Charles B. Yackulic

Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis.

Circadian rhythms in physiology and behavior are controlled by pacemaker cells located in the suprachiasmatic nucleus (SCN) of the hypothalamus. The mammalian SCN can be classified into two subdivisions (core and shell) based on the organization of neuroactive substances, inputs, and outputs. Recent studies in our laboratory indicate that these subdivisions are associated with functional specialization in Syrian hamsters. The core region, marked by calbindin‐D28K (CalB)‐containing cells, expresses light‐induced, but not rhythmic, clock genes. In the shell compartment, marked by vasopressinergic cells and fibers, clock gene expression is rhythmic. Given these findings, an important question is how photic and rhythmic information are integrated and communicated from each of these regions to effector areas. The present study used localized, intra‐SCN iontophoretic injections of the anterograde tracer biotinylated dextran amine (BDA) to investigate intra‐SCN connectivity and the neural pathways by which information is communicated from SCN subregions to targets. Intra‐SCN connections project from the core to the shell compartment of the SCN, but not from the shell to the CalB region of the SCN. Retrograde tracing experiments were performed using cholera toxin‐β (CTB) to determine more specifically whether SCN efferents originated in the core or shell using neurochemical markers for the rhythmic (vasopressin) and light‐induced (CalB) SCN subregions. The combined results from anterograde and retrograde experiments suggest that all SCN targets receive information from both the light‐induced and rhythmic regions of the SCN (albeit to varying degrees) and indicate that light and rhythmic information may be integrated both within the SCN and at target effector areas. J. Comp. Neurol. 468:361–379, 2004.

Influence of land use on water quality in a tropical landscape: a multi-scale analysis

There is a pressing need to understand the consequences of human activities, such as land transformations, on watershed ecosystem services. This is a challenging task because different indicators of water quality and yield are expected to vary in their responsiveness to large versus local-scale heterogeneity in land use and land cover (LUC). Here we rely on water quality data collected between 1977 and 2000 from dozens of gauge stations in Puerto Rico together with precipitation data and land cover maps to (1) quantify impacts of spatial heterogeneity in LUC on several water quality indicators; (2) determine the spatial scale at which this heterogeneity influences water quality; and (3) examine how antecedent precipitation modulates these impacts. Our models explained 30–58% of observed variance in water quality metrics. Temporal variation in antecedent precipitation and changes in LUC between measurements periods rather than spatial variation in LUC accounted for the majority of variation in water quality. Urbanization and pasture development generally degraded water quality while agriculture and secondary forest re-growth had mixed impacts. The spatial scale over which LUC influenced water quality differed across indicators. Turbidity and dissolved oxygen (DO) responded to LUC in large-scale watersheds, in-stream nitrogen concentrations to LUC in riparian buffers of large watersheds, and fecal matter content and in-stream phosphorus concentration to LUC at the sub-watershed scale. Stream discharge modulated impacts of LUC on water quality for most of the metrics. Our findings highlight the importance of considering multiple spatial scales for understanding the impacts of human activities on watershed ecosystem services.

Isolation by environmental distance in mobile marine species: molecular ecology of franciscana dolphins at their southern range

The assessment of population structure is a valuable tool for studying the ecology of endangered species and drafting conservation strategies. As we enhance our understanding about the structuring of natural populations, it becomes important that we also understand the processes behind these patterns. However, there are few rigorous assessments of the influence of environmental factors on genetic patterns in mobile marine species. Given their dispersal capabilities and localized habitat preferences, coastal cetaceans are adequate study species for evaluating environmental effects on marine population structure. The franciscana dolphin, a rare coastal cetacean endemic to the Western South Atlantic, was studied to examine these issues. We analysed genetic data from the mitochondrial DNA and 12 microsatellite markers for 275 franciscana samples utilizing frequency‐based, maximum‐likelihood and Bayesian algorithms to assess population structure and migration patterns. This information was combined with 10 years of remote sensing environmental data (chlorophyll concentration, water turbidity and surface temperature). Our analyses show the occurrence of genetically isolated populations within Argentina, in areas that are environmentally distinct. Combined evidence of genetic and environmental structure suggests that isolation by distance and a process here termed isolation by environmental distance can explain the observed correlations. Our approach elucidated important ecological and conservation aspects of franciscana dolphins, and has the potential to increase our understanding of ecological processes influencing genetic patterns in other marine species.

