Tracking and predation on earthworms by the invasive terrestrial planarian Bipalium adventitium (Tricladida, Platyhelminthes)

The potential ecological impact of exotic terrestrial planarians will be determined in part by their sensory abilities and predatory behavior. It has been suggested that these flatworms may only encounter their earthworm prey by chance, hence restricting the breadth of species they will feed upon and the number of microhabitats in which predator-prey interactions occur. We hypothesized that those flatworms that have already successfully invaded North America (genus Bipalium) actually detect and follow chemical trails of earthworms and possess the behavioral repertoire needed to feed on the prey in a range of microhabitats. We examined: (1) the tendency of Bipalium adventitium to follow chemical trails left by injured and un-injured earthworms; (2) the behavioral repertoire and predatory success of B. adventitium feeding on three earthworm species in subterranean tunnels; and (3) the response of flatworms to the reportedly defensive secretions of the earthworm Eisenia fetida in tunnels. B. adventitium detected and followed trails of earthworm mucus and secretions left by injured and un-injured earthworms. Flatworms followed trails on a range of substrates and pursued and captured three species of earthworms in subterranean tunnels, including individuals many times their mass. Although most behavior exhibited during underground attacks was similar to that reported for surface encounters, the flatworms also behaved in ways that blocked earthworm escape from tunnels. The flatworms were less successful at preying on E. fetida than on Lumbricus rubellus and Lumbricus terrestris in underground tunnels and showed some aversion to the secretions from E. fetida.     

Phylogeny of Courtship and Male-Male Combat Behavior in Snakes

Background

Behaviors involved in courtship and male-male combat have been recorded in a taxonomically broad sample (76 species in five families) of snakes in the clade Boidae + Colubroidea, but before now no one has attempted to find phylogenetic patterns in such behaviors. Here, we present a study of phylogenetic patterns in such behaviors in snakes.

Methodology/Principal Findings

From the literature on courtship and male-male combat in snakes we chose 33 behaviors to analyze. We plotted the 33 behaviors onto a phylogenetic tree to determine whether phylogenetic patterns were discernible. We found that phylogenetic patterns are discernible for some behaviors but not for others. For behaviors with discernible phylogenetic patterns, we used the fossil record to determine minimum ages for the addition of each behavior to the courtship and combat behavioral repertoire of each snake clade.

Conclusions/Significance

The phylogenetic patterns of behavior reveal that male-male combat in the Late Cretaceous common ancestors of Boidae and Colubridae involved combatants raising the head and neck and attempting to topple each other. Poking with spurs was added in Boidae. In Lampropeltini the toppling behavior was replaced by coiling without neck-raising, and body-bridging was added. Phylogenetic patterns reveal that courtship ancestrally involved rubbing with spurs in Boidae. In Colubroidea, courtship ancestrally involved chin-rubbing and head- or body-jerking. Various colubroid clades subsequently added other behaviors, e.g. moving undulations in Natricinae and Lampropeltini, coital neck biting in the Eurasian ratsnake clade, and tail quivering in Pantherophis. The appearance of each group in the fossil record provides a minimum age of the addition of each behavior to combat and courtship repertoires. Although many gaps in the story of the evolution of courtship and combat in snakes remain, this study is an important first step in the reconstruction of the evolution of these behaviors in snakes.     

Odorous and Non-Fatal Skin Secretion of Adult Wrinkled Frog (Rana rugosa) Is Effective in Avoiding Predation by Snakes

The roles played by nonfatal secretions of adult anurans in the avoidance of predation remain unknown. The adult Wrinkled frog (Rana rugosa) has warty skin with the odorous mucus secretion that is not fatal to the snake Elaphe quadrivirgata. We fed R. rugosa or Fejervarya limnocharis, which resembles R. rugosa in appearance and has mucus secretion, to snakes and compared the snakes’ responses to the frogs. Compared to F. limnocharis, R. rugosa was less frequently bitten or swallowed by snakes. The snakes that bit R. rugosa spat out the frogs and showed mouth opening (gaping) behavior, while the snakes that bit F. limnocharis did not show gaping behavior. We also compared the responses of the snakes to R. rugosa and F. limnocharis secretions. We coated palatable R. japonica with secretions from R. rugosa or F. limnocharis. The frogs coated by R. rugosa secretion were less frequently bitten or swallowed than those coated by F. limnocharis secretion. We concluded that compared to different frog species of similar sizes, the adult R. rugosa was less frequently preyed upon by, and that its skin secretion was effective in avoiding predation by snakes.     

