FOOD HABITS OF BREEDING BALD EAGLES (HALIAEETUS LEUCOCEPHALUS)

IN FLORIDA BAY, EVERGLADES NATIONAL PARK

by

Matthew R. Hanson

A Thesis Submitted to the Faculty of

The Charles E. Schmidt College of Science

in Partial Fulfillment of the Requirements for the Degree of

Master of Science

Florida Atlantic University

Boca Raton, Florida

December 2012

ACKNOWLEDGEMENTS

The FAU Environmental Sciences Program Everglades Fellowship provided financial support for this project during 2009-2011. The International Osprey Foundation

(TIOF) grant provided additional financial support. Florida Atlantic University granted me a teaching assistantship from 2011-2012.

I would like to thank my advisor Dr. John Baldwin for support, friendship, introducing me to Florida Bay, and for many hours on the water. My committee members, Dr. Nathan Dorn and Dr. Dale Gawlik gave exceptional guidance and feedback with my research. I also would like to thank Sonny Bass of Everglades National Park for providing his depth of knowledge on Bald Eagles and the south Florida ecosystem. Also from ENP, Mark Parry for many boat hours and navigation skills, and Lori Oberhofer for aerial surveys and many eagle notes. The Florida Museum of Natural History offered use of their fish and bird collections. Staff, including Irv Quitmyer, Thomas Webber, John

Kilmer, provided excellent knowledge for identification of my prey remains. Florida

Fish and Wildlife Research Institute (FWRI) were kind enough to collect and provide catfish for my measurements. Dave Shea was the original collector of prey remains and without him part of my thesis would not exist.

There are a lot of individuals that helped me with my thesis. I need to thank members of the Gawlik lab, Bryan Botson, Tyler Beck, Michelle Peterson, Rich Botta, and Jennifer Chastant for all their feedback and friendship. Brian Mealey provided

iii quality information on Florida Bay Bald Eagles and taught me how to band Bald Eagles.

I received field and office help from Jason Bosely, Christine Bedore, Tyler Beck, Joy

Young, Joe Welch, and Alexis Baron and thank them for their time and letting me show off Florida Bay and my research.

iv ABSTRACT

Author: Matthew Hanson

Title: Food habits of breeding Bald Eagles (Haliaeetus leucocephalus) in Florida Bay, Everglades National Park

Institution: Florida Atlantic University

Thesis Advisor: Dr. John D. Baldwin

Degree: Master of Science

Year: 2012

The population of Bald Eagles in Florida Bay, Everglades National Park has declined over the past few decades. It is hypothesized that changes in prey availabilities from alterations to ecosystem conditions have contributed to this decline. Our goals were to document diet and explore how prey availabilities may affect the Bald Eagle. For the

2009 and 2010 breeding seasons we collected prey remains from nest sites and video monitored provisioning of prey. Prey remains consisted of 33 species and were compositionally different than prey remains collected prior to ecological changes, suggesting changes in prey availabilities. Also, provisioning rates were significantly lower than Bald Eagles in other North American regions and declined throughout the breeding season. Our results suggest that prey availabilities has affected the food habits of breeding Bald Eagles in Florida Bay, which may be contributing to their decline.

v DEDICATION

This thesis is dedicated to my family, most importantly to my parents, Mary and

Dean, for all their love and support, and to my two great sisters.

FOOD HABITS OF BREEDING BALD EAGLES (HALIAEETUS LEUCOCEPHALUS)

IN FLORIDA BAY, EVERGLADES NATIONAL PARK

CHAPTER I ...... 1

CHANGES IN DIET OF AN APEX PREDATOR IN A SUBTROPICAL ESTUARY

FROM A 40-YEAR TIMESPAN

Introduction ...... 2

Methods...... 5

Analysis...... 6

Results ...... 8

Discussion ...... 9

TABLES ...... 17

FIGURES ...... 21

CHAPTER II ...... 27

PROVISIONING RATES SUGGEST FOOD-LIMITATION FOR BREEDING

BALD EAGLES (HALIAEETUS LEUCOCEPHALUS) IN THEIR

SOUTHERNMOST RANGE

Introduction ...... 28

Methods...... 30

vi Results ...... 33

Discussion ...... 34

TABLES ...... 44

FIGURES ...... 46

APPENDICES ...... 49

REFERENCES ...... 50

vii LIST OF TABLES

Table 1.1 List of species found in Bald Eagle prey remains from 1972/1973 and

2009/2010 in Florida Bay ...... 17

Table 1.2 Percent contribution of species in prey remains of Bald Eagle nest sites in

1972/1973 and 2009/2010 for all nest sites, nest sites located in west

Florida Bay, and for nest sites in which collections where made in both

time periods ...... 18

Table 2.1 Number and percent contribution of prey deliveries to four Bald Eagle

nests during the 2009 and 2010 breeding seasons in Florida Bay ...... 44

Table 2.2 Breeding season provisioning rates of four Bald Eagle nests during the

2009 and 2010 breeding seasons in Florida Bay ...... 45

Table 2.3 Provisioning rates at Bald Eagle nest sites reported from various areas in

its range ...... 45

viii LIST OF FIGURES

Figure 1.1 Map of Florida Bay, Florida with locations of prey remains collections

from 1972/1973 and 2009/2010 ...... 21

Figure 1.2 Picture of a Hardhead Catfish (Arius felis) skull with arrows indicating

where length measurements were taken ...... 22

Figure 1.3 Linear relationship of skull length and fork length for Hardhead Catfish

(Arius felis) collected in Florida in 2011 ...... 22

Figure 1.4 Mean skull length of all individual Hardhead Catfish skulls collected

from Bald Eagle nest sites in Florida Bay, Florida from 1972/1973 and

2009/2010, and mean biomass of all individual fish estimated from

regressions ...... 23

Figure 1.5 Three-dimensional scaling of prey remains compositions between

1972/1973 and 2009/2010 in Florida Bay for all nest sites ...... 24

Figure 1.6 Rarefaction curves of species richness per number of collections from

Bald Eagle nest sites from 1972/1973 and 2009/2010 in Florida Bay,

Florida ...... 25

Figure 1.7 Rarefaction curves of species richness per MNI from Bald Eagle nest

sites from 1972/1973 and 2009/2010 in Florida Bay, Florida ...... 26

Figure 2.1 Linear regression of the mean daily provisioning rate averaged per week

for four Bald Eagle nests during the 2009 and 2010 breeding seasons in

ix Florida Bay ...... 46

Figure 2.2 Linear regression of the mean daily total biomass for one Bald Eagle nest

during the 2009 breeding season in Florida Bay ...... 47

Figure 2.3 Number of deliveries per hour after sunrise for four Bald Eagle nests

during the 2009 and 2010 breeding seasons in Florida Bay ...... 48

x CHAPTER I

CHANGES IN DIET OF AN APEX PREDATOR IN A SUBTROPICAL ESTUARY

FROM A 40-YEAR TIMESPAN

ABSTRACT: Beginning in the late 1980s, Florida Bay underwent dramatic ecological changes due to altered freshwater inflows from the Everglades. At the same time, the local Bald Eagle population began to decline and has continued ever since. We documented food habits of the struggling Bald Eagle population to look into the hypothesis that food is the limiting factor to their success. We collected prey remains from nest sites at the end of the breeding season, and compared these to historical data from the 1970s. 571 individual prey remains (30 species) from 34 collections at 21 nest sites were collected in 1973-74, and 419 remains (22 species) from 13 collections at 11 nest sites were collected in 2010-11. We found remains consisted of 81% fish and 16% birds in the 1973-74 and 77% fish and 21% birds in 2010-11. Hardhead Catfish (Arius felis) made up the majority of prey remains in both time periods. The overall compositions of prey remains significantly changed between these time periods. Mullet,

Jack, Double-crested Cormorant, Red-breasted Merganser, and Hardhead Catfish where the species that added most to the dissimilarities between time periods. Skulls of the

Hardhead Catfish, the most common prey part, significantly declined in overall length by

1 >10% between periods. This results in a >35% decrease in biomass of catfish delivered to eagle nests. These results help support the hypothesis that Bald Eagle diet has changed due to altered prey availability and that it may be limiting this population.

INTRODUCTION

Ecosystem conditions influence the composition, abundance, and distribution of prey communities and affect their vulnerability to predation (Orth et al. 1984, May and

Norton 1996, Schneider 2001, Schmidt and Ostfeld 2003). These conditions, which regulate the availability of prey, influence a predator’s food habits (Estabrook and

Dunham 1976, Davies 1977, Bence and Murdoch 1986, Fryxell and Lundberg 1994).

