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.