海南岛蚯蚓物种组成及其系统发育分析

海南岛独特的地理位置和复杂的古地理事件使其成为我国生物多样性的热点地区。已有的海南岛蚯蚓资料显示, 该岛的蚯蚓区系十分特殊, 且与大陆地区蚯蚓存在扩散与迁移。然而, 当海南岛与周围大陆断开形成独立岛屿后, 海南岛蚯蚓如何为适应海南岛的环境而逐渐形成现在岛内的分布与区系, 仍然是一个值得研究和探讨的问题。因此, 本研究在海南岛全面调查和采集蚯蚓标本, 整理海南岛地区的蚯蚓物种组成及其地理分布特征, 并联合5个线粒体基因COⅠ、COⅡ、ND1、12S rRNA和16S rRNA构建海南岛蚯蚓的分子系统发育树, 推测其分化时间和祖先分布区域, 探讨海南岛蚯蚓在岛内的分化与扩散过程。研究结果表明: (1)海南岛共有蚯蚓6科9属122种, 巨蚓科蚯蚓为优势科, 且全部为环毛类蚯蚓, 其中103种为海南岛特有种。蚯蚓物种数沿海拔呈先增加后减少的趋势, 在800‒1,000 m最大; (2)海南岛环毛类蚯蚓不同水平的遗传距离与我国巨蚓科蚯蚓的遗传距离区间基本一致。物种水平上, 美丽远盲蚓(Amynthas scitulus*)与纬向远盲蚓(A. zonarius)的基因遗传距离最小。在亚种水平, 保宁腔蚓指名亚种(Metaphire magna magna)和保宁腔蚓小型亚种(M. magna minuscula)的遗传距离均接近整体的物种水平。在种群水平, 等毛远盲蚓(A. homosetus)不同种群间遗传距离均接近整体的亚种水平; (3)海南岛环毛类蚯蚓可划分为7个类群, 其祖先于68.26 Ma开始分化, 可能起源于吊罗山。在新生代, 7个类群均得到较大发展。通过对海南岛蚯蚓组成及系统发育的梳理, 不仅为我国蚯蚓物种多样性研究提供基础资料, 也为岛屿蚯蚓物种系统发育关系分析提供科学参考。     

Effects of earthworm mucus and amino acids on cadmium subcellular distribution and chemical forms in tomato seedlings

In order to investigate the basic mechanism of earthworm activities enhancing plants growth and heavy metals accumulations. A hydroponic experiment was carried out to investigate the effects of earthworm mucus and mimic amino acids solution of earthworm mucus on cadmium (Cd) subcellular distributions and chemical forms in tomato seedlings. The result showed that earthworm mucus significantly increased the concentrations of Cd stored in soluble fraction in subcellular distribution and the concentrations of inorganic and soluble forms of Cd in tomato seedlings, which may explain the increase plants growth and Cd accumulation by earthworm mucus. Meanwhile, amino acids have same function as earthworm mucus, but the effect was much lower than of earthworm mucus. These results indicated that earthworm mucus could increase tomato seedlings growth and Cd accumulations through changing Cd subcellular distribution and chemical forms in plants.     

FLIPPER RUBBING BEHAVIORS IN WILD BOTTLENOSE DOLPHINS (TURSIOPS ADUNCUS)

"Flipper rubbing" behavior was quantitatively analyzed in wild Indo-Pacific bottlenose dolphins ( Tursiops aduncus ) around Mikura Island, Tokyo, Japan. We observed two types of flipper rubbing: (1) F-B rubbing; one dolphin (Rubber) rubbed its flipper over various parts of a partner's (Rubbee) body, and (2) F-F rubbing; both dolphins rubbed each other's anterior flipper edge in alternating shifts. F-B rubbings tended to be initiated by the Rubbee and were terminated by the Rubber. The Rubbee often moved actively its body part that was in contact with the Rubber's flipper, and assumed side-up, upside-down, or other postures while the Rubber remained horizontal in most cases. These facts suggest that the Rubbee engaged in F-B rubbing more actively than the Rubber, and might receive some benefit from the frictional contact during F-B rubbing. Dolphins often switched their roles as Rubber and Rubbee between episodes of flipper rubbing bout. Adults and sub-adults exchanged F-B rubbing and F-F rubbing most often with individuals of the same sex in the same age class. F-B rubbing was frequent in mother-and-calf dyads. Our results suggest that flipper rubbing is an affiliative behavior which could be a quantitative measure of social relationships among individuals of this species in future studies.     

