First record of a structural infestation by the bird flea Dasypsyllus gallinulae perpinnatus (Siphonaptera: Ceratophyllidae) in the San Francisco Bay Area, California, USA.

Herein we present the first-known case report of a structural infestation by the bird flea (Dasypsyllus gallinulae perpinnatus) (Dale 1878) in the United States. In March of 2023, the San Mateo County Mosquito and Vector Control District was contacted by a resident in South San Francisco, CA who reported the presence of fleas inside their condominium. The resident had 2 dogs who were on oral flea medication and only 1 inhabitant out of 4 reported receiving flea bites. The front walkway, backyard, and garage were flagged and a small passerine nest was removed from a fire alarm bell in the front walkway. A total of 31 fleas (13 males, 18 females) were collected by flagging from the front entryway underneath the nest. One female flea was collected from the backyard, and 20 (9 males, 11 females) were collected by the resident from inside the house. A total of 387 fleas (163 males, 224 females) were collected from the nest of a small passerine. All life stages (egg, larvae, pupae, and adult) were observed within the nest. Additional parasites in the nest included bird lice and larval western black-legged ticks (Ixodes pacificus, Cooley and Kohls 1943). Research should be conducted into whether bird fleas are capable of transmitting avian pathogens to humans and this information should be communicated to healthcare providers as part of a One Health approach. Additionally, resources to aid in species-level flea identification should be made accessible to pest control operators as this will aid the development of targeted treatments as part of an integrated pest management plan.

Five Years of Surveillance for Tularemia Serovar B (Francisella tularensis holarctica) (Olsufjev) (Thiotrichales: Francisellaceae) Including Two Human Cases at an Endemic Site in San Mateo County, California.

Tularemia is a highly infectious, potentially fatal disease of humans and animals caused by the gram negative, intracellular bacterium Francisella tularensis. The San Mateo County Mosquito and Vector Control District conducted surveillance for F. tularensis from 2017 to 2021 in Dermacentor occidentalis (Marx) (Ixodida: Ixodidae), D. variabilis (Say) (Ixodida: Ixodidae), and Haemaphysalis leporispalustris (Packard) (Ixodida: Ixodidae) ticks in coastal southwestern San Mateo County, California. A total of 3,021 D. occidentalis and 1,019 D. variabilis were collected. Of those, 25 positive pools of F. tularensis were detected (five ticks per pool, overall minimum infection prevalence: 0.62%). Twenty-two of the 25 positive pools (88%) contained D. occidentalis. Eighty-eight percent (88%) of all positive pools were collected from the western half of the site, nearest to the ocean. We did not detect a seasonal effect on the probability of detecting a positive tick pool. There were two human cases of tularemia during the summers of 2019 and 2021. We conducted rodent surveillance in June of 2019, before the human case report. Twenty-four small mammals were collected, but none of their sera tested positive for F. tularensis. It is clear that tularemia is endemic to this region of San Mateo County, but the extent of its range and its ecology is not currently well understood.

Prevalence and Seasonality of Fleas Associated With California Ground Squirrels and the Potential Risk of Tularemia in an Outdoor Non-Human Primate Research Facility.

Ectoparasites at primate research centers may be difficult to control, e.g. without exposing non-human primates (NHPs) to toxicants, but their impact on NHP health is poorly understood. In 2010, there was an epizootic of tularemia at the California National Primate Research Center (CNPRC) in Yolo County, California that resulted in 20 confirmed and suspect clinical cases in outdoors housed rhesus macaques (Macaca mulatta [Zimmermann]) and a 53% seroprevalence in the southern section of the colony. We studied ectoparasite burdens at the CNPRC in order to understand possible conditions at the time of the epizootic and provide data for the management of ectoparasites for the future. In 2015, we recorded 52 California ground squirrel (Otospermophilus beecheyi [Richardson]) burrow systems in the southern colony and collected 560 fleas. The largest number of fleas (n = 184) was collected in October and the most common species were Hoplopsyllus anomalus (Baker) (n = 331), Oropsylla montana (Baker) (n = 158), Echidnophaga gallinacea (Westwood) (n = 60), and Ctenocephalides felis (Bouché) (n = 11), all of which are opportunistically anthropophilic. Free, non-host-associated fleas included 12 H. anomalus, 9 C. felis, 6 O. Montana, and 1 E. gallinacea. We collected 1 H. anomalus from a rhesus macaque. Our results suggest a high potential for the rapid spread of zoonotic infectious diseases via flea transmission in primate facilities with ground squirrels and that flea control measures should be given a high priority.

Abiotic and Biotic Contributors to Support Inter-Epidemic Francisella tularensis in an Agricultural Peri-Urban Environment.