The roles of competition and habitat in the dynamics of populations and species distributions.

The role of competition in structuring biotic communities at fine spatial scales is well known from detailed process-based studies. Our understanding of competitions importance at broader scales is less resolved and mainly based on static species distribution maps. Here, we bridge this gap by examining the joint occupancy dynamics of an invading species (Barred Owl, Strix varia) and a resident species (Northern Spotted Owl, Strix occidentalis caurina) in a 1000-km study area over a 22-year period. Past studies of these competitors have focused on the dynamics of one species at a time, hindering efforts to parse out the roles of habitat and competition and to forecast the future of the resident species. In addition, while these studies accounted for the imperfect detection of the focal species, no multi-season analysis of these species has accounted for the imperfect detection of the secondary species, potentially biasing inference. We analyzed survey data using models that combine the general multistate-multi-season occupancy modeling framework with autologistic modeling, allowing us to account for important aspects of our study system. We found that local extinction probability increases for each species when the other is present; however, the effect of the invader on the resident is greater. Although the species prefer different habitats, these habitats are highly correlated at the patch scale, and the impacts of invader on the resident are greatest in patches that would otherwise be optimal. As a consequence, competition leads to a weaker relationship between habitat and Northern Spotted Owl occupancy. Colonization and extinction rates of the invader are closely related to neighborhood occupancy, and over the first half of the study the availability of colonists limited the rate of population growth. Competition is likely to exclude the resident species, both through its immediate effects on local extinction and by indirectly lowering colonization rates as Northern Spotted Owl occupancy declines. Our analysis suggests that dispersal limitation affects both the invasion dynamics and the scale at which the effects of competition are observed. We also provide predictions regarding the potential costs and benefits of managing Barred Owl populations at different target levels.

Anthropogenic and environmental drivers of modern range loss in large mammals

The extinction of a species is inevitably preceded by the extirpation of a series of local populations. Ecological theory predicts that vulnerability to extirpation varies between populations and is ultimately linked to environmental heterogeneity. If populations of a species are present in multiple regions separated by abrupt changes in environmental conditions (e.g., biomes), spatial variation in vulnerability to extirpation may be closely linked to the distribution of these regions. In the absence of abrupt shifts in environmental conditions, populations at the edge of a species’ range should have low growth rates and be more vulnerable to extirpation, whereas populations located in the core of the species’ range should be exposed to more favorable environmental conditions, have higher growth rates, and be less vulnerable. Here, we ask whether the distribution of biomes or range position better reflects spatial variation in vulnerability for 43 mammal species distributed through four continents. We control for the distribution of human threats and quantify the importance of protected areas in population persistence. We conclude that the distribution of biomes is a better predictor of vulnerability than position in the geographic range. We also find that core populations are less vulnerable than edge populations (after controlling for threats levels and protected areas). Protected areas are important for the persistence of most species we studied. By providing a measure of vulnerability linked directly to the distribution of threats, our results offer insights for scaling up from species vulnerability to extinction risk.

Neighborhood and habitat effects on vital rates: expansion of the Barred Owl in the Oregon Coast Ranges

