B A C K G R O U N D
Most efforts in biogerontology have emphasized short-lived small animals that can be easily studied in the laboratory. Research on genetically defined strains of mice, flies, and nematodes continue to give remarkable insights intothe genetic basis for longevity and in mechanisms of aging. It is now clear that certain processes of aging at the molecular, cellular, and organ system levels in non-human models show similarities to those in long-lived humans, e.g., accumulation of oxidative damage to proteins in aging nematodes and aging mice. However, it is also clear that some features of aging in long-lived humans are not well represented in short-lived animals, e.g., the absence of Alzheimer-type neuropathology in aging mice. Thus,long-lived primates have acquired an important role as biogerontological models, e.g., rhesus monkeys (>30 year life span), which are being studied for brain aging changes and for dietary and pharmacological interventions.

We believe it is timely and feasible to consider additional long-lived models. We have therefore organized the first meeting to give an extended review of evidence on organisms with very slow aging. SOSA will consider additional species not in the current biogerontology literature that have life spans extending beyond those reported for primates. In some cases, these life spans exceed the record human life span of Jean Calment, who died in 1997 at 122 years.

SOSA will feature fish, birds, turtles, and vascular plants. Some of the species to be discussed came to C. E. Finch’s attention during the writing of Longevity, Senescence, and the Genome (1990), which included a chapter (#4) on the possibility that some multi-cellular organisms age so slowly that changes are undetectable ("negligible senescence").The topic of very slow aging is incidentally mentioned in diverse contexts, e.g., long-lived dwarf trees clinging to cliff-side ecosystems (Larson, 1999) and in the slow reproductive schedules of very long-lived fish, e.g. rockfish and the orange roughy, whose populations are declining sharply because of great commercial pressure (Koslow, 1997).

The possibility of negligible senescence has not been widely discussed, and appears to be in conflict with Hamilton’s (1966) mathematical deduction from population theory that "...senescence will always creep in". Evolutionary theory predicts that the force of natural selection should decline after maturation at rates which are governed by the reproductive schedule. Thus, selection for earlyreproduction will tend to shorten life span. These predictions are well validated in experimental selection for early vs late reproduction in laboratory fruit flies (Rose, 1999). Similar results are indicated in natural populations through predatory pressure for early onset of reproduction, which is associated with increased reproduction during a statistically shorter life span in opossums (Austad, 1993) and in a fish, the guppy (Reznick et al., 1997; unpublished). We note that nearly all tests of theevolutionary hypothesis have emphasized short-lived species for practical reasons and that the reproductive schedules and patterns of aging of very long-lived species is little characterized.

Candidates for the possibility of negligible senescence was discussed in half-day Workshops on Negligible Senescence (WONS 1-3), which were organized by C.E. Finch at USC in 1997, 1998, and 1999. These small workshops were supported with funds from a K07 Award to C.E. Finch which can not meet the expenses of this longer meeting with more participants who must travel longer distances. Participants in these workshops included field biology scientists who have shown their willingness to share data and tissue samples. About 40 scientists and trainees from local institutions attended each of these workshops (mainly USC and UCLA, but also several from CalTech and CalState LA). For the proposed meeting, we decided to adopt a more conservative name for this symposium, "slow aging", rather than"negligible senescence", so as to provide a the broadest possible platform for discussion to minimize implicit assumptions or hidden biases about the nature of aging processes. We give four examples in order of documented longevity: turtles, birds, rockfish, and bristlecone pines.

Turtles: The most detailed information on demography and longevity of turtles comes from studies of J. D. Congdon on Blanding’s-, painted-, and snapping turtles on the E. S. George Reserve in southern Michigan (Congdon et al. 1993, 1994). These populations have been individually marked since the 1950’s, and some individuals were marked earlier in the century, and thus aging is completely reliably. One Blanding’s turtle produced a normal clutch of eggs at an age of 77 years. Across turtles as a whole, age at maturity ranges from 6 to 21 years and the greatest recorded longevity exceeds 80 years. A number of long-term studies of turtle populations are underway in different parts of the world, particularly focusing on threatened species such as the loggerhead sea turtle (Heppell et al. 1996). Aging such long-lived animals in the wild depends on assumptions about age-length relationships or the reliability of "annual" growth rings (Bjorndal et al. 1998), but very old individuals can be identified. New isotopic andracemization techniques should give reasonable estimation of age in these populations. In addition, many species are kept in zoological parks and have detailed records associated with their husbandry. Although turtles and other reptiles can achieve old age, they also differ from mammals in their low body temperatures and low metabolic intensities. Many species, particularly in temperate latitudes, undertake extended periods of hibernation as well. It would be of great interest to determine which aspects of their physiology influence the rate of aging, e.g. through comparative experimental work on shorter lived turtle species.

