Download Ecological stoichiometry is a principle to unify the

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stxb201208171158
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Phosphorus limitation and excess carbon in zooplankton
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SU Qiang1, 2, JIANG Xin2, LI Jiajun2
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(1. Key Laboratory of Computational Geodynamics, Chinese Academy of Sciences, Beijing
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100049; 2. University of Chinese Academy of Sciences, Beijing 100049, China)
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Abstract:
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Organisms rely on a series of chemical reactions, which are constrained by the availability of key
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chemical elements, such as carbon (C), nitrogen (N), and phosphorus (P). Ecological
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stoichiometry provides a tool for analyzing how the balance of elements required by organisms
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affects food-web dynamics. Ecological stoichiometric theory suggests that the balance between
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supply and demand of elements is determined by the conversion efficiency from resources to
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organisms.
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Autotrophs and heterotrophs commonly face unequal access to and uptake of elements. The
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stoichiometric variability of autotrophs is based on their ability to maintain the balance of
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elements required for growth. This creates a challenge for their grazers. Phytoplankton can adjust
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their P content to ambient nutrient concentrations, while zooplankton cannot store excess nutrients.
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Ecological stoichiometric theory thus suggests that zooplankton have relatively fixed
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stoichiometry compared with phytoplankton.
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Nutrient limitation is common in aquatic systems. Stoichiometric imbalances between
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phytoplankton and zooplankton mean that zooplankton rarely find optimal food sources, and
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phytoplankton production is in excess. P availability potentially limits zooplankton growth,
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because of the high C:P ratio in phytoplankton relative to zooplankton demand. Based on the
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Liebig minimum principle, organisms are normally limited by a single nutrient, while everything
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else is in excess. Under P deficiency, excess C cannot be allocated to zooplankton somatic growth,
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and the net intake of C must balance the C:P ratio of zooplankton. Thus, when zooplankton
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encounter nutritionally imbalanced foods the elements in excess are released in order to maintain
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homeostasis. Excess C, released by zooplankton results in two biochemical challenges: (1) to
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sequester the limiting element and (2) to either store or dispose of the element in surplus.
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Zooplankton must resort to various physiological solutions to cope with these challenges. As
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a first option, zooplankton can reduce their C assimilation efficiency but maintain their P
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assimilation efficiency. Alternatively, after assimilation, excess C may be stored in C-rich
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compounds. Finally, assimilated excess C could also be disposed of through respiration or
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extracellular release. Excess C released by zooplankton reduces C transfer efficiency and
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sequestration in aquatic ecosystems.
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In aquatic ecosystems, C sequestration largely depends on the balance between uptake and
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demand for key nutrient elements. These feedback mechanisms have arisen only because
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organisms must obey stoichiometric rules at the cell and body levels, which greatly constrain the
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range of element values in ecosystems. Thus, the fate of C in ecosystems is determined by the
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absolute and relative demands for N and P of each organism. Limiting elements are utilized for
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growth and transferred in food chains with high efficiency, while non-limiting elements must be
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disposed of. Therefore, low C:P phytoplankton communities subject to high turnover rates and
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high productivity are selectively channeled into zooplankton. When zooplankton face high C:P
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foods, excess C is returned to the environment. Hence, nutrient-deficient phytoplankton constitute
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poor food, influencing the entire food web and adversely affecting secondary production at all
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levels.
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Excess C processed by zooplankton has far-reaching implications for ecosystem food-web
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functioning and C sequestration. Studies of the fate of excess C in zooplankton would increase the
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understanding of energy flow and material cycling in aquatic ecosystems. This paper reviews the
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reasons for P limitation and excess C in zooplankton, principal routes for the disposal of excess C,
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and the ecological effects of this. In addition, the paper aims to provide insight and a theoretical
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foundation for related studies in China.
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Key words: ecological stoichiometry; zooplankton; phosphorus limitation; excess carbon
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Ecological stoichiometry provides a rule, based on the interaction between elemental ratios
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and ecological processes, to classify all kinds of organisms in one group at the level of chemical
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elements[1], and is a subject to study the balance of energy and multiple chemical elements in
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ecosystem[2]. The ecological stoichiometric theory suggests that biological functions are
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determined by the contents and constituents of nutrients, and the realization of a certain biological
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function is corresponding to a decided elemental ratio. Accordingly, a dynamic balancing is
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established between organisms and ecosystem, in that case, different balances between organisms
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and the environment result in different ecological effects[3].
