Trophic Level Scales Positively with Body Size in Fishes

Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2011) 20, 231–240

RESEARCH Trophic level scales positively with body PAPER size in ﬁshesgeb_579 231..240

Tamara N. Romanuk*, April Hayward† and Jeffrey A. Hutchings

Department of Biology, Dalhousie University, ABSTRACT 1355 Oxford Street, Halifax, Nova Scotia, Aim The existence of a body size hierarchy across trophic connections is widely Canada B3H 4J1 accepted anecdotally and is a basic assumption of many food-web models. Despite a strong theoretical basis, empirical evidence has been equivocal, and in general the relationship between trophic level and body size is often found to be weak or non-existent. Location Global (aquatic). Methods Using a global dataset for fishes (http://www.fishbase.org), we explored the relationship between body size and trophic position for 8361 fishes in 57 orders. Results Across all species, trophic position was positively related to maximum length (r2 = 0.194, b = 0.065, P < 0.0001), meaning that a one-level increase in trophic level was associated with an increase in maximum length by a factor of 183. On average, fishes in orders that showed significantly positive trophic level–body size relations [mean = 51.6 cm Ϯ 11.8 (95% confidence interval, CI)] were 86 cm smaller than fishes in orders that showed no relation [mean = 137.1 cm Ϯ 50.3 (95% CI), P < 0.01]. A separate slopes model ANCOVA revealed that maximum length and trophic level were positively correlated for 47% (27 of 57) of orders, with two more orders showing marginally non-significant positive relations; no significant negative correlations were observed. The full model (order ¥ body size) explained 37% of the variation between body size and trophic position (P < 0.0001). Main conclusions Our results support recent models which suggest that trophic level and body size should be positively correlated, and indicate that morphological *Correspondence: Tamara N. Romanuk, constraints associated with gape limitation may play a stronger role in determining Department of Biology, Dalhousie University, body size in smaller fishes. Differences among orders suggest that the nature of the 1355 Oxford Street, Halifax, Nova Scotia, Canada B3H 4J1. trophic level–body size relation may be contingent, in part, on evolutionary history. E-mail: [email protected] Keywords †Present address: Department of Biology, University of Florida, PO Box 118525, Allometry, body mass, fish, FishBase, gape limitation, metabolic theory of Gainesville, FL 32611, USA. ecology, scaling, size classes.

Among the most important interactions affected by body size INTRODUCTION are consumer–resource interactions, as body size constrains the Body size is of paramount importance in ecological dynamics range of prey sizes a predator can consume (Cohen et al., 1993; (Elton, 1927; Peters, 1983; Calder, 1984; Schmidt-Nielsen, 1984; Arim et al., 2007; Carbone et al., 2007; Hildrew et al., 2007). The Cohen et al., 1993; Brown et al., 2004; Marquet et al., 2005; Arim existence of a body size hierarchy across trophic connections is et al., 2007; Carbone et al., 2007): it shapes the demand that widely accepted as a basic assumption of many food-web organisms place on their environment for energy and materials models (Cohen et al., 1993; Williams & Martinez, 2000; Becker- (through its well known, if poorly understood, relationship with man et al., 2006; Petchey et al., 2008). Cohen et al. (1993), for metabolic processes; Brown et al., 2004) and plays an important example, have suggested that body size provides a mechanistic role in structuring both inter- and intra-speciﬁc interactions. interpretation of the assumed trophic hierarchy of the cascade

