Harry W. Greene

Pleistocene Rewilding: An Optimistic Agenda for Twenty‐First Century Conservation

Large vertebrates are strong interactors in food webs, yet they were lost from most ecosystems after the dispersal of modern humans from Africa and Eurasia. We call for restoration of missing ecological functions and evolutionary potential of lost North American megafauna using extant conspecifics and related taxa. We refer to this restoration as Pleistocene rewilding; it is conceived as carefully managed ecosystem manipulations whereby costs and benefits are objectively addressed on a case‐by‐case and locality‐by‐locality basis. Pleistocene rewilding would deliberately promote large, long‐lived species over pest and weed assemblages, facilitate the persistence and ecological effectiveness of megafauna on a global scale, and broaden the underlying premise of conservation from managing extinction to encompass restoring ecological and evolutionary processes. Pleistocene rewilding can begin immediately with species such as Bolson tortoises and feral horses and continue through the coming decades with elephants and Holarctic lions. Our exemplar taxa would contribute biological, economic, and cultural benefits to North America. Owners of large tracts of private land in the central and western United States could be the first to implement this restoration. Risks of Pleistocene rewilding include the possibility of altered disease ecology and associated human health implications, as well as unexpected ecological and sociopolitical consequences of reintroductions. Establishment of programs to monitor suites of species interactions and their consequences for biodiversity and ecosystem health will be a significant challenge. Secure fencing would be a major economic cost, and social challenges will include acceptance of predation as an overriding natural process and the incorporation of pre‐Columbian ecological frameworks into conservation strategies.

Coral Snake Mimicry: Does It Occur?

Field observations and experimental evidence refute previous objections to the coral snake mimicry hypothesis. Concordant color pattern variation spanning hundreds of miles and several presumed venomous models strongly suggests that several harmless or mildly venomous colubrid snakes are indeed mimics of highly venomous elapids.

Social Behavior in Hatchling Green Iguanas: Life at a Reptile Rookery

Hatchling green iguanas (Iguana iguana) emerge from the ground in small groups in a communal nesting area on a small Panamanian islet and engage in complex social interactions. Iguanas from different clutches often join together before and during departure from the nest site. They also usually move around the islet and migrate from it to the larger adjacent landmass in social groups. These and other observations indicate that the sophistication of saurian social organization and neonate behavior has been underestimated.

Phylogeography of the pitviper clade Agkistrodon: historical ecology, species status, and conservation of cantils.

We used mitochondrial DNA sequences from three gene regions and two tRNAs (ND4, tRNA‐HIS‐SER, 12S, and 16S rDNA) to investigate the historical ecology of the New World pitviper clade Agkistrodon, with emphasis on the disjunct subspecies of the cantil, A. bilineatus. We found strong evidence that the copperhead (A. contortrix) is basal to its congeners, and that the cottonmouth (A. piscivorus) is basal to cantils. Phylogeography and natural history of the living terminal taxa imply that Agkistrodon primitively occupied relatively temperate habitats, with subsequent evolution of tropicality in ancestral A. bilineatus. Our best supported phylogeny rejects three gulf arc scenarios for the biogeography of A. bilineatus. We find significant statistical support for an initial divergence between populations on the east and west coasts of México and subsequent occupancy of the Yucatán Peninsula, by way of subhumid corridors in northern Central America. Based on phylogenetic relationships, morphological and molecular divergence, and allopatry we elevate A. b. taylori of northeastern México to species status. Taylor’s cantil is likely threatened by habitat destruction and small geographical range, and we offer recommendations for its conservation and management.

Empirical evidence of non-correlation between tail loss frequency and predation intensity on lizards

We examined the widespread assumption that tail loss frequency in lizards is positively correlated with predation intensity. Empirical data from a California locality show that no correlation exists. We suggest that tail loss frequencies are more likely to reflect the inefficiency of predators rather than the intensity of predation. Previous conclusions based on tail loss data regarding the effect of predators on behavioral, population, and community phenomena in lizards are consequently suspect.

