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Snakes in the wrong places: Gordon Rodda’s career in invasive species research

When USGS research zoologist Gordon G. Rodda was a graduate student at Cornell University studying behavioral biology of alligators —or later, completing a post-doc at the Smithsonian Institute studying the social behavior of green iguanas in Venezuela or following that, as a statistics and sociobiology instructor at the University of Tennessee—he did not foresee that his professional future was in snakes. Lots of snakes, and in places they don’t belong.

Report

A study of the genetic relationships within and among wolf packs using DNA fingerprinting and mitochondrial DNA

DNA fingerprinting and mitochondrial DNA analyses have not been used in combination to study relatedness in natural populations. We present an approach that involves defining the mean fingerprint similarities among individuals thought to be unrelated because they have different mtDNA genotypes. Two classes of related individuals are identified by their distance in standard errors above this mean value. The number of standard errors is determined by analysis of the association between fingerprint similarity and relatedness in a population with a known genealogy. We apply this approach to gray wolf packs from Minnesota, Alaska, and the Northwest Territories. Our results show that: (1) wolf packs consist primarily of individuals that are closely related genetically, but some packs contain unrelated, non-reproducing individuals; (2) dispersal among packs within the same area is common; and (3) short-range dispersal appears more common for female than male wolves. The first two of these genetically-based observations are consistent with behavioral data on pack structure and dispersal in wolves, while the apparent sex bias in dispersal was not expected.

Behavioral Ecology and Sociobiology

Sex differences in the ontogeny of social behavior in pikas: possible relationships to dispersal and territoriality

A laboratory study on the ontogeny of social behavior in pikas (Ochotona princeps), an alpine lagomorph, was conducted to determine the role of early relationships between adult females and young and among siblings in the development of territorial and dispersal behaviors. Sex differences during development were examined because field studies have reported greater dispersal distances in young females than young males. At birth, females were significantly heavier than males. There were no sex differences in nursing frequency until after the 2nd week of age, when males initiated more nursing attempts than females. By the end of the weaning period (weeks 5 and 6), adult females became non-interactive with young, but aggression of young toward littermates and the mother increased until the eighth week. At this time, young males outweighed their sibling females. Young were dominant over their mothers by the age of 5 weeks, and young males were dominant over their sibling females. Sex differences were observed in aggression, scent-marking, exploratory activity, and submissive vocalizations, with higher rates in young males, except for submissive vocalizations, which were higher in females (Table 2). Vocalizations and scent-marking behavior increased over time, and were positively correlated with interaction rates. These data support the hypothesis that female young disperse farther than male young largely as the result of unsuccessful competition with male siblings for available territories close to the birthplace. A dispersal strategy for pikas is proposed.

Behavioral Ecology and Sociobiology

Wolf pack spacing: Howling as a territory-independent spacing mechanism in a territorial population

Howling is a principle means of spacing in wolf populations. The relationship between a pack's responses to howling (replies, movements) and its location within its home range, was studied using human-simulated howling in a territorial population in northeastern Minnesota. The results indicated the responses were independent of the pack's location, or the locations of the pack and playback relation to the territory center. These results indicate that howling serves as a territory-independent spacing mechanism, that will result in the use of exclusive territories when coupled with strong, year-round site attachment, but with floating, exclusive, buffer-areas about migratory packs.

Behavioral Ecology and Sociobiology

Can non-breeding be a cost of breeding dispersal?

Breeding habitat selection and dispersal are crucial processes that affect many components of fitness. Breeding dispersal entails costs, one of which has been neglected: dispersing animals may miss breeding opportunities because breeding dispersal requires finding a new nesting site and mate, two time- and energy-consuming activities. Dispersers are expected to be prone to non-breeding. We used the kittiwake (Rissa tridactyla) to test whether breeding dispersal influences breeding probability. Breeding probability was associated with dispersal, in that both were negatively influenced by private information (previous individual reproductive success) and public information (average reproductive success of conspecifics) about patch quality. Furthermore, the probability of skipping breeding was 1.7 times higher in birds that settled in a new patch relative to those that remained on the same patch. Finally, non-breeders that resumed breeding were 4.4 times more likely to disperse than birds that bred in successive years. Although private information may influence breeding probability directly, the link between breeding probability and public information may be indirect, through the influence of public information on breeding dispersal, non-breeding thus being a cost of dispersal. These results support the hypothesis that dispersal may result in not being able to breed. More generally, non-breeding (which can be interpreted as an extreme form of breeding failure) may reveal costs of various previous activities. Because monitoring the non-breeding portion of a population is difficult, non-breeders have been neglected in many studies of reproduction trade-offs.