The dietary makeup of top predators, such as raptors, is highly flexible and dependent on local conditions (Preston 1990, Beier and Drennan 1997, Poole et al. 2002, Preston and

Beane 2009). Raptors, both generalist and specialist, show dietary diversity within their range corresponding with varying prey availability (Sonerud 1986, Elliott et al. 2011).

The wide-ranging generalist Red-tailed Hawk (Buteo jamaicensis), for example, preys on hares, jackrabbits, and ground squirrels more often in the more western portion of its range and voles, mice, rats, and cottontails in the eastern part (Preston and Beane 2009).

The circumglobal osprey (Pandion haliaetus), while exhibiting a more specialized feeding strategy consisting almost exclusively of fish, is comprised of a wide diversity of different fish species dependent on local availability (Poole et al. 2002).

The Bald Eagle (Haliaeetus leucocephalus) is an opportunistic and generalist predator capable of feeding on a variety of prey types and their short term diet reflects the local abundance of most available prey items (Buehler 2000). This foraging strategy has

2 assisted Bald Eagles in exploiting a diversity of prey and habitats with high regional diversity (Todd et al. 1982, Collins et al. 2005, Bryan et al. 2005, Markham and Watts

2008a). Diversity in eagle diet can also vary within a region due to differences in available prey at the microhabitat level (Elliott et al. 2005) and can vary at the same physical location if or when prey availability changes over time (Collins et al. 2005,

Anthony et al. 2008, Newsome et al. 2010).

A variety of methods have been used to assess the dietary selection of Bald Eagles and other raptors, which have served as proxy measures of local prey availability. Direct observations and video monitoring methods offer an accurate representation of true diet

(Lewis et al. 2004, Marti et al. 2007). However, they require large amounts of time and are generally more involved than another method of collection of prey remains. The use of prey remains has been well established as a valuable and informative proxy for raptor diet in a number of species (Mollhagen et al. 1972, Steenhof and Kochert 1988,

Bosakowski and Smith 1992, Hunt et al. 2002). Although it is recognized the method of prey remain collections can over represent larger and heavier-boned species, such as large birds and mammals, this procedure has merit if these biases are taken into consideration (Simmons et al. 1991, Redpath et al. 2001, Marti et al. 2007). For these reasons, collecting prey remains serves as a valid and well-supported method to examine raptor diets and has been used to monitor changes in prey selection and availability in local environments.

Bald Eagles, one of the most wide-ranging species in North America, breed as far north as the arctic and as far south as Arizona, Texas, and Florida. Located at the southern tip of Florida, the Florida Bay estuary represents Bald Eagles’ southernmost

3 breeding range. While this subtropical mangrove-dominated ecosystem has been protected as part of Everglades National Park for over sixty years, ecological changes have modified this environment, with a tipping point in the late 1980s-early 1990s. In the late 1980s, Florida Bay went through drastic ecological changes believed to be in part from alterations to the amount and distribution of water flow from Florida Bay’s freshwater source, the Everglades (Fourqurean and Robblee 1999). In the years proceeding these changes, water quality measures, including salinity, nutrients, and oxygen, uncharacteristically and severely shifted from previous levels (Fourqurean and

Robblee 1999). Although not completely understood, believed consequences of these changes in water quality were massive die-offs and redistributions of the seagrass that makes up much of the habitat in Florida bay (Zieman et al. 1988, Robblee et al. 1991,

Hall et al. 1999). Loss of this habitat aided the release of sediments into the water, causing algal blooms and increased turbidity (Phlips et al. 1993, Boyer et al. 1999).

Blooms and turbidity were stronger and covered larger areas of Florida Bay during the winter months (Butler IV et al. 1995, Boyer et al. 1999), which is the time that Bald

Eagles are breeding in Florida Bay.

The ecological transitions that have occurred in the Florida Bay estuary are hypothesized to have resulted in changes to the types, size, and availability of prey presented to Bald Eagles during the breeding season and these alterations in prey availability may be influencing the decreasing trend seen in reproductive effort (Baldwin et al. 2012). To examine the potential effects of environmental changes in Florida Bay on breeding Bald Eagle diet, we analyzed prey remains from Bald Eagle nest sites prior to these ecological changes (1972 & 1973 breeding seasons) and post changes (2009 &

4 2010 breeding seasons). We predict that composition of prey remains should be similar between these time periods if environmental changes have had no effect on availability of prey to breeding Bald Eagles.

METHODS

Prey remains were collected at nest sites that were both accessible and occupied by breeding Bald Eagles in each breeding season. Collections were made at seven nest sites in the 2009-2010 breeding season (hereafter 2009) and six in 2010-2011 (hereafter

2010) for a total of 13 collections from 11 nest sites (Fig 1). All remains were collected after the breeding season had ended to replicate methods employed for the 1972-1973

(hereafter 1972) and 1973-1974 (hereafter 1973) breeding seasons (Robertson Jr and

Shea 1975). Nineteen collections were made for 1972 and 15 for 1973, accounting for a total of 34 collections from 21 nest sites (Fig 1). The lesser amount of collections from less nest sites in 2009/2010 can mostly be attributed to a reduced breeding population in

Florida Bay. Nonetheless, the location of the majority of prey remains collected in

2009/2010 overlapped the majority of collections in 1972/1973. The breeding season was considered to have ended when all young had fledged and were no longer obtaining prey at the nest. All prey parts were removed from the nest and returned to the lab for analysis. Remains were separated first by class (avian, fish, reptile, mammal, other) and then separated by unique prey part (e.g. avian skull, feathers, fish skull). Once separated, parts were grouped into the lowest distinguishable taxonomic level. Most parts were distinguished to species or group level by comparison to museum specimens at the

Florida Museum of Natural History, Gainesville, Florida, USA. The minimum number of

5 individuals (MNI) for each species was determined by using the greatest number of a matching prey part.

ANALYSIS

Prey remains were quantified as the MNI for each nest site and each taxonomic category. Composition of remains from all nest sites made in 2009/2010 was compared to the composition of remains collected in 1972/1973. To control for regional variation in prey availability, we compared collections in both time periods from nest sites that reside only in western Florida Bay, where the majority of the remaining active nest are located. To further control for spatial variation, we also compared prey remains from nest sites in which collections were made at least once in each time period.

Species contribution to the overall composition of prey remains was calculated by the MNI for a given species divided by the MNI of all prey remains. To demonstrate any differences in prey composition between collection years, a non-metric multidimensional scaling (MDS) ordination technique was used. Sample units were prey remains composition per nest site and collection year. A 3D plot was examined because the stress level of the 2D plot was quite high.

To test for differences in prey remains composition between collection years, we used an ANOSIM (analysis of similarities), a multiple permutation procedure. To reduce the effects of prey remains that were undistinguishable beyond class level we removed them from analyses (2.7% of all remains). For some species with similar physical features, remains at times were only distinguishable to a species group (e.g. small Egretta spp.). In this case, we divided these remains evenly between the few possible species.

6 Sample units were standardized by sample total because the number of prey remains varied between samples. This variation was not due to foraging ecology of the eagles, but to habitat characteristics of and below the nest. Sample units were then log(x+1) transformed because compositions were variable from sample-to-sample and consisted of many rare species. Test statistic R was calculated and compared to the distribution created from multiple random permutations. If R is or is close to 1 or -1, than all within samples are more similar than among samples, and if R is close to 0, then similarities among and within samples are the same on average. Significance of this test was determined if the observed R-value of prey composition does not fall within the 95th percentile of the random distribution of R-values, which are calculated using multiple permutations. PRIMER-E Ltd was used to perform the MDS and ANOSIM procedures

(Clarke and Warwick 2001). Overall diversity was calculated for both time periods using

Simpson’s index and a randomization test on the Simpsons indices was used to test for a significant difference between them. Rarefaction curves were used to illustrate how species richness was influenced by the number of collections and MNI (# of prey remains).

Hardhead Catfish (Arius felis) are a prey species commonly recovered intact at eagle nest sites in Florida Bay (93% of nests, 55% of all remains). Catfish skulls were measured from the anterior end of the skull at the dermathoid bone to the posterior end of the supraoccipital bone in both 1972/1973 and 2009/2010 (Fig. 2). An ANOVA was used to test if mean length of skulls were different between time periods. Using

Hardhead Catfish collected in 2011, we extrapolated fork length from skull length using a linear model. Using predicted fork length from the linear model, we then estimated

7 biomass of individual fish using a known fork length-to-biomass conversion (wet biomass (grams) = 7.189x106(fork length)3.116, Armstrong et al. 1996). Mean estimated biomasses for each time period were compared using an ANOVA.

