Precipitous decline of mammals in the Everglades

Cite this article: McCleery RA, Sovie A, ReedRN, Cunningham MW, Hunter ME, Hart KM.2015 Marsh rabbit mortalities tie pythons to the precipitous decline of mammals in the Everglades.
About Jack Berlin

About Prizm Share
Marsh rabbit python ENP mortality site Burmese python mammal doi control site predator
Cite this article: McCleery RA, Sovie A, ReedRN, Cunningham MW, Hunter ME, Hart KM.2015 Marsh rabbit mortalities tie pythons to the precipitous decline of mammals in the Everglades.
About Jack Berlin

About Prizm Share
Marsh rabbit python ENP mortality site Burmese python mammal doi control site predator
rspb.royalsocietypublishing.org

Research
Cite this article: McCleery RA, Sovie A, Reed
RN, Cunningham MW, Hunter ME, Hart KM.
2015 Marsh rabbit mortalities tie pythons to
the precipitous decline of mammals in the
Everglades. Proc. R. Soc. B 282: 20150120.
http://dx.doi.org/10.1098/rspb.2015.0120

Received: 20 January 2015
Accepted: 23 February 2015

Subject Areas:
ecology
Keywords:
Burmese python, marsh rabbit, Everglades
National Park

Author for correspondence:
Robert A. McCleery
e-mail: ramccleery@ufl.edu

Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2015.0120 or
via http://rspb.royalsocietypublishing.org.
& 2015 The Author(s) Published by the Royal Society. All rights reserved.


Marsh rabbit mortalities tie pythons to
the precipitous decline of mammals in
the Everglades
Robert A. McCleery1, Adia Sovie1, Robert N. Reed2, Mark W. Cunningham3,
Margaret E. Hunter4 and Kristen M. Hart5
1Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL, USA
2United States Geological Survey, Fort Collins Science Center, Fort Collins, CO, USA
3Florida Fish and Wildlife Conservation Commission, Gainesville, FL, USA
4United States Geological Survey, Southeast Ecological Science Center, Gainesville, FL, USA
5United States Geological Survey, Southeast Ecological Science Center, Davie, FL, USA
To address the ongoing debate over the impact of invasive species on native
terrestrial wildlife, we conducted a large-scale experiment to test the hypoth-
esis that invasive Burmese pythons (Python molurus bivittatus) were a cause
of the precipitous decline of mammals in Everglades National Park (ENP).
Evidence linking pythons to mammal declines has been indirect and
there are reasons to question whether pythons, or any predator, could
have caused the precipitous declines seen across a range of mammalian
functional groups. Experimentally manipulating marsh rabbits, we found
that pythons accounted for 77% of rabbit mortalities within 11 months of
their translocation to ENP and that python predation appeared to preclude
the persistence of rabbit populations in ENP. On control sites, outside of the
park, no rabbits were killed by pythons and 71% of attributable marsh rabbit
mortalities were classified as mammal predations. Burmese pythons pose a
serious threat to the faunal communities and ecological functioning of
the Greater Everglades Ecosystem, which will probably spread as python
populations expand their range.

1. Background
As non-native invasive animals spread across the planet, the importance of their
impact on native terrestrial wildlife remains controversial [1] in part because of
a remarkable lack of large-scale experiments. One particularly contentious
debate is over the role of the invasive Burmese python (Python molurus bivittatus
or Python bivittatus) in the drastic declines of mammal populations in Ever-
glades National Park (ENP) over the last several decades [2]. ENP, globally
recognized for its unique biotic communities, sits at the southern end of the
Greater Everglades Ecosystem (GEE), a vast
freshwater wetland (10
000 km2) encompassing most of the southern Florida peninsula [3]. The ecologi-
cal processes, functionality and restoration efforts within this distinct ecosystem
are probably being substantially impaired by the disappearance of once
common mammalian predators and herbivores [46]. Declines in mammal
populations in ENP appear to coincide temporally and spatially with the arrival
and spread of invasive Burmese pythons [2], a large-bodied snake native to
southeast Asia that preys on vertebrates. Pythons were probably introduced
into ENP several decades ago via releases or escapes from private ownership
[7]. Sightings and removals of pythons in ENP were sporadic in the 1980s
and 1990s, increasing sharply in the early 2000s [2]. During this time, gut con-
tent analysis of invasive pythons in ENP indicated that mammals accounted for
about 75% of their diet [8].
Nonetheless, previous evidence linking pythons to mammal declines has been
indirect [2], and there are reasons to question whether pythons or any predator
could have caused the precipitous declines seen across a range of mammalian