© 2010 Blackwell Publishing Ltd DOI: 10.1111/j.1466-8238.2010.00579.x www.blackwellpublishing.com/geb 231 T. N. Romanuk et al. model and have shown that, when species are ranked by body METHODS size, food webs conform more closely to a trophic hierarchy than would be expected if ranks were assigned at random. Data on body size (Lmax) and trophic position (Troph)were The ability of a species to fulfil its energetic demands at a obtained for 8361 species of fish from FishBase (http:// particular trophic level depends on the availability of basal www.fishbase.org; see Appendix S1 in Supporting Information). resources, trophic transfer efficiency and morphological and Maximum length is an important parameter in fishes that is behavioural constraints on a predator’s ability to consume highly correlated with metabolic processes and other life-history available prey (Arim et al., 2007, 2010). In aquatic systems, the traits (Binohlan & Froese, 2009). The metric of body size we transfer of energy through a food web is predicted to be used was maximum total length (Lmax), defined as the longest strongly constrained by body size because of the constraints individual recorded for a given species (Froese & Pauly, 2010). associated with gape-limited predation, a morphological limi- In FishBase, trophic position is calculated by adding 1 to the tation particularly prevalent in fishes (Pimm, 1982; Hairston & mean trophic position, weighted by relative abundance, of all Hairston, 1993; Jennings et al., 2001; Arim et al., 2007). food items consumed by a species (Froese & Pauly, 2010). Esti- However, notwithstanding its logical premise, empirical evi- mates of trophic position in FishBase, using the TROPH routine dence for a size-based trophic hierarchy in aquatic systems is (Pauly et al., 2000), have been found to correlate closely with surprisingly limited. estimates based on stable isotope ratios (Kline & Pauly, 1998). Empirically based exploratory analyses suggest that trophic For a consumer species i, trophic position is defined as: level–body size relationships are highly idiosyncratic: some studies report strong positive correlations (France et al., 1998), G Troph=+1 ∑ DC × Troph some weakly positive relations (Fry & Quiñones, 1994) and iijj j=1 others no relationship at all (Layman et al., 2005). France et al.

(1998), for example, documented strong, positive correlations where Troph j is the fractional trophic level of prey j, DCij repre- between body size and trophic position in benthic food webs sents the fraction of j in the diet of i and G is the total number that included both invertebrates and fish in four proximally of prey species. Calculations of trophic position are based on located lakes and two proximally located seagrass meadows. diet information and food items in FishBase, which are assigned Fry & Quiñones (1994) also found a small positive correlation discrete trophic levels (Froese & Pauly, 2010). Prey items include between trophic position and body mass when comparing organisms that have been found in stomach contents or are across log2 size classes for zooplankton from the north-west otherwise known to be ingested by a given species. More than Atlantic. In contrast, Layman et al. (2005) reported no 800 citations have been used to support the diet information in association between body size and trophic position for preda- FishBase, in addition to the verification of over 16,000 records. tory fishes in Venezuela. Trophic position–body size relations In FishBase, primary producers and detritus (including associ- have also been shown to vary with geographic area (Jennings ated bacteria) are assigned a definitional trophic level of 1 et al., 2001) and functional group identity (Deudero et al., (Mathews, 1993), following the convention established in the 2004). For example, Jennings et al. (2001) showed that body 1960s by the International Biological Program. Primary con- size was unrelated to trophic position at the species level for sumers (herbivores), which consume mainly plants or detritus, fishes in the North Sea but was positively related for fishes in are assigned trophic positions between 2 and 2.19 (Troph = the Celtic Sea. Similarly, Deudero et al. (2004) reported strong 2–2.19). We excluded these from the analysis because their relations between body size and trophic position in the trophic position did not vary with body size and thus cannot Mediterranean for some macro-carnivorous littoral fishes, usefully inform an analysis of the relationship between body size but only weak relations for fishes that feed on small benthic and trophic position in fishes. Omnivores, which consume invertebrates. plants or detritus as well as animals, have trophic positions Here, we examine the relationship between trophic level and between 2.2 and 2.79 (2.2 < Troph > 2.79); secondary (Troph > body size within the most species-rich group of vertebrates, 2.8) and tertiary (Troph > 4) consumers (carnivores) are fishes, which make ideal subjects for broad-scale comparative assigned trophic positions greater than 2.8 (see http:// analyses: The more than 28,000 species that occur globally www.fishbase.org).

(Nelson, 2006) are distributed throughout a wide range of habi- Body size (Lmax) and trophic position (Troph)werelog10- tats (ranging from depths of 8000 m to elevations of 5200 m and transformed and a separate slopes ANCOVA was used to deter- in temperatures ranging from less than -2 °C to more than mine the relation between trophic level and body size across all 40 °C), and represent a diverse array of morphologies, physiolo- species (n = 8361), while taking into account differences emerg- gies, behaviours and life-history strategies with highly variable ing as a consequence of evolutionary history by examining the diets involving diverse feeding strategies (Le Comber & Smith, relation between trophic level and body size by order. Only 2004). Furthermore, and of particular relevance here, adult orders that contained at least three species were included in the ﬁshes vary in size by more than four orders of magnitude analysis (n = 57; Table 2). We also examined the relation between (Hutchings, 2002; Le Comber & Smith, 2004), the entire range of trophic position and body size across all species, using an ordi- which may be experienced by a single individual during its nary least squares (OLS; Type III sum of squares) regression. lifetime. Because it is mass and not length per se that is the most relevant

