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A theoretical integration of Cambrian explosion and post-Permian quiescence
BioSystems 43 (1997) 63 – 68
A theoretical integration of Cambrian explosion and post-Permian quiescence Yoshinori Takahara a,*, Nobuaki Ono b a
Department of BioEngineering, Nagaoka Uni6ersity of Technology, Nagaoka 940 -21, Japan b Ichinoseki National Technical College, Ichinoseki 021, Japan
Received 28 September 1996; received in revised form 10 January 1997; accepted 4 March 1997
Abstract Trophic dynamics is internally causative. Each trophic level is causative in initiating changes in trophic flow either as a supplier towards the upper level or as a consumer towards the lower. Resource presentation followed by its subsequent exploitation makes suppliers causative, while resource exploitation followed by its subsequent presentation makes consumers causative. Trophic dynamics of supplier domination gradually alternates with that of consumer domination while being punctuated by occasional mass extinctions due to depletion of the resources towards the lowest trophic level. The Cambrian explosion could be associated with trophic dynamics of supplier domination, whereas the post-Permian quiescence with that of consumer influencing supplier domination © 1997 Elsevier Science Ireland Ltd. Keywords: Cambrian; Consumer; Permian; Supplier; Trophic dynamics
1. Introduction Despite its acclaimed usefulness in evolutionary processes, the idea of a fitness landscape first proposed by Wright (1932) faces two serious problems. One is the separation between forming the fitness landscape and experiencing it as such (Jongeling, 1996). Take, for instance, any individ-
* Corresponding author.
ual evolutionary participant such as a population or a species. We are, however, not sure whether it is involved in forming the fitness landscape to others or simply experiencing the one already made by others. The fitness increase may have been merely passive, instead of being causative (Vermeij, 1987). One more problem is how the fitness landscape would evolve over a long period of time from, say, a rugged uncorrelated landscape to a smooth correlated one as modeled for the transition from the Cambrian explosion about 540 million years ago (Ma) to the post-Permian
0303-2647/97/$17.00 © 1997 Elsevier Science Ireland Ltd. All rights reserved. PII S 0 3 0 3 - 2 6 4 7 ( 9 7 ) 0 0 0 2 9 - 4
64
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
quiescence 250 Ma (Wimsatt, 1986; Kauffman, 1989). In particular, recent geological studies reveal that the sedimentary record of the past 500 million years (My) including the late Permian events are unusual compared to the preceding one at an earlier time comprising the late Neoproterozoic era ( 800–543 Ma) (Knoll et al., 1996). These findings invite us to shed new light on a likely theoretical scenario on how the post-Permian quiescence could be compared to the Cambrian explosion while either huge cleared or opened up ecospace was available in both cases (Sepkowski, 1985; Ghiselin, 1995). We, in this paper, try to explore a theoretical possibility to argue for how the Cambrian explosion and the post-Permian quiescence could differ between each other dynamically without direct recourse to the notion of fitness and its landscape.
