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ECOGRAPHY
Ecography
–––––––––––––––––––––––––––––––––––––––– © 2019 The Authors. Ecography © 2019 Nordic Society Oikos Subject Editor: Anna Eklöf
Editor-in-Chief: Miguel Araújo Accepted 16 May 2019
42: 1579–1586, 2019
doi: 10.1111/ecog.04307doi: 10.1111/ecog.04307 42 1579–1586
The energetic demand of consumers increases with body size and temperature. This implies that energetic constraints may limit the trophic position of larger consumers, which is expected to be lower in tropical than in temperate regions to compensate for energy limitation. Using a global dataset of 3635 marine and freshwater ray-finned fish species, we addressed if and how climate affects the fish body size–trophic position relationship in both freshwater and marine ecosystems, while controlling for the effects of taxonomic affiliation. We observed significant fish body size–trophic position rela-tionships for different ecosystems. However, only in freshwater systems larger tropical fish presented a significantly lower trophic position than their temperate counterparts. Climate did not affect the fish body size–trophic position relationship in marine sys-tems. Our results suggest that larger tropical freshwater fish may compensate for higher energetic constraints feeding at lower trophic positions, compared to their temperate counterparts of similar body size. The lower latitudinal temperature range in marine ecosystems and/or their larger ecosystem size may attenuate and/or compensate for the energy limitation of larger marine fish. Based on our results, temperature may determine macroecological patterns of aquatic food webs, but its effect is contingent on ecosystem type. We suggest that freshwater ecosystems may be more sensitive to warming-induced alterations in food web topology and food chain length than marine ecosystems. Keywords: Actinopterygii, energy limitation, food web, global warming, metabolic theory
Introduction
Body size plays a major role in structuring consumer–resource interactions. The idea that trophic interactions are size-structured is widely assumed in many food-web models (Loeuille and Loreau 2005, Petchey et al. 2008, de Roos and Persson 2013) and well supported by empirical data (Cohen et al. 1993, 2003, Brose et al. 2006).
Climate effects on fish body size–trophic position relationship
depend on ecosystem type
Danyhelton D. F. Dantas, Adriano Caliman, Rafael D. Guariento, Ronaldo Angelini, Luciana S. Carneiro, Sergio M. Q. Lima, Pablo A. Martinez and José L. Attayde
D. D. F. Dantas (https://orcid.org/0000-0001-9400-4843), A. Caliman, L. S. Carneiro and J. L. Attayde (https://orcid.org/0000-0002-8372-4172)
✉ ([email protected]), Dept of Ecology, Federal Univ. of Rio Grande do Norte, Natal, RN 59078-970 Natal, Brazil. DDFD also at: Natl Res. Center of
Amazonic Biodiversity (CEPAM), Manaus, AM, Brazil. – R. D. Guariento, Laboratory of Ecology, Federal Univ. of Mato Grosso do Sul, Campo Grande, MS, Brazil. – R. Angelini, Dept of Civil Engineering, Federal Univ. of Rio Grande do Norte, Natal, RN, Brazil. – S. M. Q. Lima, Dept of Botany and Zoology, Federal Univ. of Rio Grande do Norte, Natal, RN, Brazil. – P. A. Martinez (https://orcid.org/0000-0002-5583-3179), PIBi Lab – Laboratorio de Pesquisas Integrativas em Biodiversidade, Dept of Biology, Federal Univ. of Sergipe, São Cristóvão, SE, Brazil.
The size-related constraints on prey consumption (i.e. gape limitation) impose a mechanical limit to the trophic posi-tion of consumers, resulting in a positive correlaposi-tion between trophic position and predator size (Jennings et al. 2001, Arim et al. 2007, 2016, Dalponti et al. 2018). However, the increase in energy demand with body size and the reduced availability of energy at higher trophic positions may impose an energetic constraint to food chain length and may pro-mote a negative correlation between trophic position and body size (Burness et al. 2001, Arim et al. 2007, 2016). When combined across a large range in body size variation, these opposing trends can generate a humped relationship between trophic position and body size (Arim et al. 2007, 2016, Segura et al. 2015).
