Sensory integration of danger and safety cues may explain the fear of a quiet coyote.

Sensory integration theory predicts natural selection should favour adaptive responses of animals to multiple forms of information, yet empirical tests of this prediction are rare, particularly in free-living mammals. Studying indirect predator cues offers a salient opportunity to inquire about multimodal risk assessment and its potentially interactive effects on prey responses. Here we exposed California ground squirrels from two study sites (that differ in human and domestic dog activity) to acoustic and/or olfactory predator cues to reveal divergent patterns of signal dominance. Olfactory information most strongly predicted space use within the testing arena. That is, individuals, especially those at the human-impacted site, avoided coyote urine, a danger cue that may communicate the proximity of a coyote. By contrast, subjects allocated less time to risk-sensitive behaviours when exposed to acoustic cues. Specifically, although individuals were consistent in their behavioural responses across trials, 'quiet coyotes' (urine without calls) significantly increased the behavioural reactivity of prey, likely because coyotes rarely vocalize when hunting. More broadly, our findings highlight the need to consider the evolution of integrated fear responses and contribute to an emerging understanding of how animals integrate multiple forms of information to trade off between danger and safety cues in a changing world.

Standardization of in situ coral bleaching measurements highlights the variability in responses across genera, morphologies, and regions.

Marine heatwaves and regional coral bleaching events have become more frequent and severe across the world's oceans over the last several decades due to global climate change. Observational studies have documented spatiotemporal variation in the responses of reef-building corals to thermal stress within and among taxa across geographic scales. Although many tools exist for predicting, detecting, and quantifying coral bleaching, it remains difficult to compare bleaching severity (e.g., percent cover of bleached surface areas) among studies and across species or regions. For this review, we compiled over 2,100 in situ coral bleaching observations representing 87 reef-building coral genera and 250 species of common morphological groups from a total of 74 peer-reviewed scientific articles, encompassing three broad geographic regions (Atlantic, Indian, and Pacific Oceans). While bleaching severity was found to vary by region, genus, and morphology, we found that both genera and morphologies responded differently to thermal stress across regions. These patterns were complicated by (i) inconsistent methods and response metrics across studies; (ii) differing ecological scales of observations (i.e., individual colony-level vs. population or community-level); and (iii) temporal variability in surveys with respect to the onset of thermal stress and the chronology of bleaching episodes. To improve cross-study comparisons, we recommend that future surveys prioritize measuring bleaching in the same individual coral colonies over time and incorporate the severity and timing of warming into their analyses. By reevaluating and standardizing the ways in which coral bleaching is quantified, researchers will be able to track responses to marine heatwaves with increased rigor, precision, and accuracy.

Ocean currents magnify upwelling and deliver nutritional subsidies to reef-building corals during El Niño heatwaves.

Marine heatwaves are triggering coral bleaching events and devastating coral populations globally, highlighting the need to identify processes promoting coral survival. Here, we show that acceleration of a major ocean current and shallowing of the surface mixed layer enhanced localized upwelling on a central Pacific coral reef during the three strongest El Niño-associated marine heatwaves of the past half century. These conditions mitigated regional declines in primary production and bolstered local supply of nutritional resources to corals during a bleaching event. The reefs subsequently suffered limited post-bleaching coral mortality. Our results reveal how large-scale ocean-climate interactions affect reef ecosystems thousands of kilometers away and provide a valuable framework for identifying reefs that may benefit from such biophysical linkages during future bleaching events.

Toward an evolutionary ecology of (in)equality.

Inequality is increasingly recognized as a major problem in contemporary society. The causes and consequences of inequality in wealth and power have long been central concerns in the social sciences, whereas comparable research in biology has focused on dominance and reproductive skew. This theme issue builds on these existing research traditions, exploring ways they might enrich each other, with evolutionary ecology as a possibly unifying framework. Contributors investigate ways in which inequality is resisted or avoided and developed or imposed in societies of past and contemporary humans, as well as a variety of social mammals. Particular attention is paid to systematic, socially driven inequality in wealth (defined broadly) and the effects this has on differential power, health, survival and reproduction. Analyses include field studies, simulations, archaeological and ethnographic case studies, and analytical models. The results reveal similarities and divergences between human and non-human patterns in wealth, power and social dynamics. We draw on these insights to present a unifying conceptual framework for analysing the evolutionary ecology of (in)equality, with the hope of both understanding the past and improving our collective future. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Mechanisms of equality and inequality in mammalian societies.