2. Trophic dynamics The Permian– Triassic boundary is peculiar in that no new phyla or classes arose after the mass extinction at the end of the Permian in spite of the presence of huge cleared ecospace while the beginning of the Cambrian explosion, which brought birth to new phyla and classes, is marked by the filling of the then available empty niches (Valentine, 1994). Direct reference to ecospace or niche space in both cases suggests a theoretical likelihood of applying the notion of trophic dynamics to evolutionary processes in terms of phyla and classes in addition to lower level taxa including species up to families (Shear, 1991). Basic to any trophic dynamics is the presence of metabolic trophic levels. In addition, each trophic level is characterized by two more basic capacities. One is resource exploitation from the lower level, and the other is resource presentation to the upper level if any. What is significant to the trophic dynamics is the absence of synchronization among different trophic levels in coordinating their resource exploitation and presentation (Matsuno, 1989). For instance, an increase of the biomass of phytoplankton due to a slight increase of carbon dioxide in freshwater pelagic ecosys-
tems can be detected by predatory zooplankton only through the subsequent increase of grazing zooplankton. Occurrence of variations in resource presentation to grazing zooplankton at the upper level is not synchronized with the subsequent variations in resource exploitation at the level of predatory zooplankton. The absence of synchronization among different trophic levels in their manner of resource presentation and exploitation makes each trophic level a causative agent carrying two independent capacities; behaving as a supplier that presents resources to the upper level and as a consumer that exploits resources from the lower. Herbivores are consumers of trophic energy stored in plants, whereas they are also suppliers of trophic energy to carnivores. Intervening trophic flow between two adjacent trophic levels is regulated by two factors. The lower level supplies the upper with trophic energy through resource presentation whereas the upper level consumes trophic energy usurped from the lower through resource exploitation. Since there is no pre-established synchronization between the resource presentation and exploitation, the actual completed transaction of trophic energy between the two levels could be a resultant of both the resource presentation on the lower level followed by its subsequent exploitation by the upper and its reversal, namely, the resource exploitation followed by its subsequent presentation. As far as the completed transaction is concerned, the amount of resources exploited has to be equal to those presented. Nonetheless, if one is concerned with the causal chain under the premise that there is no pre-established synchronization between resource presentation and exploitation, either one can be causative towards the other. A record of the completed transactions could be guaranteed only at the expense of dispensing with the causal relationship that was responsible for actualizing the very transactions in the first place. Consider, for instance, an auction of antiques. There are both the price-givers and the price-takers in the market. After the auction has been settled, the completed transaction does not tell the causal chain of how the auctioneer and the buyers behaved in each step of bidding in the scene while a causal sequence did definitely operate internally.
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
Trophic dynamics can thus be parameterized in terms of the relative ratio of supplier regulation or causation that measures the amount of variations in the trophic flow in the form of resource presentation followed by its subsequent exploitation, that is supplier causative, relative to the resultant variations in the intervening trophic flow actualized in and retrieved from the completed transactions (Matsuno, 1995; Matsuno and Ono, 1996). In the completed transactions, the resultant resource presentation of course equals the resultant resource exploitation. If the relative ratio of supplier causation approaches unity, variations in the trophic flow would come to be initiated mostly by changes in the strategy of resource presentation at the lower level. In contrast, if the ratio almost vanishes, variations in the trophic flow would be initiated mostly by changes in the strategy of resource exploitation exerted from the upper level. A use for the relative ratio of supplier causation is found in that it directly addresses a causative factor inducing changes in the structure of trophic dynamics. As a matter of fact, trophic dynamics could have been dominated by suppliers at the onset of life on the primitive Earth whatever it may have looked like, because resource presentation of any use could have been of primary significance there. Similarly, the Cambrian explosion was the first radiation of metazoans to empty niches where resources were plentiful. At issue is to what extent trophic dynamics could be supplier or consumer dominated and how it would develop in time.
3. Supplier domination In view of the fact that resource presentation happens prior to an emergence of the agents to feed upon them, trophic dynamics would have to be supplier dominated initially in evolutionary processes as suggested in a possible origination of chemolithoautotrophs in a heated Arcean ocean (Kandler, 1993). Once resources preparing empty niches are available, emergence of consumers to feed upon them would follow. Supplier dominated trophic dynamics would then let the resultant of both resource exploitation followed by its presen-
65
tation by suppliers and resource presentation followed by its exploitation by consumers meet the total resource consumption by consumers in the long run. All of the available niches can be occupied in the end. Initial domination of suppliers is reflected by the fact that the relative ratio of supplier causation is greater than zero implying that the net trophic flow from suppliers to consumers is the resultant of both resource exploitation followed by its presentation by suppliers and resource presentation followed by its exploitation by consumers. The Cambrian explosion may happen to be another significant instance of supplier domination in the form of large excess quantities of carbon dioxide and other nutrients including phosphorite due to massive submarine volcanism (Braiser, 1992; Cook, 1992; Hallam, 1992). Nonetheless, supplier dominated trophic dynamics is intrinsically unstable against exogenous disturbances. If the amount of resource presentation caused by suppliers happens to decrease due to some geological or geochemical changes at a well developed stage of supplier dominated dynamics the consumers would have to increase the extent of resource exploitation to meet the consumption. Increase in the resource exploitation would further decrease the amount of resource presentation by the suppliers that would already have been exploited and further increase the extent of subsequent resource exploitation. This type of positive feedback of resource exploitation would soon deplete the trophic level of suppliers (White, 1978; Birkeland, 1982; DeAngelis, 1992). Supplier dominated trophic dynamics is internally driven toward decreasing the relative ratio of supplier causation (McShea, 1994). Supplier dominated trophic dynamics would have to alternate with others or there could be no sustainable trophic dynamics. One possibility for such alternation is consumer domination.
