Migratory connectivity and the conservation of migratory animals.

• Author: Marra, Peter P.

1. INTRODUCTION II. THE IMPORTANCE OF MIGRATORY CONNECTIVITY III. APPROACHES FOR MEASURING MIGRATORY CONNECTIVITY A. Marked Animal Approaches B. Molecular Genetic Approaches C. Stable Isotope Approaches IV. LEGAL IMPLICATIONS OF MIGRATORY CONNECTIVITY STUDIES A. Improving Conservation Decision Making with Migratory Connectivity. 1. Acquiring Habitat Through Eminent Domain 2. Conserving Critical Habitat of Endangered Species 3. Assessing Impacts to Migratory Species 4. Expanding Judicial and Administrative Standing B. Implications for Regime Design in International Wildlife Conservation Treaties 1. General Conservation Agreements 2. Threat-Specific Conventions 3. Site-Specific Conventions 4. Conventions Aimed at Migratory Species C. Customary Law: Shifting Migration from Common Concern to Shared Resource V. Strengthening Social Connectivity A. Enhancing Conservation Connectivity B. Educational Connectivity VI. CONCLUSION I. INTRODUCTION

   Migration is the repeated seasonal movement to and from a breeding area. (1) The linking of individuals or populations within a species range is known as migratory connectivity. This includes not only the geographic linking of breeding, migratory, and wintering areas of given populations, but also an understanding of how demographic components, such as sex and age, relate to the annual distribution of these populations in geographically linked areas. Currently, we know the overall year-round ranges for most species, but we have a poor understanding of their migratory connectivity. (2) Not known is where individuals or populations, including different age and sex classes, go subsequent to breeding or whether these populations mix or remain independent of one another. (3) What is known is that events during one period of the annual cycle, such as reproductive success and survival, can be driven by events in previous periods--often thousands of miles away and often across international boundaries--where legal protection can be different, if not absent.

   In this Article, we review and discuss why understanding migratory connectivity is essential for the conservation of migratory animals and consider legal and other approaches in response to this understanding. Both the individuals and the habitats upon which they depend for their various life history stages (e.g., reproduction, molt, growth, and migration) throughout the year need protection. We argue that existing conservation efforts, including domestic laws and international treaties, can be made more effective by considering information on migratory connectivity. Advances in our understanding of the migratory connectivity of different species populations between regions and countries could also help to build "social connectivity"--the cultural, educational, economic, and institutional linkages between these same regions and countries. Increased social connectivity between distant locations that share biological resources will build a more reliable foundation for effective and sustainable conservation efforts to protect migratory species.

2. THE IMPORTANCE OF MIGRATORY CONNECTIVITY

   Migration varies across species and can include seasonal migrations across latitudes, altitudinal migrations up and down mountains, and migrations that can span multiple generations over space and time. (4) It is found in all major groups of animals, both invertebrates and vertebrates, including insects (e.g., dragonflies and butterflies), (5) fish (e.g., eels and salmon), (6) amphibians (e.g., salamanders and toads), (7) reptiles (e.g., snakes and sea turtles), (8) birds (e.g., terns and warblers), (9) and mammals (e.g., wildebeest and whales). (10)

   The Gray Catbird (Dumatella carolinensis) is an example of a longdistance migratory songbird that migrates across latitudes and is also a common backyard breeder in the eastern United States. (11) Post-breeding in the autumn, catbirds leave on a long-distance migration for their wintering grounds where they spend the majority of their annual cycle and then return north the following spring to breed. (12) The birds often return to the same exact location (within meters) where they bred the previous year. (13) Although the general nature of this remarkable boomerang journey has been known for years and continues to inspire and befuddle us, only recently--due to technological advances in our ability to track birds--did we come to learn where specific breeding individuals and populations spent the winter. During the 2009 breeding season, scientists from the Smithsonian's Migratory Bird Center attached miniature daylight level data loggers to the backs of 20 breeding catbirds in the Washington, D.C. suburb of Takoma Park, Maryland. (14) Diiring the subsequent breeding season, six of these catbirds were recaptured, the data loggers recovered and the mysteries of their migratory journey revealed. (15) Scientists learned the exact day of departure from Takoma Park and the exact day of arrival at the wintering grounds. (16) Four of the catbirds spent the winter on the island of Cuba and two in the Everglades of Florida. (17) The scientists also discovered which states the individuals stopped in during migration to build fat stores for their migratory journey. (18) Such advances in understanding "migratory connectivity" are still in their infancy, but the implications for wildlife conservation in the future could be profound.

