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Hutto, R. L. 1998. Using landbirds as an indicator species group. Pp. 75-92 in Marzluff, J. M., and R. Sallabanks (eds.), Avian conservation: Research and Management. Island Press, Covelo, CA.
In reference to the National Forest Management Act of 1976, the Code of Federal Regulations [36 CFR 219.19(a)(1 and 6)] specifies that the U. S. Forest Service monitor vertebrate indicator species as a means to ensure that they are maintaining populations of all vertebrates. The approach has not met with a great deal of success, however, partly because traditional indicator species are too few, and partly because monitoring itself has proven difficult. By initiating a landbird monitoring program designed to uncover habitat distribution patterns and population trends of a large number (>100) of non-traditionally monitored landbird species, the USFS Northern Region has recently begun to rectify some of the problems associated with the indicator species approach to wildlife conservation. Between 1989 and 1994, field crews conducted more than 8815 point counts across 955 multi-point transects that were geographically stratified across the region. Results reveal that the vast majority of possible breeding species was detected, and that more than 100 species were detected on 30 or more points, which is probably sufficient to build reliable bird-habitat relationship models. These first-generation models reveal that numerous landbird species are extremely specialized in their use of vegetation cover types that are either much less widespread on the landscape now than they were at the turn of the century (e.g., post-fire standing-dead forests, old-growth cedar, grassland) or, if not less widespread, are much altered due to grazing practices (e.g., riparian bottomlands). Even though populations of a species fluctuate from year to year, the relative abundances among broadly defined vegetation cover types are not likely to do so. Thus, one benefit of such a monitoring program is that objectively based, field derived habitat relationship models are possible to obtain from as little as a single year's field effort. Results from monitoring in the USFS Northern Region already demonstrate some clear limits within which any agency aspiring to maintain ecological integrity must work.
The broad goal of conservation biology is to maintain "biodiversity", which has been defined as the diversity of life at all levels of biological organization, from genes to landscapes (Office of Technology Assessment 1987). A variety of laws, beginning with the Organic Administration Act of 1897 through the Multiple-Use Sustained-Yield Act of 1960 to the National Forest Management Act of 1976 [16 USC 1604(g)(3)(B)], either encourage or mandate that the U.S. Forest Service provide for the diversity of plant and animal communities. The Code of Federal Regulations [36 CFR 219.19(a)(1 and 6)] specifies that this be accomplished by monitoring vertebrate indicator species as a means to ensure the maintenance of populations of all native vertebrate species. Numerous laws require essentially the same thing of the U.S. Fish and Wildlife Service, the Bureau of Land Management, and many state agencies.
Because of the operational difficulties of implementing the aforementioned legislation, agencies typically attempt to accomplish this task by assuring the maintenance of a small number of "indicator" species that, in turn, supposedly assure the maintenance of the complete range of vertebrate species (Severinghaus 1981). Agencies such as the U.S. Forest Service also typically work at a regional (or smaller) level to implement such legislation (Morrison and Marcot 1995). Thus, I wish to focus attention here toward avian conservation efforts at the within-region level and away from avian conservation programs that are national in scope (e.g., BBS, CBC, BBIRD, MAPS), even though the latter may provide data that influence management decisions at the local level.
Which species should serve as indicators for implementation of the NFMA? The earliest suggestion (Graul et al. 1976, Graul and Miller 1984) was to use a series of the more stenotopic species. If we choose the most stenotopic species as indicators, however, it is unlikely that the maintenance of viable populations of all species can be assurred throughout their historic ranges (as required by the National Forest Management Act of 1976, for example) unless we use enough of them to cover the entire range of ecological conditions.
Landres 1983, DeGraaf et al. (1985), Roberts and O'Neil (1985), Fry et al. (1986), and Roberts (1987) subsequently suggested using representative species from different ecological guilds (guild indicators), but empirical data do not support the idea that population trends of species within a guild mirror one another at all closely (Mannan et al. 1984, Szaro 1986, Block et al. 1987, Bayer and Porter 1988, Reader 1988). Consequently, the suggestion to use selected species from each of a variety of guilds has been met with criticism (Hutto et al. 1987, Landres et al. 1988, Morrison et al. 1992).
Verner (1984) suggested using management-guild indicators, which he defined as groups of species that are suspected to respond in a similar way to changes in the environment. The latter, whole-guild approach avoids the problems inherent in the guild-indicator approach because it is designed to identify species that would be expected to share either the negative or positive effects of land management activity because they share a particular forest zone. Even here, however, the problem is that populations are affected by numerous factors that operate at different times of the year (Sherry and Holmes 1995). Thus, it is quite possible for the declining populations of one member of a management guild to be hidden by a general increase in the populations of others. In fact, using population trend data from the Breeding Bird Survey, Paige (1990) showed that there is really no group of species whose population trends mirror one another and which, therefore, would serve as a good group for a combined-species analysis.