4. Consumer domination When the relative ratio of supplier causation is maintained above zero, trophic dynamics is vulnerable to a positive feedback of resource ex-
66
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
ploitation. A candidate for circumventing the vulnerability intrinsic to supplier dominated trophic dynamics is a consumer dominated one in the sense that the relative ratio of supplier causation at each level is maintained in the region of zero. The resulting consumer domination would let resource consumption at the trophic level of consumers be met mostly by resource exploitation towards suppliers at the lower level (Strong, 1992). Consumer dominated trophic dynamics could be much more durable compared to it’s supplier dominated counterpart because of the absence of room for resource presentation which may induce an unstable growth of resource exploitation resulting in the depletion of suppliers. Nonetheless, consumer dominated trophic dynamics is not free from its built-in instability. Consumer dominated trophic dynamics lets a higher trophic level exploit the lower level to meet resource consumption there, and lets the lower level exploit the further lower level and so on. Resources towards the lowest trophic level are sun light, detritus, carbon dioxide, water and other inorganic materials. These resources indispensable to the lowest trophic level are certainly regulated and controlled by the relevant non-biological suppliers such as volcanism (Vermeij, 1995). This would imply that even consumer dominated trophic dynamics is, though to a limited extent, supplier regulated at the lowest level. Supplier regulation at the lowest trophic level, like supplier domination in general, would yield a positive feedback of resource exploitation at the lowest level once the amount of resources available to the lowest level happens to decrease and cannot meet their consumption by chance due to, say, changes in geological conditions. Consumer dominated trophic dynamics is intrinsically vulnerable to depletion of the resources available to the lowest trophic level. The extent of depletion of the resources towards the lowest level could be global on the whole Earth. However, historical records reveal that none of the major mass extinctions, including those at the boundaries of the end of the Cretaceous, Triassic, late Permian, late Devonian and Ordovician was globally exhaustive
(Raup, 1994). Even the biggest mass extinction at the Permian–Triassic boundary left a few percent of species intact. Geological heterogeneity could leave some of the tandem sequences of trophic levels in restricted regions invulnerable to a mass extinction at large. Mass extinction due to consumer dominated trophic dynamics expected on the Earth would thus let those surviving trophic levels influence how trophic dynamics would subsequently develop in ecospace cleared accordingly.
5. Consumer influencing supplier domination The occurrence of cleared or opened up ecospace due to mass extinction could again make suppliers dominate the dynamics, though under the influence of quite a limited number of the incumbent consumers and suppliers. However, the influence of the surviving consumers towards the species newly originated in the cleared ecospace can be substantial in determining the fate of those newcomers. The incumbent trophic levels set the reference, that is to say, the fitness to be experienced by the newly originated species. Since the framework determining the fitness to newly originated species in the post mass extinction era is part of the whole trophic dynamics in the pre-extinction period, resurgence of a terribly similar trophic dynamics could be highly likely in the post-extinction period (Knoll, 1989). Once trophic dynamics of consumer influencing supplier domination reaches a stationary condition keeping the relative ratio of supplier causation greater than zero, it has to eventually alternate with that of consumer domination maintaining the relative ratio in the region of zero, otherwise, evolutionary durability of trophic dynamics could not be attainable. Nonetheless, consumer dominated trophic dynamics is intrinsically vulnerable to depletion of the resources towards the lowest trophic level. Consumer domination and consumer influencing supplier domination would thus come to alternate while being demarcated by intermittent mass extinctions.
