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The Society for Integrative and Comparative Biology
The Evolution of Life Histories in Holo-anhydrobiotic Animals: A First Approach1
1 Department of Theoretical Ecology, Lund University, Ecology Building, S-223 62 Lund, Sweden
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SYNOPSIS |
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TOP
SYNOPSIS
CHARACTERISTICS OF HOLO...The life histories of holo-anhydrobiotic animals differ from those of all other organisms by a regular or irregular entrance into an ametabolic state induced by desiccation. Such ametabolic periods will arrest growth and reproduction completely and thus affect primary life history parameters dramatically. The selective forces and the genetic and physiological trade-offs acting on anhydrobiotic animals are to a large extent unknown. Assuming low growth rates and low juvenile to adult survival, general theoretical models on life history responses to stress predict that anhydrobiotic animals will be selected for a high degree of iteroparity, with low fecundity, large egg size, and low total reproductive investment. A high degree of variability in growth and reproduction should create a selective force in the same direction. Although basic empirical data on life history parameters are very scarce, available observations seem to be consistent with this prediction.
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CHARACTERISTICS OF HOLO-ANHYDROBIOTIC LIFE HISTORIES |
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Anhydrobiosis represents one of several distinguished categories of cryptobiosis, or ametabolic dormant life forms (Keilin, 1959
; Womersley, 1981; Wright, et al., 1992; Wright, 2001). In anhydrobiotic organisms, the ametabolic state is induced by desiccation. Such organisms are obviously able to survive in generally very dry and/or cold environments, such as deserts or polar areas. Very often, however, anhydrobiotic organisms are found in much less extreme environments but within microhabitats that are exposed to more or less frequent periods of desiccation. For anhydrobiotic organisms inhabiting these habitats we would expect the conditions for growth and reproduction to be strongly influenced by the recurrent desiccating conditions. Still, life histories in these organisms and the selective forces acting on them are poorly known.
Anhydrobiotic organisms are found in a variety of biological taxa, including both unicellular and multicellular organisms, and from both the animal and plant kingdom (Keilin, 1959; Clegg, 2001). In this paper, I will focus on anhydrobiotic animals, and more specifically those in which anhydrobiosis is utilised throughout the life cycle, from the egg to the adult stage. Such populations may be called holo-anhydrobiotic in order to distinguish them from animals where anhydrobiosis is restricted to specific developmental stages (e.g., Artemia cysts [Clegg 1967], Polypedium larvae [Hinton, 1960]). The main taxonomic groups where holo-anhydrobiotic animals are found are nematodes, rotifers and tardigrades. The life histories of these organisms consist of active periods of growth and reproduction, interrupted by periods of total metabolic inactivity imposed by desiccating environmental conditions. Growth and reproduction then come to a complete halt, and the only demographic characteristic of the organism is survival. Anhydrobiosis represents an escape in time from hostile conditions, as opposed to an escape in space employed by organisms with an ability to migrate away from unfavourable conditions. The frequency of periods inducing anhydrobiosis is often high enough, and the life span of the organism long enough, to make the environment "fine-grained" sensu Levins (1968), i.e., an individual organism will experience both dry and wet conditions repeatedly during its life-time. Fine-grained environments generally favour single-type phenotypes (Levins, 1968, 1969). Among fine-grained heterogeneous environments, those experienced by holo-anhydrobiotic organisms must be considered some of the most extreme, in terms of the physical extremes of temperature and water potential.
Although my main focus here is on anhydrobiosis, most of the discussion in this paper is equally relevant to other forms of cryptobiotic life states, in particular cryptobiosis induced by cold (cryobiosis). Supposedly, the general life history effects will be the same regardless of whether the animal becomes ametabolic from desiccation or freezing. Under this assumption, I will refer to studies in both dry and cold environments.
