Discussion
Over a period of 36 years, our results indicated few changes to the
overall bird community with respect to species abundances or point alpha
diversity, although we did observe a decline in overall community
biomass. We find these results somewhat surprising considering the plot
is located in mature floodplain forest bordering a dynamic whitewater
river. For example, in spite of large shifts of the Manu River, there
were few changes to species associated with primary successional
habitat. Our findings, contrary to other studies in similar locations
throughout the Neotropics, suggest that community dynamics and
composition in this area are mostly determined by local processes, and
that neither local nor regional environmental changes have affected the
majority of the bird community. Perhaps most remarkable is the stability
in the insectivore community, excepting canopy flocks. Given extensive
documentation of the sensitivity of insectivores to forest disturbance
and fragmentation, it is somewhat surprising that a group that responds
precipitously to perturbations(Blake & Loiselle 2015; Stouffer et
al. 2020) shows such little natural variation in undisturbed forest.
In spite of the striking similarity in community composition between the
two time periods, we did find changes in some species’ abundances. We
found a drastic decrease in Cacicus cela, likely stemming from a
loss of a single nesting tree, a decrease in canopy flocks (Fig. 3), and
a significant decrease in some bamboo specialists consistent with the
complete disappearance of bamboo in the plot after a flowering event
circa 2001. One guild that showed a decline in abundance (nectivores)
had low sample sizes that led to large variance in model estimations of
their abundance. Granivores also showed declines; however, as many of
these (e.g., parrots) cue in on patchy ephemeral resources, we speculate
that this may be driven by stochastic fluctuations in local resources
(e.g., parrots often respond to seasonal changes in fruiting activity on
scales much larger than the plot), whereas others (i.e.,Odontophorus stellatus ) may be due to inadequate sampling of
group sizes. Some ground dwelling granivores show large scale
fluctuations that may be susceptible to nest predation by white-lipped
peccaries although this species was absent during both the 1982 and 2018
census periods (Terborgh et al. 1990). The fact that we
identified other outlier species when evaluating changes in abundance
between the two time periods within ecological guilds merits further
exploration, and may be targets for future population dynamics studies.
The strong 1:1 relation between the overall abundances then and now (see
Fig. 2A) was not mirrored in biomass. Indeed, after correcting for
phylogeny, the biomass totals per species between the two time periods
showed a less than 1:1 relationship. Bird species in the lower
biomass-per-individual quantiles decreased in abundance, whereas bird
species in the upper-biomass-per individual quantiles increased in
abundance (Fig. 2B). Additionally, we speculate that some of the small
differences in group size estimates for larger species can lead to
substantially different biomass estimates. For example, there was a
particularly large decline in Cacicus cela . Overall, our results
could also suggest possible changes to some habitats as drivers for the
few observed changes.
A curious contrast appears in the apparent differences between
understory and canopy flocks. Previous research has documented the
unique interdependence of these permanent associations, which would
suggest that the assemblage of species in these flocks would experience
similar trajectories of growth or decline (Munn & Terborgh 1979).
Although there is not a clear explanation for the decline in canopy
flock densities, this decline is rather strong (see Fig. 3). Because
more fruits are found in the canopy, shifts in phenology and the
dependent arthropod assemblage therein, may have a greater effect on the
omnivores, frugivores and insectivores common to canopy flocks. On a
regional scale, there is evidence suggesting vegetation in the canopy
may be sensitive to changes in precipitation patterns (Hilker et
al. 2014) and that southern Amazonia has experienced a lengthened dry
season since 2000 (Marengo et al. 2018). Interpolated
precipitation patterns, however, do not seem to have changed in Cocha
Cashu during the last 30 years (Fig. S8) (Aybar et al. 2017).
Furthermore, the extent to which canopy birds are affected by changes in
canopy tree fruiting phenology at the local level at Cocha Cashu is
unknown. Evaluating changes in forest phenology would help us evaluate
this mechanism as a potential driver of change to canopy species.
Studies in other lowland tropical sites showed marked changes to
specific groups in terms of abundances. Blake and Loiselle report long
term declines for multiple guilds of understory species over
~ 8-year period from a remote site in Ecuador (Blake &
Loiselle 2015). In the absence of any anthropogenic impact, changing
regional precipitation events are one of the remaining plausible
explanations. Consistent with the results of Blake and Loiselle (2015),
declines in several species over 20 years have been confirmed from a
remote forest plot in Panama (Brawn et al. 2017). This lowland
forest plot has also experienced little to no direct human impact but
has undergone species declines related to prolonged seasons of low
precipitation. More recently, the same research team has used long-term
mist-net data for a larger group of species and found consistent
declines in capture rates across the majority of bird species (Pollock
et al. unpublished data). In Central Brazil, terrestrial insectivores
have steadily declined from undisturbed forests, partially driving the
overall shift of the community from a historical baseline (Stoufferet al. 2020).