RESULTS

The total MNIs of prey remains collected were 571 in 1972/1973 and 491 in

2009/2010. The remains in 1972/1973 accounted for 30 species, of which 17 were avian,

10 fish, and 3 other (1 mammal, 1 reptile, and 1 crustacean; Table 1). In 2009/2010 there were 33 total species, of which 20 were bird, 10 fish, and 3 other (1 mammal, 1 reptile, and 1 crustacean; Table 1). The most common species in the prey remains in both time periods was the Hardhead Catfish (Table 2). Hardhead Catfish made up 67.7% of fish remains and 54.6% of all remains in 1972/1973 and 77.1% of fish remains and 53.6% of all remains in 2009/2010. The mean total length of hardhead catfish skulls was 10% greater in the early period than in the later period (p<0.0001, Fig 4). Skull length was highly correlated with fork length (Fig 3) and therefore biomass per nest in the early period was 35.7% greater (p<0.0001) as well (Fig 4).

Analysis of Similarities (ANOSIM) showed prey remain compositions were significantly different between 1972/1973 and 2009/2010 (r-value=0.171, p=0.024).

There was also a significant difference when comparing only nest sites from west Florida

Bay (r-value=0.192, p=0.019) and nest sites in which collections were made during both time periods (r-value=0.238, p=0.007). The Similarity Percentages (SIMPER) method showed that mullet (Mugilidae), jack (Caragnidae), Double-crested Cormorant

(Phalacrocorax auritus), Red-breasted Merganser (Mergus serrator), and Hardhead

8 Catfish were the species that contributed most to dissimilarities between time periods in each comparison (Table 3). In general there was a shift to more Hardhead Catfish, mullet, and Double-crested Cormorant and less jack, and Red-breasted Merganser in the later period. The 3 most common fish in 1972/1973 were jack, mullet, and mojarra

(Gerreidae), in order of rank, and mullet, jack, and Ladyfish (Elops saurus) in

2009/2010. Jack decreased by 6% (7% for fish), mullet increased by 0.5%, (2% for fish) and mojarra and Ladyfish were never present in the opposite time period than they were found. The top four common avian species in 1972/1973 were Red-breasted Merganser,

Horned Grebe (Podiceps auritus), Tricolored Heron (Egretta tricolor), and Laughing

Gull (Larus atricilla) and in 2009/2010 were Double-crested Cormorant, Great Blue

Heron (Ardea herodias), Great Egret (Ardea alba), and White Ibis (Eudocimus albus).

Multi-dimensional scaling demonstrated the compositional differences between time periods (Fig 5). There was no difference in overall diversity between the two collecting periods using Simpson’s Index (1-D) (1972/1973=0.65, 2009/2010=0.69, p=0.296).

Rarefaction illustrated that while there was no difference in overall diversity between time periods, 2009/2010 would have a higher number of species present for fewer collections and a lower MNI (Figs 6 and 7).

DISCUSSION

Collecting prey remains is a useful tool to examine diets of birds and how diets change over time in response to environmental conditions. This method has successfully been used with a number of raptors (Steenhof and Kochert 1985, 1988), including the

Bald Eagle. Anthony et al. (2008) witnessed significant differences in Bald Eagle prey

9 remains collected from before and after local ecosystem changes in the Aleutian

Archipelago, Alaska. Decline of kelp forests, the characteristic habitat type, and kelp- related species both directly and indirectly affected prey communities and were suggested as likely causes for the shifts in eagle diet. Also, prey remains excavated from historic

Bald Eagle nest sites in the Channel Islands, California were used to look at shifts in Bald

Eagle diets over 70-160 years (Collins et al. 2005, Erlandson et al. 2007). These Channel

Islands diets correlated with increases and decreases in availability of multiple prey types in the altered environment, especially when ungulate species were introduced (Newsome et al. 2010), demonstrating the usefulness of analysis of prey remains in examining changes in prey availability.

Range wide, the highest prey contribution typically comes from fish (Dunstan and

Harper 1975, McEwan and Hirth 1980, Haywood and Ohmart 1986, Thompson et al.

2005). Consistent with this, fish contributed the majority to prey remains collected from

Florida Bay from 1972/1973 and 2009/2010 (80.7 and 69.5%, respectively). Birds were second (15.8 and 29.1%) and other classes (reptiles, mammals, crustaceans) made a small contribution (3.5 and 1.4%). In some regions of North America, mammal prey remains have contributed more to eagle diet (Stalmaster 1987, Dominguez et al. 2003, Anthony et al. 2008), however mammals are not abundant on the keys of the Florida Bay estuary.

There was a significant change in the overall composition of Bald Eagle prey remains from 1972/1973 to 2009/2010 in Florida Bay. We assume eagles have not changed their basic foraging strategy between these two time periods and the change in diet likely indicates a change in prey availability. This observed change was significant in all spatial contrasts, suggesting there was no nest site bias. In addition, because we

10 compared within time period composition differences vs. among time periods in

ANOSIM, the change was likely not a function of inter-annual fluctuations in prey availability.

Changes in prey availability to a predator are determined by prey abundance, distribution, and vulnerability. For specialist predators that feed on only one species, these parameters are important to that predator for only that one prey species, while for generalist and opportunistic predators, these parameters apply to a suite of species. In this study, we were able to determine changes in prey availability to eagles by quantifying changes in their diet reflected by changes in a multitude of species’ contributions to the diet. These changes represent a shift in the prey assemblages of the

Florida Bay estuary. Ecosystem changes have the ability to affect prey availabilities to a predator (Reid and Croxall 2001, Diamond and Devlin 2003), and suggests that the ecological changes of Florida bay have affected both the fish and bird communities in such ways that affected their availability to Bald Eagle predation.

These changes, including alterations to water quality and submerged vegetative habitat (Zieman et al. 1988, Robblee et al. 1991), are known to have negatively altered some fish populations. Fish communities are dependent on the seagrass and microhabitats that characterize Florida Bay (Sogard et al. 1989) and these communities have changed at locations that were affected by ecological changes that occurred between our sampling periods (Matheson, Jr. et al. 1999). For instance, mullet populations, a common prey item, are associated with varying salinity levels in Florida Bay (Sogard et al. 1989). High salinities can affect the metabolic rate, reproduction, and survival of

Mugil cephalus, one of the Florida Bay mullet species (DeSilva and Perera 1976, Lee and

11 Menu 1981, Cardona 2000). Consistent with this, mullet, the second most common fish was the species that added most of the dissimilarity to overall compositions. Jack, the third most common fish, also added much of the difference between sampling periods, even though their overall contributions did not shift dramatically. Also, the distribution, egg survival, and growth of Spotted Seatrout (Cynoscion nebulosus), the fifth most abundant fish species in both time periods, vary with salinity levels and seagrass (Thayer et al. 1999, Powell 2003, Neahr et al. 2010). Although we did not see a significant change in the contribution of this species between sampling periods, it serves as an example of how fish communities have been, and may be affected by these ecological changes.

Unique to prey remains of both time periods is majority contribution of one species, the Hardhead Catfish. This strictly marine species is found in southern coastal waters of the Gulf of Mexico and the Atlantic coast. They are normally found in a few feet of water and in a variety of substrate types, but common to seagrass habitats typical of Florida Bay and southern coastal ecosystems. The high contribution of Hardhead

Catfish does not necessarily mean that Bald Eagles have strong preference for this fish or that they are the most available prey type in Florida Bay. It has been previously documented that certain individual species and species types may be over or under represented in prey remains. Hardhead Catfish may be overrepresented in prey remains due to the fact its skull is relatively large and dense which seems to persist far longer than other prey parts. However, the contribution of catfish to fish remains increased by nearly

10% from 1972/1973 to 2009/2010 at all nest sites and by 16% for nest sites in which remains were collected in both time periods. This could be attributed to an increase in

12 available catfish in Florida Bay, but also representative of a decrease of other available fish. The Hardhead Catfish, as with other catfish, can handle changes and degradation in their environment more adequately than other fish. Sogard (1989) was able to show that

Hardhead Catfish distributions in Florida Bay were associated with salinity level and that their populations were not negatively affected by extreme salinities.

