MOVEMENT, DISPERSAL AND INTERPRETING HEALTH ASSESSMENT
PARAMETERS FOR FREE-RANGING RAPTORS AND A REPTILE IN A
COMPROMISED ESTUARINE ECOSYSTEM
by
Brian K. Mealey
A Dissertation Submitted to the Faculty of
The Charles E. Schmidt College of Science
in Partial Fulfillment of the Requirements for the Degree of
Doctor of Philosophy
Florida Atlantic University
Boca Raton, Florida
August 2014
Copyright by Brian K. Mealey 2014
ii
ACKNOWLEDGEMENTS
I wish to express sincere gratitude to my committee for all of their guidance, patience and support, and special thanks to my advisor, Dr. John D. Baldwin for his persistence and continuing encouragement as I pursued one of the most challenging goals of my life, a Ph.D. A special gratitude to Dr. Michael R. J. Forstner, a true friend and excellent mentor, for his insight, sense of humor and always believing that I would complete my candidacy for a Ph.D. My warmest appreciation to Dr. Gregory Bossart,
V.M.D. for his mentoring, insightful approach and friendship during the 20 years of collecting data for this investigation. To my wife and soul mate, Greta Mealey, my field partner, who shared my frustrations and challenges in pursuit of this major milestone of my life. Also my incredible children, Caitlin and Sean, for their field work and being so patient with my life sermons as we trekked where so few have gone before. A special thanks to George E. Batchelor, a pioneer in American aviation, for your support, patience and mentorship, we will be forever indebted. “Godspeed and until we meet again.” Our warmest appreciation is extended to S. Batchelor, J. Batchelor, D. Ferraresi and J. Falk and the Batchelor Foundation, Inc. for their support, suggestions, funding and participation from the onset of this project. K. Meyer and G. Kent from the Avian
Research and Conservation Institute (ARCI) for their mentorship, enthusiasm and contributions to this manuscript. We thank The A. D. Henderson Foundation, The
Chingos Foundation, Florida Fish and Wildlife Conservation Commission, U.S. Fish and
Wildlife Service and the South Florida Water Management for providing partial funding iv for the project. We appreciate the collaboration of the National Audubon Society and the
Florida Audubon Society for their energy and dedication to the protection of South
Florida’s fragile ecosystem. I very much appreciate the Everglades National Park (ENP)
Rangers, D. King and D. Fowler for their advice, eyes and safety protocols while we were in the field. We extend special acknowledgements for the ENP’s Dispatch Service,
Rangers and the Biologists for their support, guidance and vigilance over this most precious ecosystem.
v ABSTRACT
Author: Brian Keith Mealey
Title: Movement, Dispersal and Interpreting Health Assessment Parameters for Free-Ranging Raptors and a Reptile in a Compromised Estuarine Ecosystem
Institution: Florida Atlantic University
Dissertation Advisor: Dr. John D. Baldwin
Degree: Doctor of Philosophy
Year: 2014
This investigation compared statistical parameters for the blood serum chemistries of free ranging Osprey nestlings from Florida Bay and an Osprey population from Lake
Istokpoga, in Central Florida (Chapter 1). Florida Bay Ospreys showed higher mean rank values for alanine aminotransferase (H=6.79, P=.009), alkaline phosphatase (H=6.48,
P=.011), and sodium (H=5.7, P=.017), and Central Florida had higher mean rank values potassium (H=13.19, P=.000) and carbon dioxide (H=6.23, P=.013). Serum chemistries values were also compared between free-ranging Bald Eagle and Osprey nestling in
Florida Bay estuary in southern Florida (Chapter 2). There were significant differences between serum values of Bald Eagle and Osprey nestlings. Bald Eagle serum values were higher for total protein (H=17.833, P=.00002), Albumin (H=7.449, P=.006), Aspartate aminotransferase (H=113.153, P =.0001), and Calcium (H=7.148, P = 008). Osprey
vi serum values were higher for alanine aminotransferase (H=11.824, P = 0.0005), alkaline phosphatase (H=105.5, P =.0001), creatine kinase (H=13.465, P = 0.0002), carbon dioxide (H=4.443, P = 0.035) and cholinesterase (H=99.3, P=.0001).
Sixteen nestling Bald Eagles were fitted with satellite platform transmitter terminal (PTT) or VHF radio transmitter package for a duration of six years (Chapter 3) to identify their movement and dispersal. One of the 15 eagles migrated to North
Carolina, whereas the other 14 (93%) confined their movements to Florida. Tracking duration per individual ranged from 82 to 1,531 days. We estimated first-year survival as
52% and 67% for the period from 1.5 to 3 years.
Diamondback Terrapins (Chapter 4) were evaluated by an integrated assessment of physical, chemical, and physiological parameters. Extreme site fidelity of the turtles to mangrove habitat was evident along with a strong female biased sex ratio. There was a significant difference in the total number of individuals collected at the two sites (P =.
01) despite the total size and shorelines of the two sites being very nearly the same. Total recapture rate was 70% for combined population (TLK = 80% and CKW = 48%). We provide blood serum values and microbial cultures as baselines from these turtles in the wild.
vii MOVEMENT, DISPERSAL AND INTERPRETING HEALTH ASSESSMENT
PARAMETERS FOR FREE-RANGING RAPTORS AND A REPTILE IN A
COMPROMISED ESTUARINE ECOSYSTEM
LIST OF FIGURES ...... x
LIST OF TABLES ...... xiii
INTRODUCTION ...... 1
I. COMPARING AND INTERPRETING SERUM CHEMISTRY VALUES OF OSPREY NESTLINGS, PANDION HALIAETUS, FROM CENTRAL FLORIDA AND FLORIDA BAY, EVERGLADES NATIONAL PARK ...... 5
Methods ...... 6
Results ...... 10
Discussion ...... 11
II. COMPARING AND INTERPRETING SERUM CHEMISTRY OF NESTLING BALD EAGLES (HALIAEETUS LEUCOCEPHALUS) AND OSPREYS (PANDION HALIAETUS) IN FLORIDA BAY, EVERGLADES NATIONAL PARK ...... 27
Methods ...... 28
Results ...... 31
Discussion ...... 33
III. MIGRATORY, DISPERSAL AND MOVEMENT PATTERNS OF BALD EAGLES (HALIAEETUS LEUCOCEPHALUS) FLEDGED FROM FLORIDA BAY, EVERGLADES NATIONAL PARK ...... 55
Methods ...... 57
Results ...... 59 viii Discussion ...... 62
IV. CHARACTERISTICS OF MANGROVE DIAMONDBACK TERRAPINS (MALACLEMYS TERRAPIN RHIZOPHORARUM) INHABITING ALTERED AND NATURAL MANGROVE ISLANDS ...... 109
Methods ...... 110
Results ...... 113
Discussion ...... 115
CONCLUSION ...... 123
Chapters 1 and 2 ...... 123
Chapter 3 ...... 124
Chapter 4 ...... 124
APPENDICES ...... 126
LITERATURE CITED ...... 135
ix LIST OF TABLES
Table 1.1. Hematological Value (PCV) and Metabolic Chemistry Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida ...... 19
Table 1.2. Serum Enzymology Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida ...... 19
Table 1.3. Serum Electrolytes and Mineral Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida ...... 20
Table 1.4. Blood Mercury (Hg) Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida ...... 20
Table 1.5. Mann-Whitney U Test Results Comparing Similar Sample Sizes for FLB and CFL Osprey Nestling’s Serum Chemistry Values ...... 21
Table 1.6. Environmental Stresses as They Relate to Statistical Difference in Serum Parameters for the Osprey Populations ...... 24
Table 1.7. Tabulation of Hematology and Biochemistries of Nestling Ospreys from Florida Bay and Central Florida with Published Values for Osprey Nestlings ...... 25
Table 1.8. Tabulation of Hematology and Biochemistries of Nestling Ospreys from Florida Bay and Central Florida with Published Values for Global Raptors ...... 26
Table 2.1. Defining The Serum Chemistry Parameters and Their Application to Ecological Field Studies ...... 40
Table 2.2. Mean Blood Serum Values for Bald Eagles in Florida Bay, Everglades National Park ...... 43
Table 2.3. Mean Blood Serum Values for Ospreys in Florida Bay, Everglades National Park ...... 44
x Table 2.4. Mann-Whitney U Test Results Comparing Ospreys and Bald Eagle Blood Serum Values in Florida Bay ...... 47
Table 2.5. Mean Blood Serum Values for Osprey in Eastern Florida Bay and Western Florida Bay ...... 48
Table 2.6. Results for the Mann-Whitney U Test Comparing Ospreys Blood Serum Values for Eastern and Western Florida Bay ...... 51
Table 2.7. Environmental Stresses as They Relate to Statistical Difference in Serum Parameters for the Osprey Populations ...... 51
Table 2.8. Mean Blood Serum Values for Bald Eagles in Eastern and Western Florida Bay ...... 52
Table 2.9. Results for the Mann-Whitney U Test for Bald Eagle Serum Values for Eastern and Western Florida Bay ...... 53
Table 2.10. Environmental Stresses as They Relate to Statistical Difference in Serum Parameters for the Osprey Populations ...... 53
Table 2.11. A Comparative View of Serum Values of Multiple Raptor Species ...... 54
Table 3.1. Platform Terminal Transmitter (PTT) Packages Were Attached to Bald Eagle NestlingThat Were < 9 Weeks Old in Florida Bay, Everglades National Park ...... 69
Table 3.2. Results for Sixteen Bald Eagles Fledged from Florida Bay, Everglades National Park ...... 70
Table 3.3. Number of Transmission Locations for Each Year the Bald Eagles Were Transmitting ...... 71
Table 3.4. The Graph Shows the Month That the Florida Bay Fledged Bald Eagles Departed fromTheir Natal Territory ...... 72
Table 3.5. Natal Site Departure Date, Total Distance Since Transmitting and the Distance Traveled Each Day ...... 73
Table 3.6. Depicting the Distance Traveled by Year for Bald Eagles Surviving through the Second and Third Year ...... 74
Table 3.7. Two Results Are Calculated to Determine the Home Range of the Fledged Bald Eagle ...... 75
xi Table 3.8. Comparing Annual Survivorship of Bald Eagles in FL Bay, Central Florida (CFL) (Wood and Collopy 1994), FL Suburban and FL Rural (Millsap et al. 2004), Chesapeake Bay (CB) (Buehler et al. 1991) and Maine (McCollough 1986) ...... 76
Table 4.1. Morphometric Measurements (mm) Millimeters and Weight (g) Grams for the Terrapin, Malaclemys terrapin rhizophorarum, for the Study Sites TLK and CKW ...... 120
Table 4.2. Serum Chemistry Values for 20 Mangrove Diamondback Terrapins (M. t. rhizophorarum) from the Lower Florida Keys ...... 121
Table 4.3. The Microbial Results of 17 Individual Cloacal Cultures of Mangrove Diamondback Terrapins (M. t. rhizophorarum) from Two Study Sites ...... 122
xii LIST OF FIGURES
Figure 1.1. Lake Istokpoga and Florida Bay were the study sites for this project ...... 18
Figure 1.2. Serum parameter values for Osprey populations in Florida Bay (FL) and Central Florida (CFL) and south Florida (Total) for all years examined ...... 23
Figure 2.1. Satellite view of Florida Bay identifying eastern and western Florida Bay as the study site ...... 39
Figure 2.2. Serum parameter values for Bald Eagles and Osprey populations in Florida Bay (FL) for all years examined ...... 46
Figure 2.3. Serum parameter values for Osprey populations in eastern and western Florida Bay (FL) for all years examined ...... 50
Figure 2.4. Serum parameter values for Bald Eagle populations in eastern and western Florida Bay (FL) for all years examined ...... 53
Figure 2.2. Serum parameter values for Bald Eagles and Osprey populations in Florida Bay (FL) for all years examined ...... 46
Figure 2.3. Serum parameter values for Osprey populations in eastern and western Florida Bay (FL) for all years examined ...... 50
Figure 2.4. Serum parameter values for Bald Eagle populations in eastern and western Florida Bay (FL) for all years examined ...... 53
Figure 3.1. Map of Florida identifying the initial tagging site for the fledged bald eagles ...... 68
Figure 3.2. Movement pattern for Eaglet 73338 ...... 77
Figure 3.3. Fixed Kernel Home Ranges for bald eagle 73338 ...... 78
Figure 3.4. Movement pattern for Eaglet 73335 ...... 79
Figure 3.5. Fixed Kenel Home Ranges for Bald Eagle 73335 ...... 80
xiii Figure 3.6. Movement pattern for Eaglet 46264 ...... 81
Figure 3.7. Fixed Kenel Home Ranges for Bald Eagle 46264 ...... 82
Figure 3.8. Movement pattern for Eaglet 46265 ...... 83
Figure 3.9. Fixed Kernel Home Ranges for bald eagle 46265 ...... 84
Figure 3.10. Movement pattern for Eaglet 56105 ...... 85
Figure 3.11. Fixed Kernel Home Ranges for bald eagle 56105 ...... 86
Figure 3.12. Movement pattern for Eaglet 56106 ...... 87
Figure 3.13. Fixed Kernel Home Ranges for bald eagle 56106 ...... 88
Figure 3.14. Movement pattern for Eaglet 56107 ...... 89
Figure 3.15. Fixed Kernel Home Ranges for Bald Eagle 56107 ...... 90
Figure 3.16. Movement pattern for Eaglet 56108 ...... 91
Figure 3.17. Fixed Kernel Home Ranges for Bald Eagle 56108 ...... 92
Figure 3.18. Movement pattern for Eaglet 56109 ...... 93
Figure 3.19. Fixed Kernel Home Ranges for Bald Eagle 56109 ...... 94
Figure 3.20. Movement pattern for Eaglet 64555 ...... 95
Figure 3.21. Fixed Kernel Home Range for Bald Eagle 64555 ...... 96
Figure 3.22. Movement pattern for Eaglet 64556 ...... 97
Figure 3.23. Fixed Kernel Home Ranges for Bald Eagle 64556 ...... 98
Figure 3.24. Movement pattern for Eaglet 64557 ...... 99
Figure 3.25. Fixed Kernel Home Ranges for Bald Eagle 64557 ...... 100
Figure 3.26. Movement pattern for Eaglet 73336 ...... 101
Figure 3.27. Fixed Kernel Home Ranges for Bald Eagle 73336 ...... 102
Figure 3.28. Movement pattern for Eaglet 73337 ...... 103
xiv Figure 3.29. Fixed Kernel Home Ranges for Bald Eagle 73337 ...... 104
Figure 3.30. Movement pattern for Eaglet 73339 ...... 105
Figure 3.31. Fixed Kernel Home Ranges for Bald Eagle 73339 ...... 106
Figure 3.30. Depicts the localized movement within the state of Florida of 15 eaglets fledged from Florida Bay and one from Port St. Lucie ...... 107
Figure 3.31. Movement patterns for all Eaglets sampled within the project ...... 108
xv INTRODUCTION
Areas of southern Florida, the Florida Keys, and Florida Bay are undergoing rapid human development and are experiencing an increasing loss of biodiversity alongside the collapse of ecologically functioning systems (Mealey et al., 2005; Meshaka and Ashton
2005). Nutrient run-offs, dead reefs, habitat and species loss are but a few serious issues that wildlife face in the Florida Keys. The ecology of insular wildlife remains poorly understood and continues to be very difficult to compile due to continued habitat alterations and the rarity of species retaining a suitable number of individuals upon which to conduct accurate surveys. Wildlife living in areas of the Florida Keys that are easily accessible is under incredible pressure from continuing development, constant vehicular traffic and frequent human encounters. This is complicated by larger scale modifications fragmenting the landscape. For example, U.S. Highway 1 symmetrically divides this archipelago. Adjacent roads leading off U.S. Highway 1 to home and business sites heavily fragment and compromise the remaining habitat on the developed keys. Larger wildlife such as the American Crocodile (Crocodylus acutus) (Moler 1992),
Diamondback Terrapin (Malaclemys terrapin), (pers. obs. by the author) and large birds of prey are killed by cars (Mealey et al. 2005). Smaller wildlife has additional pressures like predation by feral and domestic dogs and cats (Iverson 1979) and the introduction of other non-native flora and fauna (Krysko and King 2002). These anthropogenic stressors act to reduce species densities and may result in the extirpation of these unique insular wildlife species (Rocha 2002). Unfortunately, documenting such effects can be very 1 difficult and there is significant lack of primary data for purportedly healthy species, from which, to evaluate changes in their numbers caused by direct or indirect human activities.
The National Academies of Science, stated that the current knowledge base in the environmental and social sciences, is simply not yet adequate to enable anyone to determine the innate resiliency of the Florida Keys ecosystem to withstand all impacts of additional land development activities (Huber et al. 2002). It will only come from patient work and support, rare moments of creative insight, and a continuing investment in synthetic efforts.
Natural events such as hurricanes, fires and severe droughts remain as a background of natural pressures continuing to affect the remaining natural habitat for these reptile and avian species. Historically the effects of drought or storm could be avoided by dispersal to areas not as hard hit. This option has become extremely limited due to the fragmented habitat. Thus, for each of these islands, the anthropogenic factors interact with the already considerable effects of small population size and limited habitat to place them at risk. Unless public awareness and conservation efforts are enhanced for many of these vulnerable species in south Florida, the Florida Keys, and Florida Bay, these unique insular wildlife species will simply be added to the list of threatened and vanishing Florida fauna. The first step toward a public awareness program is to provide scientific documentation of the most basic biological parameters for these animals.
Determining solutions is complex when dealing with human communities and a compromised ecosystem. This emergent conundrum involves human societies with different ethnicities, development fragmenting the continuous flow of an ecosystem,
2 impacts of climatic change, water conservation issues and how to maintain the biological integrity of all species.
Mangrove and estuarine communities are tied to a variety of ecosystem functions, but seldom are reptile and avian components within the system integrated in the evaluations. Bald Eagles (Haliaeetus leucocephalus) and Ospreys (Pandion haliaetus) and one turtle species in particular, the diamondback terrapin, are dependent on a very broad array of the ecosystem services provided by the estuarine and mangrove community. This investigation intends to describe and identify key aspects of the ecology and several health assessment parameters for the Diamondback Terrapin, Bald Eagles and
Ospreys from the mangrove keys present in the Florida Bay estuary. As a consequence, the viability of the avian and reptilian populations may be reflective of the integrity of the ecosystem on which they depend. This study evaluated the utility of these species meristics and demographics alongside metabolic indices as comparative metrics in comparing the health of these animals in a relatively pristine mangrove community and within a compromised estuarine ecosystem.
