The functional microclimate of an urban arthropod pest: Urban heat island temperatures in webs of the western black widow spider.

Urbanization alters natural landscapes and creates unique challenges for urban wildlife. Similarly, the Urban Heat Island (UHI) effect can produce significantly elevated temperatures in urban areas, and we have a relatively poor understanding of how this will impact urban biodiversity. In particular, most studies quantify the UHI using broad-scale climate data rather than assessing microclimate temperatures actually experienced by organisms. In addition, studies often fail to address spatial and temporal complexities of the UHI. Here we examine the thermal microclimate and UHI experienced in the web of Western black widow spiders (Latrodectus hesperus), a medically-important, superabundant urban pest species found in cities across the Western region of North America. We do this using replicate urban and desert populations across an entire year to account for seasonal variation in the UHI, both within and between habitats. Our findings reveal a strong nighttime, but no daytime, UHI effect, with urban spider webs being 2-5 °C warmer than desert webs at night. This UHI effect is most prominent during the spring and least prominent in winter, suggesting that the UHI need not be most pronounced when temperatures are most elevated. Urban web temperatures varied among urban sites in the daytime, whereas desert web temperatures varied among desert sites in the nighttime. Finally, web temperature was significantly positively correlated with a spider's boldness, but showed no relationship with voracity towards prey, web size, or body condition. Understanding the complexities of each organism's thermal challenges, the "functional microclimate", is crucial for predicting the impacts of urbanization and climate change on urban biodiversity and ecosystem functioning.

Ecdysteroid responses to urban heat island conditions during development of the western black widow spider (Latrodectus hesperus).

The steroid hormone 20-hydroxyecdysone (20E) controls molting in arthropods. The timing of 20E production, and subsequent developmental transitions, is influenced by a variety of environmental factors including nutrition, photoperiod, and temperature, which is particularly relevant in the face of climate change. Environmental changes, combined with rapid urbanization, and the increasing prevalence of urban heat islands (UHI) have contributed to an overall decrease in biodiversity making it critical to understand how organisms respond to elevating global temperatures. Some arthropods, such as the Western black widow spider, Latrodectus hesperus, appear to thrive under UHI conditions, but the physiological mechanism underlying their success has not been explored. Here we examine the relationship between hemolymph 20E titers and spiderling development under non-urban desert (27°C), intermediate (30°C), and urban (33°C) temperatures. We found that a presumptive molt-inducing 20E peak observed in spiders at non-urban desert temperatures was reduced and delayed at higher temperatures. Intermolt 20E titers were also significantly altered in spiders reared under UHI temperatures. Despite the apparent success of black widows in urban environments, we noted that, coincident with the effects on 20E, there were numerous negative effects of elevated temperatures on spiderling development. The differential effects of temperature on pre-molt and intermolt 20E titers suggest distinct hormonal mechanisms underlying the physiological, developmental, and behavioral response to heat, allowing spiders to better cope with urban environments.

Urban heat island conditions experienced by the Western black widow spider (Latrodectus hesperus): Extreme heat slows development but results in behavioral accommodations.

While shifts in organismal biology stemming from climate change are receiving increased attention, we know relatively little about how organisms respond to other forms of anthropogenic disturbance. The urban heat island (UHI) effect describes the capture of heat by built structures (e.g. asphalt), resulting in elevated urban temperatures. The UHI is a well-studied phenomenon, but only a handful of studies have investigated trait-based shifts resulting from the UHI, and even fewer have attempted to quantify the magnitude of the UHI experienced at the microclimate scale. Here, using a common urban exploiter, the Western black widow spider (Latrodectus hesperus), we show that the UHI experienced by spiders in July in their urban Phoenix, AZ refuges is 6°C hotter (33°C) than conditions in the refuges of spiders from Sonoran Desert habitat outside of Phoenix's development (27°C). We then use this field microclimate UHI estimate to compare the development speed, mass gain and mortality of replicate siblings from 36 urban lineages reared at 'urban' and 'desert' temperatures. We show that extreme heat is slowing the growth of spiderlings and increasing mortality. In contrast, we show that development of male spiders to their penultimate moult is accelerated by 2 weeks. Lastly, in terms of behavioral shifts, UHI temperatures caused late-stage juvenile male spiders to heighten their foraging voracity and late-stage juvenile female spiders to curtail their web-building behavior. Trait-based approaches like the one presented herein help us better understand the mechanisms that lead to the explosive population growth of urban (sometimes invasive) species, possibly at the expense of urban biodiversity. Studies of organismal responses to the present day UHI can be used as informative surrogates that help us grasp the impact that projected climate change will have on biodiversity.

Juvenile social experience generates differences in behavioral variation but not averages.

