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Biomass and body size of oceanic plankton
TREE vol. 1, no. 3, September
news
1986
Body size affects some important physiological and ecological parameters of marine organisms, such as their metabolic and potential growth ratesle3 and the size range of organisms that they can feed on or be eaten by. The distribution of body size in the ocean is a controversial topic. Some investigators”4 have proposed a flat spectrum in which different size groups have approximately the same total biomass, whereas others5f6 have proposed a spectrum of decreasing biomass with increasing body size. In a recent publication, Rodriguez and Mullin present an empirical size spectrum of living oceanic plankton from the Central North Pacific, revealing a regular and precise decrease of the total biomass with increasing body size between 10 km and 8 mm. The observations and methodology presented by Rodriguez and Mullin may be a significant step in studies of community structure and trophic relationships in pelagic ecosystems. The concept of discrete trophic levels with structured food chains in the marine environment has been criticized, primarily on the basis of the difficulties in assignin a trophic level to a given species 8! lo. These difficulties may be attributed to ontogenetic and seasonal changes in feeding habits of many species, as well as to the cyclic nature of pelagic food webs; adults of many marine invertebrate and fish taxa eat different food items from their juvenile and larval stages (e.g. Ref. 11) and eggs or larvae of fish may become food for planktonic species on which the adult fish themselves feed”. Most pelagic animals, however, feed on whatever food of suitable size is accessible by their feeding mode (see Refs 9 and 12). This allometric relationship between predator and prey has led to an increasing interest in the body size of marine organisms and to the use of size as an alternative to taxonomic and trophic characteristics of plankton. The first size spectrum of oceanic particles was reported by Sheldon and coworkers’ who combined their direct observations, in the size range of l-100 pm, with data from the literature and proposed that roughly equal concentrations of material (presented as p.p.m.) occur at all particle sizes from bacteria to whales. Their measurements, which have served for many years as the single published reference for the marine environment, were made Amatzia Genin is at the Scripps Institution of Oceanography,A-008,La Jolla, CA 92093,USA. 0
1986. Elsevier Science Publishers
B VI Amsterdam
Biomass andBodySizeofOceanic Plankton AmatziaGenin with a Coulter Counter (which automatically counts and measures particles, both living and non-living) and therefore included some unknown proportion of detrital particles. A similarly flat biomass spectrum has also been proposed by Kerr“, who based his theoretical model on the existence of discrete trophic levels. A different spectrum, of decreasing biomass with increasing body size, has been proposed by Platt and Denman506; their theoretical model is independent of the concept of trophic levels and assumes a continuous flow of biomass, or energy, from the smallest to the largest organisms. In lakes, on the other hand, the biomass spectra are apparently highly variable around a mean spectrum with a bimodal shape13. Rodriguez and Mullin’s observations are in agreement with the prediction of Platt and Denman and are clearly at odds with those of Sheldon et a/. and Kerr. The spectrum presented by Rodriguez and Mullin (Fig. 1) comprises two parts, each obtained by a different technique: phytoplankton and heterotrophic organisms larger than 10 pm but smaller than 200 pm (microplankton) were measured and counted under a microscope for later conversion to carbon weight, whereas animals larger than 183 km and smaller than 8 mm (macrozooplankton) were fractionated through a filter column of different mesh sizes and then weighed. Samples were collected from the euphotic zone of the nearsteady-state ecosystem of the Central North Pacific Gyre, during six cruises between 1972 and 1974. The results (Fig. 1) show a regular decrease of biomass, roughly as the negative one-sixth power of body weight, and the slopes obtained for microplankton and macrozooplankton are remarkably similar. Superimposed on this regularity is a variability with depth (larger organisms are relatively more important at greater depths), a seasonal variability, and an increase of the proportion of larger organisms during night time, caused by their diurnal vertical migration. In a se arate report, RodP, riguez and Mullin describe an additional source of variability caused by an unusually cold year. The methodology applied by Rodriguez and Mullin will probably become a standard procedure by which
0169-5347186150
200
additional spectra can be obtained for other oceanic regions such as temperate, coastal, and upwelling zones, and for depths below the euphotic zone. There is also a need to expand the spectrum to larger animals, such as fish and marine mammals, as well as to bacteria and organisms smaller than 10 pm. Biomass spectra, when available,, will provide an important means of different comparison between regions. This will unoceanic doubtedly contribute to our understanding of processes determining community structures in pelagic ecosystems, and may also be used to improve the management of fishery resources.