In order to augment other aspects of the study of life history of the species, clinical study of field physiological parameters such parasites, blood mercury levels, feather mercury levels, serum chemistries and microbial swabs were initiated (Mealey et al. 2006). This clinical investigation will partially involve determining baseline health parameters for two raptor species and one turtle. The consequences of the presence of certain microbial organisms, high levels of mercury in the blood or feathers, unusual fecal parasites or aberrant readings in the serum chemistries will be investigated. In a recent publication, in reference to serum chemistries values for eaglets, it was concluded
3 that until more is known about the applications of these values as a monitoring tool for free-ranging raptors, these results should complement and be used with good ecological data for a species assessments (Mealey et al. 2004).
These projects will provide data on the movement and dispersal and interpreting health assessment parameters of two avian species, Bald Eagles, (Haliaeetus leucocephalus), and the Osprey, (Pandion haliaetus), and one reptilian species,
Diamondback Terrapins, (Malaclemys terrapin rhizophorarum), providing evidence, among the first, to support the very tight linkage of these species to their respective habitat in Florida Bay and the Florida Keys. Determining health parameters and if these values are site specific will enable veterinarians and wildlife agencies to better wildlife populations. Health assessment parameters will be compared with other species sharing the same ecosystem. Integrating health assessment parameters with traditional ecological techniques offers wildlife agencies additional ways of monitoring wildlife at risk.
4 I. COMPARING AND INTERPRETING SERUM CHEMISTRY VALUES OF
OSPREY NESTLINGS, PANDION HALIAETUS, FROM CENTRAL FLORIDA AND
FLORIDA BAY, EVERGLADES NATIONAL PARK
Serum values are functional tools in the diagnosis of metabolic diseases and physiological parameters, which could impact survivorship of individuals. Depressed and hyperactive values of serum may also identify levels of pesticide and pollutant exposure, impacting a species reproductive cycle (Toschick et al. 2005). Researchers are attempting to decipher mechanisms to integrate serum and hematological values into practices of wildlife management, as of now they are peripheral (Muriel et al. 2013). An integrative biological approach to raptor management offers more tools to enhance the decision process of species management.
Contemporary serum and blood manuscripts address serum values of a species and very few take into account the possibility of a species niche influencing a serum value (Casado et al. 2002). Global raptor species, such as Ospreys, Pandion haliaetus, inhabit an array of different niches. Could the environmental factors of a niche impact the serum levels of a particular species?
Florida Ospreys are associated with the state’s aquatic ecosystems. Florida serves as a wintering ground for many of the northern migratory Ospreys but also as a permanent residence and breeding site for a non-migratory population of Ospreys.
Martell et al. (2004) through satellite monitoring found that the central Florida Ospreys were partially resident and also migratory to South America, while the Florida Bay 5 Ospreys (FLB) were suspected to be a local resident group not moving far from the breeding territories. Comparing serum values of the two groups may provide insight on applications of serum assessment parameters.
Serum values from the Florida Bay population, an estuarine system could significantly differ from the Lake Istokpoga population, a freshwater lake system. Serum values may vary due to the ingestion of exterior dried salt crystals while the young are consuming prey. The objective of this study was to determine and compare selected serum chemistry parameters for two nestling groups of free-ranging Ospreys in Florida.
Methods
Study Site - The Florida Bay estuary lies between the southern portion of the
Florida peninsula to the north, the Florida Keys to the east and south and the Gulf of
Mexico to its west. It covers approximately 2200 square kilometers and lies within the boundaries of the Everglades National Park. East Florida Bay is the region east of Black
Betsy Keys. Central Florida Bay is bordered by Dump Key in the west and Black Betsy
Key in the east. West Florida Bay is designated as the region west of Dump Keys (Boyer et al. 1997) (Figure 1.1).
Aging and Sexing - Thirty nests per year containing Osprey nestlings from 35 to
45 days old were visited from 1 February through 1 June 1993 to 2007. Nestling development was monitored chronologically or through feather formation by way of repeated nest visits (Poole, 1984). Most of the nests were surveyed no more than three times. Each nest was visited only once for blood sampling. Thirty nests were surveyed and estimating a sample size of 15 Ospreys annually from each study site.
6 Blood Samples - Osprey nestling blood sampling was conducted between 1993 and 2007. The number of nests varied over the years depending on the reproductive activity of a territory. Blood sampling was conducted primarily during mornings, with only a few samples taken later in the day or evening. Tides and weather play an extremely significant role when attempting to reach the islands. Circadian rhythms were considered prior to sampling, but the window within the sampling period was extremely narrow due to tides, weather and other logistical constraints, resulting in opportunistic sampling. Nestlings were removed from the nests by the investigators and hooded with a traditional falconry hood manufactured by Northwoods, Inc. P.O. Box 874, Rainier, WA,
98576. Blood was extracted from the brachial vein (Cooper, 1975, Hoysak and
Weatherhead, 1991). The area surrounding the vein was cleaned with 70% isopropyl alcohol and a sterile 22, 23 or 25-gauge needle attached to a 3-ml syringe (Becton
Dickinson Co.), was used to extract 1 - 3 ml of blood from each nestling. All blood extraction sites had pressure applied and were observed for approximately 5 minutes post sampling to insure proper clotting prior to placing the nestling back into the nest (Hoysak and Weatherhead, 1991). Nests were resurveyed approximately 7-10 days post sampling to re-evaluate the nestlings’ condition. Hematocrit tubes were filled, for determining pack cell volume (PCV), prior to dispensing serum into the appropriate containers.
Blood serum samples were placed in small 1-ml red top plastic microtainer tubes with a serum separator (Becton Dickinson Co., Franklin Lakes, New Jersey) and heparinized hematocrit tubes (Jorgensen Laboratories, Inc., Loveland, Colorado) and allowed to clot for 15 minutes prior to centrifugation. Samples were spun for approximately 20 minutes with a portable Mobile spin centrifuge manufactured by (Vulcan Technologies, MO),
7 with a relative centrifugal force of 1100-x g. The spinning separates the molecules based on their density. Heavier molecules, red blood cells and then white blood cells settle on the bottom of the microtainer tubes. Centrifuging will be completed when the serum separator, denser than the serum, distinctly walled off the serum from the red blood cells.
The serum was transferred with a pipette to another blood tube to prevent hemolysis.
Field blood samples were placed in an ice cooler and later frozen. Samples were stored at
–16.1oC and analyzed within 30 days.
Serum Samples - Osprey sample sizes varied for each serum chemistry test depending on the amount of serum available. Some results were above or below the analyzer’s range, which resulted in smaller sample sizes due to test repetition. There was also some disparity in the samples sizes, with fewer being collected in CFL (N=31) compared with FLB (N=124). In addition to the initial analysis we selected and compared sampling years 1997 and 1999, for the two areas, which had comparable sample sizes (FLB=27 and CFL=15). One hematological value, packed cell volume
(PCV), and sixteen serum values were analyzed. Serum chemistries analyzed include seven enzymes: albumin (ALB), aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALP), lactate dehydrogenase (LDH), creatine kinase (CK), and cholinesterase (CHE); four metabolites: total protein (TP), uric acid (URIC), phosphorus (PHOS), and glucose (GLU); Four electrolytes: sodium (Na+), potassium (K+), carbon dioxide (CO2), and chloride (Cl-). One mineral, calcium
(Ca2++) was also analyzed. Blood samples were analyzed on a Kodak Ektachem DT II
System (Johnson & Johnson, Rochester, New York). Analysis and methodology followed the protocol in the Johnson & Johnson Ektachem DT II System manual.
8 Ektachem controls were run once a week to assure quality analysis control with all samples.
Banding - Osprey nestlings were banded with U.S. Fish and Wildlife Service bands during sampling. Red auxiliary aluminum bands (Acraft Sign and Nameplate Co.,
Alberta, Canada) were used to identify Ospreys in east Florida Bay and Green aluminum bands for the western Florida Bay Osprey nestlings. Michael McMillan, Highlands
County Parks and Natural Resources, banded the Central Florida Osprey population.
Statistical Analysis - The data analysis within the scope of this project scrutinized two groups of Ospreys nestlings in Florida between 1993-2007. Serum chemistry results were compared between following regions: central Florida (CFL), Florida Bay (FLB), east Florida Bay and west Florida Bay. Several serum chemistries were converted from micromoles/L to mg/dl to assist in establishing relationship between our units
(McConnell 1998-2000). The statistics to determine the parameters of serum values was accomplished by running the data through statistical software programs. Approximately
160 samples were tested for nineteen serum chemistries. Statistical values were analyzed using JMP SAS statistical discovery software (JMP SAS 2003). A Mann-Whitney U Test was conducted on the serum samples that were not normally distributed in order determine if there are variances between the regions (McDonald 2009).
This investigation was conducted under the guidelines of IACUC, U.S.
Department of the Interior (USDI), National Park Service permit number EVER-2010-
SCI-0009, USDI Bird Banding Laboratory Master Bander Permit number 22418 and
State of Florida Fish and Wildlife Conservation Commission permit number WB03367b
(Appendixes).
9 Results
One hundred and twenty four blood samples were collected from nestling Ospreys in Florida Bay and 37 samples from central Florida. Our blood sampling studies did not appear to have visible adverse effects on the health or fledging of the nestlings. The sampling area was devoid of markings and infections confirming the effectiveness of this blood sampling technique. Osprey nestling inactivity lasted for approximately 20 minutes after the sampling technique. Parents, primarily the female, were very diligent in returning to the nest within a few minutes of our departure. Females are identified through a dark bib on their chest compared to males with virtually no bib.
The results for PCV and serum chemistry values for the Osprey nestlings from
Florida Bay and central Florida are shown in Table 1. Some results were above or below the range measured by the Kodak platform, which resulted in lower sample sizes. The
Kodak serum analyzer has preset limits therefore unable to give results for certain values.
Several attempts were made to dilute above range values with mixed results of success.
Limited amounts of serum also prevented samples from being diluted.
One hematological value, PCV, and metabolic chemistry values: TP, GLU, PHOS and Uric acid for the Osprey populations are shown in Table 1.1. Serum enzymology values: ALB, AST, ALT, ALKP, LDH, CK and CHE are described in Table 1.2. Serum electrolytes: Na, K, CL, CO2 and one mineral Ca are provided in Table 1.3. Blood mercury values for the Ospreys nestlings are in Table 1.4.
Student-T tests were conducted on serum values between the Florida Bay population and the central Florida population. There were no significant differences in
10 the serum values, except for ALKP, (t = 3.08, p = .0001), between the FL and CF two osprey populations (Figure 1.2).
A Mann -Whitney U Test was conducted on a comparable sample size of Osprey serum between 1997-1999 for FLB (N=18) and CFL (N=15) (Table 1.5). Sample sizes were smaller for CFL due to inaccessible nests from the boat. The results for the Mann-
Whitney U test were significant indicating the mean ranks of serum values were different for the two populations. There were significant differences for five serum chemistries
(Figure 1.2). FL showed higher mean rank values for ALT (H=6.79, P=.009), ALKP
(H=6.48, P=.011), and Na+ (H=5.7, P=.017), and CF had higher mean rank values K+
(H=13.19, P=.000) and CO2 (H=6.23, P=.013) (Table 1.5).
Discussion
The enzyme ALT is found in various tissues, which catalyze the transfer of alanine amino groups. High levels of ALT indicate tissue injury but unfortunately its not tissue specific in birds. The ALT (P=. 0009) (Table 1.5) statistical difference between the Osprey populations is difficult to interpret but may relate to the lack of food in FLB.
The nestling could be starving and frantically injuring each other when the parents arrive with the food.
Levels of ALKP are indicative of osteoblastic activity such as mineralization of fractures or rickets (Leung et al. 1993). ALKP mean value results for free-ranging Osprey nestlings from FLB (461.4 U/L) and CFL (330.8 U/L) were significant (H=6.48, P=. 011)
(Table 1.5) and much higher than Bald Eagle nestlings in FLB (147.5 U/L) but similar to results from eaglets in Michigan (449 U/L) (Bowerman 2000) and lower than Balbontin
(2002) in Spain (2148 UI L-1), Golden Eagles, 1331 U/L (Sonne et al. 2010), Northern
11 Goshawk, 1381 U/L (Sonne et al. 2010) Montagu’s Harriers, 1242 U/L, (Liminanna et al.
2009) and the Iranian Chukar Partridge, 1041 U/L (Nazifi et al. 2011). Our values fall between the German (Muriel et al. 2013) and the Mexican Ospreys (Rivera-Rodriguez and Rodriguez-Estrella 2011) (Table 1.6).
The ALKP value discrepancies are difficult to interpret. Bhatti (2002) observed increased levels of ALKP during egg laying in chickens. It’s been suggested that aflatoxin poisoning of the liver, caused by the fungus Aspergillus, elevates levels of
ALKP (Coles 2007). In coastal Georgia, Hg and PCB’s altered the chemical composition of the bone in Clapper Rail chicks resulting in accelerated bone maturation (Rodriguez-
Navarro 2006). In this study, blood mercury (Hg) values are different (t = 6.72, p =
0.001) between the sites and could they account for the difference in ALKP values? The
Osprey population in FLB had significantly higher levels of ALKP (mean = 462 U/L) and blood Hg levels (mean = 0.68 ppm) (Table 1.4).
Muscle and tissue damage are correlated with high levels of CK and LDH
(Harrison and Harrison 1986). The CK and LDH values in this study may be due to the handling and physiology of nestling Ospreys and is in accord with the results found in free-living Bonelli’s Eagle, Booted Eagle, Hieraaetus pennatus, and the Spanish Imperial
Eagle, Aquila adalberti, (Polo et al. 1992, Balbontin and Ferrer 2002, Casado et al.
2002). OSPR CK values 1514.05 U/L were higher than FLB BAEA nestlings’ values of
1268.71 U/L. CK values for Scottish Ospreys at 2166 U/L (Meredith et al. 2012),
Swallow-tailed Kites nestlings 3084.44 U/L (Mealey et al. 2006) and Bearded Vulture nestlings 2645.10 U/L (Hernandez and Margalida 2010) were considerably higher (Table
1.7). CK values in German Ospreys were much lower at 302.43 U/L. A wildlife
12 veterinarian (Kramer pers. comm.) suggested a difficult venipuncture could result in tissue trauma and elevate CK/LDH values.
There is controversy in using CHE as an indicator for exposure to an organophosphate pesticide due to the variations in CHE levels over a short period of time
(P. Mineau pers. comm.). CHE blood values must be determined promptly since levels rapidly recover after exposure (Fildes et al.2009). Depressed levels in wildlife can also identify specific locations of exposures (Parsons et al. 2000). CHE levels < .9 u/ml is considered depressed and likely due to intoxications (Porter 1993, Heatley 2000). CHE mean values for FLB OSPR were 2.06 u/ml and for central Florida OSPR were 2.02 u/ml.
CHE values for FLB Bald Eagles were 1.29 U/L (Mealey et al. 2004) and Swallow-tailed
Kites were 0.8 U/L (Mealey et al. 2006). Values for Spanish Imperial Eagles were 1.24
U/L (Garcia-Montijano et al. 2002) and similar to the FL Bay Bald Eagles values. Even though there is limited published data on raptor CHE levels it appears that some raptor species may have a unique signature value for CHE (Roy et al. 2005). When diagnosing toxicity exposure with CHE values, it’s important to also use other clinical signs and examinations.
Electrolytes levels are useful in analyzing an avian gastrointestinal system. They are vital in controlling osmotic pressure and a system homeostasis. Na levels may elevate due to regurgitation and dehydration, while K+ levels may be depressed with vomiting and increase with dehydration (Doneley 2007). The statistical difference in Na
(P=. 017) is probably due to the FLB estuary and higher intake of sodium while the nestlings are fed (Table 1.6). Results for K+ (P=. 000) are difficult to interpret but may be due to fertilizer run-offs in the lake (Table 1.6). The FLB Osprey values were below
13 the ranges of Bald Eagle nestling studies (Redig et al. 1983, Bowerman et al. 2000,
Mealey et al. 2004). The difference in CO2 values (P=013) is difficult to interpret between the populations. High levels of CO2 are indicative of alkalosis. There were variations when compared with the Bonelli’s Eagle (Balbontin and Ferrer 2002) and below the values of several European raptors (Polo et. al. 1992, Jenkins 1994, Stein
1998). The electrolytes result of recent studies shows more equivalency between FLB and CFL Ospreys and several global raptor species (Ferrer and Dobados-Berrios 1998,
Hollamby et al. 2004).
In healthy birds, total serum Ca is important in maintaining homeostasis, muscle and nerve conduction, blood coagulation and controls the secretion of hormones such as vitamin D3.Total serum Ca may overlook diseases related to calcium deficiencies.
Ospreys Ca levels were low in the Scottish and English nestlings (.03 mg/dl) (Meredith et al. 2012) compared to our study sites (8.9 mg/dl) and those in Germany (7.27 mg/dl)
(Muriel 2013) and in Mexico (8.19 mg/dl) (Rivera-Rodriguez and Rodriguez-Estrella
2011) (Table 1.7). Low levels of Ca are indicative of a bird afflicted with hypocalcemia.
Measuring only total serum Ca may under diagnose for birds inflicted with hypocalcemia since these values may rise when bonded with albumin. During egg formation, high serum levels of albumin inflate total serum Ca level may result in a misdiagnosis of birds with hypocalcemia (Stanford 2003). It’s now recommended to measure as two fractions: ionized as a salt and protein bound, especially with albumin (Stanford 2003).
PCV of free-ranging raptors are quite variable among the species (Hunter and
Powers 1980). Variation may be a consequence of age, sex, migrating status, nutrition, health, hydration and reproductive status (Boal et. al. 1998, Stein et al. 1998). High PCV
14 (>50%) can be indicative of dehydration while low values (<20%) can be anemia
(Harrison and Harrison 1986). Osprey nestlings PCV mean values (Table 1) were within the range (31-38%) reported for free-ranging nestling Ospreys (Rivera-Rodriguez and
Rodriguez-Estrella 2011, Meredith et al. 2012) (Table 5), Bald Eagles, Haliaeetus leucocephalus, in Florida Bay (Mealey et al. 2004) and the common kestrel (Shen et al.
2008). In contrast, results for PCV mean values for free-ranging Spanish Imperial Eagles,
Aquila adalberti, was 43% (Garcia-Montijano et al. 2002), African Fish Eagle,
Haliaeetus vocifer, was 45% (Hollamby et al. 2004) and Black Vultures, Aegypius monachus, was 49.5% (Villegas et al. 2002). High PCV volumes can be indicators of dehydration due to a xeric environment the raptors are inhabiting (Harrison and Harrison
1986). Seabirds PCV mean values ranged from 40 – 57.9 %, which are much higher and may be attributed to the marine environment (Wanless et al. 1997).
Most normal avian values for TP range between 3.0 and 5.0 g/dl. Values that fall below 2.5 g/dl may reflect parasitism, environmental stress, starvation or other diseases.
