CHARACTERISTICS AND CONSEQUENCES OF A MUTUALISM BETWEEN LONG-LEGGED WADING BIRDS AND THE AMERICAN ALLIGATOR IN THE
SOUTHEASTERN US
By
WRAY GABEL
A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
UNIVERSITY OF FLORIDA
2019
© 2019 Wray Gabel
To my parents, who don’t really know what I’m doing but support me regardless
4
ACKNOWLEDGMENTS
Firstly, I would like to humbly thank my advisor Peter Frederick for his excellent
guidance and advice throughout this entire experience and for so generously supporting
my frequent left-brain antics. I would also like to acknowledge and appreciate the
contributions to this project made by my other committee members Scott Robinson and
Katie Sieving.
I owe many thanks to Ash Meade and Will Kennerley for being amazing field
technicians and even better friends. I am also grateful to Lindsey Garner for her infinite
wisdom on the Everglades, general project logistics, and for serving as my resident
expert on alligators in North Carolina. Thank you also to Jabi Zabala for putting up with
my constant interruptions into his own workload from my endless inquiries. None of this
would have been possible without his statistics, coding, and excel mastery.
I would like to give a huge thank you to Dr. Carmen Johnson at the North
Carolina Wildlife Resources Commission for providing me with the wading bird colony
location data needed to complete the second half of this thesis and for her timely and
thurough responses to my many emails. I would also like to extend my gratitude to Dr.
Joe Afmuth, who spent many hours patiently meeting with me and showing me how to
master GIS. He taught me how to think independently and how to solve my own
problems using the software, which I didn’t enjoy as much at the time but am now very
grateful to him for the skills that I have.
A special thank you to Rock Delliquanti for volunteering his time to help me
deploy my chickens, for lending me his very creative mind to help me invent a chicken
dropping mechanism (and his patience as I did so in our 300 square foot apartment),
but most of all for his unwavering support. Without you I would probably still be watching
5
game camera footage. Finally, I would like to thank my parents for their constant
encouragement and for showing me how to really “wow” people.
This work was supported by the United States Army Corps of Engineers through
contracts to Dr. Peter Frederick (W912HZ-15-2-0007 and W912HZ-15-2-0017).
6
TABLE OF CONTENTS page
ACKNOWLEDGMENTS .................................................................................................. 4
LIST OF TABLES ............................................................................................................ 8
LIST OF FIGURES .......................................................................................................... 9
ABSTRACT ................................................................................................................... 10
CHAPTER
1 OVERVIEW ............................................................................................................ 12
2 NESTLING CARCASSES FROM COLONIALLY NESTING WADING BIRDS: PATTERNS OF ACCESS AND ENERGETIC RELEVANCE FOR THE AMERICAN ALLIGATOR AND OTHER SCAVENGERS ........................................ 14
Introduction ............................................................................................................. 14
Methods .................................................................................................................. 18 Study Site ......................................................................................................... 18 Bait Characteristics and Placement .................................................................. 20
Environmental Covariates of Bait Consumption ............................................... 21 Monitoring Fate of Baits.................................................................................... 22 Data Analysis ................................................................................................... 23 Energetic Caluclations ...................................................................................... 24
Results .................................................................................................................... 26 Description of Consumers ................................................................................ 27
Correlatess of Alligator Consumption ............................................................... 28 Correlates of Vulture Consumption .................................................................. 28 Significance of Nestling Carcasses to Scavengers .......................................... 29
Discussion .............................................................................................................. 29
3 EFFECTS OF ALLIGATOR PRESENCE ON BREEDING COLONY SITE SELECTION BY LONG-LEGGED WADING BIRDS ............................................... 44
Introduction ............................................................................................................. 44
Methods .................................................................................................................. 48 Study Site ......................................................................................................... 48 Colony Data and Main Methods of Defense ..................................................... 50 Alternative Methods of Defense ....................................................................... 52 Colony Control Points ....................................................................................... 54 Data Analysis ................................................................................................... 55
Results .................................................................................................................... 56 Main Methods of Protection .............................................................................. 56 Alternative Methods of Protection ..................................................................... 57
7
Discussion .............................................................................................................. 58
4 SUMMARY ............................................................................................................. 72
APPENDIX CHAPTER 3 SUPPORTING MATERIAL: DETAILED SURVEY METHODS FOR WADING BIRD COLONIES IN NORTH CAROLINA .... 74
LIST OF REFERENCES ............................................................................................... 76
BIOGRAPHICAL SKETCH ............................................................................................ 92
8
LIST OF TABLES
Table page 2-1 Comparison of biotic and abiotic qualities of bait deployment sites on defined
island and colony types ...................................................................................... 37
2-2 Raw counts and relative percent consumption of 160 baits with known fates by consumers on different island types and colony types in the Everglades ...... 38
2-3 Consumption of baits by alligator size class on islands or colonies of different types in the Everglades ...................................................................................... 39
2-4 Results of the best generalized linear mixed-effects model assessing effect of covariates on probability of carcass consumption by alligators ...................... 40
2-5 Results of the best generalized linear mixed-effects model assessing effect of covariates on probability of carcass consumption by Turkey Vultures ............ 42
3-1 Results of the best linear mixed-effects model assessing effect of alligator probability and alternative methods of protection on relative colony distance from the mainland.. ............................................................................................. 67
3-2 Results of the best linear mixed-effects model assessing effect of alligator probability and alternative methods of protection on relative colony distance from islands >5ha.. ............................................................................................. 68
9
LIST OF FIGURES
Figure page 2-1 Map of the study area with locations for all wading bird nesting colonies
sampled.. ............................................................................................................ 36
2-2 Modeled probabilities of bait consumption by alligators and vultures in relation to main covariates .................................................................................. 41
2-3 Estimated number of scavengers supported annually during a wading bird nesting period of 60 days for alligators and Turkey Vultures.. ............................ 43
3-1 Map of the study area with locations for all wading bird colonies and control islands in areas with alligators likely and unlikely ............................................... 65
3-2 Map of a section of the study area showing locations for wading bird colonies and associated control points on islands, the mainland, and landmasses >5ha. .................................................................................................................. 66
3-3 Colony island distance relative to control islands from A) the mainland and from B) landmasses >5ha, as a fcuntion of alligator probability .......................... 69
3-4 Colony island distance relative to control islands from A) the mainland and from B) landmasses >5ha, as a function of distance to human development and alligator probability ....................................................................................... 70
3-5 Mainland and island colony caracteristics of A) longevity (number of years) and B) colony size (total number of nesting birds) relative to alligator probability ........................................................................................................... 71
10
Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science
CHARACTERISTICS AND CONSEQUENCES OF A MUTUALISM BETWEEN LONG-
LEGGED WADING BIRDS AND THE AMERICAN ALLIGATOR IN THE SOUTHEASTERN US
By
Wray Gabel
December 2019
Chair: Peter C. Frederick Major: Wildlife Ecology and Conservation
Ecological mutualisms shape community ecology by ensuring protection from
predators and increased access to limited nutrients. Evidence suggests a mutualism
between nesting wading birds (Ciconiiformes) and the American Alligator (Alligator
mississippiensis), where alligators deter mammalian predators from wading bird nesting
colonies and, in turn, gain a food source from nestling carcasses.
The magnitude and relevance of nestlings as a food source to alligators and the
scavenger community is poorly understood. I used trail cameras to quantify the
proportion of available nestlings that were consumed by scavengers in the Everglades
of Florida. Overall, 85% of 160 carcasses were consumed, with Turkey Vultures
(Cathartes aura, 47%) and American Alligators (29%) the primary consumers.
Probability of consumption by alligators or vultures was related to distance from nest to
water, nesting density, and island type. I estimate fallen nestlings throughout this
ecosystem could support 16% of the alligator population and 147 adult Turkey Vultures
during the nesting season.
11
I predicted that nesting wading birds change colony site preferences when
alligators are not present to serve as nest protectors. I compared colony characteristics
with likely and unlikely alligator presence in colonies throughout North Carolina,
controlling for availability of habitat. Wading birds prefer islands that are farther from the
mainland, farther from landmasses >5ha, and farther from human development when
alligator presence is unlikely compared to when alligators are likely. Understanding the
complexities of this mutualistic relationship has global implications for management,
since colonially nesting birds and crocodilians co-occur in many tropical and subtropical
wetlands.
12
CHAPTER 1 OVERVIEW
Ecologists have long recognized the role of predation and competition as primary
species interactions that shape natural communities (Bruno et al. 2003). However,
positive ecological interactions, such as mutualisms and commensalisms, now also
appear to be a strong force shaping community ecology in many cases as an evolved
response to predation pressures (Stachowicz 2001, Bruno et al. 2003, Silliman et al.
2011, van der Zee et al. 2016, Altieri et al. 2017). Both mutualisms and commensalisms
are considered facilitative relationships (Stachowicz 2001, Bronstein 2009), and while
facilitation can take on many different definitions (described in Bronstein 2009), it is
defined here as an ecological interaction that benefits at least one of the participants
while causing harm to neither (Bruno et al. 2003). These positive ecological interactions
can benefit the associated species in various ways, often ensuring protection from
predators and increased access to limited nutrients (Stachowicz 2001). It is important to
understand these interactions in order to fully comprehend the intricacies of
codependence, community dynamics, and species distribution (Brooker et al. 2008, Nell
et al. 2016).
Predation and limited nutrient availability appear to have driven the emergence of
a non-obligate mutualistic relationship between nesting wading birds (Ciconiiformes)
and the American Alligator (Alligator mississippiensis). Alligators facilitate a safer
nesting location for wading birds by serving as nest protectors and deterring dangerous
mammalian mesopredators such as North American raccoons (Procyon lotor) and
Virginia opossums (Didelphis virginiana), which are prevalent nest predators, from
wading bird colonies (Nell et al. 2016, Burtner and Frederick 2017). Alligators receive
13
food from nesting wading birds in the form of fallen nestlings, supplied by the normal
process of brood reduction. These chicks may be an important form of energy transfer
that is delivered directly to large-bodied scavengers such as the American Alligator (Nell
and Frederick 2015). Despite being a facultative association, this interaction between
alligators and wading birds appears to be highly beneficial for both species and
illustrates how selective pressures of nutrient stress and predation may have acted to
form and reinforce a strongly positive ecological association.
Overall, there are many gaps in our knowledge of alligator-wading bird
interactions that are slowing the progress in our understanding of how this mutualistic
relationship evolves and persists. First, while alligators and other vertebrate scevengers
in this ecosystem appear to benefit from this additional food source of fallen nestlings, it
is unclear the extent to which they are utilizing it. Second, to understand the strength
and durability of these nest protector relationships in the natural community we need to
observe the effects of an absence of the benefits provided by the nest protector
(Bronstein 2009).
Here, I advance the understanding of this interspecific relationship with tests
concerning benefits to both species by (1) quantifying the proportion of available heron
and egret nestlings consumed by different scavengers and identifying the conditions
under which scavengers consume carcasses and (2) determining how wading birds
change their colony site selection preferences based on the likelihood of alligator
presence. This thesis will explore the effect of a mutualistic nest protector relationship
on both parties in these respects.
14
CHAPTER 2 NESTLING CARCASSES FROM COLONIALLY NESTING WADING BIRDS:
PATTERNS OF ACCESS AND ENERGETIC RELEVANCE FOR THE AMERICAN ALLIAGTOR AND OTHER SCAVENGERS
Introduction
Energy transfer underlies many fundamental ecosystem processes (Lindeman
1942, Bertness 1984, Frederick and Powell 1994, Ehrenfeld and Toth 1997, Høberg et
al. 2002), and nutrient subsidies and flow are critical to community composition and
productivity (Bildstein et al. 1992, Subalusky and Post 2019). In wetland systems, inputs
of allochthonous materials are broadly thought to occur via physical processes (Sutula
et al. 2001). However, aggregations of colonially breeding birds may also constitute
significant nutrient and energy vectors because they concentrate energy from a much
larger foraging area (Bildstein et al. 1992, Frederick and Powell 1994, Post et al. 1998,
Sekercioglu 2006). For example, seabirds transport marine productivity to land (Polis
and Hurd 1996, Stapp et al. 1999, Sanchez-Pinero and Polis 2000, Ellis 2005), which
provides energy that supports a variety of different consumers and scavengers
(Sanchez-Pinero and Polis 2000, Sekercioglu 2006) in otherwise unproductive coastal
islands. In wetland ecosystems, White Ibises (Eudocimus albus) were found to import
33% as much phosphorus to an estuary as atmospheric sources (Bildstein et al. 1992),
and this additional nutrient concentration can have lasting effects on the
biogeochemistry of nesting sites (Oliver and Schoenberg 1989, Davis 1994, Irick et al.
2015). At roosting sites or in breeding colonies, waterbirds can import enough nutrients
to cause major shifts in the trophic status of wetlands (Green and Elmberg 2014) and
migratory waterfowl may be responsible for 40% of the nitrogen and 75% of the
phosphorous contributions to their roosting wetlands (Post et al. 1998). These effects
15
from nutrient subsidy are more pronounced when the receiving ecosystem productivity
is less than that of the donor ecosystem (Subalusky and Post 2019). Allochthonous
input and redistribution via the action of animals appears to be a key process driving the
dynamics of these naturally oligotrophic aquatic ecosystems.
Previous research has focused on input of nutrients through feces as the main
mechanism of nutrient subsidy by colonially nesting birds (Bildstein et al. 1992,
Frederick and Powell 1994, Irick et al. 2015). Carcasses from nesting birds or their
chicks may also be a major contribution of readily available energy (Williams et al. 1978,
Sanchez-Pinero and Polis 2000, Nell and Frederick 2015, Nell et al. 2016), and
carcasses are a high quality animal subsidy input (Subalusky and Post 2019).
Scavengers appear to be attracted to large colonial aggregations of nesting birds both
because the density of readily available food sources is high, and because minimal
effort may be required to find and acquire nestling prey (Butler et al. 1985, Hunter 1991,
Howald et al. 1999, Wilson and Wolkovich 2011). However, carcass consumption by
vertebrate scavengers is a phenomenon infrequently quantified (DeVault et al. 2003,
2016), especially at bird colonies.
By directly consuming carcasses, scavengers can maintain energy flows higher
up in the food chain (DeVault et al. 2003, Sekercioglu 2006), which can have a
stabilizing effect on asynchronous ecosystem dynamics (Rooney et al. 2006, Moleón et
al. 2014, Subalusky and Post 2019). Scavenging is a significant form of energy transfer
between trophic levels distinct from predation, parasitism, and disease and large inputs
of biomass from bird colonies can maintain multispecies scavenger communities that
dominate the carnivore trophic level in many ecosystems (Wilson and Wolkovich 2011).
16
Vertebrate scavengers undergo intensive intraguild competition for these carrion
resources in terrestrial environments (Ruxton and Houston 2004, Beasley et al. 2012,
2015, Moreno-Opo and Margalida 2013, Kane et al. 2016), especially in warm climates
(DeVault et al. 2003). Temporal pulses of carcass availability, such as herd migrations
(Subalusky et al. 2017) or salmon runs (Hewson 1995, Ben-David et al. 1997), can be
important for sustaining vertebrate scavenger populations (Wilson and Wolkovich 2011,
DeVault et al. 2016, Subalusky and Post 2019), and scavenger community composition
changes with environmental conditions (Beasley et al. 2012, Kane et al. 2016). The
importance of facultative scavenging may be largely under-represented in food studies,
because stomach content analyses cannot differentiate scavenging from predation
(DeVault et al. 2003).
Scavenging may be particularly favored when available energy density is high, as
in concentrations of breeding birds. In addition to breeding densely, some colonially
nesting birds lay more eggs than they can raise and adjust their brood size to fit
available food resources by reducing the size of the resultant broods (Ricklefs 1965,
Clark and Wilson 1981, Mock 1984, Stenning 1996, Nell and Frederick 2015). During
brood reduction, 1–2 chicks, which are usually in poor condition, are ejected or fall from
the nest when environmental conditions do not favor their survival. Particularly in large
breeding aggregations, the biomass of fallen chicks can constitute a large pool of
potential food for scavengers. This life-history strategy interacts strongly with population
size to determine the overall quantity and quality of nutrient subsidies (Subalusky and
Post 2019). Nell and Frederick (2015) estimated that fallen nestling carcasses of long-
legged wading birds (Ciconiiformes) in the Florida Everglades ecosystem could support
17
hundreds of American Alligators (Alligator mississippiensis) for periods of several
months, assuming all carcasses were consumed solely by alligators. They also found
that alligators residing within wading bird colonies had improved body condition
compared to those not in colonies (Nell et al. 2016). Alligators and other ectotherms
with low maintenance metabolisms have a physiology that is well suited to taking
advantage of the typically ephemeral availability of carrion (DeVault and Krochmal
2002).