Behavioral Ecology and Sociobiology

Wildlife contact analysis: Emerging methods, questions, and challenges

Recent technological advances, such as proximity loggers, allow researchers to collect complete interaction histories, day and night, among sampled individuals over several months to years. Social network analyses are an obvious approach to analyzing interaction data because of their flexibility for fitting many different social structures as well as the ability to assess both direct contacts and indirect associations via intermediaries. For many network properties, however, it is not clear whether estimates based upon a sample of the network are reflective of the entire network. In wildlife applications, networks may be poorly sampled and boundary effects will be common. We present an alternative approach that utilizes a hierarchical modeling framework to assess the individual, dyadic, and environmental factors contributing to variation in the interaction rates and allows us to estimate the underlying process variation in each. In a disease control context, this approach will allow managers to focus efforts on those types of individuals and environments that contribute the most toward super-spreading events. We account for the sampling distribution of proximity loggers and the non-independence of contacts among groups by only using contact data within a group during days when the group membership of proximity loggers was known. This allows us to separate the two mechanisms responsible for a pair not contacting one another: they were not in the same group or they were in the same group but did not come within the specified contact distance. We illustrate our approach with an example dataset of female elk from northwestern Wyoming and conclude with a number of important future research directions.

Behavioral Ecology and Sociobiology

Sea lamprey orient toward a source of a synthesized pheromone using odor-conditioned rheotaxis

Characterization of vertebrate chemo-orientation strategies over long distances is difficult because it is often not feasible to conduct highly controlled hypothesis-based experiments in natural environments. To overcome the challenge, we couple in-stream behavioral observations of female sea lampreys ( Petromyzon marinus ) orienting to plumes of a synthesized mating pheromone, 7a,12a,24-trihydroxy-5a-cholan-3-one-24-sulfate (3kPZS), and engineering algorithms to systematically test chemo-orientation hypotheses. In-stream field observations and simulated movements of female sea lampreys according to control algorithms support that odor-conditioned rheotaxis is a component of the mechanism used to track plumes of 3kPZS over hundreds of meters in flowing water. Simulated movements of female sea lampreys do not support that rheotaxis or klinotaxis alone is sufficient to enable the movement patterns displayed by females in locating 3kPZS sources in the experimental stream. Odor-conditioned rheotaxis may not only be effective at small spatial scales as previous described in crustaceans, but may also be effectively used by fishes over hundreds of meters. These results may prove useful for developing management strategies for the control of invasive species that exploit the odor-conditioned tracking behavior and for developing biologically inspired navigation strategies for robotic fish.

Behavioral Ecology and Sociobiology

Factors influencing the movement biology of migrant songbirds confronted with an ecological barrier

Whether or not a migratory songbird embarks on a long-distance flight across an ecological barrier is likely a response to a number of endogenous and exogenous factors. During autumn 2008 and 2009, we used automated radio tracking to investigate how energetic condition, age, and weather influenced the departure timing and direction of Swainson’s thrushes ( Catharus ustulatus ) during migratory stopover along the northern coast of the Gulf of Mexico. Most birds left within 1 h after sunset on the evening following capture. Those birds that departed later on the first night or remained longer than 1 day were lean. Birds that carried fat loads sufficient to cross the Gulf of Mexico generally departed in a seasonally appropriate southerly direction, whereas lean birds nearly always flew inland in a northerly direction. We did not detect an effect of age or weather on departures. The decision by lean birds to reorient movement inland may reflect the suitability of the coastal stopover site for deposition of fuel stores and the motivation to seek food among more extensive forested habitat away from the barrier.

