LINKED PAPER
Long-term change in the avifauna of undisturbed Amazonian rainforest: ground-foraging birds disappear and the baseline shifts. Stouffer, P.C., Jirinec, V., Rutt, C.L., Bierregaard, R.O., Hernández‐Palma, A., Johnson, E.I., Midway, S.R., Powell, L.L., Wolfe, J.D., Lovejoy, T.E. Ecology Letters. DOI: 10.1111/ele.13628 VIEW

Few places drew me more than Amazonia—a place synonymous with adventure, where shadowy forests teeming with outlandish wildlife spread over an area the size of Australia. When I began undergraduate studies in 2004, partaking in Amazonian research was a pipe dream I was closest to when leafing through yellowed pages of library field guides and peering at the striking Ara macaws and Tangara tanagers—in my mind the avian emblems of the world’s largest rainforest.

But fast forward a decade, and I was about to start my PhD in the lab of Phil Stouffer. Phil was spearheading ornithological research at the Biological Dynamics of Forest Fragments Project (BDFFP) just north of the Brazilian city Manaus, in central Amazonia. The project was established in 1979 by Tom Lovejoy and Rob Bierregaard to study the effects of forest fragmentation on rainforest biota, but has since broadened its scope to become a nexus of research on Amazonian biology. Phil, after 30 years of ringing birds at the BDFFP, was about to pass the bird project to another principal investigator, and I was slated to be his last grad student to work with birds in fragments. Phil’s US National Science Foundation grant—one that also funded me—has recently paid for cutting around fragments that were largely reclaimed by the surrounding forest. We were about to examine how bird communities changed following re-isolation.

However, soon the flipside of international work became apparent: permits. The slow-turning wheels of Brazilian bureaucracy were recently further hampered by changes to requirements for foreign researchers. Waiting for the obligatory VITEM I visa, I missed my 2015 field season, and then the one in 2016. Fragments were swallowed once again by vigorous regrowth, and I was forced to rethink my dissertation.

Many students in my situation would be despondent (and I was), but I also had the benefit of sitting on a pile of 70,000 bird captures extracted from BDFFP mist-nets over nearly four decades. These birds were ringed in fragments, secondary forest, as well as in pristine, continuous forest which acted as the control for fragmentation research. The dataset provides a window into bird status that is unparalleled in Amazonia, and Phil encouraged his grad students to take advantage of this trove, offering project ideas that emerged over the years. While waiting for my visa paperwork to come through, I was especially receptive to these suggestions.

One proposition that Phil mentioned during our weekly meetings was especially intriguing. Drawing on his perspective moulded by 30 years of birding at the BDFFP, Phil noticed that some birds were now nearly impossible to encounter even far from human disturbance. Despite the “fragments” part, the BDFFP area remained >90% forested throughout the years (Rutt et al. 2019), leaving plenty of real estate for birds who fare poorly in small forest patches (Stouffer 2020). The recognition that some birds might be declining within intact forest first transpired in 2008 when Erik Johnson, now the director of bird conservation at Audubon Louisiana but then a grad student eager to see Amazonian birds, was unable to spot some species like the Wing-banded Antbird (Myrmornis torquata) despite living in the forest for months. Rufous-bellied Antwren (Isleria guttata)—another once-reliable bird—was also nowhere to be seen. Phil recalled that he regularly encountered these species in the “old days”.

Figure 1 Above the rainforest canopy at the BDFFP. © Vitek Jirinec

With the prospect to search for Myrmornis myself uncertain, I took on Phil’s proposal and together we compiled bird captures throughout the years within continuous, primary forest at the BDFFP. We ended up with two sensible groups for comparison: a historical primary sample (early 1980s) and modern primary sample (2008+). When the initial analysis was complete, the results were striking: compared to the old days, many birds were much less common in the modern sample. Furthermore, the identity of those declines was remarkable—the disappearing species were not a random draw from the community, but rather they clustered by their ecological foraging guilds. The hardest-hit species were insectivorous birds which feed on or near the ground (terrestrial insectivores and near-ground insectivores)—the same sensitive birds that plummet in fragments shortly after isolation (Stouffer 2020). We knew then we had an important story to tell, but we needed to develop the paper more. To that end, we recruited Cameron Rutt—Phil’s previous grad student who just returned (looking a bit haggard) from living at the BDFFP for 15 months to offset his own visa delays, and Steve Midway—an analysis polymath at LSU. We added more data and complexity to the study and reanalysed the captures with more robust models.

Figure 2 Study concept. With the primary forest changing, controls in modern forest will yield weaker effects than if comparisons were made with historical baselines.

The conclusions held—terrestrial and near-ground insectivores have declined in what should be pristine forest. Myrmornis dropped to about 40% of captures in the 1980s, Musician Wren (Cyphorhinus arada) to 41%, Wing-banded Wren (Microcerculus bambla) to 27%, and the Rufous-bellied Antwren to 17%. The Black-tailed Leaftosser (Sclerurus caudacutus) numbers fell to 12% and the species occurred now at only a fifth of sites it occupied in the 80s. Additionally, we showed that if researchers accounted for this temporal change (a “baseline shift”) in their studies of landscape effects in modern forests, the absolute change they would see would be even greater. In other words, comparing modern fragments to historical undisturbed forest—as opposed to comparisons with modern undisturbed forest—would show fragments to be even more barren.

Figure 3 Musician Wren (Cyphorhinus arada) is one of several ground-foraging birds that are disappearing from what should be intact forest. © Vitek Jirinec

Considering all this, the modern forest might not deserve the label “undisturbed”. Something insidious seems to be driving down sensitive species, leaving the rainforest more and more depauperate. We cannot say for certain why this is happening, but the first suspect—and one that is emerging in our more recent work—is climate change, a force to which even the vast forests of Amazonia are not immune. If this is the case, slash and burn deforestation for which we often blame the locals is not the only threat to Amazonia. Individual choices of people half a world away likely also play a role in the degradation of the world’s largest rainforest.

Figure 4 Bruna Amaral, a BDFFP ornithologist, requires additional light when processing a bird in the dark understory of primary rainforest. © Vitek Jirinec

I did eventually get to work at the BDFFP. I also saw more than one Myrmornis, although that took a lot of effort. On the other hand, I regularly spotted Ara macaws and Tangara tanagers flying over Manaus—a city of two million people. Now I understand the real avian emblems of Amazonia are Sclerurus, Myrmornis, Isleria, and other nondescript birds of the shady forest floor. But these are vanishing and the high biodiversity of Amazonia fades with them.

References

The Guardian 2020. Nine insect-eating bird species in Amazon in sharp decline, scientists find. VIEW
Rutt, C.L., Jirinec, V., Cohn‐Haft, M., Laurance, W.F. & Stouffer, P.C. 2019. Avian ecological succession in the Amazon: a long-term case study following experimental deforestation Ecology and Evolution 9:13850–13861. VIEW
Stouffer, P.C. 2020. Birds in fragmented Amazonian rainforest: lessons from 40 years at the Biological Dynamics of Forest Fragments Project. The Condor 122. VIEW
Mongabay 2021. Patches of Amazon untouched by humans still feel impact of climate change. VIEW

Image credit

Top right: Wing-banded Antbird Myrmornis torquata © Vitek Jirinec

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