The extent of (in)equality is highly diverse across species of social mammals, but we have a poor understanding of the factors that produce or inhibit equitable social organizations. Here, we adopt a comparative evolutionary perspective to test whether the evolution of social dominance hierarchies, a measure of social inequality in animals, exhibits phylogenetic conservatism and whether interspecific variation in these traits can be explained by sex, age or captivity. We find that hierarchy steepness and directional consistency evolve rapidly without any apparent constraint from evolutionary history. Given this extraordinary variability, we next consider multiple factors that have evolved to mitigate social inequality. Social networks, coalitionary support and knowledge transfer advantage to privilege some individuals over others. Nutritional access and prenatal stressors can impact the development of offspring, generating health disparities with intergenerational consequences. Intergenerational transfer of material resources (e.g. stone tools, food stashes, territories) advantage those who receive. Nonetheless, many of the same social species that experience unequal access to food (survival) and mates (reproduction) engage in levelling mechanisms such as food sharing, adoption, revolutionary coalitions, forgiveness and inequity aversion. Taken together, mammals rely upon a suite of mechanisms of (in)equality to balance the costs and benefits of group living. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Sex differences in cooperative coalitions: a mammalian perspective.

In group-living species, cooperative tactics can offset asymmetries in resource-holding potential between individuals and alter the outcome of intragroup conflicts. Differences in the kinds of competitive pressures that males and females face might influence the benefits they gain from forming intragroup coalitions. We predicted that there would be a female bias in intragroup coalitions because females (1) are more like to live with kin than males are, and (2) compete over resources that are more readily shared than resources males compete over. We tested this main prediction using information about coalition formation across mammalian species and phylogenetic comparative analyses. We found that for nearly all species in which intragroup coalitions occur, members of both sexes participate, making this the typical mammalian pattern. The presence and frequency of female or male coalitions were not strongly associated with key socio-ecological factors like resource defensibility, sexual dimorphism or philopatry. This suggests that once the ability to form intragroup coalitions emerges in one sex, it is likely to emerge in the other sex as well and that there is no strong phylogenetic legacy of sex differences in this form of cooperation. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Evidence of Biological Self-Organization in Spatial Patterns of a Common Tropical Alga.

AbstractTropical reef communities contain spatial patterns at multiple scales, observable from microscope and satellite alike. Many of the smaller-scale patterns are generated physiologically (e.g., skeletal structures of corals at <1-m scale), while some of the larger patterns have been attributed to scale-dependent feedbacks (e.g., spur and groove reefs at 10-100-m scales). In describing the spatial patterning of reef benthic communities at landscape levels, we uncovered unique spatial patterning among living marine algae. Populations of the calcifying green alga Halimeda were observed to form a consistent polygonal pattern at a characteristic scale of 3-4 m. The pattern showed no clear evidence of having been formed through biologically created shifts in hydrodynamical conditions or related mechanisms. In considering the specifics of Halimeda growth patterns, a model of self-organization involving separation and patterned extension is proposed, a mechanism revealed in some geological pattern formation. This observation reinforces the diversity of pathways by which striking spatial patterns can occur in ecosystems.

Consequences of Warming and Acidification for the Temperate Articulated Coralline Alga, Calliarthron Tuberculosum (Florideophyceae, Rhodophyta).

Global climate changes, such as warming and ocean acidification (OA), are likely to negatively impact calcifying marine taxa. Abundant and ecologically important coralline algae may be particularly susceptible to OA; however, multi-stressor studies and those on articulated morphotypes are lacking. Here, we use field observations and laboratory experiments to elucidate the impacts of warming and acidification on growth, calcification, mineralogy, and photophysiology of the temperate articulated coralline alga, Calliarthron tuberculosum. We conducted a 4-week fully factorial mesocosm experiment exposing individuals from a southern CA kelp forest to current and future temperature and pH/pCO2 conditions (+2°C, -0.5 pH units). Calcification was reduced under warming (70%) and further reduced by high pCO2 or high pCO2 x warming (~150%). Growth (change in linear extension and surface area) was reduced by warming (40% and 50%, respectively), high pCO2 (20% and 40%, respectively), and high pCO2 x warming (50% and 75%, respectively). The maximum photosynthetic rate (Pmax ) increased by 100% under high pCO2 conditions, but we did not detect an effect of pCO2 or warming on photosynthetic efficiency (α). We also did not detect the effect of warming or pCO2 on mineralogy. However, variation in Mg incorporation in cell walls of different cell types (i.e., higher mol % Mg in cortical vs. medullary) was documented for the first time in this species. These results support findings from a growing body of literature suggesting that coralline algae are often more negatively impacted by warming than OA, with the potential for antagonistic effects when factors are combined.