232 Global Ecology and Biogeography, 20, 231–240, © 2010 Blackwell Publishing Ltd Trophic level and body size in ﬁshes size metric to explore energetic constraints, we used data from Table 3). The full model explained 37% of the variation between

Pauly (1980) to determine if mass was a better predictor of Lmax and Troph (Table 1). On average, fishes in orders that trophic position than length for 18 orders for which mass– showed significantly positive trophic level–body size relations length data were available. [mean = 51.6 cm Ϯ 11.7 (95% confidence interval, CI)] were We also undertook a simple analysis to examine the degree to 86 cm smaller than fishes in orders that showed no relation which phylogeny might influence the relationships between [mean = 137.1 cm Ϯ 50.3 (95% CL); P < 0.01]. Mean trophic trophic position and body size, given that previous studies have position was lower in species that showed positive correlations revealed strong phylogenetic patterns with body size (Diniz- (mean Troph = 3.45 Ϯ 0.01 SD) than in those that showed no

Filho & Tôrres, 2002). Following Nelson (2006), we assigned relation between trophic position and Lmax (mean Troph = 3.51 ranks to all orders of ﬁshes; a rank of 1 represented the most Ϯ 0.03 SD, P < 0.001). Simple, bivariate regression results for ancestral order. After regressing the mean trophic position and relations between Lmax and Troph for all 57 orders can be found

Lmax for each order (each of which represented their respective in Appendix S2. log-transformed averages across all species in each order) Using data from Pauly (1980) for 18 orders for which infor- against phylogenetic rank, we then did the same for the slopes of mation on both Lmax and average maximum mass (in g) were the log(Troph):log(Lmax) for each order. A non-significant rela- available, we found a high correlation between size measured as 2 tionship between rank and the slopes log(Troph):log(Lmax) for length (Lmax) and size measured as mass (in g) (r = 0.94, P > each order indicates that the data points are independent and 0.001). For these data, Lmax explained 22% of the variability in there is no consistent change in the body size–trophic position trophic position while average maximum mass showed no addi- relation according to phylogenetic rank. tional explanatory power with respect to trophic level (Fig. 3). 2 2 Mean trophic position (r = 0.18, P > 0.01) and Lmax (r = 0.27, P > 0.00001) declined significantly with increasing phylogenic RESULTS rank, where a rank of 1 represented the most ancestral order Across all omnivorous and carnivorous fish species (n = 8361) (Fig. 4a, b). Despite this, there was no relationship between the slopes of the log(Troph): log(Lmax) for each order (see Fig. 4c). there was a positive correlation between Lmax and trophic position (r2 = 0.196, P < 0.0001) with a slope of 0.065 (Fig. 1; see Fig. 1 in Appendix S3 for the same figure with herbivores and DISCUSSION detritivores included in the analysis). Significant interaction effects were observed between slope and order, suggesting that Our analysis, based on a global dataset of 8361 species in 57 the slopes and intercepts of the relationship between body orders, identified a number of patterns regarding relations size and trophic position differ among orders (Table 1). An between trophic position and body size in fishes that are of ANCOVA with separate slopes for each order revealed signifi- significant interest. First, across all fish species, body size cant, positive relations between Lmax and Troph for 47% (27 of explained 20% of the variability in trophic position (Fig. 1). The 57) of orders, with two more orders showing marginally non- considerable scatter we observed (Fig. 1) was due in part to significant positive relations (Tables 1 & 2). No significant nega- phylogeny. When evolutionary history was included in the tive correlations between Lmax and Troph were observed for any explanatory model, the amount of variance explained increased order (Table 2; see Appendix S2). Eleven orders showed strong to 37%, which is impressive considering the wide diversity of 2 (r > 0.30) positive relations between Lmax and Troph (Fig. 2, species morphologies, life-history strategies (e.g. anadromy/ catadromy, age/size at maturity, social structure) and habitat characteristics (e.g. primary productivity, benthic versus pelagic,

6 y = 0.442 + 0.065logx temperature) included in the data (Table 1). Indeed, the remain- r2= 0.19 der of the observed variation in trophic level probably stems 5 p < 0.0001 from such important characteristics. Second, the relation between trophic position and body size was more often 4

3 Table 1 Whole-model ANCOVA with separate slopes for the

Trophic Level effect of order and body size (Lmax, maximum length in cm) on trophic level (Troph).