The impact of diet,habitat use,and behaviour on head shape evolution in homalopsid snakes

An organism's morphology is driven by selection on function while being constrained by phylogenetic and developmental factors as well as functional trade‐offs. If selection on function is strong and solutions limited, then convergence is expected. In this paper we quantify head shape in a group of ecologically diverse snakes (homalopsid snakes) differing in habitat use and diet using three‐dimensional geometric morphometric approaches. Using data on head shape we explore whether snakes eating different prey show different morphologies. Moreover, we test whether head shape is constrained by other factors such as habitat use, burrow use, or activity pattern. Our results demonstrate similar head shapes in species consuming similar prey. Snakes that capture elusive prey under water differ from those that capture and swallow prey like frogs or crustaceans. Moreover, habitat use, the use of burrows, and activity pattern also significantly impact head shape in this group of snakes. However, this signal appears to be partly confounded by the diet signal. For axes discriminating specifically between habitat use groups or animals that use burrows vs. those that do not shapes were in accordance with our predictions. Our results suggests an adaptive signal in the evolution of head shape in homalopsid snakes with diet, habitat use and the use of burrows all influencing the evolution of head shape in the group.     

Non-native earthworms alter the assembly of a meadow plant community

Non-native earthworms can alter ecosystems by modifying soil structure, depredating seeds and seedlings, and consuming soil organic matter, yet the initial responses of plant communities to earthworm invasions remain poorly understood. We assessed the effect of non-native earthworms on seedling survival during germination and after establishment using six native and six non-native plant species grown from seed in single- and multi-species experimental mesocosms. We examined the extent to which earthworms (1) influenced seedling survival, (2) selectively depredated native versus non-native plants, (3) impacted establishment based on seed size and/or root morphology, and (4) shaped community assembly. The effect of earthworms on seedling survival varied temporally and among species but inconsistently with respect to species origin. Differences in seed/seedling survival translated to changes in community assembly. Earthworms tended to reduce species abundance, richness, evenness, and diversity in multi-species mesocosms and led to the divergence of communities by treatment. In general, species with large seeds and fibrous roots dominated communities with earthworms present, whereas species with small seeds and taproots only persisted in multi-species mesocosms without earthworms. Our findings suggest that earthworms act as ecological filters in the early stages of invasion to shape community composition based on plant morphological traits.

     

Susceptibility of indigenous UK earthworms and an invasive pest flatworm to the slug parasitic nematode Phasmarhabditis hermaphrodita

We exposed five earthworm species, one flatworm species and the susceptible slug Deroceras reticulatum to the recommended field application rate and five times this rate of Phasmarhabditis hermaphrodita. P. hermaphrodita caused significant mortality to D. reticulatum at the recommended rate and five times the recommended rate. Survival of the earthworms and the flatworm was not different from the untreated controls. P. hermaphrodita is a safe biological control agent causing no harm to earthworms and could not be used to kill Arthurdendyus triangulatus.     

Contexts of rubbing behavior in Alouatta guariba clamitans: a scent‐marking role?

Rubbing behaviors are well known in several primate species and are usually seen as scent-marking behaviors, with several functions proposed but still widely debated. The genus Alouatta is highly sexually dimorphic and a suitable subject for the study of sexual and hierarchical divergences associated with rubbing behavior: males should mark more than females, and dominant individuals more than subordinate ones. Three wild groups of Southern brown howler monkeys, Alouatta guariba clamitans, were studied at Morro Geisler, Indaial, Brazil, from September 2004 to February 2005. One hundred and twenty-three rubbing episodes were registered; data on performers and associated contexts showed that anogenital, dorsum and hyoid regions were the most often rubbed. Adult males rubbed significantly above expected levels, whereas subordinated females and juveniles tended to rub below the expected levels. Females were the main performers of anogenital rubbing, often preceded by defecation. The predominance of rubbing in males probably serves an important function in intrasexual communication and social interactions. Intrasexual competition can also lead to a relationship between rubbing and social status in females. Hyoid and sternum rubbing by males are probably agonistic signals associated with extragroup conflict. The possible cleaning function of anogenital rubbing does not preclude a communicative function. Whether rubbing behavior in howlers is solely for the function of scent marking or can also be a visual signal (e.g. as a display or to color the substrate with pigment) requires further study.     

