Eradicating invasive rodents from wet and dry tropical islands in Mexico
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Eradicating invasive rodents from wet and dry
tropical islands in Mexico
ARACELI SAMANIEGO-HERRERA, ALFONSO AGUIRRE-MUÑOZ
YULIANA BEDOLLA-GUZMÁN, ANA CÁRDENAS-TAPIA, MARÍA FÉLIX-LIZÁRRAGA
FEDERICO MÉNDEZ-SÁNCHEZ, ORLANDO REINA-PONCE
E V A R I S T O R O J A S - M A Y O R A L and F L O R T O R R E S - G A R C Í A
Abstract Eradications of invasive rodents from tropical is- Introduction
lands have a lower success rate compared to temperate is-
lands. In the tropics the wide range of physical and
biological conditions results in a wide variety of island
biomes, with unique challenges and windows of opportun-
I nvasive mammals are the primary driver of biodiversity
loss in island ecosystems (Towns et al., ). Of the
four invasive rodent species of major concern (the
ity for rodent eradications. We describe and compare re- Polynesian rat Rattus exulans, the ship rat R. norvegicus,
search and operational details of six successful the black rat R. rattus and the house mouse Mus musculus;
eradications of invasive mice Mus musculus and ship rats Amori & Clout, ), two are particularly widespread in
Rattus rattus carried out during –. The work was the tropics: the ship rat and the house mouse (Singleton &
conducted on six islands in two distinct tropical archipela- Krebs, ; Harper & Bunbury, ). Ship rats are the
gos in Mexico (one dry in the Gulf of Mexico; one wet in the most damaging invasive rodent to island ecosystems
Caribbean), and included the first eradication of rats from a (Towns et al., ; Shiels et al., ), and are therefore
mangrove-dominated island . ha. Invasive rodent po- the most frequently targeted species for eradication
pulations varied among species and islands, even neigh- (Howald et al., ; DIISE, ). On islands where
bouring islands; overall density was higher on wet islands. house mice are the only invasive mammal they can also
Physical and biological features, including the presence of have devastating, ecosystem-changing effects (Angel et al.,
land crabs, determined eradication timing and rates of ), and they have been targeted for eradication on is-
bait broadcast (higher on wet islands). An interval of – lands all over the world (DIISE, ).
days between the two bait applications per island was suffi- The . attempts at rodent eradication on islands
cient to eradicate actively breeding mouse and rat popula- worldwide (Russell & Holmes, ) reflect the wide use of
tions. Impacts on non-target species were negligible, this type of conservation intervention as one of the most ef-
including those on wild and captive iguanas. Eradication ficient actions to restore island ecosystems (Jones et al., ).
success was rapidly confirmed based on ground monitoring Overall, rat eradication using toxic bait has had a high global
and statistical modelling. Rodent eradications on larger success rate (.%; Russell & Holmes, ). However, the
tropical islands should be achievable with directed research failure rates of eradications on tropical (.%) vs non-
to inform planning and implementation. tropical islands (.%) suggest that some aspects of successful
Keywords Eradication, invasive rodents, land crabs, operations in the tropics are not well understood. Improving
Mexico, non-target impacts, restoration, tropical island the success rate on tropical islands is crucial, as the region in-
cludes priority sites with high numbers of species threatened
Supplementary material for this article can be found at by invasive rodents (Keitt et al., ).
https://doi.org/./S Tropical island ecosystems range from simple unvege-
tated systems to seasonal forests and evergreen rainforests,
despite their narrow latitudinal range (Osborne, ).
Large tropical islands can even contain microcosms with
ARACELI SAMANIEGO-HERRERA* (Corresponding author), ALFONSO AGUIRRE- contrasting physical and biological conditions, and under-
MUÑOZ, YULIANA BEDOLLA-GUZMÁN, ANA CÁRDENAS-TAPIA, MARÍA FÉLIX-
LIZÁRRAGA, FEDERICO MÉNDEZ-SÁNCHEZ, EVARISTO ROJAS-MAYORAL and FLOR
standing how these conditions influence invasive rodent
TORRES-GARCÍA Grupo de Ecología y Conservación de Islas, A.C., Moctezuma ecology and non-target populations is key to eradication
836, Zona Centro, Ensenada, Baja California, Mexico, C.P. 22800 planning (Harper et al., ). To improve the success rate
E-mail araceli.samaniego@islas.org.mx
of rodent eradications in the tropics, and based on current
ORLANDO REINA-PONCE Asociación Veterinaria de Reptiles y Anfibios, Puebla,
Mexico
knowledge, best practice guidelines for rat eradication on
tropical islands were published by an international team
*Also at: Pacific Invasives Initiative, University of Auckland, Private Bag 92019,
Auckland 1142, New Zealand. E-mail ara.samaniego.mx@gmail.com (Keitt et al., ). Simultaneously, the probability of rat
Received June . Revision requested July .
eradication success was evaluated according to three
Accepted September . First published online February . categories of tropical islands: savannah (dry), seasonal forest,
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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https://doi.org/10.1017/S0030605316001150560 A. Samaniego-Herrera et al.
and tropical rainforest (wet), and wet islands were found to
be the most challenging (Russell & Holmes, ). Within the
wet category, mangrove-dominated islands, which are ever-
green and permanently or regularly flooded, are particularly
challenging for rodent eradication (Harper et al., ;
Samaniego-Herrera et al., ; Harper & Bunbury, ).
