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Robert Reed

Publications and source records attributed to Robert Reed.

At least 19 recordsLinked to original sources

Demographic responses to experimental manipulation of an enclosed population of invasive brown treesnakes (Boiga irregularis)

Understanding how invasive species populations respond to perturbations can give insight into effective management. However, opportunities to test theoretical population responses are rare, as experimental perturbations often run counter to management goals (e.g., suppression). On the island of Guam, a 5-ha outdoor enclosure (with no immigration or emigration) constructed in 2003 serves as a unique population-scale study area for invasive brown treesnakes ( Boiga irregularis ). Capture-mark-recapture studies (CMR) and several experiments have taken place since 2004. Here, we analyze a subset of the CMR data collected between 2008 and 2012, a time period encompassing two experimental perturbations: (1) supplemental feeding to determine if the population is food limited and (2) targeted removal of adult and large-subadult cohorts to quantify the timing and magnitude of the population's demographic response to a simulated control effort. We used the CMR data to fit a Pradel model in a Bayesian framework to compare the population growth rate, survival probability, and recruitment rate prior to, during, and post perturbations. We found that increasing food resources increased population growth and recruitment rates, but that survival remained relatively constant. The removal perturbation resulted in a decrease in population growth rate and survival immediately after the removal, but population growth rate and recruitment began increasing 1 year after the removal perturbation. Our results suggest that brown treesnakes in the enclosed population are prey limited, likely constraining population growth, and that the suppression of population growth after removal of adults and large sub-adults is short-lived (i.e., less than a year).

Guam

Reproductive condition of an invasive snake in urban, savanna, and forest habitats

Predation by Brown Treesnakes ( Boiga irregularis ) has caused the decline or extinction of all native forest vertebrates on Guam, including birds, lizards, and bats. Loss of the highest-quality prey has caused shifts in Brown Treesnake size and life history. We sought to understand how reproductive condition varies among habitats island-wide, particularly comparing urban and savanna habitats (where some primarily non-native large prey remain) with prey-depauperate forest habitats. We dissected 100 snakes from each of 18 sites stratified by 6 habitat types and calculated a body condition index, relative follicle size (for females; N = 817) and relative testes size (for males; N = 992) for each. Low detection of reproductive females continues to hamper research on their biology, as only 11% of females had secondary vitellogenic follicles (N = 89). Although variation among sites within habitats was high, above-average reproductive development of both males and females was most frequently observed in urban and savanna habitats, emphasizing the potential for prey subsidies in these habitats to fuel population growth and affect invasive snake management objectives. Furthermore, the trade-off between body condition and reproductive condition appeared to be more severe in forested habitats and less severe in urban habitats for both males and females. There were few obvious seasonal patterns, although there was a slightly lower probability of females having secondary vitellogenic follicles in the wet season compared to the dry season.

NeoBiota

Growth rate variation in Brown Treesnakes (Boiga irregularis): An invasive species of conservation concern

Somatic growth rate is a fundamental trait that influences metabolism, lifespan and reproductive maturity and is critical for understanding population dynamics and informing management actions. Brown Treesnakes ( Boiga irregularis ) introduced to Guam are highly invasive and can reproduce year-round without discrete cohorts. We compared snake size trajectories described by the conventionally used von Bertalanffy growth function versus the Gompertz model. Using quantile regression with a regularized effect for individual snakes we modeled growth rates of 270 marked, wild snakes as a function of size. The Gompertz model explained more of the variation in growth and rendered more realistic predictions of asymptotic sizes than did the von Bertalanffy model. With the Gompertz model, growth rates were 1.05–1.16× faster in males than in females. Females reached asymptotic sizes at shorter snout-vent lengths than males. Growth rate was positively correlated with amount of precipitation, and modeling wet-dry seasonality on Guam as a sinusoidal function identified a growth peak in September—October. Effects of seasonality and precipitation, however, were minor compared to individual and sex related differences in size-adjusted growth rates. We estimated that the 50th (and 5th, 95th) growth-rate percentile males in our study population become sexually mature at an age of 33 (∞, 15) months, while females mature at 41 (∞, 18) months, where ∞ indicates that the slowest growing snakes never reach maturity. However, 50% of the snakes mature at a size below the median, and age at maturity may be as low as 10.4 (males) and 13.7 (females) months for average-sized hatchlings that grow fast. Our results have implications for the timing of management options for this species and our approach can be broadly applied to animals where repeated growth data are obtained and age is unknown.

