Integrating biogeography and behavioral ecology to rapidly address biodiversity loss.

Addressing climate change and biodiversity loss will be the defining ecological, political, and humanitarian challenge of our time. Alarmingly, policymakers face a narrowing window of opportunity to prevent the worst impacts, necessitating complex decisions about which land to set aside for biodiversity preservation. Yet, our ability to make these decisions is hindered by our limited capacity to predict how species will respond to synergistic drivers of extinction risk. We argue that a rapid integration of biogeography and behavioral ecology can meet these challenges because of the distinct, yet complementary levels of biological organization they address, scaling from individuals to populations, and from species and communities to continental biotas. This union of disciplines will advance efforts to predict biodiversity's responses to climate change and habitat loss through a deeper understanding of how biotic interactions and other behaviors modulate extinction risk, and how responses of individuals and populations impact the communities in which they are embedded. Fostering a rapid mobilization of expertise across behavioral ecology and biogeography is a critical step toward slowing biodiversity loss.

Promoting inclusivity in ecology, evolution, and behavioral biology education through course-based undergraduate research experiences.

Access to independent research experiences is a persistent barrier that stifles the recruitment and retention of students from diverse backgrounds in ecology, evolution, and behavioral biology. The benefits of field experiences are not equitably available to historically excluded and minoritized students. In this article, we summarize evidence that indicates course-based undergraduate research experiences (CUREs) provide a solution to ensure equitable access to independent research experiences in the life sciences. We draw from our own experiences of teaching CUREs in ecology, evolution, and behavioral biology and provide the complete curriculum for our effective and largely materials-free CURE in behavioral ecology (CURE-BxEco). We advocate for greater access to and synthesize the benefits of CUREs to promote inclusivity in education. The proliferation of such innovative pedagogical practices benefits science because these classroom methods are critical in recruiting and retaining historically excluded and minoritized students, who offer diverse perspectives in research.

The active space of sperm whale codas: inter-click information for intra-unit communication.

Sperm whales (Physeter macrocephalus) are social mega-predators who form stable matrilineal units that often associate within a larger vocal clan. Clan membership is defined by sharing a repertoire of coda types consisting of specific temporal spacings of multi-pulsed clicks. It has been hypothesized that codas communicate membership across socially segregated sympatric clans, but others propose that codas are primarily used for behavioral coordination and social cohesion within a closely spaced social unit. Here, we test these hypotheses by combining measures of ambient noise levels and coda click source levels with models of sound propagation to estimate the active space of coda communication. Coda clicks were localized off the island of Dominica with a four- or five-element 80 m vertical hydrophone array, allowing us to calculate the median RMS source levels of 1598 clicks from 444 codas to be 161 dB re. 1 µPa (IQR 153-167), placing codas among the most powerful communication sounds in toothed whales. However, together with measured ambient noise levels, these source levels lead to a median active space of coda communication of ∼4 km, reflecting the maximum footprint of a single foraging sperm whale unit. We conclude that while sperm whale codas may contain information about clan affiliation, their moderate active space shows that codas are not used for long range acoustic communication between units and clans, but likely serve to mediate social cohesion and behavioral transitions in intra-unit communication.

Human behaviors driving disease emergence.

Interactions between humans, animals, and the environment facilitate zoonotic spillover-the transmission of pathogens from animals to humans. Narratives that cast modern humans as exogenous and disruptive forces that encroach upon "natural" disease systems limit our understanding of human drivers of disease. This review leverages theory from evolutionary anthropology that situates humans as functional components of disease ecologies, to argue that human adaptive strategies to resource acquisition shape predictable patterns of high-risk human-animal interactions, (2) humans construct ecological processes that facilitate spillover, and (3) contemporary patterns of epidemiological risk are emergent properties of interactions between human foraging ecology and niche construction. In turn, disease ecology serves as an important vehicle to link what some cast as opposing bodies of theory in human ecology. Disease control measures should consider human drivers of disease as rational, adaptive, and dynamic and capitalize on our capacity to influence ecological processes to mitigate risk.