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ANHYDROBIOSIS AND THE CONCEPT OF STRESS |
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Exposure to desiccating conditions imposes a high level of potential physiological stress. The concept of stress has been defined in many ways (see, e.g., Hoffmann and Parsons, 1991
), some definitions focusing on the source of stress (stress factor, or stressor) while other definitions focus on the effects on organism performance of the stress factor. It is clear, however, that an ecological or evolutionary definition of stress must take the latter perspective, i.e., evaluating stress from the impact on organism performance, eventually in terms of fitness (Sibly and Calow, 1989; Calow, 1989).
Hoffmann and Parsons (1991) distinguished between two main responses to stress: stress resistance and stress evasion. Anhydrobiotic organisms do not readily fall into one or the other categories of this classification. Anhydrobiotic organisms do not resist desiccation, although the rate of desiccation may be controlled and modified by various behavioural, morphological or physiological adaptations (Womersley and Ching, 1989; Wright, 2001; Ricci et al., 2003). However, they also do not escape an impact of the stress factor, since at least growth and reproduction is dramatically reduced. Thus they do not readily fit into the concept of stress evasion. However, in one (rather peculiar) sense anhydrobiotic organisms do evade the stress of desiccation, by dehydrating to such an extent that further desiccation is not possible under natural conditions. The organism has then escaped desiccation as a factor of stress. But it has certainly not escaped the impact of the stress factor on fitness. At least with respect to survival, "stress tolerance" may be a more appropriate term than stress evasion since anhydrobiotic organisms may tolerate the physiological stress of being desiccated without serious effects on survival.
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THE GENERAL CONTEXT OF LIFE HISTORY EVOLUTION |
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Current life history theory builds on two main components: impact of external environmental factors (biotic and abiotic), and constraints and trade-offs at the population and individual organism level (Roff, 1992
; Stearns, 1992). Environmental factors, both abiotic (such as temperature) and biotic (such as competition), determine the demographic environment (Williams, 1966) within which specific life histories are fine-tuned in the face of genetic and physiological trade-offs and constraint. Thus in order to understand how life histories evolve in anhydrobiotic organisms both the general environmental conditions and the genetic and physiological trade-offs must be considered. It is also important to distinguish between the question "what life histories do we expect in anhydrobiotic organisms" and the question "how does anhydrobiosis as a phenotypic trait affect the evolution of life histories." While an answer to the former question must take into account both general biotic/abiotic environmental effects on life histories and effects of anhydrobiotic trade-offs, the latter question deals mainly with the genetic and physiological trade-offs connected with anhydrobiosis. Below I will discuss these two questions on the basis of general life-history theory and the current knowledge of anhydrobiotic organisms. |
ENVIRONMENTAL EFFECTS IN SELECTION FOR LIFE HISTORIES IN HOLO-ANHYDROBIOTIC ANIMALS |
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Adversity selection
The abiotic environment should be a central factor in the analysis and prediction of life histories in anhydrobiotic organisms because abiotic factors such as temperature, wind and relative humidity largely determine the amplitude, frequency, and length of desiccation periods. In the classical dichotomy of r- and K-selection (MacArthur and Wilson, 1967
; MacArthur, 1972), effects of population density are the primary focus, emphasizing biotic factors (competition, resource availability) in selection for life histories. Later developments of these models attempted to incorporate also environmental stress imposed by abiotic factors, and life histories were connected to the general favourableness and predictability of the habitat (Whittaker, 1975; Southwood, 1977, 1988; Greenslade, 1983; Grime, 1977). Among these conceptual extensions, the characteristics of adversity selection (A-selection, Whittaker, 1975; Greenslade, 1983) may be the one that comes closest to the habitats of anhydrobiotic organisms. Adversity selection has also been suggested as the category that best describe the conditions and life histories of invertebrates in polar environments (Convey, 1997, 2000). Habitats promoting adversity selection were described by Greenslade (1983) as unfavourable and predictable (Fig. 1). The degree of unfavourableness referred to "physicochemical factors and the availability of resources," while predictability referred to "the length of time for which it (the habitat) remains suitable for breeding in relation to an organism's generation time" (Greenslade, 1983, p. 356). This view of habitat predictability is consistent with that of Southwood (1977), who described unpredictable habitats as having a large "variance in length of unfavourable periods," and large "variance in the level of favourableness at different times."
