Animal Life History Research Articles

Warm winters lead to increased reproductive effort, but lower reproductive success: Hidden costs of climate warming in a threatened bird

Abstract Climate warming is affecting the phenology and life history of animals around the world. In birds, although warm winters have been shown to advance breeding dates and affect reproductive success in a diverse range of taxa, few studies document whether changes in breeding phenology are associated with variability in reproductive effort by breeders. We leveraged a 37-year dataset on the demography of Aphelocoma coerulescens (Florida Scrub-Jay) to investigate not only whether winter weather affects jay phenology and reproductive success, but also whether winter weather affects overall reproductive effort. Jays bred early but fledged fewer offspring in springs following warm winters. Surprisingly, this reduced reproductive success came at the expense of increased reproductive effort (number of nests built, number of eggs laid, and length of the breeding period across all attempts) by the breeders. Given the well-known trade-off between reproductive effort and survival, we highlight an important but typically unrecognized cost of climate warming on birds, as revealed by a long-term study of a large, well-protected population.

Environment and diet shape the geography-specific Drosophila melanogaster microbiota composition.

The microbial communities of animals influence their hosts' evolution and wild fitness, but it is hard to predict and explain how the microbiota varies in wild animals. Here, we describe that the microbiota composition of wild Drosophila melanogaster can be ordered by temperature, humidity, geographic distance, diet decomposition, and diet type. We show how these determinants of microbiota variation can help explain lactic acid bacteria (LAB) abundance in the flies, including the rarity of LAB in some previous studies. Finally, we show that wild fly phenotypes segregate with the flies' diet and microbiota composition, illuminating links between the microbiota and host evolution. Together, these findings help explain how variation in microbiota compositions can shape an animal's life history.

Identification of the principal neuropeptide MIP and its action pathway in larval settlement of the echiuran worm Urechis unicinctus.

Larval settlement and metamorphosis represent critical events in the life history of marine benthic animals. Myoinhibitory peptide (MIP) plays a pivotal role in larval settlement of marine invertebrates. However, the molecular mechanisms of MIP involved in this process are not well understood. In this study, we evaluated the effects of thirteen MIP mature peptides on triggering the larval settlement of Urechis unicinctus (Xenopneusta, Urechidae), and determined that MIP2 was the principal neuropeptide. Transcriptomic analysis was employed to identify differentially expressed genes (DEGs) between the MIP2-treated larvae and normal early-segmentation larvae. Both cAMP and calcium signaling pathways were enriched in the DEGs of the MIP2-treated larvae, and two neuropeptide receptor genes (Spr, Fmrfar) were up-regulated in the MIP2-treated larvae. The activation of the SPR-cAMP pathway by MIP2 was experimentally validated in HEK293T cells. Furthermore, fourteen cilia-related genes, including Tctex1d2, Cfap45, Ift43, Ift74, Ift22, Cav1 and Mns1, etc. exhibited down-regulated expression in the MIP2-treated larvae. Whole-mount in situ hybridization identified two selected ciliary genes, Tctex1d2 and Cfap45, were specially expressed in circumoral ciliary cells of the early-segmentation larvae. Knocking down Tctex1d2 mRNA levels by in vivo RNA interference significantly increased the larval settlement rate. Our findings suggest that MIP2 inhibits the function of the cilia-related genes, such as Tctex1d2, through the SPR-cAMP-PKA pathway, thereby inducing larval settlement in U. unicinctus. The study contributes important data to the understanding of neuropeptide regulation in larval settlement.

Boldness suppresses hoarding behavior in food hoarding season and reduces over-wintering survival in a social rodent.