Making Your Own Luck: Weak Vertical Swimming Improves Dispersal Success for Coastal Marine Larvae.

Dispersive early life stages are common in nature. Although many dispersing organisms ("propagules") are passively moved by outside forces, some improve their chances of successful dispersal through weak movements that exploit the structure of the environment to great effect. The larvae of many coastal marine invertebrates, for instance, swim vertically through the water column to exploit depth-varying currents, food abundance, and predation risk. Several swimming behaviors and their effects on dispersal between habitats are characterized in the literature, yet it remains unclear when and why these behaviors are advantageous. We addressed this gap using a mathematical model of larval dispersal that scored how well behaviors allowed larvae to simultaneously locate habitats, avoid predators, and gather energy. We computed optimal larval behaviors through dynamic programming, and compared those optima against passive floating and three well documented behaviors from the literature. Optimal behaviors often (but not always) resembled the documented ones. However, our model predicted that the behaviors from the literature performed robustly well, if not optimally, across many conditions. Our results shed light on why some larval behaviors are widespread geographically and across species, and underscore the importance of carefully considering the weak movements of otherwise passive propagules when studying dispersal.

Effects of forest fragmentation on the dietary ecology and activity of a nocturnal lemur community in North West Madagascar.

Deforestation and habitat fragmentation is the primary threat to primate populations. The primates that live within degraded and anthropogenically disturbed habitats typical of fragmented landscapes have to cope with lower availability of resources in comparison to primates in continuous, undisturbed forests. While some species are sensitive to forest fragmentation, some evidence exists to suggest that primates can alter their behavior and adapt to such changes, which enables their survival in suboptimal habitat. In this study, we assessed how forest fragmentation and its associated edge-effects impact the feeding ecology and activity levels of a nocturnal primate community in the Sahamalaza-Iles Radama National Park, North West Madagascar. From March 06, 2019 to May 17, 2022, we collected data on tree and invertebrate phenology at our study site, and feeding ecology and activity for 159 lemur individuals from four species. Fruit and flower availability varied significantly between continuous and fragmented forest, and between forest core and edge areas, with continuous forest exhibiting higher continuous fruit and flower availability. Lemur feeding ecology varied significantly too, as the feeding niches of all four species were significantly different between continuous and fragmented forest and between core and edge areas. However, lemur activity levels were mostly consistent among all forest areas. The results of this study suggest that nocturnal lemurs are able to adapt their dietary ecology in response to the available food sources within their habitat. Due to this flexible ecology and dietary plasticity, the lemurs do not need to significantly alter their behavior in different environments to fulfill their dietary needs. While nocturnal lemurs demonstrate adaptability and flexibility to degraded habitat, it is unclear how far this plasticity will stretch considering that Madagascar's forests are still being cleared at an alarming rate. Urgent conservation action is therefore needed to ensure the future of lemur habitat.

A field-based quantitative analysis of sublethal effects of air pollution on pollinators.

While the impact of air pollution on human health is well studied, mechanistic impacts of air pollution on wild systems, including those providing essential ecosystem services, are largely unknown, but directly impact our health and well-being. India is the world's largest fruit producer, second most populous country, and contains 9 of the world's 10 most polluted cities. Here, we sampled Giant Asian honey bees, Apis dorsata, at locations with varying air pollution levels in Bangalore, India. We observed significant correlations between increased respirable suspended particulate matter (RSPM) deposition and changes in bee survival, flower visitation, heart rate, hemocyte levels, and expression of genes related to lipid metabolism, stress, and immunity. Lab-reared Drosophila melanogaster exposed to these same sites also exhibited similar molecular and physiological differences. Our study offers a quantitative analysis on the current impacts of air pollution on insects, and indicates the urgency for more nonhuman studies to accurately assess the effects of pollution on our natural world.

Characterizing long-range search behavior in Diptera using complex 3D virtual environments.