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There are several problems with connecting Greenslade's (1983)
view on adversity selection to life history evolution in anhydrobiotic invertebrates. First, although predictions of life history parameters were included in the classification, they were not derived explicitly from formal theory but derived a posteriori from empirical observations. Second, as indicated above, the view of high predictability connected with A-selection seems to imply a coarse-grained environment, which contrasts with the fine-grained environments of the anhydrobiotic populations considered here. The question of whether we consider a habitat as predictable or not naturally depends on how we define predictability, and how we relate this concepts to another concept, habitat variability. Many microhabitats of anhydrobiotic invertebrates are probably highly variable in time with respect to effects on growth and reproduction. Whether the same habitats should be classified as predictable or not is less clear. The dependence of stochastic weather conditions for induction of dry periods seems to imply a high degree of unpredictability. On the other hand, in a fine-grained environment each individual will experience both dry and wet periods with high degree of certainty, which in this respect imply predictable conditions. Thus, Levins (1968) considered fine-grained environments as "certain" and coarse-grained environments as "uncertain." Greenslade's (1983) view of unpredictable conditions and Levins (1968) view of an uncertain environment therefore seems to diverge. Although holo-anhydrobiotic organisms often live in unfavourable, adverse, environments they do not fit very well into the picture of a predictable coarse-grained habitat with long periods suitable for growth and reproduction. Rather, they seem to fit into the lower left corner of unfavourable and unpredictable habitats in Figure 1.
A life history theoretical approach to environmental stress
As Sibly and Calow (1985) point out, early attempts to incorporate environmental stress in the extensions of the r- and K-selection theory (e.g., Grime, 1977; Greenslade, 1983; Southwood, 1977) were not based on rigorous theory but were rather vaguely defined. It was therefore based mainly on a posteriori reasoning rather than a priori predictions from formal theory (Sibly and Calow, 1986). In particular, fitness effects of age-specific survival and reproduction were not explicitly considered. Sibly and Calow (1985, 1989) therefore provided a theoretical framework based on the standard life history model (Euler-Lotka equation) for predicting life history patterns in response to stress. Their analysis included trade-offs between fecundity and adult survival, and between fecundity and initial offspring size. They proposed two key parameters, S and G, representing the ratio of juvenile to adult age-specific survival (S = Sj/Sa) and juvenile growth rate, respectively. These parameters were used to predict variation in optimal reproductive effort (total investment into reproduction at a particular breeding attempt), fecundity and offspring size (Fig. 2). In what corner of Figure 2 should we expect to find holo-anhydrobiotic organisms? Since juvenile growth rate is strongly affected by periods of anhydrobiosis, the parameter G will probably be low in many anhydrobiotic populations. Also, if increased environmental stress affects younger age-classes more than old ones, as may be expected due to a higher general sensitivity to stress of developing tissues (e.g., von Sonntag, 1987), stressful conditions should modify S towards lower values. This would imply that holo-anhydrobiotic organisms should be found in the upper left corner of Figure 2 (low G, low S), i.e., they would be selected for low fecundity, low reproductive investment, and large initial offspring size. A low juvenile to adult average survival is also in line with the prediction of a higher degree of iteroparity (Charnov and Schaffer, 1973), which in the face of a cost of reproduction also predicts low reproductive investment. If survival prospects of juveniles are assumed to be higher while growth conditions are kept low, fecundity and total reproductive investment should increase while initial offspring size should remain high (upper right corner of Fig. 2).