control (capture/release) site
donor sites
procedural control recipient site
treatment recipient sites
rare
python observations
occasional
frequent
study sites
Figure 1. Location of study sites in south Florida, United States. Relative frequency of Burmese python observations were based on 20082013 records in the Early
Detection and Distribution Mapping System [18]. ETS, East Taylor Slough; CPT, Coastal Prairie Trail; FAK, Fakahatchee Strand Preserve State Park; LOX, Arthur
R. Marshall Loxahatchee National Wildlife Refuge; STA, Storm Water Treatment Area.
rspb.royalsocietypublishing.orgProc.R.Soc.B282:201501202
functional groups. Introduced predators, including snakes, have
reduced or eliminated fauna on islands [911], yet there are no
accounts of a lone introduced apex predator (apart from
humans) removing a functionally diverse, continental mammal
community. Additionally, ecological theory provides little sup-
port for the hypothesis that an apex predator could extirpate
small, broadly dispersed, fecund, generalist herbivores [1214].
To test the hypothesis that pythons are driving the decline of
mammal populations, we experimentally manipulated marsh
rabbit (Sylvilagus palustris) populations in ENP.
Marsh rabbits are small (1 kg) lagomorphs found near
fresh and brackish water throughout the southeastern USA
[15]. Sexually active throughout the year, marsh rabbits can
produce up to six litters of three to five young annually
[15]. Through the 1980s, this species was one of the most
commonly seen mammals in ENP [2,3]. Despite having a
wide variety of natural predators, marsh rabbits are still
common in areas of the GEE outside of ENP. For these
reasons, and because rabbit populations are generally resili-
ent and capable of persisting under considerable predation
pressure [16,17], we chose marsh rabbits as a model to under-
stand the impacts of pythons on mammals in ENP. If pythons
caused the declines of marsh rabbits in ENP, we predicted
that (i) pythons would be the dominant cause of marsh
rabbit mortality in ENP, (ii) mammals would cause more
marsh rabbit mortalities in areas of the GEE where pythons
were rare or absent, (iii) marsh rabbit populations introduced
in ENP would not persist, and (iv) unlike endothermic preda-
tors (i.e. mammals), the timing of python-caused mortality
would vary with seasonal climate conditions.

2. Material and methods
(a) Study design
Using marsh rabbits as a model, we experimentally manipulated
their populations to determine the role of pythons in driving
mammal declines within ENP. We compared the risk of mortality
from different causative agents
in areas with established
Burmese python populations to similar areas where pythons
were rare or absent (figure 1). We also evaluated the influence
of environmental factors on temporal variation in mortality
rates from the dominant predators of marsh rabbits (e.g. pythons
and mammals) in the GEE.
We captured marsh rabbits from donor populations and ran-
domly assigned them to one of three sites: two sites in ENP and a
procedural control site in the GEE, where pythons had not been
observed (figure 1). The purpose of the procedural control was to
account for the influence of translocation on mortality events. We
also established a control site where pythons were rare or absent
to compare causes of mortality in ENP with an established popu-
lation of marsh rabbits that was not manipulated. At the control
site, we captured and released rabbits without translocating them.

(b) Study sites
ENP is a large (600 000 ha) federally protected wetland listed as an
International Biosphere Reserve, a World Heritage Site and a
Wetland of International Importance in the Ramsar Convention.
The park has a diversity of vegetative communities that once
supported a varied mammalian community, including a large
population of marsh rabbits. However, recent reports suggest
that there are few, if any, self-sustaining marsh rabbit populations
in ENP [2]. ENP also hosts a well-established population of

rspb.royalsocietypublishing.orgProc.R.Soc.B282:201501203
invasive Burmese pythons [18]. To capture some of the variations
in natural communities within the park, we translocated marsh
rabbits to two locations (figure 1; electronic supplementary
material, Study Sites): a coastal marsh wetland (Coastal Prairie
Trail; CPT) and a freshwater wetland (East Taylor Slough; ETS).
We used approximately 2000 python presence records from
the Early Detection and Distribution Mapping System [19] to
select control sites in areas where pythons were rarely or never
detected. We used presence records because low detection and
capture probabilities of cryptic pythons over the vast Everglades
landscape have hindered the development of rigorous popu-
lation estimates for these snakes [20]. We selected Arthur
R. Marshall Loxahatchee National Wildlife Refuge (LOX) as
our procedural control site. Loxahatchee National Wildlife
Refuge is approximately 60 000 ha of protected wild land located
about 100 km northeast of ENP (figure 1). At the initiation of our
study, no Burmese pythons had been detected within 10 km of
the refuge. For our control site, we selected Fakahatchee Strand
Preserve State Park (FAK; figure 1), an approximately 30 000 ha
protected area at the westernmost edge of the GEE. Marsh rabbits
were commonly seen on this site during the study, and only two
Burmese pythons had been detected and removed within 10 km
of the study site since 2003.
Our sites with donor marsh rabbit populations were located in
the northern section of the GEE, and included Storm Water
Treatment Areas (STAs) and the adjacent Holey Lands Wildlife
Management Area (figure 1). Within these areas, we captured rab-
bits on levees that provide an elevated platform where the rabbits
congregated. We also captured rabbits from the shoulders of
roads where the dominant vegetation was brush broom grass
(Andropogon spp.) and Brazilian pepper trees (Shinus terebinthifolius).

