Research Article |
Corresponding author: Shane R. Siers ( shane.r.siers@usda.gov ) Academic editor: Jonathan Jeschke
© 2024 Shane R. Siers, Melia G. Nafus, Jeried E. Calaor, Rachel M. Volsteadt, Matthew S. Grassi, Megan Volsteadt, Aaron F. Collins, Patrick D. Barnhart, Logan T. Huse, Amy A. Yackel Adams, Diane L. Vice.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Siers SR, Nafus MG, Calaor JE, Volsteadt RM, Grassi MS, Volsteadt M, Collins AF, Barnhart PD, Huse LT, Yackel Adams AA, Vice DL (2024) Limitations of invasive snake control tools in the context of a new invasion on an island with abundant prey. NeoBiota 90: 1-33. https://doi.org/10.3897/neobiota.90.103041
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In October 2020, a new population of invasive brown treesnakes (Boiga irregularis) was discovered on the 33-ha Cocos Island, 2.5 km off the south coast of Guam. Cocos Island is a unique conservation resource, providing refuge for many lizards and birds, including endangered species, which were extirpated from mainland Guam by invasive predators including brown treesnakes. We sought to evaluate the usefulness of toxic baiting with acetaminophen-treated carrion baits and cage trapping, common tools for the control of brown treesnakes on mainland Guam, as potential eradication tools on Cocos Island. We evaluated multiple bait types and bait presentations: on the ground, suspended in the canopy emulating aerial bait applications and in four plastic-tube bait station configurations intended to exclude non-target species. We monitored all baits with time-lapse cameras. Despite improved exclusion of non-targets by bait station design, most baits were quickly removed by non-target species, particularly coconut crabs (Birgus latro) and Mariana monitors (Varanus tsukamotoi). Monitoring of 1,250 baits available for 2,427 bait nights resulted in no observations of brown treesnakes taking any bait. Subsequently, we tested two trap types commonly used on Guam and compared trapping success with live versus dead mouse lures. In 10,553 trap nights using live and dead mouse lures, we only captured one brown treesnake, in a trap with a live mouse lure. These baiting and trapping rates are so low as to be ineffectual for all practical purposes. Concurrent visual searching and hand capture of brown treesnakes during initial rapid response efforts demonstrates that these low baiting and trapping success rates are not a result of low snake density. We make a case for our assumption that the ineffectiveness of these tools on Cocos Island is due to the context of extremely high abundance of preferred live prey, primarily large geckos and birds. Our results have profound conservation ramifications, because any future island invasions by brown treesnakes are likely to occur within similarly prey-rich environments where these baiting and trapping methods might be similarly ineffective.
bait stations, Boiga irregularis, camera traps, conservation, eradication feasibility, incipient population, non-target species, trapping
The pace and scale of the introduction and spread of non-native reptiles continues to increase, as does recognition of the attendant ecological and economic harms they cause (
The most well-known and well-studied example of an island snake invasion is that of the brown treesnake (Boiga irregularis) on the island of Guam in the Western Pacific. Accidentally transported from the Admiralty Islands to Guam in shipments of military equipment following World War II (
Methods and strategies for brown treesnake control are being developed, tested and implemented for the protection and restoration of Guam’s native flora and fauna (e.g.
Cocos Island (CHamoru name: Islan Dåno’) is a small atoll island situated approximately 2.5 km off the southern tip of the main island of Guam. Cocos Island was considered to comprise the majority of remaining snake-free habitat in Guam and is home to many vertebrates susceptible to brown treesnake predation, including some species that no longer persist on mainland Guam. Guam rails (Hypotaenidia owstoni: ko’ko’), once extinct in the wild due to brown treesnake predation, were introduced to Cocos Island where they have reproduced and thrived (
While the high volume of commercial and military cargo and vessels originating from central and northern Guam has been scrupulously inspected for stowaway snakes, traffic between southern Guam and Cocos Island has received relatively little attention. A biosecurity plan was developed for the Island (
In October 2020, a local fisherperson reported killing snakes on Cocos Island during a night-time visit to the atoll. Subsequent search efforts by the U.S. Geological Survey’s (USGS) Brown Treesnake Rapid Response Team (RRT;
Several tools and techniques have been developed and continue to be improved for management of invasive brown treesnakes on Guam (
Since the early 1990s, live trapping with cage traps has been the primary method of brown treesnake removal and continues to be a foundational tool for research and management programmes (
It is important to conduct pilot evaluations of the utility of potential control tools to establish their effectiveness prior to substantial investments in planning eradication projects (
Cocos Island (33.6 ha; Fig.
