Introduction
Population sizes and total community diversity are regulated by an array of forces, ranging from long term climatic conditions and energy availability, to diminished survival due to antagonistic interactions from predators or parasites, to extreme climatic events, or resource restriction due to competition. Such forces are often divided into those related to restriction in energy acquisition (e.g. food availability), in which case the population is regulated from the ‘bottom-up’, versus forces imposed from the ‘top-down’ by higher trophic levels (e.g. through consumption of the focal population by predators). The potential for top-down forces to establish ecosystem structure has become increasingly clear over time (Hairston et al. 1960, Estes et al. 2011, Ripple and Beschta 2012, Pringle et al. 2019), but the relative strengths of top-down versus bottom-up forces varies depending on the individual ecosystem and focal trophic level within it making generalizations difficult so far (Hairston et al. 1960, Hunter and Price 1992, Denno et al. 2005). Current evidence suggests that at global and regional scales, species diversity is linked closely to climate, such that areas with more available energy (warmer temperatures and greater precipitation) generally possess more species (Evans et al. 2005). But the relative importance of bottom-up versus top-down influences at local scales is less clear (Gripenberg and Roslin 2007).
Complicating matters, top-down forces such as predation, parasitism, and disease can both promote and limit diversity (Sih et al. 1985, Sinclair and Krebs 2002). The addition of predators to a community generally has a negative impact on the population size of its prey (Sih et al. 1985), which then scales up to impact prey community structure. But how this scaling works varies depending on food web structure. Over-consumption of a species can cause it to go extinct, thereby reducing diversity (Medina et al. 2011, Doherty et al. 2016). Additionally, predation may decrease coexistence by increasing competitive pressure for resources like refuges, or foraging availability in predator-free space (Hixon and Menge 1991, Pringle et al. 2019). Indeed, in some cases coexistence between multiple species is maintained in the absence of predation, but collapses when a predator is added to the system, resulting in species loss (Pringle et al. 2019).
Alternatively however, ecological theory suggests that, in some circumstances, predation can instead increase diversity (Paine 1966). By reducing population sizes of superior competitors, predators can alleviate competition between species and facilitate coexistence, thereby increasing species richness of a community (Gurevitch et al. 2000, Canter et al. 2018). Doing so often decreases the species that would otherwise be most abundant, thereby increasing evenness between prey species. In this case, total prey community abundance may either decrease or stay the same, depending on how predation directly affects the other species. On the one hand total abundance might not change if predation is focused on the dominant competitor. In such a circumstance lesser competitors can undergo compensatory population growth with the decline of the dominant competitor. However, if subordinate competitors are themselves also prey of a generalized predator, then overall prey community abundance would decline with increased predation.
In contrast to the multidirectional predictions elicited from top-down forcing on prey communities, the predictions generated from the bottom-up are relatively straight forward. In such cases, abundance and diversity would simply follow the total energy resources available in the system, as dictated by seasonal and climatological forces. If this is the case, we would see patterns where predator and prey abundance increase together, and indeed studies have often shown positive associations between the abundances of species and their prey (Fisher et al. 2002). Further, pulses of resources, such as those caused by rainfall, cascade through the food web, providing greater energy availability in the environment, and thus resulting in an increase in abundances of producers and consumers at higher trophic levels (Meserve et al. 2003, Báez et al. 2006). This work suggests that when food availability is high, consumer abundance will also be high (Guyer 1988, Wright et al. 2013, Wright et al. 2020).
Island lizards—and insular Anolis lizards particularly—provide an attractive system for asking questions about the drivers of community diversity, particularly because islands are isolated systems where communities have assembled independently and can thus be easily compared. Anoles are a highly diverse genus of neotropical arboreal lizards that have adaptively radiated on islands in the Caribbean. The larger islands of the Caribbean each harbors an evolutionarily distinct anole fauna, with members that sort ecologically into communities across various biogeographic regions of each island (Losos 2009, Frishkoff et al. 2022). But the role of predation, rather than competition or food limitation, in controlling such insular communities has beguiled ecologists for decades. Andrews (1979) initially proposed that top-down forces were of paramount importance for structuring anole communities, but only on the mainland, where predators are diverse. On the islands of the Caribbean, where predators are much less common, and anoles reach higher abundances, the supposition was that bottom-up forces dominate. This view was embraced by Wright (1981), who envisioned predation playing at best a minor role in the islands of the Caribbean, and where a dearth of avian competitors allowed high lizard abundances. However, Wright’s interpretation of island diversity was vigorously contested by Waide and Reagan (1983) who noted a strong negative correlation between predator species richness and anole abundances across Caribbean islands. This negative correlation between predator diversity and abundance of their prey is supported by Buckley and Jetz (2007) who showed that on a global scale, lizard populations on small islands are more dense than on larger islands, which in turn had denser populations than on the mainland. These trends were well explained by the number of predator species that occurred on the islands in question (although the effects of competition could not be ruled out).
