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1 stxb201208171158 2 Phosphorus limitation and excess carbon in zooplankton 3 SU Qiang1, 2, JIANG Xin2, LI Jiajun2 4 (1. Key Laboratory of Computational Geodynamics, Chinese Academy of Sciences, Beijing 5 100049; 2. University of Chinese Academy of Sciences, Beijing 100049, China) 6 Abstract: 7 Organisms rely on a series of chemical reactions, which are constrained by the availability of key 8 chemical elements, such as carbon (C), nitrogen (N), and phosphorus (P). Ecological 9 stoichiometry provides a tool for analyzing how the balance of elements required by organisms 10 affects food-web dynamics. Ecological stoichiometric theory suggests that the balance between 11 supply and demand of elements is determined by the conversion efficiency from resources to 12 organisms. 13 Autotrophs and heterotrophs commonly face unequal access to and uptake of elements. The 14 stoichiometric variability of autotrophs is based on their ability to maintain the balance of 15 elements required for growth. This creates a challenge for their grazers. Phytoplankton can adjust 16 their P content to ambient nutrient concentrations, while zooplankton cannot store excess nutrients. 17 Ecological stoichiometric theory thus suggests that zooplankton have relatively fixed 18 stoichiometry compared with phytoplankton. 19 Nutrient limitation is common in aquatic systems. Stoichiometric imbalances between 20 phytoplankton and zooplankton mean that zooplankton rarely find optimal food sources, and 21 phytoplankton production is in excess. P availability potentially limits zooplankton growth, 22 because of the high C:P ratio in phytoplankton relative to zooplankton demand. Based on the 23 Liebig minimum principle, organisms are normally limited by a single nutrient, while everything 24 else is in excess. Under P deficiency, excess C cannot be allocated to zooplankton somatic growth, 25 and the net intake of C must balance the C:P ratio of zooplankton. Thus, when zooplankton 26 encounter nutritionally imbalanced foods the elements in excess are released in order to maintain 27 homeostasis. Excess C, released by zooplankton results in two biochemical challenges: (1) to 28 sequester the limiting element and (2) to either store or dispose of the element in surplus. 29 Zooplankton must resort to various physiological solutions to cope with these challenges. As 30 a first option, zooplankton can reduce their C assimilation efficiency but maintain their P 31 assimilation efficiency. Alternatively, after assimilation, excess C may be stored in C-rich 32 compounds. Finally, assimilated excess C could also be disposed of through respiration or 33 extracellular release. Excess C released by zooplankton reduces C transfer efficiency and 34 sequestration in aquatic ecosystems. 35 In aquatic ecosystems, C sequestration largely depends on the balance between uptake and 36 demand for key nutrient elements. These feedback mechanisms have arisen only because 37 organisms must obey stoichiometric rules at the cell and body levels, which greatly constrain the 38 range of element values in ecosystems. Thus, the fate of C in ecosystems is determined by the 39 absolute and relative demands for N and P of each organism. Limiting elements are utilized for 40 growth and transferred in food chains with high efficiency, while non-limiting elements must be 1 disposed of. Therefore, low C:P phytoplankton communities subject to high turnover rates and 2 high productivity are selectively channeled into zooplankton. When zooplankton face high C:P 3 foods, excess C is returned to the environment. Hence, nutrient-deficient phytoplankton constitute 4 poor food, influencing the entire food web and adversely affecting secondary production at all 5 levels. 