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
67
6. Discussion
Acknowledgements
The Cambrian explosion generated 100 or so new phyla with those novelties such as predators, burrowers, mineralized skeletons and new body plans while many of them become extinct with only 35 phyla extant today (Conway Morris, 1993). In contrast, the post-Permian quiescence is unique in generating no new phyla or classes while the period extending over the late Triassic to the mid-Cretaceous was full of novelties including a great diversification of predators (Vermeij, 1995). This comparison suggests an association of the Cambrian explosion with trophic dynamics of supplier domination because of the absence of the incumbents to interfere, and the post-Permian quiescence with that of consumer influencing supplier domination because of the presence of a limited number of incumbent consumers, while cleared or opened up ecospace was available in both cases. In the long run, however, consumer domination would take over until the next mass extinction comes to intervene. Trophic dynamics parameterized in terms of the relative ratio of supplier causation is internally causative in letting the ratio itself decrease towards zero endogenously. This aspect exhibits a marked contrast to climbing up peaks in the fitness landscape, in which the climbing is totally exogenous to the process of forming the landscape itself. The notion of climbing up peaks in the fitness landscape can approximately be applicable to trophic dynamics only in the realm of consumer influencing supplier domination, in which newly originated consumers come to experience the fitness landscape formed by the pre-existing incumbent consumers and suppliers. Once the period of consumer influencing supplier domination is over, on the other hand, the distinction between forming and experiencing the fitness landscape would be blurred again. Accordingly, natural selection conceived within the framework of trophic dynamics is internally unidirectional in time in decreasing the relative ratio of supplier causation while being punctuated by intermittent sudden increases in the ratio due to occasional mass extinctions.
We should like to thank Koichiro Matsuno and Geerat J. Vermeij for helpful comments on an earlier draft of this paper.
References Birkeland, C., 1982, Terrestrial runoff as a cause of outbreaks of Acanthaster planci (Echinodermata: Asteroidea). Marine Biol. 69, 175 – 185. Braiser, M.D., 1992, Paleoceanography and changes in the biological cycling of phosphorus across the Precambrian – Cambrian boundary. In: Lipps, J.H. and Signor, P.W. (ed.) Origin and Early Evolution of the Metazoa (Plenum Press, New York) pp. 483 – 523. Conway Morris, S., 1993, The fossil record and the early evolution of the Metazoa. Nature 361, 219 – 225. Cook, J.P., 1992, Phosphogenesis around the Proterozoic – Phanerozoic transition. J. Geol. Soc. London 149, 615 – 620. DeAngelis, D.L., 1992, Dynamics of Nutrient Cycling and Food Webs (Chapman and Hall, London). Ghiselin, M.T., 1995, Perspective: Darwin, progress, and economic principles. Evolution 49, 1029 – 1037. Hallam, A., 1992, Phanerozoic Sea-Level Changes (Columbia University Press, New York). Jongeling, T.B., 1996, Self-organization and competition in evolution: a conceptual problem in the use of fitness landscape. J. Theor. Biol. 178, 369 – 373. Kandler, O., 1993, The early diversification of life, in: Bergtson, S. (ed.) Early Life on Earth. Nobel Symposium 84 (Columbia University Press, New York) pp. 152 – 160. Kauffman, S.A., 1989, Cambrian explosion and Permian quiescence: implications of rugged fitness landscape. Evol. Ecol. 3, 274 – 281. Knoll, A.H., 1989, Evolution and extinction in the marine realm: some constraints imposed by phytoplankton. Phil. Trans. R. Soc. Lond. B 325, 279 – 290. Knoll, A.H., Bambach, R.K., Canfield, D.E. and Grotzinger, J.P., 1996, Comparative Earth history and late Permian mass extinction. Science 273, 452 – 457. Matsuno, K., 1989, Protobiology: Physical Basis of Biology (CRC Press, Boca Raton, FL). Matsuno, K., 1995, Consumer power as the major evolutionary force. J. Theor. Biol. 173, 137 – 145. Matsuno, K. and Ono, N., 1996, How may trophic levels are there? J. Theor. Biol. 180, 105 – 109. McShea, D.W., 1994, Mechanisms of large-scale evolutionary trends. Evolution 48, 1747 – 1763. Raup, D.M., 1994, The role of extinction in evolution. Proc. Natl. Acad. Sci. USA 91, 6758 – 6763. Shear, W.A., 1991, The early development of terrestrial ecosystems. Nature 351, 282 – 289.