2 1101001000 Separate slopes Body Size (cm) Effect FP Whole model

Figure 1 Positive relationship between body size (Lmax, maximum 2 length in cm) and trophic level (Troph) for all 8631 species of ﬁsh Lmax vs. Troph L max 29.661 < 0.0001 r = 0.37 > with Troph 2.18. Clusters of points at discrete trophic levels (e.g. By order Order ¥ Lmax 2.567 < 0.0001 P < 0.0001 4.5) occur when prey assigned discrete trophic levels in FishBase dominate the diet (see methods for more details). Slopes (b) are presented in Table 2.

Table 2 Relations between body size 2 Order Lmax Troph r Slope -95% CI +95% CI Pn (Lmax, mean maximum length in cm) and trophic level (Troph) for 57 orders of Acipenseriformes 269.5 3.39 0.267 0.086 0.086 -0.002 0.057 23 ﬁshes from FishBase, showing results of Albuliformes 62.3 3.31 0.110 0.056 0.056 -0.100 0.482 20 within-order correlations (R) between Anguilliformes 106.8 3.86 0.116 0.057 0.057 0.025 0.000 157 Lmax and Troph, the slope of the relation Ateleopodiformes 172.0 4.35 0.508 0.070 0.070 -0.450 0.793 3 with 95% conﬁdence intervals (CI), Atheriniformes 12.7 3.11 0.000 -0.002 -0.002 -0.053 0.938 65 P-value and number of species included Aulopiformes 42.1 3.99 0.075 0.053 0.053 0.013 0.009 95 in the analysis. Batracoidiformes 34.9 3.77 0.051 0.056 0.056 -0.118 0.526 21 Beryciformes 31.3 3.7 0.000 0.004 0.004 -0.048 0.875 68 Carcharhiniformes 155.3 4.03 0.101 0.034 0.034 0.006 0.018 135 Characiformes 19.2 3.24 0.083 0.058 0.052 0.035 0.000 214 Chimaeriformes 104.8 3.61 0.033 0.087 -0.087 -0.285 0.391 14 Clupeiformes 26.4 3.3 0.202 0.038 0.035 0.011 0.004 184 Cypriniformes 26.9 2.97 0.005 0.011 0.010 0.001 0.039 732 Cyprinodontiformes 7.8 3.05 0.002 0.038 0.013 -0.042 0.648 102 Elopiformes 138.2 4.01 0.003 0.045 0.045 -0.225 0.745 7 Esociformes 35.3 3.75 0.614 0.108 0.108 0.028 0.008 9 Gadiformes 56.7 3.67 0.449 0.112 0.112 0.086 0.000 165 Gasterosteiformes 26.9 3.49 0.301 0.070 0.070 0.038 0.000 101 Gymnotiformes 50.0 3.19 0.345 0.071 0.071 0.011 0.020 22 Heterodontiformes 120.9 3.56 0.019 0.031 0.030 -0.271 0.843 8 Hexanchiformes 260.4 4.3 0.263 0.040 0.040 -0.199 0.744 5 Lamniformes 466.7 4.26 0.118 -0.074 -0.074 -0.198 0.238 14 Lampridiformes 237.5 3.97 0.011 0.015 0.018 -0.063 0.663 13 Lepidosireniformes 112.8 3.37 0.000 0.001 0.001 -0.205 0.993 7 Lophiiformes 41.0 4.12 0.266 0.061 0.063 0.021 0.004 60 Mugiliformes 54.8 2.55 0.036 -0.059 -0.059 -0.171 0.304 32 Myctophiformes 12.1 3.23 0.098 0.028 0.028 -0.023 0.284 100 Myliobatiformes 147.7 3.6 0.105 0.044 0.044 0.000 0.051 84 Myxiniformes 51.3 4.09 0.017 0.039 0.039 -0.107 0.602 19 Ophidiiformes 39.4 3.55 0.461 0.066 0.066 0.028 0.001 49 Orectolobiformes 268.1 3.8 0.002 -0.004 -0.004 -0.066 0.904 17 Osmeriformes 23.1 3.24 0.128 0.026 0.041 0.009 0.013 87 Osteoglossiformes 66.7 3.26 0.149 0.052 0.052 0.013 0.009 41 Perciformes 35.6 3.46 0.202 0.068 0.068 0.064 0.000 3822 Percopsiformes 10.4 3.33 0.064 -0.022 -0.022 -0.243 0.843 8 Petromyzontiformes 36.7 3.98 0.265 0.177 0.177 0.083 0.000 21 Pleuronectiformes 36.8 3.55 0.046 0.026 0.026 0.005 0.013 164 Polymixiiformes 40.6 4.06 0.541 -0.04 -0.040 -0.327 0.787 4 Polypteriformes 59.7 3.48 0.398 0.261 0.261 0.082 0.004 12 Pristiformes 596.5 4.2 0.001 0.012 0.012 -0.577 0.968 4 Pristiophoriformes 147.7 4.06 0.253 0.186 0.186 -1.104 0.777 3 Rajiformes 95.6 3.78 0.023 0.021 0.021 -0.030 0.420 76 Rhinobatiformes 148.8 3.7 0.072 0.038 0.038 -0.058 0.440 20 Saccopharyngiformes 44.7 3.74 0.863 0.106 0.106 0.033 0.004 7 Salmoniformes 82.6 3.56 0.320 0.117 0.116 0.065 0.000 62 Semionotiformes 174.0 4.12 0.426 0.165 0.165 -0.230 0.414 6 Scorpaeniformes 35.4 3.61 0.106 0.046 0.046 0.027 0.000 309 Siluriformes 48.4 3.42 0.117 0.048 0.048 0.038 0.000 525 Squaliformes 116.9 4.18 0.009 0.009 0.009 -0.035 0.694 55 Squatiniformes 156.1 4.04 0.042 -0.041 -0.041 -0.283 0.739 11 Stephanoberyciformes 13.2 3.33 0.243 0.047 0.047 -0.023 0.188 17 Stomiiformes 23.1 3.89 0.519 0.133 0.133 0.106 0.000 145 Synbranchiformes 44.7 3.25 0.045 -0.024 -0.024 -0.075 0.349 28 Tetraodontiformes 36.9 3.27 0.070 0.042 0.042 0.019 0.001 161 Torpediniformes 68.1 3.81 0.443 0.15 0.150 0.073 0.000 20 Zeiformes 52.4 3.97 0.381 0.147 0.147 0.010 0.036 14