6 Excess C processed by zooplankton has far-reaching implications for ecosystem food-web 7 functioning and C sequestration. Studies of the fate of excess C in zooplankton would increase the 8 understanding of energy flow and material cycling in aquatic ecosystems. This paper reviews the 9 reasons for P limitation and excess C in zooplankton, principal routes for the disposal of excess C, 10 and the ecological effects of this. In addition, the paper aims to provide insight and a theoretical 11 foundation for related studies in China. 12 Key words: ecological stoichiometry; zooplankton; phosphorus limitation; excess carbon 13 14 Ecological stoichiometry provides a rule, based on the interaction between elemental ratios 15 and ecological processes, to classify all kinds of organisms in one group at the level of chemical 16 elements[1], and is a subject to study the balance of energy and multiple chemical elements in 17 ecosystem[2]. The ecological stoichiometric theory suggests that biological functions are 18 determined by the contents and constituents of nutrients, and the realization of a certain biological 19 function is corresponding to a decided elemental ratio. Accordingly, a dynamic balancing is 20 established between organisms and ecosystem, in that case, different balances between organisms 21 and the environment result in different ecological effects[3]. 22 Zooplankton make significant effects on governing the energy flux and the material recycling 23 in aquatic ecosystems, and are featured by multiple species, widely distribution, and large 24 quantities[4]. It has been suggested that phytoplankton vary greatly in elemental composition and 25 tent to experience a relatively deficiency in nutrients[5]; Due to phytoplankton’s high demands for 26 nutrients and their high homeostasis[3],the major subjects of planktonic trophodynamics are 27 focused on the imbalance of elements in phytoplankton supplies and the difference in homeostasis 28 with zooplankton[6-7]. 29 Based on the homeostasis of organisms, ecological stoichiometry suggests that the elemental 30 composition of food influence the growth and reproduction of the grazers[3, 8]. In order to maintain 31 homeostasis, zooplankton must release some nutrients when the supplies are deficient[9]. The low 32 phosphorus: carbon (P:C) ratio in phytoplankton results in the P limitation of their grazers. 33 Therefore, with the constrain of homeostatic elemental ratios, excess C must be disposed of in 34 various ways by zooplankton[5], and there comes the question of P limitation and excess C. This 35 question has been studied widely in the world but rarely in China[4]. Thus, based on the 36 international and domestic researches in recent years and ecological stoichiometric theory, this 37 paper reviews the reasons for P limitation and excess C in zooplankton, principal routes for the 38 disposal of excess C and the concomitant ecological effects. In addition, the paper aims to provide 39 insight and a theoretical foundation for related studies in China. 1 1.Difference in ecological stoichiometry homeostasis 2 On one hand, the elemental composition of organisms is influenced by the ambient and is a 3 reflection of the nutritional conditions of the environment; on the other hand, organisms are 4 required to maintain the balance of the elemental ratios[1], which is called homeostasis[10]. 5 Homeostasis is one of the essential features of life, including homeostasis of many parameters, e.g. 6 temperature, moisture content, and pH. Homeostasis (or the degree of homeostasis) in this paper 7 manly implies stability of the nutrient elemental composition (C:N:P). The degree of 8 stoichiometry homeostasis is characterized by the homeostasis coefficient 1/H which takes values 9 between zero and one. Species with 1/H→0 are strictly homeostatic, i.e. the change of ambient 10 nutritional conditions cannot change the elemental composition of organisms[3]. According to the 11 homeostasis coefficient 1/H, some researchers ranked the homeostasis of organisms in two levels: 12 'strong homeostatic' (0—0.25) and 'weakly homeostatic' (0.25—0.5)[8]. Homeostasis of elemental 13 composition varies from autotrophs to heterotrophs[9, 14 maintain relatively strict homeostasis in stoichiometry compared with phytoplankton (Fig. 1)[3]. 