The fate of avian carrion has received comparatively less attention than that of
mammals, and the relevance of the effect of environmental complexity in resource
sharing among scavengers has only recently been described. Smith et al. (2017)
showed that the fate of avian carcasses in trees differed from those on the ground,
suggesting that habitat complexity could alter access to food by scavengers. However,
the relevance of other environmental factors, such as vegetation complexity or distance
to water, on scavenger accessibility and the ecological significance of bird carcasses to
the scavenger community remains largely unknown. This is particularly pertinent in bird
breeding colonies because they are a source of dense, temporally pulsed
concentrations of carcasses that are widespread in many regions of the globe. In most
bird colonies, the proportion of carcasses that are actually consumed by scavengers,
and their fate in relation to environmental features is undescribed.
Here, I quantify the proportion of available heron and egret nestlings consumed
by different scavengers and identify the conditions under which scavengers consume
carcasses in a variety of colonies in a large wetland ecosystem. Based on the
observation that scavengers are attracted to aggregations of breeding birds (Butler et al.
18
1985, Hunter 1991, Howald et al. 1999), I hypothesized that carcasses would be more
readily consumed in active colony islands (islands with breeding birds) than in non-
colony islands (islands of similar characteristics but no breeding pairs present). I also
hypothesized that carcass consumption would be higher where access by alligators
appears to be easier or more rewarding (smaller Egretta heron islands, denser nesting,
closer proximity to water). I also assumed that alligators might defend this potentially
valuable food resource from one another (Nifong 2014), and that competitive outcomes
would be size dependent (Garrick and Lang 1977, Kushlan and Kushlan 1980, Vliet
1989). I therefore predicted that alligators consuming baits in active colony islands
would be larger than alligators on inactive islands. I examined environmental features
correlated with carcass consumption by different scavengers to better understand
resource partitioning. By using long-term systematic surveys of wading bird colonies in
this ecosystem and ground-based monitoring of reproductive success in select colonies,
I was able to determine the number and energetic relevance of nestlings available
during each breeding season and to estimate the net effect of this food source on
scavenger populations over many years.
Methods
Study Site
I studied wading bird colonies on tree islands in Water Conservation Areas 3A
and 3B (hereafter WCA-3A and WCA-3B) of the central Everglades, Miami-Dade and
Broward counties, Florida (Figure 2-1). These wetlands (2,370 km2) are seasonally
flooded with slightly elevated sawgrass (Cladium jamaicense) dominated ridges
interspersed with deeper-water channels (sloughs) and small tree islands scattered in
the grassland (Loveless 2006, Lodge 2016). Within the study area, egrets and herons
19
nest almost exclusively on inundated tree islands (depth typically <0.5m) dominated by
willow (Salix caroliniana) or cypress (Taxodium ascendens and Taxodium distichum,
Frederick and Collopy 1988, 1989). These tree islands usually feature one or more
small ponds or depressions created and used by alligators as dry-season refugia
(Mazzotti and Brandt 1994, Palmer and Mazzotti 2004). All heron and egret nesting
takes place during the dry season (January through June). I located wading bird
colonies using annual full-coverage systematic aerial surveys conducted monthly in
WCA-3A and WCA-3B (Frederick and Ogden 2002).
I studied scavenging by monitoring baits placed on two island types: active and
inactive. Active colonies included all active wading bird colony islands with enough
nests and nesting area to meet the bait placement requirements (N=26, see below). I
also defined a set of comparison islands without nesting activity (N=6, “inactive”
hereafter) as islands that were low in elevation, had willow or cypress vegetation, were
in the same size range and general location as breeding colonies (<5km away), and had
evidence of alligator activity such as alligator trails or sightings (Figure 2-1, Table 2-1).
Active colonies were categorized into two colony types: Ardea heron islands and
Egretta heron islands. Ardea heron islands are large oblong islands (average 11,816.86
m2) dominated by larger sized Ardea herons including Great Egrets (Ardea alba) and
Great Blue Herons (Ardea herodias). Egretta heron islands are small round islands
(average 1,554.79 m2) dominated by smaller sized herons and egrets such as Snowy
Egrets (Egretta thula), Little Blue Herons (Egretta caerulea), and Tricolored Herons
(Egretta tricolor; Figure 3, Table 5). The obvious differences in species composition
between these two colony types led us to treat them as separate.
20
Bait Characteristics and Placement
I used chicken carcasses 284-397 grams (RodentPro, Inglefield, IN, USA) as a
standardized surrogate for all Egretta heron chicks (N=31) and carcasses 397-510
grams as a standardized surrogate for all Ardea heron chicks (N=171). These sizes
were based on the average size of chicks of these species at the average age of
nestling death in reduced broods (Nell and Frederick 2015).
On each colony island, I selected 3-5 active wading bird nests and deployed
baits on the ground (N=146) or in water (N=54) immediately below them. I buffered all
baited nests by 9.1m (30 feet) and avoided deploying consecutive baits along existing
waterways within islands. I did not deploy more than five baits per island-visit to prevent
resident scavengers from being unnaturally attracted to baits. I chose nests that had live
chicks matching the approximate size of the baits to control for possible age-related
effects of attractive nest noises or feces. I used a stratified-random method to select
nests that included a range of values for covariates of interest (see below).
Baits on inactive islands were placed along east-west transects, under trees,
using a 9.1m (30 foot) buffer between baits. Transects began when the first tree was
observed as I proceeded onto the island from the water’s edge and ended when I had
deployed all five baits or reached the far side of the island. I deployed baits at colony
and inactive islands between one and three occasions, with a minimum of two weeks
between successive visits to the same island. I tethered all baits using 2.7kg (6lb) test
fishing line to ensure baits were not displaced by currents if placed in the water. At the
time of deployment baits were thawed but not yet decomposing. The fate of baits was
monitored using trail cameras (see below).
21
Environmental Covariates of Bait Consumption
In addition to island type and colony type, we measured nine environmental
covariates of bait consumption for inclusion in our model: distance to water, distance to
canal, distance to alligator hole, temperature, vegetation complexity, vegetation density,
colony size, nest density, and carcass latency.
I hypothesized that the horizontal distance of the bait from surface water or
alligator refugia would affect the likelihood that an aquatic scavenger would consume
the bait. I used shortest distance from bait to nearest alligator hole, continuous edge of
surface water, and nearest canal as measures of proximity to continuous water. If the
bait was placed in the water or in an alligator hole the distance was recorded as 0.
Continuous surface water was defined as >5cm deep, which is half of the depth that is
needed to keep an alligator from touching the bottom of a tank (Fish et al. 2007). I
defined alligator holes as an open, largely unvegetated depression in the muck or
limestone bedrock that is filled with water (Kushlan and Hunt 1979, Campbell and
Mazzotti 2004, Palmer and Mazzotti 2004). Distance to the nearest canal was
calculated using ArcGIS Spatial Analysis software (Esri 2018).
I also predicted vegetation complexity could affect access by scavengers (Smith
et al. 2017). Stem density was measured using the Point Quarter Method (Cottam and
Curtis 1956, Loya 1978) using the bait location as the starting point. Stems were
defined as any woody plant or vegetation clump >6cm in diameter. I also categorized
understory vegetation complexity as high, medium, or low subjectively as an indication
of the relative ease of a fallen nestling to reach the ground as well as an indication of
the ease of access for larger vertebrates moving through vegetation to reach individual
22
baits. Stem density and vegetation complexity thus represented different characteristics
of vegetation.
I hypothesized that numbers of nests at a site could affect available biomass of
nestlings, leading to attraction of scavengers via smell and noise cues. I predicted that
scavengers would be more common and baits more likely eaten in areas within colonies
with higher nest densities. I measured numbers of nests within 4.6m (15 feet) of each
bait site.
Feeding activity of reptiles and amphibians is strongly affected by temperature,
and I used daily average air temperature on the date of consumption collected from a
continuously recording NOAA station at Raccoon Point (Collier County, Big Cypress
National Preserve, 25.9708oN, -80.9000oW). For instances where the bait was not
consumed, I used daily average temperatures during the average latency to
consumption for baits that were consumed (two days after placement). I calculated the
time elapsed between placement and consumption based on camera time stamps.
I assessed the possibility that sound cues associated with chicks falling from the
nest into water might affect the probability of them being consumed. I suspended 10
chicken baits below active nests in paper supports, which allowed the bait to drop to the
water after the paper became soaked with moisture one to six hours after I had left the
colony. This methodology also served as a procedural control for the bait being present
in the water and available for consumption at the same time as the researcher was in
the colony.
Monitoring Fate of Baits
I used Reconyx HyperFire HC500 cameras set to record continuous still images
at a 1 min interval for one week at each nest. Cameras were mounted 45cm above the
23
ground and aimed at the carcass. During review of the imagery, I defined “consumer” as
the species that ate the majority of the biomass. If the consumer was an alligator the
total length (TL) of the animal was estimated from the images as small (<1.25m),
medium (≥1.25-<1.75m), or large (≥1.75m) (Fujisaki et al. 2012, Waddle et al. 2015).
Data Analysis
To determine the effects of covariates and main effects of colony and heron size
on consumption, I ran generalized linear mixed-effects models (GLMM) with a logit
linking function and binomial error type (Crawley 2007). Since the vast majority of
consumers were either alligators or vultures, I ran binomial GLMMs predicting
consumption probability by these two consumer species separately (eaten vs not eaten
by the target scavenger). To account for possible pseudo spatial and pseudo temporal
correlation in bait fates, both models included a site random effect (island id) nested in
week in the nesting season. I determined the best model using a manual backward
stepwise selection process, and AICc to compare resulting competitive models. All
continuous variables in the models were scaled.
I inspected correlations among predictor covariates and I removed any
continuous variables that had a Spearman’s correlation coefficient (rs) >0.5. I compared
size class of alligators accessing baits on active vs inactive islands, and on Egretta vs
Ardea heron islands using a Pearson’s two-tailed Chi-squared test of equal proportions.
I compared latency to carcass consumption at active and inactive islands using a two-
way ANOVA. I found no evidence that the sound cues of nestlings falling influenced
consumption probability (β= -0.054, ± 0.130 s.e.m., p=0.96, N=11), so I combined
responses of baits dropped with those placed on the ground for analysis. All analyses
24
were conducted in R 3.4.3 (Team 2018), and I ran GLMMs using the “lme4” package
(Bates et al. 2014). Alpha was set at 0.05 for all cases.
Energetic Calculations
I estimated the number of scavengers that could be supported by fallen nestlings
from colonies in the Everglades during a typical breeding period of 60 days. I used the
reported energetic estimates of fallen White Ibis, Great Egret, and Wood Stork (Mycteria
Americana) chicks for 2011-2014 (Nell and Frederick 2015) and calculated the
energetic estimates in 2018 for all three wading bird species by correcting the overall
average nestling energy based on observed chick mortality per nest in 2018. I used
numbers of estimated nest starts from WCA-3A, WCA-3B, WCA-2, and WCA-1 based
on aerial surveys (South Florida Water Management District, Wading Bird Reports) and
assumed equal carcass consumption rates throughout the entire area. I modified the
available nestling energy based on observed scavenger consumption rates, then
compared the estimated available nestling energy to daily energetic demands for each
scavenger species to determine the number of individuals that could be supported by
nestlings from each wading bird species each year. I also compared observed alligator
consumption to the reported energetic requirements of a mature female population of
alligators using the 756km2 portion of the Shark Slough hydrological basin (Dalrymple
2001, Nell and Frederick 2015). The Shark Slough basin is a similar, adjacent ridge and
slough system to my study area. I reported the average number of individuals that could
be supported by all three wading bird species for years when I had nest success
information for all three (2011-2014 and 2018).
25
To determine total energy intake (TEI) on large heron islands, I used the reported
nestling carcass energy per nest week (cEn, kJ nest-week-1)(Nell and Frederick 2015)
for Great Egrets, White Ibises, and Wood Storks for each year (2011-2014) as follows:
𝑇𝐸𝐼 = (𝑐𝐸𝑛)𝑊𝑛−1𝑁𝑠𝐶𝑠𝑝 (2-1)
where 𝑊𝑛−1 is the average number of weeks before nestlings become branchlings
(3 weeks; Kahl 1962, Frederick and Collopy 1989a, Nell and Frederick 2015), 𝑁𝑠 is the
total number of nests for WCA-3A, WCA-3B, WCA-2, and WCA-1, and 𝐶𝑠𝑝 is the
observed proportion of chicks consumed for that species. I then compared the total
energy consumed to either the reported individual alligator energy budget (821.4 kJ
day-1), the reported mature female alligator population of Shark Slough energy budget
(957600 kJ day-1), or a baseline energetic demand of 1652 kJ day-1 for Turkey Vultures
(Cathartes aura; based on reported energetic demand of Cape Vultures; Komen 2007).
I estimated the nestling carcass energy per nest week (cEn) in 2018 for all three wading
bird species separately by correcting the overall average cEn, (238.63 kJ nest-week-1)
based on observed average chick mortality per nest in 2018.
I calculated similarly derived values for Egretta heron chicks (Tricolored Herons,
Little Blue Herons, and Snowy Egrets) separately, using parameters appropriate for this
group of species. To determine total energy intake (TEI) on Egretta heron islands, I
used the same equation described above (Equation 2-1), but first estimated nestling
carcass energy per nest week using the following equation (Nell and Frederick 2015):
𝑐𝐸𝑛 = Wn−1𝑝ℎE(𝑐𝐸|ℎ) (2-2)
Where 𝑝ℎ is the probability of a nest hatching ≥1 nestling and E(𝑐𝐸|ℎ) is the
expected nestling-carcass energy from nests that hatched ≥1 nestling. To determine
26
E(𝑐𝐸|ℎ), I found the average number of chicks that die in Egretta heron nests per nest
(1 chick) and the average age at which chicks die (7 days). I used Erwin et al. (1996) to
determine the mass (g) of chicks at 7 days and assumed a linear increase from 2.9 kJ
g−1 wet mass at hatching to 8.4 kJ g−1 at fledging (Dunn 1975) to estimate the energy
(kJ) from each chick. For Egretta herons the average number of weeks before nestlings
become branchlings (Wn−1) was 2.5 weeks (Raye and Burger 1979). To determine total
energy intake (TEI) of scavengers feeding on Egretta heron chicks, I averaged historical
data from systematic ground surveys conducted in 2013-2017 to estimate the total
number of nests for WCA-3A only (𝑁𝑠). I used the observed consumption rates for
alligators and Turkey Vultures on Egretta heron islands for 𝐶𝑠𝑝. I then compared the
total energy consumed to the same energy budgets as described previously. I assumed
each scavenger had equal carcass consumption rates for all large and Egretta heron
chicks. For Egretta herons I only had nest start counts for WCA-3A, based on ground
surveys.
Results
I deployed a total of 202 baits from 27 February to 5 May 2018 and could
determine the fate of 160 of them from camera footage. 42 (20%) baits did not have an
identifiable outcome (bait shifted out of camera, bait was consumed between images,
etc.), and I did not include those cases in analyses. Of the 160 with known fates 137
were on active colony islands, 116 on islands with Ardea heron nests, 21 on islands
with Egretta heron nests, and 23 on inactive islands. Hereafter I refer to the remaining
160 baits with known fates as the effective sample size (N=160).
27
Description of Consumers
Overall, there was a relatively high rate of scavenging, with 85% of baits
consumed (N=136) and only 15% (N=24) of baits left unconsumed. Most baits were
eaten by Turkey Vultures (N=75, 47%) followed by alligators (N=46, 29%, Table 2-2).
Two-toed Amphiumas (Amphiuma means) and Black Vultures (Coragyps atratus) were
each primary consumers for 3% (N=5) of the baits, and the remaining 15% (N=24) of
the baits were not eaten (Table 2-2).