Ecology and Evolution

Vertebrates in trade that pose high invasion risk to the United States

The United States imports thousands of live vertebrate species annually as part of legal trade. Escapes and releases from captivity are major pathways of invasion, however, the risk posed by the thousands of imported vertebrate species has not been systematically assessed. We conducted a horizon scan that used a data-driven climate match to filter a list of nearly 15,000 taxa drawn from across the globe of imported fish, amphibians, reptiles, birds, and mammals for rapid assessment by taxonomic experts. Experts evaluated 840 species and identified 32 (22 reptiles and 10 fishes) as having the highest risk for establishment, spread, and negative impacts. Of those high-risk species, the majority have the capacity to disrupt ecosystem processes via their role as top predators or the unique ecological niches that they occupy, while several of the snake species pose a threat to human health. High-risk species were often scored with high confidence while in contrast, low scores were attributed to a combination of ecological redundancy, low propagule pressure, or low climate match while low confidence arose from a lack of information in the literature (i.e., data deficiency). Our study therefore highlights legally imported species likely to cause the greatest harm with the recognition that many other species could also become invasive in the United States. The ranked list of vertebrate threats can be used to prioritize watchlists and inform the development of targeted regulations for importation can be applied to regions to provide a rapid, preliminary screening for large pools of potential invaders.

Biological Conservation

Identifying invasive species threats, pathways, and impacts to improve biosecurity

Managing invasive species with prevention and early-detection strategies can avert severe ecological and economic impacts. Horizon scanning, an evidence-based process combining risk screening and consensus building to identify threats, has become a valuable tool for prioritizing invasive species management and prevention. We assembled a working group of experts from academic, government, and nonprofit agencies and organizations, and conducted a multi-taxa horizon scan for Florida, USA, the first of its kind in North America. Our primary objectives were to identify high-risk species and their introduction pathways, to detail the magnitude and mechanism of potential impacts, and, more broadly, to demonstrate the utility of horizon scanning. As a means to facilitate future horizon scans, we document the process used to generate the list of taxa for screening. We evaluated 460 taxa for their potential to arrive, establish, and cause negative ecological and socioeconomic impacts, and identified 40 potential invaders, including alewife, zebra mussel, crab-eating macaque, and red swamp crayfish. Vertebrates and aquatic invertebrates posed the greatest invasion threat, over half of the high-risk taxa were omnivores, and there was high confidence in the scoring of high-risk taxa. Common arrival pathways were ballast water, biofouling of vessels, and escape from the pet/aquarium/horticulture trade. Competition, predation, and damage to agriculture/forestry/aquaculture were common impact mechanisms. We recommend full risk analysis for the high-risk taxa; increased surveillance at Florida's ports, state borders, and high-risk pathways; and periodic review and revision of the list. Few horizon scans detail the comprehensive methodology (including list-building), certainty estimates for all scoring categories and the final score, detailed pathways, and the magnitude and mechanism of impact. Providing this information can further inform prevention efforts and can be efficiently replicated in other regions. Moreover, harmonizing methodology can facilitate data sharing and enhance interpretation of results for stakeholders and the general public.

Ecosphere

Burmese pythons in Florida: A synthesis of biology, impacts, and management tools

Burmese pythons ( Python molurus bivittatus ) are native to southeastern Asia, however, there is an established invasive population inhabiting much of southern Florida throughout the Greater Everglades Ecosystem. Pythons have severely impacted native species and ecosystems in Florida and represent one of the most intractable invasive-species management issues across the globe. The difficulty stems from a unique combination of inaccessible habitat and the cryptic and resilient nature of pythons that thrive in the subtropical environment of southern Florida, rendering them extremely challenging to detect. Here we provide a comprehensive review and synthesis of the science relevant to managing invasive Burmese pythons. We describe existing control tools and review challenges to productive research, identifying key knowledge gaps that would improve future research and decision making for python control.