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Zooplankton make significant effects on governing the energy flux and the material recycling
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in aquatic ecosystems, and are featured by multiple species, widely distribution, and large
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quantities[4]. It has been suggested that phytoplankton vary greatly in elemental composition and
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tent to experience a relatively deficiency in nutrients[5]; Due to phytoplankton’s high demands for
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nutrients and their high homeostasis[3]，the major subjects of planktonic trophodynamics are
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focused on the imbalance of elements in phytoplankton supplies and the difference in homeostasis
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with zooplankton[6-7].
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Based on the homeostasis of organisms, ecological stoichiometry suggests that the elemental
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composition of food influence the growth and reproduction of the grazers[3, 8]. In order to maintain
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homeostasis, zooplankton must release some nutrients when the supplies are deficient[9]. The low
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phosphorus: carbon (P:C) ratio in phytoplankton results in the P limitation of their grazers.
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Therefore, with the constrain of homeostatic elemental ratios, excess C must be disposed of in
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various ways by zooplankton[5], and there comes the question of P limitation and excess C. This
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question has been studied widely in the world but rarely in China[4]. Thus, based on the
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international and domestic researches in recent years and ecological stoichiometric theory, this
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paper reviews the reasons for P limitation and excess C in zooplankton, principal routes for the
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disposal of excess C and the concomitant ecological effects. In addition, the paper aims to provide
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insight and a theoretical foundation for related studies in China.
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1．Difference in ecological stoichiometry homeostasis
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On one hand, the elemental composition of organisms is influenced by the ambient and is a
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reflection of the nutritional conditions of the environment; on the other hand, organisms are
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required to maintain the balance of the elemental ratios[1], which is called homeostasis[10].
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Homeostasis is one of the essential features of life, including homeostasis of many parameters, e.g.
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temperature, moisture content, and pH. Homeostasis (or the degree of homeostasis) in this paper
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manly implies stability of the nutrient elemental composition (C:N:P). The degree of
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stoichiometry homeostasis is characterized by the homeostasis coefficient 1/H which takes values
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between zero and one. Species with 1/H→0 are strictly homeostatic, i.e. the change of ambient
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nutritional conditions cannot change the elemental composition of organisms[3]. According to the
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homeostasis coefficient 1/H, some researchers ranked the homeostasis of organisms in two levels:
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'strong homeostatic' (0—0.25) and 'weakly homeostatic' (0.25—0.5)[8]. Homeostasis of elemental
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composition varies from autotrophs to heterotrophs[9,
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maintain relatively strict homeostasis in stoichiometry compared with phytoplankton (Fig. 1)[3].
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The strong homeostasis in stoichiometry of zooplankton is comparative to phytoplankton.
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Zooplankton are not absolute homeostatic either.
11].
It is considered that zooplankton
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The growth of organism is restricted by ecological stoichiometry homeostasis, including
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absorption, assimilation, storage, and release of elements[11]. The elemental composition in
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phytoplankton is for the material balance of physiological functions. Thus, the elemental
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composition in phytoplankton varies from different phases of growing[9]. Phytoplankton will store
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more C content for photosynthesis, under the condition of high light but low nutrients, both C:N
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and C:P ratios will chang[12]. The elemental composition in phytoplankton is regulated by ionic
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equilibrium, while N and P of zooplankton are stored in the form of amino acids, proteins, and
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other organic matters[8]. Zooplankton maintain relatively strict homeostasis in stoichiometry
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compared with phytoplankton[13-14], i.e. the composition of elements keeps nearly fixed[9, 11].
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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].
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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
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zooplankton[9]. In essence, it is the difference in homeostasis of phytoplankton that result in P
limitation and excess C in zooplankton.
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2．Nutritional imbalances in food supplies
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In addition to the difference of homeostasis between zooplankton and phytoplankton, P
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limitation and excess C in zooplankton is resulted from nutritionally imbalanced food supplies.
