Animals can elicit strong, direct effects on nutrient dynamics in aquatic ecosystems by releasing nutrient wastes back into their environments, forming feedbacks on nutrient availability and shaping ecosystem processes [1
]. Since freshwater ecosystems are often limited by phosphorus (P) and nitrogen (N), rates and ratios of animal nutrient release can be important in determining ecological structure and function [3
]. Within freshwaters, many studies have quantified roles of animal excretion of dissolved inorganic N (DIN) as ammonium and dissolved inorganic P (DIP) as phosphate, showing direct connections to algal community composition, algal N versus P limitation, and basal resource N and P contents [5
]. Still other studies have shown a direct contribution of DIN and DIP excretion to food web compartments within riverine ecosystems [7
], and ecosystem-level N and P dynamics [8
]. Despite substantial taxonomic, temporal, and spatial variability that merit further study [10
], excretion represents a clear pathway for animal community dynamics and evolutionary processes to affect ecosystem processes in many aquatic settings.
Although excretion of DIN and DIP is the best-studied component of consumer-driven nutrient dynamics, animals can also affect nutrient cycling by the production of particulate nutrient wastes such as egesta, exuvia, and carcasses [2
]. These primarily organic wastes are less-studied due to a lack of standard quantitative methods, as well as comparatively low bioavailability of organic relative to inorganic N and P, which is assumed to equate to reduced ecological significance (e.g., [12
]). However, animal particulate wastes can be highly bioavailable, nutrient-rich, and highly diverse produced via processes including egestion [13
] and mortality [14
]. For example, rates of animal N and P egestion can equal or exceed rates of DIN and DIP excretion among the few taxa among which the two fluxes have been directly compared [15
]. Decomposing animal carcasses, too, can supply limiting N and P and elicit enduring effects on recipient ecosystems [17
]. Many animal particulate wastes are available to microbial heterotrophs and are thus an important nexus between “green” autotrophic and “brown” heterotrophic food webs [19
]. Further study of the comparative importance of dissolved versus particulate nutrient wastes will provide a broader understanding of the role of animals in freshwater ecosystems.
Animal egestion contrasts with animal excretion, because the former represents materials which are ingested but not digested/assimilated whereas the latter represents materials which are assimilated but not retained for long-term growth or storage. Given this, relative nutrient fluxes of egesta versus excreta from animals may vary with trophic mode (e.g., herbivore versus predator), body size, and taxonomic identity. Specifically, organisms that face high consumer-resource elemental imbalances (e.g., exhibit high nutrient demands or feed on low-nutrient foods) may release nutrients at lower rates [20
], but may also release nutrients primarily via egestion, because they are growth- and assimilation-limited, whereas organisms facing lower imbalances may primarily excrete excess nutrients through post-assimilatory regulation [2
]. Still, animals may partly reduce the effects of imbalances through flexible changes in the gut [23
]. To adapt or acclimate to highly imbalanced diets, for example, some animals develop longer digestive tracts, as illustrated by comparisons of herbivorous versus carnivorous fish [24
], and among tadpoles reared on low- versus high-N diets [25
]. When facing high elemental imbalances, animals may also meet energetic and nutritional needs by increasing feeding rates (compensatory feeding; [26
]) which combined with low assimilation efficiencies, may result in greater egestion relative to excretion rates [28
]. Despite the potential roles of food nutrient content and trophic mode in nutrient release, recent syntheses suggest that excretion rates are only weakly related to trophic imbalances and are best predicted by body size and, to some degree, taxonomy [29
]. Comparative fluxes of nutrient egestion versus excretion may similarly vary across animals, but to date, no study has examined both fluxes across a diversity of animal taxa ranging in body size and trophic modes.
Here, we conducted a literature survey and meta-analysis of existing studies directly measuring N, P, and N:P egestion and excretion by 47 freshwater animal species. We used our synthesis to directly compare egestion and excretion and test the following predictions: (1) Egestion rates will approximately equal excretion rates across animal taxa, as found in previous comparisons among select taxa [16
]; (2) given the importance of both factors for predicting excretion rates, ratios of nutrient release as egestion, relative to excretion, will be best-predicted by a combination of both body size and taxonomic identity [29
]; and (3) because egestion is more sensitive to individual-level variation in feeding time and behavior, variance of N and P egestion rates and N:P ratios will be greater than variance of excretion rates and ratios across all taxa.