Signiﬁcant within-order correlations between Lmax and Troph are shown in bold.

Esociformes Gadiformes Gasterosteiformes

6 y = 0.387 + 0.108logx 6 y = 0.375 + 0.112logx 6 y = 0.451 + 0.070logx r2= 0.614 r2= 0.449 r2= 0.301

5 n 5 5 n p<0.01 p < 0.001 p < 0.001

tio

4 position 4

4 posi

3 3 3

log Trophic

log Trophic positio

2 2 2 1 10 100 1000 1 10 100 1000 1101001000 log Body Size (cm) log Body Size (cm) log Body Size (cm)

Gymnotiformes Ophidiiformes Polypteriformes

6 y = 0.394 + 0.071logx 6 y = 0.456 + 0.066logx 6 y = 0.080 + 0.261logx r2= 0.345 r2= 0.461 r2= 0.398 5 5 5 p < 0.05 p < 0.01 p < 0.01

tion 4 4 4

posi

3 3 rophic position 3

log Trophic position log Trophic

2 2 2 1 10 100 1000 1 10 100 1000 1101001000 log Body Size (cm) log Body Size (cm) log Body Size (cm)

Saccopharyngiformes Salmoniformes Stomiiformes

6 6 y = 0.429 + 0.106logx 6 y = 0.334 + 0.116logx y = 0.417 + 0.133logx 2 r2= 0.863 r2= 0.320 r = 0.519

n 5 n 5 5 p < 0.01 p < 0.001 on p < 0.001

4 4 4 positi

rophic positio 3 3 rophic 3

g Trophic positio

log T lo log T

2 2 2 1 10 100 1000 1 10 100 1000 1 10 100 1000 log Body Size (cm) log Body Size (cm) log Body Size (cm) Torpediniformes Zeiformes