The exemplary search capabilities of flying insects have established them as one of the most diverse taxa on Earth. However, we still lack the fundamental ability to quantify, represent, and predict trajectories under natural contexts to understand search and its applications. For example, flying insects have evolved in complex multimodal three-dimensional (3D) environments, but we do not yet understand which features of the natural world are used to locate distant objects. Here, we independently and dynamically manipulate 3D objects, airflow fields, and odor plumes in virtual reality over large spatial and temporal scales. We demonstrate that flies make use of features such as foreground segmentation, perspective, motion parallax, and integration of multiple modalities to navigate to objects in a complex 3D landscape while in flight. We first show that tethered flying insects of multiple species navigate to virtual 3D objects. Using the apple fly Rhagoletis pomonella, we then measure their reactive distance to objects and show that these flies use perspective and local parallax cues to distinguish and navigate to virtual objects of different sizes and distances. We also show that apple flies can orient in the absence of optic flow by using only directional airflow cues, and require simultaneous odor and directional airflow input for plume following to a host volatile blend. The elucidation of these features unlocks the opportunity to quantify parameters underlying insect behavior such as reactive space, optimal foraging, and dispersal, as well as develop strategies for pest management, pollination, robotics, and search algorithms.

Reciprocity and behavioral heterogeneity govern the stability of social networks.

The dynamics of social networks can determine the transmission of information, the spread of diseases, and the evolution of behavior. Despite this broad importance, a general framework for predicting social network stability has not been proposed. Here we present longitudinal data on the social dynamics of a cooperative bird species, the wire-tailed manakin, to evaluate the potential causes of temporal network stability. We find that when partners interact less frequently and when social connectedness increases, the network is subsequently less stable. Social connectivity was also negatively associated with the temporal persistence of coalition partnerships on an annual timescale. This negative association between connectivity and stability was surprising, especially given that individual manakins who were more connected also had more stable partnerships. This apparent paradox arises from a within-individual behavioral trade-off between partnership quantity and quality. Crucially, this trade-off is easily masked by behavioral variation among individuals. Using a simulation, we show that these results are explained by a simple model that combines among-individual behavioral heterogeneity and reciprocity within the network. As social networks become more connected, individuals face a trade-off between partnership quantity and maintenance. This model also demonstrates how among-individual behavioral heterogeneity, a ubiquitous feature of natural societies, can improve social stability. Together, these findings provide unifying principles that are expected to govern diverse social systems.

Bioluminescent backlighting illuminates the complex visual signals of a social squid in the deep sea.

Visual signals rapidly relay information, facilitating behaviors and ecological interactions that shape ecosystems. However, most known signaling systems can be restricted by low light levels-a pervasive condition in the deep ocean, the largest inhabitable space on the planet. Resident visually cued animals have therefore been hypothesized to have simple signals with limited information-carrying capacity. We used cameras mounted on remotely operated vehicles to study the behavior of the Humboldt squid, Dosidicus gigas, in its natural deep-sea habitat. We show that specific pigmentation patterns from its diverse repertoire are selectively displayed during foraging and in social scenarios, and we investigate how these behaviors may be used syntactically for communication. We additionally identify the probable mechanism by which D. gigas, and related squids, illuminate these patterns to create visual signals that can be readily perceived in the deep, dark ocean. Numerous small subcutaneous (s.c.) photophores (bioluminescent organs) embedded throughout the muscle tissue make the entire body glow, thereby backlighting the pigmentation patterns. Equipped with a mechanism by which complex information can be rapidly relayed through a visual pathway under low-light conditions, our data suggest that the visual signals displayed by D. gigas could share design features with advanced forms of animal communication. Visual signaling by deep-living cephalopods will likely be critical in understanding how, and how much, information can be shared in one of the planet's most challenging environments for visual communication.

Systems Neuroscience of Natural Behaviors in Rodents.