Many are now coming to believe that we need some sort of ecosystem-level approach whereby we maintain and monitor the full range of "ecosystems". Some (Franklin 1993, 1994) claim that this is the only way some species will be conserved because we cannot monitor all of them. Others argue that an ecosystem approach is destined to fail because we cannot even define an ecosystem (Orians 1993); we have a hard enough time trying to define what a species is for conservation purposes (Rojas 1992)! There are still other discussions that revolve around the recommended use of compositional indices (e.g., Anderson 1991; Götmark 1992; Karr 1987, 1991; Angermeier and Karr 1994; Kremen et al. 1994).
Given the difficulties of working with indicators based on the ecosystem level of biological organization, sentiment seems to be converging toward something like that expressed by Noss (1990), who suggests using a hierarchical approach that includes monitoring compositional, structural, and functional elements at a variety of spatial scales. This plays on earlier ideas (expressed by Franklin 1988) that a preoccupation with compositional diversity has come at a cost in terms of awareness of structural and functional diversity. Neither Noss nor Franklin recommends creating a composite index of biological integrity; rather, they recommend monitoring a variety of parameters across combinations of elements and levels. Thus, at the species level of biological organization, we will need to know what is present (composition) and something about the demographics associated with those species (function), as advocated by DeSante and Rosenberg (this volume, chapter xx). While species are not likely to be the only indicators of ecosystem health, it is likely that we will continue to use them as indicators at that particular level of biological organization, which brings us right back to the question of which species to use.
If we are going to retain the use of indicator species in conservation efforts, we must recognize that, from a purely theoretical standpoint, the indicator species approach to maintaining populations of all vertebrate species cannot be expected to work well (Hutto et al. 1987, Landres et al. 1988). Specifically, because no two species occupy the same niche, the maintenance of several indicators cannot be expected to assure the maintenance of all other species, despite arguments to the contrary (e.g., Tracy and Brussard 1994). There is little reason to expect that a small group of species will serve as much more than a crude "coarse filter". Evidence from the Northern Spotted Owl (Strix occidentalis) scenario shows that current conservation plans do not come close to meeting needs of fish, the Marbled Murrelet (Brachyramphus marmoratus), and other species (Franklin 1994).
From a practical standpoint, the indicator species approach has not worked very well either. There are at least four reasons for the practical failure of this approach to conserve vertebrates in general, and birds in particular. First, because we cannot monitor all species, we spend excessive amounts of time trying to decide which species to monitor (Thibodeau 1983), and when all is said and done, the majority of indicator species are still relatively restricted to a combination of Threatened and Endangered species, and those taken for food, sport, or hides. The transition from an ecologically narrow "game production" mentality to truly broad-based conservation biology has been slow at best. In addition, we are destined to keep adding species to the list of difficult-to-monitor "indicators" because most agencies are required to include (the ever increasing number of) Threatened and Endangered Species. We cannot develop and maintain regional monitoring programs for an ever increasing number of rare species (Franklin 1993).
Second, the only way we might expect a subset of species to represent the needs of all others is for the subset to subsume the ecological conditions of all others. Unfortunately, the indicator lists are almost certainly too short and too ecologically narrow to accomplish such a task. Some forests in the USFS Northern Region, for example, have as few as five "Management Indicator Species", and no forest includes more than 22 on its list (Table 1). Moreover, most indicators are traditionally managed game species and fur bearers which, coupled with the small number, brings the efficacy of such indicator groups into question.
Third, the cost required to monitor traditional indicator species has been prohibitive because of the techniques needed to monitor rare species. Consequently, there is virtually no monitoring of either population trends or land-use effects on selected indicator species, even though such monitoring has been legally mandated for more than 20 years.
Lastly, despite what many view as an enormous success story associated with the few indicator species that are monitored (e.g., elk), numerous vertebrate species, including fish (Moyle and Williams 1990, Frissell 1993), amphibians (Barinaga 1990, Blaustein and Wake 1990, Phillips 1990), and migratory songbirds (Terborgh 1989, Askins et al. 1990, Robbins et al. 1993) are apparently falling through the cracks.
These limitations suggest that wildlife biologists in agencies such as the Forest Service, Fish and Wildlife Service, and Bureau of Land Management may need to change the approach they use to meet their legal mandates to maintain wildlife populations. While the agencies themselves are in the midst of changing their operational emphases away from maximizing the production of certain commodities toward both sustainable commodity production and the maintenance of ecological systems, this is an ideal time to either abandon (e.g., Morrison and Marcot 1995) or modify the current indicator species approach.
