INTRODUCTION
The coexistence between species with similar ecological niches is
allowed by the partitioning of the niche requirements between the
species involved, being the spatial, dietary, and temporal dimensions
the most common mechanisms of segregation (Schoener 1974). Temporal
partitioning is more common among predators, since their prey shows
peaks of activity, unlike herbivores, where plants and its parts can be
found at any time (Schoener 1974). Temporal partitioning is especially
important for large carnivore mammals, as they have large body-mass and,
therefore, larger home ranges (Lindstedt et al. 1986), which do not
allow for spatial partitioning in the current scenario of tropical
forest depletion worldwide (Keenan et al. 2015). In this scenario,
dietary partitioning is also unlikely, since smaller remnants support
fewer species (Pardini et al. 2005; Cáceres et al. 2014) that could be a
potential prey for medium- to large-sized carnivores. Therefore,
temporal partitioning might be an important strategy for the coexistence
between large carnivores in the current forest remnants.
The lack of an efficient niche partitioning between carnivores can lead
to an Intraguild Predation (IGP) or Interspecific Killing (IK; Polis et
al. 1989). IGP occurs when the dominant predator kills and eats the
subordinate predator that uses similar resources, thus reducing
competition, whereas IK occurs when the dominant predator kills the
subordinate predator without any immediate energy gain to the dominant
predator (Polis et al. 1989). The species with the highest body-mass is
the dominant predator on the IGP/IK relationships and the smaller (and
subordinate) predators are directly affected, a phenomenon that can
directly influence the community structures (Polis et al. 1989) and may
even result in local species extinction.
To avoid competition, subordinate predators can change their temporal
activity, diet, and habitat use according to the specific conditions of
each location at each time. This is possible because the niche of the
subordinate predator is generally broader than the niche of the dominant
predator, which is embedded into the niche of former species (Polis et
al. 1989). However, few cases of complete inversion in the activity
pattern were reported among mammals, perhaps because of the phylogenetic
constrain of species, as observed in rodents by Roll et al .
(2006). Usually, changes in the temporal activity or its limitation that
acts as a response to the predation risks, thus reducing forage and
energy gain by the subordinate competitor (Kronfeld-Schor and Dayan
2003).
The Atlantic Forest is an excellent biome for studying temporal
partitioning between predators. It was greatly reduced and fragmented in
the last decades, with few remaining areas of continuous native forest,
and is currently composed primarily by fragments with less than 50 ha
(Ribeiro et al. 2009). Among other smaller predators, there are two
species of large predators that inhabit the Atlantic Forest: the jaguar
(Panthera onca ) and the puma (Puma concolor ). Jaguars lost
most of its historical distribution (Tôrres et al. 2008), but they are
still present in some large Atlantic Forest remnants, while pumas have a
broader current distribution in the biome (Beisiegel et al. 2012).
Most studies with these two large felids found great similarities
between their activity patterns, as in Argentina (Di Bitetti et
al . 2010), Belize (Harmsen et al . 2009; Harmsen et al .
2011), Brazil (Gómez et al . 2005; Foster et al . 2013),
Mexico (Núñez et al . 2002), and Venezuela (Scognamillo et
al . 2003). Conversely, there were no significant differences between
their activity patterns in some cases (Romero-Muñoz et al . 2010;
Blake et al . 2012). Usually, the temporal partitioning between
jaguars and pumas was either associated with species avoidance
(Romero-Muñoz et al . 2010) or activity synchronization with their
main prey (Blake et al . 2012).
The temporal activity pattern of jaguars and pumas can also be
influenced by the environment characteristics. Paviolo et al .
(2009) found the higher nocturnal activity of pumas in areas where hunt
pressure was higher in comparison with more protected areas, which might
be a strategy to avoid conflict with humans, as also observed with other
predators (Schuette et al. 2013; Massara et al. 2018). The temporal
activity of predators may also be influenced by the temporal activity of
their preys. The relationship between the temporal activity of predators
and their prey might be linked either to the predation risk of the prey,
or an alignment of the predator temporal activity to the activity peaks
of their prey, which is related to coevolution strategies
(Kronfeld-Schor and Dayan 2003). The synchronization with the temporal
activity of preys is advantageous for predators since they can optimize
its energy use foraging in a day period when their preys are more
active.
There are several studies of temporal partitioning between other
terrestrial carnivore mammals in the Neotropics with variated results
(Di Bitetti et al. 2009; Massara et al. 2016; Ramírez-Mejía and Sánchez
2016), especially on ocelots (Leopardus pardalis ) and other
smaller felids (Lucherini et al. 2009; Blake et al 2012; Massara et al.
2018; Santos et al. 2019). The temporal activity pattern of these
smaller carnivores depended mainly on their habitat characteristics
(i.e., prey availability and human disturbance level) and the presence
of potential competitors.
We aimed to evaluate whether the coexistence of terrestrial mammal
carnivores may be facilitated by temporal partitioning in an isolated
Atlantic Forest remnant. We expected jaguars, the largest predator, to
influence the activity patterns of all other predators, which may
temporally segregate with jaguars to avoid IGP or IK. We also expected
the same strategy for all the remaining predator relationships, where
dominant predators may influence the temporal activity of the
subordinate predators. Since some predators are naturally diurnal, we
expected them to segregate temporally with nocturnal predators. We also
expected nocturnal predators to be mostly or exclusively nocturnal in
human-related locations, as a more nocturnal activity reduces the
chances of encounters with humans that are usually more active during
the daylight. Lastly, because differences in the temporal activity
patterns are not necessarily relate with competition strategies to avoid
dominant predators, we also evaluated whether the temporal activity of
predators could be a strategy to maximize their chances to find
potential preys, as observed by several studies with neotropical felids
(Harmsen et al . 2011; Foster et al . 2013; Nagy-Reiset al . 2019).