Although alligators took proportionally fewer baits on inactive than active islands
(13% N=3 compared to 31% N=43 at active islands), the best model did not retain this
covariate (ΔAICc=2.30, β=0.35, ±0.89 s.e.m., p=0.69). There was no significant
difference in latency to carcass consumption between active and inactive islands
(F(1,158)=0.119, p=0.731). I found a lower diversity of consumers on inactive islands (4
species) compared to colony islands (8 species), though this could be related to the
smaller sample size. On Egretta heron islands, most baits with known fates were eaten
by alligators (N=17, 81%) compared to only 10% (N=2) eaten by Turkey Vultures. On
Ardea heron islands 22% (N=26) of baits with known fates were consumed by alligators
and 51% (N=59) were consumed by Turkey Vultures (Table 2-2). For all islands, the
average time elapsed between consumption of different baits deployed on the same
island on the same day was 25 hours, suggesting consumption events were
independent.
Of baits that were scavenged by alligators, 20% (N=28) were consumed by
individuals in the large size class on active islands, while only 9% (N=2) of baits were
consumed by large alligators on inactive islands. Baits on Egretta heron islands were
taken by large (N=13, 62%) and medium (N=3, 14%) alligators, and 14% (N=48) of all
28
baits were not consumed (Table 2-3). I found no significant difference in the proportion
of baits consumed by large alligators either among Egretta or Ardea heron colony types
(Pearson’s X2 =3.6514, N=43, p=0.3017) or between colony and inactive islands
(Pearson’s X2 =2.2584, N=46 , p=0.5205).
Correlates of Alligator Consumption
Baits were more likely to be consumed by alligators when located close to water,
in areas with higher nest density, on Egretta heron islands, and when temperatures
were higher (Table 2-4, Figure 2-2). The best model retained average temperature and
colony type because these variables improved the model in terms of AICc despite the
variables being only marginally insignificant (Table 2-4). On either colony type, baits that
were farther from water were less likely to be eaten by an alligator, and the fitted model
results suggested that there was a threshold distance to continuous water, beyond
which fallen nestlings are unlikely to be eaten by alligators (10-25 m, Figure 2-2a).
Probability of alligator consumption also increased with density of nests (Figure 2-2b),
suggesting alligators are attracted to higher density nesting areas or that nestling
availability could be higher or more predictable in these areas. Baits on Egretta heron
islands were more likely to be consumed by alligators than on Ardea heron islands
(Figure 2-2c).
Correlates of Vulture Consumption
Distance to water, colony type, local nest density, and elapsed exposure time
were all significant predictors of vulture consumption (Table 2-5). While most of the
same covariates were important in both alligator and vulture models, the directions of
the relationships were different. Nestlings that were farther from water, in areas of lower
nest density and on Ardea islands were more likely to be consumed by vultures (Table
29
2-5, Figure 2-2). Consumption by vultures decreased with bait exposure time (Table 2-
5), while probability of alligator consumption did not show any temporal trend.
Significance of Nestling Carcasses to Scavengers
Based on observed rates of consumption I estimated that on average fallen
nestlings from all Egretta heron nests in our study area (WCA-3A) could support 2.8
adult female alligators and less than 1 Turkey Vulture for a period of 60 days annually. I
estimated that on average fallen nestlings from nests of Great Egrets, White Ibises, and
Wood Storks throughout all WCAs could support an average of 181 alligators, or 16% of
the females in the Shark Slough population, and 147 Turkey Vultures for 60 days
annually. This estimation varied depending on the annual avian reproductive success
and the total number of nest initiations (Figure 2-3).
Discussion
Turkey Vultures (N=75, 47% of baits) and alligators (N=46, 29% of baits) were
the primary consumers of fallen nestlings in our study. Access to nestlings by different
scavengers was explained by local environmental covariates. This quantitative
information on scavenger identity and opportunities for scavenging greatly informs our
understanding of the transfer of some 17.40 GJ/season (Nell and Frederick 2015) of
nestling carcass energy from nesting wading birds, most of which (85%) appears to
become an important source of energy for large-bodied vertebrate scavengers.
Carcasses closer to water, in higher nesting densities, and on Egretta heron islands
were more likely to be consumed by alligators, whereas carcasses farther from water, in
lower nesting densities, and on Ardea heron islands were more likely to be consumed
by Turkey Vultures. It’s unclear to what degree these results are due to differences in
accessibility or direct competition between the scavengers. While Turkey Vultures prefer
30
to feed on the ground (Owre and Northington 1961), they will readily wade into shallow
water to fish and feed on carcasses (Jackson et al. 1978), and we observed several
(N=9) Turkey Vultures doing this. It is likely that this preference for land-based
carcasses was a factor affecting Turkey Vulture consumption, but vultures may also be
avoiding areas that are likely to be inhabited by alligators due to fear of predation.
These two dominant scavenger species seem to be utilizing this food source differently
based on key environmental variables. Differences in accessibility to carcasses among
scavengers appears to arbitrate scavenger coexistence in this ecosystem, and mobility
is a key feature in scavenger usage of resource subsidies (Subalusky and Post 2019).
Few studies have analyzed scavenging communities in this ecosystem, and the
spatial partitioning between carcasses described here appears to arbitrate scavenger
coexistence. Scavengers experience high amounts of competition for carcasses due to
limited availability and the ephemeral nature of carrion (Byrne et al. 2019), and thus,
must partition the resource to coexist. Partitioning can occur based on carcass size
(Byrne et al. 2019), scavenger body size (Travaini et al. 1998), scavenger morphology
(Hertel 1994), or temporally (Kendall 2014). Our findings that scavenger identity is
based on local environmental features (proximity to water, nesting density, and colony
type) add to the knowledge of how carcasses are partitioned, and how coexistence of
multiple scavenger species may be maintained.
Black Vultures (Coragyps atratus) and Turkey Vultures engage in a well-
documented partitioning of carrion (Wallace and Temple 1987, Lemon 1991, Byrne et
al. 2019). Black Vultures prefer food sources that are larger (>20kg), more reliable
(Coleman and Fraser 1987), and in more open areas (Byrne et al. 2019) compared to
31
Turkey Vultures. They are also more aggressive and often displace Turkey Vultures
from carcasses (Haskins 1972, Carrete et al. 2010). Given that wading bird colonies
represent large areas of reliable, predictable, and easily detectable carrion I would
expect that Black Vultures would be the dominant vulture scavenger in this system.
However, Black Vultures were the primary consumers of less than 5% of carcasses
compared to Turkey Vultures (47%). This could be because wading bird carcasses are
much smaller than the preferred carcass size for Black Vultures (Coleman and Fraser
1987, Byrne et al. 2019) or because wading bird colonies tend to have dense vegetation
and packed wading bird nests. On inactive islands, which are generally more open and
accessible than active islands, Black Vulture consumption of carcasses increased
drastically (from <1% to 17%, Table 2-2). I suggest that carcass size and vegetation
density give Turkey Vultures a competitive advantage over Black Vultures for nestling
carcasses in this ecosystem.
Carcasses on Egretta heron islands were 3.6 times more likely to be consumed
by an alligator than on Ardea heron islands. While Egretta heron islands may contain
fewer total nests and produce smaller sized nestlings, the tradeoff may be that alligators
expend less energy to access these nestlings than on Ardea heron islands. This result
agrees with our initial prediction that carcass consumption by alligators would be higher
on islands where the energy expenditure required to find nestlings is less. Energy
expenditure during scavenging is an important consideration because the encounter
rate of scavenger to carrion is one of the principal parameters defining optimal foraging
(Kane et al. 2016).
32
While I did find a trend towards lower nestling consumption probability by any
scavenger on inactive than active islands, these differences were not significant. There
was also no difference in latency to carcass consumption between these island types.
We originally predicted that nestling carcasses on islands with active wading bird
colonies would be consumed more readily by scavengers due to the predictability of
carcasses and general attractants of the wading bird colony. Our results could be
influenced by smaller sample sizes on inactive islands; however, it seems that
predictability does not always lead to increased consumption by scavengers. Hill et al.
(2018) found that roads, which provide reliable foraging opportunities, do not increase
carrion use by vertebrate scavengers compared to areas with a less predictable carrion
supply. The concentration of carcasses from active wading bird colonies inevitably
results in an increase in the spatial and temporal predictability of carrion, but our results
do not suggest that this leads to higher scavenging probabilities. The importance of
predictability of carrion on scavenger foraging behavior remains an important question
(Boutin 1990, Monsarrat et al. 2013, Hill et al. 2018).
I also hypothesized that competition for carcasses would be higher in areas of
high carcass density and predicted that larger alligators would be more prevalent
scavengers on active than inactive islands. Yet, I found a nonsignificant trend in size
distribution (Table 2-3). This could be because large alligators have more difficulty than
smaller ones moving among the more densely packed tree stems characteristic of
vegetation in active islands (Table 2-1). Consideration of spatial complexity in carcass
distribution is an important factor when determining access by scavengers (Subalusky
and Post 2019).
33
My estimate that 85% of carcasses are consumed, and that nestling carcasses
alone can annually support, on average, 181 alligators (16% of the local alligator
population) and 147 Turkey Vultures for 60 days suggests that fallen nestlings are an
important energy subsidy for large-bodied vertebrate scavengers during the wading bird
nesting season. The magnitude of the trophic transfer I describe between breeding
wading birds and two major scavengers is fundamentally dependent on several
characteristics of the system. First, the birds are densely packed in colonies and
regularly practice brood reduction, resulting in most nests producing one or more
nestlings that fall to the ground, a condition that may not be met by many colonially
nesting species. Secondly, the islands I studied were isolated by shallow water (0.5 –
1.5m), resulting in access mostly by flying or swimming scavengers, hence greatly
reducing the number of species capable of consuming carcasses. Isolation is typical for
many colonial nesting situations, so this characteristic may be broadly applicable. Third,
the colonies are often partially or wholly inundated by water, often allowing access to
the area directly underneath nests by swimming or wading scavengers. It is also worth
mentioning that we collected information on scavenging during a year of abnormally
large numbers of wading bird nesting starts (4.7 times average of the last 20 years), and
it is possible that these conditions may have affected our results of scavenger
consumption (Figure 2-3).
The degree of benefit of carcasses to individual scavengers that I have
measured appears to be large enough to help drive the evolution of a facultative
mutualism by which alligators and other scavengers benefit by associating with nesting
birds (Nell and Frederick 2015, Nell et al. 2016). While the number of wading bird nests
34
varies depending on the year (Figure 2-3), fallen nestlings stand to serve as a reliable
food source for scavenegers, with 13,182 wading bird nests even in the season with the
lowest turnout. As discussed previously, nesting wading birds also may benefit from
predator protection provided by alligators, and wading birds actively choose predator-
protected nesting locations with alligators present (Burtner and Frederick 2017).
Alligators that reside around wading bird colonies are in better body condition than
those not in colonies, and this nutritional subsidy corresponds with an energetically
demanding time for reproductively active female alligators who are mobilizing body
resources for egg-laying (Mazzotti and Brandt 1994). It has previously been
hypothesized that fallen nestlings by brood reduction is a vital component of this
relationship (Nell et al. 2016). Our results support this hypothesis and show that fallen
nestlings are a significant source of food for other scavengers in addition to alligators.
Nestling carcasses from aggregations of breeding birds probably have a
pronounced effect on the scavenger community in the Everglades. The Everglades
wetland is considered highly oligotrophic (Davis 1994), and alligators that reside there
tend to grow slowly and be in poor body condition because of food limitation (Jacobsen
and Kushlan 1989, Mazzotti and Brandt 1994, Dalrymple 1996). In general, carcass
availability has a special significance to consumers in nutrient-poor ecosystems, where
nutrient limitation promotes the importance of any nutrient inputs (Subalusky and Post
2019). For instance, mammalian and avian scavengers alike depend on kangaroo
carcasses as a major food source in the arid regions of South Australia (Read and
Wilson 2004) and various species in the abyssal sea floor ecosystem rely on detritus
deposition because primary productivity is absent (Smith et al. 2008). While carrion may
35
generally be unpredictable and ephemeral as a food source (DeVault et al. 2003,
Ruxton and Houston 2004, Kane et al. 2016), persistent breeding colonies of birds and
other animals may provide a seasonally predictable source of carrion. While the effect
of seasonally predictable carrion may be comparatively less in mesotrophic or
eutrophic systems, this energy source is still likely to be nontrivial in these areas simply
because of its magnitude.
Breeding bird colonies that undergo brood reduction can be found globally, and
there are probably many undescribed scavenger communities that benefit from
concentrated carcass deposition (Frederick and Collopy 1989b, Hunter 1991, Emslie et
al. 1995, Howald et al. 1999), in areas such as the Brazilian Pantanal, Numidia in
Algeria, central Llanos of Venezuela, Kakadu National Park in Australia, and Uttar
Pradesh India. Nutrient redistribution between aquatic environments, where wading
birds forage, and island ecosystems, where wading birds nest, is a key process driving
the dynamics of this nutrient deprived ecosystem. Our results suggest that fallen
nestling carcasses in colonially breeding bird colonies may generally constitute an
important source of energy for obligate and facultative scavengers that can shape
community structure, population dynamics of scavenger species, and ecosystem
dynamics, especially in oligotrophic ecosystems.
36
Figure 2-1. Map of the study area with locations for all wading bird nesting colonies
sampled. Solid white circles represent Ardea heron islands, solid white triangles represent Egretta heron islands, and empty white circles represent inactive islands. Inset maps show the difference in size (note scale) and shape typical of a) Egretta and b) Ardea heron islands. Map generated in ESRI ArcMap 10.6.1 (Esri 2018; http://www.esri.com/). Main map satellite imagery is the World Imagery basemap within ArcGIS 10.6 software (http://www.esri.com/data/basemaps), credited to Esri, DigitalGlobe, Earthstar Geographics, CNES/Airbus DS, GeoEye, USDA FSA, USGS, Aerogrid, IGN, IGP, and the GIS User Community. Gray inset extent map imagery is the Light Gray Canvas basemap within ArcGIS 10.6 software (http://www.esri.com/data/basemaps), credited to Esri, HERE, Garmin, FAO, NOAA, USGS, © OpenStreetMap contributors, and the GIS User Community. Inset satellite imagery (a, b) image data © Google 2019: Google Earth (Map data: Google; https://www.google.com/earth/).
37
Table 2-1. Comparison of biotic and abiotic qualities of bait deployment sites on defined island and colony types used in this study. Values are expressed as average ± standard deviation. Active islands include Ardea and Egretta heron colony types. Inactive islands are islands with no nesting birds.
Ardea heron islands Egretta heron islands Inactive islands Active islands
Feature Mean Range Mean Range Mean Range Mean Range
Distance to water (meters)
6.60±9.81 0.1375–26.74
3.12±4.58 0.61–5.91 18.02± 20.88
0.54–30.07
6.09±9.31 0.14–26.74
Local density (nests/100m2)
2.73±2.61 0.5–6.4 5.58±3.05 0.75–4.67 0±0 0–0 3.15±2.86 0.5–6.4
Area (square meters)
11,816.86±16,092.32
2,428.6–36,210.77
1,554.79± 2,697.77
982.11–5,903.98
16,255.28± 21,387.69
6,387.52–52,410.98
11,915.52± 14,144.02
982.11–36,210.77
Colony size (number of nests)
144.91± 76.92
16–254 56.83± 19.03
30–88 0±0 0–0 132.10±77.93 16–254
Vegetation density (stems/area)
1.76±0.95 0.45–3.50 5.84±2.66 2.23–10.03 1.17±0.63 0.76–2.26 2.71±2.28 0.45–10.03
38
Table 2-2. Raw counts and relative percent consumption of 160 baits with known fates by consumers on different island types and colony types in the Everglades. The “Other” category includes five single-instance consumers: Black Crowned Night Heron (Nycticorax nycticorax), Common Snapping Turtle (Chelydra serpentina), Purple Gallinule (Porphyrio martinicus), Red Shouldered Hawk (Buteo lineatus), and Florida Softshell Turtle (Apalone ferox), which together make up less than 5% of baits consumed.
Active islands Inactive islands Ardea heron islands Egretta heron islands
Consumer % Count % Count % Count % Count
Turkey Vulture 44.53 61 60.87 14 50.86 59 9.52 2
Alligator 31.39 43 13.04 3 22.41 26 80.95 17
Amphiuma 3.65 5 0.00 0 4.31 5 0.00 0
Black Vulture 0.73 1 17.39 4 0.86 1 0.00 0
Not eaten 16.79 23 4.35 1 18.10 21 9.52 2
Other 2.91 4 4.35 1 3.46 4 0.00 0
39
Table 2-3. Consumption of baits by alligator size class on islands or colonies of different types in the Everglades. Alligator size classes were defined as small (<1.25m), medium (≥1.25-<1.75m), or large (≥1.75m).