Although there is no indication that the population of catfish has decreased, it appears that the size structure has changed with changes in the bay. Comparing the lengths of catfish skulls found at eagle nest sites showed a >10% decrease between the two time periods. Skeletal structures of fish have been previously used to document changes in growth characteristics of fish populations over long periods of time previously. For example, four hundred-year-old Atlantic Sturgeon (Acipenser oxyrinchus oxyrinchus) spines were compared to modern day spines, showing that the older population consisted of larger and older individuals, possibly altered by overharvesting and temperature changes (Balazik et al. 2010). Assuming eagles have not changed their preference towards smaller catfish in their diet, this suggests that there has indeed been change in the size structure of Catfish in Florida Bay. The decrease in skull length of catfish, which is correlated to fork length, could be a sign of a change in the age structure

(less older individuals), size (slower growth rate) structure of this population, and/or a stunted population. The estimated decrease in biomass (26%) of these catfish shows that this decrease in size could play a role in particularly the amount of available biomass per foraging trip for the eagles, especially if their actual contribution is near 54% as reported in prey remains. Of the documented changes to water characteristics in Florida Bay, varying salinity level, oxygen level, and temperatures have all been shown to affect the

13 growth and survival of many catfish species and may be a reason for this decrease

(Kilambi et al. 1970, Buentello et al. 2000, Bringolf et al. 2005, Copatti et al. 2011).

In addition to changes in fish communities of Florida Bay, bird communities were also affected by ecological changes. Large predatory bird populations in Florida Bay have varied in abundance and distribution over time (Powell et al. 1989). For instance, the nesting population of Roseate Spoonbills (Ajaia ajaja) in Florida Bay has decreased in size between our sampling periods, of which has been attributed to hydrologic conditions and salinity (Lorenz et al. 2009). While we were not able to connect these changes to prey availability of Bald Eagles, we did see significant changes in the contributions of prey remains for many bird species. Most significant of these changes was a shift from the Red-breasted Merganser as the most abundant avian remain in

1972/1973 (35.6%) to making up only 4% of avian remains in 2009/2010. In contrast, the Double-crested Cormorant made up only 4% of avian remains in 1972/1973 and then became the most abundant avian remain in 2009/2010 (32.9%). These two species add the third and fourth most to the dissimilarities of prey remain compositions between sampling periods. It has not been documented how these species have responded to ecological changes in Florida Bay, but they have some differences in foraging behavior and habitat use. Mergansers are relatively more of a prey and habitat specialist. In other regions, they prey on a smaller size-range of fish (Titman 1999) and choose seagrass habitats over sand substrates, which have declined and shifted in Florida Bay between our sampling periods. These factors could have altered their abundance and distributions and in turn their availability to eagles. Double-crested Cormorants prey on a larger size-range of fish and are characterized as opportunistic and flexible in their foraging habitat (Hatch

14 and Weseloh 1999) and prey selection (Hobson et al. 1989, Blackwell et al. 1995).

Hobson (1989) even suggested that an increase in the cormorant population size on Lake

Winnipegosis, Manitoba was due to an increase in the abundance of certain prey species that was a result of a reduction in a larger predatory fish. Double-crested Cormorants in

Florida Bay may be able to more adequately deal with and possibly evade limitation due to ecosystem changes. This may have lead to an increase in their availability and/or be attributed to a decrease in availability of other species. Also unlike the cormorant, the

Red-breasted Merganser is migratory, making the breeding population of concern to the size of this wintering population in Florida Bay. There is indication that the overall size of the breeding population has increased over the past 20 years, further suggesting this fluctuation is unique to Florida Bay (Titman 1999).

Detailed population monitoring of bird populations in Florida Bay is limited to a few number of species, and data are sporadic during the first sampling period (72/73).

Therefore we used the Christmas Bird Count as a tool to compare trends in the occurrence of prey remains to surveyed populations. Unfortunately, the Florida Bay survey route (FL04) has only been surveyed once (1940). We decided to use the two closest routes to Florida Bay, being Coot Bay (FLCE) and Key Largo (FLKL), and look at the top five birds contributing to the dissimilarities. Only three of the five had similar trends (decreasing or increasing in occurrence) between the CBC and prey remains from the first sampling period to the next. Double-crested Cormorant increased 1.5x in the

CBC, but 6.5x in prey remains. Tricolored Heron decreased 7% in the CBC, but decreased 70% in prey remains. Showing a trend of the most similar magnitude, Red- breasted Merganser decreased 6% in the CBC, and decreased 30% in remains. These

15 help suggest that the changes in the contributions of prey remains, which we believe is a result of changes in the prey assemblages of Florida Bay, is indeed unique to this local environment and not a wider-spread event.

We were able to find evidence for changes in the diet of a top-level predator in

Florida Bay, which we suggest is result of ecological changes. While a change in diet does not necessarily result in harm to an individual or population, especially for opportunistic species that are capable of exploiting a wide range of prey, it certainly has the potential for a negative impact on reproductive success and life histories (Penteriani et al. 2002, Rutz and Bijlsma 2006). Baldwin et al. (2012) reported a decrease in population size and occupancy rates that coincides with the change of eagle diet in our study. It is unknown if changes in diet have caused these demographic changes, but is a reason for concern. The relationship of population size, structure, and reproduction to diet and prey availability warrants further investigation. Historical comparisons of predator diet has offered us an increased understanding of not only the changing food habits of Bald Eagles in Florida Bay, but also how it has responded to changes in this unique environment.

16 TABLES

Table 1.1 List of species found in Bald Eagle prey remains from 1972/1973 and

2009/2010 in Florida Bay.

1972/ 2009/ 1972/ 2009/ 1973 2010 1973 2010 Fish Birds Hardhead Catfish X X Laughing Gull X X Great Barracuda X X Great Blue Heron X X Mullet (Unknown) X X Great Egret X X Spotted Seatrout X X Horned Grebe X X Crevalle Jack X X Red-breasted Merganser X X Needlefish (Unknown) X X Little Blue Heron X X Filefish (Unknown) X Tricolored Heron X X Sheepshead X Roseate Spoonbill X X Burrfish (Unknown) X Double-crested Cormorant X X Striped Mojarra X Reddish Egret X X Red Drum X Royal Tern X X Ladyfish X American Coot X X Snapper (Unknown) X Pied-billed Grebe X Oyster Toadfish X Scaup (Unknown) X Black-necked Stilt X Fulvous Whistling Duck X Brown Pelican X Wood Stork X Other White Ibis X Diamondback Terrapin X X Yellow-crowned Night-Heron X Rat (Unknown) X X Red-shouldered Hawk X Fiddler Crab (Unknown) X X American White Pelican X Osprey X Ring-billed Gull X American Crow X

17 Table 1.2 Percent contribution of species in prey remains of Bald Eagle nest sites in

1972/1973 and 2009/2010 for all nest sites, nest sites located in west Florida Bay, and for nest sites in which collections where made in both time periods. Symbol “-“ indicates 0.

All Nest Sites West Florida Bay Nest Sites Nest Sites In Both Periods

1972/1973 2009/2010 1972/1973 2009/2010 1972/1973 2009/2010

% % % % % % Prey Species N Total N Total N Total N Total N Total N Total Fish Hardhead Catfish 312 54.6 263 53.6 227 56.2 257 56.1 101 54.0 248 57.9 Jack (Multiple/unknown) 62 10.9 22 4.5 46 11.4 19 4.1 30 16.0 18 4.2 Mullet (Multiple/unknown) 26 4.6 25 5.1 20 5.0 23 5.0 10 5.3 23 5.4 Mojarra (Multiple/unknown) 19 3.3 - - 11 2.7 - - 7 3.7 - - Seatrout (Multiple/unknown) 11 1.9 8 1.6 10 2.5 6 1.3 5 2.7 5 1.2 Red Drum - - 4 0.8 - - 4 0.9 - - 4 0.9 Needlefish (Unknown) 6 1.1 2 0.4 4 1.0 1 0.2 2 1.1 - - Ladyfish - - 11 2.2 - - 9 2.0 - - 9 2.1 Great Barracuda 3 0.5 2 0.4 2 0.5 2 0.4 - - 2 0.5 Porgies (Unknown) 8 1.4 - - 5 1.2 - - 1 0.5 - - Snapper (Multiple/unknown) - - 2 0.4 - - 2 0.4 - - 2 0.5 Oyster Toadfish - - 2 0.4 - - 2 0.4 - - 2 0.5 Filefish (Unknown) 1 0.2 ------Burrfish (Unknown) 1 0.2 ------Unknown Fish 12 2.1 - - 8 2.0 - - 4 2.1 - -