Behavioral Ecology and Sociobiology

Inferring social structure and its drivers from refuge use in the desert tortoise, a relatively solitary species

For several species, refuges (such as burrows, dens, roosts, nests) are an essential resource for protection from predators and extreme environmental conditions. Refuges also serve as focal sites for social interactions, including mating, courtship, and aggression. Knowledge of refuge use patterns can therefore provide information about social structure, mating, and foraging success, as well as the robustness and health of wildlife populations, especially for species considered to be relatively solitary. In this study, we construct networks of burrow use to infer social associations in a threatened wildlife species typically considered solitary—the desert tortoise. We show that tortoise social networks are significantly different than null networks of random associations, and have moderate spatial constraints. We next use statistical models to identify major mechanisms behind individual-level variation in tortoise burrow use, popularity of burrows in desert tortoise habitat, and test for stressor-driven changes in refuge use patterns. We show that seasonal variation has a strong impact on tortoise burrow switching behavior. On the other hand, burrow age and topographical condition influence the number of tortoises visiting a burrow in desert tortoise habitat. Of three major population stressors affecting this species (translocation, drought, disease), translocation alters tortoise burrow switching behavior, with translocated animals visiting fewer unique burrows than residents. In a species that is not social, our study highlights the importance of leveraging refuge use behavior to study the presence of and mechanisms behind non-random social structure and individual-level variation. Our analysis of the impact of stressors on refuge-based social structure further emphasizes the potential of this method to detect environmental or anthropogenic disturbances.

Behavioral Ecology and Sociobiology

Increased pheromone signaling by small male sea lamprey has distinct effects on female mate search and courtship

Male body size affects access to mates in many animals. Attributes of sexual signals often correlate with body size due to physiological constraints on signal production. Larger males generally produce larger signals, but costs of being large or compensation by small males can result in smaller males producing signals of equal or greater magnitude. Female choice following multiple male traits with different relationships to size might further complicate the effect of male body size on access to mates. We report the relationship between male body size and pheromone signaling, and the effects on female mate search and courtship in the sea lamprey ( Petromyzon marinus ). We predicted that pheromone production in the liver and the liver mass to body mass ratio would remain constant across sizes, resulting in similar mass-adjusted pheromone release rates across sizes but a positive relationship between absolute pheromone release and body mass. Our results confirmed positive relationships between body mass and liver mass, and liver mass and the magnitude of the pheromone signal. Surprisingly, decreasing body mass was correlated with higher pheromone concentrations in the liver, liver mass to body mass ratios, and mass-adjusted pheromone release rates. In a natural stream, females more often entered nests treated with small versus large male odors. However, close-proximity courtship behaviors were similar in nests treated with small or large male odors. We conclude that small males exhibit increased release of the main pheromone component, but female discrimination of male pheromones follows several axes of variation with different relationships to size.

Behavioral Ecology and Sociobiology

Occurrence of quiescence in free-ranging migratory songbirds

Quiescence is a period of inactivity that occurs before the onset of migratory activity in nocturnally migrating birds. This behavior has been observed in captive birds in migratory disposition, but its occurrence in free-ranging migratory birds has been documented only anecdotally, and causal factors and function(s), if any, are unknown. In this study, we documented and characterized quiescence in three migratory songbird species (red-eyed vireo [ Vireo olivaceus ], Swainson’s thrush [ Catharus ustulatus ], and wood thrush [ Hylocichla mustelina ]) by measuring movement and proportion of time spent inactive prior to departure from a stopover site during fall migration. Individuals of each species displayed a period of inactivity prior to departure which varied from less than 30 min to over 90 min with red-eyed vireos engaged in the longest, most pronounced quiescence. We also examined how quiescence was related to intrinsic and extrinsic factors known to influence the departure of migrating birds, and found some evidence for an effect of age and departure time but no effect of a migrant’s energetic condition, departure direction, atmospheric conditions around departure, or day of year on quiescence. Our novel application of an automated radiotelemetry system yielded a large amount of data to characterize quiescence in free-ranging migratory birds, and we provide guidance for future studies to tease apart the various causal factors and function(s) of this migratory behavior.