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Effects of environmental variability
The importance of environmental variation on optimal life histories has long been recognised (e.g., Murphy, 1968
; Schaffer, 1974; Giesel, 1976). The effects depend on how environmental variation translates into variation in the vital rates of the organism, what age-class is affected by the environmental variation, and the level of variability (Tuljapurkar, 1989). Schaffer (1974) showed that when environmental variability affects adult survival a semelparous life history with increased reproductive effort is favoured. Conversely, environmental variability affecting juvenile survival or fecundity selects for iteroparity with reduced reproductive effort (Schaffer, 1974; Charlesworth, 1994).
In holo-anhydrobiotic organisms, increased environmental variability will probably always lead to higher variability in growth and fecundity than in survival over time, since the former components of fitness go to zero during anhydrobiosis, while survival must remain above zero if the population (phenotype) is to persist. The fact that holo-anhydrobiotic organisms shut down all metabolic activities in dry periods creates a very high variability in vital rates over a life-time. Stochastic population models have shown that high levels of random variability in vital rates selects for iteroparous life histories (Tuljapurkar, 1989), with reduced reproduction and long life span as a consequence. It seems likely that holo-anhydrobiotic organisms fit well into the category of high random demographic variability, and thus would be expected to exhibit life history patterns towards strong iteroparity.
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THE COSTS OF ANHYDROBIOSIS AND TRADE-OFFS WITH OTHER LIFE HISTORY TRAITS |
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In order to survive severe desiccation, anhydrobiotic organisms have to invest in defence mechanisms. These may generally be classified into protection mechanisms and repair mechanisms, both of which require energetic investments. Former studies on anhydrobiotic organisms have mainly focused on biochemical protection mechanisms (e.g., Crowe, 2002
; Tunnacliffe and Lapinski, 2003), while the role of repair mechanisms has received little attention. In holo-anhydrobiotic organisms, the action of these two mechanisms are distinctively separated in time, because repair mechanisms cannot be applied during the dry period, but only afterwards. Activities connected with biochemical protection occur both at the beginning of the anhydrobiotic period (synthesis of protectants) and at the end (catabolism of protectants). Because no metabolism takes place during the anhydrobiotic state, there is no immediate energetic cost at that phase, but at least part of the post-anhydrobiotic repair cost represents a delayed accounting of costs incurred in the anhydrobiotic state. Jönsson and Rebecchi (2002) quantified the energetic cost of a single anhydrobiotic period in the eutardigrade Richtersius coronifer by measuring the size of storage cells before and after a period of anhydrobiosis. Storage cell area decreased by 14%, corresponding to a decrease in volume by 22%, which suggests a substantial energetic cost of anhydrobiosis. Energy consumption in connection with desiccation has also been shown in studies on nematodes (Madin and Crowe, 1975; Demeure et al., 1978; see also Womersley, 1981), but overall we currently have very little information on how costly anhydrobiotic periods are in terms of energy. In addition to the immediate costs connected with the entrance to and exit of the anhydrobiotic state, maintenance of an elevated level of protectant molecules or enzymes for synthesizing such molecules will also give rise to energetic costs. The need for such elevated levels of biochemical components will depend on the rate at which these components may be synthesised, and the time available for such biochemical preparation, when the environment starts to deteriorate.
The frequency at which an organism desiccates will influence the costs of anhydrobiosis since energy is required to enter and exit each period of anhydrobiosis. Short but frequent anhydrobiotic periods are therefore more energy demanding than long infrequent periods. Thus, populations exposed to frequent desiccation must invest more energy in anhydrobiotic survival mechanisms, and would therefore be expected to invest less in other life history traits, compared to populations exposed to more infrequent desiccation (Jönsson and Järemo, 2003). On the other hand, long anhydrobiotic periods may lead to a higher accumulation of tissue damage (Heckly, 1978) that will be more difficult to handle by the repair system and require more energy. Therefore, when comparing short frequent periods of anhydrobiosis with long infrequent periods, the net effect on residual fitness is not trivial to predict. Many anhydrobiotic populations also experience both short frequent periods of desiccation and longer permanent anhydrobiotic or cryobiotic times, e.g., in polar areas.
