egg clutches. Disregarding Darlingtonia, there is no size class of Hispaniolan colubrids between 20–90 cm SVL that does not prey primarily on Anolis. Certain prey genera are added to, or deleted from, diets depending on snake size, but the data suggest that snake SVL alone does little to dictate what prey genera (or groups) are eaten. Shannon-Wiener values (H') indicate that Darlingtonia has the narrowest trophic niche, while Alsophis and Ialtris have the widest. Values of H' are not correlated with snake SVL, but highly significant (P<0.001) correlations exist between H' and mid-body circumference, head width, and snout width, and these characters may be indicators of trophic generalists and specialists. Anolis lizards are the most ubiquitous and conspicuous vertebrates on Hispaniola, and it is not surprising that they are widely exploited as a food source. Although as some snake species grow larger, anoles play a decreasingly important role in their diets, there is no evidence to suggest that they are ever abandoned as a food source by any Hispaniolan colubrid of any size.Secretive lizards of low vagility are eaten almost exclusively by wide ranging foragers (Alsophis, Antillophis); very active prey (Ameiva) is taken by sit-and-wait strategists (Hysirhynchus, U. frenatus). Those snakes which exploit the most prey groups are active foragers. Uromacer catesbyi exhibits both foraging modes, and predictably, eats diurnally active (anoles) and diurnally quiescent (hylid frogs) prey with almost equal frequency.Within Maglio's cantherigerus species assemblage, in which an Alsophis cantherigerus-like snake was ancestral to the other species, and in which longsnouted Uromacer are the most morphologically derived, there is an obvious trend toward trophic specialization on Hispaniola. The West Indies have provided an ideal natural laboratory for the investigation of many aspects of vertebrate ecology, and an arena in which to test theories of island biogeography. The most extensively studied West Indian vertebrates have been the lizards of the iguanid genus Anolis. Conversely, the ecology of West Indian snakes has been largely ignored. This is surprising in light of the fact that much has been written about Anolis predation, but little has been written about predators of Anolis; snakes may be important, frequent consumers of anoles.Hispaniola is physiographically and ecologically the most diverse of the Greater Antilles and, concomitantly, it has the most diverse snake fauna, including six colubrid genera containing 11 described species. It has rich frog and lizard faunas, but only two endemic mammals. Study of the diets of Hispaniola's colubrid snakes was undertaken to gain initial insights into the ecology of the snakes and to determine 1) what the snakes eat; 2) what relationships exist between snake diet and snake size as well as head and body proportions; 3) what relationships exist between snake foraging mode and prey type and size; 4) if anoles, as the most ubiquitous and conspicuous vertebrates on Hispaniola, comprise an important source of food; 5) if significant geographical differences in diet exist, expecially on satellite islands; 6) if north island and south island (sensu Williams 1961) Anolis ecomorphs are preyed upon by the same snake species in similar proportions; 7) if snakes are selective or opportunistic predators.This paper, the first in a series that will address all of the above topics, will briefly describe methods, snake species and prey genera. Prey genera are analyzed in terms of what snake taxa prey upon them, what size classes of snakes prey upon them, and prey genera diversity versus snake size and proportions.     

Feeding Strategies in Marine Snakes: An Analysis of Evolutionary, Morphological, Behavioral and Ecological Relationships

Analysis of 1,063 stomach contents from 39 species of sea snakesindicates that about one-third of the shallow, warm, marine,Indo-Australian fish families are preyed upon by sea snakes.Families of eels and gobies are taken by the greatest numbersof snake species. Most species of sea snakes feed on fish familieswhose members are relatively sedentary, dwelling along the bottom,within burrows or reef crevices. With one exception, a fishegg-eating specialization found uniquely in the Aipysurus-Emydocephaluslineage, the dietary habits of sea snakes cannot be categorizedaccording to the snakes' three phylogenetic lineages. Eels,mullet-like, rabbitfish-like and goby-like fish forms are takenby all three lineages. Two or three snake species are generalists,and numerous ones specialize on eels, goby-like fish or catfish.There are differences among sea snake species in the relationshipbetween snake neck girth and the maximum diameter of the prey;in the relationships of both snake gape measurements and fanglength, to the type of prey taken; and in the relationship ofsnake shape and body proportions to the prey selected. Severalmodes of feeding have been observed among sea snakes: feedingin nooks and crannies in the bottom or in reefs, cruising nearthe bottom, and feeding in drift lines. Analysis of percentdigestion of stomach contents and projections backward to thetimes of prey capture provides evidence for feeding periodicity.The greatest amount of diet overlap is for two species of seasnakes which do not both occur at the same locality. Where speciesdo co-occur, diet overlap index values are lower. The numbersof species present as well as their relative abundances varyamong localities as does the relative importance of generalists,eel-eaters, egg-eaters and other specialized feeders.     