(4
w s
10-Z 1
; lo-4[, , , / , b, 0 us’ 10-Z
WEIGHT (PgC
m
-
)
2
0
‘idividuz-’
IO4
)
t
I
s,o‘ L.-------! 4 10-q
10-2
WEIGHT (PgC
IO0
IO*
individual-’
104
)
Fig. 1. (a) Normalized biomass spectrum in the euphotic zone of the North Pacific Central Gyre represented as the total biomass (WI in a size range (Awl divided by the magnitude of this range. The area under the graph, or the integral of the normalized spectrum over the analysed range, gives the relevant total biomass. The range of body weight presented in the graph corresponds to body sizes of approximately 10 wrn to S mm. Microplankton, open circles; macrozooplankton, filled circles; vertical lines. standard deviation. (b) The unnormalized spectrum for size ranges equal to the mean size. so that A W = W for logarithmically increasing weight categories. Reproduced, with permission, from Ref. 7.
55
TREE vol. 1, no. 3, September
References
Wiss. Meeresonters.
1 Sheldon, R.W., Prakash, A. and Sutcliffe, W.H. (1972) Limnol. Oceanogr. 17.327-340 2 Fenchel, T. (1974) Oecologia 14, 317-326 3 Banse, K. (1982) Mar. Ecol. Prog. Ser. 9,
6 Plait, T. and Denman, K. (1978) Rapp.
281-297
4 Kerr, S.R. (1974) J. Fish. Res. Board Can. 31,1859-1862 5 Platt, T. and Denman, K. (1977) He/go/.
30,576-581
P.-v. Reun. Cons. Int. Explor. Mer 173,
6C-65 7 Rodriguez, J. and Mullin, M.M. (1986) Limnol. Oceanogr. 31,361-370 6 Rigler, F.H. (1975) in Unifying Concepts in Ecology (van Dobben, W.H. and Lowe. McConnel, R.H.,eds), pp. 16-26, Junk 9 Cousins, S.H. (1980) J. Theor. Biol. 82, 607-618
BaldEagle SexRatios: Ladies Come First H. C. J. Godfray and P. H. Harvey Over the past 20 years there has been an explosion of interest in the evolution of the sex ratio. The assumptions that Fisher’ made to derive the prediction of an equal sex ratio are now known to be often violated in naturezr3. A large body of theory supported by a considerable amount of empirical evidence has accumulated describing the conditions under which biased sex ratios will evolve3”. However, biased sex ratios are more prominent in some taxonomic groups than in others. A likely explanation for this variation is that biased sex ratios will only evolve when a suitable sex determining mechanism facilitates their occurrence’. Examples of such mechanisms include environmental sex determination5 and haplodiploidy’. The sex determining mechanisms found in nearly all mammals and birds, in which sex is determined by sex chromosomes that segregate according to Mendel’s First Law, cannot easily accommodate biased sex ratios (see Ref. 5 for a lucid review). Nevertheless, quite a few cases of apparently adaptive biased sex ratios in mammals have been discovered6,7. This is currently a very active field in mammalogy, as evidenced by the number of new studies discussed this summer in Tucson at the annual meeting of the North American branch of the Association for the Study of Animal Behaviour. The examples from mammals are generally less extremely biased towards a particular sex than those from the haplodiploid hymenopterans or from reptiles and invertebrates with environmental sex determination. The situation is even Charles Godfray and Paul Harvey are at the Department of Zoology, South Parks Road, OxfordOX13PS.UK.