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Sepkowski, J.J. Jr., 1985, Some implications of mass extinctions for the evolution of complex life. Int. Astronom. Union Symp. 112, 223–232. Strong, D.R., 1992, Are trophic cascades all wet?: differentiation and donor-control in speciose ecosystems. Ecology 73, 747 – 754. Valentine, J.W., 1994, Late Precambrian bilaterians: grades and clades. Proc. Natl. Acad. Sci. USA 91,6751–6757. Vermeij, G.J., 1987, Evolution and Escalation (Princeton University Press, Princeton, NJ). Vermeij, G.J., 1995, Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21, 125–152.
White, T.C.R., 1978, The importance of a relative shortage of food in animal ecology. Oecologia (Berlin) 33, 71 – 86. Wimsatt, W.C., 1986, Developmental constraints, generative entrenchment, and the innate-acquired distinction, in: Bechtel, W. (ed.) Science and Philosophy: Integrating Scientific Disciplines (Martinus Nijhoff, Dordrecht) pp. 185 – 208. Wright, S., 1932, The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc. 6th. Int. Congr. Genetics 1, 356 – 366. Reprinted in Wright, S., 1986, Evolution: Selected Papers (University of Chicago Press, Chicago, IL) pp. 161 – 171.
. .
A theoretical integration of Cambrian explosion and post-Permian quiescence Yoshinori Takahara a,*, Nobuaki Ono b a
Department of BioEngineering, Nagaoka Uni6ersity of Technology, Nagaoka 940 -21, Japan b Ichinoseki National Technical College, Ichinoseki 021, Japan
Received 28 September 1996; received in revised form 10 January 1997; accepted 4 March 1997
Abstract Trophic dynamics is internally causative. Each trophic level is causative in initiating changes in trophic flow either as a supplier towards the upper level or as a consumer towards the lower. Resource presentation followed by its subsequent exploitation makes suppliers causative, while resource exploitation followed by its subsequent presentation makes consumers causative. Trophic dynamics of supplier domination gradually alternates with that of consumer domination while being punctuated by occasional mass extinctions due to depletion of the resources towards the lowest trophic level. The Cambrian explosion could be associated with trophic dynamics of supplier domination, whereas the post-Permian quiescence with that of consumer influencing supplier domination © 1997 Elsevier Science Ireland Ltd. Keywords: Cambrian; Consumer; Permian; Supplier; Trophic dynamics
1. Introduction Despite its acclaimed usefulness in evolutionary processes, the idea of a fitness landscape first proposed by Wright (1932) faces two serious problems. One is the separation between forming the fitness landscape and experiencing it as such (Jongeling, 1996). Take, for instance, any individ-
* Corresponding author.
