From the Cover: Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi

In contrast to higher metazoans such as copepods and fish, ctenophores are a basal metazoan lineage possessing a relatively narrow set of sensory-motor capabilities. Yet lobate ctenophores can capture prey at rates comparable to sophisticated predatory copepods and fish, and they are capable of altering the composition of coastal planktonic communities. Here, we demonstrate that the predatory success of the lobate ctenophore Mnemiopsis leidyi lies in its use of cilia to generate a feeding current that continuously entrains large volumes of fluid, yet is virtually undetectable to its prey. This form of stealth predation enables M. leidyi to feed as a generalist predator capturing prey, including microplankton (approximately 50 μm), copepods (approximately 1 mm), and fish larvae (>3 mm). The efficacy and versatility of this stealth feeding mechanism has enabled M. leidyi to be notoriously destructive as a predator and successful as an invasive species.     

From the Cover: Global sea level linked to global temperature

We propose a simple relationship linking global sea-level variations on time scales of decades to centuries to global mean temperature. This relationship is tested on synthetic data from a global climate model for the past millennium and the next century. When applied to observed data of sea level and temperature for 1880–2000, and taking into account known anthropogenic hydrologic contributions to sea level, the correlation is >0.99, explaining 98% of the variance. For future global temperature scenarios of the Intergovernmental Panel on Climate Change''s Fourth Assessment Report, the relationship projects a sea-level rise ranging from 75 to 190 cm for the period 1990–2100.     

From the Cover: Vaccinating captive chimpanzees to save wild chimpanzees

Infectious disease has only recently been recognized as a major threat to the survival of Endangered chimpanzees and Critically Endangered gorillas in the wild. One potentially powerful tool, vaccination, has not been deployed in fighting this disease threat, in good part because of fears about vaccine safety. Here we report on what is, to our knowledge, the first trial in which captive chimpanzees were used to test a vaccine intended for use on wild apes rather than humans. We tested a virus-like particle vaccine against Ebola virus, a leading source of death in wild gorillas and chimpanzees. The vaccine was safe and immunogenic. Captive trials of other vaccines and of methods for vaccine delivery hold great potential as weapons in the fight against wild ape extinction.There is growing recognition that infectious diseases pose a threat to the survival of African apes: a threat on par with poaching and habitat loss. Heightened awareness is due both to better data on rates of disease mortality in gorillas and chimpanzees and to new molecular diagnostic assays that pinpoint the cause of death. These assays tell us that wild apes are regularly infected by a variety of virulent pathogens, including simian immunodeficiency virus (SIV) (1), anthrax (2), and malaria (3). The ethical finger has been pointed squarely and quantitatively at researchers and conservationists with the discovery that “spillover” of human respiratory viruses cause about half of deaths among chimpanzees (4, 5) and gorillas (6) habituated to human approach for research or tourism. Even more widely recognized have been massive Ebola virus (EBOV) outbreaks in gorillas and chimpanzees (7, 8), which have killed roughly one-third of the world gorilla population and led to the 2007 upgrading of western gorillas to Critically Endangered status on the World Conservation Union’s Red List of Threatened Species (9).The ability to accurately diagnose diseases that afflict wild apes has opened the door to an active management response: vaccination (10). The door has been pushed further open by recent advances in vaccinology, including experimental vaccines against several previously unpreventable disease threats to wild apes, new vaccine platforms that reduce or eliminate the risk of infection or vaccine spillover into nontarget species, and new adjuvants that enhance vaccine efficacy (11). Although recognition of the magnitude of the disease threat has made a historically noninterventionist ape conservation community increasingly receptive to vaccination, park managers are still adamant that any experimental vaccine be tested for safety and immunogenicity in captive apes before being used on apes in the wild.Both to address a salient disease threat and to evaluate whether captive testing of vaccines is feasible with the meager budgets typically available to ape conservationists, we decided to test an experimental vaccine against EBOV. During a consultative process lasting several years, vaccine experts, veterinarians, and park managers persistently expressed concerns about the safety of using live (replicating) vaccines on immunologically stressed wild animals. Some cited the case of SIV, which is typically benign in well-cared-for captive chimpanzees but virulent in environmentally challenged wild chimpanzees (1). Therefore, we chose to test a new virus-like particle (VLP) that does not contain an entire replicating virus but only a fragment of viral coat protein. Because they do not cause infection, VLP-based vaccines are particularly safe and several have been recently approved for human use (12). We tested a VLP vaccine based on the virulent Zaire species of EBOV that previously has been given to more than 80 captive macaques without serious health complications (13). In the present study, we did not challenge vaccinated chimpanzees with EBOV. Rather, we simply evaluated whether the vaccine caused health complications that had not been observed in macaques and whether the vaccine induced immune responses comparable to those observed in macaques who survived Ebola challenge. We also tested whether antibodies harvested from vaccinated chimpanzees could protect mice against EBOV challenge.     

Impacts of biological globalization in the Mediterranean: Unveiling the deep history of human-mediated gamebird dispersal

Humans have a long history of moving wildlife that over time has resulted in unprecedented biotic homogenization. It is, as a result, often unclear whether certain taxa are native to a region or naturalized, and how the history of human involvement in species dispersal has shaped present-day biodiversity. Although currently an eastern Palaearctic galliform, the black francolin (Francolinus francolinus) was known to occur in the western Mediterranean from at least the time of Pliny the Elder, if not earlier. During Medieval times and the Renaissance, the black francolin was a courtly gamebird prized not only for its flavor, but also its curative, and even aphrodisiac qualities. There is uncertainty, however, whether this important gamebird was native or introduced to the region and, if the latter, what the source of introduction into the western Mediterranean was. Here we combine historical documentation with a DNA investigation of modern birds and archival (13th–20th century) specimens from across the species’ current and historically documented range. Our study proves the black francolin was nonnative to the western Mediterranean, and we document its introduction from the east via several trade routes, some reaching as far as South Asia. This finding provides insight into the reach and scope of long-distance trade routes that serviced the demand of European aristocracy for exotic species as symbols of wealth and prestige, and helps to demonstrate the lasting impact of human-mediated long-distance species dispersal on current day biodiversity.Human-mediated species translocations have played a central role in shaping global biodiversity for thousands of years (1). The dispersal of early agricultural economies out of the centers of initial domestication more than 10,000 y ago marks an acceleration of human-directed species range expansions involving both domesticates and a wide range of nondomesticated species (2, 3). The maritime and overland trade routes of the third millennium B.C. that linked major urban centers across South and Central Asia, Mesopotamia, the Arabian Peninsula, and North Africa expanded the geographic distribution and diversity of species through long-distance translocations (4). The range and impact of this process continued to increase as transportation technology improved and as demand for both staple and rare exotic species from faraway places grew among ruling elites and rising mercantile classes across the increasingly vast territory connected in these exchanges. The post-A.D. 1000 period in particular saw a surge in species translocations as emerging nation states in Medieval and Renaissance Europe received a staggering diversity of plants and animals through trade routes that linked an expansionist Islamic world with major empires in central Asia and China (1, 5).This process of biological globalization resulted in large-scale reshuffling of both wildlife and domesticates that has had an especially profound and lasting impact on native biotas in the Mediterranean Basin. Species translocations have led to substantial if not complete replacement of insular endemics (6). At the same time, human-mediated species movement and landscape management have helped preserve high biodiversity in present-day anthropogenic, yet threatened Mediterranean environments (7). The impressive pace and extent of present-day wildlife relocations raises concerns about “biotic homogenization,” the loss of biological distinctiveness in regions following replacement of native biotas by locally expanding nonnatives (8). Achieving a comprehensive understanding of the antiquity and impact of humans on Mediterranean biodiversity promises significant insight into ongoing conservation issues, and sheds new light on the role of long-distance trade and exchange in shaping the cultural identities and national destinies of people across the Mediterranean Basin.With their colorful plumage, small size, and relative ease of transport and management, birds are likely candidates for long-distance exchange and were often the animal of choice in European menageries (9, 10). The peacock (Pavo cristatus), for example, is thought to have been imported from Asia to Greece during the time of Alexander the Great, and perhaps even earlier (11). In his De Arte Venandi cum Avibus, Frederick II referred to the importation of the Guinea fowl (Numida meleagris) from the Levant to Sicily (12). Chronicles of European adventurers in Asia, such as Marco Polo (13), often contained references to gamebirds. Since the first centuries B.C., travelers along the Silk Road are known to have carried and bred chukar partridges (Alectoris chukar) as a source of food on the way to Europe (14).Another species of gamebird that may well have been included in these exchanges is the black francolin (Francolinus francolinus, Phasianidae). No longer found in the western Mediterranean, the black francolin is known from textual and iconographic sources as a species that figured prominently in courtly life in Medieval and Renaissance Europe (5, 15). Here we combine historical documentation with the genetic study of modern, archaeozoological, and archival collections of this bird to assess whether the black francolin represents an example of the extirpation of a native or an introduced species in the western Mediterranean, thus exploring what this species can tell us about the nature of human-mediated dispersals in the region.     