Such broad-scale cross-island findings have been mirrored by population studies and experimental predator introductions on small islands in the Bahamas. In comparing islands of different sizes with different numbers of predatory birds, Schoener and Schoener (1978) found lower abundances and lower survival rates in anole populations where predators were more common, without a diminishment of body condition (as would be expected if competition were the driving mechanism). Likewise, introduction of predators on small experimental islands decreased abundance of their anole prey, and even pushed populations towards extinction (Schoener et al. 2005, Pringle et al. 2019). Nevertheless, on similar small islands in the Panama canal, Wright (1979, 1984) noted that variation in predator number seemed uncorrelated with anole survival. As a result of these conflicting findings to date there is no consensus about the relative roles of predation, competition, and resource availability in structuring anole communities. However, when links between predator occurrence and lizard abundance have been investigated, findings of both macroecological and experimental studies have generally indicated a negative correlation between the two. Further, some experimental studies suggest a plausible role for anole predators in limiting species diversity, by pushing individual species towards local extirpation.
Issues of scale, however, complicate the extension of these findings to communities more generally. Macroecological approaches typically compare estimates of lizard abundances taken at specific areas within an island to the number of predator species that occur on island-wide lists (or habitat-specific lists). As such, there is no causal link between predator number and lizard abundance, given that the full complement of predators may not occur at the specific location(s) where abundance was measured. This lack of connection in scale of observations casts some doubt on the pattern of negative correlation between predator richness and prey abundance documented in cross-island comparison studies, since larger islands will have more species (predator and otherwise) regardless of how many occupy local communities, and may also have higher lizard abundances due to some reason unrelated to predation.
In contrast, mechanistic studies on small islands (Schoener and Spiller 1996, Calsbeek and Cox 2010, Lapiedra et al. 2018, Piovia-Scott et al. 2019, Pringle et al. 2019) may not translate well to more diverse and non-bounded communities. These experimental islands’ areas are typically less than 0.2 hectares, and tend to be extremely depauperate in comparison to communities on larger islands or the mainland—that is, the types of communities where most lizards occur and interact with predators. Simplified vegetation, lack of refugia, and populations that are susceptible to stochastic extinction due to small absolute size may all make abundance declines and extirpations more likely on such islands in comparison to less severely bounded environments.
Because macroecological studies and studies restricted to very small islands are the two primary research avenues used to assess predation in anoles, our knowledge of predation’s role thus largely pertains to both very large scales (often with a mismatch in resolution of predator data and prey abundance data) and very small ones (with environmental characteristics that may be non-generalizable to non-bounded communities). What is then lacking is an understanding of the effects of predation on local diversity across large, multi-community landscapes that better exemplify the types of communities in which most organisms dwell. A finding that predator abundance negatively correlates with prey abundance across communities within islands would lend credence to top-down forcing of prey communities.
To fill this gap we use fine-scale mark-recapture data on Anolislizard communities conducted broadly across the islands of Hispaniola and Jamaica in the Caribbean. We combine this with an eBird dataset spanning 10 years to quantify predatory bird presence across these islands in order to assess questions related to top-down versus bottom-up forcing between birds and lizards. Although anoles experience predation from snakes and mammals, they are primarily preyed upon by predatory birds (Wunderle Jr. 1981, Waide and Reagan 1983, Mclaughlin and Roughgarden 1989, Poulin et al. 2001). These range from specialist species, such as lizard-cuckoos, to more generalist predators such as hawks and falcons, to opportunistic feeders such as kingbirds. We first assess whether bird and lizard communities within islands show evidence of being driven by bottom-up energy availability, such that these features of the community correlate with aspects of climate that drive total energy availability. We next ask whether top-down effects of avian predators are apparent on anole community abundance within islands, and relatedly, whether predator presence promotes or limits species diversity. If predators play a large role in structuring lizard communities as suggested by past macroecological work looking across islands, then we would expect that greater predation pressure would be associated with lower anole abundances. If such predation pressure is borne equally among prey species it could push some to local extinction, decreasing diversity. Alternatively, if predation modulates dominant competitors diversity would positively correlate with predation pressure, and prey community evenness would increase.