Both herbivory and predation are key processes within food webs that control biomass distribution and species composition within and across communities (Borer et al., 2006; Halpern et al., 2006). Understanding spatial and temporal variation in consumption is crucial for predicting how ecosystems will respond to global and local change, including warming climate and fishing impacts (Ling et al., 2009; Vergés et al., 2011). Although relative variation in primary production and producer biomass can be compared efficiently in both terrestrial and marine environments, the mobility, diet, and behavior of consumers (e.g., fishes) make their distribution and top-down impacts challenging to quantify, especially in marine habitats (Duffy et al., 2015; Fraser et al., 2020; Whalen et al., 2020). However, an increasing number of studies have demonstrated that top-down processes vary predictably across latitude within a handful of marine habitats (Freestone et al., 2011; Rodemann and Brandl, 2017; Musrri et al., 2019; Whalen et al., 2020; Lefcheck et al., 2021), which may give insight into fish presence and behaviors, and help with the interpretation of consumption processes (Ferreira et al., 2004; Navarrete et al., 2005).

Tropical marine seascapes contain a patchwork of nearshore habitats and therefore are an ideal test bed for understanding variation in consumption among habitat types and trophic guilds, including various types of consumers. In the past decade, a landscape-level perspective has informed the value of coastal habitats as nurseries (Nagelkerken et al., 2015), and this perspective could also help to unite the large body of literature examining within-habitat variation in consumption rates. Coral reefs, for example, are among the best-studied marine ecosystems with respect to trophic processes, and there is a long history exploring how grazing by herbivorous fishes is critical in maintaining a coral-dominated state (Lewis, 1986; Burkepile and Hay, 2010; Tootell and Steele, 2016). Seagrasses have also long been the focus of comparative experiments to understand how predation—generally in the form of tethered prey—varies across space and through time (Heck and Wilson, 1987). Nevertheless, fewer studies explore how consumption changes across multiple habitats within the same coastal seascape, and those that do have revealed inconsistent patterns in terms of the degree of consumption observed in different habitats (Chittaro et al., 2005; Hammerschlag et al., 2010). Indeed, a recent meta-analysis on nursery function uncovered only a dozen or so studies comparing among multiple habitats (coral reefs, mangroves, and/or seagrasses), and these failed to reveal any general patterns in terms of juvenile survival/predation risk associated with each (Lefcheck et al., 2019a). One potential explanation is that studies to date have rarely had temporal breadth to uncover such generalities, as longer time series may reduce natural variability enough to resolve differences among habitats in trophic processes.

The question of how consumption varies across tropical seascapes is timely, as both the habitats and the species they support are changing rapidly and might lead to substantial changes in ecosystem functioning. Caribbean marine ecosystems in particular have suffered declines in coral cover and structural complexity (Gardner et al., 2003; Alvarez-Filip et al., 2009), seagrass cover and density (Stallings, 2009), and mangrove forest extent (Wilson, 2017). Concurrently, herbivorous, omnivorous, and predatory fishes have all declined in abundance, biomass, and diversity in the Caribbean (Paddack et al., 2009; Stallings, 2009), leaving them less able to control macroalgal accumulation on coral reefs (Rasher et al., 2013; Adam et al., 2015; Lefcheck et al., 2019b). Establishing a strong baseline for consumption throughout the region is a critical step in evaluating change, including recovery. Belize, for example, has recently banned the harvest of parrotfishes and surgeonfishes, leading to a recovery in parrotfish abundance and consequent reductions in macroalgae and increases in coral cover (Mumby et al., 2021).

To better understand how the intensity of consumption by herbivores and predators varies with habitat, over time, and with fish assemblage across a Caribbean seascape, we deployed standard assays of macrophyte and dried squid consumption annually over five consecutive years (2015–2019) across seventeen sites and five habitats around Carrie Bow Cay, Belize, including fore reef, patch reef, mangrove, seagrass, and sand. Additionally, we conducted visual surveys of fish communities annually in habitats to quantify fish biomass and diversity and, in 2017, used video analysis at a subset of habitats to directly identify the fish species responsible for consumption. Our primary goal was to establish a baseline of relative consumption, and further we expected that—as in previous studies (e.g., Hay, 1984; Duffy et al., 2015)—consumption would be highest on highly structured reefs and lowest on unstructured sand flats, and that most consumption would be attributable to a small number of consumer species (Adam et al., 2015).