Whole organism metabolic rate scales with the 3/4 power of body mass and increases exponentially with temperature (Gillooly et al. 2001, Brown et al. 2004), until enzymes start to denature. The quarter-power scaling of whole organism metabolic rate with body mass is caused by the fractal-like design of exchange surfaces and distribution networks, while temperature governs metabolism through its effects on rates of biochemical reactions (Gillooly et al. 2001, Brown et al. 2004). Thus, larger individuals in tropical regions, when compared to temperate ones, have higher absolute energetic demands and may be more limited by the amount of energy available. This implies that energetic constraints may limit the trophic position of larger consumers in the tropics, at least in the absence of another ecological mechanism (e.g. higher prey diversity) compensating for energy limitation (Arim et al. 2007, 2010) or other limiting factors (e.g. distur-bance frequency, Post 2002).
The expected increase in an individual’s absolute ener-getic demand, with increasing body size and temperature (Gillooly et al. 2001, Brown et al. 2004), requires an increase in the individual’s energy consumption (Arim et al. 2007, 2010). Recent investigations have shown that the rela-tive demand for carbon (respiration) versus other nutrients increases with temperature (Cross et al. 2015). This may imply that larger consumers in tropical regions are required to feed more directly on plant, algae or detritus than their temperate counterparts, a prediction which agrees with the fact that digestion of plant tissue is easier at higher tem-peratures (Floeter et al. 2005). On the other hand, lower temperatures change diet preferences and increase the need for other nutrients relative to carbon, therefore increasing the need for animal food sources (Boersma et al. 2016, González-Bergonzoni et al. 2016, Moody et al. 2019). Therefore, the expected temperature sensitivity to food quality limitation might increase the incidence of herbivory/omnivory in larger consumers in the tropics, affecting the trophic position–body size relationship.
A clear latitudinal gradient exists with respect to the preva-lence of herbivory/omnivory among fish in both marine and freshwater ecosystems (Floeter et al. 2005, Behrens and Lafferty 2007, González-Bergonzoni et al. 2012, Iglesias et al. 2017), with higher relative incidences of herbivory/omnivory in the tropics. Such macroecological pattern in the structure of fish
food webs has been partially attributed to the effect of tempera-ture on individual catabolic metabolism; ultimately increasing animal food limitation as systems get warmer. However, to the best of our knowledge, no previous studies have investigated the effects of temperature on the relationship between fish trophic position and body size across a global scale.
Here we tested the hypothesis that the trophic position of larger fish in tropical waters would be relatively lower compared to similarly sized individuals in temperate waters in both freshwater and marine ecosystems. We asked how temperature (i.e. climate – tropical/temperate) affects the fish body size–trophic position relationship and, therefore, food-chain length, while controlling for the effect of the non-independence of species taxonomic affiliation. This control is necessary because the nature of the body-size–trophic posi-tion relaposi-tionship is contingent, in part, on evoluposi-tionary his-tory (Romanuk et al. 2011). We obtained data of maximum total body length and trophic position of 3635 ray-finned fish (Actinopterygii) species, the dominant lineage of freshwater and marine vertebrate fauna (Near et al. 2012), from FishBase (www.fishbase.org). Our choice of Actinopterygians fish is justified since they form a monophyletic group and are mainly ectothermic, depending on water temperature to regulate their metabolism (Wegner et al. 2015). Freshwater and marine ecosystems have demonstrated differences in the structure of fish food webs (Sánchez-Hernández and Amundsen 2018) and may differ in abiotic and structural properties (i.e. temperature variation, size, isolation, land– water connectivity and disturbance regime) we also explored the potential climate effects on fish body size–trophic position relationship separately for these two ecosystem types.
Methods
Data sampling
We used maximum total body length (MBL) as a metric of body size, defined as the longest individual recorded for a given species (Froese and Pauly 2012). Even though mass, and not length, is the most relevant size metric for exploring energetic constraints, MBL was used as a proxy for maximum body mass due to the strong relationship between these two variables (r2 = 0.94, p < 0.001; Romanuk et al. 2011) and because data on maximum body mass was unavailable for the majority of species. The trophic position was calculated based on FishBase by adding 1 to the mean trophic position, weighted by relative abundance, for all food items consumed by a species (Froese and Pauly 2012). For a given consumer i, the trophic position is defined as:
Trophi DC Troph j S ij j = + ´ =
å
1 1where Trophj is the fractional trophic level of preyj, DCij is
the proportion of prey i in the diet of a consumer (j), and S is the total number of prey species. Trophic position values
were based on the diet information of each species, sup-ported by more than 800 references and verification of over 16 000 records (Froese and Pauly 2012). Prey items included organisms found in the stomach content analysis or that were otherwise known to be ingested by a given species. Any species whose trophic position was not directly measured (i.e. but estimated via diet similarity with close relatives), was excluded from our analysis.