(c) Trapping, handling and tracking
To capture rabbits, we identified areas with extensive rabbit
activity and saturated those areas with Tomahawk live traps
(model no. 107, Tomahawk, WI, USA), reinforced to protect cap-
tured marsh rabbits. We placed traps near rabbit runs, pellet piles
and in dense vegetation, and baited them with apples and apple
cider. We opened traps in the evening, and checked and closed
them in the morning.
We placed trapped rabbits in a handling bag and manually
restrained them. We recorded mass (g), sex, right ear length
(mm), right hind foot length (mm), total body length (mm) and
unique markings, and classified rabbits as adult (more than
700 g) or juvenile (less than 700 g) [21]. We excluded rabbits
with a body mass index (calculated as the ratio between foot
size and mass) less than 80% of average from the study and
released them at the capture site because of their potentially
poor condition. We fitted adult rabbits in good condition with
a Sirtrack (Havelock North, New Zealand) V5C 161 (28 g)
radio transmitter in the 166 MHz range with a mortality sensor.
We immediately released rabbits captured at the control site
(FAK) and transported marsh rabbits captured from donor sites
(STA) in individual 58  37  29 cm plastic pet carriers. Given
the successful implementation of hard release (directly into the
environment) protocols for other marsh rabbit translocations
[22], we released translocated marsh rabbits within 6 h of proces-
sing. We maintained a balanced sex ratio at each site and released
members of the same sex at least 60 m apart [22].
We tracked rabbits via triangulation at least once every 48 h
using a hand held receiver (TRX-2000, Wildlife Materials
Murphysboro, IL, USA; or R-1000, Communication Specialists,
Orange, CA, USA) and a three-element Yagi antenna (Wildlife
Materials, Murphysboro, IL, USA). If we detected a mortality
signal or if a rabbit was in the same location for consecutive
tracking sessions, we homed in on the rabbit to obtain a visual
observation. We recorded mortality locations using a Garmin

(Olathe, KS, USA) eTrex 20 handheld global position system
unit at the physical location of the animal.

(d) Cause-specific mortality
We examined mortality sites to determine the likely cause of
death, and classified mortalities as predations by python,
avian, mammalian,
reptilian
(non-python) and unknown
endothermic predators. We classified rabbit mortalities as from
an avian predator based on bird faecal sprays, presence of feath-
ers, removal of eyes, fur and internal organs spread around the
carcass in a 2050 cm diameter circle and/or beak impressions
on the collar [23,24]. We classified rabbit mortalities as from a
mammalian predator based on the presence of mammal scats
and tracks, opening of the body and removal of organs, skin
'pulled over the legs', bite marks to the head, the breaking of
one or more long bones and/or the burial of the carcass [24]. Pre-
dation by pythons and other reptiles was unique because reptiles
consumed the entire rabbit, allowing visual confirmation that the
transmitter was inside a snake or alligator. We identified repti-
lian predators to species and recorded the weight, length and
sex of animals when it was safe and reasonable to do so.
We stored carcasses of rabbits not obviously killed by a predator
at 2208C for 112 months and performed complete necropsies on
them at the Wildlife Research Laboratory (Florida Fish and Wildlife
Conservation Commission, Gainesville, FL, USA). We examined
fixed tissue samples embedded in paraffin, sectioned at 56 mm
and stained with haematoxylin and eosin. Following necropsy,
we classified rabbits that died within 10 days of release with signs
of pulmonary edema, severe autolysis, and cuts and laceration
consistent with trap injuries as trapping-related mortalities.
We used molecular techniques to further investigate rabbits
that showed signs of snake predation (anterior of body exhibiting
signs of partial ingestion). Specifically, we used quantitative PCR
(qPCR) to test for Burmese python DNA on the fur of two pre-
dated rabbits. We isolated DNA for all samples following
Qiagen's DNeasy Blood and Tissue kit (Valencia, CA, USA). We
used species-specific Burmese python qPCR primers with
TaqMan probes and TaqMan Fast Advanced Master Mix (Applied
Biosystems, Foster City, CA, USA) on the ABI StepOne-Plus
Real-Time system using the Fast qPCR profile. To avoid cross-
contamination of reagents and equipment, we included negative
controls and positive controls (rabbit and python tissue DNA
samples) in each qPCR. We conducted qPCR assays using three
technical replicates and sequenced traditional PCR products to
confirm species identification in positive samples. After necrop-
sies, we ruled out the possibility of predation by non-Burmese
python ectotherms. We categorized the remaining marsh rabbit
mortalities with signs of predation as caused by unknown
endothermic predators (mammals and birds).