Florida

Divergent Serpentoviruses in free-ranging invasive pythons and native colubrids in southern Florida, United States

Burmese python ( Python bivittatus ) is an invasive snake that has significantly affected ecosystems in southern Florida, United States. Aside from direct predation and competition, invasive species can also introduce nonnative pathogens that can adversely affect native species. The subfamily Serpentovirinae (order Nidovirales ) is composed of positive-sense RNA viruses primarily found in reptiles. Some serpentoviruses, such as shingleback nidovirus, are associated with mortalities in wild populations, while others, including ball python nidovirus and green tree python nidovirus can be a major cause of disease and mortality in captive animals. To determine if serpentoviruses were present in invasive Burmese pythons in southern Florida, oral swabs were collected from both free-ranging and long-term captive snakes. Swabs were screened for the presence of serpentovirus by reverse transcription PCR and sequenced. A total serpentovirus prevalence of 27.8% was detected in 318 python samples. Of the initial swabs from 172 free-ranging pythons, 42 (24.4%) were positive for multiple divergent viral sequences comprising four clades across the sampling range. Both sex and snout-vent length were statistically significant factors in virus prevalence, with larger male snakes having the highest prevalence. Sampling location was statistically significant in circulating virus sequence. Mild clinical signs and lesions consistent with serpentovirus infection were observed in a subset of sampled pythons. Testing of native snakes (n = 219, 18 species) in part of the python range found no evidence of python virus spillover; however, five individual native snakes (2.3%) representing three species were PCR positive for unique, divergent serpentoviruses. Calculated pairwise uncorrected distance analysis indicated the newly discovered virus sequences likely represent three novel genera in the subfamily Serpentovirinae. This study is the first to characterize serpentovirus in wild free-ranging pythons or in any free-ranging North America reptile. Though the risk these viruses pose to the invasive and native species is unknown, the potential for spillover to native herpetofauna warrants further investigation.

Florida

Size distribution and reproductive phenology of the invasive Burmese python (Python molurus bivittatus) in the Greater Everglades Ecosystem, Florida, USA

The design of successful invasive species control programs is often hindered by the absence of basic demographic data on the targeted population. Establishment of invasive Burmese pythons ( Python molurus bivittatus ) in the Greater Everglades Ecosystem, Florida USA has led to local precipitous declines (> 90%) of mesomammal populations and is also a major threat to native populations of reptiles and birds. Efforts to control this species are ongoing but are hampered by the lack of access to and information on the expected biological patterns of pythons in southern Florida. We present data from more than 4,000 wild Burmese pythons that were removed in southern Florida over 26 years (1995–2021), the most robust dataset representing this invasive population to date. We used these data to characterize Burmese python size distribution, size at maturity, clutch size, and seasonal demographic and reproductive trends. We broadened the previously described size ranges by sex and, based on our newly defined size-stage classes, showed that males are smaller than females at sexual maturity, confirmed a positive correlation between maternal body size and potential clutch size, and developed predictive equations to facilitate demographic predictions. We also refined the annual breeding season (approx.100 days December into March), oviposition timing (May), and hatchling emergence and dispersal period (July through October) using correlations of capture morphometrics with observations of seasonal gonadal recrudescence (resurgence) and regression. Determination of reproductive output and timing can inform population models and help managers arrest population growth by targeting key aspects of python life history. These results define characteristics of the species in Florida and provide an enhanced understanding of the ecology and reproductive biology of Burmese pythons in their invasive Everglades range.

