DISCUSSION
Occupancy values varied across species and landscapes, however a clear
pattern emerged when comparing mammal species shared between the two
landscapes, that larger species have a higher occupancy in the OL while
smaller species have a higher one in the MML. The few previous studies
in these regions agree with these results. Gómez et al., (2016) found
high levels (>0.55) of occupancy for ungulates (tapirs and
both species of peccaries) in the eastern highland savannas of El
Tuparro National Park; while Boron et al., (2019) reported occupancy
levels even lower than the ones reported here (<0.30) for
smaller mammals (Cuniculus, Dasypus, Eira) in a human-modified landscape
in the Middle Magdalena Valley. No studies however, had compared the
same species across landscapes.
While differences in occupancy values between landscapes for a same
species could be expected naturally (different ecosystems and context),
the pattern of size-related occupancy suggests that human modification
of the landscape is a determining factor. Populations of larger species
like tapirs, pumas and giant ant-eaters have been reduced in the Middle
Magdalena modified ecosystems. Larger mammals tend to be more affected
by deforestation and human pressures like hunting, as they require
larger areas of habitat and are more susceptible to hunting (Chichorro
et al., 2019; Forero-Medina et al., 2009; Ripple et al., 2017). On the
other hand, smaller, common species (not endemic, small-ranged), and
especially rodents, habitat generalists with high reproductive rate, may
become more abundant at sites with substantial human use (Dias et al.,
2019; Gibb et al., 2020). Such is the case for Cuniculus ,Dasyprocta and Dasypus , in the MML.
Both natural and human-mediated factors influenced occupancy of species
in the two landscapes. However, in the less modified areas of the OL,
mostly natural factors, such as area of flooded grassland, area of
different types of forests and distance to water bodies were
determinant, both for unique species and for species shared with the
MML. Only two species in the OL were influenced by distance to human
settlements, the puma and the tapir. On the other hand, in the more
disturbed MML, ten out of the thirteen species were influenced by
anthropic factors determining occupancy, such as distance to human
settlements and the area of artificial land cover types. The area of
forest was also an important factor in this landscape. Most notably, all
shared species except the puma and tapir (same variable opposite
effect), were influenced by a different factor in each landscape,
usually moving from an anthropic factor in the MML to a natural factor
in the OL.
These differences could highlight how in the more modified landscape,
where forests are now represented by small, fragmented patches
surrounded by crops and other agricultural land cover types,
human-mediated factors have a stronger influence on the presence or
absence of some terrestrial birds and mammals. This effect can be
negative or positive, with some species apparently thriving in more
disturbed conditions, while others avoiding them. Previous studies in
tropical ecosystems have shown how many species of mammals and other
game vertebrates are affected by human activities, like hunting, and
therefore their abundance or occupancy increases away from human
settlements or in no-hunting areas (Cavada et al., 2019; Nuñez-Iturri et
al., 2008). On the other hand, some species of rodents and small mammals
can benefit from such changes in the landscape, being favored by human
settlements, through the increase in open areas, water reservoirs and
food availability from garbage or agriculture (Fedriani et al., 2001;
Mendelssohn & Yom-Tov, 1999; Oro et al., 2013). Species of Dasyprocta,
Cuniculus and Pecari have been reported as some of the main consumers of
human-cultivated plants (crop raiders) in the Amazon (Abrahams et al.,
2018), and armadillos have been reported to consume arthropods
associated with cultivated lands (Gallo et al., 2019). In the MML, these
rodent species and armadillos are increasing their occupancy closer to
human settlements or in open, disturbed areas, perhaps as a consequence
of the presence of crops; however, these same species in the OL, are
more influenced by natural variables like distance to water, and area of
riverine forests. In a less disturbed site (like the OL) natural factors
become more important.