Human impacts notwithstanding, we find it surprising that the Cocha
Cashu site shows little change overall compared to other locally
unaffected tierra firme forest plots, given that Cocha Cashu is a mature
floodplain plot that experiences succession due to changes in the course
of the Manu River. Data on long-term regional environmental variation
(i.e., precipitation patterns) at the Cocha Cashu site do not show
strong consistent changes that would influence community composition
(Figure S8) (Aybar et al. 2017). Given the observed bird
community declines in other Neotropical sites that are attributed to
changes in rainfall patterns, bird communities experiencing little to no
change, such as those in Cocha Cashu, may be good candidates for
biodiversity refugia in the face of such global change (Guisan et
al. 2013; Morelli et al. 2020).
Unfortunately, because our sampling focused on a snapshot of the
ecological process in two time periods, we were not able to evaluate the
role of random year-to-year variation on community stabililty/resilience
per-se. Given the small changes we found in abundance and territory
distribution, however, we predict that these communities are composed of
species with low population variability and thus collectively, are in
fact stable (sensu ecological theory) (MacArthur 1955; Ives & Carpenter
2007). Long-term temporal population variability has previously been
demonstrated for specific components of insectivorous bird communities
in several locations. Loiselle and Blake (1992), for example, suggested
that community dynamics of Neotropical bird communities are likely
guild-dependent, with insectivores showing much less population
variability over time compared to frugivores. However, our data extend
beyond specific groups of insectivorous birds and show some level of
constancy across a far larger percentage of the community irrespective
of guild or functional traits.
Ultimately, we cannot speak to the mechanistic processes driving the
similarity in community structure that we observed. Evaluating subtle
changes to forest structure will be critical in understanding whether
the bird community is 1) resilient to local or regional environmental
change, or 2) whether overall changes to the forest have been so small
that they translate into small effects on the bird community. The first
two scenarios would underscore different aspects of community stability
that maintain community equilibrium (Ives et al. 2003; Ives &
Carpenter 2007). Understanding the likelihood of each these scenarios is
critical for understanding how resilient tropical bird communities are
to natural environmental dynamics and will allow us to decouple the
effects of local processes from those of larger regional scale
processes, including those linked to climate change.
A major limitation of our study compared to the approaches of the
studies mentioned above is our lack of time-series data (Ives et
al. 2003; Robinson & Curtis 2020). No effort has been focused on
evaluating bird communities at regular time intervals in Cocha Cashu
between the two time periods. This lack of continuity and time-series
data-gathering reflects funding challenges for complex, large scale
censuses at this remote locale. However, the intense behavior
observation efforts that we carried out may allow us to design new
analytical approaches that efficiently combine a diverse array of
sampling techniques that will hopefully allow for longer-term
sustainable sampling of neotropical bird communities (Toms et al.2006; Gomez et al. 2018). For example, it is well-known that
point count techniques yield largely unreliable density estimates of
rarer species in hyper-diverse bird communities (Robinson et al.2018), yet this problem is now largely surmountable if point counts are
coupled with behavioral field observations thanks to the recent
development of large families of statistical models (Sauer & Link 2002;
Yamaura et al. 2012, 2016; Gomez et al. 2018). Combining
geo-referencing of the movement and territory occupancy in obligatory
understory flocking species with the spot-mapped territories allowed us
to calibrate the density estimates obtained from additional point counts
that we carried in the same year, and we found a surprising degree of
accuracy among the two techniques (unpublished data). We suggest that
using supplementary visual group size data to estimate group means for
monospecific flocking species, which are normally excluded from point
count estimates, would permit a larger percentage of species to be
tracked with point counts than previously thought possible. These
combined methodologies, together with the increasing availability of
inexpensive data loggers, automatic recorders and camera traps, allows
for far more financially feasible rapid efficient sustainable sampling
(Burton et al. 2015; Shonfield & Bayne 2017). For future
fieldwork efforts here and elsewhere, we strongly advocate for a more
intimate design and combination of field and statistical sampling
techniques in situ by inter-disciplinary teams.
In contrast to most similar studies, which have found profound impacts
of climate change on Neotropical bird communities, we report few
significant abundance changes in most bird species in this hyper-diverse
community. This pattern of little change seems to be a peculiarity of
our sampling study; however, to date there is no easy way to directly
compare currently available data in order to understand
continental-scale biodiversity changes.
The region of Madre de Dios within which Manu National Park is situated
is facing ever-mounting pressure from extractive industries and road
construction to increase commerce between Brazil and Peru. Given the
current focus on determining and predicting refugia in the face of
future environmental change, our results suggest that the consequences
of development around such sites should be another consideration among
stakeholders within the region.