Map of Cocos Island 2.5 km from the southern tip of Guam, USA. Orange lines indicate locations of trails used for bait applications and trapping. The top of the image is orientated to the north. Image: Maxar Intelligence 2021.
The north-eastern 80% of the Island is under private ownership and the south-western 20% is owned by the Government of Guam and managed by the Guam Department of Parks and Recreation. The Island is uninhabited, but Cocos Island Resort operates as a day resort offering water-sports, trail walks and food and beverages. The resort closed when the Governor of Guam declared an island-wide public emergency shutdown in response to the COVID-19 pandemic on 13 March 2020. The resort has not yet reopened since then.
To minimise disturbance of threatened and endangered species present on the Island, our activities were limited to the edges of existing cart paths and footpaths as per the conditions of our U.S. Fish and Wildlife Service Endangered Species Act consultation (Fig.
We sought to evaluate the relative merits of a variety of potential baits and bait presentation methods on Cocos Island. Preliminary evidence from mainland Guam indicates that brown treesnakes with recent experience feeding on birds may be preferentially attracted to dead bird baits over dead rodents (
Dead animal baits used in this study. Left to right: 4–6-g dead neonatal mouse (DNM); 10–17-g small mouse (SM); 18–35-g large mouse (LM); 10–14-g small bird (quail chick, SB); and 25–35-g large bird (chicken chick, LB).
Canopy presentation: USDA Wildlife Services has engineered an Aerial Delivery System (ADS) for the automated assembly and aerial distribution of bait cartridges containing a DNM treated with a tablet containing 80 mg of acetaminophen (
Camera orientations for canopy and ground bait monitoring A infrared camera set-up mimicking aerial application of dead neonatal mouse (DNM) baits via the USDA Wildlife Services Aerial Delivery System (ADS) for landscape-scale brown treesnake control; the camera and bait are elevated into the forest canopy atop a telescoping painter’s pole B ground bait monitoring set-up, with an infrared camera mounted directly over a large mouse (LM) bait on a tripod constructed from extruded metal tubing (conduit); the bait and a lightweight PVC background with circular size standards were lashed to a 0.9-kg lead diving weight to prevent small crabs from dragging the bait out of the camera’s field of view.
Ground presentation: As some ADS baits fail to tangle in the canopy or DNM may become unstuck from the cartridge and fall through to the forest floor, we sought to evaluate the fate of DNM on the ground. Additionally, recent evidence indicates that ADS treatments might not adequately expose large brown treesnakes to baits; larger brown treesnakes on prey-depleted Guam are more prone to foraging on the ground, might be preferentially attracted to larger baits and might require greater doses of acetaminophen for effective removal (
Bait station presentations: Polyvinyl chloride (PVC) tube bait stations (‘bait tubes’) are intended to exclude non-target species that might interfere with baits, making them unavailable to brown treesnakes and to protect native species from unintentional exposure to acetaminophen intoxication. Standard operational baiting methods include placing a DNM treated with a tablet containing 80 mg of acetaminophen into a 5-cm diameter, 30-cm long PVC bait tube, with 6.35-mm bolts crossing the openings at the ends to further prevent ingress by non-targets. Bait tubes are usually suspended horizontally by two lengths of paracord from existing vegetation or structures, such as fence lines (
Camera orientations and bait station configurations for bait monitoring A standard 5-cm diameter × 30-cm long polyvinyl chloride (PVC) horizontal bait station suspended by nylon paracord from a wooden dowel armature with infrared camera positioned with the bait in the field of view; the two ends of the armature are temporarily lashed to natural vegetation with elastic cords B extended 5 × 45-cm horizontal bait tube C capped 5 × 30-cm vertical bait tube D capped 10 × 30-cm vertical bait tube. Baits in horizontal bait tubes were held in place by gravity, while baits were held in the caps of vertical bait tubes by spring clamps on one foot of the bait. As baits in vertical bait tubes were not visible to the camera, a length of biodegradable flagging was tied to one leg of the bait and pulled through a small hole in the side of the tube for ease of identifying when the bait was taken during camera image review.