Values greater than 5 g/dl may indicate dehydration, shock or infection (Harrison and
Harrison 1986). Plasma protein levels were found to vary in female American Kestrels during prelaying and incubation (Dawson and Bortolotti 1997). Total protein mean values in this study were FLB 4.49 g/dl and CFL 3.17 g/dl and fall within the values of
Ospreys in Scotland (Meredith et al. 2012) and Mexico (Rivera-Rodriguez and
Rodriguez-Estrella 2011) (Table 5). Michigan eaglets at 3.4 g/dl and eaglets found in
CNF at 4.7 g/dl (Redig et al. 1983). FLB values were lower than those found for captive
Common Kestrels of 6.94 g/dl in Beijing, China (Shen et al. 2008) and Golden Eagles in
15 Iran 4.9 g/dl (Nazifi et al. 2008). TP values may be very distinct for each species and therefore high or low levels do not necessarily reflect a physiological issue.
Uric acid values for Osprey nestlings in Florida Bay and central Florida were comparable with FLB Bald Eagle values 13.46 mg/dl (Mealey et al. 2004) and lower than
Swallow-tailed Kite values of 14.38 mg/dl (Mealey et al. 2006) and White-tailed eagles
61.1 mg/dl (Sonne et at. 2010). Meredith et al. (2012) reported Uric acid levels of 6.5 mg/dl for Ospreys in Scotland and England. Ospreys in Germany had levels of 11.07 mg/dl (Muriel et al. 2013) and in Mexico 15.69 mg/dl (Rivera-Rodriguez and Rodriguez-
Estrella 2011). Elevated levels of uric acid in free ranging Osprey nestlings may be attributed to food stress, which may compromise the health of the kidneys (Ferrer 1993).
In India, high levels of uric acid and precipitates throughout the body of Gyps Vultures were linked to the prescription pain killer diclofenac being used in Indian cattle.
Deceased cattle treated with diclofenac were consumed by vultures resulting in kidney failure and death of these birds prompting a global concern (Naidoo and Swan 2009).
Reference values for PHOS in domestic birds are 2 to 6 mg/dl (Hochleithner
1989). The FLB and CFL Osprey mean values (Table 1) were higher than Bald Eagle nestling studies (Redig et al. 1983, Bowerman et al. 2000 and Mealey et al. 2004) and adult Spanish Imperial Eagles (5.8 mg/dl), Golden Eagles, Aquila chrysaetos, (4.7 mg/dl), Griffin Vultures, Gyps fulvus, (4.3 mg/dl) but similar with the Egyptian Vultures,
Neophron percnopterus, (7.3mg/dl) (Polo et al. 1992), and nestlings Bearded Vultures,
6.46 mmol/L, Gypaetus barbatus, (Hernandez and Margalida 2010). Phosphorus levels are a good indicator of renal function and also assists in evaluating nutritional
16 deficiencies. High values of PHOS are associated with renal disease/failure but should be used with uric values and other clinical values for an accurate diagnosis.
GLU mean levels in Ospreys in FLB and CFL are lower than Bald Eagle nestlings in Michigan (280 mg/dl) (Redig et al. 1983) but both fall within the normal range of 200 -
500 mg/dl for free-ranging birds of prey (Bowerman et al. 2000, Villegas et al. 2002).
Levels higher than 900 mg/dl are associated with diabetes and levels below 150 mg/dl are considered life threatening (Doneley 2007). GLU levels are highly variable since due to metabolic rates, body size and food intake. Prior to fledging glucose levels are augmented due to increased nest activity prior to their first flight (Muriel et al. 2013).
The results of this study are within the reported ranges for other free-ranging raptor (Table 1.8) (Mealey et al. 2006, Nazifi et al. 2008, Meredith et al. 2010, Muriel et al. 2013). Two isolated Osprey populations in Florida showed a few significant differences in their serum values but overall depicting consistency of the values within the species. Comparing these values, even though sometimes consistent with other raptor species, may be better utilized if looking within a specific species. As further serum studies evolve a more thorough understanding of raptor serum values will emerge. The consistent values become another tool for wildlife biologists and officials to incorporate into future surveys of free-ranging Ospreys.
17 Lake Istokpoga
Florida Bay
Figure 1.1. Lake Istokpoga and Florida Bay were the study sites for this project.
18 Table 1.1
Hematological Value (PCV) and Metabolic Chemistry Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida
Florida Bay Central Florida Variable N M SD N M SD
PCV (%) 66 33.06 4.72 9 32.89 2.57
TP (g/dl) 124 4.49 6.91 28 3.17 1.32
GLU (mg/dl) 124 218.31 41.5 31 232.87 31.96
PHOS (mg/dl) 120 9.06 21.3 30 7.03 3.81
URIC (mg/dl) 115 12.64 4.8 31 12.9 3.81
Table 1.2
Serum Enzymology Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida
Florida Bay Central Florida Variable N M SD N M SD
ALB (g/dl) 82 1.57 0.55 27 1.7 0.86
AST (U/L) 117 38.4 24.09 29 74.63 136.59
ALT (U/L) 109 24.2 11.66 29 22.45 29.92
ALKP (U/L) 106 462.68 211.46 27 330.78 137.24
LDH (U/L) 64 2521.33 1108.71 19 2700.16 1490.57
CK (U/L) 106 1514.05 594.73 29 1372.83 609.77
CHE (U/ml) 123 2.06 0.4 31 2.02 0.8
19 Table 1.3
Serum Electrolytes and Mineral Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida
Florida Bay Central Florida Variable N M SD N M SD
Na+(mmol/L) 115 134.21 16.01 31 127.76 28.52
K+ (mmol/L) 117 4.97 10.8 29 5.41 1.57
CL- (mmol/L) 120 104 15.8 30 101 16.9
CA++ (mg/dl) 114 8.9 2.69 31 8.97 2.49
CO2 (mmol/L) 129 20.5 5.85 31 21 5.3
Table 1.4
Blood Mercury (Hg) Values for Osprey Nestlings in Florida Bay, Everglades National Park and Lake Istokpoga in Highlands County, Florida
Florida Bay Central Florida Variable N M SD N M SD
Hg (ppm) 112 0.68 0.53 37 0.3 0.16
20 Table 1.5
Mann-Whitney U Test Results Comparing Similar Sample Sizes for FLB and CFL Osprey Nestling’s Serum Chemistry Values
Mann- Whitney U Test 97+99 FLB CFL FB vs CF N Mean SD N Mean SD P Adj. H
TP (g/L) 18 2.70 0.25 15 3.09 1.14 0.466 0.531
ALB (g/dl) 19 1.42 0.13 14 1.64 0.75 0.726 0.122
AST (U/L) 18 33.4 21.7 15 51.6 34.4 0.105 2.632
ALT (U/L) 18 25.1 11.2 14 15.6 11.6 0.009 6.790
ALKP (U/L) 17 527.2 137.5 6 386.7 101.8 0.011 6.480
LDH (U/L) 17 3216.8 1685.7 16 3919.2 1972.8 0.575 0.314
CK (U/L) 18 1593.8 606.9 16 1338.6 258.7 0.449 0.572
Uric acid (mg/dl) 17 14.20 4.42 16 12.19 3.98 0.208 1.586
Ca (mmol/L) 17 8.70 2.15 14 9.99 2.80 0.249 1.330
PHOS (mmol/L) 19 7.58 2.05 16 6.49 1.15 0.171 1.878
GLU (mmol/L) 18 231.6 12.3 16 238.4 31.8 0.908 0.013
Na+ (mmol/L) 18 139.1 5.0 14 137.4 22.4 0.017 5.704
K+ (mmol/L) 18 3.39 1.57 15 5.00 1.41 0.000 13.185
Cl- (mmol/L) 18 107.1 4.7 16 107.9 19.1 0.098 2.732
C02 (mmol/L) 18 18.4 2.8 15 22.4 5.7 0.013 6.226
CHE (U/L) 18 2.023 0.258 15 2.002 0.351 0.971 0.001
21 Total Protein (TP) Albumin (ALB)
9 5 8 4.5 4 7 3.5 6 3 l l
5 d d /
/ 2.5 g g 4 2 3 1.5 2 1 1 0.5 0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Aspartase Aminotransferase (AST) Alanine Aminotransferase (ALT)
180 60 160 50 ** 140 120 40 L
L 100 / / 30 U U 80 60 20 40 10 20 0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Alkaline Phosphatase (ALKP) Lactate Dehydrogenase (LDH)
1000 9000 900 8000 800 * ** 7000 700 6000 600
L 5000 L / / 500 U U 4000 400 300 3000 200 2000 100 1000 0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Creatinine Kinase (CK) Uric Acid (URIC)
4000 30 3500 25 3000
2500 20 l d L / / 2000
g 15 U 1500 m 10 1000 5 500
0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Calcium (Ca) Phosphorus (PHOS)
20 20 18 18 16 16 14 14 L 12 l 12 / d l / o
10 g 10 m m m 8 8 6 6 4 4 2 2 0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
22 Glucose (GLU) Sodium (Na)
400 250 350 300 200 **
250 L l
/ 150 d l / o
g 200 m m
150 m 100
100 50 50
0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Chloride (Cl) Potassium (K) 200 12 180 160 10 ** 140 120
8 L L / l / l o 100 o 6 m m m 80 m 4 60
2 40 20 0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Cholinesterase (CHE) Carbon Dioxide (CO2) * 4 40 ** 3.5 35 3 30 2.5
L 25 L / l / 2 o 20 U m 1.5 m 15 10 1 5 0.5 0 0 Total FB CF FB97+99 CF97+99 Total FB CF FB97+99 CF97+99
Figure 1.2. Serum parameter values for Osprey populations in Florida Bay (FL) and Central Florida (CFL) and south Florida (Total) for all years examined. Statistical differences between FL and CFL values were examined using a Student's t test and an asterisk (*) indicates significance (p< 0.05). For the years 1997 and 1999 (FB97+99 and CF97+99) statistical differences of serum values were examined using a Mann -Whitney U Test and a double asterisk (**) indicates significance (p< 0.05).
23 Table 1.6
Environmental Stresses as They Relate to Statistical Difference in Serum Parameters for the Osprey Populations
Mean Parameter FLB vs CFL P Value Adj. H Response Environment
ALT 25.1 vs 15.6 0.009 6.79 Tissue damage Stressed
ALKP 527.2 vs 386.7 0.011 6.48 Bone Development Unknown
CO2 18.4 vs 22.4 0.017 6.226 pH balance
K+ 3.39 vs 5.00 0 13.185 > renal disease Unknown
high salt diet NA 139.1 vs 137.4 0.013 5.704 /dehydration Estuary
24 Table 1.7
Tabulation of Hematology and Biochemistries of Nestling Ospreys from Florida Bay and Central Florida with Published Values for Osprey Nestlings
Florida Bay Central Florida Meredith Rivera- Muriel et al. et al. Rodriguez et al. Variable Mean SD Mean SD Mean SD Mean SD Mean SD
PVC (%) 33.06 4.72 32.89 2.57 40 6 29.04 6.49
TP (g/dl) 4.49 6.91 3.17 1.32 3.42 0.37 5.32 0.94 2.37 0.46
GLU (mg/dl) 218.3 41.5 232.9 31.96 246.18 31.61 326.3 50.5
PHOS (mg/dl) 9.06 21.3 7.03 3.81 2.57 1.65
URIC (mg/dl) 12.64 4.8 12.9 3.81 15.69 5.93 11.07 3.69
ALB (g/dl) 1.57 0.55 1.7 0.86 1.68 0.23
AST (U/L) 38.4 24.1 74.63 136.6 39.4 11.9 15.69 7.31
ALT (U/L) 24.2 11.7 22.45 29.92 6.74 4.84
ALKP (U/L) 462.7 211 330.8 137.2 67.01 39.97 990.6 157
LDH (U/L) 2521 1109 2700 1491 1896 501
CK (U/L) 1514 595 1373 609.8 2166 879
URIC (mg/dl) 12.64 4.8 12.9 3.81 57.23 21.9 15.69 5.93
CHE (U/ml) 2.06 0.4 2.02 0.8
CA (mg/dl) 8.9 2.69 8.97 2.49 2.84 0.18 8.19 0.96 7.27 1.67
K (mmol/L) 4.97 10.8 5.41 1.57 4.16 2.03
25 Table 1.8
Tabulation of Hematology and Biochemistries of Nestling Ospreys from Florida Bay and Central Florida with Published Values for Global Raptors
Spanish Imperial African Fish Eagles Golden Eagle Eagle White-Tailed Osprey, Central FL Osprey, Bald Eagle, FL Bay (Aquila adalberti) ( Aquila (Haliaeetus Eagle Osprey, FL Bay (Pandion haliaetus) England/Scotland (Haliaeetus (Garcia- chrysaetos) vocifer) (Haliaeetus (Pandion haliaetus) (Mealey (Pandion haliaetus) leucocephalus) Montijano et al.) Nazifi et al. (Hollamby et albicilla) (Sonne Blood Values (Mealey Unpublished) Unpublished) (Meredith et al. 2010) (Mealey et al. 2004) 2002 2008 al. 2004) et al. 2010) PCV (%) 33.06 + 4.72 32.89 + 2.57 40.0 + 6.0 32.74 + 4.16 43 + 3 47 + 0.0009 45 + 2 GLU (mmol/L) 218.31 + 41.47 232.87 + 31.96 223.03 + 27.37 279 + 18 16.42 + 0.73 12.4 + 2.01 15.8 PHOS (mmol/L) 9.06 + 21.31 7.03 + 3.81 6.31 + 1.3 4 + 1.0 1.73 + 0.08 0.74 + 0.30 TP (g/L) 4.49 + 4.72 3.17 + 1.32 34.15 + 3.73 3.28 + 0.98 3.6 + 0.33 4.9 + 1.35 3.6 + 0.4 2.76
Uric (mg/dl/) 12.64 + 4.8 12.9 + 3.81 572.3 + 219.5 (mmol/L) 13.46 + 5.88 3.07 + 1.78 457.67 + 97.46 0.998 + 0.408 61.1 ALB (g/L) 1.57 + 0.55 1.7 + 0.86 16.85 + 2.31 1.48 + 0.43 20.46 + 0.79 12 + 1.3 1.27
ALKP (U/L) 462.68 + 211.46 330.78 + 137.24 147.6 + 51.96 1247 AST (U/L) 38.4 + 24.09 74.63 + 136.59 39.40 + 11.90 132.73 + 48.04 278 + 65 194 + 117 ALT (U/L) 24.2 + 11.66 22.45 + 29.92 17.11 + 7.41 28.21 + 2.36 15 Ca (mmol/L) 8.9 + 2.69 8.97 + 2.49 2.84 + .18 9.39 + 2.24 11.9 + 1.7 2.37 + 0.24 2.4 + 0.13 2.45 CHE (U/L) 2.06 + 0.4 2.02 + 0.8 1.29 + 0.31 1.24 + 319
CK (U/L) 1514.05 + 594.73 1372.83 + 609.77 2165.6 + 879.1 1268.71 + 557.69 288 + 119 217 + 53
LDH (U/L) 2521.33 + 1108.71 2700.16 + 1490.57 1895.8 + 500.5 2547.63 + 965.22 713 + 166 1209.89 + 21.73 CRSC (umol/L) 0.24 + 0.11 53.27 + 3.87 TBIL (umol/L) 1.24 + 1.06 16 + 9.9-26
BUN (mmol/L) 13.41 + 10.79 2.74 + 0.17
Na+ (mmol/L) 134.21 + 16.01 127.76 + 28.52 135.85 + 11.13 154 + 5 153 + 5.56 152 + 150-156 Cl- (mmol/L) 104 + 15.8 101 + 16.9 104.98 + 10.11 115 + 5.21
K+ (mmol/L) 4.97 + 10.8 5.41 + 1.57 4.28 + 1.82 3.4 + 1.2 1.3 + 0.33 2.9 + 0.75-3.03 C02 (mmol/L) 20.5 + 5.85 21 + 5.3 18.9 + 4.79
Cholesterol (mg/dl) 4.94 + 0.94 (mmol/L) 2.14 + 0.09 4.69 + 0.644 50
6
II. COMPARING AND INTERPRETING SERUM CHEMISTRY OF NESTLING
BALD EAGLES (HALIAEETUS LEUCOCEPHALUS) AND OSPREYS (PANDION
HALIAETUS) IN FLORIDA BAY, EVERGLADES NATIONAL PARK
The levels of several chemical compounds in the blood can be used in the diagnosis of the health status of avian species (Gelli et al. 2009). Documenting normal serum levels can also contribute in resolving enigmatic environmental events as was suspected in several recent die-offs old world vultures (Naidoo et al. 2009) and other raptor species (Di Silvestro 1996). It’s often presumed by veterinarians that avian groups such as raptors share similar blood values. Since free ranging serum values published data is still forthcoming, veterinarians are assuming closely related species are similar until there are more publications proving otherwise.
Establishing and comparing values for the serum chemistries of free ranging birds of prey will be important in order to decipher the values of a species (Sarasola et al.
2004). Discerning the significance of serum chemistry values must be done with prudence since age, sex, nutritional status and environmental conditions, circadian rhythms and plasma and serum storage methods may influence these values (Boal et al.
1998). Until a more complete database has been established for avian serum chemistries and their application as a monitoring tool in free-ranging raptors, these values should be used in combination with complementary ecological data when making raptor management assessments (Gelli et al. 2009).
27 The Osprey and Bald Eagle nesting pairs on the eastern side have declined significantly over the last 10 years (Bowman et al. 1989, Baldwin et al. 2012). The cause is unknown but ecosystem compromise and human intrusion from the Florida Keys are prime suspects. The proximity of the Florida Keys tourism and easy park access creates constant pressure on the local resources. The flow of boat traffic around the nesting keys may have deleterious effects on reproduction. The disturbance increases during the nesting season, our winter months the peak period of tourism in the Florida Keys.
This investigation compared statistical parameters for the blood serum chemistries of free ranging Bald Eagle and Osprey nestlings in Florida Bay, Everglades National
Park. My question was to determine if serum values differ between these two avian species. Comparing nestling Bald Eagles and Ospreys was an innovative comparison and a first attempt at deciphering the conundrum of avian serum values. The study will also establish serum baseline values for the nestling Ospreys in Florida Bay. Comparing the serum values of the species will assist in identifying if serum values are species specific or do the values overlap among species sharing the same ecosystem.
Methods
Study Site - The Florida Bay estuary lies between the southern portion of the
Florida peninsula to the north, the Florida Keys to the east and south and the Gulf of
Mexico to its west. It covers approximately 2200 square kilometers and lies within the boundaries of the Everglades National Park (Figure 1). East Florida Bay will be the region east of Big Key and West Florida Bay is designated as the region west of Big Key.