We found that across multiple freshwater animal species, particulate N and P fluxes in the form of egesta exceed DIN and DIP excretion fluxes. Due to a general lack of data, it is commonly assumed that excretion is the dominant nutrient release flux by aquatic animals. Indeed, many studies have empirically shown excretion to be important at ecosystem levels [7
]. However, recent empirical studies also indicate egestion and excretion rates are approximately equal among many taxa, suggesting that egestion may be an important overlooked pathway of nutrient cycling in aquatic settings [15
]. Drawn from a wide array of predominately primary consumer taxa, our results show that egestion is a major flux measured from animals in freshwater settings. Among a smaller number of datasets measuring TN or TP excretion, we also show that total nutrient egestion rates are similar to total excretion rates, affirming dissolved organic N and P excretion as an important release flux across freshwater animals [61
]. Furthermore, our synthesis shows that the variance of N egestion exceeds variance of DIN excretion rates, and we reveal major roles of body size and phylogeny in both relative rates and variance of P egestion compared to DIP excretion. Given this quantitative evidence of egestion as an important and dynamic animal-mediated nutrient flux, our study affirms the need for additional studies of animal egestion in a context additional to animal excretion of dissolved nutrients in aquatic ecosystems [2
While the contributions of egesta to ecosystem nutrient fluxes remain poorly studied in comparison to excretion, it is generally assumed that egesta are not as important, as egesta are often considered low-N and P, recalcitrant, and not as bioavailable as dissolved excreta [2
]. We show that, among species which have been measured for rates of both egestion and inorganic nutrient excretion, egestion rates often exceed excretion rates. At the physiological level, the quantitative importance of egestion reflects several patterns. First, many organisms are likely unable to completely digest and assimilate ingested N and P, owing to the inefficiency of digestive enzymes and uptake pathways within the gut, combined with selective investment in uptake of limiting nutrients, which can cause non-limiting nutrients to be egested instead of assimilated [23
]. Second, many organisms may have evolved to undergo faster (e.g., compensatory) feeding instead of maximizing assimilation efficiency, causing the majority of ingested nutrients to pass through the gut [26
]. Finally, all of the animals included in our study were primary herbivores or detritivores with the datasets not including any higher-level consumers. Among carnivores, egestion rates may be lower than excretion rates due to greater assimilation efficiency of nutrient-rich animal tissues [63
], but N:P ratios of egestion may be lower than N:P of excretion among some carnivores because P-rich bone is difficult to assimilate.
At the ecosystem level, our results also establish that egestion may be equally or more important than excretion within the nutrient budgets of aquatic ecosystems—yet, the two pathways of nutrient release may exhibit contrasting ecological implications. Broadly, DIN and DIP in excreta should be more bioavailable than N or P in egesta, because the latter is mostly organic and requires breakdown by heterotrophs [12
]. However, this contrast may depend on the proportions of egested N and P that are inorganic versus organic, which may depend on trophic level and remains poorly understood. Previous work suggests that egesta can accrue in depositional zones and may act as sinks rather than sources of dissolved inorganic nutrients, serving as long-term stores of organic nutrients [13
]. These differing effects of excretion versus egestion are key to understanding benthic-pelagic coupling, such as the role of sessile filter-feeders in spurring sediment biogeochemical processes [48
]. However, Halvorson et al. (2017) [13
] noted that whether egesta became a sink for inorganic nutrients, and whether egested nutrients are mineralized, varies as a result of the taxonomic identity of the source animal. Further, few studies have considered egesta as a potential resource for microbes or other animals [67
]. Our study calls for further study of the diverse fates of animal egesta in aquatic ecosystems, to better link animal physiological processes with ecosystem functions such as nutrient cycling and the interaction between autotrophic versus heterotrophic ecosystem processes [19
As shown in previous work on excretion rates across broad sets of freshwater taxa and marine invertebrates and fish [29
], our study shows that body size and taxonomic identity play a role in determining nutrient fluxes by animals. In particular, P egesta fluxes relative to excreta were best predicted by both taxonomy and body size, exhibiting greater release ratios and relative variance among small-bodied taxa. The negative effect of body size on release ratios suggests that P excretion and egestion rates may scale differently with body size—generally, smaller-bodied species exhibit proportionally greater P egestion compared to larger-bodied species. These patterns may reflect contrasting scaling of gut length versus metabolic rates with increasing body size [69
]. For example, small-bodied taxa may exhibit greater post-assimilatory demands of P to support faster growth of P-rich tissues, thus reducing P excretion rates [70
]. Alternatively, body size effects may reflect trophic differences between small taxa that maximize feeding rates at the expense of assimilation, versus larger taxa that have evolved to enhance assimilation efficiencies, e.g., by increasing gut length [24
]. While both egestion and excretion release scale approximately similarly with body size when all taxa are pooled together (Figure S1
), body size effects in our analysis are significant after accounting for different random intercepts fit to each taxonomic family, because our models treated taxonomic family as a random effect.