Mexico has a history of successfully eradicating diverse
invasive mammal species from islands (Aguirre-Muñoz
et al., ). Invasive rodents have been eradicated from
islands of – ha (Samaniego-Herrera et al., , ), in-
cluding the largest rat eradication on a wet tropical island to
date, which is described here. The inherent challenges of the
tropics (e.g. land crabs and year-round-breeding rodent po-
pulations) have been faced and resolved in implementing
pest eradication projects on Mexico’s numerous tropical
islands. As conservation organizations require robust
scientific knowledge and evidence to implement successful
conservation programmes (Samaniego-Herrera et al., ),
the organization Grupo de Ecología y Conservación de Islas
has worked for years to conduct systematic eradications
to restore Mexico’s islands. Together with research, seabird
restoration and biosecurity, there have been mammal era-
dications on islands (Aguirre-Muñoz et al., ). Here
we describe research and compare the operational details
of six successful rodent eradication operations led by the or-
ganization across two contrasting Mexican tropical archipe-
lagos (one dry, one wet).
Study area
The two archipelagos to which the study islands belong are
Arrecife Alacranes in the Gulf of Mexico and Banco
Chinchorro in the Caribbean Sea (Fig. , Table ). Both
have high marine and terrestrial biodiversity and are natural
protected areas under Mexican federal law: Arrecife
Alacranes as a National Park and Banco Chinchorro as a
Biosphere Reserve (CONANP, , ). Both are also FIG. 1 Location of Arrecife Alacranes (a coral atoll) and Banco
Man and the Biosphere sites and Ramsar sites. The follow- Chinchorro Islands (a false atoll), Mexico, and their invasion
status in . By all islands were free of invasive mammals.
ing descriptions are mainly from CONANP (, ).
Arrecife Alacranes is a coral atoll comprising five small
(.– ha), flat, sandy keys (henceforth dry islands), three Onychoprion fuscatus) pairs (Tunnell & Chapman, ).
of which had invasive rodents in (Table ). The climate In addition, terrestrial migratory birds are frequent visitors
is subtropical dry semi-arid, BSw(w); the mean annual tem- (Supplementary Table S). Invasive rodents have been re-
perature is .°C and rainfall is scarce (annual mean corded on Pérez since (Fosberg, ). Pérez is the
mm) and concentrated in summer, resulting in low only island that is continually altered by human activity,
phenological variation in plants (Bonet & Rzedowski, ). which started in with the construction of a lighthouse
The open scrub community of halophytic plants is domi- and continues today, with a small permanent settlement
nated by Suriana maritima and Tournefortia gnaphalodes. (Table ). Seasonal tourism is concentrated on Pérez.
The most ubiquitous invertebrates are three species of land Banco Chinchorro is a false atoll comprising four flat keys
crabs; breeding vertebrate species include two lizards, three (.– ha; henceforth wet islands), three of which had in-
marine turtles and nine seabirds, the latter numbering several vasive rodents in (Table ). The climate is wet tropical,
hundred (Leucophaeus atricilla, Thalasseus sandvicensis, Sula Aw (x’), with a mean annual temperature of .°C. There is
leucogaster) or thousand (Sula dactylatra, Anous stolidus, rainfall (annual mean , mm) throughout the year but it is
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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https://doi.org/10.1017/S0030605316001150Eradicating rodents from islands 561
TABLE 1 Characteristics of the islands in the Arrecife Alacranes (dry) and Banco Chinchorro (wet) archipelagos, in Mexico (Fig. ), where
six rodent eradications were carried out during –, with area, ecosystem type, dominant vegetation, number of residents, and species
eradicated.
Island Area (ha) Ecosystem type Dominant vegetation No. of residents Species eradicated
Arrecife Alacranes
Pájaros 3 Tropical dry Short shrubs & grasses None Mus musculus
Pérez 13 Tropical dry Tall shrubs & herbaceous plants 15 Rattus rattus
Muertos 15 Tropical dry Short shrubs & herbaceous plants None Mus musculus
Banco Chinchorro
Cayo Norte Menor 15 Tropical wet Mangroves None Rattus rattus
Cayo Norte Mayor 30 Tropical wet Mangroves & evergreen forest 10 Rattus rattus
Cayo Centro 539 Tropical wet Mangroves & evergreen forest Up to 100 Rattus rattus*
*Feral cats Felis catus were also eradicated (by trapping in –).
concentrated in the summer and winter, with March usually camera traps, and interviews, confirmed there was only
being the driest month. The islands are covered with man- one rodent species per island. Further monitoring was con-
groves (Rhizophora mangle, Laguncularia racemosa, ducted to collect ecological information on the target rodent
Avicennia germinans and Conocarpus erectus) and typical populations (e.g. population density and reproduction) to
Caribbean tropical trees (dominated by Thrinax radiata, inform the eradication plan, and to estimate spatial detec-
Bursera simaruba and Tournefortia gnaphalodes); intro- tion parameters to inform the monitoring to confirm eradi-
duced coconut palms Cocos nucifera are also widespread. cation. Live trapping was conducted systematically across
Three species of land crabs have been recorded; breeding ver- islands, in both archipelagos simultaneously, two or three
tebrates include abundant populations of the American times per year for – years before each eradication
crocodile Crocodylus acutus, three lizard species, two igua- (Fig. ). Each trapping session lasted – consecutive
nas, one gecko and only one seabird (Fregata magnificens). nights. On each island a grid of × points, m apart,
Most terrestrial and aquatic birds are migratory was set and permanently marked. At each point a live trap
(Supplementary Table S). Rodents probably invaded as a re- (either from Tomahawk Live Trap, Hazelhurst, USA, or H.
sult of shipwrecks during the th century. The two largest B. Sherman, Tallahassee, USA) was set and baited each
islands have been directly and continually altered by afternoon, and checked and closed each morning.
human activity, beginning in the s (Table ). Feral cats Tomahawk traps baited with peanut butter were used to
Felis catus were present only on the largest island and were trap ship rats, and Sherman traps baited with oats were
eradicated by Grupo de Ecología y Conservación de Islas dur- used to trap house mice. All traps were elevated above the
ing – (Aguirre-Muñoz et al., ). ground by placing them on top of plastic containers to
avoid interference from land crabs while still being access-
ible to juvenile rodents (A. Samaniego-Herrera, pers. obs.).