15 The strong homeostasis in stoichiometry of zooplankton is comparative to phytoplankton. 16 Zooplankton are not absolute homeostatic either. 11]. It is considered that zooplankton 17 The growth of organism is restricted by ecological stoichiometry homeostasis, including 18 absorption, assimilation, storage, and release of elements[11]. The elemental composition in 19 phytoplankton is for the material balance of physiological functions. Thus, the elemental 20 composition in phytoplankton varies from different phases of growing[9]. Phytoplankton will store 21 more C content for photosynthesis, under the condition of high light but low nutrients, both C:N 22 and C:P ratios will chang[12]. The elemental composition in phytoplankton is regulated by ionic 23 equilibrium, while N and P of zooplankton are stored in the form of amino acids, proteins, and 24 other organic matters[8]. Zooplankton maintain relatively strict homeostasis in stoichiometry 25 compared with phytoplankton[13-14], i.e. the composition of elements keeps nearly fixed[9, 11]. 26 Fig. 1 The contrast between zooplankton and phytoplankton in ecological stoichiometry homeostasis: (A) Phytoplankton stoichiometric composition could vary widely with fluctuations in nutrient supply[16], and (B)zooplankton was generally thought to be strictly homeostatic[13]. 27 28 29 Because of the strict homeostasis, when the elemental composition in phytoplankton changed, it is hardly possible for zooplankton to make response[15]. Phytoplankton with weak homeostasis possess advantages in evolution,because high C:P ratio and low P content restricts the growth of 1 2 zooplankton[9]. In essence, it is the difference in homeostasis of phytoplankton that result in P limitation and excess C in zooplankton. 3 2.Nutritional imbalances in food supplies 4 In addition to the difference of homeostasis between zooplankton and phytoplankton, P 5 limitation and excess C in zooplankton is resulted from nutritionally imbalanced food supplies. 6 C:P ratio is commonly high in phytoplankton because of deficient nutrients, while the C:P ratio is 7 relatively low in zooplankton with a rather fixed elemental composition[17]. Thus, in terms of 8 zooplankton, P limitation and excess C resulted from nutrient-imbalanced food supplies has 9 become more meaningful (Fig. 2). 10 Fig. 2 The C: P ratios was higher in phytoplankton with lower P content relative to zooplankton[18]. 11 The primary problem which the grazers faced with is the difference between food supplies 12 and somatic demands[5, 9]. Daphnia magna requires more P than foods provide[19]. Zooplankton 13 tend to be limited by P because of high P demands and strong homeostasis[20]. P is the essential 14 element for RNA[12]. Thus, the synthesis of ribosomes and protein synthesis can be affected by P 15 limitation 16 growth of zooplankton is limited[21] (Fig. 3). Hence, somatic growth rate will decrease when 17 consumers are faced with P-deficient food[22]. For example, the growth of Daphnia and rotifers is 18 limited by P content[19, 23]. As a potential limiting factor in zooplankton growth, P limitation is 19 resulted from the high C:P ratio of phytoplankton[24]. [3]. Because of decrease of P content in the phytoplankton with high C:P ratio, the 20 Ecological stoichiometric theory considers Threshold Elemental Ratio (TER) as the standard 21 in judging whether nutrients are limited[17, 25]. The element X is regarded to limit the consumers if 22 the ratio of C to nutrient element X (i.e. C:X ratio) is larger than the TER, otherwise they are 23 limited by C. Taking C:P ratio for example, two approaches are commonly used to estimate TERs 24 of phytoplankton: (1) Determined by the growth rate and egg production responses of zooplankton 25 along a gradient of C:P food or different dietary P additions and (2) calculations can be undertaken 26 based on stoichiometric theory in which elemental ratios and utilized efficiency are taken into 27 account[26]. For example, if a zooplankter with C:P in biomass of 75 (by atoms) utilized C and P in 28 food with maximum efficiencies of 50% and 100%, respectively, then the TER is 75×100/50=150. 