   Species, such as the gray catbird, which move north and south between breeding areas in North America and non-breeding areas in the Caribbean, Central America, and South America, are considered Nearctic-Neotropical migratory birds. (19) Such species spend approximately three months of the year at breeding areas at temperate latitudes. Individuals then replace feathers, a process known as molting, accumulate fat stores for energy consumption during migration, and migrate south in August and September to a distant, ecologically dissimilar, and politically distinct location, often within the tropical latitudes. (20) The fall post-breeding migration can take one to three months and involve several stopovers for refueling on the way south. (21) The individuals will spend the majority of the annual cycle, approximately six to eight months, at their stationary non-breeding area. (22) Depending on the species, these animals will either remain in their territories, roam locally, or at most, roam regionally. (23) From March to May--depending on the species and wintering location--individuals once again begin to accumulate fat stores, depart wintering areas, and commence on a northward spring migration to return to breeding areas. (24) Areas to which individuals or populations of most species departing breeding or wintering areas go still remain a biological mystery, largely because of technological limitations. The animals themselves are small, and the areas they traverse are vast, making their annual cycle movements nearly impossible to track.

   In addition to challenges relating to tracking their movements, protecting these diverse species is remarkably complex, in part due to the disparate geographic areas they occupy at different times of the year. As we argue below, effective conservation requires taking into account the geographic linkages of breeding, migration, and wintering populations. This will mean protecting the habitats upon which they depend for their various life history stages (e.g., reproduction, molt, growth, and migration) throughout the year. For a sea turtle, this means protection of important nesting beaches as well as the oceans that are essential for foraging, mating, and survival during the rest of the year. For a Nearctic-Neotropical migratory bird, this means protecting important temperate breeding habitats, temperate and tropical stopover sites during fall and spring migration, and the tropical wintering habitats where they spend the majority of the annual cycle. Protecting such sites for linked populations of a species across such broad geographic expanses will be difficult and will likely necessitate novel approaches and information from the biological, social, and legal disciplines.

   The geographic linking of individuals or populations between different stages of the annual cycle, including between breeding, migration, and winter stages, is known as "migratory connectivity." (25) Currently, we know the overall year round ranges that most, but not all, animal species occupy throughout the year. (26) For some restricted-range species (i.e., those that have small breeding, migratory, or wintering areas), species conservation will depend on the protection of one or all of those restricted geographic areas.

   Two examples of range-restricted species include the monarch butterfly (Danaus plexippus) and the Kirtland's Warbler (Dendroica kirtlandii) (Figures 1 and 2). The Monarch butterfly's life cycle starts with an egg laid on the leaf of a milkweed (Asclepias spp.) plant. (27) After four days, a caterpillar (larvae) emerges, feeds on the milkweed for about two weeks, and then forms into a pupa (chrysalis).28 Approximately ten days later an adult butterfly emerges and the cycle is repeated. (29) The spectacular migratory story of the Monarch begins as individuals migrate south to a restricted wintering region in the mountains of Michoacan, Mexico, where they spend several months in one of about ten local populations. (30) Here, millions of Monarchs drape cedar trees at high elevations and then in early spring begin migrating north, stopping along the way to breed, lay eggs and die. (31) The cycle is repeated through four generations as the animals move north. The fourth generation adults are the individuals that migrate south again to Mexico. (32) Aside from small wintering populations in Florida and southern California, all Monarchs breeding in the United States and Canada winter in this small area of Mexico. (33) The long-term stability of this population is largely...