Methods All rodents caught were marked with monel ear tags, and
we recorded their age (adult or juvenile, based on genitalia),
High precautionary standards were adopted to avoid the ac- sex, standard body-size metrics (weight and head–body
cidental introduction and distribution of invasive and length) and reproductive condition (determined by the pos-
pathogenic organisms. Separate teams were working simul- ition of the testes in males, and the prominence of nipples in
taneously across the islands during the eradication opera- females) before releasing them at their capture point.
tions, each with its own camping and research equipment, Population parameters (density, sigma (σ) and g0) were es-
thus avoiding contamination. Provisions were delivered in timated using maximum-likelihood spatially explicit cap-
secured containers, and insect and rodent traps were set in ture–recapture models implemented with package SECR
boats and store rooms, both on the islands and in our base in R v. . (R Development Core Team, ).
on the mainland. Capture and handling techniques, for both
native and invasive alien species, conformed to high stan-
dards of animal welfare (NOM, ). Eradication planning and implementation
Each archipelago was a separate project, each managed by
Rodent monitoring Grupo de Ecología y Conservación de Islas in coordination
with federal government agencies. For each project a cost–
Preliminary work, which consisted of directed trapping and benefit analysis determined the best bait delivery option to
searches for signs of rodents, the use of chew-blocks and deliver sufficient bait to every rodent territory and achieve
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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https://doi.org/10.1017/S0030605316001150562 A. Samaniego-Herrera et al.
eradication. Such analyses included helicopter cost (inter-
national and national travel, daily rate, fuel and permits),
FIG. 2 Timeline of two complex rodent eradication projects on tropical islands in the Arrecife Alacranes (dry islands) and Banco Chinchorro (wet islands) archipelagos, in Mexico
cost and potential risks of ground-based operations (based
(Fig. ). a, Simultaneous trapping on invaded islands; b, using island-wide grids of detector devices and rapid eradication assessment; c, one male rat caught through biosecurity
on island size and accessibility), and local capacity (of both
trained staff and partners).
The bait used was the rodenticide CI- (Conservation-D
in USA), developed by Bell Laboratories (Madison, USA)
specifically for ecological restoration operations. CI- consists
of green, unwaxed, compressed grain, g pellets containing
ppm brodifacoum (second-generation anticoagulant).
We used both the original version of the bait, designed
for dry environmental conditions, and a newer version
(Conservation-W in USA) resistant to high humidity
(Wegmann et al., ). The use of the original version on
the dry islands meant that leftover bait pellets on the ground
would be broken down relatively quickly by physical and
biological agents. However, using the newer version for the
wet islands was crucial to ensure that the bait pellets retained
their shape for several days in the humid environment. On the
wet islands, g bait blocks ( ppm brodifacoum), also by Bell
Laboratories, were used. All bait batches contained the
biomarker pyranine, which facilitates the detection of bait
consumption across a wide range of invertebrates and
vertebrates.
All dry islands were treated by hand broadcast of bait
(Broome et al., ), given their small size and easy acces-
sibility, and the relatively high cost of aerial broadcast.
Evenness in bait coverage was particularly important
where house mice were being targeted, and was achieved
by distributing bait along a × m grid. This
higher-than-usual level of accuracy was also desired for
the purpose of monitoring bait consumption, which was re-
ported elsewhere as part of a meta-analysis (Pott et al., ).
To plan and track the operation, a cm resolution
WorldView satellite image was used. In contrast, all wet is-
lands were treated using the aerial broadcast technique
(Broome et al., ) because of their larger size and com-
plexity (Supplementary Fig. S shows details for Cayo
Centro). The project was conducted in two phases: two sim-
ultaneous eradications on the smaller islands ( and ha)
measures; d, confirmation across the archipelago.
as a learning phase (including extensive research), and a
later eradication on the largest island ( ha), with an im-
proved approach and a more experienced team, as the com-
pletion phase. Bait was broadcast from a helicopter using a
spreader bucket purchased from Helicopters Otago Ltd
(Mosgiel, New Zealand). To obtain accurate geographical
data, the helicopter (Bell Jet Ranger, Aspen
Helicopters, Oxnard, USA) was equipped with a differential
global positioning system (TracMap, Mosgiel, New
Zealand). To track the aerial work and map bait densities
on the ground, a cm resolution Quickbird satellite
image was used. Maps were produced using a geographical
information system to confirm that bait distribution and ap-
plication rates conformed with the planned strategy
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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https://doi.org/10.1017/S0030605316001150Eradicating rodents from islands 563
(Supplementary Fig. S shows details for Cayo Centro). In TABLE 2 Comparison of successful approaches used to eradicate ro-
addition, for the largest operation (in ) we used a dents from dry (Arrecife Alacranes) and wet (Banco Chinchorro)
novel method to evaluate the aerial work (the Numerical tropical islands in Mexico (Fig. ) during –.