The "pace-of-life" syndrome (POLS) framework can encompass multiple personality axes that drive important functional behaviors (e.g., foraging behavior) and that co-vary with multiple life history traits. Food hoarding is an adaptive behavior important for an animal's ability to adapt to seasonal fluctuations in food availability. However, the empirical evidence for the relationships between animal personality and hoarding behavior remains unclear, including its fitness consequences in the POLS framework. In this study, the Mongolian gerbil (Meriones unguiculatus), a social rodent, was used as a model system to investigate how boldness or shyness is associated with food hoarding strategies during the food hoarding season and their impact on over-winter survival and reproduction at both individual and group levels. The results of this study showed that, compared with shy gerbils, bold gerbils had a lower effort foraging strategy during the food hoarding season and exhibited lower over-winter survival rates. However, bold-shy personality differences had no effect on over-winter reproduction. These findings suggest that the personality is a crucial factor influencing the foraging strategy during the food hoarding season in Mongolian gerbils. Personality may be related to energy states or the reaction to environmental changes (e.g., predation risk and food availability) in bold or shy social animals. These results reflect animal life history trade-offs between current versus future reproduction and reproduction versus self-maintenance, thereby helping Mongolian gerbils in adapting to seasonal fluctuations in their habitat.

Modeling post-Pleistocene megafauna extinctions as complex social-ecological systems

Abstract The role of human hunting behavior versus climate change in the mass extinction of megafauna during the Late Quaternary is much debated. To move beyond monocausal arguments, we treat human–megafauna–environment relationships as social–ecological systems from a complex adaptive systems perspective, to create an agent-based model that tests how human hunting may interact with environmental stress and animal life history to affect the probability of extinction. Using the extinction of Syncerus antiquus in South Africa at 12–10 ka as a loose inspirational case study, we parameterized a set of experiments to identify cross-feedbacks among environmental dynamics, prey life history, and human hunting pressure that affect extinction probability in a non-linear way. An important anthropogenic boundary condition emerges when hunting strategies interrupt prey animal breeding cycles. This effect is amplified in patchy, highly seasonal environments to increase the chances of extinction. This modeling approach to human behavior and biodiversity loss helps us understand how these types of cross-feedback effects and boundary conditions emerge as system components interact and change. We argue that this approach can help translate archaeological data and insight about past extinction for use in understanding and combating the current mass extinction crisis.

Resting posture drives the evolution of agonistic displays in bats.

Agonistic displays are one of the most diverse social behaviors that have important functions in animal's life history. However, their origin and driving factors have largely been unexplored. Here, we evaluated agonistic displays of 71 bat species across 10 families and classified these displays into two categories: (a) boxing displays where a bat attacks its opponent with its wrist and thumb and (b) pushing displays where a bat uses its head or body to hit a rival. We estimated the strength of the phylogenetic signal of the agonistic displays, revealed their origin, and tested the potential evolutionary relationships between agonistic behaviors and body size or resting posture (free hanging vs. contact hanging where the bat is in contact with some surface). We found that agonistic displays were phylogenetically conserved and that boxing displays are the ancestral state. Moreover, we found that bats with a free-hanging resting posture were more likely to exhibit boxing displays than pushing displays. In addition, bats with longer forearms do not have a higher propensity for boxing displays. This study expands our limited knowledge of the evolution of agonistic displays and highlights the importance of resting posture as a driving force in the diversity of agonistic displays.

Interpopulation variation in prebreeding energy reserves of plateau brown frog (Rana kukunoris)

The energy storage plays a prominent part in the life histories of many animals inhabiting cold harsh environment, thus anuran amphibians rely on larger residual energy stores from post-hibernation to cope with unfavourable weather conditions before breeding. As the habitat conditions often change in different locations, selective pressure for energy storage could also vary. However, we still have limited knowledge on whether anurans living under different environmental backgrounds would adopt suitable strategies to cope with energy demands during reproduction. Here, we examined patterns of energy storage in spring (after hibernation and before reproduction) in seven plateau brown frog (Rana kukunoris) populations with different climatic conditions in the eastern Tibetan Plateau. After removing the effects of age and body size, liver weights of both sexes and fat body weights in males were negatively correlated with temperature, suggesting that these reserves were critical for this anuran to survive through harsh and extended dormancy period under uncertain environmental conditions. Additionally, reproductive investment in both sexes could partly explain the increase in post-hibernation energy stores with decreasing temperature. Males had relatively heavier liver and fat body weights than females, indicating that males store more energy reserves for breeding activity compared with females. Therefore, we suggest that both the variation of environmental conditions and sexual differentiation of reproductive roles play a prominent role in shaping the energy allocation and reserve patterns in the dormancy and breeding of amphibian species.