Animals evolved in complex environments, producing a wide range of behaviors, including navigation, foraging, prey capture, and conspecific interactions, which vary over timescales ranging from milliseconds to days. Historically, these behaviors have been the focus of study for ecology and ethology, while systems neuroscience has largely focused on short timescale behaviors that can be repeated thousands of times and occur in highly artificial environments. Thanks to recent advances in machine learning, miniaturization, and computation, it is newly possible to study freely moving animals in more natural conditions while applying systems techniques: performing temporally specific perturbations, modeling behavioral strategies, and recording from large numbers of neurons while animals are freely moving. The authors of this review are a group of scientists with deep appreciation for the common aims of systems neuroscience, ecology, and ethology. We believe it is an extremely exciting time to be a neuroscientist, as we have an opportunity to grow as a field, to embrace interdisciplinary, open, collaborative research to provide new insights and allow researchers to link knowledge across disciplines, species, and scales. Here we discuss the origins of ethology, ecology, and systems neuroscience in the context of our own work and highlight how combining approaches across these fields has provided fresh insights into our research. We hope this review facilitates some of these interactions and alliances and helps us all do even better science, together.

Neither environmental unpredictability nor harshness predict reliance on alloparental care among families in Cebu, Philippines.

Alloparental caregiving is key to humans' highly flexible reproductive strategies. Across species and across societies, alloparental care is more common in harsh and/or unpredictable environments (HUEs). Currently, however, it is unclear whether HUEs predict intra-population variation in alloparental care, or whether early life HUEs might predict later alloparental care use in adulthood, consistent with adaptive developmental plasticity. We test whether harshness measures (socioeconomic status (SES), environmental hygiene, crowding) and unpredictability measures (parental unemployment, paternal absence, household moves) predicted how much alloparental assistance families in Cebu, Philippines received, in a multigenerational study with data collected across four decades. Though worse environmental hygiene predicted more concurrent alloparental care in 1994, we found little evidence that HUEs predict within-population variation in alloparental care in this large-scale, industrialized society. Indeed, less-crowded conditions and higher SES predicted more alloparental care, not less, in the 1980s and in 2014 respectively, while paternal absence in middle childhood predicted less reliance on alloparental care in adulthood. In this cultural context, our results generally do not provide support for the translation of interspecific or intersocietal patterns linking HUEs and alloparental care to intra-population variation in alloparental care, nor for the idea that a reproductive strategy emphasizing alloparental care use may be preceded by early life HUEs.

Sublethal effects of organophosphorus insecticide phoxim on patch time allocation and oviposition behavior in a parasitoid wasp Meteorus pulchricornis.

Parasitoid wasps are key agents for controlling insect pests in integrated pest management programs. Although many studies have revealed that the behavior of parasitic wasps can be influenced by insecticides, the strategies of patch time allocation and oviposition have received less attention. In the present study, we forced the endoparasitoid Meteorus pulchricornis to phoxim exposure at the LC30 and tested the foraging behavior within patches with different densities of the host, the larvae of the tobacco cutworm Spodoptera litura. The results showed that phoxim treatment can significantly increase the patch-leaving tendency of female wasps, while host density had no impact. The number of oviposition and the number of previous patch visits also significantly influenced the patch time allocation decisions. The occurrence of oviposition behavior was negatively affected by phoxim exposure; however, progeny production was similar among patches with different host densities. Phoxim exposure shaped the offspring fitness correlates, including longer durations from cocoon to adult wasps, smaller body size, and shorter longevity. The findings of the present study highlight the sublethal effects that reduce the patch residence time and the fitness of parasitoid offspring, suggesting that the application of phoxim in association with M. pulchricornis should be carefully schemed in agroecosystems.

Social alliances improve rank and fitness in convention-based societies.