Estimation of Rodenticide Dispersal model), which im- Dry islands Wet islands
proves the accuracy of results by modelling more parameters Range in monthly 4–95 16–278
(e.g. helicopter speed) and speeds up the process of identi- rainfall (mm)
fying bait gaps (Rojas-Mayoral et al., ). Dry season November–July February–April
Bait uptake experiments conducted in dry seasons (Pott Month of rodent December (2011) April (2012), March
et al., ) were useful for determining bait application eradication (2015)
rates, and also took into account the type (hermit vs Main bait Small hermit crabs Large burrowing crabs
burrowing) and abundance of land crabs on each island competitors
Max. abundance of Medium High
(A. Samaniego-Herrera, unpubl. data). Bait application crabs
rates for the dry islands, where hermit crabs are dominant, Fluctuation of crab Low High
were lower than the rates for the wet islands (Table ), which activity
host abundant populations of large burrowing crabs. For all Main baiting Hand broadcast Aerial broadcast
six islands, two bait applications – days apart were technique
planned (Table ), and a detailed hand broadcast was con- Bait version* Conservation-25D Conservation-25W
ducted along the shore after each main application. On the No. of bait 2 2
applications
dry islands this shore application was done on foot by walk-
Days between 6 7 (2012), 10 (2015)
ing along open sandy beaches on the same day as the main applications
bait application. By hand broadcasting bait, the distribution Bait application 12 + 5 kg ha−1 30 + 12 kg ha−1
of sufficient bait for the rodents was ensured while minim- rate (first + second (2012), 30 + 30 kg
izing the risk of bait being washed out at high tide. On the application) ha−1 (2015)
wet islands, which have permanently flooded, mangrove- *Details in Methods
vegetated shores, the shore application was a sub-project in it-
self and required teams working simultaneously on foot and and non-target species confirmed that operating in the
in boats and kayaks. This work involved navigating around dry season would significantly decrease interference by
dense mangrove forests, including patches in interior lagoons, bait competitors (mainly land crabs), maximize the likeli-
and took full days after each main bait application. Bait was hood of rodents being food-stressed (although breeding ac-
delivered along the shore in the form of bait blocks attached to tivity never ceases), and minimize non-target impacts by
the mangrove branches every – m, because of the avoiding the peak of bird migration (Samaniego-Herrera
flooded terrain on all wet islands (Supplementary Fig. S et al., ; GECI, ).
shows details for Cayo Centro). To achieve even coverage of
bait in a timely and safe manner (e.g. avoiding crocodile
nests), a mobile app (the Field Reporting and Navigation Mitigating non-target impacts
app) was designed to facilitate navigation and speed up report-
ing. For the islands with human settlements (Cayo Centro, On the dry islands, where birds are seasonally abundant and
Cayo Norte Mayor and Pérez), bait stations (– per m) reptiles are naturally scarce, as evidenced by their low abun-
filled with bait blocks were set inside and underneath dance on the two rodent-free islands (Grupo de Ecología y
constructions, as well as around piers. Conservación de Islas, unpubl, data), impacts on native
Climate and reproductive cycles of both target and native fauna were minimized by operating in winter, thus avoiding
species are the main factors to be considered for timing ro- activity peaks of nesting seabirds, turtles and terrestrial mi-
dent eradications. On the dry islands the climatic window of gratory birds. Masked boobies Sula dactylatra and frigate-
opportunity was significantly larger, as most of the year is birds Fregata magnificens were nesting in low numbers
dry and windy, which explains the low seasonal fluctuation (both eggs and chicks were recorded) on both
in plant phenology (Bonet & Rzedowski, ), land crab ac- mouse-infested islands, and the last few turtle hatchlings
tivity (A. Samaniego-Herrera, unpubl. data) and rodent of the season emerged days before the eradication.
biology, including reproduction (Samaniego-Herrera, On the wet islands, where reptiles are diverse and
), all confirmed during the planning phase. Thus, abundant and birds are usually present in low numbers,
other factors, such as bird and turtle nesting and human ac- black Ctenosaura similis and green iguanas Iguana iguana
tivities such as tourism, which ideally should be avoided, were kept in captivity because their susceptibility to brodi-
were the main determinants of eradication timing. On the facoum was undetermined and preliminary experiments
contrary, climate was the most important factor for the tim- had confirmed their interest in the bait. In addition, iguana
ing of eradications on the wet islands. Research on target presence was artificially high around the human settlements
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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https://doi.org/10.1017/S0030605316001150564 A. Samaniego-Herrera et al.
TABLE 3 Median and % credible intervals (CI) of estimated probability of rodent eradication from dry (Arrecife Alacranes) and wet
(Banco Chinchorro) tropical islands in Mexico (Fig. ), using island-wide grids of detector devices and the rapid eradication assessment
model. All islands were evaluated twice: month or earlier after baiting (in bold), and months or later after baiting (during visits con-
ducted for research purposes).
Probability of success
Island No. of months after first bait application No. of nights of monitoring Median Lower CI Upper CI
Dry islands (Arrecife Alacranes)
Muertos 0.5 15 0.96 0.91 0.98
48 5 1.00 1.00 1.00
Pájaros 0.5 20 0.98 0.91 0.99
48 5 1.00 1.00 1.00
Pérez 0.5 20 0.98 0.92 0.99
48 5 1.00 1.00 1.00
Wet islands (Banco Chinchorro)
Cayo Centro 1 25 0.93 0.87 0.98
14 10 0.96 0.99 1.00
Cayo Norte Mayor 0.5 21 0.93 0.85 0.98
36 10 1.00 1.00 1.00
Cayo Norte Menor 0.5 21 0.94 0.87 0.99
36 10 1.00 1.00 1.00
for reasons of commensalism, and the risk of iguanas inter- model, a novel spatial-survey model that quantitatively esti-
fering with the eradication operation was determined to be mates the probability of eradication success, using a grid of
high, because of their potentially excessive bait consump- detection devices across an island and parameters obtained
tion around human settlements (i.e. creating gaps in bait from prior rodent monitoring (Table ; Russell et al., ).