29 In Daphnia, the range from 3–7 mg atomic P [mg atomic C]-1 (atomic ratio C:P =150–300) have 30 been proposed as thresholds for the onset of P limitation[27]. In actually, however, C:P ratio often 31 exceeds 230 in phytoplankton[26]. 32 The somatic growth rate of zooplankton will decrease when P is limited [24, 28] and 1 zooplankton are not able to utilize C fully in phytoplankton for secondary production[19, 21]. Then, 2 when the P content in phytoplankton decreases to a very low level, zooplankton contenting more P 3 suffers negative population growth regardless of algal biomass[28]. The transfer efficiency of C is 4 determined by assimilation efficiency of trophic levels[21], so excess C will return into the 5 6 environment with the deficiency of P [12]. 3.P limitation and excess C 7 Liebig minimum principle——the core section of ecological stoichiometry——suggest that 8 other elements be in excess when there is one limiting nutrient element[12]. Therefore there exist 9 two inevitable related problems, deficiency and excess of elements, when organisms with strict 10 homeostasis encounter mismatches between their own demands and dietary supplies. P limitation 11 tends to occur[12] because P content in phytoplankton is low while the demand for P of 12 zooplankton is high[17, 23]. With the rather tight homeostatic control in zooplankton, the C-use must 13 balance the P-use[28]. Thus, in addition to P limitation in zooplankton[17, 23], excess C occurs at the 14 same time[12, 14]. 15 Fig. 3 The higher C: P ratios and lower P content of phytoplankton could potentially limit zooplankton growth[12]. 16 The preconditions of P limitation and excess C in zooplankton are: (1) P deficiency in food 17 supplies of phytoplankton and (2) high P demands of zooplankton with strict homeostasis. C is in 18 excess when C:P of food supplies exceeds TER[9]. With increasing of the C:P ratio in 19 phytoplankton, the growth rate of zooplankton declines, P becomes the limiting factor and C must 20 be disposed of and transform into waste[12, 20]. The deficient elements and excess elements will 21 changeover in certain conditions, i.e. when limited by C or N in zooplankton, P could be in 22 excess[12]. 23 Though zooplankton use lipids as a source storing C, lipids account for a relatively small 24 fraction of body mass[17]. Thus, the growth of zooplankton is a process to concentrate deficient 25 elements and dispose of excess compounds[29]. For accomplishing this process, zooplankton must 26 take some measures, and pre- or post-assimilatory regulations in the gut are two main 27 approaches[17]. 28 4.Disposal of the excess C 29 Consumers dispose excess elements [30]and assimilate limiting elements efficiently[12, 17] in 1 order to maintain homeostasis. As for organisms with strict homeostasis, concentrating deficient 2 elements and disposing off excess compounds complement with each other. Under the condition 3 of P limitation, intaking of P is comparatively increasing with higher consumption of C in 4 zooplankton[15]. To cope with P limitation, zooplankton will increase sequestration of P, or dispose 5 of excess C or do both[14]. 6 When faced with P limitation, zooplankton will sort to different strategies in homeostatic 7 regulation[23, 31] basing on elemental composition and food supplies[11]. With the increase of C:P 8 ratio in phytoplankton, both the release of P and assimilation of C in zooplankton will decrease[14, 9 19] . Feeding on food with high C:P ratio, the respiratory rate and the release of dissolved organic 10 carbon (DOC) in Daphnia increase[19]. The excretion of particles in zooplankton may be the main 11 approach to disposing of the ‘leftover C’[11, 17]. 