Social hierarchies are widespread in human and animal societies, and an individual's position in its hierarchy affects both its access to resources and its fitness. Hierarchies are traditionally thought of in terms of variation in individual ability to win fights, but many are structured around arbitrary conventions like nepotistic inheritance rather than such traits as physical strength or weapon size. These convention-based societies are perplexing because position in the hierarchy appears to be gained irrespective of individual physical ability, yet social status strongly affects access to resources and fitness. It remains unclear why individuals abide by seemingly arbitrary conventions regarding social status when they stand to benefit by ignoring these conventions and competing for top positions or access to resources. Using data from wild spotted hyenas collected over 27 y and five generations, we show that individuals who repeatedly form coalitions with their top allies are likely to improve their position in the hierarchy, suggesting that social alliances facilitate revolutionary social change. Using lifetime reproductive success as a fitness measure, we go on to demonstrate that these status changes can have major fitness consequences. Finally, we show that the consequences of these changes may become even more dramatic over multiple generations, as small differences in social rank become amplified over time. This work represents a first step in reconciling the advantages of high status with the appearance of "arbitrary" conventions that structure inequality in animal and human societies.

Understanding the Enemy: A Review of the Genetics, Behavior and Chemical Ecology of Varroa destructor, the Parasitic Mite of Apis mellifera.

Varroa destructor (Mesostigmata: Varroidae) is arguably the most damaging parasitic mite that attacks honey bees worldwide. Since its initial host switch from the Asian honey bee (Apis cerana) (Hymenoptera: Apidae) to the Western honey bee (Apis mellifera) (Hymenoptera: Apidae), Varroa has become a widely successful invasive species, attacking honey bees on almost every continent where apiculture is practiced. Two haplotypes of V. destructor (Japanese and Korean) parasitize A. mellifera, both of which vector various honey bee-associated viruses. As the population of Varroa grows within a colony in the spring and summer, so do the levels of viral infections. Not surprisingly, high Varroa parasitization impacts bees at the individual level, causing bees to exhibit lower weight, decreased learning capacity, and shorter lifespan. High levels of Varroa infestation can lead to colony-wide varroosis and eventually colony death, especially when no control measures are taken against the mites. Varroa has become a successful parasite of A. mellifera because of its ability to reproduce within both drone cells and worker cells, which allows populations to expand rapidly. Varroa uses several chemical cues to complete its life cycle, many of which remain understudied and should be further explored. Given the growing reports of pesticide resistance by Varroa in several countries, a better understanding of the mite's basic biology is needed to find alternative pest management strategies. This review focuses on the genetics, behavior, and chemical ecology of V. destructor within A. mellifera colonies, and points to areas of research that should be exploited to better control this pervasive honey bee enemy.

Commentary: New Directions in the History of Ethology.

This welcome set of original and instructive papers illuminates and enriches the history of twentieth-century ethology in multiple ways. It adds a wealth of actors, animals, methods, and places to those featured in previous treatments of ethology's development. Some of the papers extend the chronology beyond the heyday of ethology's disciplinary construction to consider exciting developments in the 1970s and beyond. Others consider animal behavior research programs pursued contemporaneously with but independently of mainline ethology's development from the 1930s through the 1960s. Another paper takes us inside an ethologist's archive of visual images to examine the importance of such images (and such a setting) for ethological practice. Collectively, the papers provide new opportunities to contemplate how research programs and disciplines evolve; the relations between concepts, practices, and places; ethology and politics, and much more. At the same time, the individuality of the papers is conspicuous. They have not been constructed on the same model. The authors have followed their own approaches, corresponding to their own, respective interests. A short commentary is not sufficient to do justice to each of them. Rather than attempt to review them one by one, I will consider a pair of themes that may help relate the papers to each other and to the history of ethology: (1) the ongoing challenge of defining ethology and identifying who the ethologists were (or are); (2) the practices and places of animal behavior study.

Landscapes of Time: Building Long-Term Perspectives in Animal Behavior.