6 y = 0.315 + 0.150logx 6 y = 0.350 + 0.147logx r2= 0.443 r2= 0.381

n 5 n 5 p < 0.001 p < 0.05

itio 4 positio 4

3 3

log Trophic

log Trophic pos

2 2 1 10 100 1000 1 10 100 1000 log Body Size (cm) log Body Size (cm)

Figure 2 Relationship between body size (Lmax, maximum length in cm) and trophic level (Troph) for 11 orders of ﬁshes that showed strong (> 30%) positive relations between body size and trophic level.

2 Table 3 Eleven orders that showed strong (r > 0.30) positive relations between body size (Lmax, maximum length) and trophic level (Troph).

Order (common name) Morphological or behavioural adaptation suggestive of gape limitation Reference(s)

Esociformes (pikes and Tend to swallow their prey whole Bond (1996), Hart (1997) mudminnows) (Gadiformes cods and allies) Tend to swallow prey whole; elongate bodies Moyle & Cech (1988) Gasterosteiformes (sticklebacks, Voracious predators; tend to swallow their prey whole; suck in prey from Bond (1996), Hart (1997), tubesnouts, pipefish) relatively large distances and engulf them whole (tubesnouts and pipefish) Moyle&Cech(1988) Gymnotiformes (knifefishes) Use electric shocks to stun prey and swallow them whole; elongate bodies Bond (1996) Ophidiiformes (pearlfishes, cusk Elongated or eel-like body forms with very large heads or jaws relative to Carpenter (2002) eels, and brotulas) their body size Polypteriformes (bichirs and Jaw is modified to expand in the horizontal plane that allows strong biting Bartsch (1997) ropefish) and sucking action while breathing atmospheric air Saccopharyngiformes Elongated or eel-like body forms with very large heads or jaws relative to Carpenter (2002) (saccopharynx fishes) their body size Salmoniformes (salmonids) Tend to swallow their prey whole Stomiiformes (dragonfishes) Elongated or eel-like body forms with very large heads or jaws relative to Carpenter (2002) their body size Torpediniformes (electric rays) Use electric shocks to stun prey and swallow them whole. have elongate Compagno (1999) bodies highly distensible jaws Zeiformes (dories and boarfish) Possess highly distensible jaws Moyle & Cech (1988)

Shown are the order, common name and morphological and behavioural adaptations that are suggestive of gape limitation.

significant for orders that contained fishes with smaller body level might be expected to be more strongly limited by energetic sizes than for orders that contained fishes with larger body sizes, constraints associated with the mass and temperature depen- with the strongest correlations between trophic level and body dence of organism metabolism in combination with the quan- size observed in orders that show distinct adaptations to pres- tity of available basal resources and trophic transfer efficiency, sures associated with gape-limited feeding modes (Fig. 2, resulting in a negative relation between trophic level and body Table 3). Below we expand on the above patterns in more detail. size over the larger end of the size spectrum (Arim et al., 2007). Our analysis suggests that trophic position is an increasing Consequently, trophic level might be expected to first increase function of body size. A one-level increase in trophic level was with body size for smaller species, which are constrained by associated with an increase in maximum length by a factor of mechanisms other than energetic limitation, and then decrease