Birds: The demography of birds, including aging-related increase in mortality rate, has been well characterized in both natural and captive populations (Holmes and Austad 1995; Ricklefs 1998, 2000). Maximum life spans of birds vary from about 10 years to more than 100 years. Life span increases with body size, but also varies by a factor of three or more among species of similar size.More strikingly, considering individuals of the same size, birds can live three or four times longer than mammals on average, for example up to 20 years in the case of mouse-sized sparrows and 40 years in the case of 40-gram storm petrels. The longest recorded life spans among birds to date are albatross 75 years, condor 80 years, macaw 90 years. Even the tiniest of birds, the hummingbirds, have recorded life spans of 15 years (Calder 1989).

Many long-lived birds require 10-12 years to reach sexual maturity, have low reproductive rates, and exhibit demographic characteristics similar in many ways to humans. These longevity records must also be viewed in the physiological context of the high body temperatures, high blood glucose, and high metabolic rates ofbirds relative to mammals (Holmes and Austad, 1995). For example, the combination of 4-fold higher basal blood glucose and 4 C higher temperature would predict rampant nonenzymatic glycation during long avian life spans. But there are no measurements ofglycooxidation in avian collagen or elastin from long-lived individuals to evaluate this issue! Clearly, birds possess mechanisms to prevent or repair deterioration associated with aging while maintaining a high level of individual performance. At present, prospects for non- to moderately-invasive aging research on natural and captive populations of birds is excellent, owing to many continuing population studies in the field and large numbers of individuals in captive populations of some species in zoological institutions.

Demographic analyses suggest increasing mortality rates with age due to an increase in intrinsic causes of death (e.g., tumors, cardiovascular disease), although causes of death are not well understood. Thus, in addition to physiological measurements, compilation of medical records for captive zoo populations will be very instructive. Finally, little is known about reproductive senescence in birds, but data currently available can be compiled for many natural and captive populations. The most prominent candidates for studies of slow aging in the wild are various species of seabirds, including gulls, petrels, albatrosses, and penguins, whose populations have been monitored for decades. Among captive birds, likely candidates include largeraptors (e.g., condors) and psittacines (especially macaws and cockatoos). Many smaller, readily available species, such as sparrows and starlings, provide useful models for experimentally invasive studies of aging in species that can live to 20 years or more.

Aquatic vertebrates Important candidates for very slow aging are certain deep-dwelling rockfish of the genus Sebastes in the Northwest Pacific, which that live beyond 100 years, and to at least 140 years, according to natural radioisotope dating (Fenton et al., 1991; Mulligan and Leaman, 1992). Other supracentenarians occupy similar habitats in the southern hemisphere: the orange roughy (Koslow, 1997) and warty oreo (Stewart et al 1992). Reviewers of this proposal may have enjoyed the tasty orange roughy which is being harvested towards extinction (Koslow, 1997). The few old rockfish examined had abundant, newly formed eggs and no gross organ pathology or other indications of ill health at advanced ages (X. de Bruin, R.. Gosden, C.E. Finch, B..M. Leaman, in prep.). Studies of telomerase have been started on other fish (Klapper et al., 1998a). Moreover, some marine mammals also achieve centenarian life spans, as recently indicated for two species of whales by D-aspartate dating ( George et al., 1999;Jeffrey Bada, pers. comm). Study of these fascinating animals has barely begun. Collections of specimens for detailed histopathology and assessment of molecular oxidation is a high priority.

Bristlecone pines Many studies indicate undiminished reproduction and growth functions in extremely long-lived conifers. The record life span is held by a Great Basin bristlecone pine at 4,862 years in the high Nevada mountains, but many other individuals are 2000+ years (Lanner, 1999). Of great interest is the absence of age changes in sexual reproduction of trees aged 700 to 4,700 years, as judged by lab studies of pollen germination, by seed weight, and by seedling growth rates (Connor and Lanner, 1991). Remarkably, parental age did not alter the frequency ofabnormal germinants (putative mutations). Nor did age alter the annual vegetative growth of shoots and cambium (Connor and Lanner, 1989). It is of high interest to know seed viability in trees of many other genera that live and grow for millennia (Larsonet al., 1999; Lanner, 1999).

Natural death of these ancient trees seems to be due to external hazards, particularly fire, loss of root mass through soil erosion, and fungal rot enabled by boring insects (Lanner, 1999). The oldest trees live at the highest elevations, whereas at lower altitudes, life spans rarely exceed 1,500 years; at higher altitudes, these trees are less exposed to boring insects and competition from other trees. Many other plants show striking ecological influences on maximum life span (to be described at this symposium by Deborah Roach; Roach et al., in press). One may consider that the recent expansion of human life spans (Vaupel et al., 1998) parallels that of bristlecone pines at high altitude, and may be due, in our case, to improvements of hygiene and nutrition that adventitiously favored greater life spans.