12 Three important links to maintain homeostasis in zooplankton are: (1) food selectivity, (2) 13 regulation of assimilation efficiencies, and (3) disposal of the excess elements[23, 32]. Zooplankton 14 also use lipids to store C but account for a relatively small fraction[17]. Regulating through changed 15 food selectivity is a pre-feeding method. Food supplies in the environment for Zooplankton vary 16 frequently[17]. The food zooplankton preying on range in broad particle sizes, and zooplankton are 17 unable to reject poor-quality particles individually[17]. Thus Pre- and post-assimilatory regulations 18 in the gut are bound to the main approaches to maintaining homeostasis in zooplankton. 19 4.1 Pre-assimilatory regulation 20 Zooplankton are able to change the assimilation efficiency of C[14, 26]. The C assimilation 21 efficiency will change when zooplankton experience different nutritional conditions[17] (Fig. 4). 22 The C assimilation efficiency decreases by 30% in Daphnia magna when the C:P ratio in 23 phytoplankton increase from 80 to 164[19]. The regulation of C assimilation efficiency has nothing 24 to do with the metabolic machinery, and production of certain enzymes (like lipases and 25 carbohydrases) could be relaxed[12]. The benefit of pre-assimilatory regulation, in conclusion, is 26 that the metabolic cost would be reduced when zooplankton experience changing food supplies[26]. 27 Fig. 4 The C assimilation efficiency of zooplankton under different food C: P[19]. 28 Gut residence time may be the reason why P assimilation efficiency of zooplankton actually 29 decreases, while the C:P ratio in food increase[12]. Because of the short gut residence time of 30 high-C:P food, P may be disposed of without being fully absorbed[33]. This accounts for the reason 1 why zooplankton dispose of P in spite of P limitation[33-34]. The absolute non-release of P is 2 impossible[12], so improving P assimilation efficiency works little for maintaining homeostasis. 3 Therefore, the main part of pre-assimilatory regulation in zooplankton should be the way of 4 changing C assimilation efficiency. 5 4.2 Post-assimilatory regulation 6 Elemental Components identification and following adjustments can be done only after food 7 is assimilated by grazers[12]. The absorption of macromolecules is variable, which accurately 8 monitors compounds hydrolyzed into their constituents, such as monosaccharides and amino 9 acids[17]. Hence, post-assimilatory regulation is more effective than pre-assimilatory regulation[14, . Some zooplankton dispose of ‘leftover C’ mainly by post-assimilatory regulation, including 10 17] 11 increasing respiration and release of organic C compounds[14]. 12 Release of organic C compounds through zooplankton[12, 23] originates from three different 13 sources: (1) feeding losses, (2) faecal particles, and (3) extracellular secretion[19]. Elements losses 14 are related to the components in original food without exception and can not be regulated. C 15 release from faeces is linked to the assimilation when transferring in the gut. For pre-assimilatory 16 regulation, if less C is assimilated from food during transfer in the gut, more C will potentially be 17 lost via faeces[19]. While post-assimilatory regulation is mainly based on the secretion of organic 18 matters[17]. Daphnia magna, for example, the secretion of DOC increase by 1 time when fed with 19 high C:P ratio food[19, 23] (Fig. 5). 20 Fig. 5 Under P deficiency, excess C could be coped by zooplankton extracellular release DOC[19]. 21 Respired as CO2 can also be a way of releasing excess C in post-assimilatory regulation[14, 19]. 