蚯蚓基因组学的研究进展: 基于全基因组及线粒体基因组

蚯蚓被喻为土壤中的“生态系统工程师”, 具有高度的多样性且在全世界都有分布, 被用作土壤健康的指示生物。蚯蚓具有极强的环境适应能力, 在不断适应的过程中促进了自身基因组的进化。本文对近年来蚯蚓全基因组以及线粒体基因组的研究进展进行了综述。蚯蚓全基因组的测序、拼装和分析为研究蚯蚓生态学、污染物对蚯蚓致毒的分子机制、免疫防御的分子机制、蚯蚓再生的分子机制等奠定基础。而线粒体基因组多应用于蚯蚓分子系统发育方面的研究, 目前已有多种蚯蚓通过线粒体基因组测序完成了物种的鉴定。本文建议今后重点开展以下几方面的研究: (1)针对现有的4种蚯蚓全基因组测序结果, 进一步进行比较基因组学、进化基因组学和功能基因组学的研究。(2)完善不同种蚯蚓的基因文库和表达序列标签。(3)建立线粒体基因组、全基因组与蚯蚓物种多样性的关联分析。     

Nest mounds of red wood ants (Formicaaquilonia): hot spots for litter-dwelling earthworms

A previously undocumented association between earthworms and red wood ants (Formicaaquilonia Yarr.) was found during an investigation of the influence of wood ants on the distribution and abundance of soil animals in boreal forest soil. Ant nest mounds and the surrounding soil of the ant territories were sampled. The ant nest mound surface (the uppermost 5-cm layer) harboured a much more abundant earthworm community than the surrounding soil; the biomass of the earthworms was about 7 times higher in the nests than in the soil. Dendrodrilusrubidus dominated the earthworm community in the nests, while in soils Dendrobaenaoctaedra was more abundant. Favorable temperature, moisture and pH (Ca content), together with abundant food supply (microbes and decomposing litter) are likely to make a nest mound a preferred habitat for earthworms, provided that they are not preyed upon by the ants. We also conducted laboratory experiments to study antipredation mechanisms of earthworms against ants. The experiments showed that earthworms do not escape predation by avoiding contact with ants in their nests. The earthworm mucus repelled the ants, suggesting a chemical defence against predation. Earthworms probably prevent the nest mounds from becoming overgrown by moulds and fungi, indicating possible mutualistic relationships between the earthworms and the ants. Received: 21 November 1996 / Accepted: 3 April 1997     

'Candidatus Lumbricincola', a novel lineage of uncultured Mollicutes from earthworms of family Lumbricidae

Molecular signatures of new, as yet uncultured mollicute-like organisms (MLOs) have been detected in total rRNA and DNA extracted from tissues, gut contents and casts of four species of the earthworm family Lumbricidae. The MLO 16S rRNA sequences exhibited low identity to those of known Mollicutes species and formed a monophyletic cluster distantly affiliated to the ' Candidatus Bacilloplasma' (84.9%) and almost equidistant to the other main phylogenetic group of Mollicutes (< 79.8%) and the classes Bacilli (< 79.5%) and Clostridia (< 76.1%). SSCP profiling and sequence analysis of bands and bacterial clones derived from the earthworms and substrata revealed high phylogenetic relatedness of MLOs in earthworms from different geographic locations (Russia and Germany), with no obvious host species specificity being observed. Fluorescence in situ hybridization (FISH) analysis with a nucleotide probe specific for the new MLO group localized them to the coelomic fluids of earthworms. A new taxonomic group within the Mollicutes , designated ' Candidatus Lumbricincola', is proposed to include these as yet uncultured organisms.     

Policy and management responses to earthworm invasions in North America

The introduction, establishment and spread of non-native earthworm species in North America have been ongoing for centuries. These introductions have occurred across the continent and in some ecosystems have resulted in considerable modifications to ecosystem processes and functions associated with above- and belowground foodwebs. However, many areas of North America have either never been colonized by introduced earthworms, or have soils that are still inhabited exclusively by native earthworm fauna. Although several modes of transport and subsequent proliferation of non-native earthworms have been identified, little effort has been made to interrupt the flow of new species into new areas. Examples of major avenues for introduction of earthworms are the fish-bait, horticulture, and vermicomposting industries. In this paper we examine land management practices that influence the establishment of introduced species in several ecosystem types, and identify situations where land management may be useful in limiting the spread of introduced earthworm species. Finally, we discuss methods to regulate the importation of earthworms and earthworm-containing media so that introduction of new exotic species can be minimized or avoided. Although our focus in this paper is necessarily North American, many of the management and policy options presented here could be applicable to the problem of earthworm invasions in other parts of the world.     