Subtotal 461 80.7 341 69.5 333 82.4 325 71.0 160 85.6 313 73.1

Avian Red-breasted Merganser 32 5.6 6 1.2 18 4.5 3 0.7 12 6.4 2 0.5 Horned Grebe 10 1.8 5 1.0 4 1.0 3 0.7 1 0.5 3 0.7 White Ibis - - 8 1.6 - - 8 1.7 - - 8 1.9 Tricolored Heron 9 1.6 4 0.8 4 1.0 3 0.7 2 1.1 3 0.7 Laughing Gull 6 1.1 1 0.2 3 0.7 1 0.2 1 0.5 1 0.2 Double-crested Cormorant 4 0.7 47 9.6 4 1.0 44 9.6 1 0.5 36 8.4 Great Egret 1 0.2 14 2.9 - - 14 3.1 - - 13 3.0 Roseate Spoonbill 3 0.5 6 1.2 - - 6 1.3 - - 5 1.2 American Coot 2 0.4 3 0.6 1 0.2 3 0.7 1 0.5 2 0.5 Scaup (Unknown) 2 0.4 - - 2 0.5 - - 1 0.5 - - Black-Necked Stilt 2 0.4 - - 1 0.2 ------Brown Pelican 2 0.4 - - 2 0.5 ------Great White Heron 1 0.2 - - 1 0.2 - - 1 0.5 - - Pied-Billed Grebe 1 0.2 - - 1 0.2 - - 1 0.5 - - Reddish Egret 1 0.2 5 1.0 - - 5 1.1 - - 5 1.2 Little Blue Heron 1 0.2 1 0.2 - - 1 0.2 - - 1 0.2 Fulvous Whistling- Duck 1 0.2 - - 1 0.2 ------

18 Royal Tern 1 0.2 3 0.6 1 0.2 3 0.7 - - 1 0.2 Grebe (Unknown) - - 4 0.8 - - 2 0.4 - - 2 0.5 Wood Stork - - 1 0.2 - - 1 0.2 - - 1 0.2 Great Blue Heron - - 14 2.9 - - 14 3.1 - - 13 3.0 American Crow - - 1 0.2 - - 1 0.2 - - 1 0.2 Gull (Unknown) - - 2 0.4 - - 1 0.2 - - 1 0.2 Night Heron (Unknown) - - 4 0.8 - - 3 0.7 - - 3 0.7 American White Pelican - - 1 0.2 - - 1 0.2 - - - - Ring-billed Gull - - 4 0.8 - - 3 0.7 - - 3 0.7 Osprey - - 1 0.2 - - 1 0.2 - - 1 0.2 Red-shouldered Hawk - - 1 0.2 - - 1 0.2 - - 1 0.2 Unknown Wading Bird 4 0.7 3 0.6 4 1.0 3 0.7 1 0.5 3 0.7 Unknown Bird 7 1.2 4 0.8 6 1.5 3 0.7 3 1.6 3 0.7 Subtotal 90 15.8 143 29.1 53 13.1 128 27.9 25 13.4 112 26.2

Other Diamondback Terrapin 17 3.0 5 1.0 15 3.7 3 0.7 1 0.5 1 0.2 Fiddler Crab (Unknown) 2 0.4 1 0.2 2 0.5 1 0.2 - - 1 0.2 Rat (Unknown) 1 0.2 1 0.2 1 0.2 1 0.2 1 0.5 1 0.2 Subtotal 20 3.5 7 1.4 18 4.5 5 1.1 2 1.1 3 0.7

Total 571 491 404 458 187 428

19 Table 1.3 Percent contribution to dissimilarities between compositions of prey remains between 1972/1973 and 2009/2010 for all nest sites.

Average Contribution +/- Change In

Dissimilarity % Contribution Mullet 5.72 9.57 + Jack 5.31 8.88 _ Double-crested Cormorant 4.4 7.37 + Red-breasted Merganser 4.09 6.85 _ Hardhead Catfish 3.1 5.19 + Seatrout 2.9 4.86 _ Horned Grebe 2.86 4.78 _ Diamondback Terrapin 2.8 4.69 _ Mojarra 2.18 3.65 _ Tricolored Heron 1.88 3.14 _ Great Blue Heron 1.76 2.95 + Roseate Spoonbill 1.71 2.87 + Needlefish 1.61 2.69 _ Ladyfish 1.57 2.63 + Great Egret 1.5 2.51 + American Coot 1.46 2.44 + Ring-billed Gull 1.4 2.35 + Royal Tern 1.36 2.27 + Porgies 1.24 2.08 _ Pied-billed Grebe 1.18 1.98 _ Redfish 1.07 1.79 + Barracuda 1.02 1.7 _ Laughing Gull 0.98 1.4 _ Yellow-crowned Night-Heron 0.66 1.11 +

20 FIGURES

= 2009/2010 = 1972/1973

Figure 1.1 Map of Florida Bay, Florida with locations of prey remains collections from

1972/1973 and 2009/2010.

21

Figure 1.2 Picture of a Hardhead Catfish (Arius felis) skull with arrows indicating where length measurements were taken.

Figure 1.3 Linear relationship of skull length and fork length for Hardhead Catfish

(Arius felis) collected in Florida in 2011 (n = 24).

22

Figure 1.4 Mean skull length (mm) of all individual Hardhead Catfish skulls collected from Bald Eagle nest sites in Florida Bay, Florida from 1972/1973 (n = 145) and

2009/2010 (n = 153), and mean biomass (g) of all individual fish estimated from regressions. Error bars represent 1 standard error.

23 All Nest Sites

= 2009/2010 3D Stress: 0.14 =1972/1973

Figure 1.5 Three-dimensional scaling of prey remains compositions between 1972/1973 and 2009/2010 in Florida Bay for all nest sites.

24 2009/2010

1972/1973

Figure 1.6 Rarefaction curves (solid lines) of species richness per number of collections

(samples) from Bald Eagle nest sites from 1972/1973 and 2009/2010 in Florida Bay,

Florida. With 95% +/- confidence intervals (dashed lines).

25 2009/2010

1972/1973

Figure 1.7 Rarefaction curves (solid lines) of species richness per MNI (number of prey remains collected) from Bald Eagle nest sites from 1972/1973 and 2009/2010 in Florida

Bay, Florida. With 95% +/- confidence intervals (dashed lines).

26 CHAPTER II

PROVISIONING RATES SUGGEST FOOD-LIMITATION FOR BREEDING BALD

EAGLES (HALIAEETUS LEUCOCEPHALUS) IN THEIR SOUTHERNMOST RANGE

ABSTRACT: Beginning in the late 1980s, Florida Bay underwent dramatic ecological changes due to altered freshwater inflows from the Everglades. At the same time, the local Bald Eagle population began to decline and has continued ever since. We documented diet and provisioning rates of eagles to look into the hypothesis that food is a limiting factor to their success. We monitored four nests with video cameras in the

2009/2010 (2009) and 2010/2011 (2010) breeding seasons. A total of 546 prey deliveries were recorded, with 93% determined to class and 46% determined to family. Fish contributed 86.1% of all deliveries, birds made up 7%, and undeterminable made up 7%.

The mean daily provisioning rates for all nest sites combined were 1.75 deliveries/young/day and 2.64 deliveries/day and significantly declined throughout the breeding season. The rates are strikingly smaller than other stable Bald Eagle populations from across its range and compares to the rates of another struggling population. The total biomass of prey deliveries/young/day also declined throughout the breeding season (one nest only). Deliveries were mostly frequently made to the nest during 3-5 hours after sunrise and then again at a less frequent rate 9-12 hours after

27 sunrise and did not vary between nests or change throughout the breeding season. These results suggest that the Bald Eagle population in Florida Bay is experiencing inadequate prey availability, and this may be contributing to their decline.

INTRODUCTION

Inadequate availability of prey can led to changes in diet and food limitation in a many predators (Shine and Madsen 1997, Ford et al. 2010). Raptors, both generalist and specialist foragers, are top-level predators in nearly all ecosystems and their life history traits, population sizes, and community structure have been affected by limitations from prey availability (Poole 1982, Martin 1987a, Rutz and Bijlsma 2006). Prey availability to a predator is determined by the composition, densities, and vulnerability of prey to predation (Orth et al. 1984, May and Norton 1996, Schneider 2001, Schmidt and Ostfeld

2003), which influence a predator’s diet through selection of potential prey species

(Estabrook and Dunham 1976, Davies 1977, Bence and Murdoch 1986, Fryxell and

Lundberg 1994). For example, the highly endangered Spanish Imperial Eagle (Aquila adalberti) whose population has seen significant decline (Gonzalez et al. 1989), has higher reproductive success and occupancy rate in territories in which high densities of their main prey item are found (Gonzalez et al. 1990, Ferrer and Bisson 2003). The

Golden Eagle (Aquila chrysaetos) also exhibits higher nesting densities and breeding success where there is high prey availability (Smith and Murphy 1979, Watson et al.

1992, Steenhof et al. 1997).

Many methods have been used to assess prey use of a raptor in an ecosystem.

Prey remains have been collected to observe composition of prey species in diet

28 (Steenhof and Kochert 1985, Redpath et al. 2001, Marti et al. 2007). Direct observations and video monitoring have also been used to measure diet composition, but also for monitoring provisioning rates during the breeding season (Rogers et al. 2005, Glass and

Watts 2009). Measuring provisioning rates of breeding raptors is important, as it can provide a metric of the ability of adults to supply an adequate amount of prey to the young, and has been used to help show or suggest limited prey availability with raptor populations previously (Dykstra et al. 1998, Warnke et al. 2002, Gill and Elliott 2003).