Active islands Inactive islands Ardea heron islands Egretta heron islands
Size Class % Count % Count % Count % Count
Large 20.44 28 8.70 2 12.23 17 61.90 13
Medium 6.57 9 0.00 0 4.32 6 14.29 3
Small 2.92 4 4.35 1 3.60 5 0.00 0
Not alligator 53.28 73 82.61 19 64.03 89 14.29 3
Not eaten 16.79 23 4.35 1 15.83 22 9.52 2
40
Table 2-4. Results of the best generalized linear mixed-effects model assessing effect of covariates on probability of carcass consumption by alligators. Model includes site nested in week as random factor. All continuous variables were scaled.
Estimate Standard Error z value Pr(>|z|)
(Intercept) -1.72 0.42 -4.06 <0.001
Distance to Water (m) -1.43 0.55 -2.59 <0.001
Colony Type (Egretta) 1.61 0.90 1.79 0.074
Local Nesting Density 0.56 0.26 2.20 0.028
Average Temperature (°F) 0.52 0.29 1.76 0.078
41
Figure 2-2. Modeled probabilities of bait consumption by alligators and vultures in relation to main covariates: a) distance to
water (meters), b) nesting density (number of nests/30ft), and c) colony type (Ardea or Egretta ) for alligators and Turkey Vultures. Blue lines represent the trends for alligators and red lines represent the trends for Turkey Vultures. Lines show a smoother fitted to predicted individual values (indicated by points) from best generalized linear mixed effects model output for alligator and vulture models. Shaded areas indicate standard error of the smoother. In boxplots, central line shows the median, boxes include all values within the 0.25 and 0.75 quantiles and whiskers indicate range excluding outliers.
A B C
42
Table 2-5. Results of the best generalized linear mixed-effects model assessing effect of covariates on probability of carcass consumption by Turkey Vultures. Model includes site nested in week as random factor. All continuous variables were scaled.
Estimate Standard Error Z value Pr(>|z|)
(Intercept) 1.01 0.46 2.19 0.029
Distance to Water (m) 1.20 0.46 2.63 0.009
Colony Type (Egretta) -3.36 1.36 -2.48 0.013
Local Nesting Density -0.39 0.20 -1.99 0.047
Bait Exposure Time (min) -1.88 0.47 -3.98 <0.001
43
Figure 2-3. Estimated number of scavengers supported annually during a wading bird nesting period of 60 days for a)
alligators and b) Turkey Vultures. The dotted line is the estimated average number of alligators sustained and the solid line is the estimated average number of Turkey Vultures sustained. Open circles represent the total number of nest starts for each year. Stacked bars show the relative contribution of each wading bird species to the total energy available and the number of individual scavengers that can be supported from it. Bars marked with an asterisk have nest success data from all three wading bird species. Note that there are no estimates for number of nests for Wood Storks or White Ibis before 2010 and that there were zero nesting Wood Storks in 2012.
a b
44
CHAPTER 3 EFFECTS OF ALLIGATOR PRESENCE ON BREEDING COLONY SITE
SELECTION BY LONG-LEGGED WADING BIRDS
Introduction
In addition to competition and predation, positive ecological interactions
are increasingly seen as an important force in community organization (Bronstein
2001, 2009, Bruno et al. 2003). Facilitation is one such positive ecological
interaction that occurs when the presence of one species alters the environment
in a way that increases the survival or reproduction of another species (Boucher
et al. 1982, Stachowicz 2001, Bronstein 2009, Bulleri et al. 2016). As defined by
Bronstein (2009), facilitation can be mutualistic or commensal. The effects of
facilitative relationships can be strong enough to cause changes in the
distributions of species (Boucher et al. 1982, Bruno et al. 2003, Tirado and
Pugnaire 2005). While facilitation is best described among plant species (Brooker
et al. 2008), there are fewer examples within the animal kingdom (Kotler et al.
1992, Nummi and Hahtola 2008, Odadi et al. 2011, Harvey et al. 2016).
Protection from predation is a common facilitative effect, which is predicted to be
most common in communities where predation pressure has a high effect on
survival and reproduction, and thus, a stronger selective force (Bronstein 2009).
Nest predation is one of the biggest threats to the reproductive success in
birds (Oliveras de Ita and Rojas-Soto 2006), and protective nesting associations
are a geographically widespread type of predation refuge often sought through
facilitation by nesting birds (Quinn and Ueta 2008). These protective nesting
associations occur when one species places its nest near a more formidable
species that drives away predators of the first species simply by defending its
45
own territory (Haemig 2001, Quinn and Ueta 2008, Burtner and Frederick 2017).
Descriptive studies of protective nesting associations can be found amongst
birds in a variety of taxa (Myers 1929, Moreau 1936, Durango 1949, Grimes
1973, Uchida 1986, Pius and Leberg 1998, Richardson and Bolen 1999, Quinn
and Ueta 2008, Burtner and Frederick 2017) and are generally assumed to be
commensal, although few researchers have investigated benefits to the
protective associates (Quinn and Ueta 2008). While it is established that these
nest protector relationships often affect the reproductive success of the protected
species locally (reviewed in Haemig 2001, Freestone 2006), it is unclear whether
these associations are widespread and have strong enough effects to change the
habitat use or even distribution of the protected species (Freestone 2006).
Nest predation by mammalian mesopredators such as raccoons (Procyon
lotor) and Virginia opossums (Didelphis virginiana) is a major factor in
determining reproductive success of nesting long-legged wading birds (Frederick
and Collopy 1989b). Access to breeding sites by only a few individuals can result
in destruction of nest contents and colony-wide nest abandonment (Rodgers
1987a, Frederick and Collopy 1989b, Burtner and Frederick 2017). Although
wading birds are generally colonial nesters, there is almost no group or individual
nest protection behavior, and there is no effective behavioral defense against
mammalian predation (Hoogland and Sherman 1976, Møller 1987, Rodgers
1987a, White et al. 2005, Jungwirth et al. 2015, Burtner and Frederick 2017).
Selecting inaccessible breeding sites that reduce the harmful effects of predation
by these key predators appears to the main form of nest defense.
46
A facultative mutualistic nest protector relationship is known to exist
between long-legged wading birds (Ciconiiformes and Pelecaniformes, e.g.
herons, egrets, ibises, storks and spoonbills) and the American Alligator (Alligator
mississippiensis). In this positive ecological association, alligators facilitate a
safer nesting location for wading birds by deterring mammalian nest predators
from wading bird colonies, and alligators receive food in the form of fallen
nestlings (Nell and Frederick 2015, Chapter 2). Wading birds are also attracted to
nesting sites with alligators present (Burtner and Frederick 2017). This
apparently mutualistic interaction between alligators and wading birds appears to
offer significant benefits for protector and protectee, despite being non-obligate,
and illustrates how selective pressures of predation may have acted to form and
reinforce a strongly positive ecological association. However, alligators do not
occur throughout the entire breeding range of all species of wading birds in the
United States, but mammalian predators do. It is unclear how the absence of
alligators may alter the costs of reproduction for wading birds. Since colony site
selection is the only known form of defense against mammalian predators, we
predicted that colony site selection would be altered in the absence of alligators.
Wading birds nest in large colonies and employ collective decision-making
when establishing new colony locations and returning to previously used colonies
(Deneubourg and Goss 1989, Couzin 2009). Colony site selection is based on a
careful evaluation of the prevailing safety of the site (Burger 1981, Fasola and
Alieri 1992, Van Eerden et al. 1995, Hafner 2000). Wading birds prefer colony
site characteristics that reduce nest predation such as islands (Rodgers 1987a,
Ogden 1991), which create a buffer against land predators (White et al. 2005).
47
Wading birds have been noted to nest exclusively on islands in the middle of
large bays (Parsons et al. 2001, Parsons 2003a, Paton et al. 2005) rather than in
shallower wetlands, and islands isolated from the mainland may have decreased
predation risks (Robinson 1985a, Post 1990, Strong et al. 1991, Kelly et al. 1993,
Erwin et al. 1995, Tsai et al. 2016), and may be occupied more consistently (Tsai
et al. 2016). Raccoon predation in colonies increases significantly as water depth
decreases to the point that raccoons can walk rather than wade (Rodgers 1987b,
Frederick and Collopy 1989a, Post and Seals 1991, Kelly et al. 1993, Coulter and
Bryan 1995, Hoover 2006, Burtner and Frederick 2017). Nesting directly over
water or on islands with a protective moat of water probably encourages the
protective effect of crocodilians by forcing nest predators to swim to access the
colony, which makes them highly vulnerable to alligator predation (Dusi and Dusi
1968, Jenni 1969, Robinson 1985b, Post and Seals 1991, Coulter and Bryan
1995). However, most of these apparent habitat preferences have been
measured in the presence of alligators or other crocodilians, and it is unclear how
they may be altered in the absence of alligators.
Here, I compare habitat selection preferences of nesting wading birds
relative to characteristics of available colony sites and describe how those
preferences change based on the likelihood of alligator presence at the northern
edge of the alligator’s present range. I predicted that in the absence of alligators
wading birds would make increased use of islands, and that islands preferred by
wading birds would be farther from features that attract or host land predators.
Both predictions are based on the idea that islands and distance from shore may
reduce accessibility by mammalian nest predators. We also predicted that
48
wading birds would prefer colonies with environmental features that made access
by raccoons harder or less enticing when alligator presence is unlikely, such as
greater colony isolation from other colonies and from human development, lower
percent composition of surrounding land with human development, taller
vegetation, and smaller sized islands.
Methods
Study Site
We studied wading bird colony locations in 28 counties in eastern North
Carolina, predominantly in the Coastal Plain (57,565.8 km2): Wayne, Currituck,
Gates, Nothampton, Perquimans, Dare, Franklin, Bertie, Nash, Martin,
Washington, Davidson, Wilson, Pitt, Hyde, Lenoir, Sampson, Cumberland,
Jones, Carteret, Duplin, Onslow, Robeson, Bladen, Pender, Columbus, New
Hanover, and Brunswick. The Coastal Plain is a geologically unified region that is
flat, low lying, and includes rivers, marshes, and swamplands (Tiner 1984). This
area encompasses the northern extent of the alligator’s range (Elsey and
Woodward 2010, Parlin et al. 2015, Gardner et al. 2016), and densities of
alligators here are relatively low compared to more Southern parts of their range
(Dunham et al. 2014, Parlin et al. 2015, Gardner et al. 2016). This makes it ideal
for an equal spatial distribution of colonies with varying alligator occupancy
probabilities while also reducing the amount of variation introduced from different
geographic regions and inconsistent survey efforts and methods between
multiple state organizations. There is also extensive previous research describing
current and historical alligator occupancy probabilities throughout this area
(O’Brien and Doerr 1986, Parlin et al. 2015, Gardner et al. 2016). Wading birds
49
nest throughout the coastal plain in mixed species colonies (Bent 1963, Custer
and Osborn 1977, Beaver et al. 1980). Colonies were located on barrier islands,
estuarine non-barrier islands, forested freshwater wetlands, impoundments,
swamps/ponds, manmade/diked ponds, freshwater islands, and the shorelines of
river streams. Colony sizes ranged from 3 to 2,750 birds and colony substrates
included dredged and diked materials, dredged and undiked materials,
impoundments, and natural substrates.
Colonially nesting wading birds were surveyed periodically by the North
Carolina Wildlife Resources Commission in coast-wide surveys (Schweitzer et al.
2017) and complete inland surveys (Annual Performance Report 1996). Colony
species composition and numbers of nesting pairs of each species are recorded
as well as various colony site characteristics including percent cover of
vegetation, vegetation height, and colony substrate. Coastal surveys were
conducted on foot following methods described by Soots Jr. and Parnell (1979)
and Parnell and McCrimmon (1984). Inland surveys were conducted via fixed-
wing aircraft at an altitude of 800’ and counts are confirmed with a ground
survey. See Appendix A for a full description of all survey methods.
We used colony locations from 2000 to 2019, only considering colonies
containing Great Egrets (Ardea alba), Little Blue Herons (Egretta caerulea),
Green Herons (Butorides virescens), Snowy Egrets (Egretta thula), and/or
Tricolored Herons (Egretta tricolor). In addition to the above constraints, only
colonies with ≥3 birds were considered, totaling 90 unique colonies (N=90; Figure
3-1). Of those 90 colonies, 44 were located on islands and 46 were located on
50
non-islands (Figure 3-1). Wading bird colony locations were provided by the
North Carolina Wildlife Resources Commission.
Colony Data and Main Methods of Defense
For each colony, we determined the probability that an alligator would be
present at that site (classified as either likely or unlikely). Alligator presence
probability was determined using several sources of information about alligator
population density and occurrence throughout North Carolina, mainly studies
done by Gardner et al. (2016), Parlin et al. (2015), and O’Brien and Doerr (1986)
and research grade iNaturalist observations (iNaturalist.org 2019), but was also
based on general information about alligator physiological tolerances and
limitations (Birkhead and Bennett 1981, Brisbin Jr. et al. 1982, Lauren 1982,
Dunson and Mazzotti 1989, Seebacher 2005, Gardner et al. 2016).
Alligator probability was judged to be likely (N=40) if the colony was located
upstream or downstream ≤5 km of an area with a predicted occupancy
probability >40% or it had ≥2 sensical iNaturalist sightings within 5 km from the
same year that the colony was observed. Colonies that did not meet those
criteria had an alligator probability classified as unlikely (N=50). Previous
research for North Carolina has shown that alligator occupancy and abundance
decreases in more northern sites, in sites with higher salinity, and in sites that
were generally more westward. Alligators in general are more likely to occur in
coastal areas (Gardner et al. 2016) and typically don’t occupy barrier-islands
(Parlin et al. 2015). Although alligators do not prefer to continually reside in saline
environments (McIlhenny 1935, Joanen and Mcnease 1989), they will temporarily
frequent marine influenced areas where salinities exceed those typically tolerated
51
by alligators to forage (Rosenblatt and Heithaus 2011). Our alligator probability
classifications match these observations and understandings of alligator
environmental tolerances and behaviors (Figure 3-1).
Islands isolated from the mainland have decreased predation risks from
terrestrial predators (Robinson 1985a, Strong et al. 1991, Kelly et al. 1993, Tsai
et al. 2016), and wading birds seem to prefer nesting on islands because of this
safety buffer they provide (Parsons 2003b, Paton et al. 2005, White et al. 2005,
Tsai et al. 2016). We predicted that wading birds would prefer to nest on islands
and that those islands would be farther from the mainland when alligator
presence is unlikely. We defined islands using the North Carolina Center for
Geographic Information and Analysis (CGIA) 1996 landcover vector digital data
layer, which was produced through contract with Earth Satellite Corporation
(EarthSat) in ESRI’s ArcGIS ArcMap software (Esri 2018). This layer had a 28.5
meter resolution and 23 different land class classifications. Any land mass that
was completely surrounded by open water (endpoint class 19) was defined as an
island and this classification was confirmed using historically appropriate satellite
imagery from the year the colony was surveyed (Figure 3-2). Any other landforms
that were not islands were classified as mainland (Figure 3-2). We calculated the
distance of each island colony to the nearest mainland.
We also considered the possibility that larger islands could sustain resident
terrestrial mammals. We predicted that wading birds would prefer to nest on
islands that were farther from any landmass that could potentially host a raccoon
when alligator presence is unlikely. Reported population densities of raccoons
range from 1 raccoon every 5 ha to 1 raccoon every 43 ha (Schneider et al.
52
1971, Lotze and Anderson 1979, Pedlar et al. 1997). According to this literature,
islands with an area of less than 5 ha could not sustain a resident raccoon, so we
also identified landmasses that were >5 ha (Figure 3-2) and calculated the
distance of each island colony to the nearest landmass that was >5 ha.
Alternative Methods of Defense
At each colony site we also collected data on various alternative
mechanisms of protection that we hypothesized could be used by nesting wading
birds as an alternative defense against predators when alligator presence is
unlikely. This included five other characteristics: colony distance from other
colonies, colony distance to human development, percent composition of
surrounding land with human development, vegetation height, and island size.