From the Cover: Threat of plastic pollution to seabirds is global,pervasive, and increasing

Plastic pollution in the ocean is a global concern; concentrations reach 580,000 pieces per km² and production is increasing exponentially. Although a large number of empirical studies provide emerging evidence of impacts to wildlife, there has been little systematic assessment of risk. We performed a spatial risk analysis using predicted debris distributions and ranges for 186 seabird species to model debris exposure. We adjusted the model using published data on plastic ingestion by seabirds. Eighty of 135 (59%) species with studies reported in the literature between 1962 and 2012 had ingested plastic, and, within those studies, on average 29% of individuals had plastic in their gut. Standardizing the data for time and species, we estimate the ingestion rate would reach 90% of individuals if these studies were conducted today. Using these results from the literature, we tuned our risk model and were able to capture 71% of the variation in plastic ingestion based on a model including exposure, time, study method, and body size. We used this tuned model to predict risk across seabird species at the global scale. The highest area of expected impact occurs at the Southern Ocean boundary in the Tasman Sea between Australia and New Zealand, which contrasts with previous work identifying this area as having low anthropogenic pressures and concentrations of marine debris. We predict that plastics ingestion is increasing in seabirds, that it will reach 99% of all species by 2050, and that effective waste management can reduce this threat.Introduction of plastic waste into the marine environment is a global concern. Plastic production is rapidly rising, with a doubling of production every 11 y since commercial production began in the 1950s (1). This growth in production has been accompanied by a corresponding increase in the concentration of plastics in the marine environment although it has been suggested that marine organisms may be a major sink reducing this increase (2–4). The durability of plastic implies that it is retained for years to centuries, in some cases failing to degrade at all if it is not exposed to bacterial activity or UV radiation (5).Plastic fragments can be found throughout the world’s oceans, with observed concentrations up to 580,000 plastic pieces per square kilometer (2, 3, 6). Modeling studies, validated by global sampling efforts, demonstrate that plastics are ubiquitous, with high concentrations in all five subtropical convergence zones and along the coastal margins near human population centers (3, 6, 7).In addition to the evidence of its prevalence, there is emerging evidence of the threats plastics pose to wildlife, and indirectly to human health. Plastic waste affects wildlife via two means: entanglement and ingestion (8). A recent review for the United Nations Convention on Biological Diversity documented over 600 species, ranging from microorganisms to whales, affected by marine plastic waste, largely through ingestion (9). Ingestion is known to have many effects, ranging from physical gut blockage (10) to organ damage from leaching toxins (11). Recent experimental studies have also demonstrated transmission and toxicological effects of plastics, or adsorbed chemicals, at environmentally relevant concentrations in higher vertebrates (11–13).The effect of plastic ingestion on seabirds in particular has been of concern. This concern is due to the frequency with which seabirds ingest plastic (12) and because of emerging evidence of both impacts on body condition and transmission of toxic chemicals, which could result in changes in mortality or reproduction (13–16). Understanding the contribution of this threat is particularly pressing because half of all seabird species are in decline, a higher fraction than other comparable taxa (17). Despite a recent extensive review of the threats to seabirds by a globally recognized authority (17), however, pollution has been identified only in a coastal context, and there is little mention of the impact of plastic ingestion, particularly on the high seas where the most threatened seabirds forage (17).We predict the extent of plastics exposure for 186 pelagic seabird species worldwide, excluding coastal taxa such as shorebirds, sea ducks, and gulls and species for which distribution data were not available (SI Appendix, Table S1). We compare our predictions with diet studies published over the last 40 y and incorporate additional factors such as foraging strategy, body size, and sampling method that may affect the relationship between exposure and ingestion. Based on this adjusted model of risk, we map the global distribution of plastic ingestion risk for seabirds and highlight global areas of concern.     

From the Cover: Ecosystem responses in the southern Caribbean Sea to global climate change

Over the last few decades, rising greenhouse gas emissions have promoted poleward expansion of the large-scale atmospheric Hadley circulation that dominates the Tropics, thereby affecting behavior of the Intertropical Convergence Zone (ITCZ) and North Atlantic Oscillation (NAO). Expression of these changes in tropical marine ecosystems is poorly understood because of sparse observational datasets. We link contemporary ecological changes in the southern Caribbean Sea to global climate change indices. Monthly observations from the CARIACO Ocean Time-Series between 1996 and 2010 document significant decadal scale trends, including a net sea surface temperature (SST) rise of ∼1.0 ± 0.14 °C (±SE), intensified stratification, reduced delivery of upwelled nutrients to surface waters, and diminished phytoplankton bloom intensities evident as overall declines in chlorophyll a concentrations (ΔChla = −2.8 ± 0.5%⋅y⁻¹) and net primary production (ΔNPP = −1.5 ± 0.3%⋅y⁻¹). Additionally, phytoplankton taxon dominance shifted from diatoms, dinoflagellates, and coccolithophorids to smaller taxa after 2004, whereas mesozooplankton biomass increased and commercial landings of planktivorous sardines collapsed. Collectively, our results reveal an ecological state change in this planktonic system. The weakening trend in Trade Winds (−1.9 ± 0.3%⋅y⁻¹) and dependent local variables are largely explained by trends in two climatic indices, namely the northward migration of the Azores High pressure center (descending branch of Hadley cell) by 1.12 ± 0.42°N latitude and the northeasterly progression of the ITCZ Atlantic centroid (ascending branch of Hadley cell), the March position of which shifted by about 800 km between 1996 and 2009.     

From the Cover: Ant colonies outperform individuals when a sensory discrimination task is difficult but not when it is easy

“Collective intelligence” and “wisdom of crowds” refer to situations in which groups achieve more accurate perception and better decisions than solitary agents. Whether groups outperform individuals should depend on the kind of task and its difficulty, but the nature of this relationship remains unknown. Here we show that colonies of Temnothorax ants outperform individuals for a difficult perception task but that individuals do better than groups when the task is easy. Subjects were required to choose the better of two nest sites as the quality difference was varied. For small differences, colonies were more likely than isolated ants to choose the better site, but this relationship was reversed for large differences. We explain these results using a mathematical model, which shows that positive feedback between group members effectively integrates information and sharpens the discrimination of fine differences. When the task is easier the same positive feedback can lock the colony into a suboptimal choice. These results suggest the conditions under which crowds do or do not become wise.     