I eliminated the central area of Florida Bay due to low or non-existing nesting pairs in the area (Boyer et al. 1997).
28 Ageing and Sexing - Approximately 20 nests containing 10 eaglets and 30 nests containing 20 Osprey nestlings from 35 to 45 days old were visited annually from 1
January through 1 May from 1992 through 2007. Nestling development is monitored chronologically or through feather formation by way of repeated nest visits (Bortolotti
1984). Avian Biotech International, Tallahassee, Florida 32312, did the bird’s sex determination genetically. The nests were surveyed three times for ageing, sampling and evaluation. Each nest was visited only once for blood sampling. Approximately 15 Bald
Eagle nests and 30 Osprey nests were surveyed and sampled annually. Blood Samples.
Blood sampling, when possible, was conducted primarily in the mornings. Tides and weather play an extremely significant role when attempting to reach the islands.
Circadian rhythms were considered prior to sampling but occasionally the window within a ten-day period to reach an island is extremely narrow and therefore samples were taken opportunistically. Nestlings were hooded with a traditional falconry hood manufactured by Northwoods, Inc P.O. Box 874, Rainier, WA, 98576 and removed from the nests by the investigators. Blood was extracted from the brachial vein (Cooper 1985). The area surrounding the vein was cleaned with 70% isopropyl alcohol and a sterile 22, 23 or 25- gauge needle attached to a 3-ml syringe, manufactured by Becton Dickinson $ Co., was used to extract 1 - 3 ml of blood from each nestling. All blood extraction sites had pressure applied and observed for approximately 5 minutes post procedure to insure proper clotting prior to placing the nestling back into the nest. Nests were revisited approximately 7-10 days post sampling, when possible, to re-evaluate the nestlings’ condition. The eaglets defensive posturing with wings open allowed us to view the sampling area.
29 Blood samples were placed in small 1-ml red top plastic microtainer tubes with a serum separator, manufactured by Becton Dickinson & Co., and a heparinized, anti- clotting agent, hematocrit tubes, made by Jorgensen Laboratories, Inc. Blood for serum analysis was allowed to clot for 15 minutes prior to centrifugation. The clotting allows for molecule separation during centrifugation of the plastic blood container. Packed cell volume (PCV) was determined through the centrifugation of the heparinized hematocrit tubes. Samples were spun for approximately 20 minutes with a portable Mobilespin centrifuge manufactured by Vulcan Technologies, 718 Main, Grandview, MO 64030, with a relative centrifugal force of 1100-x g. Centrifuging was completed when the serum separator was distinctly walled off the serum from the red blood cells. The serum was transferred with a pipette to another blood tube to prevent hemolysis. Field samples were placed in an ice cooler and later frozen. Samples were stored at –16.1oC in a
Kenmore, Sears Roebuck Co., Joinville, SC freezer and analyzed within 30 days.
Serum Samples - Eaglet and Osprey sample sizes will vary for each serum chemistry test depending on the amount of serum available (Table 1). One hematological, packed cell volume (PCV) and nineteen serum chemistries was determined including: total protein (TP), albumin (ALB), aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALKP), lactate dehydrogenase (LDH), creatine kinase (CK), uric acid (URIC), calcium (CA2+), phosphorus (PHOS), glucose
(GLU), total bilirubin (TBIL), blood urea nitrogen (BUN), creatinine (CRSC), sodium
+ + - (NA ), potassium (K ), chloride (CL ), carbon dioxide (CO2) and cholinesterase (CHE).
Blood samples were analyzed on a Kodak Ektachem DT II System. Analysis and methodology followed the protocol in the Johnson & Johnson Ektachem DT II System
30 manual. Ektachem controls were run once a week to assure quality analysis control with all samples.
Statistical Analysis - Serum chemistry results were analyzed and compared between Bald Eagles and Ospreys territories in eastern and western Florida Bay. In the discussion several serum chemistries were converted from micromoles/L to mg/dl to assist in establishing relationship between our units (McConnell 1998-2000) and those of foreign countries. Statistical parameters were analyzed through several statistical software programs. Approximately 160 samples were tested for nineteen serum chemistries. Mean and standard deviations statistical values were analyzed using JMP
SAS statistical discovery software (JMP 2003). The Mann-Whitney U test was conducted to compare serum values between the groups using the Handbook of
Biological Statistics (McDonald 2009).
This investigation was conducted under the guidelines of IACUC, U.S.
Department of the Interior (USDI), National Park Service permit number EVER-2010-
SCI-0009, USDI Bird Banding Laboratory Master Bander Permit number 22418 and
State of Florida Fish and Wildlife Conservation Commission permit number WB03367b
(Appendix A).
Results
Approximately 51 to 87 blood samples (Table 2.3) were analyzed from nestling
Ospreys and 44 to 83 blood samples for Bald Eagles in Florida Bay during 1992 through
2007 (Table 2.2). The number of samples analyzed varied due to the quantity of blood collected and the inability of the analyzer to read low and high results due to its preset ranges. Our blood sampling studies did not appear to have visible adverse affects on the
31 health or fledging of the nestlings. The sampling area was devoid of markings and infections confirming the effectiveness of this blood sampling technique. Osprey and
Bald Eagle nestling inactivity lasted for approximately 20 minutes after the sampling technique. Parents, primarily the female, were very diligent in returning to the nest within a few minutes of our departure.
Sample size, mean values and standard deviations for the Bald Eagle (Table 2.2) and Osprey population are shown in Table 2.3. Mann-Whitney U test (MWT) (Table
2.4) was conducted on serum values between the Osprey and Bald Eagle populations in
Florida Bay. Summary of the serum values are shown through Box and Whisker Plots in
Figure 2.2. There were no significant differences in the PCV, GLU, LDH, PHOS, or K+ values between the species. There were significant differences (p < 0.05) between the populations. Bald Eagle serum values were higher for TP (H=17.833, P=.00002), ALB
(H=7.449, P=.006), AST (H=113.153, P =.0001), and CA (H=7.148, P = 008). Osprey serum values were higher for ALT (H=11.824, P = 0.0005), ALKP (H=105.5, P = .0001),
CK (H=13.465, P = 0.0002), C02 (H=4.443, P = 0.035), and CHE (H=99.3, P=.0001) .
The Osprey population was divided into the eastern and western populations
(Table 2.5). Samples sizes are similar between the areas and range from 66-84 individuals for serum chemistry analysis. There was a significant difference in four serum values between the eatern and western FLB Osprey populations. The eastern
Osprey population showed increased serum values for PCV (H=4.613, P = 0.032), ALT
(H=14.98, P = 0.0001),CK (H=6.707, P = 0.009), and the western Osprey population had one higher serum value for K (H=7.544, P=.006) (Table 2.6, Figure 2.3). There were no differences in the remaining serum values between the FLB eastern and western regions.
32 Bald Eagles serum values were compared using results from eastern Florida Bay and western Florida Bay (Table 2.8). Samples sizes were smaller for eastern Florida Bay
(N=57) due to a smaller Bald Eagle nesting population. Serum value was higher (P <
0.05) for K (H=5.266, P=.022,) in the eastern region of FLB (Table 2.9, Figure 2.4).
There we no significant differences between the remaining serum values.
Discussion
Comparing serum chemistry results of two free ranging species sharing the same ecosystem during the same period of time has not been mentioned in the literature. Many of the published studies result from captive animals, which may not reflect free ranging values of the species (Olsen et al. 2001). Captive wildlife serum results are very useful in maintaining standards as health assessment parameters for captive animals fed a very particular diet (Table 2.1). Free ranging species have a more opportunistic variable diet, which may result in different values (Power and Pokras 1994).
The Bald Eagles had significantly higher values (p < 0.05) for TP, ALB, AST, and Ca, while Osprey values were higher for ALT, ALKP, CK, , C02 and CHE (Table
2.4). Table 2.11 compares the Bald Eagles aan Ospreys in this study with other published raptor values in the literature.. Serum values differences in Florida Bay between the species nestlings appear to be species specific.
The East and West Osprey populations in Florida Bay showed significant differences in the following chemistries: PCV (H=4.613, P= 0.032), ALT (H=14.988, P =
.0001), CK (H=6.707, P=0.0096) and K (H=7.544, P=0.006) . PCV levels are associated with dehydration and possibly anemia (Ferrer et al. 1987) (Table 2.7). The difference in
CK levels of the nestlings may be associated with stress levels and these may be a result
33 of handling during sampling, excessive activity and a combination of environmental deterioration on the eastern side of the Bay (Muriel et al. 2013). The different values of
ALT (H=14.988, P=. 0001) in eastern Osprey nestling may signify low levels of food available for parents to feed their young. Bald Eagle nestlings in Florida Bay (east vs west) have only one statistical difference in serum values, K (H=5.266, P=. 022). Plasma
K is known to lower with increased physical and muscular activity and therefore nestlings may be susceptible to the increased disturbance by naïve boaters (Wolf et al.
1985) (Table 2.10).
Studies involving avian biochemistries are becoming more prevalent in the literature. Raptor biologists and wildlife veterinarians must also be aware that values among adults, juveniles and nestlings may vary significantly (Boal et al. 1998). The data was used to establish baseline parameters of free-ranging Osprey and Bald Eagle nestlings in the Florida Bay. The results of this study appear to fall generally within the reported ranges for other free-ranging raptor nestlings (Balbontin and Ferrer 2002).
PCV of free-ranging raptors are quite variable and may be a consequence of age, sex, migrating status and reproductive status (Mauro 1987). Osprey and Bald Eagle nestlings PCV mean values (Table 2.4) were within the range (31-38%) reported for free- ranging Swallow-tailed Kite (Elanoides forficatus) nestlings (34%) in Florida and free- ranging nestling Bald Eagles (34%) in Chippewa National Forest (Redig et al. 1983,
Mealey et al. 2006). In contrast, results for PCV mean values for free-ranging nestling
Cooper’s Hawks (Accipiter cooperii) was 42.2 % for females and 38.7% for males (Boal et al. 1998). Seabirds PCV mean values ranged from 40 – 57.9 %, which are much higher
34 than the raptor species and may simply due to their physiological difference(Work et al.
1996, Wanless et al. 1997, Padilla et al. 2006).
Most normal avian values for total protein range between 3.0 and 5.0 g/dl. Values that fall below 2.5 g/dl may reflect parasitism, stress or starvation. Values greater than 5 g/dl may indicate dehydration, shock or infection (Harrison and Harrison 1986). Plasma protein levels were found to vary in female American Kestrels (Falco sparverius) during prelaying and incubation (Dawson and Bortolotti 1997). Total protein mean values in this study were Osprey 4.49 g/dl and Bald Eagles 3.32 g/dl and fall within the values of
Michigan eaglets at 3.4 g/dl and eaglets found in CNF at 4.7 g/dl (Redig et al. 1983). The
Osprey values are also similar to free ranging Iranian Golden Eagles (Aquila chrysaetos)
(4.97 g/dl), Swallow-tailed Kites (4.34 g/dl) and the Saker Falcon (Falco cherrug) (4.3 g/dl) (Samour and D’Aloia 1996, Mealey et al. 2006, Nazifi et al. 2008). Bald Eagle nestlings TP values were similar to the Eurasian Buzzard (Buteo buteo) (3.84 g/dl) (Gelli et al. 2009). The Osprey and Bald Eagle nestling values are considerably lower than captive Chinese Common Kestrel, (Falco tinnunculus) (6.96g/dl) (Shen et al. 2008).
Free-ranging diverse diets affects on serum values may be significantly different than a more specific captive diet. Uric values for Osprey (12.64 mg/dl) and Bald Eagle (13.78 mg/dl) nestlings in Florida Bay were similar to Osprey nestling values (12.9 mg/dl) in
Central Florida and Scotland (10.3 mg/dl) (Meredith et al. 2010). These values were lower than Swallow-tailed Kite values (14.38 mg/dl) and Argentina’s Swainson Hawks
(Buteo swainsoni) (males 59.0 mg/l and females 64.7 mg/l) (Sarasola et al. 2004, Mealey et al. 2006). High levels of uric acid in free ranging Osprey nestlings may be attributed to food stress (Ferrer 1993). GLU mean levels in Ospreys (210. 33 mg/dl) and Bald Eagles
35 (225.93 mg/dl) varied statistically as a species in Florida Bay but are lower than Bald
Eagle nestlings in Michigan (280 mg/dl) but both fall within the normal range of 200 and
500 mg/dl for captive birds. Osprey electrolytes results for Na+, K+ and Cl- in Florida Bay were below the ranges of Bald Eagle nestling studies (Redig et al. 1983, Bowerman et al.
2000). Bald Eagle (135.88 mmol/L) and Osprey (131.4 mmol/L) mean Na+ levels were below levels reported for swallow-tailed Kites (144.73 mmol/L) (Mealey et al. 2006).
There were variations when compared with the Bonelli’s Eagle (Aquila fasciata)
(Balbontin and Ferrer 2002) and below the values of several European raptors
(Heidenreich 1997, Balbontin and Ferrer 2002). Potassium levels were higher in Florida
Bay nestlings than in Swallow-tailed Kites nestlings (3.28 mmol/L) (Mealey et al. 2006).
LDH levels even though not specific for organ disease are useful in evaluating muscle fitness (Meredith et al. 2010). High variation of CK and LDH levels in this study may be due to the handling and physiology of nestling Ospreys and Bald Eagles and are similar with the results found in free-living Bonelli’s Eagle, Booted Eagle (Hieraaetus pennatus) and the Spanish Imperial Eagle (Aquila adalberti) (Polo et al. 1992, Balbontin and Ferrer 2002, Casado et al. 2002). Florida Bay’s Osprey CK mean values 1514.05
U/L were significantly higher (p = .001) than Bald Eagle nestling’s mean values of
1268.71 U/L but similar to Central Florida Osprey values (1372.83 U/L) but lower than samples from Scotland/England (2165.6 U/L) (Meredith et al. 2010). CK mean values for great frigate birds (Fregata minor) (536 U/L), red-footed boobies (Sula sula) (940.1
U/L), Nazca boobies (Sula granti) (871.8 U/L) and swallow-tailed Gulls (Creagrus furcatus) (263.3 U/L) were considerably lower than the Florida Bay nestlings (Padilla et al. 2006). Golden eagles LDH means (1,209.89 U/L) in Iran and Ospreys from Scotland
36 and England were comparable to the Florida Bay Bald Eagle and Osprey nestling levels
(Nazifi et al. 2008, Meredith et al. 2010). Increased CK values for domestic species have been associated with lead poisoning, chlamydiosis and bacterial septicemias (Heatley and
Jowett 2000).
CHE levels < .9 u/ml are considered clinically depressed and likely due to intoxications (Porter 1993, Heatley 2000). CHE mean values for Florida Bay Ospreys was 2.06 U/ml and Florida Bay Bald Eagles were 1.3 U/ml and for Florida swallow-tailed kites were 0.8 U/ml and peregrine falcons (Falco peregrinus) 2.29 U/ml (Lumeij et al.
1998). There is controversy in using CHE as an indicator for exposure to an organophosphate pesticide due to the variations in CHE levels over a short period of time
(P. Mineau pers. comm.).
Reference values for PHOS in domestic birds is 2 to 6 mg/dl (Harrison and
Harrison 1986). The Florida Bay Osprey and Bald Eagle mean values (Table 1) were higher than Spanish imperial eagles (5.8 mg/dl), golden Eagles (4.7 mg/dl), griffin vultures (4.3 mg/dl) but similar with the Egyptian vultures (Neophron percnopterus)
(7.3mg/dl) (Polo et al. 1992).
ALKP is an enzyme used to evaluate avian bone growth and liver function. Serum values of ALKP are quite different and may be related to age (Heatley and Jowett 2000).
Mean results free-ranging Osprey nestlings (462.68 U/L) from Florida Bay were higher than Central Florida Osprey population (330.78 U/L) and were significantly higher (t =
3.08, p = .001) than Bald Eagle nestlings in Florida Bay (147.5 U/L). Results from eaglets in Michigan (449 U/L), Spain (2148 UI /L-1) (Ferrer and Dobado-Berrios 1998,
37 Balbontin and Ferrer 2002) Florida Bay Bald Eagles nestlings and falcons (20-193 U/L)
(Lumeij et al. 1998) confirm the wide range of ALKP serum values.
Recent declines in avian populations are exposing environmental toxins, which are affecting levels of alkaline phosphatase (ALKP), uric acid and alanine aminotransferase (ALT) in several raptor species (Lumeij et al.1998, Oaks et al. 2004).
The use of diclofenac, an anti-inflammatory drug in cattle in India, precipitated a global alarm when large numbers of vultures were found incapacitated or dead (Naidoo and
Swan 2009). Old world vulture were extremely sensitive to diclofenac and resulted in a
95% population decline in the Oriental white-backed vulture, (Gyps bengalensis), and catastrophic declines involving, long-billed vulture, (Gyps indicus) and slender-billed vulture, (Gyps tenuirostris) (Swan et al. 2006, Nazifi et al. 2008). The death was associated with the vultures scavenging on the remains of dead cattle. Establishing serum chemistry profiles for these vultures became a priority in order to determine the effects of diclofenac on the organ systems of the vultures (Swarup et al. 2007).
The feasibility of incorporating serum chemistries values from nestling raptors as health monitors for free ranging raptors will be difficult due to the wide range of the serum results. Populations of Bald Eagles and Ospreys have both declined in eastern
Florida Bay since the 1990’s. Serum values results for the eastern side of Florida Bay do not identify any health issues that would explain the population decline from the area.
Even though I infer that some of the serum differences between the eastern and western side may be related to stressed nestlings, this does not necessarily indicate a certainty.
Their application as a monitoring tool in free-ranging raptors should be combined with
38 complementary ecological data when making wildlife management assessments
(Newman et al., 1997, Nazifi et al. 2008).
Figure 2.1. Satellite view of Florida Bay identifying eastern and western Florida Bay as the study site.
39 Table 2.1
Defining The Serum Chemistry Parameters and Their Application to Ecological Field Studies
Serum Units Meaning Response in Birds Physiology
Tissue damage may cause hemolysis, which elevates Increase due to tissue ALT. Aging increases ALT U/L Various tissues damage activity.
Energy source in the case of exhaustion of Limited albumin decreases glycogen and lipid Starvation decreases oncotic pressure, which ALB mg/dl reserves." concentration leads to edema.
Enzyme enables ion Juvenile bone Dephosphorylation of ATP translocation, bone development and laying for osteoblast activity development and hens correlates with results in elevated ALKP U/L reproductive activity. elevation. concentration.
Enzyme found in various tissues (Report usually paired with creatine Increase when exposed to Elevated response to AST U/L kinase) toxin hepatic damage.