Facilitating the recovery of insect communities in restored streams by increasing oviposition habitat.

Recruitment limitation is known to influence species abundances and distributions. Recognition of how and why it occurs both in natural and in designed environments could improve restoration. Aquatic insects, for instance, rarely reestablish in restored streams to levels comparable to reference streams even years after restoration. We experimentally increased oviposition habitat in five out of 10 restored streams in western North Carolina to test whether insect egg-laying habitat was limiting insect populations in restored streams. A main goal was to test whether adding oviposition habitat in the form of rocks that partially protrude above the water surface could be used to increase the abundance and richness of stream insect eggs and larval insects in restored streams. Adding egg-laying habitat enhanced several response variables (e.g., protruding rocks, number of eggs, egg masses, egg morphotype richness, and oviposition habitat stability) to levels similar to those found in reference streams. Following the addition of protruding rocks, egg mass abundance increased by 186% and richness by 77% in restored-treated streams. Densities of larval insects that attached their eggs to protruding rocks showed an overall pattern consistent with treatment effects due to the combination of nonsignificant and significant increases of several taxa and not just one taxon. Our results indicate that these stream insect populations are limited by oviposition habitat and that adding egg-laying habitat alleviated this component of recruitment limitation. However, the weaker larval response indicates that additional post-recruitment factors, such as egg or larval mortality, may still be limiting a full recovery of larval insect abundances in these restored streams. This study shows the importance of integrating information from animal life histories, ecology, and geomorphology into restoration practices to improve the recovery of aquatic insects, which are commonly used to assess water quality and the biological efficacy of stream restoration.

Non-invasive age estimation based on faecal DNA using methylation-sensitive high-resolution melting for Indo-Pacific bottlenose dolphins.

Age is necessary information for the study of life history of wild animals. A general method to estimate the age of odontocetes is counting dental growth layer groups (GLGs). However, this method is highly invasive as it requires the capture and handling of individuals to collect their teeth. Recently, the development of DNA-based age estimation methods has been actively studied as an alternative to such invasive methods, of which many have relied on used biopsy samples. However, if DNA-based age estimation can be developed from faecal samples, age estimation can be performed entirely non-invasively. We developed an age estimation model using the methylation rate of two gene regions, GRIA2 and CDKN2A, measured through methylation-sensitive high-resolution melting (MS-HRM) from faecal samples of wild Indo-Pacific bottlenose dolphins (Tursiops aduncus). The age of individuals was known through conducting longitudinal individual identification surveys underwater. Methylation rates were quantified from 36 samples collected from 30 individuals. Both gene regions showed a significant correlation between age and methylation rate. The age estimation model was constructed based on the methylation rates of both genes which achieved sufficient accuracy (after LOOCV: MAE = 5.08, R2 = 0.33) for the ecological studies of the Indo-Pacific bottlenose dolphins, with a lifespan of 40-50 years. This is the first study to report the use of non-invasive faecal samples to estimate the age of marine mammals.

Effect of resource supplementation on female Western Rattlesnake postpartum movement

Resource availability plays an important factor in an animal's life history by affecting growth and reproduction and influencing behaviours such as movement and thermoregulation. Female rattlesnakes in northern climes face shortened active seasons limiting the time available to replenish lost reserves from reproduction. Consequently, this leads to slower growth rates, small litters, and infrequent reproduction in these populations. With these challenges, it has been assumed postpartum rattlesnakes in these regions should return to their hibernacula immediately following parturition. However, our previous study revealed different tactics of postpartum movements by females across several study sites. To examine the relationship between resource availability and these movements, we experimentally supplemented resources (mice or mice injected with water) to free-ranging pregnant Western Rattlesnakes ( Crotalus oreganus Holbrook, 1840) at three sites in British Columbia, Canada, during 2019. We examined body condition and movement of snakes, finding that pregnant rattlesnakes consumed supplemented resources until late parturition and had significantly higher postpartum body condition than controls. Contrary to our expectations, increased access to resources ad libitum did not significantly halt or alter postpartum movements away from hibernacula. These results suggest that resource availability influences certain life-history traits such as body condition but not others like postpartum movement.