22 Appendage beat rate and heartbeat rate are increased under P-deficient diets[12], indicating that 23 zooplankton increase respiration by both behavioral and physiological mechanisms[33]. Disposal 24 by respiration involves biochemical oxidation that could produce energy, implying metabolic 25 advantages[23], but also cellular disadvantages such as the production of free radicals[12]. However, 26 respiration has been controversial when it comes to disposal of excess C. Because this 27 growth-related cost constitutes a significant portion of the total respiratory cost, decreased growth 28 rate should be associated with decreased total respiration[14]. Because reduced respiration due to 29 reduced growth rate could counteract an elevated release of excess C,respiration will not increase 30 significantly[14]. Although increased respiration could be a transient phenomenon in response to 1 P-deficient diets[23], it could be more important to release organic C compounds[14]. For example, 2 Brachionus calyciflorus release excess C mainly by extracellular secretion or excreting as faecal 3 material[14, 23]. 4 The excess C, released from zooplankton in organic form,is helpful to heterotrophic processes 5 in ecosystems, while somatic growth gets benefit if disposed in the form of CO2. The ecological 6 effects of those two processes are entirely different[12]. In terms of energy flow and material 7 cycling, the reduced C assimilatory efficiency will effect the C transfer efficiency in food web and 8 sequestration in aquatic ecosystems[9, 14]. 9 5.Ecological effects of excess C regulation 10 C transfer efficiency is determined by the supplies and demands of limiting elements across 11 trophic levels[9, 21]. The absolute and the relative availability of limiting elements determines C 12 transfer efficiency[14]. Phytoplankton usually concentrate excess C and thereby reduce P content 13 relatively[12], and this process will have an adverse effect on secondary production of ecosystem[5]. 14 The disposals of excess C taken by zooplankton[25], not only reducing C transfer efficiency but 15 also detaining more C in the environment[9, 14], influence the fate or sequestration of C[17, 23] (Fig. 16 6). Therefore, the system would enter a stage with high biomass of C-excess phytoplankton which 17 do not support zooplankton growth[28]. 18 Fig. 6 To maintain homeostasis, released excess C by zooplankton reduced C transfer efficiency[9]. 19 Organisms must obey stoichiometric rules, which constrain the production, intake, transfer, 20 and storage of nutrients in food web[9]. In order to maintain homeostasis, grazers dispose excess 21 substances and improve the relative content of limiting elements. Limiting elements(e.g. P)are 22 expected to be transferred in food chains with high efficiency, while excess elements(e.g. C) 23 could be recycled into the environment[9]. Palatable phytoplankton (Low C:P) subject to high 24 turnover rates, a high share of production is utilized, rather than being excluded from the food 25 web[12]. Therefore, as the major driver for material transfer, the regulation of excess C in 26 phytoplankton ensures nutrients be supplied and stabilization in the ecosystem[14]. 1 The homeostatic regulation of zooplankton results in more C accumulating in the environment. 2 In an evolutionary context, one should expect strong selective pressure towards utilization of this 3 excess C[9]. The substances released from disposals of excess C, could be a potential source for 4 bacterial production[17, 23], and enhance the functions of bacteria in C cycling[12, 14]. Furthermore, 5 vertical flux of C will increase because of the production of feces from regulation of excess C 6 and thereby more C will be sequestered in detritus[9]. If the disposal of excess C generates CO2, 7 planktonic microbial loop will get benefit [19]. In conclusion, regulation of excess C in zooplankton 8 generates several kinds of metabolites, then affects the global material cycling, and has 9 far-reaching implications for marine and global C sequestration[19]. 