Increase when Elevated urea dehydrated; abnormal concentration due to values may indicate renal reabsorption of water from BUN mg/dl Protein catabolism disease dehydration.
Component in bones, membranes, nerves and female reproductive Increase in reproductively Calcium is a vital CA mg/dl system. active female component of eggshells.
Carbon dioxide and bicarbonate work Metabolic alkalosis interchangeably in a buffer CO2 mmol/L PH balance increases CO2 levels system.
“Extracellular anion, osmotically active Maintains acid base CL mmol/L constituent of plasma” Increase with dehydration balance.
40 Table 2.1 continued
Serum Units Meaning Response in Birds Physiology
As cholinesterase is Elevation due to toxins inhibited, acetylcholine Hydrolyze and inactivate from pesticides. Used to builds up in the synapse acetylcholine to acetic monitor organophosphate and leads to disrupted CHE U/ml acid and choline and carbamate exposure. nerve functions.
Enzyme dephosphorylates phosphocreatinine to form Enzyme, which enables Increase with muscle ATP for muscle CK U/L muscle contraction. activities, mainly damage. contraction.
Catalyze the transfer of gamma glutamyl amino Failure to breakdown group. Found in brush protein enzyme in liver borders of biliary and Elevation may indicate causes elevated GGT U/L renal tubule epithelium liver disease concentration.
Diabetes mellitus and stress are seen with hyperglycemia. Indications Increase after meals. of polydipsia, polyuria and Higher concentration seen weight loss are signs of GLU mg/dl Primary energy source in juveniles. diabetes mellitus.
Increase with liver, Nonspecific avian muscle, cardiac damage Elevated concentration in LDH U/L enzyme (poor indicator) damaged organ system.
PCV % Hematocrit Dehydration/anemia Renal failure/infection
Phosphorous works High concentration inversely with Calcium. Major component of associated with renal Inhibits calcium when in PHOS mg/dl bone and energy. disease. high concentration.
Failure of renal system to Elevated concentration excrete potassium or Electrolyte found within with renal and adrenal acidosis increases K mmol/L cells disease; hemolysis concentration.
41 Table 2.1 continued
Serum Units Meaning Response in Birds Physiology
"Determine extracellular Dehydration allows for volume fluid and osmotic Increase with high salt sodium elevation in NA mmol/L pressure" diet or dehydration medulla to retain water.
Globulin levels in females Starvation decreases are elevated with the rise Protein synthesis and concentration; elevated in of estrogen hormone prior TP mg/dl degradation females for egg laying to egg laying.
Starvation induces protein Starvation increases catabolism. Renal concentration elevated damage keeps uric acid levels may indicate renal from leaving the URIC mg/dl Protein catabolism damage. individual.
42 Table 2.2
Mean Blood Serum Values for Bald Eagles in Florida Bay, Everglades National Park
FB 1993-2001 BAEA
FB Parameter 1993-2001
N Mean SD Range 95% CI
PCV (%) 61 33.3 4.50 17-42 32.2-34.5
TP (g/L) 79 3.34 1.07 2.0-10.4 3.10-3.58
ALB (g/dl) 66 1.57 0.34 1.0-3.2 1.48-1.65
AST (U/L) 76 136.8 49.49 46-357 125.5-148.1
ALT (U/L) 69 17.62 7.73 4.0-42.0 15.8-19.5
ALKP (U/L) 74 151.0 49.9 46-322 139.4-162.6
LDH (U/L) 44 2669.4 1087.0 1136-7479 2338.9-2999.9
CK (U/L) 69 1235.0 493.5 476-2906 1116.4-1353.5
Uric acid (mg/dl) 74 13.8 5.7 3.0-30.0 12.5-15.1
Ca (mmol/L) 80 9.52 1.86 2.2-17.4 9.10-9.93
PHOS (mmol/L) 75 6.57 1.19 4.1-9.7 6.29-6.84
GLU (mmol/L) 82 225.7 25.8 162-284 220.0-231.3
Na+ (mmol/L) 82 137.7 10.0 99-164 135.6-139.9
K+ (mmol/L) 83 4.09 1.68 2.2-9.7 3.73-4.46
Cl- (mmol/L) 81 106.3 8.5 72-127 104.4-108.2
C02 (mmol/L) 73 19.0 4.7 9.0-34.0 17.9-20.1
CHE (U/L) 82 1.291 0.288 0.59-2.51 1.228-1.354
43 Table 2.3
Mean Blood Serum Values for Ospreys in Florida Bay, Everglades National Park
OSPR
FB 1993-2001
N Mean SD Range 95% CI
PCV (%) 52 33.19 4.75 24-44 31.87-34.51
TP (g/L) 84 2.97 1 2.00-8.40 2.75-3.19
ALB (g/dl) 56 1.44 0.23 1.0-2.4 1.38-1.50
AST (U/L) 79 35.5 18.2 4.0-93.0 31.5-39.6
ALT (U/L) 78 24 11.5 4.0-55.0 21.4-26.6
ALKP (U/L) 75 461.4 137.3 130-863 429.8-493.0
LDH (U/L) 51 2567.2 1171.4 984-8285 2237.8-2896.7
CK (U/L) 73 1546.4 583.8 494-3132 1410.2-1682.6
Uric acid (mg/dl) 82 12.87 4.79 4.2-27.2 11.81-13.92
Ca (mmol/L) 78 8.87 2.16 3.8-17.2 8.39-9.36
PHOS (mmol/L) 83 7.23 2.55 1.7-19.0 6.68-7.79
GLU (mmol/L) 87 221.8 36.5 115-324 214.0-229.6
Na+ (mmol/L) 82 136.4 10.1 103-164 134.2-138.6
K+ (mmol/L) 82 3.96 2.04 1.1-10.8 3.51-4.41
Cl- (mmol/L) 83 105.4 10.1 71-136 103.2-107.6
C02 (mmol/L) 85 20.7 5.9 6.0-38.0 19.5-22.0
CHE (U/L) 84 2.061 0.346 0.99-2.94 1.986-2.136
44 Packed Cell Volume Total Protein (TP) Albumin (ALB) (PCV) 12 3.5 * 50 * 3 45 10 40 2.5 35 8 2 30 6 g/dl g/L % 25 1.5 20 4 15 1 10 2 0.5 5 0 0 0 BAEA OSPR BAEA OSPR BAEA OSPR
Aspartate Alanine Alkaline Phosphatase Aminotransferase Aminotransferase (ALT) (ALKP) (AST) 60 1000 400 900 * 50 * 800 * 350 700 300 40 600 250 30 500 U/L 200 U/L
U/L 400 150 20 300 100 10 200 50 100 0 0 0 BAEA OSPR BAEA OSPR BAEA OSPR
Lactate Dehydrogenase Creatine (CK) Uric Acid (URIC) (LDH) 3500 * 35 9000 3000 30 8000 7000 2500 25 6000 2000 20 5000 U/L
1500 mg/dl 15 U/L 4000 3000 1000 10 2000 500 5 1000 0 0 0 BAEA OSPR BAEA OSPR BAEA OSPR
Calcium (Ca) Phosphorus (PHOS) Glucose (GLU)
20 20 350 18 * 18 300 16 16 14 14 250
12 12 200 10 10 150 mmol/L 8 mmol/L 8 mmol/L 6 6 100 4 4 50 2 2 0 0 0 BAEA OSPR BAEA OSPR BAEA OSPR
45 Sodium (Na) Potassium (K) Chloride (Cl)
180 12 160
160 140 10 140 120 120 8 100 100 6 80 80 mmol/L mmol/L mmol/L 60 60 4 40 40 2 20 20 0 0 0 BAEA OSPR BAEA OSPR BAEA OSPR
Carbon Dioxide (CO2) Cholinesterase (CHE)
40 3.5
35 * 3 * 30 2.5 25 2 20 U/L 1.5 mmol/L 15 1 10
5 0.5
0 0 BAEA OSPR BAEA OSPR
Figure 2.2. Serum parameter values for Bald Eagles and Osprey populations in Florida Bay (FL) for all years examined. Statistical differences between Bald Eagles and Ospreys values were examined using a Mann-Whitney U Test and an asterisk (*) indicates significance (p< 0.05).
46
Table 2.4
Mann-Whitney U Test Results Comparing Ospreys and Bald Eagle Blood Serum Values in Florida Bay
Mann- Whitney U BAEA OSPR Test
FB FB 1993- 1993- BAEA VS Parameter 2001 BAEA BAEA 2001 OSPR OSPR OSPR
N Mean SD N Mean SD P<.05 Adj. H
TP (g/L) 79 3.34 1.07 84 2.97 1 0.00002 17.833
ALB (g/dl) 66 1.57 0.34 56 1.44 0.23 0.006 7.449
AST (U/L) 76 136.8 49.49 79 35.5 18.2 2.00E-26 113.153
ALT (U/L) 69 17.62 7.73 78 24 11.5 0.0005 11.824
ALKP (U/L) 74 151.0 49.9 75 461.4 137.3 9.43E-25 105.5
CK (U/L) 69 1235.0 493.5 73 1546 583.8 0.0002 13.465
Ca (mmol/L) 80 9.52 1.86 78 8.87 2.16 0.008 7.148
C02 (mmol/L) 73 19.0 4.7 85 20.7 5.9 0.035 4.443
CHE (U/L) 82 1.291 0.288 84 2.061 0.346 2.1699E-23 99.3
47
Table 2.5
Mean Blood Serum Values for Osprey in Eastern Florida Bay and Western Florida Bay
East West
Variable N M SD N M SD
PVC % 43 32.66 4.75 36 33.38 4.72
TP mg/dl 62 2.95 1.11 66 5.8 9.25
ALB mg/dl 41 1.62 0.61 41 1.51 0.49
TBIL mg/dl 14 1.54 2.05 15 2.4 3.23
AST U/L 62 42.65 25.48 59 34.61 21.43
ALT U/L 59 28.02 11.95 51 20.61 9.92
GGT U/L 7 13.86 3.63 8 65.25 142.25
ALKP U/L 54 460.56 138.44 55 468.67 262.07
LDH U/L 27 2,871.78 1,402.86 37 2,265.59 755.32
CK U/L 54 1,659.87 555.73 52 1,364.98 581.86
URIC mg/dl 60 12.74 4.83 58 12.59 4.76
BUN mg/dl 28 7.94 6.75 23 7.39 3.34
CA mg/dl 58 8.85 2.53 60 8.8 2.84
PHOS mg/dl 61 7.13 2.36 63 10.69 29.34
GLU mg/dl 65 221.3 40.22 63 213.73 42.25
NA+ mmol/l 61 133.72 10.7 58 133.92 20.27
K+ mmol/l 63 4.28 1.72 54 5.6 14.89
CL- mmol/l 62 104.66 19.14 62 102.08 15.54
CO2 mmol/l 63 20.35 5.31 62 21.41 6.63
CHE U/ml 64 2.06 0.38 62 2.03 0.41
48 Albumin (ALB) Packed Cell Volume (PCV) * Total Protein (TP)
4.5 50 9 4 45 * 8 40 7 3.5 35 6 3 30 5 2.5 %
25 g/dl g/dl 4 2 20 3 1.5 15 1 10 2 5 1 0.5 0 0 0 OSPR East OSPR OSPR OSPR OSPR OSPR West East West EAST WEST
Aspartase Aminotransferase Alanine Alkaline Phosphatase (AST) Aminotransferase (ALT) (ALKP)
200 1000 180 900 160 800 140 700 120 60 * 600 100 50 500 U/L 80 40 U/L 400 30
60 U/L 300 40 20 200 20 10 100 0 0 0 OSPR OSPR OSPR OSPR OSPR OSPR EAST WEST EAST WEST EAST WEST
Lactate Dehydrogenase Creatinine Kinase (CK) Uric Acid (URIC) (LDH) 3500 * 30 9000 3000 25 8000 2500 7000 20 6000 2000 5000 15 U/L
1500 mg/dl U/L 4000 10 3000 1000 2000 500 5 1000 0 0 0 OSPR OSPR OSPR OSPR OSPR OSPR EAST WEST EAST WEST EAST WEST
Calcium (Ca) Phosphorus (PHOS) Glucose (GLU)
25 20 350 18 300 20 16 14 250 15 12 200 10
mg/dl mg/dl 150
mmol/L 10 8 6 100 5 4 50 2 0 0 0 OSPR OSPR Total FB OSPR OSPR EAST WEST EASTWEST
Sodium (Na) Potassium (K) Chloride (Cl)
180 12 250 160 * 10 140 200 120 8 150 100 6 80
mmol/L mmol/L mmol/L 100 60 4 40 2 50 20 0 0 0 Total FB OSPR OSPR OSPR OSPR EAST WEST EAST WEST
49 Carbon Dioxide (CO2) Cholinesterase (CHE)
40 4 35 3.5 30 3 25 2.5
20 % 2
mmol/L 15 1.5 10 1 5 0.5 0 0 Total FB OSPR OSPR EAST WEST
Figure 2.3. Serum parameter values for Osprey populations in eastern and western Florida Bay (FL) for all years examined. Statistical differences between regions were examined using a Mann-Whitney U Test and an asterisk (*) indicates significance (p< 0.05).
50 Table 2.6
Results for the Mann-Whitney U Test Comparing Ospreys Blood Serum Values for Eastern and Western Florida Bay
Mann- Whitney U OSPR Test OSPR East West FB 1993- FB 1993- EAST VS Parameter 2001 2001 WEST N Mean SD N Mean SD P<.05 Adj. H
PCV (g/L) 43 32.66 4.75 36 33.38 4.72 0.032 4.613
ALT (U/L) 59 28.02 11.95 51 20.61 9.92 0.0001 14.988
CK (U/L) 54 1,659.87 555.73 52 1,364.98 581.86 0.0096 6.707
K (mmol/L) 63 4.28 1.72 54 5.6 1.89 0.006 7.544
Table 2.7
Environmental Stresses as They Relate to Statistical Difference in Serum Parameters for the Osprey Populations
OSPR Mean Parameter E vs W P Value Response Environment
PCV (g/L) 32.66 vs 33.38 0.032 Dehydration Stressed
ALT (U/L) 28.02 vs 20.61 0.0001 Tissue Damage Stressed
Muscle CK (U/L) 1660 vs 1365 0.009 damage/activity Stressed
K (mmol/L 4.28 vs 5.61 0.006 Renal Stressed
51 Table 2.8
Mean Blood Serum Values for Bald Eagles in Eastern and Western Florida Bay
East West Variable N M SD N M SD
PVC (%) 39 32.46 5.02 76 33.55 3.79
TP (mg/dl) 47 3.24 0.74 101 3.33 1.07
ALB (mg/dl) 36 1.59 0.35 84 1.51 0.28
AST (U/L) 49 128.02 39.71 97 137.27 50.02
ALT (U/L) 36 16.92 8.54 83 18.17 6.58
ALKP (U/L) 40 131.1 44.56 82 162.04 55.18
LDH (U/L) 23 2,575.30 1,193.68 65 2,951.78 1,628.30
CK (U/L) 41 1,248.00 505.58 79 1,214.87 499
URIC (mg/dl) 45 12.1 5.2 95 14.27 6.3
CA (mg/dl) 45 9.23 1.22 97 9.62 2.37
PHOS (mg/dl) 46 6.12 1.26 97 6.29 1.37
GLU (mg/dl) 50 218.6 27.59 104 230.52 27.78
NA+ (mmol/L) 49 136.06 11.86 102 136.31 10.2
K+ (mmol/L) 50 4.34 1.67 102 4.04 1.74
CL- (mmol/L) 49 103.04 11.35 99 106.41 9.42
CO2 (mmol/dl) 43 19.86 4.34 90 17.97 4.82
CHE (U/ml) 49 1.3 0.38 103 1.27 0.27
52 '"()**+,!&-./&& *
'#"
'!"
&" !!"#$%& %"
$"
#"
!" ()*)" ()*)"
Figure 2.4. A serum parameter*)+," value-*+," for Bald Eagle populations in eastern and western Florida Bay (FL) for all years examined. Statistical differences between the regions were examined using a Mann Whiney U Test and an asterisk (*) indicates significance (p< 0.05). Refer to figure 2.2 for non-significant Bald Eagle serum value parameters.