more frustrating for ornithologists, who have been allotted few places on this most fashionable of biological bandwagons. However, one intriguing example of apparently non-random sex allocation in birds has recently been revealed by Bortolotti’s studya of the US national bird, the Bald Eagle (Haliaeetus leucocephalus). Bald Eagles usually lay a pair of eggs, one or two days apart. The first egg laid apparently hatches before the second, and the first chick is bigger than its younger sibling. Depending on the sex of the young and the order in which the eggs are laid, there are four different types of brood: M-M, M-F, F-M, F-F. An F-M brood, for example, is one in which the larger sibling is a female and the smaller is a male. Random mendelian sex ratio theory predicts equal frequencies of all four classes. Bortolotti obtained data on 37 nests from a population of Bald Eagles at Besnard Lake in Saskatchewan. The numbers of the different types of brood were: 13 M-M, 1 M-F, 14 F-M and 9 F-F. These results are significantly different from random, the difference being in large part due to the very low frequency of M-F broods. Mortality between laying and the time at which the young can be sexed is very low, so the results cannot be explained by differential mortality. At least three other studies have shown an association between sex and egg sequence that does not seem to be explained by differential mortality. Snow Geese (Anser caerulescens) often lay clutches of four eggs. Ankney’ found that the first two eggs were more frequently male (64%) and the last two eggs more frequently female (72%). However, a much larger sample of the same species failed to show this
1986
10 Platt, T. (1985) Can. Bull. Fish. Aquat. Sci. 213,55-64 11 Hardy, A.C. (1924) Fish. Invest. Min. Agric. Fish. GB Ser. 2,7 (3)
12 Isaacs, J.D. (1973) Mar. Biol. 22,97-104 13 Sprules, W.G., Casselman, J.M. and Shuter, B.J. (1983) Can. J. Fish. Aquat. Sci. 40,1761-1769 14 Rodriguez, J. and Mullin, M.M. (1986) Ecology 67,215-222
trend”. Ryder” found that early eggs were male in Ring-Billed Gulls (Lams delawarensis) as did Mead (unpublished) in White-Crowned Sparrows Vonotrichia leucophreys). The two questions that these studies prompt are: why, and how? The favourite explanation for why males are laid first derives from the correlation between egg size and order of production. Large eggs are normally laid first and it may be more profitable to make these male if the marginal gain in benefit with size is greater for males than for females . For example, in polygynous species male fitness may increase with size more rapidly than female fitness if size affects the ability of a male to attract mates. In the case of Bald Eagles, Bortolotti proposes a different explanation. The larger first chick frequently kills its smaller sibling. Whether siblitide occurs depends on two factors: the quality of food being brought to the nest and the relative size difference of the young. It has been suggested that facultative brood reduction is adaptive because in years when food is in short supply the parent would not waste food on a second young that it could not rear (possibly also risking the survival of the first), while in good years both young would survive13. Male and female chicks display different patterns of growth, so that the relative difference in size between the chicks depends on their sexes. In particular, if the first chick is male and the second is female, the two are very different in size and siblicide is more likely. Bortolotti argues that M-F broods are rarely produced because they would be likely to experience brood reduction even in good years. As luck would have it, although the single M-F brood discovered displayed the expected size difference, its nest was situated next to a rich food source and no brood reduction occurred. The second question is how can parents produce the sex of their choice? In birds the female is the heterogametic sex and so non-
news
1986
Body size affects some important physiological and ecological parameters of marine organisms, such as their metabolic and potential growth ratesle3 and the size range of organisms that they can feed on or be eaten by. The distribution of body size in the ocean is a controversial topic. Some investigators”4 have proposed a flat spectrum in which different size groups have approximately the same total biomass, whereas others5f6 have proposed a spectrum of decreasing biomass with increasing body size. In a recent publication, Rodriguez and Mullin present an empirical size spectrum of living oceanic plankton from the Central North Pacific, revealing a regular and precise decrease of the total biomass with increasing body size between 10 km and 8 mm. The observations and methodology presented by Rodriguez and Mullin may be a significant step in studies of community structure and trophic relationships in pelagic ecosystems. The concept of discrete trophic levels with structured food chains in the marine environment has been criticized, primarily on the basis of the difficulties in assignin a trophic level to a given species 8! lo. These difficulties may be attributed to ontogenetic and seasonal changes in