ual evolutionary participant such as a population or a species. We are, however, not sure whether it is involved in forming the fitness landscape to others or simply experiencing the one already made by others. The fitness increase may have been merely passive, instead of being causative (Vermeij, 1987). One more problem is how the fitness landscape would evolve over a long period of time from, say, a rugged uncorrelated landscape to a smooth correlated one as modeled for the transition from the Cambrian explosion about 540 million years ago (Ma) to the post-Permian
0303-2647/97/$17.00 © 1997 Elsevier Science Ireland Ltd. All rights reserved. PII S 0 3 0 3 - 2 6 4 7 ( 9 7 ) 0 0 0 2 9 - 4
64
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
quiescence 250 Ma (Wimsatt, 1986; Kauffman, 1989). In particular, recent geological studies reveal that the sedimentary record of the past 500 million years (My) including the late Permian events are unusual compared to the preceding one at an earlier time comprising the late Neoproterozoic era ( 800–543 Ma) (Knoll et al., 1996). These findings invite us to shed new light on a likely theoretical scenario on how the post-Permian quiescence could be compared to the Cambrian explosion while either huge cleared or opened up ecospace was available in both cases (Sepkowski, 1985; Ghiselin, 1995). We, in this paper, try to explore a theoretical possibility to argue for how the Cambrian explosion and the post-Permian quiescence could differ between each other dynamically without direct recourse to the notion of fitness and its landscape.
2. Trophic dynamics The Permian– Triassic boundary is peculiar in that no new phyla or classes arose after the mass extinction at the end of the Permian in spite of the presence of huge cleared ecospace while the beginning of the Cambrian explosion, which brought birth to new phyla and classes, is marked by the filling of the then available empty niches (Valentine, 1994). Direct reference to ecospace or niche space in both cases suggests a theoretical likelihood of applying the notion of trophic dynamics to evolutionary processes in terms of phyla and classes in addition to lower level taxa including species up to families (Shear, 1991). Basic to any trophic dynamics is the presence of metabolic trophic levels. In addition, each trophic level is characterized by two more basic capacities. One is resource exploitation from the lower level, and the other is resource presentation to the upper level if any. What is significant to the trophic dynamics is the absence of synchronization among different trophic levels in coordinating their resource exploitation and presentation (Matsuno, 1989). For instance, an increase of the biomass of phytoplankton due to a slight increase of carbon dioxide in freshwater pelagic ecosys-
tems can be detected by predatory zooplankton only through the subsequent increase of grazing zooplankton. Occurrence of variations in resource presentation to grazing zooplankton at the upper level is not synchronized with the subsequent variations in resource exploitation at the level of predatory zooplankton. The absence of synchronization among different trophic levels in their manner of resource presentation and exploitation makes each trophic level a causative agent carrying two independent capacities; behaving as a supplier that presents resources to the upper level and as a consumer that exploits resources from the lower. Herbivores are consumers of trophic energy stored in plants, whereas they are also suppliers of trophic energy to carnivores. Intervening trophic flow between two adjacent trophic levels is regulated by two factors. The lower level supplies the upper with trophic energy through resource presentation whereas the upper level consumes trophic energy usurped from the lower through resource exploitation. Since there is no pre-established synchronization between the resource presentation and exploitation, the actual completed transaction of trophic energy between the two levels could be a resultant of both the resource presentation on the lower level followed by its subsequent exploitation by the upper and its reversal, namely, the resource exploitation followed by its subsequent presentation. As far as the completed transaction is concerned, the amount of resources exploited has to be equal to those presented. Nonetheless, if one is concerned with the causal chain under the premise that there is no pre-established synchronization between resource presentation and exploitation, either one can be causative towards the other. A record of the completed transactions could be guaranteed only at the expense of dispensing with the causal relationship that was responsible for actualizing the very transactions in the first place. Consider, for instance, an auction of antiques. There are both the price-givers and the price-takers in the market. After the auction has been settled, the completed transaction does not tell the causal chain of how the auctioneer and the buyers behaved in each step of bidding in the scene while a causal sequence did definitely operate internally.