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C:P ratio is commonly high in phytoplankton because of deficient nutrients, while the C:P ratio is
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relatively low in zooplankton with a rather fixed elemental composition[17]. Thus, in terms of
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zooplankton, P limitation and excess C resulted from nutrient-imbalanced food supplies has
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become more meaningful (Fig. 2).
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Fig. 2 The C: P ratios was higher in phytoplankton with lower P content relative to zooplankton[18].
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The primary problem which the grazers faced with is the difference between food supplies
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and somatic demands[5, 9]. Daphnia magna requires more P than foods provide[19]. Zooplankton
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tend to be limited by P because of high P demands and strong homeostasis[20]. P is the essential
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element for RNA[12]. Thus, the synthesis of ribosomes and protein synthesis can be affected by P
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limitation
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growth of zooplankton is limited[21] (Fig. 3). Hence, somatic growth rate will decrease when
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consumers are faced with P-deficient food[22]. For example, the growth of Daphnia and rotifers is
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limited by P content[19, 23]. As a potential limiting factor in zooplankton growth, P limitation is
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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
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Ecological stoichiometric theory considers Threshold Elemental Ratio (TER) as the standard
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in judging whether nutrients are limited[17, 25]. The element X is regarded to limit the consumers if
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the ratio of C to nutrient element X (i.e. C:X ratio) is larger than the TER, otherwise they are
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limited by C. Taking C:P ratio for example, two approaches are commonly used to estimate TERs
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of phytoplankton: (1) Determined by the growth rate and egg production responses of zooplankton
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along a gradient of C:P food or different dietary P additions and (2) calculations can be undertaken
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based on stoichiometric theory in which elemental ratios and utilized efficiency are taken into
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account[26]. For example, if a zooplankter with C:P in biomass of 75 (by atoms) utilized C and P in
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food with maximum efficiencies of 50% and 100%, respectively, then the TER is 75×100/50=150.
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In Daphnia, the range from 3–7 mg atomic P [mg atomic C]-1 (atomic ratio C:P =150–300) have
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been proposed as thresholds for the onset of P limitation[27]. In actually, however, C:P ratio often
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exceeds 230 in phytoplankton[26].
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The somatic growth rate of zooplankton will decrease when P is limited
[24, 28]
and
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zooplankton are not able to utilize C fully in phytoplankton for secondary production[19, 21]. Then,
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when the P content in phytoplankton decreases to a very low level, zooplankton contenting more P
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suffers negative population growth regardless of algal biomass[28]. The transfer efficiency of C is
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determined by assimilation efficiency of trophic levels[21], so excess C will return into the
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environment with the deficiency of P [12].
3．P limitation and excess C
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Liebig minimum principle——the core section of ecological stoichiometry——suggest that
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other elements be in excess when there is one limiting nutrient element[12]. Therefore there exist
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two inevitable related problems, deficiency and excess of elements, when organisms with strict
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homeostasis encounter mismatches between their own demands and dietary supplies. P limitation
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tends to occur[12] because P content in phytoplankton is low while the demand for P of
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zooplankton is high[17, 23]. With the rather tight homeostatic control in zooplankton, the C-use must
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balance the P-use[28]. Thus, in addition to P limitation in zooplankton[17, 23], excess C occurs at the
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same time[12, 14].
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Fig. 3 The higher C: P ratios and lower P content of phytoplankton could potentially limit
zooplankton growth[12].
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The preconditions of P limitation and excess C in zooplankton are: (1) P deficiency in food
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supplies of phytoplankton and (2) high P demands of zooplankton with strict homeostasis. C is in
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excess when C:P of food supplies exceeds TER[9]. With increasing of the C:P ratio in
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phytoplankton, the growth rate of zooplankton declines, P becomes the limiting factor and C must
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be disposed of and transform into waste[12, 20]. The deficient elements and excess elements will
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changeover in certain conditions, i.e. when limited by C or N in zooplankton, P could be in
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excess[12].
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Though zooplankton use lipids as a source storing C, lipids account for a relatively small
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fraction of body mass[17]. Thus, the growth of zooplankton is a process to concentrate deficient
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elements and dispose of excess compounds[29]. For accomplishing this process, zooplankton must
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take some measures, and pre- or post-assimilatory regulations in the gut are two main
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approaches[17].