Table 2.9
Results for the Mann-Whitney U Test for Bald Eagle Serum Values for Eastern and Western Florida Bay
BAEA East BAEA West Mann-Whitney U Test FB 1993-2001 FB 1993-2001 FB 1993-2001 East VS West Parameter N N P<.05 Adj. H K (mmol/L) 57 83 0.022 5.266
Table 2.10
Environmental Stress as They Relate to the Statistical Difference in Serum Parameters for the Bald Eagle Populations
BAEA Mean Parameter E vs W P Value Response Environment K (mmol/L) 4.34 vs 4.04 0.022 Renal Stressed
53 Table 2.11 A Comparative View of Serum Values of Multiple Raptor Species
Bald Eagle, FL Bald Eagle, Swallow-tailed African Fish White-Tailed Osprey, FL Bay Bay Michigan Spanish Imperial Kites Eagle Eagle (Pandion Osprey, (Haliaeetus (Haliaeetus Eagles ( Elan oides Golden Eagle ( Haliaeetus (Haliaeetus haliaetus) England/Scotland leucocephalus) leucocephalus) (Aquila adalberti) forficatus) (Aquila vocifer) albicilla) (Mealey (Pandion haliaetus) (Mealey et al. (Bowerman et al. (Garcia-Montijano Mealey et al. chrysaetos) (Hollamby et (Sonne et al. Blood Values Unpublished ) (Meredith et al. 2010) 2004) 2000) et al.) 2002 2006 Nazifi et al. 2008 al. 2004) 2010) PCV (%) 33.06 + 4.72 40.0 + 6.0 32.74 + 4.16 32 + 4 43 + 3 33.78 + 5.23 47 + 0.0009 45 + 2
GLU (mmol/L) 218.31 + 41.47 223.03 + 27.37 280 + 32.2 279 + 18 279.1 + 41.01 16.42 + 0.73 12.4 + 2.01 15.8
PHOS (mmol/L) 9.06 + 21.31 6.31 + 1.3 6 + 0.7 4 + 1.0 5.5 + 2 1.73 + 0.08 0.74 + 0.30
TP (g/L) 4.49 + 4.72 34.15 + 3.73 3.28 + 0.98 3.4 + 0.5 3.6 + 0.33 4.34 + 1.47 4.9 + 1.35 3.6 + 0.4 2.76
Uric (mg/dl/) 12.64 + 4.8 572.3 + 219.5 (mmol/L) 13.46 + 5.88 16.8 + 4.3 3.07 + 1.78 14.38 + 6.07 457.67 + 97.46 0.998 + 0.408 61.1
ALB (g/L) 1.57 + 0.55 16.85 + 2.31 1.48 + 0.43 1.4 + 0.2 20.46 + 0.79 12 + 1.3 1.27
ALKP (U/L) 462.68 + 211.46 147.6 + 51.96 449 + 91.7 196.75 + 61.17 1247
AST (U/L) 38.4 + 24.09 39.40 + 11.90 132.73 + 48.04 198 + 62 278 + 65 184.33 + 107.7 194 + 117
ALT (U/L) 24.2 + 11.66 17.11 + 7.41 15.5 + 6.7 28.21 + 2.36 15
Ca (mmol/L) 8.9 + 2.69 2.84 + .18 9.39 + 2.24 10.8 + 0.55 11.9 + 1 .7 8.63 + 1.37 2.37 + 0.24 2.4 + 0.13 2.45
CHE (U/L) 2.06 + 0.4 1.29 + 0.31 1.24 + 319 0.8 + 0.32
CK (U/L) 1514.05 + 594.73 2165.6 + 879.1 1268.71 + 557.69 2157 + 603 288 + 119 3084.44 + 2413.44 217 + 53
LDH (U/L) 2521.33 + 1108.71 1895.8 + 500.5 2547.63 + 965.22 713 + 166 5601.5 + 3314.73 1209.89 + 21.73
Na+ (mmol/L) 134.21 + 16.01 135.85 + 11.13 148 + 2.3 154 + 5 144.73 + 12.5 153 + 5.56 152 + 150-156
Cl- (mmol/L) 104 + 15.8 104.98 + 10.11 117 + 2.5 117.33 + 21.07 115 + 5.21
K+ (mmol/L) 4.97 + 10.8 4.28 + 1.82 3.5 + 0.63 3.4 + 1.2 3.28 + 1.32 1.3 + 0.33 2.9 + 0.75-3.03
C02 (mmol/L) 20.5 + 5.85 18.9 + 4.79 20.7 + 5.3 21.08 + 4.35
III. MIGRATORY, DISPERSAL AND MOVEMENT PATTERNS OF BALD EAGLES
(HALIAEETUS LEUCOCEPHALUS) FLEDGED FROM FLORIDA BAY,
EVERGLADES NATIONAL PARK
Avian migration can be defined as a regular seasonal movement between regions inhabited at different times of year, with one region commonly associated with reproductive needs (Mead 1983). The most common avian migrations in North America are those between breeding locations at northern latitudes during the summer and wintering locations at southern latitudes (Poole 1989). Direction and timing, however, are determined by resource availability. For instance, Bald Eagles in central Florida are known to migrate north in the summer and then south during winter for breeding. These migrant eagles show a high degree of philopatry to their natal/breeding sites (Wood
2009). Migration patterns vary among species. The Swallow-tailed Kite (Elanoides forficatus) is known to nest in Florida during the summer months and migrates in mid-
July to wintering grounds in the Southern Hemisphere (Brazil, Paraguay and Bolivia;
Zimmerman and Meyer 2004). Ospreys that breed in New England are winter migrants to the Caribbean islands and South America (Martell et al. 2004). Migration is a strenuous event, especially for recently fledged birds (Jenkins et al. 1999). Satellite tracking has identified specific patterns of movements, the often-neglected stopover areas vital to migrating birds (Mojica et al. 2008).
Fledgling dispersal is often used ambiguously. Natal dispersal is usually the movement from a natal site to a potential nesting area to avoid inbreeding, reduce 55 competition, and provide access to less-competitive foraging areas (Steenhof et al. 2005).
Very often, “dispersal” is incorrectly applied to non-migratory movements in which a species exhibit philopatry. A more appropriate term for such post-fledging behavior by immature birds would be “localized movement” (Cadahia et al. 2005). Recently fledged
Ospreys banded as nestlings in eastern Florida Bay departed their natal site and were recovered/sighted along the eastern coast of Florida throughout the following year
(Martell et al. 2004). These Ospreys exhibited localized movement within Florida State until their sexual maturity and through band sightings (BKM) returned to their natal region.
Satellite tracking has become a very efficient way to accurately document the movements of migratory and dispersing raptors (Galarza and Dennis 2009). Meyburg et al. (1995) used satellite and VHF telemetry to track one fledged Imperial Eagle (Aquila heliaca) for six weeks, obtaining 56 locations prior to its probable death, inferred from loss of the signal. Based on two Ospreys tracked from Everglades National Park (ENP),
Martell et al. (2004) suggests that the western population of Florida Bay might be resident, in contrast to the Osprey population in Lake Istokpoga (Highlands County, central FL), which consists of a mixture of migratory and localized movers.
Satellite tracking of Montagu’s Harriers (Circus pygargus) (Meyburg et al. 2001),
Lesser Spotted Eagles (Aquila pomarina) (Trierweiler et al. 2007) and Bonelli’s Eagles
(Hieraaetus fasciatus) (Cadahia et al. 2005) has provided valuable information for the management and conservation of species on a global basis. Even though the initial cost is high, the information received is accurate, frequent, and eventually comparable or lower in price after considering labor-intensive fieldwork and travel costs for tracking standard
56 VHF transmitters from the ground or air (Rafanomezantsoa 2002). The combined use of satellite and VHF tracking can be helpful by combining, respectively, long-distance and localized detections, with the latter allowing direct visual observations.
Bald Eagles fledged from Central Florida nests have been monitored through satellite tracking and shown to migrate north to spend time as far north as Chesapeake
Bay and Nova Scotia (Wood and Collopy 1994). In the fall, these migrant eagles returned to over-winter in central Florida (Mojica et al. 2008). In contrast, Curnutt
(1992) identified a Bald Eagle roost site of adult and juveniles in the ENP with heavy use during the non-breeding season (July-Nov) and less-frequent use once they returned to their breeding territories (December-June) throughout the park and the Florida Bay area.
These observations suggested that the Florida Bay population of Bald Eagles consisted of localized movement groups.
Baldwin et al. (2012) reported a declining population trend for Bald Eagles in
Florida Bay. This ecosystem is considered compromised due to the lack of freshwater flowing into the Bay, which results in significant salinity fluctuations and reduced or shifting populations of fish, a primary prey item for Bald Eagles and other predators
(Thayer et al. 1999). The objective of this study was to determine the migratory and dispersal movements of Bald Eagles fledged from nests in Florida Bay (ENP) and to determine if this population simply disperses or actually migrates out of the state for part of each year.
Methods
Study Site. The Florida Bay estuary lies between the southern portion of the
Florida peninsula to the north, the Florida Keys to the east and south and the Gulf of
57 Mexico to its west. It covers approximately 2200 square kilometers within the boundaries of the Everglades National Park (Figure 3.1). East Florida Bay will be the region east of
Big Key and West Florida Bay is designated as the region west of Big Key. The central area of Florida Bay was excluded due few, if any, nesting pairs occur in the area.
Ageing and Sexing. Nests containing Bald Eagle nestlings from 35 to 45 days old were visited annually from 1 January through 1 May from 2003 through 2007. Nestling development was monitored chronologically or through feather formation by way of repeated observations (Bortolotti 1984). The nests were surveyed three times for ageing, sampling and evaluation. The nests were visited only once for blood sampling and satellite harness placement Sex of the eagles was determined through blood samples by
Avian Biotech International, Tallahassee, Florida.
Tracking. To monitor movements and migration, sixteen eaglets were equipped with a satellite platform transmitter terminal (PTT) (Microwave Telemetry, Columbia,
Maryland) or a PTT-VHF combination package (the latter by American Wildlife
Enterprises, Monticello, Florida). A 50-g PTT packages using a harness design and materials were applied similar to those used by Wood and Collopy (1994) and Millsap et al. (2004) and modified for this study in cooperation with Meyer and Collopy (1995).
PTT’s were developed and synchronized in conjunction with the Argos Satellite System.
Backpack harnesses were designed to detach after the expected life of the transmitters, approximately five years.
Analyses. There are six Location Classes (LC) generated from the satellite locations. We used only the three of highest quality in our analysis (LC 1, 2, and 3, with maximum errors of 1500 to 250 meters, respectively). After selecting the highest-quality
58 fixes, we reviewed the entire database to remove duplicate fixes (an anomaly of the data- processing and reporting system), and then plotted all locations in ArcGIS. Each bird’s movements were examined individually to remove locations that obviously were in error. Travel distances were calculated using ArcGIS 9(ArcGis 9 2005) Hawth’s Tools extension (Beyer 2004).
This investigation was conducted under the guidelines of IACUC, U.S.
Department of the Interior (USDI), National Park Service permit number EVER-2010-
SCI-0009, USDI Bird Banding Laboratory Master Bander Permit number 22418 and
State of Florida Fish and Wildlife Conservation Commission permit number WB03367b
(Appendixes).
Results
Tracking. Sixteen eaglets were tagged in south Florida (Table 3.1) and tracked for a total of 9,103 days from March 2004 to October 2010 (Figure 3.33, Table 3.3).
Tracking duration per individual ranged from 82 to 1,531 days. Fifteen of the tracked eagles were from Florida Bay, Monroe County, FL; and one was from Tesoro Golf
Community, St. Lucie County, FL. (Figure 3.32). Total distances traveled by the Florida
Bay Bald Eagles ranged from 148.51 km to 22,488.94 km, with a mean of 7,907.39 km
(S.D. = 8,193.99 km, N = 15) (Table 3.5 and 3.6). The birds began leaving their immediate nest areas on April 9th and ranged locally until July 24th. The mean date for nest-area departure for the Florida Bay eagles was 17 June (S.D. = 5.72, N = 15) (Table
3.4). Migrating eagles moved directly north approximately 2-3 months after fledging.
Localized eagle movements are depicted in Table 3.2.
59 Survivorship. We estimated first-year survival at 52% and 67% for the period from 1.5 to 4 years (Table 3.8). Our sex ratio was skewed, 2 females and 7 males therefore survival comparisons between the sexes couldn’t be accurately analyzed. The longest surviving eagles were a male (3 years), female (3.5 years) and sex unknown (4 years).
Migration. Eaglet 73338 was banded and fitted with a transmitter in Port St.
Lucie on 3 March 2008 (Figure 3.2). The eagle remained close to its natal territory and
Florida until June 2nd 2008. On 3 June Eaglet 73338 maintained a fast northerly track to the Georgia coastline, then across South Carolina to Turkey Island on the James River before settling in at Calvert Cliffs State Park, MD, where it remained until 17 September.
On 18 September 73338 began the southerly migration back to Florida via Sandy Point,
VA and the remainder of its northbound route in reverse order. The bird followed the
Atlantic coastline south, eventually arriving in Port St. Lucie County on 20 November
2008 close to its natal territory. The eaglet meandered south and then settled in at the water catchment area west of West Palm Beach on 20 March 2009. The eagle remained in the area until its last transmission on 8 April 2009.
Eaglet 73335 was the only fledgling (N = 14) from Florida Bay that migrated north to North Carolina (Figure 3.4 and Figure 3.5). The bird was banded and fitted with a transmitter on 27 February 2007 on Derelict Key, ENP. It departed its nesting area to the north on 15 May 2007 and reached Vanceboro, N.C. and remained there until 28
October 2007. On 29 October, it headed due south to arrive back in Florida Bay on 9
November 2007, where it remained until 20 April 2008. The lack of funding resulted in no more future tracking of this eagle.
60 Localized Movement. Localized movement was the result for 93% (N=14) of the fledged eagles in Florida Bay. Eagles surviving < 4 months (N=3) remained close to their natal territory (Figures: 3.24, 3.26 and 3.30), Localized movement was initially depicted by birds surviving > 4 months and < 7 months (N=6). They utilized either a western or eastern coastal corridor (Figures: 3.12, 3.18, 3.22 and 3.28).
The eagles surviving > 2.5 years and < 4 years (Figures: 3.6, 3.8, 3.10, 3.14, 3.16 and 3.20) are of paramount interest for identifying movement corridors and roosting areas within Florida. Eaglets 64555 and 56107 moved northwest through a western coastal corridor in Collier County prior to moving across the state in a northeastern direction.
Eaglets 46264 and 46265 use a northerly central corridor as they moved and both ended up in Volusia County. Eaglet 56105 moved north utilizing an eastern coastal corridor to its destination in Okeechobee and Port St. Lucie Counties.
Ranges. Minimum convex polygons (MCP) and fixed kernel home ranges were calculated for the fledged Bald Eagles for the life of the transmitter (Table 3.7). The ranges are described in percentages. The 90%, 50% and the 10% home ranges simply give the probability of .90, .50 and .10 of locating an animal in a given area. The mean
90% MCP range for all the Bald Eagles is 42,627.04 km2, (Minimum=14.24 km2 and maximum of 283,338.95 km2) (Table 3.7). The fixed kernel range at 90%, considered to be more conservative, had a mean size 61,038.70 km2 (Minimum = 24.86 km2 and
Maximum of 487,447.19 km2). Individual Bald Eagle range data can be viewed on
Figures 3.3, 3.5, 3.7, 3.9, 3.11, 3.13, 3.15, 3.17, 3.19, 3.21, 3.23, 3.25, 3.27, 3.29 and
3.31.
61 Band Sightings. Eaglet Madeira 2004 was banded and fitted with a standard VHF transmitter on 9 April 2004. The transmitter’s signal was last detected on 14 July 2004 near Mahogany Hammock, ENP. On 16 September 2009, the Madeira eagle was photographed just west of Tamiami Airport in a recently tilled agricultural field by B. K.
Mealey, M. Hanson and J. D. Baldwin. The bird was identified through a band number visible in the photograph, the absence of the color auxiliary band and the presence of a non-functioning VHF transmitter.
Eaglet Buoy 2007 was banded (no transmitter) on Buoy Key on 13 February
2007. This eagle was photographed during the first week of March 2011 at the Solid
Waste Authority Landfill, 6880 North Jog Road, West Palm Beach, FL by an unidentified photographer.
Discussion
Migration. The dispersal and migration of Bald Eagles fledged from nests in
Florida Bay began in early April and continued until late July (Figure 17). The average date of departure was 17 June (S.D. = 5.72, N = 15). Central Florida (CF) eaglets also began their departure in April and ranging through June with the average departure date of 30 May (median = 24, N = 52) (Mojica et al. 2008). Older sub-adult CF eagles made their seasonal movements over a longer period, from March through August. Adult Bald
Eagles in San Luis Valley, CO, departed from January to April (Harmata 2002). Fledged eaglets in California began their first migration, to Canada, later than the Florida eagles, from July to August (Hunt et al. 1992b, Linthicum et al. 2007). One satellite tracked
Spanish Golden Eagle tagged at a latitude similar to that of the California eagles, began its migration in July (Urios et al. 2007) and Spanish Bonelli’s Eagles did so in August
62 (Cadahia et al. 2008). It's likely that Bald Eagles from more southerly nests begin their migration earlier because they have longer distances to travel (Hunt et al.1992a, Millsap et al. 2004).
Eaglet 73335 was the only fledged Bald Eagle from Florida Bay that migrated out of the state. Eaglet 73338 from Port Saint Lucie County also migrated north, but this was expected since it came from the southern portion of the central Florida nesting population. Eaglet 73335’s movements were rapid and direct; she left her natal area on
15 May and arrived near Greenville, North Carolina, on 6 June, remaining there until 15
September. The young eagle ranged over lakes, agricultural areas, and wetland restoration project. The bird then moved northeast to Vanceboro, North Carolina and foraged near the banks of the Neuse River, a primary agricultural area mixed with natural habitat. The bird remained there until 28 October before beginning its return to Florida.
Eaglet 73338 was fitted with a transmitter through a collaborative effort with the
National Audubon Society. Since our initial results were reflecting a strong dispersal of eagles from Florida Bay, we wanted to determine the extent of the movements by eagles from the South Florida population. However, 73338’s nest probably was within the boundaries of the CF Bald Eagle population. Both eaglet 73335 and 73338 showed distinct north/south movements with the distinctive seasonality of true migrations. Both stayed close to the Atlantic shoreline rather than exhibiting the Loop Migration pattern noted by others (see Trierweiler 2007). The Atlantic shoreline is one of several migratory routes described for CF Bald eagles (Mojica et al. 2008) Wood and Collopy
(1994) also found that the Atlantic coastline was a predominant route during their investigations of migratory movements of Bald Eagles in central and north Florida.
63 Localized Movement. Localized movement was the prevailing preference for
93% (N = 14) of the fledged eagles from Florida Bay. The Florida Bay eagles movements were different from the migration behavior of the eaglets in Central Florida (Mojica et al.
2008, Wood 2009) in that movements were restricted to the south of central Florida with eaglet 56107 taking one flight to Nassau County in Northeast Florida. Eaglets 56107 and
64555 extensively foraged on Florida’s west coast. Eaglets 46265 and 46264 used a central corridor for movement up to Volusia County and Osceola County. Whereas
56105 primarily used the transition zone between eastern Everglades and the western edge of the human sprawl. This zone was a mixture of natural vegetation and agriculture.
The eaglets used many of the state parks, wildlife management areas and state forests after leaving Everglades National Park, including Collier-Seminole State Park,
Kissimmee State Park, Merritt Island National Wildlife Refuge, Panther National
Wildlife Refuge, Three Lakes Wildlife Management Area, and Tiger Bay State Forest.
Because these eaglets were born on remote keys in Florida Bay, they may have sought less disturbed areas during their first localized movements (Millsap et al. 2004), eventually venturing into disturbed agricultural and urbanized areas after habituating to human activity. Seven eaglets surviving more than a year showed signs of philopatry. At some point during their migration or dispersal, the Florida Bay eagles and the Port St.
Lucie eagle returned to their natal area. Linthicum (2007) also observed this fidelity in
California eaglets, although some were not quantified due to poor transmitter signals.
Band recoveries from 1931 to 2005, documented in Bird Banding Laboratory records, reveal a strong degree of philopatry for the Florida Bald Eagle populations (Wood 2009).
64 Survival Rates. We estimated first-year survival as 52% and 67% for the period from 1.5 to 3 years Table 3.8. Using band re-sighting data, McCollough (1986) estimated survival of Bald Eagles in Maine at 74% during the first 1.5 years and 84% for the period
1.5 to 2.5 years. Buehler et al. (1991) estimated survival based on VHF telemetry for eagles from Chesapeake Bay at 100% during the first 1.5 years and 92% for the period
1.5 to 2.5 years-of-age. Wood and Collopy (1994) estimated survival of VHF-radio marked Bald Eagles from a rural north-central Florida study area at 63% from birth to 1.5 years and 84% from 1.5 to 2.5 years. Millsap et al. (2004) estimated survival rate for suburban fledged eaglets at 72% and rural fledged eaglets 89% to 1 year and 85 % and 90
% for 1 to 2 years. McIntyre et al. 2006 estimated Golden Eagle survival rates at 34 % for an eleven month period in 1997 and 19% in 1999. Overall, survival rates for fledged
Florida Bay Bald Eagles are lower than other published references for Bald Eagles. We also assumed the eaglets died but on one occasion a bird with a VHF transmitter presumed dead during its first year (2004) was photographed with its band and the transmitter still attached in 2009. Lost signals in most cases would probably signify mortality. Since the transmitters for eagles 73335 and 56105 were over 3 years old, we are not assuming the birds perished but a probability of equipment malfunction.