Rapid growth in a large Cambrian apex predator.

Despite the importance of ontogenetic data on early diverging euarthropods to our understanding of the ecology and evolution of past life, the data are distinctly lacking, as reconstructing life histories of fossil animals is often challenging. Here we report the growth trajectory of frontal appendages of the apex predator Amplectobelua symbrachiata, one of the most common radiodont arthropods from the early Cambrian Chengjiang biota (c. 520 Ma) of China. Analysis of 432 specimens (9.1-137.1mm length; 1.3-25.6mm height) reveals that appendages grew isometrically, with an estimated maximum size of the whole animal of c. 90cm. Individuals grew rapidly compared to extant arthropods, as assessed using the electronic length-frequency analysis (ELEFAN) approach. Therefore, we show that the Cambrian apex predator A. symbrachiata was an extremely fast-growing arthropod, with an unusual life history strategy that formed as part of the escalatory 'arms race' that shaped the Cambrian explosion over 500 Ma.

Integrating human behavior into structured population models

Human behavior shapes modern ecosystems but is difficult to parse into parameters for ecological models. We used Bayesian models of human behavior, a stage-structured population model, and a novel mortality integration approach to ask how human decisions affect animal population dynamics and conservation outcomes in the context of recreational fishing. Walleye (Sander vitreus) are a broadcast-spawning freshwater fish with large, slow-maturing females and small, fast-maturing males. We observed that simpler and less restrictive fishing regulations outperformed more complex and stricter regulations at conserving equilibrium adult female abundance and overall population abundance while still facilitating large harvests. This outcome was possible because angler behavior within the least restrictive regulation concentrated harvest on juveniles and adult males. Our findings indicate that, counter to intuitive expectations, moderate regulations can acheive conservation objectives when we account for the interaction of regulatory policy, human behavior, and animal life history. We suggest that integrating models of human behavior with models of animal life history and population dynamics will provide essential insights for conservation in ecosystems increasingly shaped by human decisions.

Marine mammal morphometrics: 3D modeling and estimation validation

Techniques of 3D modeling have earned increasing popularity in scientific studies as they offered unprecedented traits in representing objects. As with all mathematical models, the 3D model will be useful once its accuracy has been validated with direct measurements and the robustness of its predictive capability tested. Although measures of body mass and volume are essential to comprehend the life history of animals, such morphometrics, especially total volume, are challenging to obtain from marine mammals due to their elusive nature, aquatic lifestyle, and large size. In this study, accurate measurements of body volume were directly detected from fresh carcasses of eleven finless porpoises (Neophocaena asiaeorientalis sunameri) and used to validate 3D models recreated from the same animals using Blender 3D graphics. Published models using truncated cones or elliptical shapes, based on 3, 5, 8, or 19 measurements of girths or heights & widths along the body, were also applied to porpoises to verify their accuracy. The Blender-generated 3D model produced the most accurate estimates of body volume compared to conventional truncated models, with a mean error of only 2.5% to the direct volume measurements. When photogrammetric images are available, the model can predict the body volumes based on total length alone. Similar accuracy was possible with the elliptical model using 19 height & width measurements (5% increments in total length). However, significant (p < 0.001) inaccuracy resulted from truncated models with 3, 5, or 8 girth measurements and elliptical models with 3 or 5 height & width measurements, and the accuracy of these models also decreased significantly as the number of measurement sites was reduced. Moreover, Blender 3D models can be extrapolated to animals with images absent, and such predicted volumes were tested to be trustworthy (overall skill = 0.998, r = 0.998, p < 0.01). Therefore, we recommend that researchers use either digital 3D models or elliptical models with 5% increments sectioning the torso to obtain accurate estimates of the body volumes of free-ranging marine mammals.