In the 1960s, scientists fascinated by the behavior of free-living animals founded research projects that expanded into multi-generation investigations. This paper charts the history of three scientists' projects to uncover the varied reasons for investing in a "long-term" perspective when studying animal behavior: Kenneth Armitage's study of marmots in the Rocky Mountains, Jeanne Altmann's analysis of baboons in Kenya, and Timothy Hugh Clutton-Brock's studies (among others) of red deer on the island of Rhum and meerkats in the Kalahari. The desire to study the behavior of the same group of animals over extended periods of time, I argue, came from different methodological traditions - population biology, primatology, and sociobiology - even as each saw themselves as contributing to the legacy of ethology. As scientists embraced and combined these approaches, a small number of long-running behavioral ecology projects like these grew from short pilot projects into decades-long centers of intellectual gravity within behavioral ecology as a discipline. By attending to time as well as place, we can see how this long-term perspective was crucial to their success; they measured evolutionary changes over generations of animals and their data provided insights into how the animals they studied were adapting (or not) to changing local and global environmental factors.

"It Felt More like a Revolution." How Behavioral Ecology Succeeded Ethology, 1970-1990.

As soon as ethology's status diminished in the early 1970s, it was confronted with two successor disciplines, sociobiology and behavioral ecology. They were able to challenge ethology because it no longer provided markers of strong disciplinarity such as theoretical coherence, leading figures and a clear identity. While behavioral ecology developed organically out of the UK ethological research community into its own disciplinary standing, sociobiology presented itself as a US competitor to the ethological tradition. I will show how behavioral ecology took the role of legitimate heir to ethology by rebuilding a theoretical core and an intellectual sense of community, while sociobiology failed to use its public appeal to reach disciplinary status. Meanwhile, ethology changed its disciplinary identity to encompass all biological studies of animal behavior.

Ecological perspectives on technological diversity at Kanjera South.

The aspects of hominin behavior responsible for Oldowan stone tool variation are the focus of much debate. There is some consensus that this variation arises from a combination of ecological and cultural factors. The diversity of raw material types and technological strategies present at Kanjera South, Kenya, provide an opportunity to examine the interacting influences of ecology and culture on Oldowan stone tool variation. Here, we combine previous analyses of raw material properties, provenance, and technology with quantitative measures of core reduction intensity and tool utilization to examine the influence of both ecological and technocultural factors on stone tool variation at Kanjera South. The results of this analysis reflect a dynamic relationship between raw material properties, provenance, and hominin mobility. Exotic raw materials are generally more resistant to edge attrition compared with those available locally, which may have incentivized their transport over long distances and more extensive reduction. Cores produced on raw materials from distant sources also exhibit more complex core reduction strategies than locally acquired materials. While this pattern is partially due to the differences in the quality of knappable stone, bifacial centripetal and multifacial core reduction strategies also arise due to the continuous transport and use of exotic raw materials. Moreover, the variation in stone tool reduction is not consistent with neutral models of stone tool transport and discard. These results demonstrate that ecological factors such as raw material provenance and physical properties have strong impacts on reduction intensity and the technological strategies used by hominins.

Could woodworking have driven lithic tool selection?

Understanding early stone tools, particularly relationships between form and function, is fundamental to understanding the behavioral evolution of early hominins. The oldest-claimed flake tools date to ca. 3.3 million years ago, and their development may represent a key step in hominin evolution. Flake form, and its relationship to function, has long been a focus of Paleolithic studies, almost exclusively with respect to meat acquisition. However, evidence for woodworking is now known from sites dating to 1.5 Ma. Additionally, Pan troglodytes are known to manufacture wooden tools for hunting and foraging, thus creating a phylogenetic (parsimony) argument for more ancient woodworking. However, few studies examining woodworking and Paleolithic tools have been completed to date. Indeed, it remains an open question whether woodworking may have instigated specific selective demands on the form of early stone tools. Here, we conducted an experiment testing the comparative woodworking efficiency (measured by time) of small and large flakes. Two groups of participants used either a relatively small or large unretouched flake to remove a predefined area from standardized samples of wood. Those using larger flakes were significantly more efficient (i.e., required less time) during this woodworking task. Our results demonstrate that larger flakes could have been preferentially chosen by hominins for woodworking, consistent with previous data generated experimentally in other (non-woodworking) tasks. Moreover, the production of relatively large flakes, such as those at Lomekwi, could have been motivated by woodworking, rather than, or in addition to, butchery. Such issues may also have encouraged the use of Levallois production strategies in later times.