183 (since the slope of the regression of log(troph) on log(Lmax) with body size in larger species, assuming that no other mecha- is 0.442: 1/0.442 = 2.2624 and 102.2624 = 182.997; see Jonsson et al. nisms are operating to counteract strong energetic constraints 2005). Thus, fishes with high trophic levels have very large body (Arim et al., 2007). Such a hump-shaped pattern has only ever sizes relative to fishes with lower trophic levels. It is likely that been reported by Genner et al. (2003) for the Lake Malawi some combination of lower relative metabolic rates for large cichlid Pseudotropheus callainos, which shows a strong ontoge- predators, decreases in trophic transfer efficiency toward the top netic diet shift from planktonic to benthic organisms during of the food web, a higher sequestration of energy for mainte- ontogeny. nance in larger predators and less frequent encounters with prey Our analysis, which was based on a global dataset for fishes, based on smaller population sizes of prey might all contribute to cannot be used to explicitly test the community-based hypoth- the increase in trophic level with body size (Hildrew et al., 2007). eses of Arim et al. (2007), which predict a hump-shaped Interestingly, this pattern, which highlights the metabolic con- pattern whereby trophic level increases with body size for sequences of larger body sizes, may also partially explain why the smaller organisms and decreases with body size for larger length of food chains has such strong upper bounds in aquatic organisms. However, the relation between body size and systems (Arim et al., 2007). trophic level was significant more often for orders that con- It has been hypothesized that, within a food web, the relation tained fishes with smaller body sizes. On average, the mean between trophic level and body size should be hump-shaped as body size of the 27 orders of fishes that showed a significant a consequence of differential effects of gape limitation and ener- positive relation between trophic level and body size were getic constraints across body size (Arim et al., 2007). For small 86 cm smaller than the mean body size of the 20 orders of consumers, morphological constraints related to gape limita- fishes that showed no relation between trophic level and body tion may strongly affect trophic level, resulting in a strong, posi- size. These results suggest a broad, macroecological pattern tive relation between trophic level and body size across the wherein trophic level and body size are more tightly coupled small end of the size spectrum. In contrast, maximum trophic for smaller fishes.

Figure 4 Phylogenetic rank analysis. Following Nelson (2006), Figure 3 Data from Pauly (1980) showing the relation between we assigned ranks to all orders of ﬁshes; a rank of 1 represented body size measured as maximum length (Lmax, cm), average the most ancestral order: (a) mean trophic level (Troph) and (b) maximum mass (g) and trophic level (Troph) for 18 orders for mean body size (Lmax, maximum length in cm) for each order which mass–length data were available: (a) correlation between against phylogenetic rank. For both (a) and (b), mean values Lmax and mass; (b) correlation between Lmax and Troph; (c) represent log-transformed averages across all species in each correlation between mass and Troph. order. (c) The slope of the relation between log(Troph) and

log(Lmax) for each order against phylogenetic rank.

Our results also suggest a strong evolutionary pattern, where osteiformes, Gymnotiformes, Ophidiiformes, Polypteriformes, the existence of a trophic level–body size relation is at least Saccopharyngiformes, Salmoniformes, Stomiiformes, Torpe- partially dependent on morphological adaptations suggestive of diniformes, Zeiformes (Tables 2 & 3, Fig. 2). The species in these gape limitation. Order-level relationships between body size and orders are characterized by distinct morphological features or trophic level varied from negative, albeit non-significant, corre- feeding modes, such as the ability to swallow prey whole, from lations in some orders to highly significant positive associations which strong gape limitation can be inferred. Species in the in others (e.g. r2 = 0.86 for Saccopharyngiformes). The strongest orders that showed strong relations between body size and relations between trophic level and body size were observed in trophic level were generally piscivores. Specific adaptations in orders that show distinct adaptations to pressures associated these orders suggestive of strong gape limitation include large, with strongly gape-limited feeding modes and smaller average elongate bodies coupled with very large heads or jaws relative to body sizes (Table 3, Fig. 2). Eleven orders showed strong (> 30% their body size such as in Saccopharyngiformes (sackpharynx of the variance explained) significant, positive relations between fishes), Stomiiformes (dragonfishes) and Ophidiiformes (pearl- trophic level and body size: Esociformes, Gadiformes, Gaster- fishes, cusk eels, and brotulas; Carpenter, 2002). Highly disten-

Table 4 Eight orders that showed non-signiﬁcant negative trends between body size (Lmax, maximum length) and trophic level (Troph).

Order (common name) Morphological or behavioural characteristic that may circumvent gape limitation Reference(s)