We suspended all bait station types by paracord from a wooden dowel armature to which the trail camera was affixed, locking the bait in the FOV of the camera. We temporarily attached these armatures to existing vegetation by elastic cords, with minor vegetation pruning to ensure that leaves or branches did not obstruct the view of the bait. We placed baits in the centre of horizontal tubes where they were held in place by gravity and friction alone. Within vertical bait tubes, we attached baits within the caps clipping one foot with a small metal spring clamp, holding baits in place, but making them easily removed with a slight tug from snakes or non-targets. As cameras could not directly view baits in the vertical tubes, we tied a length of white biodegradable flagging tape to one leg of each bait and pulled the tape through a small hole in the side of the tube; when the bait was removed, the flag disappeared and the animal within the FOV of the camera at that time was attributed with the bait removal.
As bait stations offered some degree of protection from non-target interference, we treated baits in bait stations with tablets containing 80 mg of acetaminophen inserted into the body of the bait via the oral cavity, to remove any brown treesnakes that took baits.
We spaced bait placements at approximately 20-m intervals along existing paths and trails on Cocos Island (Fig.
This portion of the study was performed during Guam’s cooler, drier months. Average daily temperatures for Guam ranged from highs of 30.4 °C (standard deviation = 0.903 °C) to lows of 24.7 °C (SD = 1.03 °C) and rainfall averaged 2.16 mm/day (SD = 5.3 mm/day, max = 48 mm/day), based on National Oceanic and Atmospheric Administration data (www.weather.gov).
After years of experimentation with multiple live trap designs, a modified crayfish or minnow trap was adopted as the standard brown treesnake live trap used on Guam. The original trap is a two-piece dual-funnel design of galvanised wire mesh with the entrances modified with a PVC ring holding a one-way wire mesh flap that allows access to the trap body, but blocks escape by snakes (Fig.
Two types of traps used. Left: Galvanised wire mesh two-piece trap with separate live mouse lure chamber within the trap body. Centre: Stainless steel one-piece Wildlife Services Standard trap with integrated live mouse lure chamber. Right: Integrated lure chamber in one-piece trap showing live mouse, feed block of pellets and seeds immersed in paraffin wax and piece of fresh potato to provide moisture; mice in both trap types are provisioned in this manner.
The use of live mouse lures is less than desirable due to maintenance expense and perceptions regarding animal welfare; however, despite extensive efforts, no trap lure has been found to be nearly as effective and practical as a live mouse (
To evaluate differences in efficacy and durability between trap types and capture success between live and dead mouse lures, we alternated 99 one-piece WS Standard and 99 original two-piece traps approximately every 20 m along the same existing trails as the previous baiting trials (Fig.
We monitored a subset of 20 traps via infrared game cameras (Hyperfire 2, Reconyx, Holmen, Wisconsin). We distributed 10 cameras evenly along a rock retaining wall and another 10 along a transect through a bird roosting area. We positioned half of these cameras on traps with live mouse lures and the other half on traps with dead mice. We recorded time-lapse images (one photo every 60 seconds) between 1800 and 0600 h to observe for brown treesnakes investigating traps, but failing to enter, as has been documented on mainland Guam (
We performed trapping from 17 June to 12 August, 2021, earlier months of Guam’s warmer, rainier season. Guam daytime highs averaged 31.4 °C (SD = 1.04) with night-time lows of 25.6 °C (SD = 0.969) and rainfall of 9.22 mm/day (SD = 13.5mm, max = 71.9mm) (www.weather.gov). We measured snout-vent length (SVL, mm) of trapped snakes by gently stretching them along a flexible tape and measured weight using handheld spring scales with maximum ranges from 10 g (0.1 g precision) to 1000 g (10 g precision) (Pesola, Schindellegi, Switzerland). We determined sex by probing for inverted hemipenes with steel sexing probes (
Throughout the evaluation of control tools, USGS conducted nocturnal visual searches and hand-removal of brown treesnakes (December 2020 through July 2021). Methods followed those applied on Guam in which individuals surveyed transects after dusk using powerful headlamps (Wilma, Lupine Lighting System, Lebanon, PA, USA) walking a slow searcher pace, such that each transect (~ 400 m) lasted approximately 1 hour. During snake searches, observations of potential prey items (lizards, birds and bats) were recorded. Visual survey data are available for download (
All summary statistics, statistical tests and graphing were performed in the R environment for statistical computing, Version 4.2.2 (
This study was carried out in compliance with relevant laws and guidelines. All animal use was approved by the USDA National Wildlife Research Center Institutional Animal Care and Use Committee under protocols QA-3106 and QA-3340 and USGS Institutional Animal Care and Use Committee protocol 2021-02. Compliance with the Endangered Species Act was ensured through informal consultation with the U. S. Fish and Wildlife Service (01EPIF00-2021-I-0087 and 01EPIF00-2021-I-0087-R001).