If anhydrobiosis is connected with energetic or other kinds of costs, there should be trade-offs with other life history traits. The extent to which periods of anhydrobiosis affects the expression of subsequent life history traits should therefore be an important component in analysing the life history consequences of anhydrobiosis. Unfortunately, there is very little information about the nature of such trade-offs. However, C. Ricci and coworkers have investigated the extent to which periods of anhydrobiosis affect subsequent survival and reproduction of anhydrobiotic rotifers and nematodes. Post-anhydrobiotic life history traits in the rotifer Macrotrachela quadricornifera did not seem to be affected by a period of anhydrobiosis (Ricci and Caprioli, 1998). Age-specific fecundity and survival following a period of anhydrobiosis was similar to that of permanently hydrated rotifers of an equivalent metabolic age (i.e., time spent in activity). In contrast, the same life history traits in the nematode Panagrolaimus rigidus seemed to be influenced by the anhydrobiotic period, as if the animal had been active. Post-anhydrobiotic life history traits were therefore reduced compared to permanently active controls (Ricci and Pagani, 1997). Ricci and Pagani (1997) discussed these results within the context of a "biological clock," and the extent to which anhydrobiotic periods are disregarded in the subsequent part of the life cycle. From this conceptual perspective, the rotifer studied did not seem to count the time spent in anhydrobiosis while the nematode acted as if some of its potential life was consumed during the anhydrobiotic state. These observations are of great interest and should be followed up by additional studies in other populations and taxa. The main focus should be put on the actual mechanisms that underlie a modified life history schedule following anhydrobiotic periods. In particular, we should ask what changes in the state of the organism may take place during anhydrobiosis. Two possible factors are energy status and general physiological condition. Although energy is not consumed during anhydrobiosis, longer anhydrobiotic periods may lead to higher energy requirements for repair functions. Failure to repair damaged tissues should also reduce the general capability of the organism. These effects may well affect the expression of life history components after the anhydrobiotic period. Interpreted in these terms, the results of Ricci and Pagani (1997) and Ricci and Caprioli (1998) would indicate that the rotifer species has a better capability to cope with anhydrobiotic periods than the nematode species examined.
Differences among age-classes in the ability to survive periods of desiccation would create selection for different life history tactics. This would probably be a particularly important evolutionary force when periods of desiccation are relatively predictable in time and of long duration, such as summer or winter periods with more or less continuous dry or cold conditions. For instance, if anhydrobiotic survival of eggs were considerably lower than that of juveniles and adults, there would be a selection pressure to time reproduction so that eggs would hatch before the arrival of a long dry period.
Effects of desiccation on age-specific survival have been investigated in rotifers and tardigrades. In rotifers, a tendency towards higher survival in old age classes compared to juveniles and eggs has been reported (Ricci et al., 1987; Ricci, 2001). In tardigrades, both positive and negative relationships between body size and anhydrobiotic survival have been obtained for different species and in different studies of the same population. In the eutardigrade Richtersius coronifer, anhydrobiotic survival generally tends to increase with body size (Jönsson et al., 2001), although survival declined dramatically in very large tardigrades, perhaps due to senescence (Jönsson and Rebecchi, 2002). In another eutardigrade species, Ramazzottius oberhaeuseri, survival tended to decline with body size (Jönsson et al., 2001). Comparative studies on anhydrobiotic survival of eggs and juveniles has so far not been investigated in tardigrades, but eggs of the tardigrade R. oberhaeuseri hold the record of long-term survival among all age categories and were found to hatch after 9 years in anhydrobiosis (Guidetti and Jönsson, 2002). This indicates that tardigrade eggs may have a very high ability to survive anhydrobiotic periods, but more systematic studies on this are obviously needed.