Sex bias in intergroup conflict and collective movements among social mammals: male warriors and female guides.

Intergroup conflict is a major evolutionary force shaping animal and human societies. Males and females should, on average, experience different costs and benefits for participating in collective action. Specifically, among mammals, male fitness is generally limited by access to mates whereas females are limited by access to food and safety. Here we analyse sex biases among 72 species of group-living mammals in two contexts: intergroup conflict and collective movements. Our comparative phylogenetic analyses show that the modal mammalian pattern is male-biased participation in intergroup conflict and female-biased leadership in collective movements. However, the probability of male-biased participation in intergroup conflicts decreased and female-biased participation increased with female-biased leadership in movements. Thus, female-biased participation in intergroup conflict only emerged in species with female-biased leadership in collective movements, such as in spotted hyenas and some lemurs. Sex differences are probably attributable to costs and benefits of participating in collective movements (e.g. towards food, water, safety) and intergroup conflict (e.g. access to mates or resources, risk of injury). Our comparative review offers new insights into the factors shaping sex bias in leadership across social mammals and is consistent with the 'male warrior hypothesis' which posits evolved sex differences in human intergroup psychology. This article is part of the theme issue 'Intergroup conflict across taxa'.

The benefits of being dominant: health correlates of male social rank and age in a marmot.

The benefits of dominance may not come without costs, particularly for males. For example, the "immunocompetence handicap hypothesis" states that males with enhanced mating success allocate resources to enhance reproductive output at a cost to their current health, whereas the "resource quality hypothesis" predicts that high-ranking males may benefit from increased reproduction and good health. Whereas the predictions from each have been well tested in captive animals and in a variety of highly social primates, fewer studies have been carried out in free-living, facultatively social animals. Using adult male yellow-bellied marmots (Marmota flaviventer), we evaluated predictions of these hypotheses by examining the relationship between social rank and 2 health indicators-fecal glucocorticoid metabolite (FCM) levels, and neutrophil/lymphocyte (N/L) ratios-after accounting for variation explained by age, body mass, and seasonality. We found that higher-ranking males tended to have a lower N/L ratio (reflecting good health) than lower-ranking individuals, whereas FCM levels were not significantly related to rank. In addition, heavier male marmots had lower N/L ratios, whereas body mass was not associated with FCM levels. We also found that older adult males had lower FCM levels (reflecting less physiological stress) but higher N/L ratios than younger adults. Finally, we found that FCM levels decreased as the active season progressed and FCM levels were associated with the time of the day. Overall, our results suggest that socially-dominant male marmots enjoyed better, not worse health in terms of lower N/L ratios.

Brilliantia kiribatiensis, a new genus and species of Cladophorales (Chlorophyta) from the remote coral reefs of the Southern Line Islands, Pacific Ocean.

The marine green alga Brilliantia kiribatiensis gen. et sp. nov. is described from samples collected from the coral reefs of the Southern Line Islands, Republic of Kiribati, Pacific Ocean. Phylogenetic analysis of sequences of the large- and small-subunit rDNA and the rDNA internal transcribed spacer region revealed that Brilliantia is a member of the Boodleaceae (Cladophorales), containing the genera Apjohnia, Boodlea, Cladophoropsis, Chamaedoris, Phyllodictyon, and Struvea. Within this clade it formed a distinct lineage, sister to Struvea elegans, but more distantly related to the bona fide Struvea species (including the type S. plumosa). Brilliantia differs from the other genera by having a very simple architecture forming upright, unbranched, single-celled filaments attached to the substratum by a rhizoidal mat. Cell division occurs by segregative cell division only at the onset of reproduction. Based on current sample collection, B. kiribatiensis seems to be largely restricted to the Southern Line Islands, although it was also observed on neighboring islands, including Orona Atoll in the Phoenix Islands of Kiribati, and the Rangiroa and Takapoto Atolls in the Tuamotus of French Polynesia. This discovery highlights the likeliness that there is still much biodiversity yet to be discovered from these remote and pristine reefs of the central Pacific.