After eliminating incomplete trials (camera failure etc.), we successfully monitored a total of 1,250 baits between December 2020 and April 2021. During these trials, we observed no baits being investigated or taken by brown treesnakes. As there were no bait takes by brown treesnakes, we could not make comparisons of bait take rates amongst bait types or presentation types. Of the 701 baits that were taken, we could not identify the species in 30 (4.3%) of the cases. The 95% binomial confidence interval for brown treesnake takes for the 671 baits for which a species ID was confirmed is 0–0.548%; if this rate were applied to the 30 unknown takes, the upper confidence limit for brown treesnake bait takes would be 0.164 baits; thus, we consider it highly unlikely that any of the unknown animals taking these 30 baits was a brown treesnake.
A high overall proportion of the baits (56.1%) were taken by non-target species (Fig.
Fates of carrion baits applied on Cocos Island. No brown treesnakes were observed taking any baits. DNM = dead neonatal mouse (4–6 g); SM = small mouse (10–14 g); LM = large mouse (25–35 g); SB = small birds (10–14 g quail chick); LB = large bird (25–35 g chicken chick). Sample size is the number of baits successfully monitored after eliminating incomplete trials.
Coconut crabs and Mariana monitors were by far the most common consumers of baits. Plotting the recorded time of bait takes by coconut crabs and Mariana monitors (Fig.
Times of bait removal by the primary non-target consumers on Cocos Island. Most baits were removed by coconut crabs (Birgus latro) and Mariana monitors (Varanus tsukamotoi). Light grey strips indicate changes in sunrise and sunset over the study period.
We recorded the duration of bait availability before being taken by non-targets or removed at the end of the trial and subjected these data to survival analysis (Fig.
Persistence of all baits offered in various presentation types. Curves depict reduction in proportion of baits available over time as non-targets remove them. Baits typically decline in viability through putrefaction and consumption by insects after 48 to 96 hours. Shaded areas represent 95% confidence intervals.
Summing all the time that baits were available to brown treesnakes before being taken by non-targets, we recorded a total of 2,427 “bait days” with no takes by brown treesnakes. This amounts to an overall daily estimated brown treesnake bait take rate of 0.000 per 100 bait days with an upper 95% binomial confidence interval of 0.151 baits per 100 bait days.
We operated 198 traps (99 one-piece, 99 two-piece) with mouse lures (100 live, 98 dead) for 55 nights, for a total of 10,890 trap nights (Table
Trapping effort (trap nights) by trap type and lure type. Values reflect overall effort and effort adjusted for non-functioning traps (e.g. lure missing, entrance flaps stuck open or closed, holes due to crab damage). Traps were functional at the previous check, so non-functional traps were presumed to be functional for one-half of the check interval, on average.
Trap type | Overall effort (trap nights) | Adjusted for non-functioning traps | ||||
---|---|---|---|---|---|---|
Live mouse | Dead mouse | Total | Live mouse | Dead mouse | Total | |
One-piece | 2,750 | 2,695 | 5,445 | 2,682.5 | 2,620.0 | 5,302.5 |
Two-piece | 2,750 | 2,695 | 5,445 | 2,663.0 | 2,588.0 | 5,251.0 |
TOTAL | 5,500 | 5,390 | 10,890 | 5,345.5 | 5,208.0 | 10,553.5 |
During this effort, we captured only one brown treesnake: a 1,249-mm SVL male weighing 360 g (Fig.