In addition to wading birds potentially isolating themselves from the
mainland and from landmasses that could host raccoons, we thought wading
birds might also seek out islands that are more isolated from other colonies when
alligator presence is unlikely. We predicted that islands farther from other wading
bird colonies would be less enticing to raccoons, who will readily travel between
close colony islands (Porter et al. 2015). We measured the shortest distance
from the focal colony to the next nearest wading bird colony.
Raccoons are abundant in human environments (Prange et al. 2003, Page
et al. 2009), so we suspected that wading birds would avoid areas with human
development when alligator presence is unlikely. We calculated the percent
composition of the land use type associated with human infrastructure within an
8.95km buffer of the colony, as well as the nearest distance from each colony to
human development. To determine the percent composition of human
53
development for each colony we combined the low intensity development land
class (endpoint class 2) and high intensity development land class (endpoint
class 3) and calculated the total percent cover of the combined layer within the
buffer. These categories included all areas where the land is covered
predominantly by human structures, including densely populated urban and
suburban areas (Siderelis 1994).
Within a colony, there are considerable differences in nesting site
preference among species (Burger 1978, White et al. 2009), but generally, the
height of the nest can be an effective method for deterring predators (Best and
Stauffer 1980, Nilsson 1984, Post 1990). We thought wading birds might be
utilizing vegetation height as a means of deterring predators and predicted that
the height of the nesting vegetation would be higher when alligator presence is
unlikely. Vegetation height was a site-specific colony attribute that was
categorized as bare, 25cm-1m, 1-3m, 3-7m or 7+m at the time of the survey.
Previous research has shown that island size is an important predictor of
wading bird colony site selection (Greer et al. 1985). Intermediate and small
sized islands may be a better defense against mammalian predators than larger
islands, which can potentially sustain a resident raccoon population or are
otherwise more attractive to them (Eason et al. 2012, Tsai et al. 2016). For this
reason, we hypothesized that wading birds would utilize smaller islands more
often when alligator presence is unlikely. We measured the total area of each
colony island.
54
Colony Control Points
To better understand colony site preference relative to the availability of
each resource we used a buffer with an 8.95km radius surrounding each colony.
Resources within this buffer were deemed “available” while resources in the
colony itself were deemed “used”. Colonial nesting birds establish spatially
packed centralized colonies from which they recurrently depart to forage in the
surrounding landscape (Wittenberger and Hunt, G. L 1985, Kelly et al. 2008).
Recognizing this behavior, we based the buffer distance on the average foraging
distance reported for herons in eastern North America (Custer and Osborn 1978,
Thompson 1979, Bancroft et al. 1994, Gibbs and Kinkel 1997, Custer and Galli
2006, Stolen et al. 2007).
We generated between 1-3 random points per island colony (depending on
availability) on suitable islands that 1) were within the 8.95km buffer of the
colony, 2) had a land class that was used by nesting wading birds based on
existing colony location data, 3) had an island size ≥ the minimum observed
colony island size (482 m2), and 4) did not already host an active colony. Each
control point had the same alligator probability classification as the associated
colony island. These points represented potential colony locations that were
available, yet unused, and they functioned as controls for the island colonies
(N=102). Control points allowed me to assess wading bird colony site selection
preferences and ensured that observed trends were not due to changes in
availability throughout the study system. If there were more than three suitable
control islands available for a given colony island then we selected three at
random using ArcGIS Sampling Software (Esri 2018). For each control island we
55
generated the same data as the colony islands using the same methodologies
(see above). We measured the control point’s distance to the nearest colony that
was not the associated colony. We estimated vegetation height classifications at
control points based on satellite imagery. We calculated the relative colony
distance to the mainland and to landmasses >5ha by subtracting the control
island distance from the associated colony island distance. For example, a
positive value indicated that the associated colony island was farther from the
mainland than the control island. In addition to relative island distance, we also
calculated the relative value of each continuous variable (relative island size,
relative percent composition of human development, relative colony distance to
other colonies) following the same procedure. To get an idea of the availability of
suitable islands throughout the entire study area we recorded the total number of
islands within each colony buffer that matched the above criteria that were
unused by wading birds.
Data Analysis
To determine the effects of alligator occurence on relative island distance
from the mainland and relative island distance from areas >5ha we ran a linear
mixed-effects model (LMER) using the “lmerTest” package (Kuznetsova et al.
2017). We included each control island’s associated colony as a random effect
and included alternative methods of protection as covariates. In each case, we
determined the best model using a manual backward stepwise selection process
and used AICc to compare resulting competitive models without the restricted
maximum likelihood estimator (REML). All continuous variables in the models
were scaled.
56
We inspected correlations among continuous variables, but none had a
Spearman’s correlation coefficient (rs) >0.5. We used a Tukey’s method to
identify and remove 5 outliers ranged above or below the 1.5 Inter Quartile
Range based on relative distance to the mainland (N=97). We included latitude
and longitude as scaled continuous fixed effects in the model to reduce the
probability that observed changes in colony site preference was due to a
geographical cline. We compared the proportion of island colonies and mainland
colonies, and the proportion of islands used and islands available, with alligator
probability using a Pearson’s two-tailed Chi-squared test of equal proportions.
We compared the longevity, defined as the number of successive years the
colony was active, and the colony size, defined as the total number of nesting
birds, between island and mainland colonies using a two-way ANOVA. For all
statistical analyses the alpha was set to 0.05 and all analyses were conducted in
R 3.4.3 (Team 2018).
Results
Main Methods of Protection
Overall, wading birds nested on a small portion (4.9%) of apparently
suitable islands in coastal North Carolina, and were more likely to nest on islands
when alligator presence was likely than when unlikely (Pearson’s X2 =3.5591,
N=90, p=0.0358). However, there was no significant difference in the number of
islands that were used by nesting wading birds relative to alligator probability
after we considered the availability of islands in each of these areas (Pearson’s
X2 =0.0903, N=950, p=0.7638). So wading birds were apparently more likely to
nest on islands when alligator presence was likely than when alligator presence
57
was unlikely because there were just more islands available in areas where
alligators are likely. Thus, we found no evidence to support the prediction that
wading birds are nesting on islands more often when alligator presence is
unlikely.
Colonies on islands where alligator presence was unlikely were farther
from the mainland (Table 3-1, Figure 3-3A) and were also farther from any
landmass >5ha (Table 3-2, Figure 3-3B), compared to available control islands.
In general, and without regard to control islands, when alligator presence was
unlikely, colony islands were an average of 913m from the mainland and an
average of 254m from landmasses >5ha. When alligator presence was likely,
colony islands were an average of 730m from the mainland and an average of
164m from landmasses >5ha. This evidence suggests that wading birds actively
select nesting islands that are farther from any landmass that could potentially
contain mammalian predators when alligators are absent from colonies, be it
mainland or large islands.
Alternative Methods of Protection
In the absence of alligators, wading birds did not alter their colony site
preferences based on colony distance from other colonies (ΔAICc=2.32, β=-
141.57±157.72, p=0.3765), percent composition of human development within
buffer (ΔAICc=2.33, β=6.51±150.65, p=0.9657), vegetation height (ΔAICc=1.75,
β=-268.78±188.17, p=0.1574), or island size (ΔAICc=2.15, β=-24.74±80.68,
p=0.7602). However, when alligators were not present, wading birds preferred to
nest on islands that were farther from human development (Table 3-1, Table 3-2,
Figure 3-4). The interaction between likely alligator presence and proximity to
58
human development was not significant (Table 3-1, Table 3-2), meaning when
alligator occupancy is likely, wading birds don’t select colony sites based on the
distance to human development (Figure 3-4). This trend holds up when
considering the relative distance to human development, which was based on
availability (β=543.77±237.03 p=0.0242). When alligators were unlikely to be at
colonies, wading birds actively selected colony locations at sites that were farther
from the mainland or other large islands and farther from human activities and
habitation.
Latitude and Longitude had no effect on colony site selection preferences
(latitude ΔAICc=2.313, β=-184.04±231.17, p=0.4313; longitude ΔAICc=1.417,
β=208.29±326.98, p=0.2349). Colonies on the mainland (e.g. not on islands) had
significantly lower longevity than colonies on islands (F(1,88)=28.42, p<0.0001;
Figure 3-5A), but did not have a significant difference in colony size
(F(1,88)=0.202, p=0.654; Figure 3-5B).
Discussion
We hypothesized that without alligators as nest protectors, wading birds
alleviate predation pressure by altering their colony site selection preferences to
favor locations that provide them with additional protection from land predators.
When alligator occupancy was unlikely, nesting wading birds preferred colony
sites that were farther from the mainland, or other landmasses potentially
occupied by land predators, and farther from anthropogenic influence. These
results fall in line with our initial predictions that alligator presence plays a role in
wading bird colony site selection, and that in the absence of alligators, wading
birds prefer sites that are farther from areas that may attract or host land
59
predators. This suggests that nest protector occupancy allows wading birds to
nest in areas of the landscape that otherwise would not be chosen. This
reinforces the hypothesis that alligators facilitate a safer environment for nesting
wading birds, and when alligators are present wading birds have more relaxed
preferences regarding colony site selection.
Our results suggest that birds were no more or less likely to nest on
islands based on presence of alligators. This may be because water serves as a
partial barrier and an effective deterrent to mammalian predators (Erwin et al.
1986, White et al. 2005) with or without alligators. Alligators may be less
successful at deterring predators in dry conditions or very shallow water where
their mobility is more limited (Fleming et al. 1976, Frederick and Collopy 1989a,
Hunt and Ogden 1991, Burtner and Frederick 2017) and wading birds experience
greater amounts of predation by mammals in areas that are less inundated
(Rodgers 1987a, Ruckdeschel and Shoop 1987, Frederick and Collopy 1989a,
Kelly et al. 1993, Coulter and Bryan 1995). Mainland colonies in this study also
had a lower longevity compared to islands (Figure 3-5A), similar to a finding for
Wood Storks (Mycteria americana) in the southeastern US (Tsai et al. 2016).
Wading birds may be forced into mainland colonies in situations where viable
island sites are limited, and they likely experience increased nest predation in
these sites as a result.
The idea that water itself may be an effective buffer to predation was
further supported by wading bird preferences for islands that were farther from
mainland than controls. When alligator presence at the colony was unlikely,
wading birds preferred to nest on islands that were, on average, 913 meters from
60
the mainland, and 254 meters from landmasses >5ha in area. These colony
islands were also 193 meters farther from the mainland, and 90 meters farther
from landmasses >5ha in area, compared to islands where alligator presence is
likely. However, it seems possible that even these distances may not completely
eliminate mammals from colonies because many mammalian predators have
substantial swimming abilities. North American raccoons readily make water
crossings less than 400 meters but have been observed swimming across
open-water crossings of up to 950 meters (Hartman and Eastman 1999). Wading
birds evaluate the safety of the colony site from land predators such as raccoons
based on these abilities, and they prefer islands that are a farther distance from
the mainland or other areas that might host raccoons.
Anthropogenic disturbance may attract and subsidize certain nest
predators, increasing local nest predation (Haskell et al. 2001, Marzluff 2001,
Liebezeit et al. 2009). Wading birds preferred islands that were farther from
human development when alligator presence was unlikely but did not select
colony sites relative to human development when alligator presence was likely.
There are several interpretations of these results. First, wading birds may not
perceive human development as a direct threat if alligators are present. This
would be in line with previous research, which found that waterbirds and wading
birds are willing to tolerate increased levels of human disturbance found along
developed shorelines if it means being able to take advantage of the favorable
habitat located there (Traut and Hostetler 2004). In the absence of alligators,
however, it is unclear if the increased isolation of colonies is an attempt to reduce
human disturbance itself, or an attempt to reduce the effects of an elevated
61
density of raccoons and other mammalian predators. Raccoons are abundant in
human environments because of anthropogenic food sources such as pet food,
garbage, and bird feed that attract raccoons (Page et al. 2009). Wading birds
might be taking extra precautions to avoid areas that attract land predators, such
as areas with anthropogenic disturbance, when alligators aren’t present at colony
sites.
These results suggest that the relationship between nesting wading birds
and the American Alligator are a unique example of the presence of one animal
modifying the ability of a second animal in a way that allows the first to tolerate
close proximity to human development. This effect has been previously
undescribed in other nest protector relationships.The mechanisms that result in
this pattern are unclear, however, and future studies should focus on elucidating
exactly how alligator presence allows wading birds to tolerate proximity of human
development.
Urban and suburban areas generally have a higher raccoon density than
rural sites (Prange et al. 2003), because of supplemental food sources (Schinner
and Cauley 1974, Hoffmann 1979, Slate 1985), supplemental den sites (Schinner
and Cauley 1974, Hoffmann and Gottschang 1977, Hadidian et al. 1991), and
decreased vehicle related deaths (Prange et al. 2003). Urban ecosystems may
also offer year-round food resources for wading birds (McKinney et al. 2010,
Dorn et al. 2011, Murray et al. 2018) in a stable environment (Traut and Hostetler
2004). Colonies of several species have been shown to initiate and persist near
residential areas (Rodgers and Schwikert 1997, Tsai et al. 2016, Roshnath and
Sinu 2017). The predator paradox (Fischer et al. 2012) could explain why wading
62
birds in other areas choose urban sites for nesting despite likely increased
predator density. While this pattern seems well established, it is unclear whether
wading birds associate with human development due to a perceived lack of
threat from humans themselves, due to the perception of safety from nest
predators, or due to the ability to take advantage of abundant food resources.
This work suggests that alligator occupancy is an important determinant of
wading bird colony site selection preferences in North America. We would expect
to see a continuation, and perhaps expansion, of the preference for islands that
are farther from the mainland and farther from human development in more
northern parts of wading bird range where wading birds are nesting well outside
the farthest extent of alligators. Great Blue Herons (Ardea herodias) in Maine
nested exclusively on islands, and these islands were father from human
development than control islands even if it meant being farther from foraging
areas (Gibbs et al. 1987). On the other hand, we would expect to see wading
birds continue to choose colony sites that are on islands closer to the mainland
and without regard to human development in more southern parts of wading bird
range where alligators are more likely to be present. Colony locations in Florida,
where alligators are ubiquitous, were not influenced by the distance to the
mainland (Cox et al. 2019), and wading birds in Louisiana prioritized colony sites
that were closer to the mainland over more distant islands (Erwin et al. 1986).
Also, Wood Stork colonies in South Carolina, Georgia, and Florida that were
closer to human disturbance experienced a greater longevity (Rodgers and
Schwikert 1997, Tsai et al. 2016).
63
The evidence presented here supports the idea that facilitation can alter
the relationship between the fundamental and realized niche (Bruno et al. 2003,
Stachowicz 2012, Bulleri et al. 2016). In this case, alligator occupancy of a site
presumably releases additional potential wading bird nesting habitat by
facilitating a greater number of colony sites safe from nest predators, and thus,
allowing nesting wading birds to expand their realized niche in areas where these
species distributions overlap. This niche-based perspective on the effects of
facilitation can provide us with a greater understanding of the role of nest
protectors and other examples of animal-animal facilitation in community ecology
at landscape scales.
This study contributes to a better understanding of the ecosystem-level
impacts associated with wading bird colonization of island habitats and provides
regionally applicable management criteria for prioritizing colonies for high
conservation or management action. By describing the change in wading bird
colony site selection preference based on habitat occupancy of alligators, we
have demonstrated that at least one consequence of the nest protector
relationship can be realized at a large spatial scale. Enhanced numbers or
concentrations of human-subsidized predators poses a threat for nesting wading
birds, and these results suggest that increased urbanization may limit the number
of island sites that are viable for wading bird colonies outside the range of
alligators. It is crucial to understand the role of both natural and anthropogenic
influences when managing centralized breeding sites such as wading bird
colonies (Carrasco et al. 2014), especially given the advance of anthropogenic
influence in coastal environments. Additionally, our results have implications for
64
climate change given that alligator distribution limits are most likely driven by cold
temperatures (Brisbin Jr. et al. 1982). It is possible that as the earth warms there
will be an expansion in the distribution of alligators and other crocodilians, and
therefore a predicted change in the characteristics of wading bird colonies. Our
results further prove that it is important to fully understand mutualistic interactions
and the mechanisms by which they operate in order to fully comprehend the
intricacies of codependence, community dynamics, and species distribution.