Conservation and Management. Monitoring movements of Bald Eagles assists federal and state wildlife agencies in identifying stopover and flyways for species listed in the South Florida Multi–Species Recovery Program (U.S Fish and Wildlife Service
1987) and Bald Eagle Habitat Guidelines for the state of Florida (Nesbitt et al. 1993). In
2007, the Bald Eagle was delisted from the Endangered Species Act due to their population recovery across the United States (Fish & Wildlife Service 2009). The
65 Spanish Imperial Eagle, much like the North American Bald Eagle, is recovering due to applications of data and recommendations from extensive monitoring and research and is recovering outside the original protection areas established by the Spanish government
(Gonzalez et al. 2008). Satellite tracking and global positioning system (GPS) are identifying migratory routes and important stopovers, and are allowing governments to protect key habitats (Galarza and Dennis 2009).
Florida Bay is a compromised ecosystem showing serious population declines in
Bald Eagles (Baldwin et al. 2012) and in the historical nesting sites of Ospreys. One remarkable result is the lower survival rates of first year Bald Eagles in Florida Bay compared with other bald eagle studies in Florida, Chesapeake Bay and Maine. The results could be attributed to the small sample size in the investigation. Their poor survivability may also be linked to the Florida Bay ecosystem. Once they depart their natal territory and the parents are no longer providing food, the fledged eagles may be having difficulty foraging and their health is compromised prior to their movement/migration.
As eagle territories in Florida Bay continue to decline in number, it appears that some Bald Eagles are establishing nesting territories on the edge of residential areas in south Florida. One confirmed nest is in western Broward County, suspected nest
Turnpike and I-75 Broward County (BKM), and Blackpoint Marina (Miami-Dade
County). One of our last satellite tracked bird continued to return for a period of 2 years to the vicinity of Tree Top Park, Davie, FL Broward County. Funding from Federal, state and private sources are needed to maintain long-term surveys and expand monitoring projects of imperiled avian and other species of Florida Bay to capitalize on
66 the value of these animals as critical barometers for evaluating the progress of the
Everglades restoration project and its impact on the Florida Bay ecosystem.
67 Florida Bay
Figure 3.1. Map of Florida identifying the initial tagging site for the fledged bald eagles.
68 Table 3.1
Platform Terminal Transmitter (PTT) Packages Were Attached to Bald Eagle Nestling That Were < 9 Weeks Old in Florida Bay, Everglades National Park
Auxiliary Tagging Bird Band Number Band PTT’s Sex Lat-Lon Key Date
1 629-504-01 46264 L-U 250-0805 Buoy 3/13/04
2 629-504-02 46265 L-U 250-0805 Buoy 3/13/04
3 629-504-03 46263 L-U 250-0805 Camp 3/13/04
4 629-504-06 GB 2/0 56105 F 250-0805 Camp 3/13/05
5 629-504-07 GB 2/1 56106 L-U 250-0805 Buoy 3/17/05
6 629-504-09 GB 2/3 56107 L-U 250-0803 Madeira 3/27/05
7 629-504-10 GB 2/4 56109 M 250-0804 Murray 3/13/06
8 629-504-11 GB 2/5 64555 M 250-0805 Murray 3/13/06
9 629-504-12 GB 2/6 56108 F 250-0806 Clive 3/13/06
10 629-504-13 GB 2/7 64557 M 250-0805 Buoy 4/2/06
11 629-504-14 GB 2/8 64556 M 250-0803 Madeira 4/16/06
12 629-504-15 GB 2/9 73337 M 250-0803 Lake 1/24/07
13 629-504-16 GB 3/0 73335 M 250-0805 Derelict 2/23/07
14 629-504-19 GB 3/3 73336 L-U 250-0805 Buoy 2/14/07
15 629-504-21 GB 3/5 73339 L-U 250-0803 Madeira 2/8/08
16 629-504-25 GB 4/0 73338 M 271-0802 St Lucie 3/4/09
69 Table 3.2
Results for Sixteen Bald Eagles Fledged from Florida Bay, Everglades National Park
Key Tagging Date Signal End Reason Ended Days Trans No. Loc Total
Buoy 3/13/04 9/15/06 Unknown 785 1561
Buoy 3/13/04 5/23/07 Unknown 1399 2657
Camp 3/13/04 7/19/04 Died 124 209
Camp 3/13/05 10/24/08 Funding 1300 5101
Buoy 3/17/05 7/3/09 Died 93 206
Madeira 3/27/05 6/29/08 Unknown 1183 2934
Murray 3/13/06 7/31/06 Died 140 278
Murray 3/13/06 10/23/08 Unknown 890 3421
Clive 3/13/06 10/22/08 Unknown 954 2112
Buoy 4/2/06 2/16/07 Unknown 300 473
Madeira 4/16/06 7/4/06 Died 49 148
Lake 1/24/07 6/16/07 Died 112 378
Derelict 2/23/07 10/23/08 Funding 604 2190
Buoy 2/14/07 9/23/07 Died 200 246
Madeira 2/8/07 6/22/07 Died 72 219
St Lucie 3/4/08 10/24/09 Unknown 234 830
Total 8439 22963 Note. Total transmission days were 8,439 with total of 22,963 location points.
70 Table 3.3
Number of Transmission Locations for Each Year the Bald Eagles Were Transmitting
Key Tagging Date Signal End No. Loc. Yr 1 No. Loc. Yr 2 No. Loc. Yr 3
Buoy 3/13/04 9/15/06 614 856
Buoy 3/13/04 5/23/07 811 968 580
Camp 3/13/04 7/19/04 209
Camp 3/13/05 10/24/08 1316 1315 1531
Buoy 3/17/05 7/3/09 206
Madeira 3/27/05 6/29/08 841 841 1067
Murray 3/13/06 7/31/06 278
Murray 3/13/06 10/23/08 1177 1488
Clive 3/13/06 10/22/08 988 672
Buoy 4/2/06 2/16/07 473
Madeira 4/16/06 7/4/06 148
Lake 1/24/07 6/16/07 378
Derelict 2/23/07 10/23/08 1259
Buoy 2/14/07 9/23/07 246
Madeira 2/8/07 6/22/07 219
St Lucie 3/4/08 10/24/09 830
Total 9993 6140 3178
71 Table 3.4
The Graph Shows the Month That the Florida Bay Fledged Bald Eagles Departed from Their Natal Territory
Month Departing Natal Territory
6
5
4
3 No. of Bald Eagles
2
1
0
Note. Mean date of departure from the natal territory was June 17 + 5.72 days.
72 Table 3.5
Natal Site Departure Date, Total Distance Since Transmitting and the Distance Traveled Each Day
Key Natal site Departure Dist since leave (km) Dist/day km
Buoy 7/25/04 8052.41 10.3
Buoy 7/21/04 16076.23 11.49
Camp 5/5/05 22488.94 17.74
Buoy 5/29/05 633.08 17.59
Madeira 6/4/05 17866.49 15.94
Clive 6/25/06 2251.14 2.65
Murray 6/1/06 16737.46 19.15
Madeira 6/25/06 245.26 24.53
Buoy 6/23/06 338.38 1
Derelict 5/12/07 12789.64 24.6
Lake 4/10/07 640.35 9.42
St Lucie 5/28/08 4528.21 30.19
Calusa 6/9/07 148.51 11.42
Sum 102796.12 196
St Dev 8193.99 9.13
Average 7907.39 14
Min 148.51 0
Max 22488.94 30.19
73 Table 3.6
Depicting the Distance Traveled by Year for Bald Eagles Surviving through the Second and Third Year
Total distance in Total distance in Total distance in PTT Key 1st year 2nd year 3rd year
46264 Buoy 3777.42 3753.11
46265 Buoy 6355.07 7174.95 2158.27
56105 Camp 6208.11 5913.31 7282.27
56106 Buoy
56107 Madeira 6686.99 5441.72 5468.32
56108 Clive 1481.32 720.95
56109 Murray
64555 Murray 7585.11 6761.13
64556 Madeira
64557 Buoy
73335 Derelict 8506.73
73336 Buoy
73337 Lake
73338 St Lucie
73339 Calusa Note. Derelict eagle was only monitored for one year due to funding restrictions.
74 Table 3.7
Two Results Are Calculated to Determine the Home Range of the Fledged Bald Eagles
Fixed kernel home range, total data range (km2) 90%MCP Key (km2) 90% 50% 10% Buoy 5800.47 5876.92 1304.99 100.57 Buoy 13436.54 17450.21 3355.81 320.99 Camp 22250.49 13203.95 3627.43 418.04 Buoy 33788.13 55792.25 10329.82 947.74 Madeira 5357.18 10952.76 2284.91 152.36 Clive 63.99 46.34 7.95 0.00 Murray 65.87 185.17 33.13 4.37 Murray 38717.75 21635.50 4147.47 250.47 Madeira 1771.76 1239.53 213.36 15.94 Buoy 60.41 38.32 7.43 0.75 Derelict 283338.95 300098.18 70469.33 6148.44 Buoy 14.24 24.86 3.37 0.37 Lake 571.19 1444.02 362.71 40.24 St Lucie 233799.37 487447.19 119364.06 10297.00 Calusa 369.29 145.32 25.09 1.26 Average 42,627.04 61,038.70 14369.12 1246.57 St. Dev 89,070.37 140,406.49 34,092.37 2949.53 Min 14.24 24.86 3.37 0.00 Max 283,338.95 487,447.19 119,364.06 10,297.00 Note. The Minimum convex polygon (MCP) and the Fixed Kernel Home range are depicted in the table as percentages (%). The 90% home range is the probability of locating the animal in a particular area.
75 Table 3.8
Comparing Annual Survivorship of Bald Eagles in FL Bay, Central Florida (CFL) (Wood and Collopy 1994), FL Suburban and FL Rural (Millsap et al. 2004), Chesapeake Bay (CB) (Buehler et al. 1991) and Maine (McCollough 1986)
FL Bay Central FL FL Suburban FL Rural CB Maine
1-1.5 years (%) 52 63 72 89 100 75
1.5-2.5/3.5 years (%) 67 84 84 85 92 84
76
Figure 3.2. Movement pattern for Eaglet 73338.
77
Figure 3.3. Fixed Kernel Home Ranges for bald eagle 73338.
78
Figure 3.4. Movement pattern for Eaglet 73335.
79
Figure 3.5. Fixed Kenel Home Ranges for Bald Eagle 73335.
80
Figure 3.6. Movement pattern for Eaglet 46264.
81
Figure 3.7. Fixed Kenel Home Ranges for Eaglet 46264.
82
Figure 3.8. Movement pattern for Eaglet 46265.
83
Figure 3.9. Fixed Kernel Home Ranges for bald eagle 46265.
84
Figure 3.10. Movement pattern for Eaglet 56105.
85
Figure 3.11. Fixed Kernel Home Ranges for bald eagle 56105.
86
Figure 3.12. Movement pattern for Eaglet 56106.
87
Figure 3.13. Fixed Kernel Home Ranges for bald eagle 56106.
88
Figure 3.14. Movement pattern for Eaglet 56107.
89
Figure 3.15. Fixed Kernel Home Ranges for Bald Eagle 56107.
90
Figure 3.16. Movement pattern for Eaglet 56108.
91
Figure 3.17. Fixed Kernel Home Ranges for Bald Eagle 56108.
92
Figure 3.18. Movement pattern for Eaglet 56109.
93
Figure 3.19. Fixed Kernel Home Ranges for Bald Eagle 56109.
94
Figure 3.20. Movement pattern for Eaglet 64555.
95
Figure 3.21. Fixed Kernel Home Range for Bald Eagle 64555.
96
Figure 3.22. Movement pattern for Eaglet 64556.
97
Figure 3.23. Fixed Kernel Home Ranges for Bald Eagle 64556.
98
Figure 3.24. Movement pattern for Eaglet 64557.
99
Figure 3.25. Fixed Kernel Home Ranges for Bald Eagle 64557.
100
Figure 3.26. Movement pattern for Eaglet 73336.
101
Figure 3.27. Fixed Kernel Home Ranges for Bald Eagle 73336.
102
Figure 3.28. Movement pattern for Eaglet 73337.
103
Figure 3.29. Fixed Kernel Home Ranges for Bald Eagle 73337.
104
Figure 3.30. Movement pattern for Eaglet 73339.
105
Figure 3.31. Fixed Kernel Home Ranges for Bald Eagle 73339.
106
Figure 3.32. Depicts the localized movement within the state of Florida of 15 eaglets fledged from Florida Bay and one from Port St. Lucie.
107
Figure 3.33. Movement patterns for all Eaglets sampled within the project.
108 IV. CHARACTERISTICS OF MANGROVE DIAMONDBACK TERRAPINS
(MALACLEMYS TERRAPIN RHIZOPHORARUM) INHABITING ALTERED AND
NATURAL MANGROVE ISLANDS
The mangrove diamondback terrapin (Malaclemys terrapin rhizophorarum) is one of seven subspecies of Malaclemys terrapin that range along the US east coast from New
Jersey (M. t. terrapin) to Texas (M. t. littoralis). Although the boundaries between these taxa and the number of stocks within each taxon are unclear, their population levels appear to be in decline or have not been adequately surveyed to allow their status to be determined (Seigel and Gibbons 1995). Coastal development has destroyed and degraded terrapin habitats and exploitation has severely depleted their abundance (Roosenburg
2000). South Florida mangroves host three of the seven recognized subspecies of
Malaclemys terrapin in North America, the east coast diamondback terrapin, M. t. tequesta, (Biscayne Bay northward to Merritt Island), the mangrove diamondback terrapin, M. t. rhizophorarum, (lower Florida Keys west to the Marquesas) and the ornate diamondback terrapin, M. t. macrospilota, (Florida Bay and on the Florida's gulf coast to
Tampa Bay (Hauswaldt and Glenn 2005, Forstner et al., 2000).
Ecological and life history data are sparse for all of the Malaclemys terrapin populations in south Florida (Baldwin et al. 2005). Their presence is seldom reported on the highly altered human occupied Florida Keys. These terrapins are under tremendous pressure as a consequence of urban development resulting in decreased mangrove coastline, habitat fragmented by roadways and canals and frequent human encounters 109 (Mealey et al.,2005). The remaining south Florida insular Malaclemys populations are found in “pockets” isolated on keys within Florida Bay, Everglades National Park and the
Florida Keys National Wildlife Refuges. In this respect, the terrapin populations mimic the communities of mangroves upon which they are dependent, representing only fragments of the historical abundance (Garber 1990). Primary threats to the terrapins come from habitat degradation and destruction, leading to decreases in water quality and fresh water availability. The terrapins also suffer from the established insular populations of the black rat, Rattus rattus, a nest raider (Draud et al., 2004).
Here we provide limited demographic data on M. t. rhizophorarum, suggesting dependency of the species on the mangrove community. We also provide integrated health assessment parameters for two disjunct wild populations of M. t. rhizophorarum in the lower Florida Keys. One population was located on a private key in a highly altered island habitat where free ranging primates and other major anthropogenic changes were present. The second population was on an undisturbed key in the Key West National
Wildlife Refuge. We compare mark and recapture data, and several animal health assessment parameters to determine if there are major differences between populations of
M. t. rhizophorarum from human-altered versus relatively natural mangrove habitats.
Methods
Study sites – This project reports results from contemporaneous monitoring of two keys/islands in the lower Florida Keys monthly (1997-2000). The perimeters of both keys are fringed with red mangroves (Rhizophora mangle) and the interiors dominated by black mangroves (Avicennia germinans). Due to the vulnerability of M. t. rhizophorarum to collecting and harvesting, we wish to keep the study sites anonymous and designate
110 them TreatmentSiteLK (TLK) and ControlSiteKW (CKW). TLK was privately owned when the study began with extensive damage to the red and black mangrove trees due to the introduction of non-indigenous wildlife. By comparison, ControlSiteKW (CKW)
(46.69 ha) is located in the Key West National Wildlife Refuge.
Capture techniques – TLK and CKW were visited monthly, March through
December, from 1997 to 2000. M. t. rhizophorarum were hand caught by targeted searches of 8 person hours a month. Our surveys were restricted on TLK because of tidal fluctuations but not so on CKW. On TLK terrapin encounters often occurred at high tide while they were swimming in open shallow tidal pools but still retreated into black mangroves as it receded. Terrapins on CKW were located by searching under shoreline debris or among the pneumatophores of the black mangroves.
Mark/Recapture – Each terrapin was marked with 12 mm passive integrated transponder (PIT) tags (AVID, 3185 Hamner Avenue, Norco, CA 92860) following the protocols established by Camper and Dixon (1988). The PIT tags were injected in the posterior peritoneum slightly above and parallel to the plane of the plastron.
Morphometrics – Measurements were taken with Haglof calipers to the nearest millimeter. Straight-line carapace length (CL), carapace width (CW), plastron length
(PL), plastron width (PW), and body depth (BD), were recorded as well as weight (g) and gender for each terrapin captured. Markings, shell abnormalities, and general health and appearance were noted. Terrapins were released in the same area of capture.
Blood – After swabbing with 70% ethanol, 1-2ml blood samples were extracted from the femoral vein, using a 25 or 27 gauge needle and syringe. Field samples were stored in an ice cooler and later frozen. The blood was used for serum chemistry
111 analyses and future genetic analysis. Fifteen serum chemistry levels were analyzed on a
Johnson & Johnson Ektachem DT II System within 30 days of sampling for: total protein
(TP), albumin (ALB), uric acid (URIC), calcium (CA2++), glucose (GLU), phosphorus
(PHOS), cholinesterase (CHE), creatine kinase (CK), lactate dehydrogenase (LDH) aspartate aminotransferase (AST), alkaline phosphatase (ALKP), sodium (NA+), potassium (K+), chloride (CL-), and carbon dioxide (CO2). Aliquots from blood samples were placed in small 1-ml plastic blood tubes and allowed to clot for 15 minutes prior to centrifugation. Samples were centrifuged for 20 minutes and serum was transferred with a pipette to separate tubes to prevent hemolysis. Analyses followed the protocol specified in the Ektachem DT II System manual.
