Exploring how prey types and seasonality affected the deposition of elements by Carolina wolf spiders, we found significant differences in concentrations of a variety of elements between excreta, prey remains, and whole prey carcasses. Spiders appeared to preferentially assimilate certain elements (Ca, Cd, Cu, Fe, Mg, Mn, Mo, Na, and Zn) while other elements appeared to be either weakly assimilated, not regulated, or preferentially excreted (Al, B, Ba, K, P, S, Si, Sr, and V) (Fig. 4). There were also three elements where prey species affected differences in elemental concentrations between excreta and whole prey (Cr, Li, and Ni). Additionally, while excreta elemental concentrations displayed little variation, remains and whole prey varied significantly across prey species (Fig. 4). There were also seasonal effects, such that spiders collected in the spring produced excreta with higher concentrations of trace elements than spiders from the fall (Figs. 6 & 8). These results highlight the complex interactions between predator physiology and prey composition that determine the elemental content of nutrients deposited in forms that are more labile (i.e., excreta) versus recalcitrant (i.e., prey remains) following predation.
It has been previously demonstrated that there are differences in C and N content among insect taxa (Fagan et al. 2002, Woods et al. 2004, Wilder et al. 2013, & Reeves et al. 2021). For whole prey, prey remains, and excreta, there were differences among species in the concentrations of C and N regardless of season (Fig. 1, 2, 3, and 4). This is likely due to life history strategies, dietary requirements, and physiology differing among prey groups (caterpillars, cockroaches, crickets, and flies). For instance, caterpillars are holometabolous insects, which feed on C-rich plant tissue during their larval stage and require high energy stores, which are high in C, to fuel metamorphosis. Alternatively, crickets are hemimetabolous, and feed on food sources that consist of higher concentrations of N (e.g., dog food that was provided ad libitum) (Fagan et al. 2002, Wilder et al. 2013, González et al. 2020, Reeves et al. 2021). Additionally, cockroaches can store excess N as uric acid in their bodies, which can result in higher N% compared to other prey (Sabree et al. 2009). Phylogeny, ecology, and life history traits could be important factors explaining the differences in C and N concentrations that were observed between whole prey (Lease & Wolf 2010, Wilder 2018, Barnes et al 2019). Although further work is needed to determine how and why prey species vary in these macro-elements (C and N).
Compared to C and N, much less is known about consumer-driven nutrient cycling of other elements, especially trace elements (e.g., Na, Zn, Ca, etc.), which could have different effects on ecosystems (Clay et al. 2017, Welti et al. 2019, & Kaspari 2021). For instance, there were differences among species in the concentrations of trace elements in prey remains (e.g., Na, Zn, Ca, etc.), regardless of season (Fig. 4, 6, and 8). Prey remains are nearly all exoskeleton which are largely indigestible to predators, including spiders (Foelix 1996 & Barnes et al. 2019). Between insect taxa there are differing degrees and types of exoskeletons (i.e., soft and flexible vs. hard and protective) which may require different combinations of elements (including trace elements) or chemicals to achieve these properties (Gallant and Hochbert 2017). This may directly affect the amount and types of nutrients in the prey body that are not available to predators (e.g., beetles have greater proportions of indigestible exoskeleton to body mass than caterpillars) (Reeves et al. 2021). For instance, cricket and caterpillar remains had higher concentrations of sodium, a biologically important element, in their undigested prey remains (Fig. 4) (Clay et al. 2017 & Welti et al. 2019). Therefore, not only is there variation in elemental concentration of different insect taxa, but there are also differences among species in how much of the nutrients are locked in the chitinous matrix of the exoskeleton and inaccessible to predators (Reeves et al. 2021). This poses a challenge to studying insectivore nutrition as measures of whole arthropods will not identify how much of the nutrients are digestible versus indigestible by the consumer. While indigestible to spiders and many other consumers, discarded prey remains still contain valuable nutrients (e.g., Na, K, etc.) and may affect ecosystem function (i.e., nutrient availability to primary producers) (Bump et al. 2009 & Kaspari 2021). Although, it may take years for these nutrients in the exoskeleton to be released (Seastedt and Tate 1981) and hence, the short-term effects of prey remains on ecosystem processes remain unclear.