Tree leaf litter composition and nonnative earthworms influence plant invasion in experimental forest floor mesocosms

Dominant tree species influence community and ecosystem components through the quantity and quality of their litter. Effects of litter may be modified by activity of ecosystem engineers such as earthworms. We examined the interacting effects of forest litter type and earthworm presence on invasibility of plants into forest floor environments using a greenhouse mesocosm experiment. We crossed five litter treatments mimicking historic and predicted changes in dominant tree composition with a treatment of either the absence or presence of nonnative earthworms. We measured mass loss of each litter type and growth of a model nonnative plant species (Festuca arundinacea, fescue) sown into each mesocosm. Mass loss was greater for litter of tree species characterized by lower C:N ratios. Earthworms enhanced litter mass loss, but only for species with lower C:N, leading to a significant litter × earthworm interaction. Fescue biomass was significantly greater in treatments with litter of low C:N and greater mass loss, suggesting that rapid decomposition of forest litter may be more favorable to understory plant invasions. Earthworms were expected to enhance invasion by increasing mass loss and removing the physical barrier of litter. However, earthworms typically reduced invasion success but not under invasive tree litter where the presence of earthworms facilitated invasion success compared to other litter treatments where earthworms were present. We conclude that past and predicted future shifts in dominant tree species may influence forest understory invasibility. The presence of nonnative earthworms may either suppress of facilitate invasibility depending on the species of dominant overstory tree species and the litter layers they produce.     

Earthworm invasions of ecosystems devoid of earthworms: effects on soil microbes

Recent studies document North American earthworm invasions and their profound effects on the structure of the soil profile, which is the habitat for soil microorganisms (mainly fungi and bacteria). Dramatic alterations made to these layers during earthworm invasion significantly change microbial community structure and therefore microbial activities such as C transformations. Understanding the impacts of earthworm invasion on the microbes themselves will give insight into earthworm effects on microbial activities. Bacterial and actinomycete communities in earthworm guts and casts have not been studied in environments recently invaded by earthworms. Earthworm invasion tended to decrease fungal species density and fungal species diversity and richness. The presence of earthworms decreased zygomycete species abundance probably due to disruption of fungal hyphae. Physical disruption of hyphae may also explain decreased mycorrhizal colonization rates, decreased mycorrhizal abundance and altered mycorrhizal morphology in the presence of earthworms. Mixing of organic layers into mineral soil during earthworm invasion tended to decrease microbial biomass in forest floor materials while increasing it in mineral soil. In newly invaded forest soils, microbial respiration and the metabolic quotient tended to decline. In forests where either the microbial community has had time to adapt to earthworm activities, or where the destruction of the forest floor is complete, as in invasions by the Asian Amynthas hawayanus, the presence of earthworms tends to increase the metabolic quotient indicating a shift to a smaller, more active microbial community.     

Effects of Exotic Earthworms on Soil Phosphorus Cycling in Two Broadleaf Temperate Forests

We compared the biogeochemical cycling of phosphorus (P) in northern hardwood forest plots invaded by exotic earthworms versus adjacent uninvaded reference plots. In three of the six pairs of plots, earthworm invasion resulted in significantly more total P in the upper 12 cm of soil. The finding of increased amounts of unavailable and occluded inorganic P forms in the invaded plots suggests that earthworm activity mobilized unweathered soil particles from deeper layers of the soil, increasing the stocks of total P in surface soils. In two pairs of plots, the earthworm-invaded soils had less total P than the reference soils. In these plots, earthworm activity resulted in augmented rates of P cycling and alteration of the physical structure of the soil that increased loss of P in leaching water, reducing the total amount of P. We hypothesize that the different effects of earthworm invasion on the soil P cycle result from unique characteristics of the ecological groups of earthworms dominating each site. The invaded plots with increased total P were dominated by the anecic species Lumbricus terrestris, a large earthworm that constructs deep, vertical burrows and is effective at moving soil materials from and to deeper layers of the profile. In contrast, the earthworm-invaded plots where the total P in the surface soil decreased were dominated by the epi-endogeic species L. rubellus, which feeds and lives in the upper organic layers of the soil. In these plots, earthworms significantly increased the amount of readily exchangeable P in the soil, increasing the loss of this element in leaching water.     