The Bald Eagle (Haliaeetus leucocephalus) is a wide-ranging top-level generalist predator in North America, and as with many other raptor species in North America, suffered dramatically from the effects of pesticides, such as DDT, and human persecution over the past couple hundred years. While nearly the entire range of Bald Eagles in the lower 48 states shared this population fluctuation, some local populations however did not. Florida Bay, located at the southern tip of Florida, represents Bald Eagles’ southernmost breeding range. Residing within Everglades National Park since its inception in 1948, this population stayed at what is thought to be carrying capacity up until the late 1980s (Baldwin et al. 2012). Over the past few decades however, this population has experienced a significant population decline (Baldwin et al. 2012) that coincided with drastic ecological changes to the ecosystem (Fourqurean and Robblee

1999). These ecological changes in Florida Bay, which affected the distribution and population of prey communities (Powell et al. 1989, Sogard et al. 1989, Matheson, Jr. et al. 1999, Lorenz et al. 2009), have already been thought to affect diet of the Bald Eagle.

Major dietary components of eagles in Florida Bay shifted from the early 1970s to late

2000s (Chapter 1), suggesting that prey availability has been altered. In addition, prey

29 availability looks to be limiting another large raptor in this ecosystem. The population of

Ospreys (Pandion haliaetus), who share breeding and foraging grounds with Bald Eagles in Florida Bay, has decreased by 58% in Florida Bay from 1973-1980 (Kushlan and Bass

Jr. 1983). Toward the end of this timespan in the same area Poole (1982) correlated brood reduction with lowered provisioning rates. And between 1986-1987, Osprey reproductive success was lower in Florida Bay than nearby sites (Bowman et al. 1989).

Foraging trips at the least successful sites were made more commonly from Florida Bay, and ospreys that foraged equally in both locations, provisioned less from Florida Bay

(Bowman et al. 1989).

It is possible that inadequate prey availability is contributing to the decline of the

Florida Bay Bald Eagle population. In this study we monitored prey deliveries and measured provisioning rates of eagle nests with video monitoring throughout the 2009-

2010 (hereafter 2009) and 2010-2011 (hereafter 2010) breeding seasons. If there is adequate prey availability for eagles, then provisioning rates will be high enough to supply young with an adequate amount of food. Also, provisioning rates should be high enough throughout the entirety of the breeding season to meet growing energetic demands of the young. We made comparisons to other eagle populations from throughout its range, healthy/growing and relatively less healthy, to provide insight on the meaning of the provisioning rates from this population in Florida Bay.

METHODS

To determine the nest sites that were included in our study, we first used current and historical productivity trends to determine the nest sites that had the highest

30 likelihood of raising young to fledging age (Baldwin et al. 2012). Next, it was determined if these nest sites were accessible and whether video-monitoring equipment could be installed. Certain nest sites were not included because they could not be fitted with video-monitoring equipment.

A total of three nest sites were monitored with video cameras in the 2009 breeding season and one in 2010. Camera equipment was installed before November 1 of the corresponding breeding season, which ensured the eagles had time for acclimation with the equipment before egg laying. Full-color video cameras (Supercircuits PC263;

3.5”x0.9”) were installed approximately five to six feet from the center of the nest at an angle greater than parallel. When possible, the camera was attached to a limb on the south side of the nest to limit sun glare. Audio, video, and power cords were run down the nest tree and away from the nest at a distance that helped decrease disturbance to the eagles. The cords were attached to a digital video recorder (DVR) (Secumate MDVR-14;

1.18”x3.58”x5.61”) to record video footage. A 12-volt deep-cycle battery, which was continuously charged with a solar panel (Asunpower KIT-020P-S60; 21.7”x13.8”x0.98”), powered the camera and DVR. The DVR recorded all video footage from one half-hour before sunrise to one half-hour after sunset. All video data was recorded to a removable

SD card (Sandisk 32GB SDHC). The equipment (not including solar panel) was placed in a weatherproof box in a location below the nest that was least visible to the adults.

Video-monitoring equipment was visited typically every week, but no longer than two weeks, to replace memory cards. Equipment was checked for proper function and young eagles were checked on with a portable TV set that connected to the DVR.

Visitation time was minimized as much as possible to decrease distraction to the eagles

31 and lasted no more than five minutes. All footage recorded was transferred to multiple hard drives and digitally stored for future reference. Analysis was made by observing all video data using VLC multimedia computer software (VideoLan Organization). For each prey delivery, date and time of delivery, lowest-determinable taxonomic classification of prey, overall length of fish (when determinable), and sunrise/sunset times were noted.

Time of delivery was represented as length of time after sunrise.

Mass of each prey item was estimated when possible. For avian deliveries, the

CRC Handbook of Avian Body Masses (Dunning Jr 1993) was used to estimate mass from the average mass listed for each species. Fish length was estimated by visually comparing it to adult talon length. Measurements were made to the one half talon length

(e.g. a fish=three and one half talon lengths). The fish length was converted to millimeters by using average Bald Eagle talon length data from Buehler (2000). Mass was then calculated by using species-specific length-weight conversions. If the conversion for a certain species was not available, the regression of a taxonomically similar species was used.

The daily provisioning rates (# of deliveries/day) and daily total biomass (total biomass/day) of prey deliveries were averaged from the third week after hatching to fledging. To determine how frequently and how long eagles deliver prey to the nest after fledging, we calculated provisioning rate from the third week after hatching until deliveries were no longer made to the nest for each nest and all nests combined as well.

To determine whether eagles changed their rate of delivery and size of deliveries, we regressed the mean daily # of deliveries per week and the mean daily total biomass of deliveries per week, respectively, against the age of the young. The slope was

32 determined different from zero if the p-value was <0.05. We also used linear regression models to test whether the contribution of each prey group (fish, bird, other) and species, calculated as the proportion of the total amount of deliveries, changed throughout the breeding season. Prey deliveries determined to at least family level were separated from beginning to end of the breeding season into four quarters, and then a randomization test of independence was used to see if the composition was different between these time periods. To determine whether eagles provision at different frequencies throughout the day, the number of deliveries for the entire breeding season was summed and plotted against each hour after sunrise.

RESULTS

A total of 546 prey deliveries were recorded over the two breeding seasons. 93%

(n = 508) were determined to class and 46% (n=253) were determined to family. Fish contributed 86.1% of all deliveries (sd = 9.2), birds made up 7% (sd = 1.1), and prey items that could not be determined to class made up 7% (Table 1). There were no other classes that were distinguishable in the video footage. The mean daily provisioning rates for all nest sites combined were 1.75 (sd = 0.31, range 1.33-2.07) deliveries/young/day and 2.64 (sd = 0.7, range 1.33-3.71) deliveries/day (Table 2). These rates were correlated to age of young and significantly declined throughout the breeding season (t = 5.3 r2 =

0.80, p = 0.0012, Fig 1). Each nest site showed declining provisioning rates throughout the progression of the breeding season, although only 2 were statistically significant (1 and 2 young). Prey was delivered to the nest and eaten by the recent fledglings up to two weeks after fledging. As expected, this provisioning rate for all nest sites combined was

33 lower than the breeding-season provisioning rate (1.56 (sd = 0.22, range 1.33-1.79) prey deliveries/young/day; 2.31 (sd = 0.92, range 1.43-3.51) deliveries/day), and declined throughout the breeding season (t = 8.1, r2 = 0.88, p < 0.0001).

We were able to estimate the biomass of prey deliveries at only one nest site. The total biomass of prey deliveries/young/day also declined throughout the breeding season

(t = 2.9 r2 = 0.68, p = 0.0066, Fig. 3). The randomization test showed that the compositions of prey deliveries throughout the breeding season were significantly different (p=0.012), of which there was a slight trend to more fish and fewer birds as the breeding season progresses (t = 4.5, r2 = 0.65, p = 0.0028) with 7% of deliveries are unknown. Deliveries were mostly frequently made to the nest during 3-5 hours after sunrise and then again at a less frequent rate 9-12 hours after sunrise (Fig. 4). The timing of when the most deliveries were made did not vary between nests (p = 0.84) or change throughout the breeding season (p = 0.42).