(e) Predation risk analysis
We estimated cause-specific mortality risks among causative
agents using a non-parametric cumulative incidence function
estimator that is an extension of the Cox proportional hazards
model. We used animals in the study from 24 September 2012
until they died or were censored on 19 August 2013. We exam-
ined difference among sites and sex for the most common
causes of mortality by comparing cumulative incidence of com-
peting risk using a K-sample test [25]. To control for stress and
increased susceptibility to predators after translocation, we
excluded animals that had died within 10 days of their release
from the analysis (electronic supplementary material, table S1).
Similar to other studies [26,27], we observed that most rabbits
established stable home ranges and ceased extreme exploratory
behaviour after 10 days. We conducted our analysis using the
cmprsk package (v. 2.27) for R.

Table 1. Sources of mortality for marsh rabbits living more than 10 days in ENP at the Costal Prairie Trail (CPT) and East Taylor Slough (ETS) sites, and at
control and procedural control sites from 14 September 2012 to 19 August 2013. Number of mortalities outside parentheses, percentage of classified mortalities
per site inside brackets.a
endothermic
ectothermic
avian
mammalian
unknown
python
reptilian (non-python)
censored/alive
total
ENP (CPT)
1 (11%)
1 (11%)
1 (11%)
6 (66%)
0
3
12
ENP (ETS)
0
0
2 (15%)
11 (85%)
0
1
14
control
5 (18%)
20 (71%)
9 (24%)
0
3b (8%)
8
45
procedural
control
3 (38%)
3 (33%)
1 (11%)
0
2c (22%)
0
9
aThe percentages of mortalities classified as python and reptilian (non-python) were calculated using unknown endothermic mortalities values, the percentages
of classified avian and mammalian mortalities excluded unknown endothermic mortalities. Unknown endothermic mortalities were probably caused by mammals
and birds but not reptiles.
bRattlesnake.
cAmerican alligator.
rspb.royalsocietypublishing.orgProc.R.Soc.B282:201501204
For our comparative analysis, we pooled rabbits by sex after
finding no difference in cumulative hazard risk between the
sexes (test statistic  1.06, p  0.30). We also pooled both ENP
sites upon finding no difference in the cumulative hazard risk
between the sites from python (test statistic  0.55, p  0.50),
mammalian
(test
statistic  1.16, p  0.28) or avian
(test
statistic  1.27, p  0.28) predators. Similarly, we pooled the con-
trol and procedural control sites upon finding no difference in
the hazard risk from mammalian (test statistic  0.002, p  0.97)
and avian predators (test statistic  2.93, p  0.087).

( f ) Temporal variation in mortality rates
Like most ectothermic animals, python behaviour and physi-
ology are closely linked to environmental temperatures. Many
pythons feed more during warm seasons and their digestion
operates most efficiently at body temperatures greater than
258C [28,29]. Pythons are also highly aquatic and higher water
levels during summer may allow for easier access to areas of con-
gregated prey [21]. Accordingly, we predicted that, unlike that of
endothermic predators, predation by pythons would vary
with environmental conditions. We specifically hypothesized
higher python predation rates (i) with increasing temperatures
(temperature), (ii) when average biweekly temperatures excee-
ded 258C (more than 258C), (iii) with increased water levels in
major sloughs (water level), (iv) when water levels in major
sloughs exceeded 800 cm, flooding surrounding areas (more
than 800 cm), (v) with the additive influence of increased temp-
eratures and water levels (water level  temperature), (vi) under
the interactive influence of increased water levels and tempera-
tures (water level  temperature) and (vii) with temperature more
than 258C and water depths more than 800 cm (.800 cm &
258C). To determine if these environmental factors could explain
heterogeneity in marsh rabbit mortalities from pythons or other
major predators, we evaluated their influence on rabbit mortality
rates from pythons and mammals over the same time period,
which was 12 October 2012 (first week  4 rabbits on all sites)
to 25 July 2013 (end of week the last rabbit died in ENP).
We examined our hypotheses by developing two sets
(python and mammal) of seven candidate models that reflected
each hypothesis, as well as a constant model, and evaluated them
in a known-fate survival framework using MARK v. 7.1. We
pooled data from the release sites in ENP and pooled both con-
trol sites because we found no difference in the risk of
predation from mammals and pythons between these paired

sites. We populated climate variables using temperatures
recorded at the Homestead Air Force Base (National Climatic
Data Center) and water-level readings from the Everglades
Depth Estimation Network (EDEN) [30]. We identified the
most parsimonious models based on changes in Akaike's infor-
mation criterion corrected for small sample sizes (DAICc) and
AIC weights (vi).
(g) Pellet surveys
Prior to the translocation of marsh rabbits to ENP, we surveyed
the park for marsh rabbits using faecal pellet counts [31], road
cruising surveys and artificial latrines [32] near the CPT and
ETS study sites. To determine the persistence of the marsh
rabbit population after translocation to ENP, we checked and
cleared the artificial latrines at ETS once a month throughout
the course of the study. Additionally, after the translocations to
ENP, we searched for the presence of juvenile (less than 6 mm
in diameter) and adult (greater than 6 mm) marsh rabbit pel-
lets [21] in areas used by introduced marsh rabbits with a
grid of 10  10 m cells. We calculated mean pellet densities
(pellets m22) as the average number of pellets in a 1 m2 circular
plot at each grid node. In February 2013 (five months post-
release), we sampled a total of 5 ha of habitat; in December
2013 (15 month post-release), we resampled the same 5 ha and
expanded the survey area to encompass an additional 10 ha
used by radiotracked marsh rabbits.