In FishBase, primary producers and detritus (including associated bacteria) are assigned a trophic level of 1, while primary consumers, which consume mainly plant or detri-tus, are assigned trophic positions between 2 and 2.19. We excluded these primary consumers from our analysis because their trophic position is relatively constrained by morpho-logical and physiomorpho-logical adaptations that make them special-ists on plant food sources (living or dead) or dead animal carcasses or even animal waste (e.g. feces). Moreover, the number and body size distribution of herbivorous and detri-tivorous species were very heterogeneous between tropical and temperate climates. Therefore, these species could affect the potential differences in body size–trophic position rela-tionship between climates through a myriad of mechanisms which are difficult to interpret. The observed pattern could result from evolutionary mechanisms determining the pres-ence or abspres-ence of large species with low trophic positions in warmer tropical waters and not due to a potential energetic limitation of larger species as hypothesized.
Species with preferred upper depth range below 200 m were also excluded from our analysis due to their classification as cold-water types, regardless of their climatic zone (tropical or temperate). Likewise, species classified as subtropical were excluded from our analysis since this category includes many cosmopolitan fishes found in both tropical and temperate zones. FishBase classifies ecosystem type as saltwater, brackish and freshwater, based on the species occurrence and tolerance reported in the literature, and considers primary freshwater (or primary marine) species as fish that evolved in freshwater (or salt water) and spend their entire life in a given ecosystem type. For this study, we only considered species attributed exclusively to either the freshwater or saltwater (i.e. marine) category.
After excluding primary consumers and applying all specified search filters (i.e. depth range, climate, ecosystem type) the most representative taxa (orders, family and genus) from the actinopterygian group remained nearly unchanged. Although our subset of 3635 species represents approximately 12% of all actinopterygians present in the FishBase database, we still have a large and reliable representation of tropical and temperate actinopterygians from both freshwater and marine ecosystems (Supplementary material Appendix 1).
Data analysis
Since species have shared an evolutionary history, species-level studies require controlling phylogenetic dependence. The phylogenetic generalized least squares (PGLS) regression is the most widely used method for this (Felsenstein 1985,
Garamszegi 2014). Unfortunately, the actinopterygians, which comprise about half of the vertebrate species rich-ness (Thomson and Shaffer 2010), are an unknown group of vertebrates from a phylogenetic perspective (Thomson and Shaffer 2010, Near et al. 2012). The most robust phyloge-netic hypothesis for bony fishes only represents 1990 extant species (nearly 6.5% of actinopterygians). Such low repre-sentativeness hinders a PGLS analysis. Given the lack of a large consensus phylogeny, a valid alternative are mixed-effect models using hierarchical taxonomic categories as random intercept effects. Linear mixed effect models have proven to be the most valid alternative in macroecological studies of fishes (Bunnefeld and Phillimore 2012, Luiz et al. 2012, 2013) and others organisms (Horne et al. 2015, Bidau and Martínez 2018).
Due to the non-linear pattern generally observed for the trophic-position and body-size relationship (Arim et al. 2007, 2016, Segura et al. 2015) we opted for a general additive mixed model (GAMM). The GAMM was imple-mented using the function ‘bam’ (package ‘mgcv’) in R, with automatic cross-validation for optimal amount of smoothing (Zuur et al. 2009). The response variable was the species trophic position, while climate (temperate or tropical) was included as a fixed variable. The MBL was included as a smoothing function. Species genus, family and order were included as random effects in the model to account for the dependence between phylogenetically related species. We conducted separate models for each ecosystem type (freshwater or marine) to avoid three-way interaction terms in the analysis that are difficult to inter-pret. The interaction between climate and body size was determined adding a second smoother term, calculating the maximum total body length smoother only for observations in the tropical climate (Zuur et al. 2009; Supplementary material Appendix 2). In this case, the additional body size smoother represents the deviation at the tropical climate from the overall body size–trophic position relationship and was labeled as the interactive term. A visual inspec-tion of the diagnostic plots of the model is available in the Supplementary material Appendix 3.