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
Trophic dynamics can thus be parameterized in terms of the relative ratio of supplier regulation or causation that measures the amount of variations in the trophic flow in the form of resource presentation followed by its subsequent exploitation, that is supplier causative, relative to the resultant variations in the intervening trophic flow actualized in and retrieved from the completed transactions (Matsuno, 1995; Matsuno and Ono, 1996). In the completed transactions, the resultant resource presentation of course equals the resultant resource exploitation. If the relative ratio of supplier causation approaches unity, variations in the trophic flow would come to be initiated mostly by changes in the strategy of resource presentation at the lower level. In contrast, if the ratio almost vanishes, variations in the trophic flow would be initiated mostly by changes in the strategy of resource exploitation exerted from the upper level. A use for the relative ratio of supplier causation is found in that it directly addresses a causative factor inducing changes in the structure of trophic dynamics. As a matter of fact, trophic dynamics could have been dominated by suppliers at the onset of life on the primitive Earth whatever it may have looked like, because resource presentation of any use could have been of primary significance there. Similarly, the Cambrian explosion was the first radiation of metazoans to empty niches where resources were plentiful. At issue is to what extent trophic dynamics could be supplier or consumer dominated and how it would develop in time.
3. Supplier domination In view of the fact that resource presentation happens prior to an emergence of the agents to feed upon them, trophic dynamics would have to be supplier dominated initially in evolutionary processes as suggested in a possible origination of chemolithoautotrophs in a heated Arcean ocean (Kandler, 1993). Once resources preparing empty niches are available, emergence of consumers to feed upon them would follow. Supplier dominated trophic dynamics would then let the resultant of both resource exploitation followed by its presen-
65
tation by suppliers and resource presentation followed by its exploitation by consumers meet the total resource consumption by consumers in the long run. All of the available niches can be occupied in the end. Initial domination of suppliers is reflected by the fact that the relative ratio of supplier causation is greater than zero implying that the net trophic flow from suppliers to consumers is the resultant of both resource exploitation followed by its presentation by suppliers and resource presentation followed by its exploitation by consumers. The Cambrian explosion may happen to be another significant instance of supplier domination in the form of large excess quantities of carbon dioxide and other nutrients including phosphorite due to massive submarine volcanism (Braiser, 1992; Cook, 1992; Hallam, 1992). Nonetheless, supplier dominated trophic dynamics is intrinsically unstable against exogenous disturbances. If the amount of resource presentation caused by suppliers happens to decrease due to some geological or geochemical changes at a well developed stage of supplier dominated dynamics the consumers would have to increase the extent of resource exploitation to meet the consumption. Increase in the resource exploitation would further decrease the amount of resource presentation by the suppliers that would already have been exploited and further increase the extent of subsequent resource exploitation. This type of positive feedback of resource exploitation would soon deplete the trophic level of suppliers (White, 1978; Birkeland, 1982; DeAngelis, 1992). Supplier dominated trophic dynamics is internally driven toward decreasing the relative ratio of supplier causation (McShea, 1994). Supplier dominated trophic dynamics would have to alternate with others or there could be no sustainable trophic dynamics. One possibility for such alternation is consumer domination.
4. Consumer domination When the relative ratio of supplier causation is maintained above zero, trophic dynamics is vulnerable to a positive feedback of resource ex-
66
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
ploitation. A candidate for circumventing the vulnerability intrinsic to supplier dominated trophic dynamics is a consumer dominated one in the sense that the relative ratio of supplier causation at each level is maintained in the region of zero. The resulting consumer domination would let resource consumption at the trophic level of consumers be met mostly by resource exploitation towards suppliers at the lower level (Strong, 1992). Consumer dominated trophic dynamics could be much more durable compared to it’s supplier dominated counterpart because of the absence of room for resource presentation which may induce an unstable growth of resource exploitation resulting in the depletion of suppliers. Nonetheless, consumer dominated trophic dynamics is not free from its built-in instability. Consumer dominated trophic dynamics lets a higher trophic level exploit the lower level to meet resource consumption there, and lets the lower level exploit the further lower level and so on. Resources towards the lowest trophic level are sun light, detritus, carbon dioxide, water and other inorganic materials. These resources indispensable to the lowest trophic level are certainly regulated and controlled by the relevant non-biological suppliers such as volcanism (Vermeij, 1995). This would imply that even consumer dominated trophic dynamics is, though to a limited extent, supplier regulated at the lowest level. Supplier regulation at the lowest trophic level, like supplier domination in general, would yield a positive feedback of resource exploitation at the lowest level once the amount of resources available to the lowest level happens to decrease and cannot meet their consumption by chance due to, say, changes in geological conditions. Consumer dominated trophic dynamics is intrinsically vulnerable to depletion of the resources available to the lowest trophic level. The extent of depletion of the resources towards the lowest level could be global on the whole Earth. However, historical records reveal that none of the major mass extinctions, including those at the boundaries of the end of the Cretaceous, Triassic, late Permian, late Devonian and Ordovician was globally exhaustive
(Raup, 1994). Even the biggest mass extinction at the Permian–Triassic boundary left a few percent of species intact. Geological heterogeneity could leave some of the tandem sequences of trophic levels in restricted regions invulnerable to a mass extinction at large. Mass extinction due to consumer dominated trophic dynamics expected on the Earth would thus let those surviving trophic levels influence how trophic dynamics would subsequently develop in ecospace cleared accordingly.