Changes in trophic linkages to shortfin eels (<Emphasis Type="Italic">Anguilla australis</Emphasis>) since the collapse of submerged macrophytes in Lake Ellesmere,New Zealand

Lake Ellesmere (Te Waihora) is a nationally important coastal brackish lake in New Zealand, however degradation in water quality and loss of submerged macrophytes over past decades have raised concerns in regards to the declining status of the lake’s commercial and customary fisheries, predominantly targeted at shortfin eels (Anguilla australis). We investigated foodweb dynamics and trophic linkages to shortfin eels in Lake Ellesmere using a combination of abundance assessments, dietary studies, and stable isotope analyses. Data from our study are compared with historical data sets on benthic invertebrate community composition and shortfin eel diets to trace changes in the trophic linkages to top predators that have occurred since the late 1960s. Stable isotope analyses indicate that the foodweb is predominantly driven by epipelic and phytoplankton derived carbon sources, although it was difficult to discriminate between these two carbon pools because of wind-driven resuspension of lake sediments. Comparison of our survey results with historical data sets indicates a clear shift in benthic biota from being dominated by phytofaunal species such as Potamopyrgus antipodarum (comprising 90% of total invertebrate biomass) during the 1960s, to now being almost entirely comprised of subterranean species such as Chironomus zealandicus and oligochaetes (together comprising 82% of total invertebrate biomass). This shift in benthic communities has resulted in significant changes in the size-specific diet of juvenile shortfin eels (<400 mm) from those reported for Lake Ellesmere during the mid 1970s, with Chironomus larvae now comprising 65% of the diets of juvenile eels, whereas historically P. antipodarum was the dominant food item (>30% of total biomass). This shift towards foraging on smaller sediment-dwelling species could have implications for juvenile eel bioenergetics, and may help explain why juvenile shortfin growth rates have significantly decreased in past decades. Juvenile shortfins now appear to switch to foraging on preyfish (mainly common bullies, Gobiomorphus cotidianus) at a smaller size (≈400 mm) than historically recorded (>500 mm). Dietary and stable isotope signatures indicated that small shortfins (100–299 mm) have considerable overlap in trophic position (δ¹³C = −20.4‰, δ¹⁵N = 13.6‰) with common bullies (δ¹³C = −20.5‰, δ¹⁵N = 13.7‰), the dominant fish in Lake Ellesmere (92% of total abundance CPUE), potentially indicating that these two species may directly compete for food resources. These findings again highlighted the importance of C. zealandicus in sustaining the fish populations of the lake. Handling editor: S. Declerck     

Using stable-isotope analysis of feathers to distinguish moulting and breeding origins of seabirds

To determine whether stable isotope measurements of bird feathers can be used to identify moulting (interbreeding) foraging areas of adult seabirds, we examined the stable-carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopic composition of feathers of chicks and adults of black-browed albatrosses (Diomedea melanophrys) from Kerguelen Islands, southern Indian Ocean. Albatross chicks are fed primarily fish (75% by mass), the diet being dominated by various species of the family Nototheniidae and Channichthyidae which commonly occur in the shelf waters in the vicinity of the colony. δ¹³C and δ¹⁵N values in chick feathers, which are grown in summer in the breeding area, were lower than values in adult feathers, which are grown in winter (δ¹³C: –19.6‰ versus –17.6‰ and δ¹⁵N: 12.4‰ versus 15.7‰, respectively). No differences in δ¹³C and δ¹⁵N values were found in adult wing feathers moulted in 1993 and 1994 and in adult feathers formed at the beginning, middle and end of the 1994 moulting period. These data are consistent with adults moulting in the same area and feeding at the same trophic level from one year to the next and with no major changes in foraging ecology within a given moulting season; they suggest that foraging grounds were different in summer and winter and that these differed in their stable-isotope signature. Changes in both feather δ¹³C and δ¹⁵N values indicated feeding south of the Subtropical Front (STF) during chick rearing, which is in agreement with the known foraging ecology at this time and feeding north of the STF during moult. This, together with band recoveries from adult birds, indicates that black-browed albatrosses from Kerguelen Islands wintered in subtropical waters off southern Australia. The stable-isotope markers in feathers, therefore, have the potential for locating moulting areas of migratory seabird species moving between isotopically distinct regions and for investigating seabirds’ foraging ecology during the poorly known interbreeding period. Such information is needed for studies of year-round ecology of seabirds as well as for their conservation and the long-term monitoring of the pelagic environment. Received: 28 June 1999 / Accepted: 14 September 1999     