The only brown treesnake captured in over 10,500 trap nights on Cocos Island. This was a 1,249 mm snout-vent length, 360 g, male. This trap contained a live mouse in a protected chamber as the lure.
Non-target lizards and crabs were commonly found in brown treesnake traps (Table
Non-target captures in brown treesnake traps. Results are tabulated by trap type (one-pieces stainless steel versus two-piece galvanised) and lure type (live mouse or dead mouse). Counts are per trap observation; multiple individuals in the trap at the same time are counted as only one observation.
Common name | Latin name | One-piece Live | Two-piece Live | One-piece Dead | Two-piece Dead | Total |
---|---|---|---|---|---|---|
Lizards | ||||||
Green anole | Anolis carolinensis | 1 | 0 | 2 | 3 | 6 |
Blue-tailed skink | Emoia caeruleocauda | 0 | 0 | 1 | 0 | 1 |
Oceanic gecko | Gehyra oceanica | 0 | 0 | 2 | 0 | 2 |
Other geckos | Gekkonidae | 1 | 1 | 1 | 1 | 4 |
Mariana monitor | Varanus tsukamotoi | 8 | 11 | 14 | 5 | 38 |
Crabs | ||||||
Hermit crabs | Coenobita spp. | 183 | 24 | 14 | 1 | 222 |
Coconut crab | Birgus latro | 57 | 9 | 22 | 17 | 105 |
Totals | 250 | 45 | 56 | 27 | 378 |
Stainless steel one-piece traps were non-functional for 5.2% of trap nights, while galvanised two-piece traps were non-functional for 7.1% of nights (P < 0.001). Live mouse lure traps were non-functional 5.6% of trap nights and dead mouse lure traps were non-functional 6.8% of nights (P = 0.015). Stainless steel one-piece traps required 21 field repairs for a total of 2.83 hours of labour, while galvanised two-piece traps required 82 repairs totalling 12.4 hours of field labour. Only one trap, a two-piece galvanised trap, was removed for workshop repairs. At the end of the trapping effort, repair and cleaning requirements were recorded by trap type (Table
Repair and cleaning requirements by trap type. Minor repairs included straightening wire deformations from coconut crab damage, while major repairs required patching of holes in the mesh from crab damage.
Trap type | No repair (n) | Minor repair (n) | Major repair (n) | Repair labour (hr) | Cleaning labour (hr) |
---|---|---|---|---|---|
One-piece stainless steel | 28 | 47 | 24 | 13 | 20 |
Two-piece galvanised wire | 31.5* | 0 | 67.5 | 27 | 7 |
Totals | 59.5* | 47 | 31.5 | 40 | 27 |
During 1,100 trap nights monitored by infrared cameras (20 cameras, 647,733 total photos), we recorded only two trap encounters by brown treesnakes, of 2 and 8 minutes in duration (Fig.
A large brown treesnake at a two-piece trap with a live mouse lure recorded via time-lapse infrared photograph. The snake probed the body of the trap for 8 minutes, then left without returning that night. A snake of a similar size (likely the same snake) attempted to enter the same trap for 2 minutes 10 days later.
