Local Extinctions of Terrestrial Insectivorous Birds in a Fragmented Landscape near Manaus, Brazil

“…leaf bryophytes (Zartman, 2003), tree seedlings (Benítez-Malvido and Martinez-Ramos, 2003a), palms (Scariot, 1999), understory insec-tivorous birds (Stratford and Stouffer, 1999; Ferraz et al., 2007), primates (Gilbert and Setz, 2001; Boyle and Smith, 2010a), and larger herbivorous mammals (Timo,…”

“Stratford and Stouffer (1999) support their list with 12 references to specific, well-documented cases.”

“Connectivity and patch size are important parameters for the persistence of species in fragmented landscapes (Karr, 1982; Blake and Karr, 1987; Bierregaard and Stouffer, 1997; Stratford and Stouffer, 1999; Crooks et al., 2000).”

“…as the Black-faced Anthrush (Formicarius analis) and Ringed Antpipit (Corythopis torquatus) were uncommon in connected and absent in unconnected corridors, perhaps due to terrestrial mammal overabundance resulting in increased rates of nest predation for these species (Stratford & Stouffer 1999).”

“…are thought to hinder understory bird movements (Laurance 2004), and terrestrial insectivores – the most dispersal-limited guild in our study – are disproportionately likely to become locally extinct in isolated forest patches (Robinson 1999; Stratford & Stouffer 1999; Sekercioglu et al. 2002).”

“These species often decline in abundance near forest edges, avoid clearings (S. G. W. Laurance 2001), and are highly vulnerable to forest fragmentation (Bierregaard & Lovejoy 1989; Stouffer & Bierregaard 1995; Stratford & Stouffer 1999).”

“…leaf bryophytes (Zartman, 2003), tree seedlings (Benítez-Malvido & Martinez-Ramos, 2003b), palms (Scariot, 1999), understorey insectivorous birds (Stratford & Stouffer, 1999; Ferraz et al., 2007), bats (Sampaio, 2000; Rocha et al., 2017), primates (Gilbert & Setz, 2001; Boyle & Smith, 2010b) and…”

“These species are flock-leaders of understorey mixed-species flocks, a guild of species considered to be particularly fragmentation-sensitive (Stratford and Stouffer 1999, Laurance et al. 2004, Laurance and Gomez 2005).”

“We studied flocks along the ZF-3, an unpaved road that bisects the site from west to east (seen in a satellite image given by Stratford and Stouffer 1999).”

“Here, we focus on the issue of land-use policies, especially on the ecological relationship between natural areas and the surrounding agricultural matrix.”

“5: species significantly more abundant in control Delomys sublineatus missing because feeding guilds could not be detected Püttker et al. 2008a ind Table 2: no significant correlation of parasite load with fragment size and connectivity ind Table 1: no significant correlation of condition index with fragment size and…”

“Many bird studies report detrimental responses to the isolation of tropical forest patches (Bierregaard and Lovejoy, 1989; Stratford and Stouffer, 1999; Stouffer and Borges, 2001; Robinson, 1999; Lambert and Collar, 2002).”

“…have shown that body mass is correlated with minimum patch size (e.g. Leck, 1979; Beier et al., 2002) and is inconsistent with the hypothesis that if home range size scales to body mass, area-sensitive birds will be absent from patches smaller than a few home ranges (Stratford & Stouffer, 1999).”

“Some of these species may be persisting in fragments, rather than recolonizing, accounting for the strong area effect (Stratford & Stouffer 1999; see also Robinson 1999; Blake & Conservation Biology Volume 20, No. 4, August 2006 Loiselle 2001).”

“Birds living in fragmented habitats are frequently subject to higher extinction risks than those in continuous environments (Wiens 1995; Stratford and Stouffer 1999; Brooker and Brooker 2001).”

“Insectivorous bird species are frequently used as sensitive focal species for studies on the effects of fragmentation in the Amazon basin (e.g., Stratford & Stouffer 1999).”

“Stratford and Stouffer, 1999 ) are all inextricably linked to patch size.”

“Finally, we examine whether response to natural gas exploration varies by avian feeding guild, with the expectation that insectivorous birds will respond more acutely to activities, based on previous studies showing understory avian insectivores to be particularly sensitive to anthropogenic disturbance (Canaday, 1996;…”

“A severe reduction in the species richness of terrestrial/understorey foragers, as observed in this study, is consistent with most tropical forest fragmentation studies (e.g. Newmark, 1991; Stratford & Stouffer, 1999).”