In this paper, we modify dynamic occupancy models developed for detection-nondetection data to allow for the dependence of local vital rates on neighborhood occupancy, where neighborhood is defined very flexibly. Such dependence of occupancy dynamics on the status of a relevant neighborhood is pervasive, yet frequently ignored. Our framework permits joint inference about the importance of neighborhood effects and habitat covariates in determining colonization and extinction rates. Our specific motivation is the recent expansion of the Barred Owl (Strix varia) in western Oregon, USA, over the period 1990-2010. Because the focal period was one of dramatic range expansion and local population increase, the use of models that incorporate regional occupancy (sources of colonists) as determinants of dynamic rate parameters is especially appropriate. We began our analysis of 21 years of Barred Owl presence/nondetection data in the Tyee Density Study Area (TDSA) by testing a suite of six models that varied only in the covariates included in the modeling of detection probability. We then tested whether models that used regional occupancy as a covariate for colonization and extinction outperformed models with constant or year-specific colonization or extinction rates. Finally we tested whether habitat covariates improved the AIC of our models, focusing on which habitat covariates performed best, and whether the signs of habitat effects are consistent with a priori hypotheses. We conclude that all covariates used to model detection probability lead to improved AIC, that regional occupancy influences colonization and extinction rates, and that habitat plays an important role in determining extinction and colonization rates. As occupancy increases from low levels toward equilibrium, colonization increases and extinction decreases, presumably because there are more and more dispersing juveniles. While both rates are affected, colonization increases more than extinction decreases. Colonization is higher and extinction is lower in survey polygons with more riparian forest. The effects of riparian forest on extinction rates are greater than on colonization rates. Model results have implications for management of the invading Barred Owl, both through habitat alteration and removal.

Vegetation dynamics drive segregation by body size in Galapagos tortoises migrating across altitudinal gradients

Seasonal migration has evolved in many taxa as a response to predictable spatial and temporal variation in the environment. Individual traits, physiology and social state interact with environmental factors to increase the complexity of migratory systems. Despite a huge body of research, the ultimate causes of migration remain unclear. A relatively simple, tractable system - giant tortoises on Santa Cruz Island, Galapagos, was studied to elucidate the roles of environmental variation and individual traits in a partial migratory system. Specifically, we asked: (i) do Galapagos tortoises undergo long-distance seasonal migrations? (ii) is tortoise migration ultimately driven by gradients in forage quality or temperature; and (iii) how do sex and body size influence migration patterns? We recorded the daily locations of 17 GPS-tagged tortoises and walked a monthly survey along the altitudinal gradient to characterize the movements and distribution of tortoises of different sizes and sexes. Monthly temperature and rainfall data were obtained from weather stations deployed at various altitudes, and the Normalized Difference Vegetation Index was used as a proxy for forage quality. Analyses using net displacement or daily movement characteristics did not agree on assigning individuals as either migratory or non-migratory; however, both methods suggested that some individuals were migratory. Adult tortoises of both sexes move up and down an altitudinal gradient in response to changes in vegetation dynamics, not temperature. The largest tagged individuals all moved, whereas only some mid-sized individuals moved, and the smallest individuals never left lowland areas. The timing of movements varied with body size: large individuals moved upward (as lowland forage quality declined) earlier in the year than did mid-sized individuals, while the timing of downward movements was unrelated to body size and occurred as lowland vegetation productivity peaked. Giant tortoises are unlikely candidates for forage-driven migration as they are well buffered against environmental fluctuations by large body size and a slow metabolism. Notably the largest, and presumably most dominant, individuals were most likely to migrate. This characteristic and the lack of sex-based differences in movement behaviour distinguish Galapagos tortoise movement from previously described partial migratory systems.

Biophysical and Socioeconomic Factors Associated with Forest Transitions at Multiple Spatial and Temporal Scales