coverage). A total of black and green iguanas were The model was originally developed to confirm the rat
caught by hand a few days before each eradication operation eradication on Isabel Island, Mexico (Samaniego-Herrera
(only around human settlements), individually marked, and et al., ), and since then Grupo de Ecología y
kept in captivity (in situ) until the bait had disappeared from Conservación de Islas has used this tool systematically to
the ground. They were then released following a health confirm mouse and rat eradications. The spacing of the con-
check. Additional iguanas ( on Cayo Norte Mayor and firmation grid on all three dry islands was m, whereas on
on Cayo Centro) were marked, checked for health and the two smaller and the largest wet islands the grid was
released immediately (i.e. before bait application) for mon- and m, respectively (Supplementary Fig. S shows the
itoring purposes. All marked iguanas ( wild and captive grid on Cayo Centro).
individuals on two islands) were also monitored months Additionally, radio-telemetry was used to monitor ro-
and year after the eradications. Professional reptile hand- dent time to death during the eradications, as such infor-
lers managed the entire iguana subproject, including the mation is scarce for tropical environments. One week
construction of appropriate facilities and the management before the first bait application on each island, –
of the iguanas’ diet (Supplementary Material ). adult rodents (balanced sex ratio) were trapped in dis-
persed locations, fitted with radio-collars and monitored
daily to make sure they were alive on the day of the first
Post-eradication monitoring bait application and to investigate how long afterwards
they remained active.
Island-wide monitoring was conducted for weeks following
the first bait application on each island. Diurnal and noctur-
nal surveys (– person-hours per day) were conducted daily
to search for, collect and dissect fresh vertebrate carcasses. Results
Bait consumption was checked through biomarker signs
(fluorescent green colour under UV light) and dissections.
Rodent monitoring We confirmed only one rodent species
was present on each island in (M. musculus on two dry
Evaluating eradication efficacy islands and R. rattus on one dry and all three wet islands;
Table ). Rodent data were analysed in detail by
Rodent absence was evaluated within weeks after each oper- Samaniego-Herrera () and the main results relevant to
ation (Table ) using the rapid eradication assessment eradication planning are in Table . Overall, significant
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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https://doi.org/10.1017/S0030605316001150Eradicating rodents from islands 565
TABLE 4 Biological data from two invasive rodent species, Mus musculus and Rattus rattus, on dry (Arrecife Alacranes) and wet (Banco
Chinchorro) tropical islands in Mexico (Fig. ).
Dry islands Wet islands
Mus musculus
Population density (mice ha−1: 95% CI) Muertos: 4.1–30.9
Pájaros: 18.9–76.1
Weight (g; mean ± SD) Muertos: 17.6 ± 2.8 (n = 29)
Pájaros: 13.9 ± 2.3 (n = 142)
Parameter g01 (95% CI) Muertos: 0.04–0.07
Pájaros: 0.08–0.14
Parameter σ2 (95% CI) Muertos: 20.46–34.63
Pájaros: 14.62–24.75
Rattus rattus
Population density (rats ha−1: 95% CI) Pérez: 6.3–32.7 Cayo Norte Mayor: 25.3–102.5
Cayo Centro: 6.5–47.9
Weight (g: mean ± SD) Pérez: 174.0 ± 42.3 (n = 90) Cayo Norte Mayor: 189.0 ± 42.6 (n = 228)
Cayo Centro: 154.9 ± 26.7 (n = 125)
Parameter g01 (95% CI) Pérez: 0.07–0.10 0.05–0.07
Parameter σ2 (95% CI) Pérez: 20.21–23.17 14.33–22.69
The probability of detection when trap and range centres coincide
The spatial scale of the detection function
TABLE 5 Approximate cost (USD), per item, of the principal phases of the rodent eradications implemented in Arrecife Alacranes and
Banco Chinchorro archipelagos, in Mexico (Fig. ).
Arrecife Alacranes1 (3 dry islands; 31 ha) Banco Chinchorro2 (3 wet islands; 584 ha)
Eradication Post-eradication surveys Eradication Post-eradication surveys
implementation (2 visits) implementation (2 visits)
Preparation & planning3 43,545 42,348
Helicopter Not applicable 202,695
Aerial bucket Not applicable Already owned
Bait 22,581 124,025
Boat expenses 2,196 4,526
Staff 126,538 7,500 190,790 22,500
Food, travel, fuel, materials 64,615 4,643 113,902 3,840
Lodging, air transportation, 34,231 1,786 79,528 1,232
ground transportation
Field equipment & materials 62,462 1,071 130,969 755
Total 356,168 15,000 888,783 28,327
All three islands were treated simultaneously in .
Two islands were treated simultaneously in , and a third island was treated in .
Includes work shown in Fig. .
differences in rodent size and population density were found on the two smaller and the largest wet island, respectively.
between species and among islands, including neighbouring Each project (i.e. on each archipelago) required – years of
islands; for example, the lowest population density was research and preparation (legal, financial and logistical;
recorded for house mice on the dry island of Muertos ( Fig. ). The main difference in cost between projects
ha−), whereas the highest density was recorded for ship resulted from bait quantity and helicopter use on the wet
rats on the wet island of Cayo Norte Mayor ( ha−); islands (Table ). As planned, two bait applications were
however, the maximum rat density on nearby Cayo Centro implemented on each island, – days apart, using
( ha−), where cats were present until recently, was closer contrasting bait application rates between dry ( kg ha−)
to that of the dry island of Pérez ( ha−). and wet (– kg ha−) islands (Table ; Supplementary
Fig. S shows details for Cayo Centro). A team of –
Eradication planning and implementation Rodent people was required for each operation, which consisted of a
eradication operations were carried out in December core team of experienced practitioners (Grupo de Ecología y
on the three dry islands, and in April and March Conservación de Islas staff) plus partners and volunteers, who
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https://doi.org/10.1017/S0030605316001150566 A. Samaniego-Herrera et al.