Defensive Tail Display by Snakes and Amphisbaenians

Seventy-six species of snakes and 2 species of amphisbaenians are reported to display the tail so that it becomes unusually conspicuous. This behavior is ordinarily a response to stress, such as a sudden tactile stimulus, and is probably an antipredator strategy. The snakes can be placed in 3 groups on the basis of coloration and caudal morphology. (1) Five species are obscurely patterned or unicolored and have short tails with blunt tips. (2) Fifty-four species have contrasting or brightly colored tails without stout, blunt tips. (3) Seveeen species have either blunt, brightly colored tails or tapered, dull colored tails. Display is correlated with a brightly colored, autotomizeable tail in one amphisbaenian and with a blunt, heavily reinforced tail tip in another. A study of injuries on the tails of 52 Eryx johnii and 63 Calabaria reinhardtii suggests that these snakes display their blunt tails to misdirect the attacks of predators. Skeletal peculiarities of several boids (Charina and Eryx) and of Amphisbaena alba might be adaptations for this function of tail display. The injury data for 156 pipe snakes (Cylindrophis rufus) imply that misdirection of attack is not an important function of the display of this brightly colored species. Bright colors associated with the tail displays of many snakes and of A. fuliginosa might serve as intimidating devices, aposematic signals, or mimetic signals. The display of A. fuliginosa probably also facilitates caudal autotomy. Different functions of tail display need not, of course, be mutually exclusive. A comprehensive bibliography of tail display behavior, new information for many species, a brief discussion of terminology, speculation on the origins of tail displays, and suggestions for future investigations are also presented.

Who Speaks with a Forked Tongue

State-of-the-art molecular and morphological phylogenies for lizards differ fundamentally. At the dawn of molecular phylogenetics, much was made of the conflict between results from morphological and molecular data sets. Although molecular data have rarely changed our understanding of the major multicellular groups of the evolutionary tree of life, they have suggested changes in the relationships within many groups, such as the evolutionary position of whales in the clade of even-toed ungulates (1). Further investigation has usually resolved conflicts, often by revealing inadequacies in previous morphological studies. This has led to a presumption by many in favor of molecular data, but a recent morphological analysis by Gauthier et al. (2) argues persuasively that we should reconsider whether DNA is always inherently superior for inferring lifes history.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems

Looking back to move forward The current impacts of humanity on nature are rapid and destructive, but species turnover and change have occurred throughout the history of life. Although there is much debate about the best approaches to take in conservation, ultimately, we need to permit or enhance the resilience of natural systems so that they can continue to adapt and function into the future. In a Review, Barnosky et al. argue that the best way to do this is to look back at paleontological history as a way to understand how ecological resilience is maintained, even in the face of change. Science, this issue p. eaah4787 BACKGROUND The pace and magnitude of human-caused global change has accelerated dramatically over the past 50 years, overwhelming the capacity of many ecosystems and species to maintain themselves as they have under the more stable conditions that prevailed for at least 11,000 years. The next few decades threaten even more rapid transformations because by 2050, the human population is projected to grow by 3 billion while simultaneously increasing per capita consumption. Thus, to avoid losing many species and the crucial aspects of ecosystems that we need—for both our physical and emotional well-being—new conservation paradigms and integration of information from conservation biology, paleobiology, and the Earth sciences are required. ADVANCES Rather than attempting to hold ecosystems to an idealized conception of the past, as has been the prevailing conservation paradigm until recently, maintaining vibrant ecosystems for the future now requires new approaches that use both historical and novel conservation landscapes, enhance adaptive capacity for ecosystems and organisms, facilitate connectedness, and manage ecosystems for functional integrity rather than focusing entirely on particular species. Scientific breakthroughs needed to underpin such a paradigm shift are emerging at the intersection of ecology and paleobiology, revealing (i) which species and ecosystems will need human intervention to persist; (ii) how to foster population connectivity that anticipates rapidly changing climate and land use; (iii) functional attributes that characterize ecosystems through thousands to millions of years, irrespective of the species that are involved; and (iv) the range of compositional and functional variation that ecosystems have exhibited over their long histories. Such information is necessary for recognizing which current changes foretell transitions to less robust ecological states and which changes may signal benign ecosystem shifts that will cause no substantial loss of ecosystem function or services. Conservation success will also increasingly hinge on choosing among different, sometimes mutually exclusive approaches to best achieve three conceptually distinct goals: maximizing biodiversity, maximizing ecosystem services, and preserving wilderness. These goals vary in applicability depending on whether historical or novel ecosystems are the conservation target. Tradeoffs already occur—for example, managing to maximize certain ecosystem services upon which people depend (such as food production on farm or rangelands) versus maintaining healthy populations of vulnerable species (such as wolves, lions, or elephants). In the future, the choices will be starker, likely involving decisions such as which species are candidates for managed relocation and to which areas, and whether certain areas should be off limits for intensive management, even if it means losing some species that now live there. Developing the capacity to make those choices will require conservation in both historical and novel ecosystems and effective collaboration of scientists, governmental officials, nongovernmental organizations, the legal community, and other stakeholders. OUTLOOK Conservation efforts are currently in a state of transition, with active debate about the relative importance of preserving historical landscapes with minimal human impact on one end of the ideological spectrum versus manipulating novel ecosystems that result from human activities on the other. Although the two approaches are often presented as dichotomous, in fact they are connected by a continuum of practices, and both are needed. In most landscapes, maximizing conservation success will require more integration of paleobiology and conservation biology because in a rapidly changing world, a long-term perspective (encompassing at least millennia) is necessary to specify and select appropriate conservation targets and plans. Although adding this long-term perspective will be essential to sustain biodiversity and all of the facets of nature that humans need as we continue to rapidly change the world over the next few decades, maximizing the chances of success will also require dealing with the root causes of the conservation crisis: rapid growth of the human population, increasing per capita consumption especially in developed countries, and anthropogenic climate change that is rapidly pushing habitats outside the bounds experienced by today’s species. Fewer than 900 mountain gorillas are left in the world, and their continued existence depends upon the choices humans make, exemplifying the state of many species and ecosystems. Can conservation biology save biodiversity and all the aspects of nature that people need and value as 3 billion more of us are added to the planet by 2050, while climate continues to change to states outside the bounds that most of today’s ecosystems have ever experienced? Photo: E. A. Hadly, at Volcanoes National Park, Rwanda Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.