Developmental plasticity is known to influence the mean behavioral phenotype of a population. Yet, studies on how developmental plasticity shapes patterns of variation within populations are comparatively rare and often focus on a subset of developmental cues (e.g., nutrition). One potentially important but understudied developmental experience is social experience, as it is explicitly hypothesized to increase variation among individuals as a way to promote "social niches." To test this, we exposed juvenile black widow spiders (Latrodectus hesperus) to the silk of conspecifics by transplanting them onto conspecific webs for 48 h once a week until adulthood. We also utilized an untouched control group as well as a disturbed group. This latter group was removed from their web at the same time points as the social treatment, but was immediately placed back on their own web. After repeatedly measuring adult behavior and web structure, we found that social rearing drove higher or significant levels of repeatability relative to the other treatments. Repeatability in the social treatment also decreased in some traits, paralleling the decreases observed in the disturbed treatments. Thus, repeated juvenile disturbance may decrease among-individual differences in adult spiders. Yet, social rearing appeared to override the effect of disturbance in some traits, suggesting a prioritization effect. The resulting individual differences were maintained over at least one-third of the adult lifespan and thus appear to represent stable, canalized developmental effects and not temporal state differences. These results provide proximate insight into how a broader range of developmental experiences shape trait variation.

Urbanization as a facilitator of gene flow in a human health pest.

Urban fragmentation can reduce gene flow that isolates populations, reduces genetic diversity and increases population differentiation, all of which have negative conservation implications. Alternatively, gene flow may actually be increased among urban areas consistent with an urban facilitation model. In fact, urban adapter pests are able to thrive in the urban environment and may be experiencing human-mediated transport. Here, we used social network theory with a population genetic approach to investigate the impact of urbanization on genetic connectivity in the Western black widow spider, as an urban pest model of human health concern. We collected genomewide single nucleotide polymorphism variation from mitochondrial and nuclear double-digest RAD (ddRAD) sequence data sets from 210 individuals sampled from 11 urban and 10 nonurban locales across its distribution of the Western United States. From urban and nonurban contrasts of population, phylogenetic, and network analyses, urban locales have higher within-population genetic diversity, lower between-population genetic differentiation and higher estimates of genetic connectivity. Social network analyses show that urban locales not only have more connections, but can act as hubs that drive connectivity among nonurban locales, which show signatures of historical isolation. These results are consistent with an urban facilitation model of gene flow and demonstrate the importance of sampling multiple cities and markers to identify the role that urbanization has had on larger spatial scales. As the urban landscape continues to grow, this approach will help determine what factors influence the spread and adaptation of pests, like the venomous black widow spider, in building policies for human and biodiversity health.

Behavioral syndromes: an intergrative overiew.

A behavioral syndrome is a suite of correlated behaviors expressed either within a given behavioral context (e.g., correlations between foraging behaviors in different habitats) or across different contexts (e.g., correlations among feeding, antipredator, mating, aggressive, and dispersal behaviors). For example, some individuals (and genotypes) might be generally more aggressive, more active or bold, while others are generally less aggressive, active or bold. This phenomenon has been studied in detail in humans, some primates, laboratory rodents, and some domesticated animals, but has rarely been studied in other organisms, and rarely examined from an evolutionary or ecological perspective. Here, we present an integrative overview on the potential importance of behavioral syndromes in evolution and ecology. A central idea is that behavioral correlations generate tradeoffs; for example, an aggressive genotype might do well in situations where high aggression is favored, but might be inappropriately aggressive in situations where low aggression is favored (and vice versa for a low aggression genotype). Behavioral syndromes can thereby result in maladaptive behavior in some contexts, and potentially maintain individual variation in behavior in a variable environment. We suggest terminology and methods for studying behavioral syndromes, review examples, discuss evolutionary and proximate approaches for understanding behavioral syndromes, note insights from human personality research, and outline some potentially important ecological implications. Overall, we suggest that behavioral syndromes could play a useful role as an integrative bridge between genetics, experience, neuroendocrine mechanisms, evolution, and ecology.

Behavioral syndromes: an ecological and evolutionary overview.

Recent studies suggest that populations and species often exhibit behavioral syndromes; that is, suites of correlated behaviors across situations. An example is an aggression syndrome where some individuals are more aggressive, whereas others are less aggressive across a range of situations and contexts. The existence of behavioral syndromes focuses the attention of behavioral ecologists on limited (less than optimal) behavioral plasticity and behavioral carryovers across situations, rather than on optimal plasticity in each isolated situation. Behavioral syndromes can explain behaviors that appear strikingly non-adaptive in an isolated context (e.g. inappropriately high activity when predators are present, or excessive sexual cannibalism). Behavioral syndromes can also help to explain the maintenance of individual variation in behavioral types, a phenomenon that is ubiquitous, but often ignored. Recent studies suggest that the behavioral type of an individual, population or species can have important ecological and evolutionary implications, including major effects on species distributions, on the relative tendencies of species to be invasive or to respond well to environmental change, and on speciation rates. Although most studies of behavioral syndromes to date have focused on a few organisms, mainly in the laboratory, further work on other species, particularly in the field, should yield numerous new insights.