Paleobiological implications of the bone histology of the extinct Australian marsupial Nimbadon lavarackorum

AbstractDespite the recognition that bone histology provides much information about the life history and biology of extinct animals, osteohistology of extinct marsupials is sorely lacking. We studied the bone histology of the ca. 15-million-year-old Nimbadon lavarackorum from Australia to obtain insight into its biology. The histology of thin sections of five femora and five tibiae of juveniles, subadult, and adult Nimbadon lavarackorum was studied. Growth marks in the bones suggest that N. lavarackorum took at least 7–8 years (and likely longer) to reach skeletal maturity. The predominant bone tissue during early ontogeny is parallel-fibered bone, whereas an even slower rate of bone formation is indicated by the presence of lamellar bone tissue in the periosteal parts of the compacta in older individuals. Deposition of bone was interrupted periodically by lines of arrested growth or annuli. This cyclical growth strategy indicates that growth in N. lavarackorum was affected by the prevailing environmental conditions and available resources, as well as seasonal physiological factors such as decreasing body temperatures and metabolic rates.

Cover Picture and Issue Information

Methods in Ecology and EvolutionVolume 14, Issue 4 p. 991-993 COVER PICTURE AND ISSUE INFORMATIONOpen Access Cover Picture and Issue Information First published: 05 April 2023 https://doi.org/10.1111/2041-210X.13885AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Graphical Abstract This month’s cover image shows a researcher tracking for an animal fitted with a radio collar as part of wildlife population monitoring. Such monitoring activities often involve observing the life histories of individual animals to determine key demographic indicators of a population, such as birth, death, and dispersal rates. In most wildlife studies, however, it is common for monitored animals to disappear under unexplained circumstances, making it difficult to draw reliable conclusions about death and dispersal. Have these missing individuals died or dispersed? Hodel et al. present a method that draws on information about known death and dispersal events to reconstruct the fate of missing individuals. Their approach offers the potential to reduce bias in mortality estimates, which is of fundamental importance for ecology, evolution, and conservation research. © Dominik Behr Volume14, Issue4April 2023Pages 991-993 RelatedInformation

Stratification of lipids, fatty acids and organochlorine contaminants in blubber of white whales and killer whales

The biopsy 2 via dart, trocar or surgery 2 is becoming the preferred protocol for sampling skin and blubber of many cetacean species, because a small sample from a healthy animal may provide better information than a larger sample collected via necropsy from an ill or emaciated animal. Furthermore, the biopsy is often the only means of obtaining samples (e.g. for threatened or endangered species). Because biopsy darts collect only a small sample of tissue 2 and blubber can be heterogeneous in structure and composition 2 it is essential to compare the results obtained from biopsies to those found by analysing full-thickness blubber samples obtained via necropsy. This manuscript compares blubber stratification in two odontocete species, white whales (Delphinapterus leucas) and killer whales (Orcinus orca). Five parameters (i.e. lipid percent and classes, contaminant concentrations and profiles, fatty acid profiles) were measured by blubber depth. Results of these comparisons strongly suggest that biopsy results must be interpreted with caution and in conjunction with results from species-specific blubber depth profiling. For example, lipid classes measured in biopsy samples of white whales and killer whales were similar to those for equivalent-depth samples obtained by necropsy. In addition, lipid-adjusted contaminant concentrations measured in dart or trocar samples adequately represented those obtained by necropsy of both species. Conversely, the lipid content in biopsy samples was lower than that found in same-depth necropsied samples due to loss of lipid during sampling. Also, because of the high level of fatty acid stratification observed, fatty acid profiles from the outer blubber layer collected via biopsy from both species are less likely than the metabolically active inner layer to be useful in determining the prey species consumed by these odontocetes. This study demonstrates, for white and killer whales, that properly interpreted results from blubber biopsies can provide valuable information about the body condition, health and life history of individual animals.