Standardized assays of macrophyte and dried squid consumption over a 5-year period across a Belizean tropical seascape revealed that consumption rates differed among habitats and these differences were consistent through time (Figures 2–4). Specifically, consumption was generally higher in structured coral reef and mangrove habitats, and lower in less structured seagrasses and sand flats. Video footage from 2017 indicated that a limited set of species was responsible for the observed consumption rates, and that the identities of the dominant consumers varied among habitats. Thus, it appears that a suite of common consumers may be responsible for maintaining a hierarchy of trophic processes across the coastal habitat mosaic in Belize, and that consumption across the seascape relies on this biodiversity (Supplementary Figure 3).

One explanation for the observed variation in consumption rates across habitats is structural complexity: three-dimensionally complex habitats like coral reefs and mangrove prop roots can provide refuge for numerous fishes and invertebrates that are responsible for consuming the types of bait we use here, while less complex structures like shorter seagrass canopies and sand flats do not provide such a variety of microhabitats for small fish to occupy (Dean and Connell, 1987; Hackradt et al., 2011). Although we did not directly measure habitat complexity in our study due to challenges in comparably measuring this quantity across the range of habitats sampled, we did observe the highest biomasses of most key consumer families—those which previously have been linked with habitat heterogeneity (Mumby et al., 2004; Nagelkerken, 2007)—on the fore reefs, patch reefs, and in mangroves (Supplementary Figure 5). The increased consumption of both macrophytes and squid we saw in these more complex habitats is consistent with previous studies (Valentine et al., 2007) and highlights the fact that the squid bait captures a complementary trophic group to herbivores—likely benthic invertivores and mid-sized predators—rather larger predators on them. Indeed, large predators are now scarce throughout the Caribbean (Paddack et al., 2009; Mumby et al., 2012), limiting the potential for interactions among consumers of both types of assays deployed in tandem, and some predators may only have interest in live prey.

The higher interannual variability in consumption in less structured sand and seagrass habitats (evidenced by their relatively high coefficients of variation) (Figure 2) likely reflects the transient use of these habitats by fish, creating a “hit-or-miss” assessment of consumption, where foraging grounds are spatially vast but consumers spend little time in them, such that consumers may fail to encounter baits during their foray. Another possible explanation is that the fishes that consumed our baits are more visible to their own predators in these open areas, limiting their foraging and leading to lower consumption, which is more consistent with the overall lower rates of consumption observed in seagrasses and especially sand flats. The interannual variation in consumption in unstructured habitats was unexpected and suggests the importance of including unstructured habitats in cross-habitat comparisons of ecological processes.

The generally lower rates of consumption we found in less structured habitats were accompanied by different species consuming the baits in different habitats. Previous work suggested that a diverse fish assemblage becomes more important in controlling turf algae when moving from the local to regional scale, incorporating more heterogeneity in both the foundational species and also the fish community itself (Lefcheck et al., 2019b). Our work similarly highlights that macrophyte browsing and squid consumption are attributable to largely different species, illustrating that a diverse consumer assemblage more effectively drives multiple trophic processes across the larger coastal seascape (Brandl et al., 2019).

Variation in the dominant consumers across habitats could stem from a reduced exchange of adult fishes among nearby habitats, but not from an exchange of juveniles, which are well known to mature in seagrasses and mangroves before moving to coral reefs. This would explain why squid consumption was lowest in the sand flats that act as conduits, shuttling fishes between multiple habitats. It could also be a consequence of the habitat-specific foraging adaptations of the various fish species and their familiarity with the baits. For example, acanthurid and scarid fishes were the dominant herbivores we observed on both patch reefs and fore reefs (Supplementary Figure 3B), as is typical of Caribbean reefs (Lewis and Wainwright, 1985; Burkepile and Hay, 2010; Lefcheck et al., 2019b; Dell et al., 2020). However, weedpops deployed to patch reefs were also targeted by omnivorous angelfish (pomacanthids), and the benthic invertivore Halichoeres garnoti, which frequently bites at benthic algae to access its target arthropod and echinoderm prey (Clifton and Motta, 1998).