Hunter–gatherers and other primates as prey, predators, and competitors of snakes

Relationships between primates and snakes are of widespread interest from anthropological, psychological, and evolutionary perspectives, but surprisingly, little is known about the dangers that serpents have posed to people with prehistoric lifestyles and nonhuman primates. Here, we report ethnographic observations of 120 Philippine Agta Negritos when they were still preliterate hunter–gatherers, among whom 26% of adult males had survived predation attempts by reticulated pythons. Six fatal attacks occurred between 1934 and 1973. Agta ate pythons as well as deer, wild pigs, and monkeys, which are also eaten by pythons, and therefore, the two species were reciprocally prey, predators, and potential competitors. Natural history data document snake predation on tree shrews and 26 species of nonhuman primates as well as many species of primates approaching, mobbing, killing, and sometimes eating snakes. These findings, interpreted within the context of snake and primate phylogenies, corroborate the hypothesis that complex ecological interactions have long characterized our shared evolutionary history.

Sympatric rattlesnakes with contrasting mating systems show differences in seasonal patterns of plasma sex steroids

Long-term field studies conducted in Arizona show that two species of sympatric rattlesnakes differ in the structure of their mating systems, primarily in frequency and timing of mating seasons, despite exposure to identical environmental conditions. The western diamond-backed rattlesnake, Crotalus atrox, has two distinct mating seasons within a single annual spermatogenic cycle. The first mating season occurs from late August to early October. Following a hibernation period of 4 months, the second mating season occurs from mid-March to early May. Because there is a mating season in spring, long-term sperm storage by females during winter is facultative. In contrast, the black-tailed rattlesnake, Crotalus molossus, has a single mating season (mid-July to early September) within a single annual spermatogenic cycle. Due to the absence of a mating season in spring, long-term sperm storage by females during winter is obligatory. In both species, ovulation and fertilization occur in spring, and offspring are produced from mid-July to early September. Based on these robust data, we tested the hypotheses that seasonal patterns of plasma sex steroids (testosterone, 5α-dihydrotestosterone, and 17β-estradiol) differ between males in wild populations of C. atrox and C. molossus, and that peak levels would be coincident with the mating seasons. Specifically, we predicted that there would be two peaks of sex steroids in C. atrox and one peak in C. molossus, and that baseline levels would be detected outside the periods of mating and spermatogenesis. Our results supported these predictions. Furthermore, absolute concentrations of plasma testosterone and 5α-dihydrotestosterone, but not 17β-estradiol, were higher in C. atrox than in C. molossus. We discuss a possible scenario for the evolution of the different mating seasons in these sympatric rattlesnakes, and advocate that comparative approaches to address such questions should integrate proximate and ultimate causation to increase explanatory power.