To characterize the inter-epidemic ecology of Francisella tularensis, we surveyed vertebrates and invertebrates for the abundance, spatial distribution, and status of infection at a site in northern California that had evidence of endemic type B tularemia. We collected 2910 mosquitoes, 77 biting flies, 704 ticks, 115 mammals, and 1911 aquatic invertebrates in 2013-2014. Real-time PCR on all mosquitoes, 40 biting flies, 113 aquatic invertebrates, and 650 ticks did not detect F. tularensis DNA. Indirect enzyme linked immunosorbent assay (ELISA) on 109 mammals revealed 2 (of 2, 100%) seropositive feral cats, 1 (of 24, 4.5%) seropositive black rat, and 5 (of 10, 50%) seropositive Virginia opossums. A riparian reserve, ∼1 km from the primate research center, had the highest seroprevalence in mammals and the highest capture success for invertebrate vectors whereas opossums, cats, and ground squirrels in close proximity to the primate center had high seroprevalence and abundant fleas. Well-vegetated regions with standing water appeared to be ideal habitats for biotic components of tularemia enzootic persistence. Mesocarnivores may facilitate the spread of F. tularensis, and high densities of rodents and their fleas may be a mechanism for amplification and spillover.

Are disease reservoirs special? Taxonomic and life history characteristics.

Pathogens that spill over between species cause a significant human and animal health burden. Here, we describe characteristics of animal reservoirs that are required for pathogen spillover. We assembled and analyzed a database of 330 disease systems in which a pathogen spills over from a reservoir of one or more species. Three-quarters of reservoirs included wildlife, and 84% included mammals. Further, 65% of pathogens depended on a community of reservoir hosts, rather than a single species, for persistence. Among mammals, the most frequently identified reservoir hosts were rodents, artiodactyls, and carnivores. The distribution among orders of mammalian species identified as reservoirs did not differ from that expected by chance. Among disease systems with high priority pathogens and epidemic potential, we found birds, primates, and bats to be overrepresented. We also analyzed the life history traits of mammalian reservoir hosts and compared them to mammals as a whole. Reservoir species had faster life history characteristics than mammals overall, exhibiting traits associated with greater reproductive output rather than long-term survival. Thus, we find that in many respects, reservoirs of spillover pathogens are indeed special. The described patterns provide a useful resource for studying and managing emerging infectious diseases.

Rodent-Pika Parasite Spillover in Western North America.

Competition during the Cenozoic expansion of the Rodentia may have contributed to ecological niche reduction of pikas, which are now increasingly under threat as their habitat degrades under global climate change, while some rodents expand their ranges and overlap with pikas. Range overlap carries the possibility of disease spillover. Contemporary North American pikas are cold-adapted and relegated primarily to alpine environments where they subsist on relatively low-quality herbaceous diet. Yet their evolutionary ancestors were distributed geographically even into the subtropics. Here we examine historical and contemporary records of fleas on pikas (Ochotona princeps) from sites at different elevations in the Sierra Nevada and Rocky Mountains and the Pacific Northwest. We calculated indices of diversity from each site and spillover fraction, i.e., the proportion of fleas on pikas that have a preference for rodents. Across this range there are four pika specialist flea species, with no more than two of these per site, and 18 characteristically rodent flea species. Diversity is greatest in the Pacific Northwest and lowest in Montana. Rodent flea spillover onto pikas declines with elevation in the Rocky Mountains. These data provide evidence that rodents and pikas interact enough to allow considerable parasite spillover, and which could be exacerbated as pikas are increasingly stressed by climate change at lower elevations some rodent species expand up-elevation in the face of increasing global warming. With global climate change, both biotic and abiotic niche shrinkage demand our attention.

A Molecular Survey for Francisella tularensis and Rickettsia spp. in Haemaphysalis leporispalustris (Acari: Ixodidae) in Northern California.

Francisella tularensis and Rickettsia spp. have been cultured from Haemaphysalis leporispalustris Packard, but their prevalence in this tick has not been determined using modern molecular methods. We collected H. leporispalustris by flagging vegetation and leaf litter and from lagomorphs (Lepus californicus Gray and Sylvilagus bachmani (Waterhouse)) in northern California. Francisella tularensis DNA was not detected in any of 1,030 ticks tested by polymerase chain reaction (PCR), whereas 0.4% of larvae tested in pools, 0 of 117 individual nymphs, and 2.3% of 164 adult ticks were PCR-positive for Rickettsia spp. Positive sites were Laurel Canyon Trail in Tilden Regional Park in Alameda Contra Costa County, with a Rickettsia spp. prevalence of 0.6% in 2009, and Hopland Research and Extension Center in Mendocino County, with a prevalence of 4.2% in 1988. DNA sequencing revealed R. felis, the agent of cat-flea typhus, in two larval pools from shaded California bay and live oak leaf litter in Contra Costa County and one adult tick from a L. californicus in chaparral in Mendocino County. The R. felis in unfed, questing larvae demonstrates that H. leporispalustris can transmit this rickettsia transovarially. Although R. felis is increasingly found in diverse arthropods and geographical regions, prior literature suggests a typical epidemiological cycle involving mesocarnivores and the cat flea, Ctenocephalides felis. To our knowledge, this is the first report of R. felis in H. leporispalustris. Natural infection and transovarial transmission of this pathogen in the tick indicate the existence of a previously undocumented wild-lands transmission cycle that may intersect mesocarnivore-reservoired cycles and collectively affect human health risk.