Florida

Invasive brown treesnakes (Boiga irregularis) move short distances and have small activity areas in a high prey environment

Animal movements reflect temporal and spatial availability of resources as well as when, where, and how individuals access such resources. To test these relationships for a predatory reptile, we quantified the effects of prey abundance on the spatial ecology of invasive brown treesnakes ( Boiga irregularis ) on Guam. Five months after toxicant-mediated suppression of a brown treesnake population, we simultaneously used visual encounter surveys to generate relative rodent abundance and radiotelemetry of snakes to document movements of surviving snakes. After snake suppression, encounter rates for small mammals increased 22-fold and brown treesnakes had smaller mean daily movement distances (24 ± 13 m/day, x ¯ "> x ± SD) and activity areas (5.47 ± 5 ha) than all previous observations. Additionally, snakes frequenting forest edges, where our small mammal encounters were the highest, had smaller mean daily movement distances and three-dimensional activity volumes compared to those within the forest interior. Collectively, these results suggest that reduced movements by snakes were in part a response to increased prey availability. The impact of prey availability on snake movement may be a management consideration when attempting to control cryptic invasive species using tools that rely on movement of the target species to be effective,

Guam

Egg retention in wild-caught Python bivittatus in the Greater Everglades Ecosystem, Florida, USA

Retention of eggs in oviducts beyond the normal oviposition period is a common problem for captive reptiles, but the occurrence of egg retention in wild populations is largely unknown. The Burmese python ( Python [molurus] bivittatus ; Kühl 1820) is an oviparous snake native to south-eastern Asia that is now established in southern Florida. From 2011–2019, invasive Burmese pythons were opportunistically removed from Everglades National Park and Big Cypress National Preserve, humanely euthanised, and necropsied to determine reproductive condition. A total of 258 females of reproductive size were found to exhibit various stages of oviposition which generally aligned with purported annual reproductive timing. However, we encountered five pythons during the post-ovulatory period (Aug–Feb) showing signs of recent oviposition with retained eggs. Most of these cases comprised a small number of retained eggs, likely representing some portion of the total clutch. Because this condition is nearly absent in wild animal literature, our observations suggest retained eggs in wild snakes may be more common than previously assumed, possibly slowing or otherwise impacting population growth. However, we recognise that for an invasive species like the Burmese python in Florida, the egg retention rate may be higher in the non-native range compared to the native range due to maladaptation to novel habitats or environmental conditions. Additional research is needed to determine the exact causes of egg retention and investigate the implications for population dynamics on this and other snake species.

Florida

Clutch may predict growth of hatchling Burmese pythons better than food availability or sex

Identifying which environmental and genetic factors affect growth pattern phenotypes can help biologists predict how organisms distribute finite energy resources in response to varying environmental conditions and physiological states. This information may be useful for monitoring and managing populations of cryptic, endangered, and invasive species. Consequently, we assessed the effects of food availability, clutch, and sex on the growth of invasive Burmese pythons ( Python bivittatus Kuhl) from the Greater Everglades Ecosystem in Florida, USA. Though little is known from the wild, Burmese pythons have been physiological model organisms for decades, with most experimental research sourcing individuals from the pet trade. Here, we used 60 hatchlings collected as eggs from the nests of two wild pythons, assigned them to High or Low feeding treatments, and monitored growth and meal consumption for 12 weeks, a period when pythons are thought to grow very rapidly. None of the 30 hatchlings that were offered food prior to their fourth week post-hatching consumed it, presumably because they were relying on internal yolk stores. Although only two clutches were used in the experiment, we found that nearly all phenotypic variation was explained by clutch rather than feeding treatment or sex. Hatchlings from clutch 1 (C1) grew faster and were longer, heavier, in better body condition, ate more frequently, and were bolder than hatchlings from clutch 2 (C2), regardless of food availability. On average, C1 and C2 hatchling snout-vent length (SVL) and weight grew 0.15 cm d −1 and 0.10 cm d −1 , and 0.20 g d −1 and 0.03 g d −1 , respectively. Additional research may be warranted to determine whether these effects remain with larger clutch sample sizes and to identify the underlying mechanisms and fitness implications of this variation to help inform risk assessments and management.