In contrast, squid baits presented a novel resource, isolating the effect of species identity irrespective of either prey or predator behavior. In this case, squid bait was consumed primarily by wrasses on fore reefs, by snappers in mangrove habitats, and by the widest variety of fish species on patch reefs, including two species of snapper (Figure 7). The placement of patch reefs within the coastal seascape may be an explanation for this finding, as they are generally isolated from the continuous reefs and more proximate to other habitats like seagrasses and mangroves, which could lead to greater spillover of species from these other habitats (Figure 1 and Supplementary Figure 2). Seascape configuration, or the spatial orientation of habitats in relation to one another, is likely to play a large role in the exchange of species, the connectivity of ecosystems, and ultimately the functioning of coastal habitats and is worthy of further exploration with respect to trophic processes (Mumby et al., 2004; Jones et al., 2020).

Of particular note is our finding that fish biomass (from transect surveys) was generally uncorrelated with loss of either squid baits or macrophytes except in the case of the biomass of the subset of browsing herbivores on patch reefs. It is well known that fish biomass is a strong determinant of ecosystem processes in tropical marine ecosystems, including herbivory (e.g., Lefcheck et al., 2019b). That total fish biomass did not explain consumption in the current study could stem from a few causes. First, the biomass threshold of key consumers necessary to consume all assays within 24 h is easily met in the deployment area, leading to overall high rates of consumption, which is certainly true for squid and likely also the highly palatable Acanthophora. The resulting lack of variation when consumption is uniformly high or low prevents further evaluation of potential patterns. Second, patch reefs are smaller and more isolated than fore reefs. Consequently, they may attract more and varied browsers that are concentrated in a smaller area, one which is also less likely to offer alternative resources. Hence, small patch reefs are generally associated with seagrass-depleted sand halos generated by foragers temporarily leaving the reef (Ogden et al., 1973; Madin et al., 2011; DiFiore et al., 2019). Whether reef “patchiness” (size and proximity to other habitats) plays a role in herbivores’ abilities to control algal proliferation through consumption remains a question for future research. Finally, the surveys were not conducted exactly when the assays were deployed (to avoid diver artifacts), and the fish community observed on the transects may differ somewhat from those interacting with the experimental assays (Figures 6, 7 and Supplementary Figure 3).

We raise several final caveats with our study. Since videos were only filmed in 2017 and not over the entire range of habitats for both squidpops and weedpops, we can only draw firm conclusions about the identity of consumers at the times and places filmed. Additionally, much of the consumption observed in the videos may have been the result of patchy and opportunistic feeding, possibly creating the illusion of consistency in consumer identity. These questions could be answered by capturing video footage over multiple years and habitats to improve our understanding of the role of individual species in sustaining trophic processes across the coastal mosaic.

Overall, our 5-year study of macrophyte and squid bait consumption across a nearshore tropical seascape suggests that spatio-temporal patterns in consumption are primarily explained by habitat type, with the majority of herbivory occurring in structured reef habitats and carnivorous consumption occurring in reefs and mangroves. Notably, these relative differences persisted throughout the duration of the study, establishing a baseline to evaluate future change. Moreover, differences in consumer diversity and consumption patterns emerged between patch reefs and fore reefs, likely due to seascape characteristics including patchiness, proximity, and connectivity to other habitat types. Because a large proportion of the trophic interactions we measured occurred in structurally complex habitats, continued reef flattening and mangrove and seagrass loss and fragmentation may create cascading effects in Caribbean food webs, potentially shifting this baseline. Continued management of fish communities in Belize, particularly of the species known to be strong interactors with benthic macroalgae, is therefore key in maintaining trophic processes and mitigating the consequences of habitat change.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

JED, VP, JL, and LH contributed to conception and design of the study. VP, JED, LH, RW, and SJ performed field research. CR analyzed video footage with guidance from JED and MO. JL, CR, and LH performed analysis and wrote the first draft of the manuscript. All authors contributed to manuscript revision, and read and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.