Bacterial Cultures – The utility of routine bacteriological culture in captive management has become increasingly important in recent years; however, the monitoring of wild populations is still in its infancy (Harwood et al., 1999). With sterile culture swabs and media in the field we collected a sample from the cloaca of each individual turtle. The applicator was then placed in a growth medium. Exceptional caution was required during the culture acquisition to prevent contamination. Each cloacal culture results in the isolation of one or more microbial organisms. Cultures were sent to Micrim
Laboratories, Fort Lauderdale for analysis within 48 hours of sampling.
Statistical Analysis – Descriptive statistics were conducted to establish means, ranges and standard deviations (SD) using JMP SAS Statistical Discovery Software,
(v5.1 SAS Institute, Inc., Raleigh, North Carolina). MANOVA, ANOVA and t-tests were conducted to compare measurements and serum between the genders and populations using SPSS Statistical Software, SPSS Inc., Chicago, Illinois.
112 This investigation was conducted under the guidelines of IACUC, the Florida
Keys National Wildlife Refuge permit number 41580-2009-02 and State of Florida Fish and Wildlife Commission permit number WX07477 (Appendixes).
Results
Capture Techniques – Nearly all terrapins (97% of 793 encounters) were captured in the key’s interior with 3% captured swimming in less than two meters of water near shore. The interior captures occurred primarily within or at the edges of A. germinans. A total of 23 individuals marked in the 1980s in a previous study were recaptured (R. Wood pers. comm. to BKM 1996). At both study sites, individual terrapins were routinely recaptured within just a few meters of previous capture points. We had several significant hurricanes during the study period, with at least one storm providing very close eye wall encounters with each of the study sites. Immediately after the storms we found few terrapins, but after several months/years the individuals increasingly reappeared in the same locations as their original captures, often to within a few to tens of meters. CKW had the slowest recovery, likely a consequence of extensive damage and die-off of A. germinans within the key’s interior.
Mark/Recapture – Seven hundred and ninety three terrapins were encountered, captured and recaptured, during the study, with 606 on TLK and 187 individuals on
CKW. Combining both populations we marked and sampled 462 new individuals (336 and 126 respectively). There is a significant difference in the total number of individuals collected at the two sites (P =.01) despite the total size and shorelines of the two sites being very nearly the same. Total recapture rate was 70% for combined population (TLK
= 80% and CKW = 48%). One-time recaptures of an individual were 16% of the total,
113 (TLK = 42% and ControlSiteKW = 32%), two-time recapture 7% (TLK = 18% and CKW
= 13%) and a third time recapture were 3% (TLK = 10% and CKW = 3%). The maximum recapture of an individual was 7 times, which occurred on TLK (< 1%).
Morphometrics – A student’s t-test was conducted yielding values depicting sexual dimorphism between the sexes (P < .05) (Table 4.1). TLK and CKW females were larger (P < .05) in two measurements: TLK CL (T =37.5, P =. 001), TLK weight (T =
30.4, P =. 001) and CKW CL (T = 17.2, P=. 001) and CKW weight (T = 15.5, P=0.001).
The MANOVA was significant (F=13.51, P < .05) conducted on the five measurements CL, CW, PL, PW and weight of the groups. All univariate ANOVA’s, except for PW (F = 0.11, P = .735), were significant. CKW scored higher means on: CL
(F = 10.56, P = .001), CW (F = 6.36, P = 012), PL (F = 9.67, P = .002), BD (F = 20.12, P
= .001) and weight (F = 21.56, P = .001) compared to TLK.
ANOVA values for CKW females scored higher means on CL (F = 8.35, P =
.004), PL (F = 8.88, P = .003), BD (F = 20.46, P = .001) and weight (F = 25.35, P =
.001). Only two ANOVA univariates were significant for males, PW (F = 8.40, P = .005) and BD (F = 9.40, P = .003), while all remaining meristics were not significant. The
CKW means for PW and BD were higher than TLK; and TLK was higher on CW.
Blood - Fifteen serum values were measured from M. t. rhizophorarum (Table
4.2). The CKW had higher mean values (P < .05) for TP (t = 2.35, P = .038), GLU (t =
2.41, P = .027), CL- (t = 2.39, P = .048) and ALKP (T = 2.51, P = .029) and TLK had higher mean values for CO2 (T = -3.35, P = .012), and CK (T = -3.10, P = .013) (Table
4.2). There were no differences in the remaining serum values.
114 Bacterial Cultures - We successfully analyzed 17 cloacal swabs from which twelve different organisms were isolated (Table 4.3). The most prevalent microbes were
Clostridium perfringes (59%), Aeromonas hydrophila (41%), Providencia rettgeri (35%) and Proteus mirabilis (35%). Salmonella sp. was isolated from one CKW female.
Discussion
Results suggest a high degree of fidelity within the mangrove community. Our overall design includes sites across Florida Bay with no significant movement detected after more than eleven years of study. This is additionally supported by the re- appearance of individuals at CKW after more than twenty years. This doesn’t infer that there isn’t any movement but our ongoing radio-tracking results coupled with current mark and recapture results show exceptional site fidelity of both the taxon and individuals to mangrove habitat and a particular key. Many individuals marked in a study by Wood (1981) are now micro chipped and included within our own recapture statistics. Likewise in the face of both severe droughts and hurricanes, our study individuals remained highly localized within the mangrove community.
Mark/Recapture - The population at TLK is significantly larger in total number of individuals than our CKW. In this respect, our original speculation would be met, despite nearly identical habitat sizes and configurations; there are more than twice as many terrapins and twice the biomass present at the treated site. The CKW population is half the size as that on TLK and we suggest that this is, in part, a consequence of the constraints given more limited prey availability, but additional research needs to be conducted to more directly test this statement. We have also considered the possibility that the TLK population may represent a possible intergraded population of the ornate
115 diamondback terrapin, M. t. macrospilota, with the mangrove diamondback terrapin, M. t. rhizophorarum based on the more highly variable phenotype encountered there.
However, no published study, or our own wider examination of Florida Bay would support size differences as a taxonomic indicator in this terrapin. Ultimately, discovery of detailed genetic variation will be required to delineate the two populations and other subspecies in southern Florida (Miller 2001), especially given the inconclusive recent results from microsatellite DNA analyses (Hauswaldt and Glenn 2005).
Blood - Serum chemistry analysis involves the measurements of naturally occurring enzymes and compounds in the blood, which are the result of metabolic and other physiological processes in the reptiles (Mader 2006). The analysis of reptile serum chemistries could have utility for assessing the health of free-ranging reptiles, given sufficient baseline data from natural habitats alongside data from a variety of seasonal and treatment variations. Most values for M. t. rhizophorarum fell within the parameters of other chelonians species (Table 4.2). The M. t. rhizophorarum value for alkaline phosphatase (ALKP) 112.08 U/L is much lower when compared with values for the
Trachemys sp., ALKP value 339 U/L (Mealey et al., 2002). The Florida Keys eastern diamondback rattlesnake population (Crotalus adamanteus) has higher mean values for
TP, uric acid, CHE, LDH and CL- (Mealey et al., 2005). It is notable, even though a small sample size, that there are significant differences between the treatment and control sites for several of these parameters. The application of these serum values within the wildlife management model is still in its infancy. Further studies with augmented sample sizes will be required to determine why the values differ between the sites.
116 Currently the interpretation of reptile biochemistries is difficult due to the lack of controlled studies and available references. Very often, the avian clinical interpretations are applied to reptiles. For example, depressed CHE levels are used as an indicator for wildlife exposed to organic phosphate (OP) pesticides. Sanchez-Hernandez (2003) has found that CHE activity was found to be a sensitive indicator in the Tenerife lizard,
Gallotia gallotti, of exposure to OP compounds. There is controversy in determining precise CHE levels acting as an indicator for exposure to an OP compounds due to the variations in CHE levels over a short period of time (Mineau et al., 1999).
Our data suggest that certain serum chemistries may be site-specific health indicators but augmented sample sizes and further analysis must be conducted to better support this contention. The data we collected helps establish baseline reference parameters of free-ranging reptiles, so interpreting these values is not certain (Mader
2006). We interpret our results to be representative of wild terrapins and found that all values appear to be within the reported parameters for other reptiles. We do believe that there is an effect present between the two sites (Table 4.2) but remain uncomfortable interpreting either site’s values as negative without longer term data from Florida Bay.
Bacterial Cultures - Similarly, the presence of microbial organisms does not signify a compromising infection since a degree of symbiosis occurs. Many of the organisms we detected assist in the reptilian digestive process and in the absorption of nutrients. Potential pathogens, (e.g. Salmonella spp.) in humans may be commensal in terrapins and may be acquired through ingesting selected prey and are perhaps eliminated over a period of time. Identifying particular zoonotic microbes such as Salmonella
117 immediately assists researchers by highlighting the necessity of limiting exposure and developing appropriate field hygiene techniques (Becker et al., 2006).
Twelve microbes were isolated from the swabs. Our microbial cultures provide the first measures of these microfauna for free ranging M. t. rhizophorarum (Table 4.3).
We did find it intriguing that E. coli was only found at the treatment site, alongside yeast, both potentially transmitted through ingestion consequences from influent non- indigenous wildlife feces. The only Salmonella detected was in a sample from the control site. The most abundant flora was shared between both sites and is likely to represent normal constituencies for these terrapins and the surrounding environment.
These results are similar to values published for Diamondback rattlesnake (Crotalus adamanteus) and the mangrove saltmarsh snake (Nerodia clarkii compressicauda) in the
Florida Keys (Mealey et al. 2005). Two strains of Salmonella sp. were isolated from approximately 25% of the C. adamanteus population. One strain of Salmonella sp. was isolated from two N. c. compressicauda, another mangrove dependent species.
In our examination of these terrapin populations we have documented a degree of fidelity to the mangrove community for this vertebrate that is unique. We are unaware of any taxon, with the possible exception of crocodiles that provides such a continuous occupancy and tight dependence for habitat as shown in the mangrove diamondback terrapin. We have taken advantage of a significant treatment manipulation of a mangrove key in south Florida and evaluated the potential effects on the terrapins living there.
Nutrients, particularly phosphorous, likely influence these plant communities, but the terrapins are more likely affected by dietary protein. For the treatment site, the increased protein in both dropped primate diet pellets and influent fecal matter appear to have
118 supported a larger number of individual terrapins, albeit of smaller overall size than the control site. Both blood serum chemistry and microbial flora differed between the two sites, but interpretation of those results is premature. The primates have been removed from the islands as of 2000 due to a court settlement and a mandate by the Florida Fish and Wildlife Conservation Commission. Our current work will seek to evaluate the trend for the treatment population as the system returns to the natural regime, although we predict it will be several years before any response is documented in the population.
While often overlooked in evaluations of the mangrove ecosystem, reptile components are both dependent and tightly integrated within these communities, potentially providing valuable vertebrate models for the study of these ecosystems.
119 Table 4.1
Morphometric Measurements (mm) Millimeters and Weight (g) Grams for the Terrapin, Malaclemys terrapin rhizophorarum, for the Study Sites TLK and CKW
Females Males TLK (N=289) (N=55) Mean Dimension (mm) SD Range Mean SD Range CL 166.57 10.35 102-189 119.81 5.56 110-135 CW 123.42 8.09 89-170 87.92 4.77 80-103 PL 149.21 8.53 110-173 101.38 4.77 93-115 PW 106.46 7.69 65-121 74.49 7.59 42-90 BD 66.2 4.53 53-91 43.92 3.17 38-53 Weight 766.45 122.11 345-1175 258.36 48.66 170-420
Females Males CKW (N=114) (N=8) Mean Dimension (mm) SD Range Mean SD Range CL 172.28 8.74 122-196 112.25 17.16 86-129 CW 127.37 6.03 89-140 81.38 12.01 63-94 PL 154.75 6.94 115-173 95.5 11.73 76-107 PW 107.5 5.39 72-120 68.38 10.14 53-79 BD 68.58 5.01 41-79 48.25 3.4 45-53 Weight 892.02 117 310-1150 221.25 72.19 120-320 Note. Measurements are for adult females and males only.
120 Table 4. 2
Serum Chemistry Values for 20 Mangrove Diamondback Terrapins (M. t. rhizophorarum) from the Lower Florida Keys
Measure N Mean SD Range Normal
GLU (mg/dl) 20 60.1 31.47 29-142 60.0-100.0
PHOS (mg/dl) 18 4.2 2.9 1.2-12.7 8.0-20.0
TP (g/dl) 13 3.33 1.09 2.0-4.5 3.0-8.0
URIC (mg/dl) 18 2.03 0.89 0.4-3.1 1.0-10.0
ALKP (U/L) 13 112.08 51.21 46-194 32.0-664.0
AST (U/L) 16 179.44 72.75 80-321 1.0-640.0
Ca (mg/dl) 14 10.51 2.19 6.3-13.6 8.0-20.0
CHE (U/ml) 13 0.39 0.13 0.22-0.68 -
CK (U/L) 11 402.72 469.84 39-1358 27.0-2731.0
LDH (U/L) 1 192 - - 15.0-586.0
ALB (g/dl) 11 1.49 0.33 1.1-2.0 1.6-3.1
Na+ (mmol/L) 4 152 17.8 131-170 120.0-170.0
CL- (mmol/L) 9 103 8.89 92-115 100.0-150.0
K+ (mmol/L) 4 5.41 2.2 2.1-9.1 2.0-8.0
CO2 (mmol/L) 12 17.78 6.3 27-Nov 12.0-18.0 Note. Column CKW vs. TLK describes ANOVA values (p <. 05) for ControlSiteKW (CKW) vs. TreatmentSiteLK (TLK). GLU, TP, ALKP, CHE, CK, CL- and CO2 were significantly different between the study sites. Column “Normal” reflects normal values for other chelonian species, other than Malaclemys, as described by Mader (2006).
121 Table 4.3
The Microbial Results of 17 Individual Cloacal Cultures of Mangrove Diamondback Terrapins (M. t. rhizophorarum) from Two Study Sites
Microbial Organisms No. Isolated % of Isolations Site
Clostridium perfringes 10 59 Shared
Aeromonas hydrophila 7 41 Shared
Providencia rettgeri 6 35 Shared
Proteus mirabilis 6 35 Shared
Citrobacter freundii 4 24 Shared
Escherichia coli 1 6 TLK
Pseudomonas aeromonas 1 6 CKW
Serratia marcescens 1 6 CKW
Salmonella arizona 1 6 CKW
Clostridium sordelli 1 6 CKW
Morganella morgani 1 6 CKW
Yeast 1 6 TLK Note. All samples were taken immediately upon capture.
122 CONCLUSION
Chapters 1 and 2
Organizations and private wildlife rehabilitators have been on the forefront of establishing normal baseline serum chemistry values for injured raptors. Wildlife rehabilitators alongside veterinarians were in need of normal serum values in order to diagnose ailments of incoming injured or debilitated raptors. The initial project was to establish baseline parameters for free ranging Bald Eagle and Osprey populations to be used by wildlife rehabilitators and zoological organizations. This phase of the project was accomplished with two published manuscripts related to health assessment parameters for two species of raptors, Bald Eagles and Swallow-tailed Kites (Mealey et, al. 2004, and Mealey et al. 2006). Future publications from this dissertation will hopefully assist veterinarians and wildlife rehabilitators in providing improved medical care to injured wildlife.
The feasibility of incorporating serum chemistries values from nestling raptors and reptiles as health monitors for free ranging wildlife will be difficult due to the wide range of the serum results. Populations of Bald Eagles and Ospreys have both declined in eastern Florida Bay since the 1990’s. Serum values results for the eastern side of
Florida Bay do not identify any health issues that would explain the population decline from the area. Even though I infer that some of the serum differences between the eastern and western side may be related to stressed nestlings, this does not necessarily indicate a certainty. Their application as a monitoring tool in free-ranging wildlife should 123 be combined with complementary ecological data when making wildlife management assessments (Newman et al., 1997, Nazifi et al. 2008).
Chapter 3
One remarkable result is the lower survival rates of first year Bald Eagles in
Florida Bay compared with other bald eagle studies in Florida, Chesapeake Bay and
Maine. The results could be attributed to the small sample size in the investigation.
Their poor survivability may also be linked to the Florida Bay ecosystem. Once they depart their natal territory and the parents are no longer providing food, the fledged eagles may be having difficulty foraging and their health is compromised prior to their movement/migration.
As eagle territories in Florida Bay continue to decline in number, it appears that some Bald Eagles are establishing nesting territories on the edge of residential areas in south Florida. One confirmed nest is in western Broward County, suspected nest
Turnpike and I-75 Broward County (BKM), and Blackpoint Marina (Miami-Dade
County). One of our last satellite tracked bird continued to return for a period of 2 years to the vicinity of Tree Top Park, Davie, FL Broward County. Funding from Federal, state and private sources are needed to maintain long-term surveys and expand monitoring projects of imperiled avian and other species of Florida Bay to capitalize on the value of these animals as critical barometers for evaluating the progress of the
Everglades restoration project and its impact on the Florida Bay ecosystem.
Chapter 4
In our examination of these terrapin populations we have documented a degree of fidelity to the mangrove community for this vertebrate that is unique. We are unaware of
124 any taxon, with the possible exception of crocodiles that provides such a continuous occupancy and tight dependence for habitat as shown in the mangrove diamondback terrapin. We have taken advantage of a significant treatment manipulation of a mangrove key in south Florida and evaluated the potential effects on the terrapins living there.
Nutrients, particularly phosphorous, likely influence these plant communities, but the terrapins are more likely affected by dietary protein. For the treatment site, the increased protein in both dropped primate diet pellets and influent fecal matter appear to have supported a larger number of individual terrapins, albeit of smaller overall size than the control site. Both blood serum chemistry and microbial flora differed between the two sites, but interpretation of those results is premature. The primates have been removed from the islands as of 2000 due to a court settlement and a mandate by the Florida Fish and Wildlife Conservation Commission. Our current work will seek to evaluate the trend for the treatment population as the system returns to the natural regime, although we predict it will be several years before any response is documented in the population.
While often overlooked in evaluations of the mangrove ecosystem, reptile components are both dependent and tightly integrated within these communities, potentially providing valuable vertebrate models for the study of these ecosystems. This phase of the project was accomplished with three published manuscripts related to health assessment parameters for four species of reptiles, Bimini Island Slider (Trachemys sp.),
Diamondback Terrapins, Eastern Diamondback Rattlesnake (Crotalus adamanteus) and the Mangrove Salt Marsh Snake (Nerodia clarkii compressicauda) (Mealey et al. 2002,
Mealey et al. 2006 and Mealey et al. 2014).
125 APPENDIXES
Permits
126
127
128
129
130
131
132
133
134 LITERATURE CITED
Allen, G. T., J. K. Veatch, R. K. Stroud, C. G. Vendel, R. H. Poppenga, L. Thompson, J.
A. Shafer, and W. E. Braselton. 1996. Winter poisoning of coyotes and raptors
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