65
Figure 3-1. Map of the study area with locations for all wading bird colonies and
control islands included in the analysis and the general alligator probability assignments throughout North Carolina. Solid white circles represent colony islands and small black circles represent control islands. Green blocks are areas where alligator occurence is likely and red blocks are areas where alligator occurence is unlikely. Note that control points were only created for island colonies. Map generated in ESRI ArcMap 10.6.1 (Esri 2018; http://www.esri.com/). Satellite imagery is the World Imagery basemap within ArcGIS 10.6 software (http://www.esri.com/data/basemaps), credited to Esri, DigitalGlobe, Earthstar Geographics, CNES/Airbus DS, GeoEye, USDA FSA, USGS, Aerogrid, IGN, IGP, and the GIS User Community. Gray inset extent map imagery is the Light Gray Canvas basemap within ArcGIS 10.6 software (http://www.esri.com/data/basemaps), credited to Esri, HERE, Garmin, © OpenStreetMap contributors, and the GIS User Community.
66
Figure 3-2. A section of the study area showing locations for wading bird
colonies and associated control points on islands, the mainland, and landmasses >5ha. Solid white circles represent colony locations and small black circles represent control island locations. Areas with orange transparency are landmasses >5ha (which includes the mainland) and areas with striping are classified as mainland. Islands are outlined in black. Map generated in ESRI ArcMap 10.6.1 (Esri 2018; http://www.esri.com/). Satellite imagery is the World Imagery basemap within ArcGIS 10.6 software (http://www.esri.com/data/basemaps), credited to Esri, DigitalGlobe, Earthstar Geographics, CNES/Airbus DS, GeoEye, USDA, USGS, AeroGRID, IGN, and the GIS User Community.
67
Table 3-1. Results of the best linear mixed-effects models assessing effect of
alligator probability and alternative methods of protection on relative colony distance from the mainland (meters). Model includes associated colony as random factor. All continuous variables were scaled.
Estimate Standard error t value Pr(>|z|)
(Intercept) 380.46 200.81 1.895 0.0644
Alligator probability, unlikely 1234.14 276.03 4.471 <0.001
Alligator probability, unlikely: distance to human development (m)
-357.11 324.78 -1.100 0.2744
Alligator probability, likely: distance to human development (m)
391.74 110.94 3.531 <0.001
68
Table 3-2. Results of the best linear mixed-effects models assessing effect of alligator probability and alternative methods of protection on relative colony distance from landmasses >5ha (meters). Model includes associated colony as random factor. All continuous variables were scaled.
Estimate Standard error t value Pr(>|z|)
(Intercept) 257.22 249.74 1.030 0.3097
Alligator probability, unlikely 806.08 356.52 2.261 0.0298
Alligator probability, unlikely: distance to human development (m)
34.50 37.80 0.913 0.3651
Alligator probability, likely: distance to human development (m)
306.47 104.20 2.941 0.0047
69
Figure 3-3. Colony island distance relative to control islands (meters) from A) the mainland and from B) landmasses >5ha, for
areas with alligator probability of occurence likely and unlikely. Please note that the distance represented in this figure is the relative distance of colony islands. Relative distance is the difference in distance between colony islands and control islands. For boxes, central line shows the median and boxes include all values within the 0.25 and 0.75 quantiles. Whiskers indicate range excluding outliers.
A B
70
Figure 3-4. Colony island distance relative to control islands (meters) from A) the mainland and from B) landmasses >5ha, as
a function of distance to human development (meters) for areas with alligator probability of occurrence likely (blue lines) and unlikely (red lines). Lines show a smoother fitted to predicted individual values (indicated by points) from best linear mixed effects model output for the model. Shaded areas indicate Standard Error of the smoother. Please note that the distance represented in this figure is the relative distance of colony islands. Relative distance is the difference in distance between colony islands and control islands.
A B
Development (m) Development (m)
71
Figure 3-5. Mainland and island colony characteristics of A) longevity (number of
years) and B) colony size (total number of nesting birds) relative to alligator probability. Likely alligator probability is represented by pink circles, unlikely alligator probability is represented by blue circles. For boxes, central line shows the median and boxes include all values within the 0.25 and 0.75 quantiles. Whiskers indicate range excluding outliers.
A B
Co
lony S
ize
(n
um
ber
nestin
g b
ird
s)
72
CHAPTER 4 SUMMARY
The wading bird/alligator system appears to be a particularly strong
mutualistic relationship, in which there are compelling benefits for both species.
American Alligators (Alligator mississippiensis) provide an additional defense for
nesting long-legged wading birds (Ciconiiformes) by serving as nest protectors
and deterring mammalian mesopredators. By examining the effects of alligator
presence on wading bird colony site selection preference, I have shown the
importance of this facilitative relationship to wading birds. Wading birds prefer
colony sites that provide extra protection from areas that may attract or host land
predators, such as the mainland, large islands, and areas with human
development when alligator occupancy is unlikely. Wading birds appear to
prioritize alligator protection as the main method of defense, abandoning the
preference for more distant and isolated sites when alligators are present.
Previous research has identified the potential that fallen nestlings could
have on supporting the nutrient deprived alligators of the Everglades, but we had
yet to quantify the nutrient link between these parties or estimate the impact this
large source of energy could have on the rest of the scavenger community. My
results indicate that fallen enestlings are a significant source of food for
scavengers, one that is substantial enough to support large numbers of both
alligators and vultures, the main scavenging species in colonies. Probability of
consumption by either scavenger is related to accessibility, namely distance to
water, nesting density, and island type. This work contributes to our
understanding of the true nature of the mutualistic relationship between nesting
wading birds and alligators.
73
Understanding the complexities of this relationship and how each species
depends on another is the next step to conducting more effective conservation
efforts of wading birds and Crocodilians worldwide. Comparable avian-
crocodilian codependence seems quite possible in other tropical and subtropical
wetland regions, where food-limited crocodilian populations may depend on
colonial wading birds for additional sustenance (Hutton 1987, Campbell et al.
2008, Wallace and Leslie 2008, Mazzotti et al. 2009, Nell and Frederick 2015).
Codependence between alligators and wading birds in regions where they
coexist would mean the presence of both is needed for the greatest success of
either. Outside of alligator range, wading bird habitat preference depends on
isolated islands farther from human development or other areas that may attract
or host land predators, and these important nesting areas should be the focus of
conservation efforts. Understanding this relationship could have huge
management implications for both species globally.
74
APPENDIX CHAPTER 3 SUPPORTING MATERIAL: DETAILED SURVEY METHODS FOR
WADING BIRD COLONIES IN NORTH CAROLINA
The North Carolina Colonial Waterbird Database contains a history of all
known nesting sites of colonial waterbirds in North Carolina. New colonies of
wading birds are identified and surveyed using four different methodologies:
coast-wide surveys, inland surveys, wood stork surveys, and occasionally
opportunistically.
Coast-Wide Surveys: Conducted every three to four years (75, 76, 77, 83, 88,
93, 95, 97, 99, 01, 04, 07, 11, 14, 17) using methods described by Parnell and
Soots (1979) and Parnell and McCrimmon (1984). Depending on colony size, 1-
15 observers count active nests (defined as ≥1 egg or chick) along a transect
spaced 3-15m apart. Complete ground counts are preferred, but if chicks are
mobile colonies are then counted from the perimeter or the number of breeding
pairs are estimated from adult counts.
Inland Surveys: Conducted less frequently (75, 76, 96, 08/09) than coast-wide
surveys. All river basins, main river tributaries, and large swamps are surveyed
from an altitude of 800’ by a fixed-winged aircraft. Once a colony is located it is
circled, counted, and photographed and counts between multiple observers are
averaged. A follow-up ground count is conducted for large colonies, colonies with
a species of concern, and colony counts with a lot of uncertainty. Ground counts
are done as close to aerial survey date as possible.
Wood Stork Surveys: Conducted annually since 2005 using fixed wing aircraft,
UAV, kayak, and on foot. Periphery counts of Wood Stork nests are conducted
from kayaks, counts from the ground and UAV are used to estimate numbers of
75
active nests. Exact methods of survey vary slightly by colony. While this study did
not include Wood Storks, these survyes often produced colony counts of other
types of nesting wading birds that were of interest here.
Opportunisitic Colony Finds: Any other surveys are from trusted people
reporting species numbers from colonies that they encountered, either while
conducting another survey, or some other activity. These trusted people often
include land surveyors or botanists surveying in places that otherwise would not
have been searched for wading bird colonies.
76
LIST OF REFERENCES
Altieri, Silliman, and Bertness. 2017. Hierarchical Organization via a Facilitation Cascade in Intertidal Cordgrass Bed Communities. The American Naturalist 169:195.
Annual Performance Report, Inland Colonial Waterbird Survey. 1996. .
Bancroft, T. G., A. M. Strong, R. J. Sawicki, W. Hoffman, and S. D. Jewell. 1994. Relationships among wading bird foraging patters, colony locations, and hydrology in the Everglades. Pages 615–657 in S. Davis and J. C. Ogden, editors. Everglades: the ecosystem and its restoration. St. Lucie Press, Delray Beach, FL, USA.
Bates, D., M. Maechler, B. Bolker, S. Walker, R. H. B. Christensen, H. Singmann, B. Dai, and C. Eigen. 2014. Package “lme4.”
Beasley, J. C., Z. H. Olson, and T. L. Devault. 2012. Carrion cycling in food webs: Comparisons among terrestrial and marine ecosystems. Oikos 121:1021–1026.
Beasley, J. C., Z. H. Olson, and T. L. Devault. 2015. Ecological Role of Vertebrate Scavengers. Pages 107–121 in M. Eric Benbow, J. K. Tomberlin, and A. M. Tarone, editors. Carrion Ecology, Evolution, and Their Applications. CRC Press.
Beaver, D. L., R. G. Osborn, and T. W. Custer. 1980. Nest-Site and Colony Characteristics of Wading Birds in Selected Atlantic Coast Colonies. The Wilson Bulletin 92:200–220.
Ben-David, M., T. A. Hanley, D. R. Klein, and D. M. Schell. 1997. Seasonal changes in diets of coastal and riverine mink: the role of spawning Pacific salmon. Canadian Journal of Zoology 75:803–811.
Bent, A. C. 1963. Life Histories of North American Marsh Birds. Dover Publications, Inc., New York.
Bertness, M. D. 1984. Ribbed Mussels and Spartina Alterniflora Production in a New England Salt Marsh. Ecology 65:1794–1807.
Best, L. B., and D. F. Stauffer. 1980. Factors Affecting Nesting Success in Riparian Bird Communities. Condor 82:149–158.
Bildstein, K. L., E. Blood, P. Frederick, R. Hill, and S. Carolina. 1992. The Relative Importance of Biotic and Abiotic Vectors in Nutrient Transport. Estuaries 15:147–157.
Birkhead, W. S., and C. R. Bennett. 1981. Observations of a small population of estuarine-inhabiting alligators near Southport, North Carolina. Brimleyana 6:111–117.
77
Boucher, D. H., S. James, and K. H. Keeler. 1982. The Ecology of Mutualism. Annual Review of Ecology and Systematics.
Boutin, S. 1990. Food supplementation experiments with terrestrial vertebrates: patterns, problems and the future. Canadian Journal of Zoology 68:203–220.
Brisbin Jr., L. I., E. A. Standora, and M. J. Vargo. 1982. Body Temperatures and Behavior of American Alligators during Cold Winter Weather. The American Midland Naturalist 107:209–218.
Bronstein, J. L. 2001. The costs of Mutualism. American Zoologist 839:825–839.
Bronstein, J. L. 2009. The evolution of facilitation and mutualism. Journal of Ecology 97:1160–1170.
Brooker, R. W., F. T. Maestre, R. M. Callaway, C. L. Lortie, L. A. Cavieres, G. Kunstler, P. Liancourt, K. Tielbörger, J. M. J. Travis, F. Anthelme, C. Armas, L. Coll, E. Corcket, S. Delzon, E. Forey, Z. Kikvidze, J. Olofsson, F. I. Pugnaire, C. L. Quiroz, P. Saccone, K. Schiffers, M. Seifan, B. Touzard, and R. Michalet. 2008. Facilitation in plant communities: the past, the present, and the future. Journal of Ecology 96:18–34.
Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation into ecological theory.
Bulleri, F., J. F. Bruno, B. R. Silliman, and J. J. Stachowicz. 2016. Facilitation and the niche: Implications for coexistence, range shifts and ecosystem functioning. Functional Ecology.
Burger, J. 1981. A Model for the Evolution of Mixed-Species Colonies of Ciconiiformes. The Quarterly Review of Biology 56:143–167.
Burtner, B. F., and P. C. Frederick. 2017. Attraction of Nesting Wading Birds to Alligators (Alligator mississippiensis). Testing the ‘Nest Protector’ Hypothesis. Wetlands.
Butler, R. W., M. Lemon, and M. Rodway. 1985. Northwestern Crows in a Rhinoceros Auklet Colony: Predators and Scavengers. The Murrelet 66:86.
Byrne, M. E., A. E. Holland, K. L. Turner, A. L. Bryan, and J. C. Beasley. 2019. Using multiple data sources to investigate foraging niche partitioning in sympatric obligate avian scavengers. Ecosphere 10.
Campbell, H. A., M. A. Micheli, and A. Abe. 2008. A seasonally dependent change in the distribution and physiological condition of Caiman crocodilus yacare in the Paraguay River Basin. Wildlife Research.
78
Campbell, M. R., and F. J. Mazzotti. 2004. Characterization of Natural and Artificial Alligator Holes. Southeastern Naturalist 3:583–594.
Carrasco, L., M. Mashiko, and Y. Toquenaga. 2014. Application of random forest algorithm for studying habitat selection of colonial herons and egrets in human-influenced landscapes. Ecological Research 29:483–491.
Carrete, M., S. A. Lambertucci, K. Speziale, O. Ceballos, A. Travaini, M. Delibes, F. Hiraldo, and J. A. Donázar. 2010. Winners and losers in human-made habitats: Interspecific competition outcomes in two Neotropical vultures. Animal Conservation 13:390–398.
Clark, A. B., and D. S. Wilson. 1981. Avian Breeding Adaptations: Hatching Asynchrony, Brood Reduction, and Nest Failure. The Quarterly Review of Biology 56:253–277.
Coleman, J. S., and J. D. Fraser. 1987. Food Habits of Black and Turkey Vultures in Pennsylvania and Maryland. The Journal of Wildlife Management 51:733–739.
Cottam, G., and J. T. Curtis. 1956. The Use of Distance Measures in Phytosociological Sampling Author ( s ): Grant Cottam and J . T . Curtis Reviewed work ( s ): Published by : Ecological Society of America Stable URL : http://www.jstor.org/stable/1930167 . America 37:451–460.
Coulter, M. C., and L. A. Bryan. 1995. Factors Affecting Reproductive Success of Wood Storks (Mycteria americana) in East- Central Georgia. The Auk 112:237–243.
Couzin, I. D. 2009. Collective cognition in animal groups. Trends in Cognitive Sciences 13:36–43.
Cox, W. A., B. Bankovich, K. Malachowski, A. C. Schwarzer, A. Paul, M. Rachal, J. J. Lorenz, K. D. Meyer, and G. M. Kent. 2019. Nest site selection by reddish egrets in Florida. Journal of Wildlife Management 83:184–191.
Crawley, M. J. 2007. The R Book. Page The R Book.
Custer, C. M., and J. Galli. 2006. Feeding Habitat Selection by Great Blue Herons and Great Egrets Nesting in East Central Minnesota. Waterbirds 25:115–124.
Custer, T. W., and R. G. Osborn. 1977. Wading birds as biological indicators 1975 colony survey. Special Scientific Report -- Wildlife.
Custer, T. W., and R. G. Osborn. 1978. Feeding Habitat Use by Colonially-Breeding Herons , Egrets , and Ibises in North Carolina. The Auk 95:733–743.
Dalrymple, G. H. 1996. Growth of American Alligators in the Shark Valley Region of Everglades National Park. Source: Copeia:212–216.
79
Dalrymple, G. H. 2001. American Alligator Nesting and Reproductive Success in Everglades National Park: An Analysis of the Systematic Reconnaissance Flight (SRF) Data from 1985-1998. Final Report.
Davis, S. M. 1994. Phosphorus inputs and vegetation sensitivity in the Everglades. Pages 357–378 Evergaldes, the Ecosystem and it’s Restoration. St. Lucie Press, Delray Beach, FL, USA.
Deneubourg, J. L., and S. Goss. 1989. Collective patterns and decision-making. Ethology Ecology and Evolution 1:295–311.