Invasion Patterns of Lumbricidae Into the Previously Earthworm-free Areas of Northeastern Europe and the Western Great Lakes Region of North America

We examine the patterns of expansion of exotic European earthworms in northeastern Europe and the western Great Lakes region of North America. These areas share many ecological, climatic and historical characteristics and are devoid of indigenous earthworm fauna due to Quaternary glaciations. These regions are being colonized by a similar suite of exotic lumbricid species and it is unlikely that this is the result of chance, but rather indicates that these species have particular characteristics making them successful invaders. The present macro-scale distributions of earthworm species in northern Russia show little connection to the pattern of the last glaciation. Rather, the primary factors that determine the current distributions of earthworm species include climatic conditions, the life history traits of different earthworm species, the suitability of habitat and intensity and patterns of human activity. In the western Great Lakes region of North America, there are three primary factors affecting current distributions of exotic earthworm species including the patterns of human activity and land use practices, the composition of particular source populations of earthworms associated with different vectors of transport and the soil and litter properties of habitats across the region. Disturbance of a habitat does not appear to be a prerequisite to the invasion and establishment of exotic earthworms. Analysis of the macro-scale distributions of Lumbricidae species in northeastern Europe may provide important insights into the potential of invasive European earthworm species to spread in North America, and identify potentially invasive species.     

Ecosystem Consequences of Exotic Earthworm Invasion of North Temperate Forests

The invasion of north temperate forests by exotic species of earthworms is an important issue that has been overlooked in the study and management of these forests. We initiated research to address the hypothesis that earthworm invasion will have large consequences for nutrient retention and uptake in these ecosystems. In this special feature of Ecosystems, we present five papers describing results from our experiment. In this paper, we (a) introduce our experimental approach and conceptual model of how earthworms influence forest ecosystem processes, (b) describe the characteristics of the study areas and earthworm communities at our two study locations, and (c) provide a brief overview and synthesis of the main findings. The most dramatic effect of earthworm invasion was the loss of the forest floor at an undisturbed forest site, which altered the location and nature of nutrient cycling activity in the soil profile. Invasion changed soil total carbon (C) and phosphorus (P) pools, carbon–nitrogen (C:N) ratios, the loss and distribution of different soil P fractions, and the distribution and function of roots and microbes. Response to invasion varied with site characteristics and earthworm species. Our results suggest that exotic earthworm invasion is a significant factor that will influence the structure and function of northern temperate forest ecosystems over the next few decades. Regional evaluations of these forests will need to consider the presence or absence of earthworms along with other important ecosystem drivers, such as pollution, climate, and underlying soil characteristics.     

Cryptic forcible insemination: male snakes exploit female physiology, anatomy, and behavior to obtain coercive matings

Whether males can inseminate uncooperative females is a central determinant of mating system evolution that profoundly affects the interpretation of phenomena such as multiple mating by females, mate choice, reproductive seasonality, and courtship tactics. Forcible insemination is usually inferred from direct physical battles between the sexes and has been dismissed on intuitive grounds for many kinds of animals. For example, snakes have elongate flexible bodies (making it difficult for a male to restrain a female physically), males are typically smaller than females, and copulation requires female cloacal gaping to enable intromission. Male garter snakes (Thamnophis sirtalis) do not display any overt aggression during courtship and simply lie over the female and exhibit rhythmic pulsating caudocephalic waves of muscular contraction; previous studies have interpreted this behavior as a mechanism for eliciting female receptivity. In contrast, we show that male garter snakes forcibly inseminate females. They do so by taking advantage of specific features of snake physiology, respiratory anatomy, and antipredator behavior. The snake lung extends along most of the body, with the large posterior section (the saccular lung) lacking any respiratory exchange surface. Rhythmic caudocephalic waves by courting male garter snakes push anoxic air from the saccular lung forward and across the respiratory surfaces such that females cannot obtain oxygen. Their stress response involves cloacal gaping, which functions in other contexts to repel predators by extruding feces and musk but in this situation permits male intromission. Thus, superficially benign courtship behaviors may involve cryptic coercion even in species for which intuition dismisses any possibility of forcible insemination.