feeding habits of many species, as well as to the cyclic nature of pelagic food webs; adults of many marine invertebrate and fish taxa eat different food items from their juvenile and larval stages (e.g. Ref. 11) and eggs or larvae of fish may become food for planktonic species on which the adult fish themselves feed”. Most pelagic animals, however, feed on whatever food of suitable size is accessible by their feeding mode (see Refs 9 and 12). This allometric relationship between predator and prey has led to an increasing interest in the body size of marine organisms and to the use of size as an alternative to taxonomic and trophic characteristics of plankton. The first size spectrum of oceanic particles was reported by Sheldon and coworkers’ who combined their direct observations, in the size range of l-100 pm, with data from the literature and proposed that roughly equal concentrations of material (presented as p.p.m.) occur at all particle sizes from bacteria to whales. Their measurements, which have served for many years as the single published reference for the marine environment, were made Amatzia Genin is at the Scripps Institution of Oceanography,A-008,La Jolla, CA 92093,USA. 0
1986. Elsevier Science Publishers
B VI Amsterdam
Biomass andBodySizeofOceanic Plankton AmatziaGenin with a Coulter Counter (which automatically counts and measures particles, both living and non-living) and therefore included some unknown proportion of detrital particles. A similarly flat biomass spectrum has also been proposed by Kerr“, who based his theoretical model on the existence of discrete trophic levels. A different spectrum, of decreasing biomass with increasing body size, has been proposed by Platt and Denman506; their theoretical model is independent of the concept of trophic levels and assumes a continuous flow of biomass, or energy, from the smallest to the largest organisms. In lakes, on the other hand, the biomass spectra are apparently highly variable around a mean spectrum with a bimodal shape13. Rodriguez and Mullin’s observations are in agreement with the prediction of Platt and Denman and are clearly at odds with those of Sheldon et a/. and Kerr. The spectrum presented by Rodriguez and Mullin (Fig. 1) comprises two parts, each obtained by a different technique: phytoplankton and heterotrophic organisms larger than 10 pm but smaller than 200 pm (microplankton) were measured and counted under a microscope for later conversion to carbon weight, whereas animals larger than 183 km and smaller than 8 mm (macrozooplankton) were fractionated through a filter column of different mesh sizes and then weighed. Samples were collected from the euphotic zone of the nearsteady-state ecosystem of the Central North Pacific Gyre, during six cruises between 1972 and 1974. The results (Fig. 1) show a regular decrease of biomass, roughly as the negative one-sixth power of body weight, and the slopes obtained for microplankton and macrozooplankton are remarkably similar. Superimposed on this regularity is a variability with depth (larger organisms are relatively more important at greater depths), a seasonal variability, and an increase of the proportion of larger organisms during night time, caused by their diurnal vertical migration. In a se arate report, RodP, riguez and Mullin describe an additional source of variability caused by an unusually cold year. The methodology applied by Rodriguez and Mullin will probably become a standard procedure by which
0169-5347186150
200
additional spectra can be obtained for other oceanic regions such as temperate, coastal, and upwelling zones, and for depths below the euphotic zone. There is also a need to expand the spectrum to larger animals, such as fish and marine mammals, as well as to bacteria and organisms smaller than 10 pm. Biomass spectra, when available,, will provide an important means of different comparison between regions. This will unoceanic doubtedly contribute to our understanding of processes determining community structures in pelagic ecosystems, and may also be used to improve the management of fishery resources.
(4
w s
10-Z 1
; lo-4[, , , / , b, 0 us’ 10-Z
WEIGHT (PgC
m
-
)
2
0
‘idividuz-’
IO4
)
t
I
s,o‘ L.-------! 4 10-q
10-2
WEIGHT (PgC
IO0
IO*
individual-’
104
)
Fig. 1. (a) Normalized biomass spectrum in the euphotic zone of the North Pacific Central Gyre represented as the total biomass (WI in a size range (Awl divided by the magnitude of this range. The area under the graph, or the integral of the normalized spectrum over the analysed range, gives the relevant total biomass. The range of body weight presented in the graph corresponds to body sizes of approximately 10 wrn to S mm. Microplankton, open circles; macrozooplankton, filled circles; vertical lines. standard deviation. (b) The unnormalized spectrum for size ranges equal to the mean size. so that A W = W for logarithmically increasing weight categories. Reproduced, with permission, from Ref. 7.
55
TREE vol. 1, no. 3, September
References
Wiss. Meeresonters.
1 Sheldon, R.W., Prakash, A. and Sutcliffe, W.H. (1972) Limnol. Oceanogr. 17.327-340 2 Fenchel, T. (1974) Oecologia 14, 317-326 3 Banse, K. (1982) Mar. Ecol. Prog. Ser. 9,