Bacterial flora on Cascades frogs in the Klamath mountains of California.

Amphibians are experiencing global declines due in part to the infectious disease chytridiomycosis. Some symbiotic bacteria residents on frog skin have been shown to inhibit the growth of Batrachochytrium dendrobatitis (Bd) but few studies have attempted to fully describe the resident bacterial flora of frog skin. We cultured and sequenced 130 bacterial isolates from frogs collected from the California Klamath Range, recovering predominantly Gram-negative bacteria from 20 higher order taxa and 31 genera. There were also a large number of unclassifiable isolates. Forty-three isolates were assessed for their ability to inhibit the growth of Bd in vitro; of these, two had strong and three had slight anti-Bd activity. We suggest that many bacterial species may play a secondary role in Bd resistance, acting synergistically with inhibitory species. Future research is required in order to characterize these interactions. Understanding the relationships between bacterial strains may be important in predicting and managing the effects of future anti-Bd treatments such as antimicrobial compounds or probiotic bacteria.

Investigation of tularemia outbreak after natural infection of outdoor-housed rhesus macaques (Macaca mulatta) with Francisella tularensis.

In the summer and fall of 2010, a series of outdoor-housed rhesus macaques were diagnosed with tularemia. PCR analysis or positive culture confirmed 11 cases, and 9 additional animals with similar clinical signs responded to empiric antibiotic treatment. A serosurvey conducted in the 9 mo after the outbreak found 53% (43 of 81 macaques) seropositivity in the southern outdoor colony, which had an average population of 700 animals. A prospective survey of small mammal reservoirs and arthropod vectors was conducted during the late summer and fall of 2011. PCR analyses of tissues from all 135 mice, 18 ground squirrels, 1 rat, 3 raccoons, 2 cats, and 3 jackrabbits and their fleas were negative for DNA of Francisella tularensis. Conventional PCR evaluation of stored DNA from affected macaques identified the causative organism as F. tularensis subsp. holartica. DNA evaluated from historic cases of tularemia in nonhuman primates confirmed that the organism that infected the colony during the late 1980s likewise was F. tularensis subsp. holartica. The macaque tularemia epizootic of 2010 appears to have been an extreme example of the periodic resurgence of tularemia. No evidence of rodent disease was found in the immediate vicinity during the 2011 interepizootic period. The concurrent widespread seropositivity (53%) and low incidence of clinical disease (2.7%) in 2010 suggests that this strain of Francisella has low pathogenicity in macaques.

Cryptic seedling herbivory by nocturnal introduced generalists impacts survival, performance of native and exotic plants.

Although much of the theory on the success of invasive species has been geared at escape from specialist enemies, the impact of introduced generalist invertebrate herbivores on both native and introduced plant species has been underappreciated. The role of nocturnal invertebrate herbivores in structuring plant communities has been examined extensively in Europe, but less so in North America. Many nocturnal generalists (slugs, snails, and earwigs) have been introduced to North America, and 96% of herbivores found during a night census at our California Central Valley site were introduced generalists. We explored the role of these herbivores in the distribution, survivorship, and growth of 12 native and introduced plant species from six families. We predicted that introduced species sharing an evolutionary history with these generalists might be less vulnerable than native plant species. We quantified plant and herbivore abundances within our heterogeneous site and also established herbivore removal experiments in 160 plots spanning the gamut of microhabitats. As 18 collaborators, we checked 2000 seedling sites every day for three weeks to assess nocturnal seedling predation. Laboratory feeding trials allowed us to quantify the palatability of plant species to the two dominant nocturnal herbivores at the site (slugs and earwigs) and allowed us to account for herbivore microhabitat preferences when analyzing attack rates on seedlings. The relationship between local slug abundance and percent cover of five common plant taxa at the field site was significantly negatively associated with the mean palatability of these taxa to slugs in laboratory trials. Moreover, seedling mortality of 12 species in open-field plots was positively correlated with mean palatability of these taxa to both slugs and earwigs in laboratory trials. Counter to expectations, seedlings of native species were neither more vulnerable nor more palatable to nocturnal generalists than those of introduced species. Growth comparison of plants within and outside herbivore exclosures also revealed no differences between native and introduced plant species, despite large impacts of herbivores on growth. Cryptic nocturnal predation on seedlings was common and had large effects on plant establishment at our site. Without intensive monitoring, such predation could easily be misconstrued as poor seedling emergence.