Behavioral Ecology and Sociobiology

Testing four hypotheses to explain partial migration: Balancing reproductive benefits with limits to fasting endurance

Seasonal migration is ubiquitous in animals, and yet its underlying cause(s) remain poorly known. Species exhibiting short-distance altitudinal migration and intraspecific variation in migratory behavior (partial or differential migration) are ideal study systems for examining the selective pressures that affect individual migratory decisions. We used an individually marked population of yellow-eyed juncos, breeding along a 1000-m elevational gradient and migrating up and down that gradient, to examine the morphological, behavioral, and reproductive traits associated with migratory behavior. We tested the four most well-known hypotheses proposed to explain partial migration: the thermal tolerance, fasting endurance, dominance, and arrival time hypotheses. Our results indicate that: (1) limits to juncos’ fasting endurance constrain their ability to overwinter at high elevations, in support of the fasting endurance hypothesis, (2) differences in body size mediate fasting ability and are associated with variation in migratory behavior and overwinter apparent survival, (3) migratory behavior interacts with reproductive success, in partial support of the arrival time hypothesis, and (4) additional mechanisms that are not captured by the four well-known hypotheses might better explain individual variation in migratory behavior. Less migratory females achieved greater nesting success the following breeding season. Among males, nesting success influenced migratory tendency the following winter. Successful males may either migrate to a more benign winter climate without paying reproductive costs, or high levels of parental effort might physiologically constrain their ability to overwinter in harsh climates.

Behavioral Ecology and Sociobiology

Daily foraging activity of an imperiled ground squirrel: Effects of hibernation, thermal environment, body condition, and conspecific density

Food acquisition is among the most important tasks faced by free-ranging animals. Predation and thermal risks, however, can make foraging a costly endeavor and foraging can preclude other important activities. Moreover, seasonal life cycle events such as hibernation impose energetic thresholds and time constraints on foraging. These factors interact with an animal’s endogenous state to influence foraging behavior. We tested a suite of predictions based on foraging theory to explore the effects of thermal environment, body condition, and conspecific density on aboveground activity (which is primarily foraging activity) of the northern Idaho ground squirrel ( Urocitellus brunneus ), an imperiled rodent that hibernates for 9 months each year. We took advantage of the squirrels’ semi-fossorial lifestyle to document daily aboveground activity by attaching geolocators to squirrels. We modeled squirrel activity with generalized linear mixed-effects models to document the relative importance of thermal environment, body condition, and conspecific density for daily aboveground activity. Aboveground activity by northern Idaho ground squirrels increased throughout their active season and leaner squirrels increased their activity more than heavier squirrels as residual foraging opportunities diminished. Thermal conditions also influenced squirrel activity: squirrels spent less time above ground during extreme temperatures and on days with significant precipitation. Aboveground activity of northern Idaho ground squirrels largely adhered to predictions of risk-sensitive and state-dependent foraging theory. Management actions that enhance forage will likely improve the probability of recovery for this federally threatened species by minimizing trade-offs squirrels need to make to acquire sufficient food to survive hibernation and reproduce in subsequent years.

Behavioral Ecology and Sociobiology

Offspring sex ratios are male-biased reflecting sex-biased dispersal in Idaho, USA, wolves.

Offspring sex ratios can vary widely across species, and the reasons for such variation have long intrigued ecologists. For group-living animals, predicting offspring sex ratios as a function of group and environmental characteristics can be challenging. Additionally, mortality of group members can upend traditional theory used to explain offspring sex ratios observed in populations. Gray wolves ( Canis lupus ) in Idaho, USA, are an excellent study species for asking questions about offspring sex ratios given their group-living behavior and persistent exposure to human-caused mortality. I hypothesized that offspring sex ratios would be influenced by the characteristics of individuals, groups, and populations. I generated genotypes for 419 adult and 400 pup wolves during 2008–2018. There was a significant male-bias in litters of wolf pups with nearly 12% more male pups born than females. The individual, group, and population variables I considered did not have significant associations with offspring sex ratios. Local resource competition helped explain offspring sex ratios in wolves in my study system, but not local resource enhancement theory. Although female helpers have been shown to help slightly more than males, offspring sex ratios did not favor the helping sex suggesting that the overall benefit of female helpers may have been negligible in wolf groups during my study. Three wolf groups consistently overproduced males, the dispersing sex, suggesting that habitat quality was poor in their territories. The male-biased offspring sex ratios observed throughout this population reflect sex-biased dispersal in wolves in Idaho. Such a pattern suggests breeding females may be reducing local resource competition (e.g., mates and successful reproduction) by producing more males than females.