Understanding the effects of natural and anthropic variables in
vertebrate occupancy in these two sites is further complicated by
inter-specific interactions (Table 1). Species can interact directly or
indirectly, through competition, mutualism and trophic relations, all of
which can be mediated by other variables. In the MML, all interactions
found were positive, and were influenced by the distance to human
settlements, while in OL species interactions were mediated by natural
factors.
We did not find evidence of exclusion between Cuniculus andDasyprocta, two rodents of similar size. In the MML there were no
interactions between them and in OL the occupancy of each species was
higher in the presence of the other. However, in the MMLDasyprocta occupancy was positively correlated with the presence
of Puma and Jaguar, which in turn were positively correlated with the
presence of Cuniculus , one of their preferred prey (Ávila-Nájera
et al., 2018; Gutiérrez-González & López-González, 2017; Novack et al.,
2005), raising the question of a potential competition release between
the rodents by these predators, who could be reducing the abundance of
Cuniculus (not eliminating it), favoring the presence ofDasyprocta and explaining its higher occupancy in the presence of
the predators. Curiously, the relationship between Puma andDasyproct a is inverted in the OL, where the interaction becomes
negative in both directions. This could be related to the fact that the
occupancy of both Dasyprocta and Cuniculus is much lower in the OL,
therefore there may not be competition release by the predators but
instead Dasyprocta avoids sites occupied by Puma because without
Cuniculus it also becomes a common prey. While specific experimental
designs would be necessary to test these hypothesis, results clearly
indicate how species interactions may vary from landscape to landscape
as a result of interactions with other species and the influence of
environmental or human-mediated variables.
Both Puma and jaguar occupancy was influenced by distance to human
settlements, with both preferring higher distances away from humans in
the MML, which has less remnant forest and more human-predator conflict,
while the Puma was closer to humans in the OL, where there is less
conflict with predators and less human density. There was no exclusive
interaction between these two predators in the MML, on the contrary, the
occupancy of each species was higher in the presence of the other. This
is not rare and has been documented before (Scognamillo et al., 2003),
and could be related to the fact that although their diets can be
somehow different in a well-preserved ecosystem, in a disturbed site
like the MML predators will necessarily have to occupy the few forest
remnants, where habitat and preys are available.
In the MML occupancy of predators and prey presented opposing
relationships with distance to human settlements. Apparently prey
species are favored by the heterogeneity created by human activities,
while the felids like jaguar and puma tend to distance from these areas,
perhaps as a consequence of conflict killings. This indicates a spatial
segregation, mediated by human presence, between predators and preys in
this study, a pattern that has been reported before in temperate systems
(Dorresteijn et al., 2015; Muhly et al., 2011). In natural systems, prey
species like Cuniculus and Dasyprocta prefer dense forests
and are influenced by water bodies, to escape from predators (Goulart et
al., 2009; Péres, 1992), just as it was observed for the OL, where these
variables affected their occupancy and mediated their co-occurrence
patterns with Puma.
Despite the limitations of extrapolating a local study to broader
taxonomic and geographic categories and regions, our work presents a
contribution to the understanding of the way in which human activities
impact species and the way they interact with each other in these
tropical landscapes. Considering the characteristics of the MML, it is
hard to isolate the effects of the different human activities, habitat
loss, fragmentation, hunting, subsidies for certain species (food,
garbage, etc). However, this work clearly shows that although the
effects are not simple and in the same direction across all species,
humans play a key role in the structuring of vertebrate communities.
Although species richness is similar between the two studied areas, the
probability of occupancy of species is very different, generalist
species present higher occupancy values in the MML, but lower
interactions with predators. These changes, coupled to the low occupancy
of large seed disperses like the tapir and active seed predators like
the peccaries, can result in significant changes in the structure and
composition of the vegetation and the ecosystems (Terborgh et al.,
2008). In this sense, understanding such changes in vertebrate
occupancy, both positive and negative, and the factors that cause them,
should be a key question to inform conservation and restoration
initiatives for vertebrate species and their habitat.