DeVault, T. L., J. C. Beasley, Z. H. Olson, M. Moleón, M. Carrete, A. Margalida, and J. A. Sánchez-Zapata. 2016. Ecosystem Services Provided by Avian Scavengers. Why Birds Matter: Avian Ecological Function and Ecosystem Services:235–270.
DeVault, T. L., and A. R. Krochmal. 2002. Scavenging by Snakes : An Examination of the Literature. Herpetologica 58:429–436.
DeVault, T. L., O. E. Rhodes, and J. A. Shivik. 2003. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 2:225–234.
Dorn, N. J., M. I. Cook, G. Herring, R. A. Boyle, J. Nelson, and D. E. Gawlik. 2011. Aquatic prey switching and urban foraging by the White Ibis Eudocimus albus are determined by wetland hydrological conditions. Ibis 153:323–335.
Dunham, K., S. Dinkelacker, and J. Miller. 2014. A stage-based population model for American alligators in northern latitudes. Journal of Wildlife Management 78:440–447.
Dunn, E. H. 1975. Growth, Body Components and Energy Content of Nestling Double-Crested Cormorants. The Condor 77:431.
Dunson, W., and F. Mazzotti. 1989. Salinity as a limiting factor in the distribution of reptiles in Florida Bay: a theory for the estuarine origin of marine snakes and turtles. Bulletin of Marine Science 44:229–244.
Durango, S. 1949. The nesting associations of birds with social insects and with birds of different species. Ibis 91:140–143.
Dusi, J. L., and R. T. Dusi. 1968. Ecological Factors Contributing to Nesting Failure in a Heron Colony. Source: The Wilson Bulletin 80:458–466.
Eason, P., B. Rabea, and O. Attum. 2012. Island shape, size, and isolation affect nest-site selection by Little Terns. Journal of Field Ornithology 83:372–380.
80
Van Eerden, M. R., K. Koffijberg, and M. Platteeuw. 1995. Riding on the crest of the wave: Possibilities and limitations for a thiriving population of migratoy Great Cormorant (Phalacrocorax carbo). Page 338 Man-Dominated wetlands. 83rd edition. Nederlandse Ornithologische Unie (NOU).
Ehrenfeld, J. G., and L. A. Toth. 1997. Restoration Ecology and the Ecosystem Perspective. Restoration Ecology 5:307–317.
Ellis, J. C. 2005. Marine birds on land: A review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecology 181:227–241.
Elsey, R. M., and A. R. Woodward. 2010. Alligator mississippiensis (American Alligator). Pages 1–4 in S. C. Manolis and C. Stevenson, editors. Crocodiles: Status Survey and Conservation Action Plan. Third edition. Crocodile Specialist Group, Darwin, Australia.
Emslie, S. D., N. Karnovsky, and W. Trivelpiece. 1995. Avian Predation at Penguin Colonies on King George Island , Antarctica. Wilson Ornithological Society 107:317–327.
Erwin, R. M., J. S. Hatfield, and T. J. Wilmers. 1995. The value and vulnerability of small estuarine islands for conserving metapopulations of breeding waterbirds. Biological Conservation.
Erwin, R. M., J. A. Spendelow, P. H. Geissler, and K. B. Williams. 1986. Relationships between nesting populations of wading birds and habitat features along the Atlantic Coast. Pages 55–69 in W. R. Whitman and W. H. Meredith, editors. Waterfowl and Wetlands Symposium: Proceedings of a Symposium on Waterfowl and Wetlands Management in the Coastal Zone of the Atlantic Flyway. Delaware Coastal Management Program, Delaware Department of Natural Resources and Environmental Control, Dover, Delaware.
Erwin, R. M., D. B. Stotts, and J. S. Hatfield. 1996. Reproductive Success, Growth and Survival of Black-Crowned Night-Heron (Nycticorax nycticorax) and Snowy Egret (Egretta thula) Chicks in Coastal Virginia. The Auk 113:119–130.
Esri. 2018. ArcGIS Desktop: Release 10.6.
Fasola, M., and R. Alieri. 1992. Conservation of heronry Ardeidae sites in North Italian agricultural landscapes. Biological Conservation 62:219–228.
Fischer, J. D., S. H. Cleeton, and P. Timothy. 2012. Urbanization and the Predation Paradox : The Role of Trophic Dynamics in Structuring Vertebrate Communities 62:809–818.
Fish, F. E., S. A. Bostic, A. J. Nicastro, and J. T. Beneski. 2007. Death roll of the alligator: mechanics of twist feeding in water. Journal of Experimental Biology 210:2811–2818.
81
Fleming, D. M., A. W. Palimisano, and T. Joanen. 1976. Food habits of coastal marsh raccoons with observation of alligator nest predation. Proceedings of the Annual Conference Southeastern Association of Fish and Wildlife Agencies 30:348–357.
Frederick, P. C., and M. W. Collopy. 1988. Reproductive ecology of wading birds in relation to water conditions in the Florida Everglades.
Frederick, P. C., and M. W. Collopy. 1989a. Nesting Success of Five Ciconiiform Species in Relation to Water Conditions in the Florida Everglades. The Auk 106:625–634.
Frederick, P. C., and M. W. Collopy. 1989b. The Role of Predation in Determining Reproductive Success of Colonially Nesting Wading Birds in the Florida Everglades. The Condor 91:860–867.
Frederick, P. C., and J. C. Ogden. 2002. Monitoring wetland ecosystems using avian populations: seventy years of surveys in the Everglades. Pages 321–350 in D. Busch and J. Trexler, editors. Monitoring ecosystems: interdisciplinary approaches for evaluating ecoregional initiatives. Isalnd Press, Washington DC, USA.
Frederick, P., and G. V. Powell. 1994. Nutrient transport by wading birds in the Everglades. St. Lucie Press, Boca Raton, FL, USA.
Freestone, A. L. 2006. Facilitation drives local abundance and regional distribution of a rare plant in a harsh environment. Ecology 87:2728–2735.
Fujisaki, I., F. J. Mazzotti, K. M. Hart, K. G. Rice, D. Ogurcak, M. Rochford, B. M. Jeffery, L. A. Brandt, and M. S. Cherkiss. 2012. Use of alligator hole abundance and occupancy rate as indicators for restoration of a human-altered wetland. Ecological Indicators 23:627–633.
Gardner, B., L. A. Garner, D. T. Cobb, and C. E. Moorman. 2016. Factors Affecting Occupancy and Abundance of American Alligators at the Northern Extent of Their Range. Journal of Herpetology 50:541–547.
Garrick, L. D., and J. W. Lang. 1977. Social Signals and Behaviors of Adult Alligators and Crocodiles. AMER. ZOOU 17:225–239.
Gibbs, J. P., and L. K. Kinkel. 1997. Determinants of the Size and Location of Great Blue Heron Colonies. Colonial Waterbirds 20:1–7.
Gibbs, J. P., S. Woodward, M. L. Hunter, and A. E. Hutchinson. 1987. Determinants of Great Blue Heron Colony Distribution in Coastal Maine. The Auk 104:38–47.
Green, A. J., and J. Elmberg. 2014. Ecosystem services provided by waterbirds. Biological Reviews 89:105–122.
82
Greer, R. C., C. Cordes, and C. Keller. 1985. Analysis of colonial wading habitat in Louisiana. Pages 143–151 in C. Bryan, P. Zwank, and R. Chabrek, editors. Proceedings 4th Marsh and Estuary Management Symposium. Louisiana Coop. Fish and Wildlife Research Unit, Louisiana State University, Baton Rouge, Louisiana.
Grimes, L. G. 1973. The Breeding of Heuglin’s Masked Weaver and its Nesting Association with the Red Weaver Ant. Ostrich 44:170–175.
Hadidian, J., D. A. Manski, and S. Riley. 1991. Daytime resting site selection in an urban raccoon population. Pages 39–45 in L. W. Adams and D. L. Leedy, editors. Wildlife Conservation in Metropolitan Environments. National Institute for Urban Wildlife Symposium Series 2, Colombia, Maryland.
Haemig, P. D. 2001. Symbiotic nesting of birds with formidable animals: A review with applications to biodiversity conservation. Biodiversity and Conservation.
Hafner, H. 2000. Heron nest site conservation. Pages 201–217 in J. A. Kushlan and H. Hafner, editors. Heron Conservation. Academic Press, San Diego, Californaia.
Harvey, J. A., P. J. Ode, M. Malcicka, and R. Gols. 2016. Short-term seasonal habitat facilitation mediated by an insect herbivore. Basic and Applied Ecology 17:447–454.
Haskell, D. C., A. M. Knupp, and M. C. Schneider. 2001. Nest predator abundance and urbanization. Pages 243–257 in J. M. Marzluff, R. Bowman, and R. Donnelly, editors. Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Haskins, J. W. 1972. An ecological study of two species of vultures: Cathartes aura abd Coragyps atratus. Stephen F. Austin State University.
Hertel, F. 1994. Diversity in Body Size and Feeding Morphology within Past and Present Vulture Assemblages. Ecology 75:1074–1084.
Hewson, R. 1995. Use of salmonid carcasses by vertebrate scavengers. Journal of Zoology 235:53–65.
Hill, J. E., T. L. DeVault, J. C. Beasley, O. E. Rhodes, and J. L. Belant. 2018. Roads do not increase carrion use by a vertebrate scavenging community. Scientific Reports 8:1–10.
Høberg, P., M. Lindholm, L. Ramberg, and D. O. Hessen. 2002. Aquatic food web dynamics on a floodplain in the Okavango delta, Botswana. Hydrobiologia 470:23–30.
Hoffmann, C. 1979. Weights of Suburban Raccoons in Southwestern Ohio. Ohio Journal of Science 79:139–142.
83
Hoffmann, C. O., and J. L. Gottschang. 1977. Numbers , Distribution , and Movements of a Raccoon Population in a Suburban Residential Community. Journal of Mammology 58:623–636.
Hoogland, J. L., and P. W. Sherman. 1976. Advantages and Disadvantages of Bank Swallow (Riparia riparia) Coloniality. Source: Ecological Monographs 46:33–58.
Hoover, J. P. 2006. Water depth influences nest predation for a wetland-dependent bird in fragmented bottomland forests. Biological Conservation 127:37–45.
Howald, G. R., P. Mineau, J. E. Elliott, and K. M. Cheng. 1999. Brodifacoum poisoning of avian scavengers during rat control on a seabird colony. Ecotoxicology 8:431–447.
Hunt, H. R., and J. J. Ogden. 1991. Selected aspects of nesting ecology of American Alliagtors in the Okefenokee Swamp. Journal of Herpetology 25:448–453.
Hunter, S. 1991. The impact of avian predator‐scavengers on King Penguin Aptenodytes patagonicus chicks at Marion Island. Ibis 133:343–350.
Hutton, J. M. 1987. Growth and Feeding Ecology of the Nile Crocodile Crocodylus niloticus at Ngezi , Zimbabwe. Journal of Animal Ecology 56:25–38.
iNaturalist.org. 2019. iNaturalist Research-Grade Observations. https://doi.org/10.15468/ab3s5x.
Irick, D. L., B. Gu, Y. C. Li, P. W. Inglett, P. C. Frederick, M. S. Ross, A. L. Wright, and S. M. L. Ewe. 2015. Wading bird guano enrichment of soil nutrients in tree islands of the Florida Everglades. Science of the Total Environment 532:40–47.
Jackson, J. A., I. D. Prather, R. N. Conner, and S. Parness. 1978. Fishing Behavior of Black and Turkey Vultures. The Wilson Bulletin 90:141–143.
Jacobsen, T., and J. A. Kushlan. 1989. Growth dynamics in the American alligator (Alligator mississippiensis). Journal of Zoology 219:309–328.
Jenni, D. A. 1969. A Study of the Ecology of Four Species of Herons during the Breeding Season at Lake Alice , Alachua County , Florida. Ecological Monographs 39:245–270.
Joanen, T., and L. L. Mcnease. 1989. Ecology and Physiology of Nesting and Early Development of the American Alligator. American Zoologist 29:987–998.
Jungwirth, A., D. Josi, J. Walker, and M. Taborsky. 2015. Benefits of coloniality: Communal defence saves anti-predator effort in cooperative breeders. Functional Ecology 29:1218–1224.
84
Kahl, P. M. J. 1962. Bioenergetics of Growth in Nestling Wood Storks. The Condor 64:169–183.
Kane, A., K. Healy, T. Guillerme, G. D. Ruxton, and A. L. Jackson. 2016. A recipe for scavenging in vertebrates - the natural history of a behaviour. Ecography 40:324–334.
Kelly, J. P., H. M. Pratt, and P. L. Greene. 1993. The Distribution, Reproductive Success, and Habitat Characteristics of Heron and Egret Breeding Colonies in the San Francisco Bay Area. Source: Colonial Waterbirds 16:18–27.
Kelly, J. P., D. Stralberg, K. Etienne, and M. McCaustland. 2008. Landscape influence on the quality of heron and egret colony sites. Wetlands 28:257–275.
Kendall, C. J. 2014. The early bird gets the carcass: Temporal segregation and its effects on foraging success in avian scavengers. The Auk 131:12–19.
Komen, J. 2007. Energy Requirements of Nestling Cape Vultures. The Condor 93:153–158.
Kotler, B. P., L. Blaustein, and J. S. Brown. 1992. Predator facilitation: the combined effect of snakes and owls on the foraging behavior of gerbils. Annales Zoologici Fennici 29:199–206.
Kushlan, J. A., and B. Hunt. 1979. Limnology of an alligator pond in South Florida. Florida Scientist 42:66–84.
Kushlan, J. A., and M. S. Kushlan. 1980. Function of Nest Attendance in the American Alligator. Herpetologica 36:27–32.
Lauren, D. J. 1982. Effect of salt stress on electrolyte balance, corticosterone titer, and nitrogen metabolism in the American alligator, Alligator mississippiensis (Daudin, 1802). 81:1–141.
Lemon, W. C. 1991. Foraging Behavior of a Guild of Neotropical Vultures. The Wilson Bulletin 103:698–702.
Liebezeit, J. R., S. J. Kendall, S. Brown, C. B. Johnson, P. Martin, T. L. McDonald, D. C. Payer, C. L. Rea, B. Streever, A. M. Wildman, and S. Zack. 2009. Influence of human development and predators on nest survival of tundra birds, Arctic Coastal Plain, Alaska. Ecological Applications 19:1628–1644.
Lindeman, R. L. 1942. The Trophic-Dynamic Aspect of Ecology. Ecology 23:399–417.
Lodge, T. E. 2016. The Everglades handbook: understanding the ecosystem. Crc Press.
85
Lotze, J., and S. Anderson. 1979. American Society of Mammalogists Procyon lotor. Mammalian Species:1–8.
Loveless, C. M. 2006. A Study of the Vegetation in the Florida Everglades. Ecology 40:1–9.
Loya, Y. 1978. Plotless and transect methods. Pages 197–218 in D. R. Stoddart and R. E. Johannes, editors. Monographs on Oceanic Methodology. Fifth edition. UNESCO Press.
Marzluff, J. M. 2001. Worldwide urbanization and its effects on birds. Pages 19–47 in R. Marzluff, R. Bowman, and R. Donnelley, editors. Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Mazzotti, F. J., G. R. Best, L. A. Brandt, M. S. Cherkiss, B. M. Jeffery, and K. G. Rice. 2009. Alligators and crocodiles as indicators for restoration of Everglades ecosystems. Ecological Indicators.
Mazzotti, F. J., and L. A. Brandt. 1994. Ecology of the American alligator in a seasonally fluctuating environment. Pages 485–505 in S. M. Davis and J. C. Ogden, editors. Everglades: the ecosystem and its restoration. St. Kucie Press, Delray Beach, FL, USA.
McIlhenny, E. A. 1935. Alligator’s Life History. Christopher Publishing House, USA.
McKinney, R. A., K. B. Raposa, and T. E. Kutcher. 2010. Use of urban marine habitats by foraging wading birds. Urban Ecosystems 13:191–208.
Mock, D. W. 1984. Siblicidal Aggression and Resource Monopolization in Birds. Science 225:731–733.
Moleón, M., J. A. Sánchez-Zapata, N. Selva, J. A. Donázar, and N. Owen-Smith. 2014. Inter-specific interactions linking predation and scavenging in terrestrial vertebrate assemblages. Biological Reviews 89:1042–1054.
Møller, A. P. 1987. Advantages and disadvantages of coloniality in the swallow, Hirundo rustica. Animal Behaviour 35:819–832.