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EMPIRICAL EVIDENCE OF LIFE HISTORY STRATEGIES IN HOLO-ANHYDROBIOTIC ANIMALS |
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There have been very few attempts to evaluate the patterns of life history traits in anhydrobiotic organisms. Convey (1997
, 2000) reviewed the life histories of terrestrial invertebrates (mainly arthropods) living in polar areas and noted the consistency of observed patterns with predictions of adversity selection, i.e., low growth rate, low fecundity, and high survival. Iteroparous life cycles extending over several years are common in invertebrates inhabiting polar areas (Sømme, 1995; Convey, 2000). Comparative data on life history features in aquatic holo-anhydrobiotic invertebrates (nematodes, rotifers, tardigrades) are very scarce, but seem to support the prediction of low reproductive rates in species exposed to desiccation. Thus, Ricci (1983) reported low reproductive investment (R0/Reproductive days) in rotifer species from terrestrial environments compared to species from aquatic environments. No systematic investigation of life history patterns or anhydrobiotic capacity in tardigrades exists, precluding broad-scale comparisons of life history features in anhydrobiotic and non-anhydrobiotic populations. My own observations on tardigrades from continental Antarctica (Hypsibius antarcticus, Macrobiotus krynauwi, Hebesuncus ryani) and from several dry exposed microhabitats in southern Scandinavia (Richtersius coronifer, Macrobiotus cf. hufelandi, Ramazzottius oberhaeuseri, Echiniscus testudo) suggest that fecundities are indeed very low (1– 5 eggs, Jönsson, unpublished). These observations are consistent with the predictions of optimal life history patterns from the theory by Sibly and Calow (1985, 1986; assuming low G and high S), but obviously comparative data for non-anhydrobiotic populations are needed. Also data to evaluate the prediction of low total reproductive investment and large egg size are currently lacking. Faunistic and taxonomic literature on tardigrades (e.g., Bertolani, 1982; Ramazzotti and Maucci, 1983; Dastych, 1988) may provide some information on egg size and fecundity, but usually without basic statistics (e.g., mean, standard deviation, sample size) and specific information on habitat conditions. Although it may be tempting to use such information for evaluating life history predictions, more precise data are highly preferable and could relatively easily be collected from natural populations. |
CONCLUSIONS |
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What life histories do we expect in holo-anhydrobiotic organisms? Only a tentative answer can be provided at this point. Although there are no theoretical studies that specifically address the question of how life histories in anhydrobiotic animals should evolve, predictions from some general life history models suggest that we should find this group in the iteroparity part of the life history spectrum, expressing high survival and low reproductive rates. This prediction relies on the assumptions of low growth rate, low juvenile to adult survival, and a high variability in vital rates, particularly reproduction. The limited available evidence seems to support this prediction.
How does anhydrobiosis as a phenotypic trait affect the evolution of life histories? No clear answer can yet be given. Estimates on energy costs of anhydrobiosis in tardigrades suggest that these costs may be high, but the nature of potential anhydrobiotic trade-offs is unknown. The studies by Ricci and co-workers (Ricci and Pagani, 1997; Ricci and Caprioli, 1998) on post-anhydrobiotic effects on life histories are promising and should be followed by similar investigations. The current analysis should be considered a starting point and much more work are needed before we will begin to understand life histories in anhydrobiotic animals. First, more conceptual work is needed in order to clarify the nature of holo-anhydrobiotic life cycles and how they relate to general evolutionary processes. Second, we need theoretical analyses, including stochastic models, on holo-anhydrobiotic model system where different assumptions of trade-offs and environmental variability are evaluated. And third, we badly need more comparative empirical data on life history parameters in anhydrobiotic and non-anhydrobiotic populations.
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ACKNOWLEDGMENTS |
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I am grateful to J. Järemo and an anonymous referee for valuable comments on the manuscript. This study was supported by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning.
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FOOTNOTES |
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1 From the symposium Drying Without Dying: The Comparative Mechanisms and Evolution of Desiccation Tolerance in Animals, Microbes and Plants presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2005, at San Diego, California.
2 E-mail: ingemar.jonsson{at}teorekol.lu.se
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