From the Cover: Father's brain is sensitive to childcare experiences

Although contemporary socio-cultural changes dramatically increased fathers'' involvement in childrearing, little is known about the brain basis of human fatherhood, its comparability with the maternal brain, and its sensitivity to caregiving experiences. We measured parental brain response to infant stimuli using functional MRI, oxytocin, and parenting behavior in three groups of parents (n = 89) raising their firstborn infant: heterosexual primary-caregiving mothers (PC-Mothers), heterosexual secondary-caregiving fathers (SC-Fathers), and primary-caregiving homosexual fathers (PC-Fathers) rearing infants without maternal involvement. Results revealed that parenting implemented a global “parental caregiving” neural network, mainly consistent across parents, which integrated functioning of two systems: the emotional processing network including subcortical and paralimbic structures associated with vigilance, salience, reward, and motivation, and mentalizing network involving frontopolar-medial-prefrontal and temporo-parietal circuits implicated in social understanding and cognitive empathy. These networks work in concert to imbue infant care with emotional salience, attune with the infant state, and plan adequate parenting. PC-Mothers showed greater activation in emotion processing structures, correlated with oxytocin and parent-infant synchrony, whereas SC-Fathers displayed greater activation in cortical circuits, associated with oxytocin and parenting. PC-Fathers exhibited high amygdala activation similar to PC-Mothers, alongside high activation of superior temporal sulcus (STS) comparable to SC-Fathers, and functional connectivity between amygdala and STS. Among all fathers, time spent in direct childcare was linked with the degree of amygdala-STS connectivity. Findings underscore the common neural basis of maternal and paternal care, chart brain–hormone–behavior pathways that support parenthood, and specify mechanisms of brain malleability with caregiving experiences in human fathers.Throughout human history and across cultures, women have typically assumed primary caregiving responsibility for infants (1, 2). Although humans are among the few mammalian species where some male parental caregiving is relatively common, father involvement varies considerably within and across cultures, adapting to ecological conditions (1, 3). Involved fathering has been linked with children''s long-term physiological and social development and with increases in mothers'' caregiving-related hormones such as oxytocin and prolactin (3–6). In addition, animal studies demonstrated structural brain alterations in caregiving fathers (7, 8). It has been suggested that, although maternal caregiving is triggered by neurobiological processes related to pregnancy and labor, the human father''s brain, similar to other biparental mammals, adapts to the parental role through active involvement in childcare (1–3). Despite growing childcare involvement of fathers (3, 5, 6), mechanisms for human fathers'' brain adaptation to caregiving experiences remain largely unknown, and no study to our knowledge has examined the brain basis of human fatherhood when fathers assume primary responsibility for infant care.For social species with lengthy periods of dependence, parental caregiving is key to survival and relies on brain structures that maximize survival (2, 9). Animal studies have demonstrated that mammalian mothering is supported by evolutionarily ancient structures implicated in emotional processing, vigilance, motivation, and reward, which are rich in oxytocin receptors, including the amygdala, hypothalamus, nucleus accumbens, and ventral tegmental area (VTA), and that these regions are sensitive to caregiving behavior (9, 10). Imaging studies of human mothers found activation in similar areas, combined with paralimbic insula-cingulate structures that imbue infants with affective salience, ground experience in the present moment and enable maternal simulation of infant states (11–13). These structures implicate a phylogenetically ancient network of emotional processing that rapidly detects motivationally salient and survival-related cues (14) and enables parents to automatically identify and immediately respond to infant distress, thereby maximizing survival. In humans, this emotional processing network is complemented by a cortical mentalizing network of frontopolar-medial-prefrontal-temporo-parietal structures involved in social understanding, theory of mind, and cognitive empathy, including the medial prefrontal cortex (mPFC), frontopolar cortex, superior temporal sulcus (STS), and temporal poles (15). The mentalizing network plays an important role in individuals'' ability to infer mental states from behavior, is already activated during the parents'' first weeks of parenting, and enables parents to cognitively represent infant states, predict infant needs, and plan future caregiving (11–13).The few studies examining the human father''s brain showed activation in similar areas, including the STS, lateral and medial frontal regions, VTA, inferior frontal gyrus (IFG), and orbitofrontal cortex (OFC) (16, 17). Only one study compared maternal and paternal brain response to infant cues, reporting mothers'' greater amygdala activation, fathers'' greater superior-temporal and medial-frontal activation, and maternal and paternal oxytocin''s different associations with amygdala vs. cortical activation (18). Oxytocin, a nine-amino acid neuropeptide that underpins the formation of affiliative bonds (19), supports the development of human parental caregiving (20). Research has shown that maternal and paternal oxytocin levels are associated with parent–infant synchrony, which is the parent''s careful adaptation of caregiving behavior to infant''s social signals (21). However, although oxytocin levels are similar in mothers and fathers, oxytocin is differentially linked with the parent-specific repertoire, for instance, with affectionate contact in mothers and stimulatory play in fathers (5, 20).Ethological perspectives emphasize the importance of studying the neurobiology of parenting in its natural habitat and of using a behavior-based approach to test parents'' brain adaptation to ecological pressures (22). Consistent with findings in other mammals (10), studies on brain–behavior associations in human mothers describe links between mother–infant synchrony and brain activation in the mother''s subcortical regions, including the amygdala, nucleus accumebens, and hippocampus (11, 13). In contrast, the one study testing human fathers'' brain–behavior associations showed correlations with cortical activation (17). Overall, these findings suggest that distinct brain–hormone–behavior pathways may underpin maternal and paternal care; therefore, oxytocin and parenting behavior may be associated with the emotional processing network in mothers but with the socio-cognitive circuit in fathers. Furthermore, animal studies indicate that active caregiving in biparental fathers leads to greater integration of multiple brain networks involved in nurturance, learning, and motivation (7). Hence, active involvement in caregiving may possibly facilitate integration of both parenting-related networks in human fathers, particularly among those who undertake the primary caregiver role.The present study sought to examine the brain basis of human fatherhood by using a “natural experiment,” afforded for the first time in human history, to our knowledge, by contemporary socio-cultural changes. Throughout history, infants without mothers were cared for by other women (2). Current social changes enable the formation of two-father families raising children with no maternal involvement since birth (3). Such a context provides a unique setting to assess changes in the paternal brain on assuming the traditionally maternal role. Moreover, understanding mechanisms of brain adaptation to caregiving experiences in primary-caregiving fathers may shed further light on processes that refine all fathers'' responses to childcare activities.We visited the homes of two-parent families rearing their firstborn child: heterosexual mother-father couples comprising primary-caregiving mothers (PC-Mothers) and secondary-caregiving fathers (SC-Fathers) and homosexual couples comprising two primary-caregiving fathers (PC-Fathers) (SI Materials and Methods). We videotaped parent–infant interaction in the natural habitat, measured parental oxytocin, and used the videotaped parent–child interactions as stimuli for functional MRI (fMRI) to test parental brain response to infant-related cues. Five hypotheses were proposed. First, we expected activation in both subcortical areas involved in vigilance and reward and cortical circuits implicated in social understanding in all parents raising a young infant. Second, we expected greater subcortical activation in mothers, particularly in the amygdala, which has been repeatedly linked with mammalian mothering (23, 24), and greater activation in cortical socio-cognitive circuits in fathers. Third, the brain–hormone–behavior constellation underpinning maternal care was expected to center around the emotional-processing network, whereas the brain–hormone–behavior links in fathers were expected to coalesce with the socio-cognitive network. Fourth, consistent with the context-specific evolution of human fathering (1), we expected greater variability in fathers'' brain response as mediated by actual caregiving experiences. Such variability would be particularly noted among the primary-caregiving fathers raising infants without mothers and may involve functional integration of the subcortical and cortical networks subserving parenting. Finally, we expected that the pathways leading from the parent''s primary caregiving role to greater parent–infant synchrony would be mediated by parental brain activation and oxytocin levels.     