3. Results
We captured, released and radiotracked 95 adult marsh rab-
bits from 14 September 2012 to 19 August 2013 (coastal
ENP  15, freshwater ENP  16, procedural control  15,
control  49). Eighty rabbits survived the 10-day adjustment
period needed to reduce exploratory movements and accli-
mate to the sites. Additionally, 10 rabbits were censored
after the 10-day adjustment period (e.g. lost signal from pre-
dation or equipment failure), and two rabbits were alive at
the end of the study, such that we documented 68 rabbit
mortalities. We classified the cause of mortality for 55 rab-
bits and listed the remaining 13 rabbits as mortalities from
an unknown endothermic predator (table 1). Marsh rabbits
in ENP faced the greatest risk of predation from pythons,

1.0
0.8
0.6
0.4
0.2
0
cumulative riskdays post-release
days post-release
0
50
100
150
200
250
300
0
50
100
150
200
250
300
(b)
(a)
mammalian
avian
python
mammalian
avian
reptilian (non-python)
Figure 2. Cumulative cause-specific predation risk for marsh rabbits from predators (a) in ENP (where pythons are established) and (b) at control and procedural
control site in regions of the GEE (where pythons have never or rarely been observed). Data were collected from 24 September 2012 to 19 August 2013.
0.30
0.25
0.20
0.15
0.10
0.05
0
temperature (C)
18
20
22
24
26
28
weekly mortality ratemortality from pythons
95% CI (mortality from mammals)
95% CI (mortality from pythons)
mortality from mammals
Figure 3. Estimates derived from our most parsimonious models of weekly marsh rabbit mortality from pythons and mammals as a function of temperature.
Python-induced mortality rates were generated from the known fates of 26 rabbits released in ENP. Mammal-induced mortality rates were generated from the
known fates of 55 rabbits in areas of the GEE with minimal invasive python activity. Models included data from 12 October 2012 to 25 July 2013.
rspb.royalsocietypublishing.orgProc.R.Soc.B282:201501205
which accounted for 77% of all mortalities (table 1). We attrib-
uted only one rabbit mortality in ENP to mammal predation.
This was in stark contrast to results from control sites, where
no rabbits were killed by pythons and we attributed 71%
of classified mortalities to mammals (table 1). Only three
rabbits (8%) at the control site were eaten by snakes, all
native rattlesnakes (Crotalus adamanteus).
Comparing ENP and the control sites, rabbits' cumulat-
ive hazard risk was markedly higher from pythons in ENP
(test statistic  15.28, p , 0.001; figure 2) and from mam-
mals on the control sites (test statistic  17.26, p , 0.001;
figure 2). We did not find a significant difference in the
cumulative hazard risk from avian predators (test statistic 
2.00, p  0.157; figure 2) between ENP and the control sites.
Mortality from non-python reptiles occurred only on the
control and procedural control site, and the hazard risk
was significantly higher on the procedural control site (test
statistic  10.98, p , 0.001; table 1).

We failed to detect marsh rabbits in ENP during extensive
surveys conducted prior to translocation. After translocation,
the presence of pellets on artificial latrines demonstrated that
marsh rabbits were present on the ENP release sites from
November 2012 to June 2013. We detected juvenile and adult
pellets from systematic pellet counts at the ENP release sites
in February 2013, demonstrating that reproduction was occur-
ring, but did not detect marsh rabbit pellets at either site
during extensive surveys in December 2013 (electronic sup-
plementary material, table S2). Consistent with our pellet
counts, we found temporal heterogeneity in the mortality
rates of rabbits eaten by pythons in ENP. Our most parsimo-
nious model showed rabbit mortality rates from pythons
increasing with rising temperatures (electronic supplementary
material, table S3; figure 3). Conversely, rabbit mortality rates
from the most common predators outside of ENP (mammals)
were not influenced by changing environmental conditions
(electronic supplementary material, table S4; figure 3).