5. Consumer influencing supplier domination The occurrence of cleared or opened up ecospace due to mass extinction could again make suppliers dominate the dynamics, though under the influence of quite a limited number of the incumbent consumers and suppliers. However, the influence of the surviving consumers towards the species newly originated in the cleared ecospace can be substantial in determining the fate of those newcomers. The incumbent trophic levels set the reference, that is to say, the fitness to be experienced by the newly originated species. Since the framework determining the fitness to newly originated species in the post mass extinction era is part of the whole trophic dynamics in the pre-extinction period, resurgence of a terribly similar trophic dynamics could be highly likely in the post-extinction period (Knoll, 1989). Once trophic dynamics of consumer influencing supplier domination reaches a stationary condition keeping the relative ratio of supplier causation greater than zero, it has to eventually alternate with that of consumer domination maintaining the relative ratio in the region of zero, otherwise, evolutionary durability of trophic dynamics could not be attainable. Nonetheless, consumer dominated trophic dynamics is intrinsically vulnerable to depletion of the resources towards the lowest trophic level. Consumer domination and consumer influencing supplier domination would thus come to alternate while being demarcated by intermittent mass extinctions.
Y. Takahara, N. Ono / BioSystems 43 (1997) 63–68
67
6. Discussion
Acknowledgements
The Cambrian explosion generated 100 or so new phyla with those novelties such as predators, burrowers, mineralized skeletons and new body plans while many of them become extinct with only 35 phyla extant today (Conway Morris, 1993). In contrast, the post-Permian quiescence is unique in generating no new phyla or classes while the period extending over the late Triassic to the mid-Cretaceous was full of novelties including a great diversification of predators (Vermeij, 1995). This comparison suggests an association of the Cambrian explosion with trophic dynamics of supplier domination because of the absence of the incumbents to interfere, and the post-Permian quiescence with that of consumer influencing supplier domination because of the presence of a limited number of incumbent consumers, while cleared or opened up ecospace was available in both cases. In the long run, however, consumer domination would take over until the next mass extinction comes to intervene. Trophic dynamics parameterized in terms of the relative ratio of supplier causation is internally causative in letting the ratio itself decrease towards zero endogenously. This aspect exhibits a marked contrast to climbing up peaks in the fitness landscape, in which the climbing is totally exogenous to the process of forming the landscape itself. The notion of climbing up peaks in the fitness landscape can approximately be applicable to trophic dynamics only in the realm of consumer influencing supplier domination, in which newly originated consumers come to experience the fitness landscape formed by the pre-existing incumbent consumers and suppliers. Once the period of consumer influencing supplier domination is over, on the other hand, the distinction between forming and experiencing the fitness landscape would be blurred again. Accordingly, natural selection conceived within the framework of trophic dynamics is internally unidirectional in time in decreasing the relative ratio of supplier causation while being punctuated by intermittent sudden increases in the ratio due to occasional mass extinctions.
We should like to thank Koichiro Matsuno and Geerat J. Vermeij for helpful comments on an earlier draft of this paper.
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