received appropriate training. For the dry islands the total The rapid eradication assessment model indicated a high
effort required to spread bait twice manually across the probability of success (–%) immediately after each
islands ( ha in total) was person-hours, with eradication operation (Table ). Subsequent visits for
person-hours required for setting markers. Forty-seven bait research purposes provided an opportunity for further
stations were set around human settlements (– m testing, and this work confirmed rodent absence – years
spacing). For the wet islands the total flying time required to after baiting (Table ; Fig. ). Most collared rodents
aerially spread bait twice across the islands ( ha in total) (–% on each island) were located and recovered; the
was . h. In addition, person-hours were required remaining rodents may have had faulty collars or may
for placing bait blocks in the mangroves; bait stations have died near the ocean and been washed away. The first
(– m spacing) were set around human settlements. collared rodent died on day after the first bait application
and the last died on day . Dissections confirmed poisoning
as the cause of death in all of the recovered rodents ().
Mitigating non-target impacts The iguanas caught around
the human settlements on Cayo Centro and Cayo Norte
Mayor ( in total) were kept in captivity for weeks in
and for weeks in . Survival rates in captivity were Discussion
.% (n = ) and .% (n = ), respectively. Three All six rodent eradication operations were planned and im-
weeks after the first bait application % (n = ) of wild plemented by Grupo de Ecología y Conservación de Islas
iguanas (i.e. those exposed to the bait) were alive and using the same scientific approach. Important operational
displayed normal behaviours. Three wild iguanas, in differences between dry and wet ecosystems, such as bait ap-
addition to two untagged iguanas, were found dead – plication rates and treatment of island perimeters, reflect in-
weeks after the first bait application. The cause of death was herent differences in ecological biomes rather than
probably a combination of primary poisoning and poor management preferences. Although aerial bait dispersal
health, given that in addition to bait, plastic bags were found was always preferable, bait broadcast methods varied be-
in their stomachs during dissection. No more carcasses were tween dry and wet islands because of economic constraints.
found by Grupo de Ecología y Conservación de Islas staff or Operating during the dry season was also preferred, as chal-
the island residents during the next months. The tags were lenges such as land crab interference, floods, and arboreal
not always readable after months, and therefore the presence rat activity are augmented during the wet season, particular-
of some individuals could not be confirmed. However, ly on wet islands (Samaniego-Herrera et al., ). For ex-
months after baiting we estimated . % of the surviving ample, during a bait uptake experiment conducted on
tagged iguanas were alive, based on morphometric data and Cayo Centro in late May, at the beginning of the wet season,
population counts (GECI, unpubl. data). when most land crabs are active, kg ha− of placebo bait
disappeared overnight (A. Samaniego-Herrera, unpubl.
Post-eradication monitoring On the three dry islands, data). This is . times higher than the mean daily con-
within weeks of the first bait application we collected a sumption (. kg ha−) recorded in the same plot during
total of vertebrate carcasses ( on Pájaros, on the dry season (GECI, ). The substantial decrease in
Muertos and on Pérez), all of which were birds. Of land crab activity during the short dry season, rather than
these, % (belonging to seven species) were positive for the moderate fluctuation in rat density, is the main cause
the biomarker, indicating bait consumption and showing of decreased bait consumption.
signs of poisoning. The remaining % (belonging to Balancing disturbance effects and eradication efficacy in
species) were negative for the biomarker and showed signs the tropics is challenging, as the potentially high bait rates
of starvation (Table ). The majority of the carcasses were required considerably increase the potential for negative im-
found along the shore, where bait pellets were highly visible pacts on native species (Pitt et al., ) and increase the cost
against the white sand. On the wet islands we collected a total of eradication campaigns. On temperate islands a total bait
of vertebrate carcasses (seven on Cayo Norte Mayor and rate of kg ha− is commonly used for rodent eradications
nine on Cayo Centro). Of these, % (belonging to four (Broome et al., ), whereas in the tropics the bait rate var-
species) were positive for the biomarker and showed signs ies considerably and can be substantially higher (Pott et al.,
of poisoning, and the remaining % (belonging to seven ). For example, a total bait rate of kg ha− was used
species) were negative for the biomarker. in the eradication of rats from Palmyra Atoll (Wegmann
et al., ). In comparison, the total bait rates used in our
campaigns are conservative and related to island category
Evaluating eradication efficacy The island-wide grids of ( kg ha− on the dry islands and – kg ha− on the
detection devices were active for – consecutive nights, wet islands). The apparent differences between dry and
commencing – weeks after each first bait application. wet islands warrant further investigation. In terms of cost,
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https://doi.org/10.1017/S0030605316001150Eradicating rodents from islands 567
TABLE 6 Details of carcasses found during monitoring of non-target species within weeks after bait application during rodent eradications
on three dry (Arrecife Alacranes; ha total area) and three wet (Banco Chinchorro; ha total area) tropical islands in Mexico (Fig. ).