From the Cover: Warming-induced reductions in body size are greater in aquatic than terrestrial species

Most ectothermic organisms mature at smaller body sizes when reared in warmer conditions. This phenotypically plastic response, known as the “temperature-size rule” (TSR), is one of the most taxonomically widespread patterns in biology. However, the TSR remains a longstanding life-history puzzle for which no dominant driver has been found. We propose that oxygen supply plays a central role in explaining the magnitude of ectothermic temperature-size responses. Given the much lower oxygen availability and greater effort required to increase uptake in water vs. air, we predict that the TSR in aquatic organisms, especially larger species with lower surface area–body mass ratios, will be stronger than in terrestrial organisms. We performed a meta-analysis of 1,890 body mass responses to temperature in controlled experiments on 169 terrestrial, freshwater, and marine species. This reveals that the strength of the temperature-size response is greater in aquatic than terrestrial species. In animal species of ∼100 mg dry mass, the temperature-size response of aquatic organisms is 10 times greater than in terrestrial organisms (−5.0% °C⁻¹ vs. −0.5% °C⁻¹). Moreover, although the size response of small (<0.1 mg dry mass) aquatic and terrestrial species is similar, increases in species size cause the response to become increasingly negative in aquatic species, as predicted, but on average less negative in terrestrial species. These results support oxygen as a major driver of temperature-size responses in aquatic organisms. Further, the environment-dependent differences parallel latitudinal body size clines, and will influence predicted impacts of climate warming on food production, community structure, and food-web dynamics.     

From the Cover: Sperm competition drives the evolution of suicidal reproduction in mammals

Suicidal reproduction (semelparity) has evolved in only four genera of mammals. In these insectivorous marsupials, all males die after mating, when failure of the corticosteroid feedback mechanism elevates stress hormone levels during the mating season and causes lethal immune system collapse (die-off). We quantitatively test and resolve the evolutionary causes of this surprising and extreme life history strategy. We show that as marsupial predators in Australia, South America, and Papua New Guinea diversified into higher latitudes, seasonal predictability in abundance of their arthropod prey increased in multiple habitats. More-predictable prey peaks were associated with shorter annual breeding seasons, consistent with the suggestion that females accrue fitness benefits by timing peak energy demands of reproduction to coincide with maximum food abundance. We demonstrate that short mating seasons intensified reproductive competition between males, increasing male energy investment in copulations and reducing male postmating survival. However, predictability of annual prey cycles alone does not explain suicidal reproduction, because unlike insect abundance, peak ovulation dates in semelparous species are often synchronized to the day among years, triggered by a species-specific rate of change of photoperiod. Among species with low postmating male survival, we show that those with suicidal reproduction have shorter mating seasons and larger testes relative to body size. This indicates that lethal effort is adaptive in males because females escalate sperm competition by further shortening and synchronizing the annual mating period and mating promiscuously. We conclude that precopulatory sexual selection by females favored the evolution of suicidal reproduction in mammals.Semelparity in both sexes occurs in many plants and invertebrates and in some fish. In these taxa, conditions that produce low adult survival between breeding bouts, but high juvenile survival to reproductive maturity select for semelparity, provided that high enough fecundity can evolve to compensate for reduced lifespan (1). Obligate maternal care means that mammals are constrained to a relatively low maximum reproductive rate. This should generally preclude the evolution of semelparity in mammals (2, 3). However, the maximum reproductive rate of males is much less constrained than that of females. In species with large litters such as insectivorous marsupials (4), males with low or zero postreproductive survivorship can potentially compensate by siring many offspring among multiple females in their first reproductive bout (5), so that divergence in life history strategies between the sexes can be favored by a mechanism of sexual selection.The adaptiveness of male die-off in marsupials has been debated without resolution for three decades (2–4, 6, 7). We propose that to understand why male semelparity has evolved in mammals, we must answer two separate questions: (i) why has evolution favored males that compete fatally in these marsupial species but not in other mammals and (ii) what mechanism of sexual competition facilitates this lethal effort only in males? Five potential reasons why insectivorous marsupials are prone to evolve lethal male competition have been proposed: (i) females are constrained to leave a 12-mo gap between litters because a peak in arthropod prey occurs annually in their seasonally predictable forest habitats, weaning success depends on this spike in food, and females have a long lactation time relative to body size (a marsupial trait). Environmental causes of mortality (rife in small mammals) mean that adult males of these species seldom survive for a year after maturity, and lethal competition in the first season is adaptive because males are unlikely to breed again (Braithwaite and Lee’s hypothesis) (2); (ii) phylogenetic predisposition (an unknown developmental constraint locking modern taxa into nonadaptive male die-off) (7); (iii) accumulation of deleterious mutations after breeding (6); (iv) poor survival of breeding females resulting in male bet-hedging (spreading the risk of offspring death among many mates) and therefore extreme male promiscuity (8); or (v) altruism (males sacrificing themselves to avoid competing with the next generation for limited food) (2, 3, 9). Braithwaite and Lee’s adaptive framework, based on the exceptional lactation time of dasyurids, is the only one of these suggestions to address why die-off has not evolved more widely in small mammals. This hypothesis was based on the traits of a small number of forest-dwelling species (2) and has been criticized because prey cycles appear to be less synchronized between years than the reproductive cycles of semelparous mammals (9). However, habitat and latitudinal effects on seasonality of insect abundance have not been quantified at continental scales, and dasyurid species with die-off occur in diverse, nonforest habitats (7, 10).Alternative explanations have proposed that peculiarities of the mating system lead to extreme sexual selection and that this is sufficient reason for the evolution of mammalian semelparity. Most forms of sexual selection have been proposed as the mechanism of competition in dasyurids with die-off: male contests that favor young males (2, 6), precopulatory female preference for young males (6), female choice in the form of lekking (selection for male endurance through metabolism of muscle) (11), and sperm competition (4). Of these, only sperm competition has empirical support (5). Precopulatory fighting is infrequent and minor in male semelparous marsupials (12). In the semelparous genus Antechinus, mating females reject subordinate males but are indifferent to male body size and mate promiscuously with most available males (12–14), suggesting that even if there was variation in male age, youthfulness would not motivate mate choice. Lekking occurs in some populations of only one species, if at all (11, 15). In contrast, there is rigorous evidence of the importance of sperm competition in semelparous species (4, 5, 14). In the brown antechinus Antechinus stuartii, sperm competition enables females to improve offspring survival and lifetime fitness by mating promiscuously (5). Here we use phylogenetic comparative methods to test the predictions of these competing hypotheses to explain why, among mammals, male semelparity has evolved repeatedly (10) and only in insectivorous marsupials, and to determine whether die-off is likely to have evolved through a mechanism of sperm competition.Life history variation has previously been treated as discrete life history categories in evolutionary investigations of dasyurid marsupials (10), but demographic studies of insectivorous marsupials in Australia, South America, and Papua New Guinea reveal a continuum (7, 16–18). The most extreme strategy (die-off) involves a set of peculiar physiological events that culminate in synchronous death: males irreversibly shut down sperm production a month before mating so that future reproduction is impossible. Fertilization depends on sperm stored in the epididymis, and males continuously lose sperm in the urine (spermatorrhea) so that the window of opportunity to mate before permanent infertility is very brief. Synchronous immune system collapse and death quickly follow. Die-off occurs in all males of the Australian genera Antechinus (12 species), Phascogale (3 species), and Dasykaluta (a monospecific genus) (10). One species in each of two other genera in Australia is “facultatively semelparous”; only some populations have complete male mortality. Die-off symptoms of immune collapse and abrupt, synchronous death occur in semelparous populations of the dibbler Parantechinus apicalis, but not the northern quoll Dasyurus hallucatus (7, 16). Some Brazilian, Argentinean, and Australian small marsupials also have negligible survival after breeding at some sites (17–19) (Table S1). This phenomenon in didelphid mouse opossums occurs in both sexes and has been termed “partial semelparity” (18). Most insectivorous dasyurids and didelphids are iteroparous (repeat or continuous breeding, at the other extreme of the scale), including all known species in Papua New Guinea (Table S1).     