10 [23] 6.Future work 11 Hence, the composition of zooplankton community and stoichiometric quality are the major 12 subjects of planktonic ecosystem trophodynamics[23]. Facing an excess of C is an inevitable 13 response for zooplankton to stress and rapidly changing environment. The coastal area, one of the 14 most significant ecosystems, is affected heavily by industrial activities. Recent years, 15 eutrophication has become the main problem in coastal ecosystem[35]. According to ecological 16 stoichiometry, the content in phytoplankton will enhance with the increasing input of P in aquatic 17 ecosystem[33], thereby the condition of P limitation in zooplankton will be relieved and the 18 assimilation and transfer efficiency of C will be improved [26]. In actually, however, phytoplankton 19 will be at a high risk if P content is increased. If the P content in phytoplankton is comparatively 20 high, the biomass of zooplankton will decline heavily because of great grazing pressure regardless 21 of food selectivity. Therefore, in coastal area with increasing P inputs, phytoplankton probably 22 evolve to a condition with larger biomass, less relative P content, higher C:P under the mechanism 23 of natural selection. Those evolvement might change the composition of community and 24 stoichiometry of zooplankton. The study of ecological stoichiometry in zooplankton, thus helps us 25 to explore the nutrient dynamic responses of plankton to eutrophication, and improve our 26 understanding of the regional carbon cycle and the future change of that. 27 28 29 Reference: 30 [1]Zeng D H, Chen G S. Ecological stoichiometry: a science to explore the complexity of living systems. Acta 31 Phytoecologica Sinica, 2005, 29(6): 1007-1019. 32 [2]Wang S Q, Yu G R. Ecological stoichiometry characteristics of ecosystem carbon, nitrogen and phosphorus 33 elements. Acta Ecologica Sinica, 2008, 28(8): 3937-3947. 34 [3]Sterner R W, Elser J J. Ecological stoichiometry: the biology of elements from molecules to the biosphere. 35 Princeton, New Jersey: Princeton University Press, 2002. 36 [4]Li Y. Carbon, Nitrogen and Phos Phorus Stoichimetry of Freshwater ZooPlankton in Guangdong Provinee, 37 South China [D]. Guangzhou: Jinan University, 2011. 38 [5]Van Donk E, Lürling M, Hessen D O, Lokhorst G M. Altered cell wall morphology in nutrient-deficient 39 phytoplankton and its impact on grazers. Limnology and Oceanography, 1997, 42(2): 357-364. 40 [6]Elser J. Biological stoichiometry: A chemical bridge between ecosystem ecology and evolutionary biology. 1 American Naturalist, 2006, 168(S6): S25-S35. 2 [7]Kyle M, Acharya K, Weider L J, Looper K, Elser J J. Coupling of growth rate and body stoichiometry in 3 Daphnia: a role for maintenance processes? Freshwater Biology, 2006, 51(11): 2087-2095. 4 [8]Persson J, Fink P, Goto A, Hood J M, Jonas J, Kato S. To be or not to be what you eat: regulation of 5 stoichiometric homeostasis among autotrophs and heterotrophs. Oikos, 2010, 119(5): 741-751. 6 [9]Hessen D O, Ågren G I, Anderson T R, Elser J J, De Ruiter P C. Carbon sequestration in ecosystems: The role 7 of stoichiometry. Ecology, 2004, 85(5): 1179-1192. 8 [10] Koojiman S A L M. The stoichiometry of animal energetics. Journal of Theoretical Biology, 1995, 177(2): 9 139-149. 10 [11]Frost P C, Evans-White M A, Finkel Z V, Jensen T C, Matzek V. Are you what you eat? Physiological 11 constraints on organismal stoichiometry in an elementally imbalanced world. Oikos, 2005, 109(1): 18-28. 12 [12]Hessen D O, Anderson T R. Excess carbon in aquatic organisms and ecosystems: Physiological, ecological, 13 and evolutionary implications. Limnology and Oceanography, 2008, 53(4): 1685-1696. 14 [13]Ferrão-Filho A D S, Tessier A J, Demott W R. Sensitivity of herbivorous zooplankton to phosphorus-deficient 15 diets: Testing stoichiometric theory and the growth rate hypothesis. Limnology and Oceanography, 2007, 52(1): 16 407-415. 