6 Plait, T. and Denman, K. (1978) Rapp.
281-297
4 Kerr, S.R. (1974) J. Fish. Res. Board Can. 31,1859-1862 5 Platt, T. and Denman, K. (1977) He/go/.
30,576-581
P.-v. Reun. Cons. Int. Explor. Mer 173,
6C-65 7 Rodriguez, J. and Mullin, M.M. (1986) Limnol. Oceanogr. 31,361-370 6 Rigler, F.H. (1975) in Unifying Concepts in Ecology (van Dobben, W.H. and Lowe. McConnel, R.H.,eds), pp. 16-26, Junk 9 Cousins, S.H. (1980) J. Theor. Biol. 82, 607-618
BaldEagle SexRatios: Ladies Come First H. C. J. Godfray and P. H. Harvey Over the past 20 years there has been an explosion of interest in the evolution of the sex ratio. The assumptions that Fisher’ made to derive the prediction of an equal sex ratio are now known to be often violated in naturezr3. A large body of theory supported by a considerable amount of empirical evidence has accumulated describing the conditions under which biased sex ratios will evolve3”. However, biased sex ratios are more prominent in some taxonomic groups than in others. A likely explanation for this variation is that biased sex ratios will only evolve when a suitable sex determining mechanism facilitates their occurrence’. Examples of such mechanisms include environmental sex determination5 and haplodiploidy’. The sex determining mechanisms found in nearly all mammals and birds, in which sex is determined by sex chromosomes that segregate according to Mendel’s First Law, cannot easily accommodate biased sex ratios (see Ref. 5 for a lucid review). Nevertheless, quite a few cases of apparently adaptive biased sex ratios in mammals have been discovered6,7. This is currently a very active field in mammalogy, as evidenced by the number of new studies discussed this summer in Tucson at the annual meeting of the North American branch of the Association for the Study of Animal Behaviour. The examples from mammals are generally less extremely biased towards a particular sex than those from the haplodiploid hymenopterans or from reptiles and invertebrates with environmental sex determination. The situation is even Charles Godfray and Paul Harvey are at the Department of Zoology, South Parks Road, OxfordOX13PS.UK.
more frustrating for ornithologists, who have been allotted few places on this most fashionable of biological bandwagons. However, one intriguing example of apparently non-random sex allocation in birds has recently been revealed by Bortolotti’s studya of the US national bird, the Bald Eagle (Haliaeetus leucocephalus). Bald Eagles usually lay a pair of eggs, one or two days apart. The first egg laid apparently hatches before the second, and the first chick is bigger than its younger sibling. Depending on the sex of the young and the order in which the eggs are laid, there are four different types of brood: M-M, M-F, F-M, F-F. An F-M brood, for example, is one in which the larger sibling is a female and the smaller is a male. Random mendelian sex ratio theory predicts equal frequencies of all four classes. Bortolotti obtained data on 37 nests from a population of Bald Eagles at Besnard Lake in Saskatchewan. The numbers of the different types of brood were: 13 M-M, 1 M-F, 14 F-M and 9 F-F. These results are significantly different from random, the difference being in large part due to the very low frequency of M-F broods. Mortality between laying and the time at which the young can be sexed is very low, so the results cannot be explained by differential mortality. At least three other studies have shown an association between sex and egg sequence that does not seem to be explained by differential mortality. Snow Geese (Anser caerulescens) often lay clutches of four eggs. Ankney’ found that the first two eggs were more frequently male (64%) and the last two eggs more frequently female (72%). However, a much larger sample of the same species failed to show this
1986
10 Platt, T. (1985) Can. Bull. Fish. Aquat. Sci. 213,55-64 11 Hardy, A.C. (1924) Fish. Invest. Min. Agric. Fish. GB Ser. 2,7 (3)
12 Isaacs, J.D. (1973) Mar. Biol. 22,97-104 13 Sprules, W.G., Casselman, J.M. and Shuter, B.J. (1983) Can. J. Fish. Aquat. Sci. 40,1761-1769 14 Rodriguez, J. and Mullin, M.M. (1986) Ecology 67,215-222
trend”. Ryder” found that early eggs were male in Ring-Billed Gulls (Lams delawarensis) as did Mead (unpublished) in White-Crowned Sparrows Vonotrichia leucophreys). The two questions that these studies prompt are: why, and how? The favourite explanation for why males are laid first derives from the correlation between egg size and order of production. Large eggs are normally laid first and it may be more profitable to make these male if the marginal gain in benefit with size is greater for males than for females . For example, in polygynous species male fitness may increase with size more rapidly than female fitness if size affects the ability of a male to attract mates. In the case of Bald Eagles, Bortolotti proposes a different explanation. The larger first chick frequently kills its smaller sibling. Whether siblitide occurs depends on two factors: the quality of food being brought to the nest and the relative size difference of the young. It has been suggested that facultative brood reduction is adaptive because in years when food is in short supply the parent would not waste food on a second young that it could not rear (possibly also risking the survival of the first), while in good years both young would survive13. Male and female chicks display different patterns of growth, so that the relative difference in size between the chicks depends on their sexes. In particular, if the first chick is male and the second is female, the two are very different in size and siblicide is more likely. Bortolotti argues that M-F broods are rarely produced because they would be likely to experience brood reduction even in good years. As luck would have it, although the single M-F brood discovered displayed the expected size difference, its nest was situated next to a rich food source and no brood reduction occurred. The second question is how can parents produce the sex of their choice? In birds the female is the heterogametic sex and so non-