Throughout the time period of our baiting and trapping efforts (December 2020 to July 2021), USGS personnel performed 163.3 km of linear search effort over 376 hours and sighted 31 snakes, three of which escaped capture, for a visual detection rate of 0.188 snakes per km and 0.083 per hour of search. Prey sighting rates were high, with an average lizard sighting rate of 37.8/km (including 10 species) and 32.8 birds/km (8 species). Specifically for notable species, sighting rates were 15.5 green anoles, 11.3 oceanic geckos, 22.3 black noddies and 8.1 white terns per km of searching (
The results of this study are clear: two of the primary tools for brown treesnake removal on Guam will not be effective for brown treesnake eradication on Cocos Island. Brown treesnake detection rates, based on visual CPUE, are apparently lower on Cocos Island (0.188 snakes/km) than most other detection efforts on Guam. Within a long-term 5-ha geographically enclosed population representative of disturbed limestone forest and secondary forest on Guam,
Live trapping with mouse lures prior to snake suppression on Guam yielded a capture rate of 0.3 snakes per 100 trap days (
Our failure to attract brown treesnakes to baits and traps is most likely due to the extraordinary abundance of preferred live prey on Cocos Island, particularly large geckos, birds and their eggs, compared to the relatively prey-depauperate nature of Guam’s forests resulting from prolonged brown treesnake predation (
Of all the ecological damage that have occurred since their introduction to Guam, the pervasive impacts of brown treesnake predation on birds have been the most profound (
Brown treesnakes on Guam that forage in areas of increased prey availability, including birds, such as urban areas and swiftlet caves, tend to be in better body condition (
These findings demonstrate that higher prey availability negatively affects brown treesnake detection and capture rates. On Guam, temporary experimental suppression of rodent prey abundance was demonstrated to increase trap capture rates (
Both baiting and trapping appear to be relatively safe for Cocos Island wildlife. In only two instances did a native bird (a Pacific reef heron and a Guam rail) take a bait (both DNM) from the ground. Although acetaminophen may also be toxic to birds, they are not known to have the same genetic basis for sensitivity to acetaminophen toxicosis as snakes (
The practical information on baiting and trapping is of little avail when brown treesnake removal by these techniques is almost completely ineffectual in the context of abundant alternative prey availability. Initial eradication discussions for Cocos Island included a notional plan of a 20 × 20-m grid of bait stations and a 40 × 40-m grid of traps. At this density, we might have arrayed as many as 825 bait stations and 206 traps with live mouse lures across the entire 33 ha of the Island for the duration of an eradication attempt that is expected to last at least 5 to 10 years (based on ad hoc population estimates and demographic projections;
Instead, available funding is being programmed for visual searching and manual removal of snakes, the only tactic that has thus far been effective on Cocos Island. Although night-time visual searching can be logistically challenging, disruptive to work schedules and tedious, it is also the tool that is considered to be the least biased with respect to snake sizes, putting all brown treesnake size classes at risk of detection (
Further work would be beneficial to validate whether live bird lures would be more effective than mice and carrion on Cocos Island. Field and laboratory experiments have demonstrated that traps with a live bird as the lure show increased capture rates of large, well-conditioned snakes, as well as longer trap investigation times overall compared to those with mouse lures (
In the event of future invasions, prospects for complete removal of brown treesnakes from larger, prey-rich islands with difficult-to-access terrain would be challenging, particularly when our results indicate that application of the newly developed landscape-scale aerial baiting technology would be ineffective (
Our results indicate that standard invasive brown treesnake control tools, acetaminophen baiting and trapping with mouse lures, are seemingly not effective enough to warrant significant investment of limited project resources where preferred alternative prey are abundant. These results have profound ramifications for the potential of rapid removal and eradication of incipient brown treesnake populations on any other islands at risk of invasion, such as the Hawaiian Islands, the Northern Mariana Islands and throughout Micronesia and the rest of the Pacific where snake-free islands are rich in diversity and density of potential prey (e.g.
We’d like to thank all additional participants in the field work associated with these studies, including Jordan Barcinas, Ahmi Cacapit, Juan-Carlos Mungaray, Ella Norris and Alyssa Taitano. Zach Quiogue, Elizabeth Frasch, Amn Nacpil, Brianna Montgomery, Martin Felisan, Shiho Koike, Thomas Fies, Scott Goetz, Levi Gray, Thomas Hinkle, Charlene Hopkins, Peter Xiong, Marijoy Viernes, Dusty Jordan and Karen Watson contributed to the USGS RRT efforts to remove BTS from Cocos Island mentioned in this report. Olympia Terral and Martin Kastner coordinated the volunteer brown treesnake capture efforts. The contracted support from the University of Guam was facilitated by Adrian Ares, Daniel Lindstrom, Aubrey Moore and Cathleen Moore-Linn. We also wish to thank all participants in Cocos Island eradication planning, permitting and environmental compliance consultation including Michelle Bogardus, Dawn Bruns, Jacqueline Flores, Jeffrey Flores, Thomas Hall, Steve Hanser, Martin Kastner, MaryJo Mazurek, Benton Pang, Jeff Quitigua, Haldre Rogers, Jason Suckow, Olympia Terral and Lorena Wada. This research and the USGS rapid response was made possible by funding from the U.S. Department of the Interior Office of Insular Affairs coordinated by Hailey McCoy. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.