“…to impede the movement of forest species (Fahrig & Paloheimo 1988; Opdam 1991), resulting in reduced dispersal rates (Lens & Dhondt 1994; Matthysen & Currie 1996), lower diversity (Opdam et al. 1984) and a lower probability of patch recolonization ( Verboom et al. 1991; Stratford & Stouffer 1999).”

“…forest bird declines to deforestation and the conversion of tropical forests to agricultural habitats, particularly in forest archipelagos in agricultural landscapes (Bregman et al., 2014; Newmark, 1991; S ekercioğlu, 2012a; Sigel et al., 2006; Sodhi et al., 2011; Stratford and Stouffer, 1999).”

“These species had already been lost from smaller fragments, and other members of this guild had already been lost from 100-ha fragments by 1995 (Stratford & Stouffer, 1999).”

“…sensitivity, ranging from Myrmornis torquata (Wing-banded Antbird), a species that was missing from all the forest fragments studied by Stratford and Stouffer (1999) and has never recolonized any fragment, to Myrmothera campanisona (Thrush-like Antpitta) a species that colonizes…”

“Several long-term studies have documented the decline of forest bird populations with the increase of forest loss to agriculture and other human land uses in the American tropics (Stratford and Stouffer 1999; Robinson 2001; Sekercioglu et al. 2002; Sigel et al. 2006).”

“…the main threats to regional and global biodiversity (NOSS & CSUTI 1997) because they result in several consequences to the fauna, including alteration at the community level and local to regional extinctions (LOVEJOY et al. 1984, ANDRÉN 1994, ROBINSON & ROBINSON 1999, STRATFORD & STOUFFER 1999).”

“It was not a surprise that birds with natural low abundance and the guilds of understory insectivores and large terrestrials birds were found to be more affected by habitat loss and fragmentation, as this result is congruent with many other studies (Willis 1979; Kattan et al. 1994; Stratford and Stouffer 1999; Goerck…”

“The problem of analysing patterns of species richness in fragments of differing size is that it is difficult to eliminate the effects of decreasing sampling area; both fragmentation and decreasing sampling area should result in decreasing species richness (Stratford & Stouffer, 1999).”

“Many species decline or disappear from forest fragments (Stouffer & Bierregaard 1995, Stratford & Stouffer 1999, Beier et al. 2002), logged rainforest (Thiollay 1992, Aleixo 1999), fire-disturbed forest (Barlow et al. 2002), and forest edges bordering agricultural fields (Restrepo & Gomez 1998) and…”

“For example, insectivores of understory or terrestrial microhabitats are rarely resilient to the more severe forms of disturbance (Johns 1991), and large canopy frugivores, understory insectivores, and forest interior raptors are particularly vulnerable to fragmentation (Johns 1991; Kattan et al. 1994; Renjifo 2001; S…”

“Insectivores responded negatively to fragmentation at both sites, a widespread tropical pattern (e.g., Thiollay 1997; Stratford and Stouffer, 1999; S ekercioğlu et al., 2002; Sodhi et al. 2004).”

“Nonetheless, the special case in which habitat availability is governed purely by the amount of contiguous habitat seems to be valid only under very particular conditions, such as when species strongly avoid edge environments (Stratford and Stouffer 1999) or when inter-patch distances exceed species dispersal capaciti…”

“CHRISTINA M. KENNEDY ET AL.1846 Ecological Applications Vol. 21, No. 5 reduces functional landscape connectivity (e.g., Stratford and Stouffer 1999, Sekercioglu et al. 2002); (2) increased nest parasitism and predation of birds (e.g., Chalfoun et al. 2002, Lampila et al. 2005); and (3) reduction of…”

“Our focal species were terrestrial insectivores with a range of responses to fragmentation and second-growth forest (Borges and Stouffer 1999, Stratford and Stouffer 1999; Table 1).”

“The ground insectivores of the Formicariidae are very sensitive to habitat disturbance (Canaday 1996, Canaday & Rivadeneyra 2001, Stratford & Stouffer 2001).”

“Stratford and Stouffer (1999), also working in young secondary forest at the BDFFP, speculated that the terrestrial insectivores would be the last to recover as secondary forest matures.”

