Birds trapped in mist nets killed by opportunistic predators in a forest in Southwestern Amazonia

The use of mist nets is a highly used method among researchers due to their efficiency in capture birds and bats. However, trapped animals are vulnerable to predator action. During three ornithological studies carried out in a forest fragment from southwest Amazonia, we recorded 15 predation events, with predation rate of 1.5%. Among predators, 26.7% (n = 4) of the cases were related to primates, 13.3% (n = 2) related to army ants, 13.3% (n = 2) related to an unidentified hawk species and in 46.7% (n = 7) of the cases the predators did not identified. Preventing predator access to mist nets and reducing network monitoring time are some of the measures that can prevent these events.


INTRODUCTION
Mist nets are tools used mainly in research involving birds and bats. The efficiency of mist nets in capturing these animals makes them one of the most used tools in avifauna and chiropterofauna studies (Roos, 2010;Castro et al., 2011;Ruiz-Esparza, 2012). Although effective for research, these traps have a side effect that is the exposure of animals trapped to predation risk (Hilário et al., 2017).
Predations on mist nets are not so often reported, as being unusual to happen (Ruiz-Esparza, 2012). However, a large number of predators such as primates (Melo et al., 2018), birds of prey (Legal et al., 2018), army ants (Ross, 2010) snakes and even bees and wasps (E. Guilherme, pers. obs.) become opportunistic predators when they encounter an animal trapped in a mist net. Therefore, birds caught with mist nets are quite vulnerable to predator attacks (Roos, 2010). Some actions suggested by the Brazilian Guideline for the Care and Use of Animals in Teaching or Scientific Research Activities (DBCA,

Diretriz Brasileira para o Cuidado e a Utilização de Animais em Atividades de Ensino ou de Pesquisa
Científica) can reduce this vulnerability, such as the correct use of capture techniques, the time that animals will be trapped and the training of researchers in relation to capture techniques (DBCA, 2016).
Here we describe cases of bird predations trapped in mist nets during three ornithological studies in a forest fragment from southwest Amazonia.
We conducted the study in the Humaitá Forest Reserve (HFR), that is a forest fragment located in the eastern state of Acre, southwest of the Brazilian Amazon. This fragment has approximately 2,000 ha and is predominantly covered by open forest dominated by bamboo (Guadua weberbaueri Pilg.) or palm trees, on terra firme and floodplain (várzea) soils (Barroso et al., 2011). The HFR has a very diverse avifauna with 356 confirmed species (Pedroza et al., 2020).
This report is the result of a compilation made from captures with mist nets during three different ornithological surveys conducted at HFR. We sampled birds from April to December 2018. We used a total of 18 mist nets of 12 × 2.5 m and 36 mm mesh. We opened the mist nets around 6:00 am until 16:00 pm, totaling 9,750 hours/net. We checked the mist nets at 30 min intervals. Once captured, each individual was banded on one tarsus with a permanent, numbered aluminum ring provided by the Brazilian National Center for the Conservation of Wild Birds (CEMAVE/ICMBio) for use in project 1099, coordinated by Edson Guilherme. We identified predators visually as we approached the mist nets for checking. Some predators such as primates or birds of prey were identified as they abandoned the bird carcass in the mist net as they perceived our approach. Predation rates were calculated considering the number of predations * 100 / total number of captures. Specimens were captured under ICMBio/SISBIO authorization nº 23269-1 and ringed with permission of the Center for the Conservation of Wild We captured 1063 birds during the HFR studies. We recorded 15 predation events affecting individuals of nine bird species, with the predation rate of 1.5%. In four predation events it was not possible to identify the bird species that was preyed (Table 1). Among predators, 26.7% (n = 4) of the cases were related to Toppin's titi monkey -Plecturocebus toppini ( Figure 1A); 13.3% (n = 2) related to army ants of the species Eciton burchellii ( Figure 1B); 13.3% (n = 2) related to an unidentified hawks and 46.7% (n = 7) of the cases we did not identify predators (Table 1). Birds killed by predation almost always had lacerations, abrasions, perforations in the ventral and / or cranial regions, with viscera exposures ( Figure   2).   The predation rate obtained in HFR was less than 2% which is the acceptable limit in scientific research developed with mist nets (Ralph et al., 1993). The predation rate in HFR was slightly above that recorded in two areas where ornithological studies with mist nets were developed in the Atlantic forest in the state of São Paulo, which presented 1.17% and 1.20% respectively (Melo et al., 2018) and below that recorded in an area of Caatinga in the state of Sergipe where a predation rate of 1.8% was recorded (Ruiz-Esparza, 2012). All birds cited in this study were reported for the first time as predated in mist nets.
Although we did not observe the predators in eight events, we believe that the responsible for the bird deaths in the mist nets were Toppin's titi monkey and White-fronted capuchin -Cebus albifrons. This conclusion is supported by the markings left on the carcasses and also by the fact that mist nets are within the territory of these species on the days the birds were preyed. Several studies reported primates as the main predators of birds trapped in mist nets (Silva et al., 2008;Hilário & Ferrari, 2010;Hilário et al., 2017;Melo et al., 2018). However, we report for the first time the species Toppin's titi monkey -Plecturocebus toppini preying on birds trapped in the mist nets. Due to their high mobility, adult birds are not part of the primate diet (Hilário & Ferrari, 2010). However, birds immobilized in mist nets become easy prey for primates that are attracted due to the birds' alarm vocalizations (Ross, 2010). One recommendation for decreasing primate predation is to avoid primate access to mist nets (Hilário et al., 2017). Primates may have access to prey by branches close to nets, so cutting these branches is an easy and simple way to avoid predation by this group of animals (Hilário et al., 2017).
Birds of prey (mainly hawks) are another group of vertebrates that prey on birds caught in mist nets (Freer, 1978;Komar, 2003;Curcino et al., 2009;Legal et al., 2018;Melo et al., 2018). These predatory birds realize that the nets immobilize the birds and, therefore, are under observation nearby, waiting for the moment of attack (Roos, 2010). In these situations it is necessary to temporarily close the networks or exchange them to another location (Roos, 2010).
Other predators may also be attracted to mist nets such as deer (Allan, 1978), spiders (Carvalho et al., 2016), praying mantis (Nyffeler et al., 2017) and ants (Ross, 2010;Bichinski, 2015). Ant predation is related to birds caught near ground level that are vulnerable to attack, so we need to avoid arming nets near anthills (Ross, 2010). Army ants of the species Eciton burchellii form swarm that sweep across the forest floor and surrounding vegetation. Therefore, you need to be aware of mist nets when army ants swarms are passing because they can climb onto the rods and reach the mesh of the nets where a bird may be trapped, as was the case in HFR ( Figure 1B). In our case, the army ants attack on one Black-spotted Bare-eye -Phlegopsis nigromaculata ( Figure 1B) and one on Black-banded Woodcreeper -Dendrocolaptes picumnus occurred very quickly in the interval between mist nets checks.