Atheriniformes Schooling fish that tend to feed on plankton in large groups. In schooling fish group Moyle&Cech(1988) (silversides) behaviour may be more important in determining trophic level than individual body size Lamniformes (1) Bite off large chunks of prey rather than attempting to swallow them whole. This feeding Moyle&Cech(1988) (mackerel sharks) mode is less likely to invoke gape limitation (2) Contains one of the largest species of fish in the ocean (the whale shark, Rhincodon typus) which is a planktivore, using gill rakers to filter plankton from the water column: the largest species in this order occupies a low trophic level Mugiliformes Extremely active benthic schooling fish that feed mainly on organic detritus and small alga Moyle&Cech(1988) (mullets) which they obtain by scooping their mouths through the benthos. They have the longest intestine per unit length of any fish and a muscular, gizzard-like stomach that assists them in processing the matter they ingest, which is primarily sand and other indigestible matter Orectolobiformes (1) Bite off large chunks of prey–afeedingmodethatisless likely to invoke gape-limitation Nelson (1994) (carpet sharks) (2) Incredibly diverse morphology, including one species with a tail longer than its body length (the zebra shark, Stegostoma varium) (3) Contains one of the largest species of fish in the ocean (basking shark, Cetorhinus maximus) a planktivore, uses gill rakers to filter plankton from the water column: the largest species in this order occupies a low trophic level Percopsiformes Small order (three families consisting of nine species in total) of small (maximum length c. Nelson (1994) (trout-perches) 20 cm) fish); eight species were included in our analyses. The non-significant trend may be an artefact of the small number of species examined Polymixiiformes (1) Small order consisting of one family in a single genus that contains ten species (four Carpenter (2002) (beardfishes) species included in analysis – Polymixia berndti, P. japonica, P. lowei and P. nobilis). The non-significant trend may be an artefact of the small number of species examined (2) Have 20-100+ pyloric caecae, which effectively act to increase the surface area of the gut Synbranchiformes Extremely elongated eel-like fish capable of breathing atmospheric oxygen; intestinal tract Bond (1996), Moyle (spiny eels and sometimes doubling as a respiratory system. Synbranchoidei (swamp eels) are & Cech (1988) swamp eels) amphibious, moving across land or burrowing into the mud to survive long periods of desiccation in the habitats; many Mastacemelbeloidei (spiny eels) depend on atmospheric oxygen. The coupling of unique features of respiration and digestion may have produced the non-significant negative relation between trophic level and body size Squatiniformes (angel Bite off large chunks of prey rather than attempting to swallow them whole; intermediate Moyle & Cech (1988), sharks) forms between sharks and rays, with dorso-ventrally flattened bodies, with spikelike teeth. Compagno (1984) Have highly protrusible, ‘trap-like’ jaws used to snap up small bony fishes, crustaceans, cephalopods, bivalves and gastropods at high speeds from muddy or sandy bottoms. This feeding mode is less likely to invoke gape limitation

Shown are the order, common name and morphological and behavioural characteristics that may circumvent gape limitation. sible jaws such as those present in the Zeiformes (dories and Synbranchiformes and Squatiniformes (Tables 2 & 4, see boarfish), Torpediniformes (electric rays) and Polypteriformes Appendix S2). Species in these orders tend to have unique (birchirs and ropefish) may be adaptations to counteract gape behavioural patterns, such as schooling, morphological features limitation, as are the expandable mouths used to suck prey in the such as extremely long intestines or feeding strategies that allow Aulostomidae (tubesnouts) and Syngnathidae (pipefishes and prey to be as large or larger than the predator. For schooling fish seahorses) in the order Gasterosteiformes (Moyle & Cech, 1988). such as the Atheriniformes (silversides), group behaviour may Other orders with strong positive relations between trophic level be more important in determining trophic level than individual and body size include orders composed of highly voracious body size. Extremely long intestines, such as those that occur in predators, such as Esociformes (pikes and mudminnows), Gym- the Mugiliformes (mullets), act to increase the surface area of notiformes (knifefishes) and Salmoniformes (salmon, trout, the gut, thus maximizing nutrient absorption. The feeding char), all of which tend to swallow their prey whole (Bond, 1996; mode of three of the eight orders that showed no relation Hart, 1997). between body size and trophic level – the Lamniformes (mack- Although no orders showed significant negative correlations erel sharks), Orectolobiformes (carpet sharks) and Squatini- between trophic level and body size, eight did show non- formes (angel sharks) – is to bite off large chunks from their significant negative trends, where trophic level tended to prey, a feeding mode that effectively avoids gape limitation. decrease with body size: Atheriniformes, Lamniformes, Mugili- Another feeding mode that avoids gape limitation is observed in formes, Orectolobiformes, Percopsiformes, Polymixiiformes, two of these orders, which contain the two largest fish species in

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