Monsarrat, S., S. Benhamou, F. Sarrazin, C. Bessa-Gomes, W. Bouten, and O. Duriez. 2013. How Predictability of Feeding Patches Affects Home Range and Foraging Habitat Selection in Avian Social Scavengers? PLoS ONE 8:1–11.
Moreau, R. E. 1936. Bird-Insect nesting associations. Ibis:460–471.
Moreno-Opo, R., and A. Margalida. 2013. Carcasses provide resources not exclusively to scavengers: Patterns of carrion exploitation by passerine birds. Ecosphere 4:1–15.
86
Murray, M. H., A. D. Kidd, S. E. Curry, J. Hepinstall-Cymerman, M. J. Yabsley, H. C. Adams, T. Ellison, C. N. Welch, and S. M. Hernandez. 2018. From wetland specialist to hand-fed generalist: Shifts in diet and condition with provisioning for a recently urbanized wading bird. Philosophical Transactions of the Royal Society B: Biological Sciences 373.
Myers, J. G. 1929. The nesting-together of birds, wasps and ants.
Nell, L. A., and P. C. Frederick. 2015. Fallen Nestlings and Regurgitant as Mechanisms of Nutrient Transfer from Nesting Wading Birds to Crocodilians. Wetlands.
Nell, L. A., P. C. Frederick, F. J. Mazzotti, K. A. Vliet, and L. A. Brandt. 2016. Presence of breeding birds improves body condition for a crocodilian nest protector. PLoS ONE 11:1–16.
Nifong, J. C. 2014. Use of Marine Habitat and Food Resources by Coastal Inhabiting Alligator Mississippienis (American Alligator): Implications for Food Web and Community Dynamics. University of Florida.
Nilsson, S. G. . 1984. The Evolution of Nest-Site Selection among Hole-Nesting Birds : The Importance of Nest Predation and Competition 15:167–175.
Nummi, P., and A. Hahtola. 2008. The beaver as an ecosystem engineer. Ecography 31:519–524.
O’Brien, T. G., and P. D. Doerr. 1986. Night Count Surveys for Alligators in Coastal Counties of North Carolina. Journal of Herpetology 20:444–448.
Odadi, W. O., M. Jain, S. E. Van Wieren, H. H. T. Prins, and D. I. Rubenstein. 2011. Facilitation between bovids and equids on an African savanna. Evolutionary Ecology Research 13:237–252.
Ogden, J. C. 1991. Nesting by Wood Storks in Natural , Altered , and Artificial Wetlands in Central and Northern Florida 14:39–45.
Oliver, J. D., and S. A. Schoenberg. 1989. Residual Influence of Macronutrient Enrichment on the Aquatic Food Web of an Okefenokee Swamp Abandoned Bird Rookery. Oikos 55:175–182.
Oliveras de Ita, A., and O. R. Rojas-Soto. 2006. Ant Presence in Acacias: An Association That Maximizes Nesting Success in Birds? The Wilson Journal of Ornithology 118:563–566.
Owre, O. T., and P. O. Northington. 1961. Indication of the Sense of Smell in the Turkey Vulture , Cathartes aura (Linnaeus), from Feeding Tests. The American Midland Naturalist 66:200–205.
87
Page, K. L., C. Anchor, E. Luy, S. Kron, G. Larson, L. Madsen, K. Kellner, and and T. J.Smyser. 2009. Backyard Raccoon Latrines and Risk for Baylisascaris procyonis Transmission to Humans Reemergence of Strongyloidiasis. Emerging Infectious Diseases 15:60–61.
Palmer, M. L., and F. J. Mazzotti. 2004. Structure of Everglades alligator holes. Southeastern Naturalist 9:487–496.
Parlin, A., S. Dinkelacker, and A. Mccall. 2015. Do Habitat Characteristics Influence American Alligator Occupancy of Barrier Islands in North Carolina? Southeastern Naturalist 14:33–40.
Parnell, J. F., and D. A. McCrimmon. 1984. 1983 supplement to Atlas of Colonial Waterbirds of North Carolina estuaries. Page UNC Sea Grant Publication UNC-SG-84-07. Raleigh, NC.
Parsons, K. C. 2003a. Reproductive Success of Wading Birds Using and Upland Nesting Habitats Phragmites Marsh 26:596–301.
Parsons, K. C. 2003b. Reproductive Success of Wading Birds Using Phragmites Marsh and Upland Nesting Habitats. Source: Estuaries Part B 26:596–601.
Parsons, K. C., S. R. Schmidt, and A. C. Matz. 2001. Regional Patterns of Wading Bird Productivity in Northeastern. The International Journal of Waterbird Biology 24:323–330.
Paton, P. W. C., R. J. Harris, and C. L. Trocki. 2005. Distribution and Abundance of Breeding Birds in Boston Harbor. Northeastern Naturalist 12:145–168.
Pedlar, J. H., L. Fahring, and G. Merriam. 1997. Raccoon Habitat Use at 2 Spatial Scales. The Journal of Wildlife Management 61:102–112.
Pius, S. M., and P. L. Leberg. 1998. The Protector Species Hypothesis: Do Black Skimmers Find Refuge from Predators in Gull-billed Tern Colonies? Ethology 104:273–284.
Polis, G. A., and S. D. Hurd. 1996. Linking Marine and Terrestrial Food Webs: Allochthonous Input from the Ocean Supports High Secondary …. The American Naturalist.
Porter, J. H., R. D. Dueser, and N. D. Moncrief. 2015. Cost-distance analysis of mesopredators as a tool for avian habitat restoration on a naturally fragmented landscape. Journal of Wildlife Management 79:220–234.
Post, D. M., J. P. Taylor, J. F. Kitchell, M. H. Olson, and D. E. Schindler. 1998. The Role of Migratory Waterfowl as Nutrient Vectors in a Managed Wetland. Conservation Biology 12:910–920.
88
Post, W. 1990. Nest Survival in a Large Ibis-Heron Colony during a Three-Year Decline to Extinction. The Waterbird Society 13:50–61.
Post, W., and C. A. Seals. 1991. Breeding Biology of the Common Moorhen in an Impounded Cattail Marsh. Journal of Field Ornithology 71:437–442.
Prange, S., S. D. Gehrt, and E. P. Wiggers. 2003. Demographic Factors Contributing to High Raccoon Densities in Urban Landscapes. Wildlife Management 67:324–333.
Quinn, J. L., and M. Ueta. 2008. Protective nesting associations in birds. Ibis 150:146–167.
Raye, S. S. C., and J. Burger. 1979. Behavioral Determinants of Nestling Success of Snowy Egrets (Leucophoyx thula). American Midland Naturalist.
Read, J. L., and D. Wilson. 2004. Scavengers and detritivores of kangaroo harvest offcuts in arid Australia. Wildlife Research 31:51.
Richardson, D. S., and G. M. Bolen. 1999. A nesting association between semi-colonial Bullock’s orioles and yellow-billed magpies: Evidence for the predator protection hypothesis. Behavioral Ecology and Sociobiology.
Ricklefs, R. E. 1965. Brood Reduction in the Curve-Billed Thrasher. The Condor 67:505–510.
Robinson, S. K. 1985a. Coloniality in the Yellow-Rumped Cacique as a Defense against Nest Predators. Source: The Auk 102:506–519.
Robinson, S. K. 1985b. Coloniality in the Yellow-Rumped Cacique as a Defense against Nest Predators. The Auk 102:506–519.
Rodgers, J. A. 1987a. On the Antipredator Advantages of Coloniality: A Word of Caution. Source: The Wilson Bulletin 99:269–271.
Rodgers, J. A. 1987b. On the Antipredator Advantages of Coloniality: A Word of Caution. Source: The Wilson Bulletin 99:269–271.
Rodgers, J. A., and S. T. Schwikert. 1997. Breeding success and chronology of Wood Storks Mycteria americana in northern and central Florida, U.S.A. Ibis 139:76–91.
Rooney, N., K. McCann, G. Gellner, and J. C. Moore. 2006. Structural asymmetry and the stability of diverse food webs. Nature 442:265–269.
Rosenblatt, A. E., and M. R. Heithaus. 2011. Does variation in movement tactics and trophic interactions among American alligators create habitat linkages? Journal of Animal Ecology 80:786–798.
89
Roshnath, R., and P. A. Sinu. 2017. Are the heronry birds adapting to urbanization? Bird-O-Soar #008. Zoo’s Print 32:27–33.
Ruckdeschel, C., and C. R. Shoop. 1987. Aspects of wood stork nesting ecology on Cumberland Island Georgia, USA. Oriole 52:21–27.
Ruxton, G. D., and D. C. Houston. 2004. Obligate vertebrate scavengers must be large soaring fliers. Journal of Theoretical Biology 228:431–436.
Sanchez-Pinero, F., and G. A. Polis. 2000. Bottom-up dynamics of allochthonous input: Direct and indirect effects of seabirds on islands. Ecology.
Schinner, J. R., and D. L. Cauley. 1974. The ecology of urban raccoons in Cincinnati, Ohio. Pages 125–130 in J. H. Noyes and D. R. Progulske, editors. Wildlife in an Urbanizing Environment. Planning and Resource Development Series Number 28, Amherst, Massachusetts.
Schneider, D. G., L. D. Mech, and J. R. Tester. 1971. Movements of Female Raccoons and Their Young as Determined by Radio-Tracking. Animal Behaviour Monographs 4:1–43.
Schweitzer, S. H., A. G. Andersson, N. M. Jennings, T. Technician, W. Diversity, and C. M. Johnson. 2017. Status and Distribution of Colonial Waterbirds during the 2017 Nesting Season in Coastal North Carolina.
Seebacher, F. 2005. A review of thermoregulation and physiological performance in reptiles: What is the role of phenotypic flexibility? Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 175:453–461.
Sekercioglu, C. H. 2006. Increasing awareness of avian ecological function. Trends in Ecology and Evolution 21:464–471.
Siderelis, K. 1994. A Standard Classification System for the Mapping of Land Use and Land Cover. State of North Carolina.
Silliman, B. R., M. D. Bertness, A. H. Altieri, J. N. Griffin, M. C. Bazterrica, F. J. Hidalgo, C. M. Crain, and M. V. Reyna. 2011. Whole-community facilitation regulates biodiversity on patagonian rocky shores. PLoS ONE 6.
Slate, D. 1985. Movement, activity, and home range patterns among members of a high density suburban raccoon population. Rutgers University, New Brunswick.
Smith, C. R., F. C. De Leo, A. F. Bernardino, A. K. Sweetman, and P. M. Arbizu. 2008. Abyssal food limitation, ecosystem structure and climate change. Trends in Ecology and Evolution 23:518–528.
90
Smith, J. B., L. J. Laatsch, and J. C. Beasley. 2017. Spatial complexity of carcass location influences vertebrate scavenger efficiency and species composition. Scientific Reports 7:1–8.
Soots Jr., R. F., and J. F. Parnell. 1979. Inland Heronries of North Carolina. N.C. Sea Grant Publ. UNC-SG-78-10, Raleigh NC.:10–16.
Stachowicz, J. J. 2001. The Structure of Ecological Communities. BioScience 51:235–246.
Stachowicz, J. J. 2012. Niche expansion by positive interactions: realizing the fundamentals. A comment on Rodriguez-Cabal et al. Ideas in Ecology and Evolution 5:42–43.
Stapp, P., G. A. Polis, and F. Sânchez Pinero. 1999. Stable isotopes reveal strong marine and El Nino effects on island food webs. Nature 40:467–469.
Stenning, M. J. 1996. Hatching asynchrony, brood reduction and other rapidly reproducing hypotheses.
Stolen, E. D., J. A. Collazo, and H. F. Percival. 2007. Scale-Dependent Habitat Selection of Nesting Great Egrets and Snowy Egrets. Waterbirds 30:384–393.
Strong, A. M., R. J. Sawicki, and G. Thomasbancroft ’. 1991. Effects of predator presence on the nesting distribution of White-Crowned Pigeons in Florida Bay. Wilson Bull 103:415–425.
Subalusky, A. L., C. L. Dutton, E. J. Rosi, and D. M. Post. 2017. Annual mass drownings of the Serengeti wildebeest migration influence nutrient cycling and storage in the Mara River. Proceedings of the National Academy of Sciences 114:7647–7652.
Subalusky, A. L., and D. M. Post. 2019. Context dependency of animal resource subsidies. Biological Reviews 94:517–538.
Sutula, M., J. W. Day, J. Cable, and D. Rudnick. 2001. Hydrological and nutrient budgets of freshwater and estuarine wetlands of Taylor Slough in Southern Everglades, Florida (U.S.A.). Biogeochemistry.
Team, R. C. 2018. R: A Language and Environment for Statistical Computing.
Thompson, D. H. 1979. Feeding Areas of Great Blue Herons and Great Egrets Nesting within the Floodplain of the Upper Mississippi River. Proceedings of the Colonial Waterbird Group 2:202–213.
Tiner, R. W. 1984. Wetlands of the United States: current status and recent trends. U.S. Fish and Wildlife Service, Habitat Resources, Newton Corner, Massachusetts.
91
Tirado, R., and F. I. Pugnaire. 2005. Community structure and positive interactions in constraining environments. Oikos.
Traut, A. H., and M. E. Hostetler. 2004. Urban lakes and waterbirds: Effects of shoreline development on avian distribution. Landscape and Urban Planning 69:69–85.
Travaini, A., J. A. Donázarv, A. Rodríguez, O. Ceballos, M. Delibes, F. Hiraldo, A. Travaini, and M. Funes. 1998. Use of European hare (Lepus europaeus) carcasses by an avian scavenging assemblage in Patagonia. Journal of Zoology 246:175–181.
Tsai, J. S., B. E. Reichert, P. C. Frederick, and K. D. Meyer. 2016. Breeding Site Longevity and Site Characteristics Have Intrinsic Value for Predicting Persistence of Colonies of an Endangered Bird. Wetlands.
Uchida, H. 1986. Passerine birds nesting close to nests of birds of prey. Japanese Journal of Ornithology 35:25–31.
Vliet, K. A. 1989. Social Displays of the American Alliagtor (Alligator mississippiensis). American Zoologist 29:1019–1031.
Waddle, J. H., L. A. Brandt, B. M. Jeffery, and F. J. Mazzotti. 2015. Dry Years Decrease Abundance of American Alligators in the Florida Everglades. Wetlands 35:865–875.
Wallace, K. M., and A. J. Leslie. 2008. Diet of the Nile Crocodile (Crocodylus niloticus) in the Okavango Delta, Botswana. Journal of Herpetology 42:361–368.
Wallace, M. P., and S. A. Temple. 1987. Competative interactions within and between species in a guild of avian scavengers. The Auk 104:290–295.
White, C. L., P. C. Frederick, M. B. Main, and J. A. Rodgers Jr. 2005. Nesting island creation for water birds. University of Florida IFAS Extension:7.
Williams, A. J., A. E. Burger, and H. J. Lindeboom. 1978. The mineral and energy contributions of guano of selected species of birds to the Marion Island terrestrial ecosystem. South African Journal of Antarctic research 8:59–70.
Wilson, E. E., and E. M. Wolkovich. 2011. Scavenging: How carnivores and carrion structure communities. Trends in Ecology and Evolution 26:129–135.
Wittenberger, J. F., and J. Hunt, G. L. 1985. The adaptive significance of colonality in birds. Avian Biology 8:1–78.
van der Zee, E. M., M. J. A. Christianen, K. J. van der Reijden, J. van de Koppel, T. Piersma, H. Olff, T. van der Heide, M. van der Geest, J. A. van Gils, H. W. van der Veer, C. Angelini, L. L. Govers, A. H. Altieri, B. R. Silliman, and P. C. de Ruiter. 2016. How habitat-modifying organisms structure the food web of two coastal ecosystems. Proceedings of the Royal Society B: Biological Sciences 283.
92
BIOGRAPHICAL SKETCH
Wray Gabel was born and raised in Pittsford, a suburb of Rochester New York.
She graduated from Skidmore College with an honors degree in biology and a minor in
Studio Art in 2016. After her undergraduate career she bounced around doing different
field jobs exploring her interests—she worked in rural Japan with Rhinocerus Auklets, in
the San Francisco Bay with waterbirds, and in Maine with terns, before finally deciding
to pursue a master’s at the University of Florida in the Wildlife Ecology and
Conservation Department studying wading bird and alligator ecological interactions. She
completed her M.S. degree in December 2019.
Top Related