Correlated evolution of social organization and lifespan in mammals

Discerning the relationship between sociality and longevity would permit a deeper understanding of how animal life history evolved. Here, we perform a phylogenetic comparative analysis of ~1000 mammalian species on three states of social organization (solitary, pair-living, and group-living) and longevity. We show that group-living species generally live longer than solitary species, and that the transition rate from a short-lived state to a long-lived state is higher in group-living than non-group-living species, altogether supporting the correlated evolution of social organization and longevity. The comparative brain transcriptomes of 94 mammalian species identify 31 genes, hormones and immunity-related pathways broadly involved in the association between social organization and longevity. Further selection features reveal twenty overlapping pathways under selection for both social organization and longevity. These results underscore a molecular basis for the influence of the social organization on longevity.

Temperature-dependent melanism and phenoloxidase activity in the dimorphic sepsid fly Sepsis thoracica

Climate is changing towards both higher average temperatures and more frequent and severe heat waves. Whereas numerous studies have investigated temperature effects on animal life histories, assessments of their immune function are limited. In the size- and colour-dimorphic black scavenger (or dung) fly Sepsis thoracica (Diptera: Sepsidae), we experimentally studied how developmental temperature and larval density influence phenoloxidase (PO) activity, a key enzyme in insect pigmentation, thermoregulation, and immunity. Flies from five latitudinal European populations were raised at three developmental temperatures (18, 24, 30 °C). PO activity increased with developmental temperature differently in the sexes and the two male morphs (black and orange), altering the sigmoid relationship between melanism, i.e. colouration and fly size. PO activity further positively correlated with larval rearing density, potentially because of higher risks of pathogen infection or greater developmental stress following stronger resource competition. Populations varied somewhat in PO activity, body size and colouration, however with no clear latitudinal pattern. Overall our results indicate that morph- and sex-specific PO activity, and thus likely immune function, in S. thoracica depends on temperature and larval density, modifying the underlying putative trade-off between immunity and body size. The strong dampening of the immune system of all morphs at cool temperatures suggests low-temperature stress in this warm-adapted species common in southern Europe. Our results also support the population density dependent prophylaxis hypothesis, which predicts higher investment in immunity when facing limited resource availability and increased pathogen infection probability.

Maternal effects and the legacy of extreme environmental events for wild mammals.

Maternal effects and the legacy of extreme environmental events for wild mammals.

To tag ornot to tag: comparative performance of tagging and photo-identification in a long-term mark-recapture of Juvenile Green Turtles (Chelonia mydas)

Abstract Capture-mark-recapture (CMR) methods are widely used to estimate population parameters and to collect data on animal demography, migration, and life history. Sea turtle research programs generally use artificial tags, an invasive method. Photo-identification (PID) methods have become an important tool for animal identification. Herein, we assessed the effectiveness of a PID method for marking green turtles (Chelonia mydas) compared to traditional methods (artificial tags). As a part of a long-term CMR study, green turtles have been tagged and photographed since 2001. We analyzed 1917 captures with left and right side photographs of tagged turtles using Wild-ID software, these results were compared with tag-recapture data to assess error rates (false positives and negatives), and different effectiveness metrics. A combination of PID and tags (a match from either method was considered a recapture) was the most error-free and efficient criterion for identification of recaptures; however, it was the most time consuming and invasive criterion as well. We also assessed the effect of image quality indicators on the error rates of PID. We found that turtle cleanliness increases the similarity of images (indirectly related to false negatives), but we found no effect of sharpness, angle, light condition, or width and height in pixels of images on error rates. We could conclude that if image quality is improved, tags could be substituted by PID. However, we strongly recommend researchers to consider local situations (occurrence of by-catch or stranded dead turtles, for which tags are still necessary) before deciding to apply only PID.