To illustrate the effects of body size and climate on fish trophic position we used two distinct approaches. First, to show the overall effect of fish body size on trophic position, we calculated the estimated smoothing curve of the scaled predicted values of fish trophic position across the fish body size gradient using the function ‘plot.gam’ (package mgcv) in R. We used the same function to calculate the smoothing curve of the scaled predicted values of fish trophic position for fish body size effect only for the tropical climate when the interaction between body size and climate was significant. Second, based on the statistical models with only significant smoother terms, we calculated the predicted values of tro-phic position for the distinct climate regimes for each habitat type using the function ‘gam.vis’ (package mgcv) in R. This last approach allows the visualization of climate effects on the body size–trophic position relationship for each habitat type, after controlling for taxonomic affiliation.
Data deposition
All data were obtained from FishBase (< www.fishbase.org >). Data also available from the Dryad Digital Repository: <http://dx.doi.org/10.5061/dryad.3pj6958> (Dantas et al. 2019).
Results
Fish trophic position increased with body size for both tropical and temperate climates and for both freshwater and marine ecosystems (Fig. 1). After including climate and con-trolling for taxonomic relatedness in a single statistical model, we observed that body size significantly affected trophic posi-tion in both marine and freshwater ecosystems (Table 1, Fig. 2A–B). However, we observed a significant interactive
effect between climate and fish body size on fish trophic posi-tion for freshwater ecosystems only (Table 1). Overall, the adjusted trophic position for tropical freshwater fish tends to steadily decrease along the body size gradient (Fig. 2C). This result indicates that fish trophic position is progressively lower in tropical than in temperate freshwater ecosystems as body size increases, and supports the hypothesized effect of climate (i.e. temperature) on fish body size–trophic posi-tion relaposi-tionship in freshwater ecosystems (compare Fig. 3A and Fig. 3B).
Discussion
Our results showed that larger freshwater fish forage lower in the food web in a warmer tropical climate than in a cooler temperate climate. This result supports our hypothesis that
Figure 1. Trophic position as function of body size (maximum total body length – cm) for Actinopterygii species across climates and ecosystems. Trophic position–body size relationships are shown for marine tropical (A) and temperate (B) regimes, and for freshwater tropical (C) and temperate (D) regimes. Curves represent fitted values using cubic regression splines ±95% confidence intervals.
the trophic position of larger fish would be lower in tropical waters than in temperate waters. However, this pattern was dependent on the ecosystem type, occurring only in fresh-water ecosystems. Herein, we discuss candidate mechanisms to explain why larger freshwater fish presented lower trophic positions in the tropics and why this effect was not observed for marine species.
The premise of our study was that larger fishes in warmer temperatures would experience an energetic limitation. An increase in individual fish metabolism with rising tempera-tures (Brown et al. 2004) may leads to greater food limitation (Atkinson and Sibly 1997), especially for large individuals (Segura et al. 2015). Feeding down in the food web allow consumers to access more abundant resources, which may compensate the greater food limitation in warmer tropical freshwaters. However, another mechanistic explanation for the reduction in trophic position in warmer climates can be related to stoichiometric constraints imposed by changes in organism physiology (Boersma et al. 2016). The increased metabolic demand at higher temperatures promotes higher demands for carbon, increasing organism threshold elemen-tal ratio for carbon-to-nutrients (TERC:nutrients) (Schmitz 2013). On the other hand, cooler temperatures decreases TERC:nutrients, increasing the consumer demand for nutrient rich resources i.e. meat (Boersma et al. 2016, Moody et al. 2019). Carbon-limited organisms in warmer climates, therefore, should prefer to ingest a food source with higher carbon-to-nutrient ratio, while in colder temperatures nutri-ents should assume the limiting role (Moody et al. 2019). In warmer waters, the preference to forage on carbon-rich resources can manifest for both carnivorous and omnivo-rous fish, as prey carbon-to-nutrient ratios tend to increase at lower trophic levels (Gonzalez et al. 2011, Scharler et al. 2015). However, this foraging strategy should be even more
Table 1. Results of the general additive mixed model (GAMM) for all 3635 Actinopterygii species used in this study. We present test statistics (estimated degrees of freedom (edf), t-value and F) and probabilities (p) listed for each predictor variable in the model. p-values are significant (p < 0.05) for effects in bold. Overall adjusted R2-values [R2(adj.)] for the models for each ecosystem type are also
provided. The reference level was set as ‘Tropical climate’ for the climate effect.