We further observed phylogenetic differences wherein Mollusca exhibit greater rates of P egestion, relative to DIP excretion, compared to Chordata and especially compared to Arthropoda. At a methodological level, the Mollusca datasets may have resulted in proportionally greater P egestion due to the inclusion of both pseudofeces and biodeposits in egestion measures from Bivalves. Molluscan pseudofeces represent material filtered but subsequently expelled in mucus, before true ingestion, and thus do not represent truly egested material but contain measurable amounts of N and P [42
]. However, the lack of phylum differences with respect to N or N:P release suggest additional phylogenetic drivers specific to P release, perhaps tied to phylum differences in body size, diet, or growth rates that are coupled to organism P demands, but not to N or N:P demands [70
]. Still, our study suggests a minimal role of diet, because elemental imbalances were not related to release ratios across taxa for which we were able to calculate imbalances.
Our meta-analysis further tested the prediction that egestion rates and ratios would be more variable than excretion rates and ratios across all animal species. We found that release relative variances were most often positive, supporting our prediction and indicating greater within-population variability of egestion compared to excretion. This suggests that, within species or study populations, excretion may be a relatively more uniform pathway of nutrient release compared to egestion. Greater variation of egestion may reflect higher temporal variation and individual-level differences in consumption rates and assimilation efficiency, body size, and feeding mode that are diminished post-assimilation due to homeostatic regulation which is comparatively uniform and temporally stable across individuals. While intra-specific and -population variation of stoichiometric traits remain understudied compared to inter-specific variation [74
], greater individual-level variation of egestion may promote comparatively greater spatial and temporal heterogeneity of community and ecosystem processes affected by egestion [77
]. At a methodological level, studies should investigate why egestion rates exhibit high variation, because some degree of variation may be due to a lack of standard methods for measuring egestion rates across taxa, in comparison to excretion for which methods are well-developed and standardized [78
]. Interestingly, we found no difference in variation of egestion versus excretion N:P ratios, suggesting that methodological constraints and/or inter-individual variation may affect the rate but not the stoichiometry of release. Indeed, our study shows that variation of P egestion rates is greater among smaller-bodied taxa and among Mollusca compared to Arthropoda, which may reflect either the greater proportion of these datasets derived from the field compared to the laboratory (Table 1
), or greater temporal and individual variation in feeding and assimilation processes among small-bodied individuals and Molluscs.
Our study provides the first systematic comparison of egestion and excretion rates and ratios across a diversity of animal taxa and, as such, provides several directions for future research in consumer-driven nutrient dynamics. First, our literature survey revealed many studies reporting excretion data, but was limited by a lack of paired egestion data from many taxa. This limitation will only be addressed by methods development and measures of egestion simultaneous to excretion, with field-collected data needed wherever methods allow [30
]. Future studies must also broaden the diversity of taxa considered to major taxonomic groups that remain poorly represented within our dataset—large-bodied Chordates including reptiles, mammals, and fish, many Arthropod groups (crayfish, stoneflies, beetles, mayflies), Mollusca (snails), and Annelids need better representation. Our study did not include some existing data from fish drawn from aquaculture studies. Finally, the quantitative importance of egestion compared to excretion highlights the need for further ecosystem-level studies of the ecological roles of egestion. These roles are poorly understood and merit continued study of transport/deposition processes, food web significance, and nutrient turnover [13
]. Studies of egestion will increase scientific understanding of animals’ diverse roles in ecosystems, expanding from a historic emphasis on dissolved nutrients to particulate wastes that are linked with animal phylogeny, body size, and other traits and are potentially important within many ecosystem processes [2