From the Cover: No barrier to emergence of bathyal king crabs on the Antarctic shelf

Cold-water conditions have excluded durophagous (skeleton-breaking) predators from the Antarctic seafloor for millions of years. Rapidly warming seas off the western Antarctic Peninsula could now facilitate their return to the continental shelf, with profound consequences for the endemic fauna. Among the likely first arrivals are king crabs (Lithodidae), which were discovered recently on the adjacent continental slope. During the austral summer of 2010‒2011, we used underwater imagery to survey a slope-dwelling population of the lithodid Paralomis birsteini off Marguerite Bay, western Antarctic Peninsula for environmental or trophic impediments to shoreward expansion. The population density averaged ∼4.5 individuals × 1,000 m⁻² within a depth range of 1,100‒1,500 m (overall observed depth range 841–2,266 m). Images of juveniles, discarded molts, and precopulatory behavior, as well as gravid females in a trapping study, suggested a reproductively viable population on the slope. At the time of the survey, there was no thermal barrier to prevent the lithodids from expanding upward and emerging on the outer shelf (400- to 550-m depth); however, near-surface temperatures remained too cold for them to survive in inner-shelf and coastal environments (<200 m). Ambient salinity, composition of the substrate, and the depth distribution of potential predators likewise indicated no barriers to expansion of lithodids onto the outer shelf. Primary food resources for lithodids—echinoderms and mollusks—were abundant on the upper slope (550–800 m) and outer shelf. As sea temperatures continue to rise, lithodids will likely play an increasingly important role in the trophic structure of subtidal communities closer to shore.Climate change is substantially altering the composition and function of marine and terrestrial ecosystems (1–5). Polar-marine communities are particularly vulnerable to climate change, which at this point is the principal threat to their persistence (6). The near-absence of seasonal variation in sea temperature has led to the dominance of cold-stenothermal faunas, which have limited capacities to acclimate to rapid warming (7–9). At polar latitudes, cold-stenothermy and increasing physical disturbance will shift and reduce the geographic ranges of high-latitude marine taxa, increasing their risk of extinction (10–12).Globally accelerating temperature increases are already having profound effects on polar ecosystems. Those impacts extend beyond autecological responses to include top-down and bottom-up effects on marine food webs (13–17). The endemic faunas of the Antarctic continental shelf are now at risk of invasion by durophagous (skeleton-breaking) predators (18), a functional group that (based on the limited paleontological and genetic data available) may not have been ecologically significant there for as long as tens of millions of years (19–22).“Reptant” (bottom-walking) decapod crustaceans, teleostean fishes, and neoselachian sharks and rays are key predators in shallow-subtidal communities worldwide but are at present physiologically excluded from nearshore environments in Antarctica (19). Reptant decapods, which include brachyuran crabs, anomuran crabs, and lobsters, typically cannot survive in waters colder than 1 °C, although adult stages of some of the more cold-tolerant taxa can survive down to 0.4 °C (23, 24). Their limited capacity to down-regulate naturally occurring magnesium ions in their hemolymph leads to paralysis and death at lower temperatures (25).In the absence of durophagous predators, benthic faunas of the Antarctic shelf are lightly skeletonized and dominated by epifaunal suspension-feeders. The top predators are slow-moving invertebrates, such as seastars and nemertean worms. In some respects, therefore, Antarctic-shelf communities are reminiscent of low-predation communities living in contemporary deep-sea habitats, as well as communities from shallow, Paleozoic environments (26–30). Now, as sea temperatures rise, the reintroduction of durophagous predators could radically alter the composition and trophic structure of the shelf-benthos in Antarctica (19, 20, 31).Lithodid crabs (Crustacea: Decapoda: Anomura) are common in the deep sea globally, as well as in shallow waters at subpolar latitudes (32). Also known as king crabs or stone crabs, lithodids feed on a broad range of skeletonized invertebrates, but especially on echinoderms and mollusks (33–36). They are well known from deep-sea habitats of the Southern Ocean and are common in shallow, subantarctic waters (23, 37). Two species, Paralomis birsteini and Neolithodes capensis, were first observed on the continental slope adjacent to the western Antarctic Peninsula (WAP) in 2003, and these sightings were confirmed a few years later (38, 39). P. birsteini appears to be widespread in the Bellingshausen Sea and is the most commonly recorded lithodid species on the slope south of 60° S (18, 23, 37).Phylogenetic evidence suggests multiple radiations of deep-sea lineages of lithodids into the Southern Ocean (32). How long they have been present on the Antarctic continental slope remains controversial (37), and there is virtually no information available on the status and viability of their populations. At some point, adult or larval Neolithodes yaldwyni must have moved over the shelf-break at ∼500 m to establish a reproductively viable population at slope-depths >850 m in Palmer Deep, a trough carved into the shelf of the WAP by glacial movement (40). Lithodids are, however, currently excluded from nearshore, shallow-shelf environments along the WAP, because there the shallowest waters over the shelf are colder than the slope-waters (41–44). Although they are the most cold-tolerant of the reptant decapods, lithodids are still physiologically incapable of surviving below ∼0.4 °C (18, 24, 32).The bathymetric distribution of lithodids could change in the next few decades, however. Summertime sea-surface temperatures and temperatures of the Antarctic Shelf Bottom Waters off the WAP have risen by nearly 1.5 °C over the past 50 y, approximately double the globally averaged rate (45). Rising temperatures in shallow waters off the WAP will likely remove the thermal barrier to lithodids (and other reptant decapods) within the next several decades, facilitating their expansion into shallow, nearshore habitats (18). Judging from the strong, predatory role of invasive lithodids in Arctic food webs (33, 46), as well as the predatory impacts of the brachyuran snow crab Chionoecetes opilio in the Arctic (47), the effects of predation by lithodids could be severe in shallow-benthic communities in Antarctica (19, 40).A recent critique (37) argued correctly that records of lithodids from the Antarctic slope and Palmer Deep do not by themselves constitute evidence that they could or will expand onto the shelf. Such a prediction could, however, be tested with time-series data on the population status and ecology of bathyal lithodids in Antarctica (37). Here, we take a significant first step in addressing that challenge. We describe a dense, reproductively viable population of P. birsteini living on the continental slope off the WAP. We show that there are no apparent physical or ecological barriers to impede the population from immediately expanding upward onto the deeper parts of the adjacent continental shelf, with potentially catastrophic impacts on the existing benthic fauna.     

From the Cover: Large contribution of biomass burning emissions to ozone throughout the global remote troposphere

Ozone is the third most important anthropogenic greenhouse gas after carbon dioxide and methane but has a larger uncertainty in its radiative forcing, in part because of uncertainty in the source characteristics of ozone precursors, nitrogen oxides, and volatile organic carbon that directly affect ozone formation chemistry. Tropospheric ozone also negatively affects human and ecosystem health. Biomass burning (BB) and urban emissions are significant but uncertain sources of ozone precursors. Here, we report global-scale, in situ airborne measurements of ozone and precursor source tracers from the NASA Atmospheric Tomography mission. Measurements from the remote troposphere showed that tropospheric ozone is regularly enhanced above background in polluted air masses in all regions of the globe. Ozone enhancements in air with high BB and urban emission tracers (2.1 to 23.8 ppbv [parts per billion by volume]) were generally similar to those in BB-influenced air (2.2 to 21.0 ppbv) but larger than those in urban-influenced air (−7.7 to 6.9 ppbv). Ozone attributed to BB was 2 to 10 times higher than that from urban sources in the Southern Hemisphere and the tropical Atlantic and roughly equal to that from urban sources in the Northern Hemisphere and the tropical Pacific. Three independent global chemical transport models systematically underpredict the observed influence of BB on tropospheric ozone. Potential reasons include uncertainties in modeled BB injection heights and emission inventories, export efficiency of BB emissions to the free troposphere, and chemical mechanisms of ozone production in smoke. Accurately accounting for intermittent but large and widespread BB emissions is required to understand the global tropospheric ozone burden.