Forest transitions (FT) occur when socioeconomic development leads to a shift from net deforestation to reforestation; these dynamics have been observed in multiple countries across the globe, including the island of Puerto Rico in the Caribbean. Starting in the 1950s, Puerto Rico transitioned from an agrarian to a manufacturing and service economy reliant on food imports, leading to extensive reforestation. In recent years, however, net reforestation has leveled off. Here we examine the drivers of forest transition in Puerto Rico from 1977 to 2000 at two subnational, nested spatial scales (municipality and barrio) and over two time periods (1977-1991 and 1991-2000). This study builds on previous work by considering the social and biophysical factors that influence both reforestation and deforestation at multiple spatial and temporal scales. By doing so within one analysis, this study offers a comprehensive understanding of the relative importance of various social and biophysical factors for forest transitions and the scales at which they are manifest. Biophysical factors considered in these analyses included slope, soil quality, and land-cover in the surrounding landscape. We also considered per capita income, population density, and the extent of protected areas as potential factors associated with forest change. Our results show that, in the 1977-1991 period, biophysical factors that exhibit variation at municipality scales (~100 km²) were more important predictors of forest change than socioeconomic factors. In this period, forest dynamics were driven primarily by abandonment of less productive, steep agricultural land in the western, central part of the island. These factors had less predictive power at the smaller barrio scale (~10 km²) relative to the larger municipality scale during this time period. The relative importance of socioeconomic variables for deforestation, however, increased over time as development pressures on available land increased. From 1991-2000, changes in forest cover reflected influences from multiple factors, including increasing population densities, land development pressure from suburbanization, and the presence of protected areas. In contrast to the 1977-1991 period, drivers of deforestation and reforestation over this second interval were similar for the two spatial scales of analyses. Generally, our results suggest that although broader socioeconomic changes in a given region may drive the demand for land, biophysical factors ultimately mediate where development occurs. Although economic development may initially result in reforestation due to rural to urban migration and the abandonment of agricultural lands, increased economic development may lead to deforestation through increased suburbanization pressures.

The spatial structure of hunter access determines the local abundance of forest elephants (Loxodonta africana cyclotis).

In many previously remote regions in the world, increasing and often unregulated access is leading to dramatic increases in hunting pressure and declines in the densities of prey species, sometimes to the point of local extinction. Not surprisingly, numerous studies have found a correlation between the distance to the closest access point and prey densities. Here we hypothesized that, for many wide-ranging species, local abundances are reduced by hunting associated with multiple access points as opposed to just the closest access points. We also hypothesized that the distribution of hunter access determines both patterns of occupancy and abundance in occupied areas and that these two patterns (occupancy and abundance) respond to access at different spatial scales. Using data on the distribution of abundances of African forest elephant (Loxodonta africana cyclotis) in and around five national parks in Central Africa, we tested these hypotheses using a model comparison framework. We found that models including an index based on the distance to multiple roads outperformed models including other access-based covariates, including a model based on distance to the closest road only. We also found that models that allowed us to model occupancy and abundance separately outperformed simpler models. Occupancy responds to access at the same scale as previous estimates of average maximum displacement in the subspecies, while the scale of the response of abundance is more ambiguous, but appears to be greater. Lastly, we show that incorporating indices based on multiple access points and modeling abundance and occupancy has important practical consequences for our understanding of overall regional abundances and the distribution of abundances within regions.

A quantitative life history of endangered humpback chub that spawn in the Little Colorado River: variation in movement, growth, and survival.

While the ecology and evolution of partial migratory systems (defined broadly to include skip spawning) have been well studied, we are only beginning to understand how partial migratory populations are responding to ongoing environmental change. Environmental change can lead to differences in the fitness of residents and migrants, which could eventually lead to changes in the frequency of the strategies in the overall population. Here, we address questions concerning the life history of the endangered Gila cypha (humpback chub) in the regulated Colorado River and the unregulated tributary and primary spawning area, the Little Colorado River. We develop eight multistate models for the population based on three movement hypotheses, in which states are defined in terms of fish size classes and river locations. We fit these models to mark–recapture data collected in 2009–2012. We compare survival and growth estimates between the Colorado River and Little Colorado River and calculate abundances for all size classes. The best model supports the hypotheses that larger adults spawn more frequently than smaller adults, that there are residents in the spawning grounds, and that juveniles move out of the Little Colorado River in large numbers during the monsoon season (July–September). Monthly survival rates for G. cypha in the Colorado River are higher than in the Little Colorado River in all size classes; however, growth is slower. While the hypothetical life histories of life-long residents in the Little Colorado River and partial migrants spending most of its time in the Colorado River are very different, they lead to roughly similar fitness expectations when we used expected number of spawns as a proxy. However, more research is needed because our study period covers a period of years when conditions in the Colorado River for G. cypha are likely to have been better than has been typical over the last few decades.