Sexual differences in morphology and niche utilization in an aquatic snake,Acrochordus arafurae

Filesnakes (Acrochordus arafurae) are large (to 2 m), heavy-bodied snakes of tropical Australia. Sexual dimorphism is evident in adult body sizes, weight/length ratios, and body proportions (relative head and tail lengths). Dimorphism is present even in neonates. Two hypotheses for the evolution of such dimorphism are (1) sexual selection or (2) adaptation of the sexes to different ecological niches. The hypothesis of sexual selection is consistent with general trends of sexually dimorphic body sizes in snakes, and accurately predicts, for A. arafurae, that the larger sex (female) is the one in which reproductive success increases most strongly with increasing body size. However, the sexual dimorphism in relative head sizes is not explicable by sexual selection.The hypothesis of adaptation to sex-specific niches predicts differences in habitats and/or prey. I observed major differences between male and female A. arafurae in prey types, prey sizes and habitat utilization (shallow versus deep water). Hence, the sexual dimorphism in relative head sizes is attributed to ecological causes rather than sexual selection. Nonetheless, competition between the sexes need not be invoked as the selective advantage of this character divergence. It is more parsimonious to interpret these differences as independent adaptations of each sex to increase foraging success, given pre-existing sexually-selected differences in size, habitat or behavior. Data for three other aquatic snake species, from phylogenetically distant taxa, suggest that sexual dimorphism in food habits, foraging sites and feeding morphology, is widespread in snakes.     

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.     

Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds

Some procellariiform seabirds use a dual strategy for provisioning their chicks by alternating short (ST) and long (LT) foraging trips. Parent birds gain mass during LT but they lose mass while increasing the chick feeding frequency during ST. Self-feeding during LT is crucial for the success of ST because firstly most of the energy used during ST is likely to be derived from the energy stored during LT and secondly self-feeding during ST is presumed to be negligible. Self-feeding by adult procellariiforms is thus a key issue to understand allocation processes but it is still poorly known. We tested these predictions by using the stable isotope (δ¹⁵N and δ¹³C) technique on birds’ plasma and prey with the short-tailed shearwater Puffinus tenuirostris breeding at Tasmania as a model. Parent shearwaters returning to the colony after a LT have an Antarctic/subantarctic δ¹³C signature in their plasma (−23.8‰), thus indicating that they fed in cold waters, far away from their breeding colony, for their own maintenance. Parent birds returning to the colony after a ST also have a distant Antarctic/subantarctic δ¹³C signature in their plasma (−24.3‰), thus verifying that self-feeding is negligible during ST and that birds fast at that time, using energy stores built up in cold waters. Plasma δ¹⁵N values of adults (8.8‰) indicates they mainly prey upon zooplankton-eating organisms, probably mesopelagic myctophid fishes. A simple isotopic mixing model estimates that they consume by mass 87% myctophids and 13% subantarctic krill when self-feeding. Finally and as expected, the carbon isotopic signature of chick plasma (−22.2‰) was intermediate between those of high- and low-latitude marine organisms and is thus in agreement with chicks being fed with a large diversity of prey species caught by adult birds from Antarctic to Tasmanian waters. One main consequence of this system is that reproduction of a Tasmanian species is controlled by resources available at great distances from the breeding colony that drive allocation decisions of parent birds.     

