Harnessing a mesopelagic predator as a biological sampler reveals taxonomic and vertical resource partitioning among three poorly known deep-sea fishes

Abstract

Pelagic predators are effective biological samplers of midtrophic taxa and are especially useful in deep-sea habitats where relatively mobile taxa frequently avoid observation with conventional methods. We examined specimens sampled from the stomachs of longnose lancetfish, Alepisaurus ferox, to describe the diets and foraging behaviors of three common, but poorly known deep-sea fishes: the hammerjaw (Omosudis lowii, n = 79, 0.3-92 g), juvenile common fangtooth (Anoplogaster cornuta, n = 91, 0.6-22 g), and juvenile Al. ferox (n = 138, 0.3-744 g). Diet overlap among the three species was high, with five shared prey families accounting for 63 ± 11% of the total prey mass per species. However, distinct differences in foraging strategies and prey sizes were evident. Resource partitioning was greatest between An. cornuta that specialized on small (mean = 0.13 ± 0.11 g), shallow-living hyperiid amphipods and O. lowii that specialized on large (mean = 0.97 ± 0.45 g), deep-dwelling hatchetfishes. Juvenile Al. ferox foraged on a high diversity of prey from both shallow and deep habitats. We describe the foraging ecologies of three midtrophic fish competitors and demonstrate the potential for biological samplers to improve our understanding of deep-sea food webs.

Figure 1

Summary of specimen size and collection location across our study area in the central North Pacific Ocean. Longnose lancetfish (Alepisaurus ferox, n = 138), common fangtooth (Anoplogaster cornuta, n = 91), and hammerjaw (Omosudis lowii, n = 79) were collected in the central North Pacific Ocean (a), mostly in waters surrounding the Hawaiian Islands. Heat maps describing the number of stomachs examined per 5° × 5° cell are overlaid on the sampling footprint for all specimens presented in this study (grey, includes primary lancetfish from Portner et al.). The number of stomachs is given for cells represented by more than 14 stomachs. Specimens ranged in size from 0.32–744.90 g (b), but 91% of all specimens were between 1 and 100 g. Paintings by ACLC.

Figure 2

Diet overlap is high among predator species, but there is consistent taxonomic resource partitioning. (a–c) Family-level diet composition and overlap among predators 1–100 g for prey families contributing > 1% mean proportional mass (%$\overline{M}$). (a) Alepisaurus ferox (n = 102) consumed a high diversity of fish, crustacean, and mollusk families, while Anoplogaster cornuta (n = 73) and Omosudis lowii (n = 30) diets were dominated by crustacean and fish families, respectively. The x-axis is broken into two scales to improve visualization. (b) The first two NMDS axes (stress = 0.096, RMSE = 0.001) and 95% confidence interval ellipses depict relatively high diet overlap between Al. ferox and the other two species, and low overlap between An. cornuta and O. lowii. (c) Percent frequency of occurrence (%FO) and %$\overline{M}$ recalculated just for stomachs containing the prey family (prey-specific mean proportional mass, %$\overline{M}$_ps) are given for the four most important prey families for each predator. Dashed lines distinguish specialist (> 50%$\overline{M}$_ps) from generalist (< 50%$\overline{M}$_ps) feeding strategies at individual (< 50%FO) and population levels (> 50%FO). Shapes represent the corresponding families in panel (a). (d–h) Partial effects plots from generalized additive models describe changes in the $\overline{M}$ of prey types with predator size for each species, where axes describe the relationship between a covariate and its parametric contribution (“f(x)”) or the contribution of its smoother (“s(x)”) to the model’s fitted values. Alepisaurus ferox is increasingly piscivorous with size (n = 116) (d–f), while the prey type preferences of An. cornuta (n = 81) (g) and O. lowii (n = 38) (h) did not vary across the sizes examined. Model summaries and partial effects plots for all covariates are given in Table 2 and Fig. S3, respectively.

Figure 3

Differences in the individual size and number of prey per stomach result in similar total prey mass among predators. Multi-linear regressions describing changes in individual prey size (n = 1608) and the total amount of prey per stomach (n = 237) with increasing predator mass. All metrics increased with predator mass, but although there were differences in the mass of individual prey (a) and total prey count per stomach (b) among predator species, there was no difference in the total prey mass per stomach among species (c) when acounting for predator mass. Y-axes are on the log₁₀-scale in panels (a) and (c) and on a log₂-scale in panel (b). Linear models and ANCOVA results for each model are given in Table 3 and model summaries are given in Table S6.

Figure 4

Foraging depths reflect differential vertical resource use among predators. Foraging depths were estimated for each predator (n = 216) as the weighted median depth of occurrence of all prey in a single stomach that had been identified at least to family and contributed more than 1% mean proportional abundance. Anoplogaster cornuta fed mostly on hyperiid amphipods with relatively shallow median depths of occurence (e.g., Lycaeidae 87.5 m, Platyscelus armatus 185 m, Phrosina semilunata 185.38 m; Table S1), while Omosudis lowii fed mostly on deep-dwelling hatchetfishes (e.g., Sternoptyx diaphana 675 m). Alepisaurus ferox foraged more evenly across the upper 700 m of the water column on shared prey, but also incorporated a higher diversity of prey in their shared habitats (e.g., Gempylus serpens 237 m). Paintings by ACLC.

Figure 5

Vertical habitat overlap among predator species varies with size, and predator consumption by Alepisaurus ferox increases with foraging depth. The foraging depths of Anoplogaster cornuta and Al. ferox did not vary with mass, while the foraging depth of Omosudis lowii increased with mass across the size of specimens examined in this study (a). When primary lancetfish from Portner et al. were included [>99% of specimens larger than 100 g, indicated by vertical line and shading in panels (a) and (c)], overlap in foraging depths between Al. ferox and O. lowii increased with Al. ferox mass. Regression lines in panel (a) were fit with generalized additive models (GAM) for each predator species. Partial effects plots for the full GAMs with and without primary lancetfish as described in Table 2 are given in Fig. S3. The median reported habitat depths of each predator (b) during day (“d”) and night (“n”), represented as bars extending from the right-hand y axis of panel (a), were very similar to the foraging depths estimated in this study. Only An. cornuta is known to undergo diel vertical migration. Regressions fit with generalized linear models using a binomial error distribution describe increased frequency of occurrence of all three predator species in the stomach of Al. ferox with specimen mass (c).