What kind of change might serve to improve the existing indicator species approach? I argue here for inclusion of one or more indicator species "survey groups" as part of any comprehensive indicator scheme. I define an indicator species survey group as any group containing a large number of species that can be monitored simultaneously through a single survey method. Sparrow et al. (1994) provide arguments why butterflies might make a good indicator group in this sense. Specifically, I recommend broadening the list of desired indicator species to include most landbird species because most can be detected using a simple point-count survey methodology. In fact, I would suggest that there is no better tool than a landbird monitoring program to enhance the effectiveness of wildlife conservation efforts. Why? (1) Landbirds are not only the most visible of vertebrate species, they also advertise their presence and identity through vocalizations. Thus, systematically collected field data are much easier and less expensive to gather for landbirds than they are for traditionally managed species that require trapping, radio tagging, locating, and so forth; (2) because patterns of occurrence in the field are easily uncovered, the foundation of field data upon which habitat suitability (HSI) models are built is potentially much stronger for landbirds than it is for most of the existing management indicator species; (3) using a single survey method, one can collect data on nearly 200 bird species simultaneously. Sure, many species will not be monitored well, but having to manage for the maintenance of those that can be monitored will probably bring us much closer to maintaining populations of all vertebrates than would the still prevalent approach of managing entirely on the basis of a select few indicator (mostly game) species. This is especially true if we combine landbird monitoring with continued management for the traditional indicator species; (4) having to manage for the maintenance of many landbird species will force movement toward management at broader spatial scales. This is because the indicator species list will now be large enough and ecologically broad enough to reveal some species that will benefit from, and others that will be harmed by, any proposed land-use activity. This would appear to lead managers into a no-win situation because any proposed land-use alternative will hurt something, but the way out of this apparent dilemma is to expand one's focus beyond the immediate project area. In fact, by realizing that local populations of some species will invariably be harmed by any proposed land-use action, it forces us to expand our perspective toward broader landscapes. It is only at the landscape level that we can provide a plan or vision that will provide enough of each landscape element to maintain the populations of, and honestly claim "no effect" on, all vertebrate species. The local extinction of a species due to some land management activity is fine as long as the suitability for that same species is expected to increase at the same time in another part of the landscape (due to some other land-use activity or ecological succession, for example).
Because we will never fully understand the habitat requirements of all vertebrate species, I still believe the indicator approach is necessary; it merely needs to be applied in a way that avoids the pitfalls of managing entirely on the basis of the needs of just a few high-profile species.
What generalizations emerged from these simple models of bird distribution among habitats? Some landbird species are very restricted to specific, naturally occurring ecological conditions that are themselves restricted in spatial extent, or at least less extensive than they were at the turn of the century. Obviously, the loss any one of these cover types will mean the loss of those bird species that are relatively restricted to it. Thus, it should be clear that we need to maintain each of those cover types (defined at least as finely as defined here) on the broader landscape, although it is unclear how much of each needs to be retained to maintain viable populations of any given species. Even if we are not about to lose a given cover type from the broader landscape, land use practices within and surrounding that type may have important implications, especially for species restricted to that cover type.
We need more data on occurrence of species among a broader range of existing vegetation cover types, especially cover types that result from land-use activities. As crude as such information might be, it is far better than the information provided by a typical field guide, and should be the foundation beneath speculation about the projected effects of any land management plan on a given wildlife species. Armed with a solid understanding of which cover types are occupied by a given species, we can then proceed with comparisons of various measures of fitness among the occupied cover types to ensure that presence is not a misleading indicator of habitat suitability. Altered habitats need much more attention than they currently receive because "unnatural" structural changes are likely to uncouple habitat selection stimuli from factors that ultimately determine an individual's success, thereby creating "ecological traps".
Land management agencies should be actively engaged in the process of adaptive management, whereby effects on selected species are constantly monitored by agency and other researchers so that land-use practices can be modified on the basis of this continual appraisal of land-use effects. Finally, we should seek additional groups of species that can be monitored through single field methods so that habitat relationships can be built for, and land management decisions made on the basis of, as wide a range of species as possible.
I realize that measures of presence or probability of occurrence do not necessarily reflect suitability, but before we worry too much about whether two cover types are equally suitable, we first need to be able to predict where a species is likely to occur at all! The occurrence data described here have uncovered numerous (outlined in Hutto and Young 1999) potential "ecological trap" problems that need study. Thus, monitoring data like these can serve to focus future research efforts toward particular species or situations.
Even though populations of a species fluctuate from year to year, the relative abundances among broadly defined vegetation cover types do not (e.g., Sallabanks 1996). Thus, the value of a monitoring program such as this one should be readily apparent: objective results are possible to obtain from as little as a single year's field effort, and the results already demonstrate some clear limits within which any agency aspiring to maintain ecological integrity must work.
Programs like this one would benefit other USFS regions and (especially) other agencies, but I would in no way suggest that this sort of research should take priority over other kinds of research. In fact, the limiting factor in bird conservation seems to be a willingness to use information on land-use effects, not a shortage of such information. Wildlife conservation depends, ultimately, on attitudes of the public about the value of wildlife. And perhaps people's attitudes about wildlife conservation are less likely to be changed through results from largely descriptive research such as that which I've just described than from other kinds of research (e.g., behavioral studies). We should judge the conservation potential of proposed research on the basis of the stated research justification, period. Attempts to define research "needs" otherwise are largely misdirected; what we "need" is the widest possible variety of quality research.
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