Marine ecosystem R2(adj.) = 0.732
Parametric effects Estimate t-value p
Tropical climate (TC) 0.0462 1.293 0.196
Smoother terms edf F p
Body size 1.000 9.526 0.002
Body size × TC 2.433 2.918 0.057
Freshwater ecosystem R2(adj.) = 0.544
Parametric effects Estimate t-value p
Tropical climate (TC) −0.086 −1.473 0.141
Smoother terms edf F p
Body size 2.310 9.843 <0.001
Body size × (TC) 5.382 2.771 0.020
Figure 2. Smoothing curves (cubic regression spline) representing estimated scaled fish trophic position and point-wise ±95% confi-dence bands across fish body size. The effects of fish body size on fish trophic position, as a smoothing function, are shown for (A) marine and (B) freshwater ecosystems across both climates. As we only detected a significant effect of climate on fish body size–trophic position relationship for freshwater ecosystems, therefore, panel (C) represents the adjusted pattern of fish trophic position for the tropical climate as a deviation from the pattern observed for fresh-water ecosystems across both climates. Graphs were produced with models containing only significant smoother terms.
pronounced among omnivorous consumers, which can adap-tively feed on carbon-rich plant tissues. Therefore, the ability to feed on dead and living plant tissue may compensate for energy limitation and fulfill the greater energetic demand of a considerable proportion of larger omnivorous fish species living in warmer freshwaters (Floeter et al. 2005). On the other hand, omnivorous fish from colder temperatures would prefer to feed on animal food sources with lower carbon-to-nutrient ratios. Combined, these mechanisms acting for different fish guilds could help explain the reduction in the overall trophic position of larger fish in warmer temperatures.
Omnivory may also have a crucial role for the significant effects of climate on fish body size–trophic position relation-ship in freshwaters. Jardine (2016) proposed that increasing body size would lead to a greater consumer biomass reliance on allochthonous material in freshwaters. This mechanism is supported by the strong land–water connectivity gener-ally observed in inland aquatic ecosystems (Jardine 2016), which could decrease the trophic position of larger fish in freshwaters (Ou et al. 2017). Allochthonous material in freshwater systems is mostly derived from terrestrial plant detritus rich in carbon compared to nutrients (Hecky et al. 1993), especially at lower latitudes (Boyero et al. 2017). Therefore, the association among the higher relative species richness of omnivorous fish in tropical waters (González-Bergonzoni et al. 2012), the higher reliance of large aquatic consumers on terrestrial carbon and the high availability of carbon-rich plant-derived allochthonous material in tropi-cal freshwaters may help elucidate the lower trophic position of larger tropical freshwater fish species (Ou et al. 2017), compared to their temperate counterparts.