rspb.royalsocietypublishing.orgProc.R.Soc.B282:201501206
4. Discussion
Our findings provide strong empirical evidence that pythons
caused reductions in marsh rabbit populations in ENP [2].
Not only were pythons the dominant predators of marsh rab-
bits in ENP, but only one mammalian predation event
occurred in the park. Outside of ENP, mammals (bobcats
Lynx rufus and coyotes Canis latrans) were the dominant
cause of marsh rabbit mortalities. The lack of mammalian
predations of marsh rabbits in ENP was consistent with
the reported declines of most mammalian species in the
park [2] and may be attributed to direct (predation) or indir-
ect (e.g. depletion of prey base) impacts of pythons on
populations of mammalian predators.
Five months after
their release
in February 2013,
marsh rabbits had established reproductive populations in
ENP (electronic supplementary material, table S2). However,
with
seasonally
increasing
temperatures,
ectothermic
pythons probably increased their foraging activity [33,34].
Marsh rabbit mortality increased above baseline rates at
temperatures over  258C, rising to over 11% per week
when average temperatures were more than 278C (figure 3).
Average weekly temperatures in ENP are generally over
278C for a 15-week period from mid-June to late September.
Increased water levels did not appear to have a substantial
influence on python's predation of marsh rabbits (electronic
supplementary material,
table S3). As both species are
strongly associated with water, it is possible that rising
water levels had little influence on how accessible marsh
rabbits were to pythons.
The seasonally high rates of mortality demonstrated in
this study help to explain the apparent capacity of pythons
to greatly reduce or eliminate marsh rabbits from ENP.
Nevertheless, attributing large reductions in rabbit popu-
lations to an apex predator appears to contradict ecological
theory. Reproductive parameters, not survival rates, should
most influence population growth of fecund, early-maturing
species like marsh rabbits [12]. One explanation for this con-
tradiction in theory is that marsh rabbits were naive to
predation by an introduced predator such as the Burmese
python. In fact, continental populations have often shown
elevated population suppression from alien compared with
native predators [35,36,37]. Indeed, ENP's marsh rabbits
and other mammals may have been ill-adapted to avoid pre-
dation by very large snakes, last present in the eastern USA at
20.616.3 Ma [2].
The loss of marsh rabbits and other mammals from ENP [2]
is probably causing a massive rearrangement of the ENP
food web, losses in ecosystem function, and complex and
unpredictable cascading effects [5,6,11]. As prey and predators
at multiple trophic levels, nutrient cyclers and engineers of

vegetation, mammals are an indispensable component of the
GEE [38,39]. Our research clearly establishes pythons as a
causal agent of marsh rabbit declines, a species we selected
because of its theoretical resilience to predation pressure
[16,17]. Accordingly, pythons are a logical and likely expla-
nation for the observed declines in less fecund mammalian
python prey species found in ENP (i.e. raccoon Procyon lotor,
round-tailed muskrat Neofiber alleni, bobcat) [8].
Only with the recovery of ENP's mammal populations will
it be possible to restore the health and functionality of this
World Heritage Site. However, it seems unlikely that marsh
rabbits and other mammal populations will rebound without
action to manage pythons, as pythons are capable of persisting
in the environment by switching to different prey and going
long periods without food [40,41]. Furthermore, as this study
illustrates, reintroductions and augmentations alone show
little promise for recovering the park's mammals. Without
effective tools and a strategy for reducing the prevalence of
these invasive snakes [20], the dire state of mammals in the
Everglades will probably remain unchanged, and even
spread if python populations expand northward or become
established elsewhere in the USA [42].

Disclaimer. The findings of this study do not necessarily reflect the opinion
of the Florida Fish and Wildlife Conservation Commission, Gainesville,
Florida and all opinions expressed are those of the authors.
Ethics statement. All trapping, handling and tracking protocols were
conducted under a permit from the Florida Fish and Wildlife Conser-
vation Commission (LSSC-1200039) and were approved by the
University of Florida's Non-Regulatory Animal Research Committee
(005-WEC).
Data accessibility. Data are available as electronic supplementary
material.
Acknowledgements. Special thanks to ENP, Arthur R. Marshall Loxa-
hatchee National Wildlife Refuge, Big Cypress National Preserve,
Fakahatchee Strand Preserve State Park and the Florida Fish and Wild-
life Conservation Commission for their assistance on this project.
Rabbit-capturing efforts were led by J. Schmidt and field data were col-
lected by E. Larrivee, C. Robinson, A. Waag, H. Crowell, K. Powell,
M. McEachern and M. Hanson and volunteers. Dr Teri Johnson with
the Florida Department of Agriculture and Consumer Services per-
formed the histological examinations of necropsied rabbits. Any use
of trade, product, or firm names is for descriptive purposes only and
does not imply endorsement by the US Government.
Author contributions. R.A.M., R.N.R. and K.M.H. conceived the study;
A.S. conducted and supervised data collection; R.A.M. and A.S. ana-
lysed the data; M.E.H conducted molecular analysis; M.W.C and A.S.
conducted necropsies; and R.A.M. and A.S. drafted the manuscript.
All authors contributed to the interpretation of the results and
revised the manuscript.
Funding statement. This research was funded by ENP and Big Cypress
National Preserve, the US Geological Survey Priority Ecosystem
Science Program and the University of Florida Institute of Food
and Agricultural Science.