Biology Open

Olfactory lures in predator control do not increase predation risk to birds in areas of conservation concern

Context: Lethal control of predators is often undertaken to protect species of conservation concern. Traps are frequently baited to increase capture efficacy, but baited traps can potentially increase predation risk by attracting predators to protected areas. This is especially important if targeted predators can escape capture due to low trap success. Snake traps using live mouse lures may be beneficial if traps effectively remove snakes in the presence of birds and do not attract additional snakes to the area. Aims: The present study evaluated whether mouse-lure traps in areas occupied by birds (simulated by deploying bird-lure traps) could influence predation risk from an invasive snake on Guam. Methods: Snake traps were used, with Japanese quail ( Coturnix japonica ) as a proxy for predation risk, to assess if an adjacent trap with a mouse ( Mus musculus ) would attract brown treesnakes ( Boiga irregularis ) to a focal area and increase contact between an invasive snake and avian prey. Catch per unit effort (CPUE) at stations containing either a bird-lure trap, mouse-lure trap or pair of traps (i.e. one bird-lure and one mouse-lure trap) was evaluated. Key results: Bird-lure traps paired with mouse-lure traps did not differ in CPUE from isolated bird-lure traps. At paired stations, CPUE of snakes in mouse-lure traps was 2.3× higher than bird-lure traps, suggesting mouse lures were capable of drawing snakes away from avian prey. Bird-lure traps at paired stations experienced a decay in captures over time, whereas CPUE for isolated bird-lure traps increased after 9 weeks and exceeded mouse-lure traps after 7 weeks. Conclusions: Mouse lures did not increase the risk of snakes being captured in bird-lure traps. Instead, mouse-lure traps may have locally suppressed snakes, whereas stations without mouse-lure traps still had snakes in the focal area, putting avian prey at greater risk. However, snakes caught with bird lures tended to be larger and in better body condition, suggesting preference for avian prey over mammalian prey in larger snakes. Implications: Strategic placement of olfactory traps within areas of conservation concern may be beneficial for protecting birds of conservation concern from an invasive snake predator.

Wildlife Research

Identifying negative sentiment polarity in the Judas technique

In the context of conservation science and management, the Judas technique refers to outfitting an animal (a Judas animal) with a radio transmitter or other identifier so that its movements can be tracked to locate conspecifics. Although this term is commonly used, some consider it offensive due to historical associations of the word Judas with anti-Semitic sentiments. Thus, the term has a negative sentiment polarity (i.e., the assertion that words can have positive, negative, or neutral connotations). We investigated the etymology of the Judas term in peer-reviewed scientific literature to outline its contextual introduction and use. Prior to the term being co-opted by conservation scientists Judas [animal] was a common term in the livestock industry to describe animals used to lead herds to slaughter. Subsequently, the term has been published and promulgated through conservation-related research and the literature. Due to a negative sentiment polarity linked to this term, especially among members of the public, alternative nomenclature may be preferred to increase objective and dispassionate scientific communication.

Conservation Science and Practice

Range eclipse leads to tenuous survival of a rare lizard species on a barrier atoll

Rediscovery of living populations of a species that was presumed to be extirpated can generate new narratives for conservation in areas suffering from losses in biodiversity. We used field observations and DNA sequence data to verify the rediscovery of the Critically Endangered scincid lizard Emoia slevini on Dåno′, an islet off the coast of Guam in the southern Mariana Islands, where for > 20 years it had been considered possibly extirpated. Endemic to the Marianas, E. slevini has declined throughout its range and no longer occurs on as many as five islands from which it was historically known, most likely because of interactions with invasive species and loss of native forest. Our results show that individuals from Dåno′, the type locality for E. slevini , are genetically similar but not identical to E. slevini on Sarigan and Alamagan to the north, and that E. slevini is a close evolutionary relative to another congener in the southern Marianas that is currently recognized as E moia atrocostata but probably represents an undescribed species in this archipelago. We also show that other, more broadly distributed species of Emoia occurring on Dåno′ are distant relatives to E. slevini and the Mariana lineage of E. atrocostata , providing further evidence of the distinctiveness of these taxa. The rediscovery of E. slevini on Dåno′ following rodent eradication and culling of a population of monitor lizards suggests that management of invasive species is key to the recovery of this skink in the Mariana Islands, and that a range eclipse on the larger neighbouring island of Guam best explains why the rediscovery took place at the periphery of the species’ historic range. A Chamorro abstract can be found in the supplementary material.