DISCUSSION

The Bald Eagle is generalist forager and their diet typically includes a variety of prey types (Buehler 2000). Prey remains collected from eagle nest sites in Florida Bay during the same time period consisted of 33 species from five classes (Chapter 1). While video monitoring tends to show more prey deliveries and prey groups than collecting prey remains (Lewis et al. 2004), video data was only able to distinguish 12 species (2 classes). This difference is due in part to collections of prey remains from 13 nest sites during the study period, while video data was collected from only four and video data collection from additional nests would lead to a higher number of species witnessed. In

34 addition, a number of deliveries were not distinguishable past class level (42.3% fish,

4.9% bird) or not determined at all (7% unk). While eagle diet often consists of multiple taxa, the highest contribution has typically come from fish (Dunstan and Harper 1975,

McEwan and Hirth 1980, Haywood and Ohmart 1986, Thompson et al. 2005). Similarly, fish made up 86.1% of all prey deliveries (92.5% of distinguishable) in video data from

Florida Bay. This higher contribution of fish and lower contribution of birds than reported from prey remains (Chapter 1) supports the general concept of a bias towards larger and heavier-boned species groups in prey remains (Simmons et al. 1991, Marti et al. 2007).

Provisioning rates of prey to the nest during the breeding season can be used to show or suggest how population sizes and reproductive parameters of breeding raptors can be limited by prey availability (Wiehn and Korpimaki 1997, Amar et al. 2003). The provisioning rate (1.75 deliveries/young/day, max = 2.07; 2.64 deliveries/day, max =

3.71) that we witnessed was much lower than expected, even for this dwindled population. Compared to other populations of Bald Eagles, these rates are noticeably lower (Table 3). Eagles from north-central Wisconsin had a mean provisioning rate of

3.0 deliveries/young/day (5.2 deliveries/day), almost twice that of eagles in Florida Bay

(Warnke et al. 2002). This population, unlike the population in Florida Bay, had high reproductive rates and had recently grown. Warnke et al. suggested that the population in

Wisconsin was not limited by prey availability and that these provisioning rates reflected an adequate availability of prey to support a thriving Bald Eagle population. This was further supported when nests from north-central Wisconsin were compared to relatively near-by nests close to Lake Superior. The nests near Lake Superior had a provisioning

35 rate of 1.67 deliveries/young/day (2.16 deliveries/day) versus 3.21 deliveries/young/day

(4.87 deliveries/day) with the nests at north-central Wisconsin (Dykstra et al. 1998).

Lake Superior nests have lower fledging rates (young per breeding attempt) than those in

Wisconsin and this was partially attributed to the lower provisioning rates which was presumed to reflect lower prey availability. On Vancouver Island, British Columbia,

Bald Eagles had a mean provisioning rate of 5.4 deliveries/day, similar to north-central

Wisconsin and again around twice as high as eagles in Florida Bay (Elliott et al. 2005).

Again in this same region, eagles had a provisioning rate of 3.02 deliveries/young/day

(Gill and Elliott 2003). In this study the provisioning rate was positively correlated with nesting success. Clearly caution should be used when comparing eagles from the Great

Lakes and Pacific Northwest regions to eagles in a subtropical mangrove estuary. Prey species, temperature, and weather patterns are drastically different in the regions and there may be, and are likely other factors that influence provisioning rates of these populations. Information on prey size and energetic consumption and demands of growing chicks would assist while making these comparisons. Unfortunately there are no previous estimates of provisioning rates of eagles in Florida Bay, but these other studies showing higher provisioning rates in healthy populations, offer some merit for comparison.

Ecological conditions determine how available to a prey it to a breeding raptor by influencing their total abundance, where there are located in relation to a breeding territory, and how vulnerable the prey is to predation (Orth et al. 1984, May and Norton

1996, Schneider 2001, Schmidt and Ostfeld 2003). Deviation from historic ecological conditions can elicit changes in availability of one or many prey communities. In the late

36 1980s, Florida Bay went through drastic ecological changes believed to be in part from changes in the hydrology of the Everglades that gives Florida Bay its freshwater input

(Fourqurean and Robblee 1999). In subsequent years, parameters of water quality, including salinity, showed modifications in level and variability during this time

(Fourqurean and Robblee 1999). Although not completely understood, one consequence seemed to be massive die-offs and redistributions of seagrass habitats that make up much of the habitat in Florida bay (Zieman et al. 1988, Robblee et al. 1991, Hall et al. 1999).

This aided the release of sediments into the water, causing algal blooms and increased turbidity (Phlips et al. 1993, Boyer et al. 1999). Blooms and turbidity were stronger and covered larger areas of Florida Bay during the winter months (Butler IV et al. 1995,

Boyer et al. 1999), which is the time that Bald Eagles are breeding in Florida Bay

(represented by prey remains) and requiring a higher food supply.

While there is limited knowledge of the mechanisms by which these ecological changes may have affected Bald Eagle prey assemblages in Florida Bay, it is known that they have negatively affected some fish and bird populations, the two classes that make up the majority of eagle diet (Chapter 1). Fish communities are dependent on the microhabitat differences that characterize Florida Bay (Sogard et al. 1989) and these fish communities have changed at locations that were affected by the ecological changes that occurred prior to monitoring period (Matheson, Jr. et al. 1999). For instance mullets, a common prey item, are associated with varying salinity levels in Florida Bay (Sogard et al. 1989). Salinity can also affect the metabolic rate, reproduction, and survival of Mugil cephalus, one of the Florida Bay mullet species (DeSilva and Perera 1976, Lee and Menu

1981, Cardona 2000). The distributions, egg survival, and growth of the Spotted Seatrout

37 (Cynoscion nebulosus), another fish prey, are correlated with the varying salinity levels and seagrass habitats in Florida Bay (Thayer et al. 1999, Powell 2003, Neahr et al. 2010).

In the Chesapeake Bay, the provisioning rates of both the Bald Eagle and Osprey have been linked to fish assemblages that are determined by salinity level difference within the region (Markham and Watts 2008b, Glass and Watts 2009). Bird communities have also been affected by ecological changes. Other large-predatory birds in Florida Bay have seen a change in abundance and distribution over time (Powell et al. 1989). The nesting subpopulation of Roseate Spoonbills (Ajaia ajaja) in Florida Bay has decreased over the same time frame, of which has been attributed to hydrologic conditions and salinity in this ecosystem (Lorenz et al. 2009). Information of the abundance and distributions of other fish and birds in Florida Bay is however limited.

Seasonal shifts in provisioning rates can occur if prey availabilities change throughout a breeding season, especially for bird species with long fledging periods

(Weimerskirch and Lys 2000). This presents a challenge for a pair of breeding birds to properly meet the needs of their growing young for the entirety of the breeding season.

Not only do provisioning rates at eagle nests in Florida Bay suggest an overall limit of prey availability, the provisioning rate significantly decreased throughout the breeding season. The mean provisioning rate of the populations in Wisconsin and Vancouver did not correlate with age. This was not stated in the other aforementioned studies, suggesting that it was not examined or there was neither a noticeable decrease nor increase. It may be logical to think that as young in a nest grow older and become larger, they will require more food intake causing their parents to delivery more prey. Even though there was no correlation in provisioning rate to age of young in previous Bald

38 Eagle observational studies, there was also no decrease. A decrease in provisioning rate does not seem to be a characteristic of adequate prey availability. A possible explanation of this phenomenon are if parents were able to deliver a constant or increased amount of total biomass of prey to the nest by increasing the size of prey deliveries. Determining length of fish can be difficult task, as eagles don’t always bring in whole fish and different parts of the fish are often delivered (e.g. tail vs head). Mean length of individual fish deliveries, corrected for whole length, however does not seem to change throughout the season, suggesting that a change in the mean length of available fish did not change. However, not every fish has the same length-to-mass ratio (e.g. long and skinny vs short and fat). Even so, we were able to see a decline in the total biomass of prey deliveries throughout the breeding season in addition to provisioning rates.

Although length and biomass data was only collected at one nest throughout this study it was still able to show a significant decreasing trend. This decrease in provisioning rate and biomass throughout the breeding season is another cause for concern and further suggests inadequate prey availability for these eagles.

It is a well studied aspect of avian ecology that populations of birds on the edge of their range are faced with a different set of external variables, such as weather, temperature, physical barriers (Andrewartha and Birch 1954, Root 1988). The Bald

Eagles in Florida Bay are the southernmost breeding population, and they certainly are exposed to different external environments than eagles in other areas of its range (e.g.