References

1.
Richardson DM, Ricciardi A. 2013 Misleading
criticisms of invasion science: a field guide. Divers.
Distrib. 19, 14611467. (doi:10.1111/ddi.12150)
2.
Dorcas ME et al. 2012 Severe mammal declines
coincide with proliferation of invasive Burmese
pythons in Everglades National Park. Proc. Natl
Acad. Sci. USA 109, 24182422. (doi:10.1073/pnas.
1115226109)

3.
Lodge TE. 2010 The Everglades handbook: understanding
the ecosystem. Boca Raton, FL: CRC Press.
4.
Duffy JE. 2002 Biodiversity and ecosystem function: the
consumer connection. Oikos 99, 201219. (doi:10.
1034/j.1600-0706.2002.990201.x)
5.
Duffy JE. 2003 Biodiversity loss, trophic skew and
ecosystem functioning. Ecol. Lett. 6, 680687.
(doi:10.1046/j.1461-0248.2003.00494.x)

6.
Estes JA et al. 2011 Trophic downgrading of planet
earth. Science 333, 301306. (doi:10.1126/science.
1205106)
7.
Willson JD, Dorcas ME, Snow RW. 2011 Identifying
plausible scenarios for the establishment of invasive
Burmese pythons (Python molurus) in Southern
Florida. Biol. Invasions 13, 14931504. (doi:10.
1007/s10530-010-9908-3)

rspb.royalsocietypublishing.orgProc.R.Soc.B282:201501207
8.
Snow RW, Brien ML, Cherkiss MS, Wilkins L,
Mazzotti FJ. 2007 Dietary habits of the
Burmese python, Python molurus bivittatus, in
Everglades National Park, Florida. Herpetol. Bull.
101, 57.
9.
Savidge JA. 1987 Extinction of an island forest
avifauna by an introduced snake. Ecology 68,
660668. (doi:10.2307/1938471)
10. Hays WST, Conant S. 2007 Biology and impacts of
Pacific Island invasive species: 1. A worldwide
review of effects of the small Indian mongoose,
Herpestes javanicus (Carnivora: Herpestidae). Pacific
Sci. 61, 316. (doi:10.1353/psc.2007.0006)
11. Donlan CJ, Wilcox C. 2008 Diversity, invasive species
and extinctions in insular ecosystems. J. Appl. Ecol.
45, 11141123. (doi:10.1111/j.1365-2664.2008.
01482.x)
12. Oli MK, Dobson FS. 2003 The relative importance of
life-history variables to population growth rate in
mammals: Cole's prediction revisited. Am. Nat. 161,
422440. (doi:10.1086/367591)
13.
Cole LC. 1954 The population consequences of life
history phenomena. Q. Rev. Biol. 29, 103137.
(doi:10.1086/400074)
14. McKinney ML. 1997 Extinction vulnerability and
selectivity: combining ecological and
paleontological views. Annu. Rev. Ecol. Syst. 28,
495516. (doi:10.1146/annurev.ecolsys.28.1.495)
15.
Chapman JA, Willner GR. 1981 Sylvilagus palustris.
Mamm. Species 153, 13.
16.
Trout RC, Tittensor AM. 1989 Can predators regulate
wild rabbit Oryctolagus cuniculus population-density
in England and Wales. Mamm. Rev. 19, 153173.
(doi:10.1111/j.1365-2907.1989.tb00409.x)
17.
Pech RP, Sinclair ARE, Newsome AE, Catling PC.
1992 Limits to predator regulation of rabbits in
Australiaevidence from predator-removal
experiments. Oecologia 89, 102112. (doi:10.1007/
BF00319021)
18.
Snow RW, Krysko KL, Enge KM, Oberhofer L,
Warren-Bradley A, Wilkins L. 2007 Introduced
populations of Boa constrictor (Boidae) and Python
molurus bivitattus (Pythonidae) in southern Florida.
In The biology of boas and pythons (eds
RW Henderson, R Powell), pp. 416438. Eagle
Mountain, UT: Eagle Mountain Publishing.
19.
Center for Invasive Species and Ecosystem Health
2015 Burmese python. Tifton, GA: University of
Georgia. See http://www.eddmaps.org/florida/
distribution/viewmap.cfm?sub=20461.
20.
Reed RN, Hart KM, Rodda GH, Mazzotti FJ, Snow
RW, Cherkiss M, Rozar R, Goetz S. 2011 A field test