The absence of the expected temperature effect on the trophic position of larger marine fish species is evidence of some mechanisms operating to attenuate and/or compensate for the increase in metabolic requirements of larger tropical
marine fishes. Two mechanisms may offer plausible expla-nation to this pattern. The first one may be caused by the lower latitudinal thermal amplitude in marine waters. It is reasonable to expect a wider range of water temperatures from temperate to tropical climatic zones in freshwater eco-systems than marine ecoeco-systems because water temperature in larger marine systems is probably not as strongly influ-enced by climate as it is in smaller freshwater ecosystems. Kaschner et al. (2013) showed an average difference of 15°C of sea surface temperature between tropical and temperate climates. On the other hand, such latitudinal thermal varia-tion is on average 20°C or more across tropical and temperate inland aquatic ecosystems (Sobek et al. 2005, Kosten et al. 2012). Therefore, the fish body size–trophic position rela-tionship could be less affected by climate in marine ecosys-tems. The second mechanism may be a consequence of larger area/size of marine ecosystems. Ecosystem size seems to be positively correlated with food-chain length (Post et al. 2000, Post 2002, Takimoto et al. 2012). The productive-space hypothesis argues that total ecosystem production (per-unit-size productivity × ecosystem size) reflects the capacity of an ecosystem to support additional trophic levels (Schoener 1989). Therefore, the larger size of marine ecosystems may represent a greater amount of available resources (Schoener 1989), compensating for energy limitation and fulfilling the greater energetic demand of larger fish in warm marine waters (Arim et al. 2010). For example, if maximum trophic posi-tion is limited by energy transfer inefficiencies, then preda-tors (e.g. large consumers) have to forage over a wider area to meet their energy requirements (Pimm 1982). Marine eco-systems may, therefore, allow a wider area of foraging, sup-porting organisms at higher trophic positions, even at similar productivity levels compared to smaller freshwater systems. In addition, larger ecosystems may have higher functional trophic diversity (Cohen and Newman 1991, Post et al.
Figure 3. Fitted values of fish trophic position for both climate regimes across a gradient of fish body size. The graphs show for both marine (left) and freshwater (right) ecosystems the effect of climate on body size–trophic position relationship estimated through a general additive mixed model (GAMM). Graphs were produced with models containing only significant smoother terms.
2000) to maintain longer food chains. Moreover, spatial pro-cesses in larger ecosystems may enhance the persistence and stabilize predator–prey interactions, promoting longer food chains (Wilson et al. 1998, Holt 2002, Takimoto et al. 2012, Arim et al. 2016).
A better understanding of the relationship between body size and trophic position in tropical and temperate aquatic ecosystems has immediate conservation applications. It is important to acknowledge that both ecological and macro-evolutionary mechanism may represent key drivers of trophic position of fish species across large spatial scales. Therefore, further studies focusing on trait-dependent diversification of fish species, especially concerned with dietary guilds, are needed to differentiate evolutionary and ecological drivers of the association between fish species and their trophic position. For example, resource distribution and competition among individuals can mediate the macroevolutionary fate of omni-vores and specialized dietary guilds at large spatial contexts (Price et al. 2012), which can affect the diversification rates of omnivores at distinct climate regimes (Burin et al. 2016). Despite of the fact that short-term effects of climate changes would depend on animal plasticity or rapid evolutionary changes throughout organism’s generations, we suggest that global warming may have a more prominent effect on the food-web structure in freshwater than in marine ecosystems, decreasing the trophic position of larger freshwater fish and the length of freshwater food chains. Although global warm-ing models focus on air temperature, temperature regimes of aquatic ecosystems have changed parallel to air temperature (Cane et al. 1997, Pilgrim et al. 1998). Freshwater ecosystems are already considered vulnerable to climate change due to certain characteristics, including the fact that water tempera-ture and availability are climate-dependent, and since species have limited ability to disperse as temperature increases, due to the relative isolation and fragmentation of freshwater ecosystems within terrestrial landscapes (Woodward et al. 2010). Such alterations in the topology of freshwater food webs in response to increasing global temperature may affect the connectivity and interaction strength among species, and consequently, the ecosystem attributes that are governed by these food-web properties at a macroecological scale.
Acknowledgments – We thank Guilherme Longo and Marta Coll for
their comments to improve the manuscript.
Funding – The results of this research are included in D. Dantas’
PhD thesis, which was financially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-www. capes.gov.br), under the supervision of JL. Attayde. AC is especially grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – < www.cnpq.br >) for its continuous funding through research productivity grants.
Conflicts of interest – The authors have no conflicts of interest to
declare.
Author contributions – JLA conceptualized the idea of the manuscript.
JLA, DDFD, AC, LSC, RDG and RA planned the study. JLA, DDFD, RA and SMQL discussed the criteria to include or exclude the fish species and compiled the data. AC, LSC, PAM, RDG and
DDFD analyzed the data. All authors revised the manuscript and contributed on earlier drafts.
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Supplementary material (available online as Appendix ecog-04307 at < www.ecography.org/appendix/ecog-ecog-04307 >). Appendix 1.