Host traits, identity, and ecological conditions predict consistent flea abundance and prevalence on free-living California ground squirrels.

Understanding why some individuals are more prone to carry parasites and spread diseases than others is a key question in biology. Although epidemiologists and disease ecologists increasingly recognize that individuals of the same species can vary tremendously in their relative contributions to the emergence of diseases, very few empirical studies systematically assess consistent individual differences in parasite loads within populations over time. Two species of fleas (Oropsylla montana and Hoplopsyllus anomalous) and their hosts, California ground squirrels (Otospermophilus beecheyi), form a major complex for amplifying epizootic plague in the western United States. Understanding its biology is primarily of major ecological importance and is also relevant to public health. Here, we capitalize on a long-term data set to explain flea incidence on California ground squirrels at Briones Regional Park in Contra Costa County, USA. In a 7 year study, we detected 42,358 fleas from 2,759 live trapping events involving 803 unique squirrels from two free-living populations that differed in the amount of human disturbance in those areas. In general, fleas were most abundant and prevalent on adult males, on heavy squirrels, and at the pristine site, but flea distributions varied among years, with seasonal conditions (e.g., temperature, rainfall, humidity), temporally within summers, and between flea species. Although on-host abundances of the two flea species were positively correlated, each flea species occupied a distinctive ecological niche. The common flea (O. montana) occurred primarily on adults in cool, moist conditions in early summer whereas the rare flea (H. anomalous) was mainly on juveniles in hot, dry conditions in late summer. Beyond this, we uncovered significantly repeatable and persistent effects of host individual identity on flea loads, finding consistent individual differences among hosts in all parasite measures. Taken together, we reveal multiple determinants of parasites on free-living mammals, including the underappreciated potential for host heterogeneity - within populations - to structure the emergence of zoonotic diseases such as bubonic plague.

Brain Protection in Aortic Arch Surgery: An Evolving Field.

Despite advances in cardiac surgery and anesthesia, the rates of brain injury remain high in aortic arch surgery requiring circulatory arrest. The mechanisms of brain injury, including permanent and temporary neurologic dysfunction, are multifactorial, but intraoperative brain ischemia is likely a major contributor. Maintaining optimal cerebral perfusion during cardiopulmonary bypass and circulatory arrest is the key component of intraoperative management for aortic arch surgery. Various brain monitoring modalities provide different information to improve cerebral protection. Electroencephalography gives crucial data to ensure minimal cerebral metabolism during deep hypothermic circulatory arrest, transcranial Doppler directly measures cerebral arterial blood flow, and near-infrared spectroscopy monitors regional cerebral oxygen saturation. Various brain protection techniques, including hypothermia, cerebral perfusion, pharmacologic protection, and blood gas management, have been used during interruption of systemic circulation, but the optimal strategy remains elusive. Although deep hypothermic circulatory arrest and retrograde cerebral perfusion have their merits, there have been increasing reports about the use of antegrade cerebral perfusion, obviating the need for deep hypothermia. With controversy and variability of surgical practices, moderate hypothermia, when combined with unilateral antegrade cerebral perfusion, is considered safe for brain protection in aortic arch surgery performed with circulatory arrest. The neurologic outcomes of brain protection in aortic arch surgery largely depend on the following three major components: cerebral temperature, circulatory arrest time, and cerebral perfusion during circulatory arrest. The optimal brain protection strategy should be individualized based on comprehensive monitoring and stems from well-executed techniques that balance the major components contributing to brain injury.

Observing the unwatchable: Integrating automated sensing, naturalistic observations and animal social network analysis in the age of big data.