Tropospheric ozone (O₃) has been the focus of decades of scientific research due to its central role in atmospheric chemistry (1), its adverse impact on human and ecosystem health (2, 3), and its role as a climate forcer (4, 5). Despite this focus, there remains considerable uncertainty in tropospheric O₃ production pathways, precursor sources, and long-term trends. Sources of tropospheric O₃ include downward transport from the stratosphere and photochemical production from a complex set of coupled reactions between nitrogen oxides (NO_x) and volatile organic compounds (VOCs), each of which is in turn emitted from both anthropogenic and natural sources (1, 6). The contribution of fossil fuel combustion to tropospheric O₃ has recently declined in the United States and in Europe, proportionally increasing the contribution from natural sources (7–10). However, the spatial distribution of anthropogenic O₃ precursor emissions have shifted to lower latitudes (11, 12), where they are still increasing (13). Additionally, globally averaged tropospheric O₃ has increased over the past five decades (14, 15). Understanding the sources of tropospheric O₃ is thus essential to explain this trend and to inform the development of effective mitigation strategies from regional to hemispheric scales.Biomass burning (BB) is an important source of O₃ precursors (16–19). A recent study based on observed O₃ to carbon monoxide (CO) enhancements in smoke plumes attributed 3.5% of the global tropospheric chemical O₃ production to BB emissions (19). Other studies have accounted for the numerous production and destruction pathways of O₃ in the troposphere using global chemical transport models (CTMs) to estimate the global budget of O₃ (20, 21). However, few studies separately quantify the contributions of fossil fuel combustion and BB emissions to global tropospheric O₃ (22). Global inventories attribute five times more NO_x (23, 24) but roughly equal VOC emissions (17, 25) to fossil fuel combustion (hereafter referred to as urban sources) compared with BB. However, precursor emissions do not necessarily determine tropospheric O₃ production close to the sources because of the nonlinearity of O₃ formation chemistry (26, 27). Additionally, global CTMs do not always agree on the tropospheric O₃ burden, suggesting possible deficiencies with emission inventories of O₃ precursors and/or an incomplete representation of O₃ chemistry (21, 28–30), although a recent model intercomparison study showed that the model ensemble reproduced well the salient spatial, seasonal, and decadal variability and trends of tropospheric O₃ (31).Large-scale in situ observational constraints commensurate with the grid resolution of current global CTMs are rare. Instead, modeling studies often rely on ozonesonde-derived climatologies and satellite-based remote sensing observations to constrain tropospheric O₃ distributions and precursor sources (20, 32, 33). The recent NASA Atmospheric Tomography (ATom) mission provides global-scale and seasonally resolved in situ measurements of O₃ and CO and a comprehensive suite of trace gases and aerosol parameters, including tracers of BB and urban emissions (34). ATom sampled the remote troposphere from the Arctic to the Antarctic over the Pacific and Atlantic Oceans using repeated vertical profiles from ∼0.2 to ∼13 km in altitude during four seasonal deployments between 2016 and 2018 (Fig. 1). Recently, the ubiquitous presence of dilute BB smoke in the remote troposphere and its significant contribution to aerosol mass loading was established using ATom observations (35). Here, we use ATom measurements to quantify the individual contributions of urban and BB emissions to O₃ in the remote global troposphere using tracers specific to each source. We compare this analysis with simulations from three global CTMs that alternatively set BB and urban emissions to zero to evaluate their impact on modeled tropospheric O₃.Open in a separate windowFig. 1.Map of ATom flight tracks from the four seasonal global circuits colored by tropospheric O₃ mixing ratios. Note that the color scale terminates at 70 ppbv of O₃, and higher values are shown in red. Measurements with a strong stratospheric influence were parsed out as indicated in Materials and Methods.     

From the Cover: Communication hubs of an asocial cat are the source of a human–carnivore conflict and key to its solution

Human–wildlife conflicts occur worldwide. Although many nonlethal mitigation solutions are available, they rarely use the behavioral ecology of the conflict species to derive effective and long-lasting solutions. Here, we use a long-term study with 106 GPS-collared free-ranging cheetahs (Acinonyx jubatus) to demonstrate how new insights into the socio-spatial organization of this species provide the key for such a solution. GPS-collared territory holders marked and defended communication hubs (CHs) in the core area of their territories. The CHs/territories were distributed in a regular pattern across the landscape such that they were not contiguous with each other but separated by a surrounding matrix. They were kept in this way by successive territory holders, thus maintaining this overdispersed distribution. The CHs were also visited by nonterritorial cheetah males and females for information exchange, thus forming hotspots of cheetah activity and presence. We hypothesized that the CHs pose an increased predation risk to young calves for cattle farmers in Namibia. In an experimental approach, farmers shifted cattle herds away from the CHs during the calving season. This drastically reduced their calf losses by cheetahs because cheetahs did not follow the herds but instead preyed on naturally occurring local wildlife prey in the CHs. This implies that in the cheetah system, there are “problem areas,” the CHs, rather than “problem individuals.” The incorporation of the behavioral ecology of conflict species opens promising areas to search for solutions in other conflict species with nonhomogenous space use.

Human–wildlife conflicts (HWC) are a global challenge and likely to increase in the future (1). Carnivore species are often involved in such conflicts because they prey on, or are feared to prey on, livestock. With the increasing human population and concurrent growth in livestock numbers, contact between carnivores, people, and their livestock will increase, and so will predation on livestock (2). Today, retaliatory killing of carnivores is still a common response to the perceived or actual threat of carnivore predation on livestock and can be a major threat to endangered carnivores (3). Nonlethal mitigation tools are therefore essential and also used widely, such as predator-proof bomas, kraals or electric fences (e.g., against lions (Panthera leo) (4)), livestock guarding dogs (e.g., against cheetahs (Acinonyx jubatus) (5)), light or sound deterrents (e.g., against cougars (Puma concolor) (6)), compensation payments (e.g., African wild dogs (Lycaon pictus) (7)), beef from certified carnivore-friendly farmers (e.g., gray wolves (Canis lupus) (8)), translocations (e.g., cheetahs (9)), and bylaw changes (e.g., lions (10)). These methods were successful in some cases; in others, they failed (2, 7–11).The rapidly developing field of movement ecology with its substantial improvements of tracking devices and analysis tools has unlocked new approaches in conservation science (12). In the context of HWC, collaring and tracking of conflict species already provided successful applications in geofencing and early warning systems (13). Their warning signals facilitate quick responses of livestock herders or owners to an approaching carnivore provided they are on continuous standby (13). Here, we present a method that takes advantage of this rapidly developing field of movement ecology and provides an effective and long-lasting solution to mitigate a long-term conflict between livestock farmers and a threatened carnivore, the cheetah.Conflicts between farmers and cheetahs are well documented and are a major threat to the global cheetah population, as most cheetahs occur on farmland outside protected areas (14). In this study, we focused on cheetahs on Namibian farmland, where cheetahs are the key wild carnivore to kill cattle calves because lions and spotted hyenas (Crocuta crocuta) were extirpated decades ago (15). Building on previous work, we analyzed the space use and socio-spatial ecology of Namibian farmland cheetahs in detail, developed a modification of livestock management, and experimentally tested its efficacy in substantially reducing livestock losses. This led to the development of recommendations for new management practices for cattle farmers that minimize calf losses.Cheetah males begin their adult life-history career as floaters (16, 17), living in large home ranges (in Namibia of 1,595 km²) which overlap with both female home ranges (mean, 650 km²) and several small territories (mean, 379 km²) of male territory holders (17). Floaters either wait for a territory to become vacant (queuing system) or compete and fight with territory holders to take over a territory (17). This regularly results in the death of either the territory holders or the challengers and suggests that territories contain valuable resources, most likely preferred access to females (16–18). Both floaters and territory holders may be solitary or form coalitions of two to three males, often brothers (16, 17). For this study, we used telemetry data of 106 cheetah individuals to show that in an area where all territorial male units (solitary males or coalitions) were collared, the small territories of cheetah males were distributed in a regular pattern across the landscape and, more importantly, that the territories were not contiguous with each other but were separated by a surrounding matrix. This results in farms containing a cheetah territory, or parts of it, and farms not containing any cheetah territory. Because cheetah males fight over territories, we predict that the location and shape of the territory remains approximately constant across successive territory holders. If so, then the same farms contain (or do not contain) a cheetah territory over successive territory holders, and hence different farm owners experience different levels of conflicts with cheetahs.If territories remain stable over time, we also predict that scent-marking locations operated by territory holders (16, 17) are traditional, “culturally maintained” sites used by several successive territory holders. These scent-marking locations play an important role in the communication of cheetahs (16, 17). They are marked at high frequencies by territory holders; are regularly visited by floaters, which do not mark but only collect information; and are occasionally visited and marked by females, typically when they are in estrus (16, 17). Thus, the scent-marking locations function as information centers for animals where territory defense and information exchange at a local population level are performed (19). They are often large trees (formerly termed “play trees” (20)) but can be any conspicuous structure (e.g., rocks). Scent-marking locations were typically concentrated in the core area of territories, so we termed them “communication hubs” (CHs) of cheetahs. We defined the core areas with CHs as the 50% kernel density estimator (KDE50) of the Global Positioning System (GPS) locations (“fixes”) of the territory holders (see Results). Since each CH was visited by several floaters and females, their home ranges substantially overlapped with the CHs and with each other. On average, each floater and female home range encompassed three CHs and four CHs, respectively (see Results). Each floater unit (solitary floaters or floater coalitions) spent a considerable amount of its time in the CHs (see Results). As a result of the frequent presence of territory holders and regular visits of several floater units in each CH (17), the CHs were local hotspots of cheetah activity and density.We hypothesize that predation risk should be substantially higher in CHs than in the surrounding matrix if the frequency of cheetah hunts is positively related to the number of cheetahs present in an area and the time spent there. If these areas are also used for cattle herds with calves under 6 mo of age (the animals most susceptible to predation by cheetahs), then CHs would be hotspots for cheetah–farmer conflicts. Thus, farmers containing a full CH or part of a CH on their farm are predicted to face higher cattle calf losses by cheetahs than farmers not containing a CH on their farm—a pattern consistent with some farmers reporting heavy losses and others reporting little or no losses. Furthermore, we predict that cattle calf losses can be substantially reduced when suckler herds with calves are shifted away from CHs. If cheetahs in CHs do not follow cattle herds to their new location in another “camp” (i.e., a fenced subsection on the farm permeable for wildlife but not for cattle), then we predict that this simple management adjustment would be the key to substantially reduce farmer–cheetah conflict.     