Unlike prey remains, spider excreta had relatively little overall trace elemental variation between prey groups (Fig. 4). Additionally, some elements were preferentially assimilated (i.e., concentrations in excreta were similar to or lower than that in whole prey) by Hogna carolinensis (Ca, Cd, Cu, Fe, Mg, Mn, Mo, Na, and Zn), while others were largely excreted (i.e., concentrations in excreta were significantly higher than that in whole prey: Al, B, Ba, K, P, S, Si, Sr, and V) (See Supplementary Figures). Assimilated elements likely serve a vital function for the organism. For instance, proteins containing copper facilitate oxygen transport in the hemolymph of some arthropod species like spiders, while zinc-metalloproteases assist with the extraction of nutrients during extra-oral digestion (Rhem et al. 2012 & Walter et al. 2019). Overall, the consequences of trace elements on predator biology and ecosystem function (i.e., microbial communities, plant communities, etc.) are not clear and deserve further study (Kaspari 2021 & Welti & Kaspari 2021).
For whole prey, trace elemental concentrations were more variable among species than excreta, but less than prey remains (Fig. 4). As with whole prey N and C concentrations, variation in whole prey trace elemental concentrations likely resulted from differences in life history strategies, dietary requirements, and physiology differing among prey groups (Fagan et al. 2002, Woods et al. 2004, Wilder et al. 2013, & Reeves et al. 2021). For instance, caterpillars (the only larval prey used) differed most from other whole prey (crickets, cockroaches, and flies) (Fig. 4). While previous work has focused primarily on C, N, and P content of select insect taxa, fewer studies have examined trace elemental composition of whole prey species from diverse insect taxa (Woods et al. 2004 & Bertram et al. 2008) Thus, in order to accurately predict the quantity and composition of nutrients deposited following predation, further studies should explore the elemental composition of diverse prey taxa, as other taxa (e.g., Coleoptera, Hemiptera, Hymenoptera, etc.) could have different concentrations of trace elements.
There were differences in trace elemental concentrations between fall and spring excreta of spiders (Figs. 6 & 8). In the fall Hogna carolinesis excreted greater concentrations of Fe, Mg, Mn, Mo, S, & V, while in the spring spiders excreted higher concentrations of Al, B, Ba, Ca, Cd, Cu, K, P, Na, Si, Sr, and Zn. These differences may be due to seasonal changes in the diet requirements of adult female Hogna carolinesis. As winter approaches, the assimilation of certain micronutrients could be key to the spider’s survival as it prepares for diapause (e.g., Cu, Na, Zn, etc.) (See Supplementary Figures). For example, previous work showed that female spiders that consumed supplemental dietary amino acids, produced offspring that survived overwintering conditions longer (Wilder & Schneider 2017). In addition, some potential explanations for different concentrations of trace elements from excreta in the spring versus fall could be: 1) Nutrients assimilated in the fall may not be important in spring, when the focus of the organism shifts back towards reproduction. 2) Intake of high concentrations of some nutrients may have negative effects on an organisms’ fitness in some seasons more than others (Elser et al. 2016 & Zouh & Declerck 2019). 3) Prey may vary seasonally in nutrient content (e.g., data on whole cockroaches; Fig. 1) (Ng et al. 2018). However, there is little information available in the literature for seasonal nutrient requirements for arthropod predators, especially for a wide range of elements as included in the present study. Further studies will be needed to disentangle the seasonal effects that were observed and subsequent implications that could occur for ecosystem function.
Predator mediated nutrient deposition is important for ecosystem structure and function (Schmitz et al. 2010). Here, we demonstrated that predators produce relatively similar excreta but different prey remains when feeding on different prey species (Fig. 4). Furthermore, we showed that predators (in this case, Hogna carolinensis) appeared to preferentially assimilate (Ca, Cd, Cu, Fe, Mg, Mn, Mo, Na, and Zn), or excrete (Al, B, Ba, K, P, S, Si, Sr, and V) certain elements (See Supplementary Figures). These factors can have important implications for ecosystem function as nutrient inputs or shortfalls can have cascading effects on ecosystems and some of these trace elements could be important cofactors for enzymes that catalyze a variety of biochemical reactions (Kaspari 2021). Additionally, since nutrient deposition is dependent on prey type, different predator-prey interactions could have various consequences for ecosystems. For instance, different habits (e.g., distance from a river, fields, deserts) can have different communities of prey, influencing the type (e.g., Na, Mg, Zn, etc.) and amount of nutrients deposited by predators (Schmitz et al. 2010). Moreover, spatial and temporal variations in prey or predator populations could have large implications for ecosystem structure and function, especially if predators affect the deposition of nutrients important for soil communities and primary producers. Further studies investigating other predator-prey interactions and the nutrient feedbacks associated with those interactions will provide a more mechanistic understanding of how predators regulate the flow of nutrients through ecosystems and the consequences of spatial and temporal variation in potential prey communities for ecosystem function.