Dry islands (No. of individuals) Wet islands (No. of individuals)
With signs of bait With signs of With signs of bait With signs of
Species consumption1 starvation2 consumption1 starvation2
Birds
Ruddy turnstone Arenaria 21 2
interpres
Cattle egret Bubulcus ibis 1
Sanderling Calidris alba 38 4
Swainson’s thrush Catharus 1
ustulatus
Little blue heron Egretta caerulea 1 1
Magnificent frigatebird Fregata 1
magnificens
American coot Fulica americana 2
Herring gull Larus argentatus 1 1
Sooty tern Onychoprion fuscatus 4
Northern waterthrush Parkesia 1
noveboracensis
Savannah sparrow Passerculus 11
sandwichensis
Blue grosbeak Passerina caerulea 1
Brown pelican Pelecanus 1
occidentalis
Double-crested cormorant 3
Phalacrocorax auritus
Black-bellied plover Pluvialis 1 1
squatarola
Great-tailed grackle Quiscalus 3
mexicanus
Yellow-rumped warbler 2
Setophaga coronata
Palm warbler Setophaga 1 1
palmarum
Yellow warbler Setophaga petechia 1
Masked booby Sula dactylatra 5
Reptiles
Black iguana Ctenosaura similis 5 1
Green iguana Iguana iguana 2 1
Positive for biomarker and signs of internal haemorrhage
Negative for biomarker
the eradication budget reported here is well below the aver- sandy beaches may have contributed to the higher-
age for similar projects worldwide (Holmes et al., ). than-expected consumption by non-target species. Future
We believe the detailed work on the perimeter of the wet projects should consider reducing the bait spread on large,
islands was crucial to eradication success; however, we rec- sandy, unvegetated beaches, or using bait stations in this
ognize it may not be feasible to apply this manual method type of habitat.
on larger islands. We therefore encourage the development Although the aerial broadcast of bait is the preferred op-
of more efficient alternatives (e.g. aerial methods) so that tion for conducting rodent eradications on islands (Broome
larger mangrove islands can be cleared of invasive rodents et al., ), hand broadcasting of bait is an appropriate al-
(Harper et al., ). The use of the Conservation-W ternative when suitable pilots and helicopters are not readily
bait for these particularly wet islands proved to be useful, available at a reasonable cost, provided the size and com-
as reported previously for Palmyra Atoll, as this bait is sig- plexity of the island are manageable (i.e. efficiencies of
nificantly more resistant to humidity (Wegmann et al., ) scale for cost are absent). Regardless of the broadcast tech-
than the original version (Conservation-D). On the dry is- nique, avoiding gaps and ensuring the even distribution of
lands the high visibility of the green bait pellets on the white bait are essential.
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https://doi.org/10.1017/S0030605316001150568 A. Samaniego-Herrera et al.
In this case all dry islands were small and close together, during subsequent research trips to the islands. Rapid eradi-
and therefore implementing three operations simultaneous- cation assessment is therefore a powerful tool for accelerat-
ly maximized management and research efficiency and ing the confirmation of eradication, especially on small
minimized cost and the risk of re-invasion. Wet islands (, ha), accessible islands (Russell et al., ). Given
proved to be more challenging, not only because of their the generalist diet of the eradicated rodent populations
size but also because of the complexity and novelty of the (Samaniego-Herrera, ), a wide range of native plant, in-
habitat (Harper et al., ). Until only one small wet vertebrate and vertebrate populations (including land crabs
island ( ha) with a comparable percentage of mangrove and seabirds) are expected to recover as a result of rodent
cover had been subjected to a rodent eradication removal.
(Wegmann et al., ). We agree with Harper et al. Continued funding, with long-term vision from commit-
() that the problem mangroves pose for large-scale era- ted foundations, has been essential to successful eradication
dications on wet islands is confounded by the lack of knowl- efforts. As of , Mexican islands have been cleared of
edge of rat ecology in mangroves. invasive mammals, % of which have been rodent eradica-
For both mouse-infested dry islands combined, the mean tions (Aguirre-Muñoz et al., ). Long-term, effective is-
weight (. ± SD . g) and density ( ha−) of house mice land biosecurity is now being developed as a collaborative
were lower than those reported for temperate islands national programme. International collaboration has also
(Russell, ). For rats, overall densities were higher on been important, with support from countries with extensive
wet islands (maximum ha−) and values are well within mammal eradication experience, such as New Zealand
the range reported for tropical islands, which in turn are (Towns et al., ; Russell & Broome, ).
higher than on temperate islands (Shiels et al., ; Our general approach to rodent eradication
Harper & Bunbury, ). Both invasive rodent species re- (Samaniego-Herrera et al., ) is consistent with inter-
produce year-round on dry and wet islands. national best practice guidelines (Keitt et al., ), although
The casualties of the eradication campaigns included in- we have some comments on these guidelines based on our
dividuals of native species, of which the majority were experience with programmes on Mexican islands. In par-
birds, including common carnivorous shorebirds, such as ticular, it is increasingly clear that most invasive rodent po-
ruddy turnstones Arenaria interpres and sanderlings pulations on both wet and dry tropical islands breed all year
Calidris alba, which was unexpected given their regular round, but this is not a precursor to eradication failure. We
feeding habits. No boobies or frigatebirds, which were nest- have demonstrated that – days between bait applications,
ing at the time, were harmed by the eradication operations, which is the norm in Mexico (Samaniego-Herrera et al.,
in line with findings for Isabel Island (Samaniego-Herrera , ), is sufficient to eradicate actively breeding
et al., ). Likewise, reptiles in general appeared to have mouse and rat populations from tropical islands, and this
low susceptibility to brodifacoum, as previously suggested short period between applications can result in significant
(Harper et al., ; Broome et al., ), given that scats operational savings. Although land crabs are mentioned in
with bait signs were commonly found but carcasses were the guidelines, we emphasize that understanding this com-
comparatively rare. Temporary captivity of commensal munity could be the difference between failure and success
iguanas was a successful approach to avoid gaps in bait in rodent eradication campaigns in the tropics. It is also im-
coverage around primary rat habitat near human settle- perative to over-monitor tropical islands until sufficient in-
ments. However, captivity measures may not be necessary formation has been accumulated to achieve results
as long as the reptile populations are healthy, as low mortal- comparable to those on temperate islands. The six rodent
ity, much lower than in birds, is expected. eradications reported here, including that on Cayo Centro,
The evaluation of eradication success shortly after imple- the largest wet tropical island cleared of invasive rodents,
mentation through robust statistical modelling using rapid were achieved by over-engineering the projects.
