Conservation biologists have used surrogate species as a shortcut to monitor or solve conservation problems. Indicator species have been used to assess the magnitude of anthropogenic disturbance, to monitor population trends in other species, and to locate areas of high regional biodiversity. Umbrella species have been used to delineate the type of habitat or size of area for protection, and flagship species have been em- ployed to attract public attention. Unfortunately, there has been considerable confusion over these terms, and several have been applied loosely and interchangeably. We attempt to provide some clarification and guide- lines for the application of these different terms. For each type of surrogate, we briefly describe the way it has been used in conservation biology and then examine the criteria that managers and researchers use in select- ing appropriate surrogate species. By juxtaposing these concepts, it becomes clear that both the goals and se- lection criteria of different surrogate classes differ substantially, indicating that they should not be conflated. This can be facilitated by first outlining the goals of a conservation study, explicitly stating the criteria in- volved in selecting a surrogate species, identifying a species according to these criteria, and then performing a pilot study to check whether the choice of species was appropriate before addressing the conservation prob- lem itself. Surrogate species need to be used with greater care if they are to remain useful in conservation biology.

On the Use of Surrogate Species in Conservation Biology

Environmental contamination by agricultural chemicals and industrial waste disposal results in adverse effects on reproduction of exposed birds. The diversity of pollutants results in physiological effects at several levels, including direct effects on breeding adults as well as developmental effects on embryos. The effects on embryos include mortality or reduced hatchability, failure of chicks to thrive (wasting syndrome), and teratological effects producing skeletal abnormalities and impaired differentiation of the reproductive and nervous systems through mechanisms of hormonal mimicking of estrogens. The range of chemical effects on adult birds covers acute mortality, sublethal stress, reduced fertility, suppression of egg formation, eggshell thinning, and impaired incubation and chick rearing behaviors. The types of pollutants shown to cause reproductive effects include organochlorine pesticides and industrial pollutants, organophosphate pesticides, petroleum hydrocarbons, heavy metals, and in a fewer number of reports, herbicides, and fungicides. o,p'-DDT, polychlorinated biphenyls (PCBs), and mixtures of organochlorines have been identified as environmental estrogens affecting populations of gulls breeding in polluted "hot spots" in southern California, the Great Lakes, and Puget Sound. Estrogenic organochlorines represent an important class of toxicants to birds because differentiation of the avian reproductive system is estrogen dependent.

Reproductive effects in birds exposed to pesticides and industrial chemicals.

Injection of DDT [1, 1, 1-trichloro-2,2-bis(p-chlorophenyl)ethane] into gull eggs at concentrations comparable to those found in contaminated seabird eggs in 1970 induces abnormal development of ovarian tissue and oviducts in male embryos. Developmental feminization of males is associated with inability to breed as adults and may explain the highly skewed sex ratio and reduced number of male gulls breeding on Santa Barbara Island in southern California.

DDT-induced feminization of gull embryos

Note for ornithologists who plan to use drones or model aircraft to study or monitor birds in the United States: The Airborne Hunting Act may prohibit the use of drones to study or monitor wildlife in the United States, except for state and federal agency personnel or their agents (i.e., someone who is working under contract to or in collaboration with state or federal agencies) or under a permit issued by one of those agencies. However, the USFWS will not issue such permits and only four states allow the use of drones for research. The Ornithological Council has asked the Office of the Solicitor of the Department of the Interior to determine if the use of SUA to study wildlife is subject to the AHA. Anticipating that the Solicitor will determine that the AHA does apply, The Ornithological Council has also filed a petition for rulemaking asking the USFWS to issue permits. Read more on this situation on OrnithologyExchange.org.

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Guidelines to the use of wild birds in research

-We reviewed 64 published investigations concerning effects of human disturbance on nesting colonial waterbirds. We summarized and reviewed articles, based on taxonomy, examining investigator, ecotourist, recreator, watercraft, and aircraft activity effects on physiology, reproductive behavior, reproductive success, and population trends of waterbirds. Though most studies found significant negative effects, taking careful measures minimized impact on some species. Guidelines for minimizing investigator and visitor disturbance are outlined. Little practical information for visitor management is available. Increasing pressure from the ecotourism industry to visit waterbird colonies makes research that develops scientifically-defensible tourism policies imperative. Received 27 December 1997, accepted 27 April 1998.

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A review of human disturbance effects on nesting colonial waterbirds

The human influence on seabird nesting success: Conservation implications

Although still about 30 percent too low for population stability, productivity of California brown pelicans at their two northern colonies has improved significantly since 1971. Numbers of adults breeding probably reflect food supplies and recruitment from more successful colonies to the south, but improving fledging rates (up to 0.9 young per nest in 1974) reflect better egg survival and improving eggshell condition, with declining DDE contamination in anchovies, their major food source.

Brown pelicans: improved reproduction off the southern California coast

Introduced Small Ground Predators in California Brown Pelican Colonies

1 Appendix 1. Summary of currently active and otherwise-known breeding colonies of the Appendix 2. Summary of currently active and otherwise-known breeding colonies of the Appendix 3. Summary of currently active and otherwise-known breeding colonies of the

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Daniel W. Anderson

Papers

The human influence on seabird nesting success: Conservation implications

Brown pelicans: improved reproduction off the southern California coast

Introduced Small Ground Predators in California Brown Pelican Colonies

Size of the California Brown Pelican Metapopulation During a Non-El Nino Year