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

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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

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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).

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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

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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

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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

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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

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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.

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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.

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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

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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.

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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

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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).

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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

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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.

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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

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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.

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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).

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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

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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).

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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.

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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.

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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

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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

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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

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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)

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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

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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.