Alaska, Chesapeake Bay, Wisconsin, etc). One striking environmental factor differing is ambient temperature, and it is known that thermal stress can affect the distribution and metabolic rate of avian species, including Bald Eagles (Stalmaster 1983, Stalmaster and

39 Gessaman 1984, Stalmaster and Plettner 1992). While Florida Bay has highly different extreme temperatures than the more northern breeding eagles, at the different times they are breeding (summer in the north vs winter for the south) the temperatures are not as different. The monthly mean temperatures for each of the previously mentioned eagle populations were on average only eight to nine degrees (range 4-13 degrees) cooler than

Florida Bay during the respective breeding seasons (historical temperature data retrieved from wunderground.com). And of the previous studies on thermal stress in Bald Eagles, only wintering eagles in northern latitudes experience thermal stress to the degree that negatively affects them. Also, there is a critical temperature of 10.6 degrees C at which eagles begin to feel thermal stress, and energy intake is not different between 5 and 20 degrees C (Stalmaster and Gessaman 1984). This suggests that even though these eagles share quite different temperatures than northern eagles, that temperature does not influence eagle diet to induce lower energy intake and therefore a significantly lower provisioning rate.

In addition to temperature, there are additional factors that could influence this southern population differently. Length to fledging stage can be variable in the Bald

Eagle (Buehler 2000), but distribution does not appear to affect the fledging time of this population. Fledging time in Florida Bay varied from 11-12 weeks long, which is similar to other populations of Bald Eagles (California 12, Florida 11, Maine 11-13,

Saskatchewan 11-12). However, growth rate of Bald Eagles is significantly correlated to the total biomass of pre deliveries (Bortolotti 1989). If this population was under stress from an inadequate supply of food causing the adults to provision a reduced amount of food, a longer time to fledging could be seen, even though it was not. It is also known

40 that southern Bald Eagles are generally smaller than northern birds. This smaller adult size could reduce the time that young need to reach fledging stage, which would compensate for the slower growth rate. Unfortunately, these parameters are currently not understood in great detail for this population. Southern eagles are, however, thought to be around 15-20% smaller than northern eagles (Buehler 2000). It is unknown how much of a difference the Vancouver and Wisconsin eagles are from the Florida Bay eagles, but potentially playing a roll in the much lower provisioning rates, which are on average about half of the northern populations that were compared.

Generalist raptors have the ability to take a wide variety of prey types. This trait would assist them if they were to experience changes in prey availabilities throughout a breeding season. In addition to the decreasing provisioning rates at Bald Eagle nests was the change in the contribution of prey groups throughout the breeding season. These parameters could be a function of the changing nutritional needs of the young, as stated by Gill (2007), but also as a result of seasonal population fluctuations of both fish and avian prey in Florida Bay and year-to-year variation in the timing of these seasonal population fluctuations. The composition and densities of fish communities within

Florida Bay fluctuates with changing seasons and months (Matheson, Jr. et al. 1999,

Thayer et al. 1999). In one example, the Spotted Seatrout, a common prey item of Bald

Eagles in Florida Bay, have peak densities and spawning at specific times during the year, and these peaks can occur at different times of the year from year to year (Powell

2003, Powell et al. 2007). Densities and abundance of nearly all wading bird species of

Florida Bay, also fluctuate in density seasonally and peak nesting months very between years (Powell 1987, Lorenz et al. 2002). These annual fluctuations of density of prey

41 species in Florida Bay are connected to the annual seasonal cycle of precipitation in south

Florida that represents the wet and dry seasons. This change in the amount of rain directly contributes to seasonal oscillations in salinity levels (Kelble et al. 2007) and water depths (Montague and Ley 1993) of Florida Bay. These ecosystem conditions have a direct affect on the prey composition, abundance, and distribution of prey in Florida

Bay and could be leading the Bald Eagle to change their food habits throughout the season. Florida Bay has historical regular variability, and this shift could be a natural occurrence that is unique to this local population. If this were the case, the Bald Eagle population would have evolved with this scenario along with the evolution of the ecosystem and would not lead to a reduction of the breeding population in as we have seen. Further analysis of declining provisioning rates, biomass, and change in composition of prey should be further studied to fully understand how it might affect this population of Bald Eagles.

The population fluctuation of Bald Eagles over the past couple centuries in response to pesticides, such as DDT, and human persecution have been documented in great detail. Up until the late 1980s the breeding population in Florida Bay was thought to be at carrying capacity (Baldwin et al. 2012). Residing within the boundaries of

Everglades National Park since 1948, this population did not seem to be affected by the same factors that caused declines in other Bald Eagles and raptors. However, over the past few decades this population has seen a significant loss of occupied breeding territories (Baldwin et al. 2012) that coincided with ecological changes from altered hydrology in the Everglades. Since there is no indication that pesticides, habitat loss, persecution, or other potential limiting factors are affecting these eagles, food limitation

42 is a leading hypothesis for this decline. A lack of adequate food supply can affect life history traits, population sizes, and community structure of raptors (Poole 1982, Martin

1987b, Rutz and Bijlsma 2006). Though we were not able to directly correlate provisioning rates to prey availabilities in this study, we believe there is an inadequate food supply for a healthy Bald Eagle population in Florida Bay. This could be limiting the breeding population and presents the need for further studies on how provisioning rates and reproductive success are related. With the goal to restore Florida Bay to a historical observed state, prey availabilities may continue to change and alter Bald Eagle food habits. Provisioning rates and diet may serve as a monitoring tool for the condition of prey communities in the future and gives merit to their continued examination.

43 TABLES

Table 2.1 Number and percent contribution of prey deliveries to four Bald Eagle nests during the 2009 and 2010 breeding seasons in Florida Bay.

% % Prey N Group Total Fish Ladyfish (Elops saurus) 30 6.4 5.5 Jack (Genus Caranx) 26 5.5 4.8 Drums, Croakers, Seatrout (Family Sciaenidae) 14 3.0 2.6 Seatrout (Genus Cynoscion) 11 2.3 2.0 Spot (Leiostomus xanthurus) 1 0.2 0.2 Red Drum (Sciaenops ocellatus) 4 0.9 0.7 Hardhead Catfish (Arius felis) 13 2.8 2.4 Mullet (Genus Mugil) 10 2.1 1.8 Pompanos (Genus Trachinotus) 6 1.3 1.1 Barracuda (Sphyraena barracuda) 3 0.6 0.5 Unknown Fish 352 49.1 42.3 Subtotal 470 86.1

Birds

Double-Crested Cormorant (Phalacrocorax auritus) 8 21.1 1.5 Ring-billed Gull (Larus delawarensis) 2 5.3 0.4 Roseate Spoonbill (Ajaia ajaja) 1 2.6 0.2 Unknown Wading Bird 3 7.9 0.5 Unknown Bird 24 63.2 4.4 Subtotal 38 7.0

Other 0 0.0

Unknown 38 7.0

Total 546

44 Table 2.2 Breeding season provisioning rates of four Bald Eagle nests during the 2009 and 2010 breeding seasons in Florida Bay.

Provisioning Rates Breeding Season # of Young Deliveries/Young/Day Deliveries/Day 2009 1 2.07 2.07 1 1.33 1.33 2 1.72 3.44 2010 2 1.85 3.71 Mean 1.75 2.64

Table 2.3 Provisioning rates at Bald Eagle nest sites reported from various areas in its range.

Deliveries/ Deliveries/ Location Young/Day Day Source Florida Bay (This Study) 1.75 2.64 Wisconsin 3 5.2 Warnke et al. 2002 Wisconsin 3.21 4.87 Dykstra et al. 1998 Lake Superior 1.67 2.16 Dykstra et al. 1998 Vancouver - 5.4 Elliot et al. 2005 Vancouver 3.02 - Gill and Elliott 2003

45 FIGURES

Figure 2.1 Linear regression of the mean daily provisioning rate averaged per week for four Bald Eagle nests during the 2009 and 2010 breeding seasons in Florida Bay.

46

Figure 2.2 Linear regression of the mean daily total biomass for one Bald Eagle nest during the 2009 breeding season in Florida Bay.

47

Figure 2.3 Number of deliveries per hour after sunrise for four Bald Eagle nests during the 2009 and 2010 breeding seasons in Florida Bay.

48 APPENDICES

Appendix A. List of length-weight equations used and the species that the equation was used for. (Equations retrieved from fishbase.org)

Deliveries Used For Length-Weight Equation Species Used In Equation Barracuda W = 0.0050*L^3.083 (n=10) Sphyraena barracuda Hardhead Catfish W = 0.0081*L^3.196 (n=101) Arius felis Ladyfish W = 0.0056*L^3.100 (n=776) Elops saurus Mullet W = 0.0213*L^2.750 (n=465) Mugil cephalus Pompano W = 0.0453*L^2.300 (n=9) Trachinotus carolinus Redfish W = 0.0077*L^3.098 (n=41) Sciaenops ocellatus Seatrout, Spotted Seatrout W = 0.0088*L^3.000 (n=400) Cynoscion regalis Spot W = 0.0092*L^3.072 (n=944) Leiostomus xanthurus

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