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4．Disposal of the excess C
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Consumers dispose excess elements
[30]and
assimilate limiting elements efficiently[12, 17] in
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order to maintain homeostasis. As for organisms with strict homeostasis, concentrating deficient
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elements and disposing off excess compounds complement with each other. Under the condition
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of P limitation, intaking of P is comparatively increasing with higher consumption of C in
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zooplankton[15]. To cope with P limitation, zooplankton will increase sequestration of P, or dispose
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of excess C or do both[14].
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When faced with P limitation, zooplankton will sort to different strategies in homeostatic
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regulation[23, 31] basing on elemental composition and food supplies[11]. With the increase of C:P
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ratio in phytoplankton, both the release of P and assimilation of C in zooplankton will decrease[14,
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19]
. Feeding on food with high C:P ratio, the respiratory rate and the release of dissolved organic
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carbon (DOC) in Daphnia increase[19]. The excretion of particles in zooplankton may be the main
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approach to disposing of the ‘leftover C’[11, 17].
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Three important links to maintain homeostasis in zooplankton are: (1) food selectivity, (2)
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regulation of assimilation efficiencies, and (3) disposal of the excess elements[23, 32]. Zooplankton
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also use lipids to store C but account for a relatively small fraction[17]. Regulating through changed
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food selectivity is a pre-feeding method. Food supplies in the environment for Zooplankton vary
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frequently[17]. The food zooplankton preying on range in broad particle sizes, and zooplankton are
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unable to reject poor-quality particles individually[17]. Thus Pre- and post-assimilatory regulations
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in the gut are bound to the main approaches to maintaining homeostasis in zooplankton.
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4.1 Pre-assimilatory regulation
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Zooplankton are able to change the assimilation efficiency of C[14, 26]. The C assimilation
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efficiency will change when zooplankton experience different nutritional conditions[17] (Fig. 4).
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The C assimilation efficiency decreases by 30% in Daphnia magna when the C:P ratio in
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phytoplankton increase from 80 to 164[19]. The regulation of C assimilation efficiency has nothing
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to do with the metabolic machinery, and production of certain enzymes (like lipases and
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carbohydrases) could be relaxed[12]. The benefit of pre-assimilatory regulation, in conclusion, is
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that the metabolic cost would be reduced when zooplankton experience changing food supplies[26].
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Fig. 4 The C assimilation efficiency of zooplankton under different food C: P[19].
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Gut residence time may be the reason why P assimilation efficiency of zooplankton actually
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decreases, while the C:P ratio in food increase[12]. Because of the short gut residence time of
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high-C:P food, P may be disposed of without being fully absorbed[33]. This accounts for the reason
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why zooplankton dispose of P in spite of P limitation[33-34]. The absolute non-release of P is
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impossible[12], so improving P assimilation efficiency works little for maintaining homeostasis.
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Therefore, the main part of pre-assimilatory regulation in zooplankton should be the way of
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changing C assimilation efficiency.
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4.2 Post-assimilatory regulation
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Elemental Components identification and following adjustments can be done only after food
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is assimilated by grazers[12]. The absorption of macromolecules is variable, which accurately
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monitors compounds hydrolyzed into their constituents, such as monosaccharides and amino
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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]
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increasing respiration and release of organic C compounds[14].
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Release of organic C compounds through zooplankton[12, 23] originates from three different
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sources: (1) feeding losses, (2) faecal particles, and (3) extracellular secretion[19]. Elements losses
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are related to the components in original food without exception and can not be regulated. C
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release from faeces is linked to the assimilation when transferring in the gut. For pre-assimilatory
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regulation, if less C is assimilated from food during transfer in the gut, more C will potentially be
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lost via faeces[19]. While post-assimilatory regulation is mainly based on the secretion of organic
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matters[17]. Daphnia magna, for example, the secretion of DOC increase by 1 time when fed with
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high C:P ratio food[19, 23] (Fig. 5).
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Fig. 5 Under P deficiency, excess C could be coped by zooplankton extracellular release DOC[19].
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Respired as CO2 can also be a way of releasing excess C in post-assimilatory regulation[14, 19].