Ontogenetic change in blood oxygen capacity and maximum activity in garter snakes (Thamnophis sirtalis)

Summary There is an ontogenetic increase in the time that garter snakes (Thamnophis s. sirtalis) can maintain maximum activity at 25°C. Newborn snakes are exhausted by 3–5 min of activity while adults can be active for 20–25 min. The increased endurance of adult snakes results from ontogenetic increases in both aerobic and anaerobic energy generation. At rest juvenile and adult snakes have the same whole-body lactic acid concentrations, but at exhaustion adult lactic acid concentrations are 1.5 times those of juveniles. This increase in anaerobic energy production accounts for part of the endurance of adult snakes, but increased aerobic metabolism appears to be more important. Among the mechanisms increasing aerobic metabolism are more effective pulmonary ventilation and a 3-fold ontogenetic increase in blood oxygen capacity.The rapid exhaustion of small garter snakes probably limits the microhabitats they can occupy and the sorts of hunting methods they can employ. Small garter snakes feed only on small prey that are easily subdued. There is an ontogenetic increase in the relative size of prey eaten by garter snakes that parallels the ontogenetic increase in endurance. Adult feeding habits are adopted at the same body size at which adult blood oxygen capacity and endurance are attained.     

Isotopic tracking of foraging and long-distance migration in northeastern Pacific pinnipeds

We investigated the impact of foraging location (nearshore vs offshore) and foraging latitude (high vs middle) on the carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope compositions of bone collagen of northern fur seals (Callorhinus ursinus), harbor seals (Phoca vitulina), California sea lions (Zalophus californianus), and northern elephant seals (Mirounga angustirostris). Nearshore-foraging harbor seals from California had δ¹³C values 2.0‰ higher than female northern elephant seals foraging offshore at similar latitudes. Likewise, nearshore-foraging harbor seals from Alaska had values 1.7‰ higher than male northern fur seals, which forage offshore at high latitudes. Middle-latitude pinnipeds foraging in either the nearshore or offshore were ¹³C enriched by ∼1.0‰ over similar populations from high latitudes. Male northern elephant seals migrate between middle and high latitudes, but they had δ¹³C values similar to high-latitude, nearshore foragers. Female northern fur seal δ¹³C values were intermediate between those of high- and middle-latitude offshore foragers, reflecting their migration between high- and middle-latitude waters. The δ¹³C values of California sea lions were intermediate between nearshore- and offshore-foraging pinnipeds at middle latitudes, yet there was no observational support for the suggestion that they use offshore food webs. We suggest that their “intermediate” values reflect migration between highly productive and less-productive, nearshore ecosystems on the Pacific coasts of California and Mexico. The relative uniformity among all of these pinnipeds in δ¹⁵N values, which are strongly sensitive to trophic level, reveals that the carbon isotope patterns result from differences in the δ¹³C of organic carbon at the base of the food web, rather than differences in trophic structure, among these regions. Finally, the magnitude and direction of the observed nearshore-offshore and high-to middle-latitude differences in δ¹³C values suggest that these gradients may chiefly reflect differences in rates and magnitudes of phytoplankton production as well as the δ¹³C value of inorganic carbon available for photosynthesis, rather than the input of ¹³C-enriched macroalgal carbon to nearshore food webs. Received: 8 September 1998 / Accepted: 24 February 1999     

The δ13C changes in four plant species of the Loess Plateau over the last 70 years

The relative abundance of carbon isotope (δ¹³C) was measured in four C₃ species (Sophora viccifolia, Quercus liaotungensis, Ostryopsis davidiana and Zizyphus jujuba var. spinosa) of the Loess Plateau in China from the 1930’s to 2002. The results showed that the δ¹³C values in the four species varied from −25.05‰ to −29.75‰ with their a average at −27.04‰. A decrease in the δ¹³C value with time was found in all the four species, which indicating that the water use efficiencies (WUEs) of all the measured species declined during 70 years. However, the decrease in δ¹³C value differed among the four species with its significant decreases measured in two of the species, Sophora viciifolia and Quercus liaotungensis, its relatively significant decrease found in Ostryopsis davidiana, and its slight decrease appearing in Zizyphus jujuba var. spinosa. in the δ¹³C values in the four species decreased by 14.65 ‰, 14.46‰, 11.99‰ and 2.44‰, respectively. The different species were shown to have different sensitivities to climatic change, and Zizyphus jujuba var. spinosa was found to be the most drought-tolerant species of the four, which had a high WUE.