17 [14]Jensen T C, Hessen D O. Does excess dietary carbon affect respiration of Daphnia? Oecologia, 2007, 152(2): 18 191-200. 19 [15]Hessen D O. Nutrient element limitation of zooplankton production. American Naturalist, 1992, 140(5): 20 799-814. 21 [16]Hessen D O. Efficiency, energy and stoichiometry in pelagic food webs; reciprocal roles of food quality and 22 food quantity. Freshwater Reviews, 2008, 1(1): 43-57. 23 [17]Anderson T R, Hessen D O, Elser J J, Urabe J. Metabolic stoichiometry and the fate of excess carbon and 24 nutrients in consumers. American Naturalist, 2005, 165(1): 1-15. 25 [18]Boersma M, Aberle N, Hantzsche F M, Schoo K L, Wiltshire K H, Malzahn A M. Nutritional limitation travels 26 up the food chain. International Review of Hydrobiology, 2008, 93(4-5): 479-488. 27 [19]Darchambeau F, Faerøvig P J, Hessen D O. How Daphnia copes with excess carbon in its food. Oecologia, 28 2003, 136(3): 336-346. 29 [20]Hessen D O. The role of mineral nutrients for zooplankton nutrition: reply to the comment by Brett. 30 Limnology and Oceanography, 1993, 38(6): 1340-1343. 31 [21]Hessen D O, Rukke N A. The costs of moulting in Daphnia; mineral regulation of carbon budgets. Freshwater 32 Biology, 2000, 45(2): 169-178. 33 [22]Stige L C, Hessen D O, Vøllestad L A. Severe food stress has no detectable impact on developmental 34 instability in Daphnia magna. Oikos, 2004, 107(3): 519-530. 35 [23]Jensen T C, Anderson T R, Daufresne M, Hessen D O. Does excess carbon affect respiration of the rotifer 36 Brachionus calyciflorus Pallas? Freshwater Biology, 2006, 51(12): 2320-2333. 37 [24]Wojewodzic M W, Rachamim T, Andersen T, Leinaas H P, Hessen D O. Effect of temperature and dietary 38 elemental composition on RNA/protein ratio in a rotifer. Functional Ecology, 2011, 25(5): 1154-1160. 39 [25]Andersen T, Elser J J, Hessen D O. Stoichiometry and population dynamics. Ecology Letters, 2004, 7(9): 40 884-900. 1 [26]Anderson T R, Hessen D O. Threshold elemental ratios for carbon versus phosphorus limitation in Daphnia. 2 Freshwater Biology, 2005, 50(12): 2063-2075. 3 [27]Hessen D O, Færøvig P J, Andersen T. Light, nutrients, and P : C ratios in algae: Grazer performance related to 4 food quality and quantity. Ecology, 2002, 83(7): 1886-1898. 5 [28]Hessen D O, Bjerkeng B. A model approach to planktonic stoichiometry and consumer-resource stability. 6 Freshwater Biology, 1997, 38(3): 447-471. 7 [29]Darchambeau F, Thys I, Leporcq B, Hoffmann L, Descy J P. Influence of zooplankton stoichiometry on 8 nutrient sedimentation in a lake system. Limnology and Oceanography, 2005, 50(3): 905-913. 9 [30]Vrede T, Andersen T, Hessen D O. Phosphorus distribution in three crustacean zooplankton species. 10 Limnology and Oceanography, 1999, 44(1): 225-229. 11 [31]Jensen T C, Leinaas H P, Hessen D O. Age-dependent shift in response to food element composition in 12 Collembola: contrasting effects of dietary nitrogen. Oecologia, 2006, 149(4): 583-592. 13 [32]Logan J D, Joern A, Wolesensky W. Control of CNP homeostasis in herbivore consumers through differential 14 assimilation. Bulletin of Mathematical Biology, 2004, 66(4): 707-725. 15 [33]Plath K, Boersma M. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. 16 Ecology, 2001, 82(5): 1260-1269. 17 [34]Liu S, Wang W X, Huang L M. Phosphorus dietary assimilation and efflux in the marine copepod Acartia 18 erythraea. Marine Ecology-Progress Series, 2006, 321: 193-202. 19 [35]Wang B D. Eutrophication Status and Its Ecological Effects in the Changjiang Estuary and Adjacent Coastal 20 Waters [D]. Qingdao: Ocean University of China, 2006. 21 22 参考文献: 23 [1]曾德慧, 陈广生. 生态化学计量学: 复杂生命系统奥秘的探索. 植物生态学报, 2005, 29(6): 1007-1019. 24 [2]王绍强, 于贵瑞. 生态系统碳氮磷元素的生态化学计量学特征. 生态学报, 2008, 28(8): 3937-3947. 25 [4]李莹. 南亚热带地区主要浮游动物种类 C、N、P 营养元素计量学研究 [D]. 广州: 暨南大学, 2011. 26 [35]王保栋. 长江口及邻近海域富营养化状况及其生态效应 [D]. 青岛: 中国海洋大学, 2006.