“In fragmented tropical landscapes, elevated nest predation can also reduce avian productivity causing population declines (Sodhi et al., 2004; Stratford and Robinson, 2005; Stratford and Stouffer, 1999; Willis, 1974).”

“They both cause isolation of remnant forest patches, thereby increasing risks of extinction (Bodmer et al. 1997; Laurance et al. 2011) and reducing native species richness (Stratford and Stouffer 1999; Cullen et al. 2000; Ferraz et al. 2007).”

“For example, previous studies have shown strong evidence that understorey and terrestrial (e.g. Stratford & Stouffer, 1999; Sekercioglu et al., 2002; Laurance & Gomez, 2005) and frugivorous (e.g. Githiru et al., 2002) birds are relatively more dispersal limited.”

“Fragmentation can isolate populations, thereby reducing genetic diversity and population viability, which may result in local extinctions [3–5].”

“Isolation length >0 m 37% ↓ [47] >75 m 66% ↓ [47] 100% ↓ (1 ha); 30% ↓ (10 ha) [51] >100 m 100% ↓ (1 ha); 30% ↓ (10 ha) [51] >300 m 30% ↓ [47] >425 m 100 % ↓ [47] -”

“Ground insectivores were extirpated from small Amazonian forest remnants (≤ 10 ha) following fragmentation (Stratford & Stouffer, 1999) as edge- dominated remnants could no longer sustain critical foraging microhabitats for these species (Stratford & Stouffer, 2013).”

“fragmentation, and its relevance towards extinction [8–12], has been studied exhaustively in birds [4,13–35].”

“…forests (but see Willis 1974, 1979; Leck 1979; Bierregaard & Lovejoy 1989; Bierregaard 1990; Stouffer & Bierregaard 1995 a , 1995 b ; Robinson 1999; Stratford & Stouffer 1999), even though tropical species are thought to be more sensitive to fragmentation (Terborgh 1974; Remsen & Parker 1984; Karr…”

“…of insectivores to habitat size, quality and fragmentation relative to other guilds, possibly a result of large spatial requirements, dependence on old-growth forest and altered conditions potentially resulting in lower insect abundances along the edges (Stratford and Stouffer 1999, Vetter et al.”

“…forest has been associated with declines in the richness and abundance of primary forest birds in both connected (Lees and Peres, 2008) and unconnected or poorly connected remnants (Ferraz et al., 2003; Stouffer and Bierregaard, 1995; Stratford and Stouffer, 1999; Antongiovanni and Metzger, 2005).”

“However, studies of other animals in this system found lower species richness of birds [28,29] and higher species richness of small mammals and frogs in fragmented forest relative to intact forest [30,31].”

“Traditional terrestrial application of the theory of island biogeography has been to islands of forest in a matrix of agriculture, urbanization, clearcuts, or meadows (e.g. Martin, 1980; Soulé et al., 1988; Stouffer and Bierregaard, 1995; Stratford and Stouffer, 1999; van Balen, 1999; Beier et al. 2002), i.”

“They are biased relative to the very time-consuming spot-mapping method (Raman, 2003), considered the only reliable means of determining absolute abundance (Terborgh et al ., 1990; Stratford & Stouffer, 1999).”

“The reduction and isolation of habitat patches can lead to a local loss of forest-dependent species, favouring habitat generalists (Willis 1979; Turner 1996; Stratford & Stouffer 1999; Willis & Oniki 2002; Antunes 2005; Giraudo et al. 2008).”

“Transformation of land cover for agriculture is clearly the major force driving declines and extirpations of birds (Stratford and Stouffer 1999; Estrada et al. 2000; Sodhi et al. 2011).”

“These species are phylogenetically related to understory insectivores of tropical Latin America (Ridgely and Tudor 1994) that are also fragmentation sensitive (e.g., Stouffer and Bierregaard 1995, Sieving and Karr 1997, Stratford and Stouffer 1999).”

“Many understory insectivores are also affected by habitat changes that alter moisture and humidity in forests, such as forest fragmentation and degradation (Thiollay 1992; Stouffer & Bierregaard 1995; Canaday 1997; Stratford & Stouffer 1999; Sekercioglu et al. 2002; Williams & Middleton 2008).”

“While the effects of fragmentation are well ocumented for aboveground animals such as birds or amphibians Stratford and Stouffer, 1999; Cushman, 2006), they have hardly een studied in soil organisms (Decaëns, 2010).”