Idaho

Cook Inlet beluga whale calling varies by group characteristics, behavior, and tidal state

Communication allows social species to exchange information among group members. In aquatic environments, acoustic signals are among the most effective forms of communication and are important for many species, including cetaceans. Beluga whales ( Delphinapterus leucas ) are highly social and vocal, yet little is known about the functionality of their social calls. To examine context-dependent vocal behavior in belugas, we collected passive acoustic data and fine-scale behavioral observations for the endangered Cook Inlet beluga population. The resulting dataset includes 1,720 annotated vocalizations collected over 21 behaviorally encoded encounters. We fit generalized linear mixed models to these data to investigate the effect of behavioral state, group size, calf presence, and tidal state on (1) calling rate (number of calls/minute) and (2) call category (whistles, pulsed calls, combined calls). Belugas were more likely to call when traveling and had higher calling rates during flood tides. Group-level calling rate increased sublinearly with group size, suggesting that individuals called less in larger groups, possibly reflecting increased listening, vocal coordination, or a strategy to avoid acoustic masking. Group calling rate increased before transitions between traveling and milling, suggesting a possible link between communication and behavioral transitions. Whistles were more prevalent when traveling, while pulsed calls were more prevalent when milling. Combined calls occurred only when calves were present, indicating the importance of these calls in communication with calves. Identifying these communication patterns and the contexts in which they occur can enhance our understanding of beluga whale ecology and aid in conservation efforts via passive acoustic monitoring.

Alaska

Family life is critical for migration and survival in a long-lived social bird

Extended parental care is common among birds and particularly well known among long-lived migratory species. Yet, factors influencing the duration of parental care are poorly understood, and empirical evidence for the functional importance of family life for offspring development is scarce. Using unique tracking and genetic data of 55 adult and juvenile migratory Bewick’s swans, among which 18 parent-offspring pairs and 13 sibling pairs, we quantify variation in family bond duration and identify the cause and consequences of their dissolution. Families generally broke up during the second half of the first northward migration of the offspring, when offspring were nearly one year old. Earlier separation occurred on the wintering grounds in response to disturbance ( n = 10 juveniles) and led to delayed migration and, critically, lower survival (40 vs. 86%). Our results provide rare empirical evidence that family bonds, as a pathway for social learning, are not just important, but vital to the migration and survival of young family-living birds.

Behavioral Ecology and Sociobiology

Relative importance of male and territory quality in pairing success of male rock ptarmigan (Lagopus mutus)

We studied pairing success in male rock ptarmigan (Lagopus mutus) in northern Alaska to learn whether males obtaining more females possessed phenotypic traits that influenced female choice directly, whether these traits permitted males to obtain territories favored by females, or whether both processes occurred. The number of females per male varied from zero to three. Several male and territory traits were significantly correlated with number of females per male. We used multiple regression to obtain a single measure of male quality and a single measure of territory quality. These measures of male and territory quality correlated with each other and with male pairing success. We used path analysis to separate direct effects of male quality on pairing success from indirect effects due to high-quality males obtaining high-quality territories. Both direct and indirect pathways had significant effects on pairing success, and direct and indirect effects of male traits on pairing success were about equal. This study illustrates an analytical approach for estimating the relative importance of direct and indirect causal relationships in natural systems.

Behavioral Ecology and Sociobiology

Potential of kaolin-based particle film barriers for Formosan subterranean termite (Isoptera: Rhinotermitidae) control

Effects of three particle film products on Formosan subterranean termites, Coptotermes formosanus Shiraki, were evaluated in feeding, tunneling, and contact assays. The particle films, hydrophobic M96-018 and hydrophilic Surround and Surround WP are based on the inert clay mineral kaolin. In 2-week long no-choice feeding tests, significant mortality occurred only with M96-018-coated wood. When a choice was provided, M96-018 and Surround were consumed at higher rates than untreated wood. Surround WP did not differ from controls in either test. In the tunneling assay termites were given the option of crossing a kaolin-sand mixture to reach an alternate food source. After 3-weeks, rates of 1% and 5% M96-018 provided an effective barrier to Formosan termite tunneling, while termites were not stopped by rates as high as 20% Surround and Surround WP. Dust treatments of all three formulations caused significant increases in mortality within 24 h, with mortality rates ranging from 72.0 - 97.3% within 72 h of treatment. The particle films were most effective when moisture levels were low, suggesting that desiccation was the mechanism for mortality. All particle films showed potential for use in above ground applications while hydrophobic M06-018 has the most potential as a soil barrier to subterranean termites.

Sociobiology