eradication assessment was invaluable. Given the experi-
mental approach of these conservation projects undertaken
in high-risk, poorly understood tropical ecosystems (Russell Acknowledgements
& Holmes, ), the confirmation provided by rapid eradi-
cation assessment improved decision making for each sub- This work is part of the National Island Restoration
sequent operation, representing an overall saving in Programme of Grupo de Ecología y Conservación de Islas.
eradication costs. Local and real-time parameters from We are grateful to Nic Tolentino for developing the FERN
each target population were obtained through research con- app. The projects reported here were funded through na-
ducted alongside management efforts, at low cost, and used tional and international collaborations. We thank our do-
in the confirmation analysis. The results are the first exam- nors (Packard Foundation, Marisla Foundation, Comisión
ples of the confirmation of successful rodent eradication Nacional para el Conocimiento y Uso de la Biodiversidad,
within weeks of baiting, and were verified opportunistically Global Environment Facility, United Nations Development
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https://doi.org/10.1017/S0030605316001150Eradicating rodents from islands 569
Programme, Alianza WWF–Fundación Carlos Slim, Fondo Zealand Department of Conservation internal document
Mexicano para la Conservación de la Naturaleza, U.S. Fish DOCDM-. Department of Conservation, Wellington, New
Zealand.
and Wildlife Service, National Fish and Wildlife
B R O O M E , K.G., C O X , A., G O L D I N G , C., C R O M A R T Y , P., B E L L , P. &
Foundation), partners (Secretaría de Medio Ambiente y M C C L E L L A N D , P. () Rat Eradication Using Aerial Baiting:
Recursos Naturales (SEMARNAT), Secretaría de Marina Current Agreed Best Practice Used in New Zealand (Version .).
Armada de México, Secretaría de Gobernación, Comisión New Zealand Department of Conservation internal document.
Nacional de Áreas Naturales Protegidas (CONANP), Department of Conservation, Wellington, New Zealand.
B R O O M E , K.G., F A I R W E AT H E R , A.A.C. & F I S H E R , P. ()
Secretaría de Comunicaciones y Transportes, Amigos de
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Sian Ka’an, Bell Laboratories, Aspen Helicopters and Unpublished report docdm-. Department of Conservation,
Auckland University), project reviewers (Biodiversity Hamilton, New Zealand.
Restoration Specialists and the Island Eradication Advisory C H A R R U A U , P., D E L A V E G A , A.H.D. & D E L A C R U Z , F.R.M. ()
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invertebrates on Antipodes Island. Polar Biology, , –. novel approach to rat eradication at Palmyra Atoll. In th
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eradications in New Zealand: another decade of advances. New A R A C E L I S A M A N I E G O - H E R R E R A ´ s research focuses on efficient
Zealand Journal of Ecology, , –. management of invasive species, and she oversees the rodent eradica-
R U S S E L L , J.C. & H O L M E S , N.D. () Tropical island conservation: tion projects of Grupo de Ecología y Conservación de Islas. A L F O N S O
rat eradication for species recovery. Biological Conservation, , –. A G U I R R E - M U Ñ O Z is interested in interdisciplinary approaches to ap-
S A M A N I E G O -H E R R E R A , A. () Ecology and impacts of invasive plied conservation and sustainability. Y U L I A N A B E D O L L A - G U Z M Á N
rodents on tropical islands, in relation to eradication operations. PhD is leading an extensive restoration programme focusing on seabirds
thesis. The University of Auckland, Auckland, New Zealand. on Mexican islands. A N A C Á R D E N A S - T A P I A ´s interests are the
S A M A N I E G O -H E R R E R A , A., A G U I R R E -M U Ñ O Z , A., integration of innovative tools, such as geographical information sys-
M É N D E Z -S Á N C H E Z , F., R O J A S -M AY O R A L , E. & C Á R D E N A S -T A P I A , tems and molecular markers, to advance conservation goals. M A R Í A
A.G. () Pushing the boundaries of rodent eradications on F É L I X - L I Z Á R R A G A works on conservation and restoration of seabirds
tropical islands: Ship rat eradication on Cayo Centro, Banco on Mexican islands, implementing techniques such as social attraction
Chinchorro, Mexico. th International Congress for Conservation and habitat management. F E D E R I C O M É N D E Z - S Á N C H E Z leads
Biology, Montpellier, France. GECI’s island biosecurity and environmental education programmes.
S A M A N I E G O -H E R R E R A , A., A G U I R R E -M U Ñ O Z , A., O R L A N D O R E I N A - P O N C E contributes to the conservation and protec-
R O D R Í G U E Z -M A L A G Ó N , M., G O N Z Á L E Z -G Ó M E Z , R., tion of wildlife through education and captive management projects.
T O R R E S -G A R C Í A , F., M É N D E Z -S Á N C H E Z , F. et al. () Rodent E V A R I S T O R O J A S - M A Y O R A L specializes in the development of math-
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N. Clout & D.R. Towns), pp. –. IUCN, Gland, Switzerland. menting invasive mammal eradications on Mexican islands.
Oryx, 2018, 52(3), 559–570 © 2017 Fauna & Flora International doi:10.1017/S0030605316001150
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