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Appendage beat rate and heartbeat rate are increased under P-deficient diets[12], indicating that
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zooplankton increase respiration by both behavioral and physiological mechanisms[33]. Disposal
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by respiration involves biochemical oxidation that could produce energy, implying metabolic
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advantages[23], but also cellular disadvantages such as the production of free radicals[12]. However,
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respiration has been controversial when it comes to disposal of excess C. Because this
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growth-related cost constitutes a significant portion of the total respiratory cost, decreased growth
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rate should be associated with decreased total respiration[14]. Because reduced respiration due to
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reduced growth rate could counteract an elevated release of excess C，respiration will not increase
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significantly[14]. Although increased respiration could be a transient phenomenon in response to
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P-deficient diets[23], it could be more important to release organic C compounds[14]. For example,
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Brachionus calyciflorus release excess C mainly by extracellular secretion or excreting as faecal
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material[14, 23].
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The excess C, released from zooplankton in organic form,is helpful to heterotrophic processes
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in ecosystems, while somatic growth gets benefit if disposed in the form of CO2. The ecological
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effects of those two processes are entirely different[12]. In terms of energy flow and material
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cycling, the reduced C assimilatory efficiency will effect the C transfer efficiency in food web and
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sequestration in aquatic ecosystems[9, 14].
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5．Ecological effects of excess C regulation
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C transfer efficiency is determined by the supplies and demands of limiting elements across
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trophic levels[9, 21]. The absolute and the relative availability of limiting elements determines C
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transfer efficiency[14]. Phytoplankton usually concentrate excess C and thereby reduce P content
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relatively[12], and this process will have an adverse effect on secondary production of ecosystem[5].
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The disposals of excess C taken by zooplankton[25], not only reducing C transfer efficiency but
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also detaining more C in the environment[9, 14], influence the fate or sequestration of C[17, 23] (Fig.
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6). Therefore, the system would enter a stage with high biomass of C-excess phytoplankton which
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do not support zooplankton growth[28].
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Fig. 6 To maintain homeostasis, released excess C by zooplankton reduced C transfer efficiency[9].
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Organisms must obey stoichiometric rules, which constrain the production, intake, transfer,
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and storage of nutrients in food web[9]. In order to maintain homeostasis, grazers dispose excess
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substances and improve the relative content of limiting elements. Limiting elements（e.g. P）are
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expected to be transferred in food chains with high efficiency, while excess elements（e.g. C）
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could be recycled into the environment[9]. Palatable phytoplankton (Low C:P) subject to high
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turnover rates, a high share of production is utilized, rather than being excluded from the food
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web[12]. Therefore, as the major driver for material transfer, the regulation of excess C in
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phytoplankton ensures nutrients be supplied and stabilization in the ecosystem[14].
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The homeostatic regulation of zooplankton results in more C accumulating in the environment.
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In an evolutionary context, one should expect strong selective pressure towards utilization of this
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excess C[9]. The substances released from disposals of excess C, could be a potential source for
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bacterial production[17, 23], and enhance the functions of bacteria in C cycling[12, 14]. Furthermore,
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vertical flux of C will increase because of the production of feces from regulation of excess C
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and thereby more C will be sequestered in detritus[9]. If the disposal of excess C generates CO2,
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planktonic microbial loop will get benefit [19]. In conclusion, regulation of excess C in zooplankton
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generates several kinds of metabolites, then affects the global material cycling, and has
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far-reaching implications for marine and global C sequestration[19].
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[23]
6．Future work
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Hence, the composition of zooplankton community and stoichiometric quality are the major
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subjects of planktonic ecosystem trophodynamics[23]. Facing an excess of C is an inevitable
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response for zooplankton to stress and rapidly changing environment. The coastal area, one of the
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most significant ecosystems, is affected heavily by industrial activities. Recent years,
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eutrophication has become the main problem in coastal ecosystem[35]. According to ecological
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stoichiometry, the content in phytoplankton will enhance with the increasing input of P in aquatic
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ecosystem[33], thereby the condition of P limitation in zooplankton will be relieved and the
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assimilation and transfer efficiency of C will be improved [26]. In actually, however, phytoplankton
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will be at a high risk if P content is increased. If the P content in phytoplankton is comparatively
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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
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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
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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.
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