of attractant traps for invasive Burmese pythons
(Python molurus bivittatus) in southern Florida.
Wildl. Res. 38, 114121. (doi:10.1071/WR10202)
21.
Forys EA, Humphrey SR. 1997 Comparison of 2
methods to estimate density of an endangered
lagomorph. J. Wildl. Manag. 61, 8692. (doi:10.
2307/3802417)
22.
Faulhaber CA, Perry ND, Silvy NJ, Lopez RR, Frank
PA, Peterson MJ. 2006 Reintroduction of Lower Keys
marsh rabbits. Wildl. Soc. Bull. 34, 11981202.
(doi:10.2193/0091-7648(2006)34[1198:ROLKMR]2.0.
CO;2)
23.
Brown AL, Litvaitis JA. 1995 Habitat features
associated with predation of New England
cottontailswhat scale is appropriate? Can. J. Zool.
73, 10051011. (doi:10.1139/z95-120)
24. Henning J, Pfeiffer DU, Davies PR, Stevenson MA,
Meers J. 2008 Mortality patterns over 3 years in a
sparse population of wild rabbits (Oryctolagus
cuniculus) in New Zealand, with an emphasis
on rabbit haemorrhagic disease (RHD).
Eur. J. Wildl. Res. 54, 619626. (doi:10.1007/
s10344-008-0187-6)
25. Gray RJ. 1988 Class of k-sample tests for comparing
the cumulative incidence of a competing risk. Ann.
Stat. 16, 11411154. (doi:10.1214/aos/
1176350951)
26.
Calvete C, Villafuerte R, Lucientes J, Osacar JJ. 1997
Effectiveness of traditional wild rabbit restocking in
Spain. J. Zool. 241, 271277. (doi:10.1111/j.1469-
7998.1997.tb01957.x)
27. Watland AM, Schauber EM, Woolf A. 2007
Translocation of swamp rabbits in southern Illinois.
Southeast. Nat. 6, 259270. (doi:10.1656/1528-
7092(2007)6[259:TOSRIS]2.0.CO;2)
28. Wang T, Zaar M, Arvedsen S, Vedel-Smith C,
Overgaard J. 2002 Effects of temperature on the
metabolic response to feeding in Python molurus.
Comp. Biochem. Physiol. A 133, 519527. (doi:10.
1016/S1095-6433(02)00250-7)
29.
Slip DJ, Shine R. 1988 Feeding habits of the
diamond python, Morelia s. spilotaambush
predation by a boid snake. J. Herpetol. 22,
323330.
30.
Telis P. 2006 The Everglades Depth Estimation
Network (EDEN) for support of ecological and
biological assessments. Fact sheet 3087. Jacksonville,
FL: US Geological Survey.
31.
Schmidt JA, McCleery RA, Schmidt PM, Silvy NJ,
Lopez RR. 2011 Population estimation and
monitoring of an endangered lagomorph. J. Wildl.
Manag. 75, 151158. (doi:10.1002/jwmg.17)

32.
Schauber EM, Scharine PD, Nielsen CK, Rubert L.
2008 An artificial latrine log for swamp rabbit
studies. J. Wildl. Manag. 72, 561563. (doi:10.
2193/2007-234)
33. Heard GW, Black D, Robertson P. 2004 Habitat use
by the inland carpet python (Morelia spilota
metcalfei: Pythonidae): seasonal relationships with
habitat structure and prey distribution in a rural
landscape. Austral Ecol. 29, 446460. (doi:10.1111/
j.1442-9993.2004.01383.x)
34. Madsen T, Shine R. 1996 Seasonal migration of
predators and preya study of pythons and rats in
tropical Australia. Ecology 77, 149156. (doi:10.
2307/2265663)
35.
Salo P, Korpimaki E, Banks PB, Nordstrom M,
Dickman CR. 2007 Alien predators are more
dangerous than native predators to prey
populations. Proc. R. Soc. B 274, 12371243.
(doi:10.1098/rspb.2006.0444)
36.
Simberloff D et al. 2013 Impacts of biological
invasions: what's what and the way forward.
Trends Ecol. Evol. 28, 5866. (doi:10.1016/j.tree.
2012.07.013)
37.
Paolucci EM, MacIsaac HJ, Ricciardi A. 2013
Origin matters: alien consumers inflict greater
damage on prey populations than do native
consumers. Divers. Distrib. 19, 988995. (doi:10.
1111/ddi.12073)
38. Olofsson J, de Mazancourt C, Crawley MJ. 2007
Contrasting effects of rabbit exclusion on nutrient
availability and primary production in grasslands at
different time scales. Oecologia 150, 582589.
(doi:10.1007/s00442-006-0555-4)
39. Olofsson J, de Mazancourt C, Crawley MJ. 2008
Spatial heterogeneity and plant species richness at
different spatial scales under rabbit grazing.
Oecologia 156, 825834. (doi:10.1007/s00442-008-
1038-6)
40. McCue MD. 2007 Snakes survive starvation by
employing supply- and demand-side economic
strategies. Zoology 110, 318327. (doi:10.1016/j.
zool.2007.02.004)
41.
Reed RN, Willson JD, Rodda GH, Dorcas ME.
2012 Ecological correlates of invasion impact
for Burmese pythons in Florida. Integr. Zool.
7, 254270. (doi:10.1111/j.1749-4877.2012.
00304.x)
42.
Rodda GH, Jarnevich CS, Reed RN. 2009 What parts
of the US mainland are climatically suitable for
invasive alien pythons spreading from Everglades
National Park? Biol. Invasions 11, 241252. (doi:10.
1007/s10530-008-9228-z)