In the 4.5 decades since Altmann (1974) published her seminal paper on the methods for the observational study of behaviour, automated detection and analysis of social interaction networks have fundamentally transformed the ways that ecologists study social behaviour. Methodological developments for collecting data remotely on social behaviour involve indirect inference of associations, direct recordings of interactions and machine vision. These recent technological advances are improving the scale and resolution with which we can dissect interactions among animals. They are also revealing new intricacies of animal social interactions at spatial and temporal resolutions as well as in ecological contexts that have been hidden from humans, making the unwatchable seeable. We first outline how these technological applications are permitting researchers to collect exquisitely detailed information with little observer bias. We further recognize new emerging challenges from these new reality-mining approaches. While technological advances in automating data collection and its analysis are moving at an unprecedented rate, we urge ecologists to thoughtfully combine these new tools with classic behavioural and ecological monitoring methods to place our understanding of animal social networks within fundamental biological contexts.

Dictyota cyanoloma (Dictyotales, Phaeophyceae), a Newly Introduced Brown Algal Species in California.

Here, we report for the first time the presence of Dictyota cyanoloma in southern California. Dictyota cyanoloma is conspicuous in harbors and bays by its distinctive bright blue-iridescent margins. This species was originally described from Europe, but subsequent studies have revealed that it represented an introduction from Australia. The current distribution of D. cyanoloma comprises southern Australia and the North East Atlantic, including the Mediterranean Sea and the Macaronesian islands. The presence of D. cyanoloma in southern California is supported by molecular cox1 and psbA gene sequences. A reconstruction of the invasive history based on nine polymorphic microsatellite markers reveals a close affinity of the Californian specimens with European populations. Dictyota cyanoloma in the United States appears to be (so far) restricted to the Californian coast from San Diego Bay in the south to Santa Catalina Island and Long Beach Harbor in the north. A correlative species distribution model suggests gradually declining habitat suitability north of the Southern Californian Bight and high suitability in Baja California, including the Gulf of California. Finally, its widespread abundance in bays and harbors suggests shipping is a likely transport mechanism.

The multinomial index: a robust measure of reproductive skew.

Inequality or skew in reproductive success (RS) is common across many animal species and is of long-standing interest to the study of social evolution. However, the measurement of inequality in RS in natural populations has been challenging because existing quantitative measures are highly sensitive to variation in group/sample size, mean RS, and age-structure. This makes comparisons across multiple groups and/or species vulnerable to statistical artefacts and hinders empirical and theoretical progress. Here, we present a new measure of reproductive skew, the multinomial index, M, that is unaffected by many of the structural biases affecting existing indices. M is analytically related to Nonacs' binomial index, B, and comparably accounts for heterogeneity in age across individuals; in addition, M allows for the possibility of diminishing or even highly nonlinear RS returns to age. Unlike B, however, M is not biased by differences in sample/group size. To demonstrate the value of our index for cross-population comparisons, we conduct a reanalysis of male reproductive skew in 31 primate species. We show that a previously reported negative effect of group size on mating skew was an artefact of structural biases in existing skew measures, which inevitably decline with group size; this bias disappears when using M. Applying phylogenetically controlled, mixed-effects models to the same dataset, we identify key similarities and differences in the inferred within- and between-species predictors of reproductive skew across metrics. Finally, we provide an R package, SkewCalc, to estimate M from empirical data.

Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels.

Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of "stress"), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator-prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey.

Future sea-level rise drives rocky intertidal habitat loss and benthic community change.

The impacts of sea-level rise (SLR) are likely to be the greatest for ecosystems that exist at the land-sea interface, where small changes in sea-level could result in drastic changes in habitat availability. Rocky intertidal ecosystems possess a number of characteristics which make them highly vulnerable to changes in sea-level, yet our understanding of potential community-scale responses to future SLR scenarios is limited. Combining remote-sensing with in-situ large-area imaging, we quantified habitat extent and characterized the biological community at two rocky intertidal study locations in California, USA. We then used a model-based approach to estimate how a range of SLR scenarios would affect total habitat area, areal extent of dominant benthic space occupiers, and numerical abundance of invertebrates. Our results suggest that SLR will reduce total available rocky intertidal habitat area at our study locations, leading to an overall decrease in areal extent of dominant benthic space occupiers, and a reduction in invertebrate abundances. As large-scale environmental changes, such as SLR, accelerate in the next century, more extensive spatially explicit monitoring at ecologically relevant scales will be needed to visualize and quantify their impacts to biological systems.