From the Cover: A functional analysis reveals extremely low redundancy in global mangrove invertebrate fauna

Deforestation results in habitat fragmentation, decreasing diversity, and functional degradation. For mangroves, no data are available on the impact of deforestation on the diversity and functionality of the specialized invertebrate fauna, critical for their functioning. We compiled a global dataset of mangrove invertebrate fauna comprising 364 species from 16 locations, classified into 64 functional entities (FEs). For each location, we calculated taxonomic distinctness (Δ+), functional richness (FRi), functional redundancy (FRe), and functional vulnerability (FVu) to assess functional integrity. Δ+ and FRi were significantly related to air temperature but not to geomorphic characteristics, mirroring the global biodiversity anomaly of mangrove trees. Neither of those two indices was linked to forest area, but both sharply decreased in human-impacted mangroves. About 60% of the locations showed an average FRe < 2, indicating that most of the FEs comprised one species only. Notable exceptions were the Eastern Indian Ocean and west Pacific Ocean locations, but also in this region, 57% of the FEs had no redundancy, placing mangroves among the most vulnerable ecosystems on the planet. Our study shows that despite low redundancy, even small mangrove patches host truly multifunctional faunal assemblages, ultimately underpinning their services. However, our analyses also suggest that even a modest local loss of invertebrate diversity could have significant negative consequences for many mangroves and cascading effects for adjacent ecosystems. This pattern of faunal-mediated ecosystem functionality is crucial for assessing the vulnerability of mangrove forests to anthropogenic impact and provides an approach to planning their effective conservation and restoration.

Mangrove forests, once dominant intertidal ecosystems in the tropics (1), are disappearing at devastating rates worldwide (2, 3). Estimates of their loss are often uncertain due to the nature of available datasets (4) and the imprecision in determining mangrove area (5), but the current consensus on mangrove loss in the last quarter century ranges between 35 to 86% in the worst affected countries (2). Although recent estimates show a decrease in mangrove deforestation (6), global destruction is still happening, putting mangrove ecosystem functionality and, ultimately, provisioning of ecosystem services at risk (7). As recently reassessed (8), mangroves are unrivaled carbon sinks (9) and often contribute significant carbon and nitrogen to offshore habitats (10). They also act as nurseries for species from connected ecosystems (11) and protect tropical coasts from erosion (12) as well as extreme events (13).As theoretical and empirical studies have shown (14, 15), species extinctions in natural ecosystems often lead to loss in functional diversity, reflected by a decrease in the number of functional traits (16). Models predict that species-poor systems have low functional redundancy and are more likely to experience functional loss with species extinction (14, 17). In comparison with many tropical terrestrial forests, mangroves are characterized by low tree species diversity (1). The continued reduction of mangrove area and cover, coupled with simplistic restoration efforts often establishing monocultures (18), is expected to result in a sharp decrease in mangrove tree biodiversity at a global scale (2). A relationship between such decline in tree diversity and the loss of mangrove ecosystem functionality has been assumed rather than demonstrated (19), as this relationship has proven difficult to measure. Significant positive correlations, however, have been demonstrated between the species richness of mangrove trees, the associated macrofauna, and potential influence on aboveground primary productivity (20). The nexus between biodiversity and ecosystem functionality of species-poor systems is yet to be clarified, but a recent study of scavenging (measured by rate of fish carcasses consumed by scavengers) in Australian mangrove-fringed estuaries has highlighted the vulnerability of such systems to species loss (21).While reliable datasets are available on global mangrove tree diversity (1, 5), no such information exists for the species composition, functional diversity, and functional redundancy of the associated fauna. The harsh environmental conditions characteristic of mangrove forests (i.e., wide daily or seasonal variability in salinity and pH, hypo-, or even anoxia of the soil) and the small number of foundation plant species compared to terrestrial forests (2) suggest a lower niche availability among mangrove resident macrofauna (22).Mangrove ecosystems support unique faunal assemblages (22, 23), including a diverse array of sessile and mobile invertebrates, particularly crustaceans and mollusks (24, 25). Brachyuran crab assemblages are highly diverse in Indo-West Pacific (IWP) mangroves (25, 26) and are known to play a major role in ecosystem functioning (8, 20, 23). Their bioturbation activity has a significant engineering effect on the sediment through constant irrigation and oxygenation (27, 28). These crabs can also play a critical role in shaping tree dominance (29), influencing carbon cycling (30, 31), and structuring the sediment microbiome (32). The diversity of mangrove-associated gastropods also peaks in the IWP region but shows a bimodal distribution, with modes in the eastern Pacific coast of Central and South America and in Southeast Asia (33). Both gastropods and bivalves are known to be important bioengineers and bio-irrigators, playing a major role in shaping the biochemical properties of mangrove sediment and water (23).Despite growing evidence that the functions of mangrove forests are strongly dependent on viable and diverse invertebrate assemblages (20, 23), only few studies at local scales have focused on the diversity and taxonomic structure of such assemblages. The functional richness and redundancy of the latter, critical to the ecosystems’ capacity for essential services, are unknown, as are their functional vulnerability. The functional diversity of a community with species distributed in a multidimensional functional space within a given ecosystem can be quantified through indices such as functional richness [FRi—the volume of multidimensional space occupied by all species in a community within functional space (34, 35)] and functional redundancy [FRe—how redundant species and functional groups are at a given location (36)], which are increasingly used for assessing ecosystem functioning. Recently, these measures, used in parallel with functional vulnerability [FVu—the potential decrease of functional diversity as a consequence of species loss (36)], have also proven to be useful tools for assessing impacts of disturbances on ecosystems (37, 38) and for forecasting possible responses to anthropogenic perturbations (16).In this study, we assessed the vulnerability of global mangrove ecosystems to the loss of functions mediated by macrobenthic species by computing taxonomic distinctness Δ+ (39), FRi, FRe, and FVu indices based on crustacean and mollusk assemblages recorded from 16 different mangrove forests across the world. We assigned functional traits to the 209 crustacean and 155 mollusk species in our database according to their respective 1) feeding habits, 2) behavioral traits potentially affecting ecosystem characteristics, and 3) microhabitats. By using functional traits as proxies for functions, this approach allowed us to establish global patterns of macrobenthic taxonomic richness and ecosystem functionality in mangroves and to assess the vulnerability of the mangrove fauna as well as resilience of ecosystem functions mediated by them to current and future anthropogenic threats.     