Dåno′, Guam

Thermal stability of an adaptable, invasive ectotherm: Argentine giant tegus in the Greater Everglades ecosystem, USA

Invasive species globally threaten biodiversity and economies, but the ecophysiological mechanisms underlying their success are often understudied. For those alien species that also exhibit high phenotypic plasticity, such as habitat generalists, adaptations in response to environmental pressures can take place relatively quickly. The Argentine giant tegu ( Salvator merianae ; tegu) is a large omnivorous lizard from South America that is prolific, long-lived, vagile, and highly adaptable to disturbed environments. They are well suited to the climate of southeastern United States, introduced to several disjunct areas, including the Everglades, where their voracious appetite threatens native wildlife. Tegus undergo winter dormancy (hibernation) to cope with colder temperatures, and while this behavior may facilitate invasion into more temperate regions, it may also present management opportunities. We studied the thermal habits of wild S. merianae within their invaded range in southern Florida, USA. We used radiotelemetry and trail cameras to verify aboveground behaviors, and temperature dataloggers to monitor surface (sun-exposed [ T e ] and shaded [ T s ]), ambient ( T a ), subsurface ground ( T h ), and internal body ( T b ) temperatures of a population of free-ranging tegus over several seasons. We evaluated thermal and behavioral data and identified five biologically significant periods: pre-hibernal, hibernal, cold snaps, hibernal-basking, and post-hibernal. We found tegus maintained thermal stability throughout the hibernal period, frequently at temperatures above available thermal microhabitats. Variation in T b was lowest during hibernation and cold snaps and was less variable than subsurface temperatures despite not leaving their hibernaculum. Hibernal ingress and egress were best predicted by temperature differentials between exposed soil and ambient daily mean temperatures ( T e − T a ) and daylength. Though we detected no sex differences, larger animals started hibernation sooner, stayed in hibernation longer, and retained higher fat stores over the study period. One individual did not hibernate, representing only the second record of this behavior. Despite limitations of these descriptive data, this is the first study finely detailing T b of a population of wild, free-ranging S. merianae over multiple biologically significant time periods and to associate T b with thermal habitats within its invasive range. Tegus' apparent ability for thermal stability expands the adaptability breadth of this species and underscores the invasion threat.

Florida

Invaders from islands: Thermal matching, potential or flexibility?

Native-range thermal constraints may not reflect the geographical distributions of species introduced from native island ranges in part due to rapid physiological adaptation in species introduced to new environments. Correlative ecological niche models may thus underestimate potential invasive distributions of species from islands. The northern curly-tailed lizard ( Leiocephalus carinatus ) is established in Florida, including populations north of its native range. Competing hypotheses may explain this distribution: Thermal Matching (distribution reflects thermal conditions of the native range), Thermal Potential (species tolerates thermal extremes absent in the native range) and/or Thermal Flexibility (thermal tolerance reflects local thermal extremes). We rejected the Thermal Matching hypothesis by comparing ecological niche models developed from native vs. native plus invasive distributions; L. carinatus exists in areas of low suitability in Florida as predicted by the native-distribution model. We then compared critical thermal limits of L. carinatus from two non-native populations to evaluate the Thermal Potential and Flexibility hypotheses: one matching native range latitudes, and another 160 km north of the native range that experiences more frequent cold weather events. Critical thermal minima in the northern population were lower than in the south, supporting the Thermal Flexibility hypothesis, whereas critical thermal maxima did not differ.

Florida