From the Cover: Cortical instability drives periodic supracellular actin pattern formation in epithelial tubes

An essential question of morphogenesis is how patterns arise without preexisting positional information, as inspired by Turing. In the past few years, cytoskeletal flows in the cell cortex have been identified as a key mechanism of molecular patterning at the subcellular level. Theoretical and in vitro studies have suggested that biological polymers such as actomyosin gels have the property to self-organize, but the applicability of this concept in an in vivo setting remains unclear. Here, we report that the regular spacing pattern of supracellular actin rings in the Drosophila tracheal tubule is governed by a self-organizing principle. We propose a simple biophysical model where pattern formation arises from the interplay of myosin contractility and actin turnover. We validate the hypotheses of the model using photobleaching experiments and report that the formation of actin rings is contractility dependent. Moreover, genetic and pharmacological perturbations of the physical properties of the actomyosin gel modify the spacing of the pattern, as the model predicted. In addition, our model posited a role of cortical friction in stabilizing the spacing pattern of actin rings. Consistently, genetic depletion of apical extracellular matrix caused strikingly dynamic movements of actin rings, mirroring our model prediction of a transition from steady to chaotic actin patterns at low cortical friction. Our results therefore demonstrate quantitatively that a hydrodynamical instability of the actin cortex can trigger regular pattern formation and drive morphogenesis in an in vivo setting.Self-organization is one of the principal mechanisms of biological pattern formation at the molecular, cellular, and tissue scale. Although the pioneering work of Turing (1) has suggested reaction–diffusion as a generic route toward pattern generation (2), a concrete biomolecular or mechanical understanding of how this might occur in vivo remains elusive, except in a few specific cases (3–5). For instance, Kondo and coworkers (6) demonstrated that pigment patterning on the skin of the Pomocanthus imperator can be understood quantitatively from the simple attraction–repulsion kinetics of two cell types.At the cellular level, active structures, such as the cytoskeleton, are generically expected to display a large variety of structures from a theoretical perspective (7–12), many of which have been reproduced in elegant in vitro studies (13–15). In the case of actomyosin gels, the contractile stresses arising from molecular motors have been shown to create large actin flows that can reorganize the cortex (16, 17). Because actin filaments and motors are “self-advected,” or transported, by their own flow (18), there is a self-reinforcing loop in gel density, capable of creating patterns. Nevertheless, most theoretical studies do not consider the cross-effects of polymerization and diffusion, which resist pattern formation. Interestingly, in the past years, several groups have reported in vivo examples of actin patterns: mammalian axons (19), Caenorhabditis elegans embryo (20), and Drosophila trachea (21) are all cellular cylinders that display a regular array of concentric actin rings on their cortex.In this article, we study the example of ring formation in the Drosophila trachea and propose a generic mechanism for stable actin pattern formation, arising from the interplay of actin turnover and myosin activity. The model makes clear predictions, which we test through fly genetics and drug experiments.     

From the Cover: Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs

When tropical systems lose species, they are often assumed to be buffered against declines in functional diversity by the ability of the species-rich biota to display high functional redundancy: i.e., a high number of species performing similar functions. We tested this hypothesis using a ninefold richness gradient in global fish faunas on tropical reefs encompassing 6,316 species distributed among 646 functional entities (FEs): i.e., unique combinations of functional traits. We found that the highest functional redundancy is located in the Central Indo-Pacific with a mean of 7.9 species per FE. However, this overall level of redundancy is disproportionately packed into few FEs, a pattern termed functional over-redundancy (FOR). For instance, the most speciose FE in the Central Indo-Pacific contains 222 species (out of 3,689) whereas 38% of FEs (180 out of 468) have no functional insurance with only one species. Surprisingly, the level of FOR is consistent across the six fish faunas, meaning that, whatever the richness, over a third of the species may still be in overrepresented FEs whereas more than one third of the FEs are left without insurance, these levels all being significantly higher than expected by chance. Thus, our study shows that, even in high-diversity systems, such as tropical reefs, functional diversity remains highly vulnerable to species loss. Although further investigations are needed to specifically address the influence of redundant vs. vulnerable FEs on ecosystem functioning, our results suggest that the promised benefits from tropical biodiversity may not be as strong as previously thought.The human-induced collapse of species has triggered a sixth mass extinction crisis worldwide (1). This ongoing biotic impoverishment may, in turn, markedly alter key ecosystem processes, such as productivity, nutrient cycling, and bioerosion, with undisputed consequences on ecosystem services that humanity needs to prosper (2–4).Beyond the loss of species, the loss of particular functions appears to be the main threat imperiling ecosystem processes and services (4, 5). When several species perform similar functions, this functional redundancy may ensure against the loss of ecosystem functioning following declines in species diversity (6, 7). The critical issue is whether the extraordinary species diversity on Earth matters for ecosystem functioning or whether a smaller proportion of species is enough to perform most of the key functions (8).This debate, at the core of ecological science (5), is even more vigorous in species-rich ecosystems where high functional redundancy among species is likely and where it is thus often assumed that ecosystem functioning is buffered against species loss. For instance, 75% of species could be lost before any functional group would disappear in an Argentinean plant community (6). Such high functional redundancy may ensure the level of functional diversity—i.e., the breadth of functions—against species loss following disturbance (9, 10) or explain why the relationship between species richness and ecosystem functioning may be weak (11) and asymptotic (12).Some tropical ecosystems that hold many more species than their temperate counterparts do not show a higher functional diversity (13). This pattern suggests that functional redundancy may be comparatively higher in the tropics (14). In contrast, despite high levels of species richness, some tropical ecosystems show little functional redundancy among species (15, 16), thus revealing their functional vulnerability: i.e., a potential decrease of functional diversity following species loss (17).Beyond aesthetic and moral arguments, the importance of conserving the whole of tropical biodiversity for maintaining the breadth of potential functions performed in species assemblages is still under scrutiny. Indeed, local or regional assessments are often based on a limited number of species and have offered contradictory results depending on ecosystems, taxa, and functional traits considered (9, 15, 18). We therefore still lack a global study, along a steep gradient of species richness, investigating how species are distributed among functional groups and, more particularly, the extent of functional redundancy and vulnerability.In the marine realm, tropical reefs host a remarkable diversity of fishes that sustain essential ecosystem processes (e.g., trophic control, bioerosion, nutrient cycling) (18). Within the diverse array of species, some perform unique roles and appear to be irreplaceable (19). Moreover, tropical-reef fishes from the Indo-Pacific show a richness that declines with increasing distance from the Indo-Australian Archipelago (IAA) (20), and tropical-reef fish faunas from the Atlantic Ocean have a markedly lower diversity than their Indo-Pacific counterparts (21). Thus, tropical-reef fishes constitute an archetypal situation where we expect a gradient of functional richness, redundancy, and vulnerability, depending on the distribution of species among functional groups. Instead of functional groups, built a priori or after clustering species based on an arbitrary level of trait similarity, we identified 646 functional entities (FEs) based on unique combinations of six categorical functional traits to classify the 6,316 fish species of the global pool. We also built a functional space where FEs were placed according to their trait combinations (22). We then assessed the level of functional diversity, functional redundancy, and functional vulnerability for the tropical-reef fish faunas along a ninefold gradient of species richness. Because the identity, the number, and the categorization of functional traits may influence the results (16), we also performed a series of sensitivity analyses to test the robustness of the findings when decreasing the number of FEs by up to one order of magnitude.