Anthropic activities like agriculture and urbanization drive habitat loss in terrestrial ecosystems, jeopardizing the world’s biodiversity (Vitousek et al., 1997; Corlett, 2015). Many studies have used bird communities as a model to understand biodiversity losses by assessing the shifts in abundance among species and trophic guilds in anthropized areas. Their results show that ecologically specialized birds decrease and become extinct, while generalist birds (frequently, invasive species) become dominant regardless of geographic location (McKinney and Lockwood, 1999; Davey et al., 2012; Lepczyk et al., 2017).

Given that ecological pressures affect organisms’ success by acting on their traits, and that anthropization changes ecological pressures in non-random ways, it is plausible that biodiversity loss under anthropization could follow specific patterns (Shipley, 2010; Grime and Pierce, 2012). However, the classical ecological framework is not capable to detect shifts in traits because it considers species’ abundances, but not the traits related to their responses to environmental change (Shipley, 2010). Animal ecologists have therefore increasingly adopted a functional ecology framework (Luck et al., 2012), which assesses changes in the representation of organisms’ intrinsic functional traits, such as life cycle development, resource attainment, and the organism’s effects on the ecosystem (Violle et al., 2007; Salgado-Negret and Paz, 2016). Because these traits are the vehicle by which ecological pressures act on fitness, this functional approach provides a basis for making mechanistic generalizations about species’ responses to environmental changes and the consequences of biodiversity losses (Diaz et al., 2004; Shipley, 2010; Salgado-Negret and Paz, 2016).

Trait-based studies focusing on birds in anthropized environments have detected the loss of species with large bodies, “slow” strategies (long lifespan, long development times, and low reproductive output; Cooke et al., 2019), and traits related to ecological specialization (Newbold et al., 2013). Recent studies using comprehensive global bird and mammal biodiversity databases have shown that the same trait patterns were favored in both taxa when communities faced simulated extinction scenarios due to anthropization (Cooke et al., 2019). This suggests that the responses underlying community assemblage within anthropized habitats may be broadly generalizable across taxa (Shipley, 2010).

These findings also resemble aspects of Ecological Evolutionary Strategies theory (EES, Grime and Pierce, 2012), which proposes that natural selection favors general strategies of response to a given set of ecological conditions. Specifically, EES predicts that disturbed and unstable environments favor rapid resource attainment, short lifespan, small biomass, and high reproductive output, which are known as a “ruderal” strategy, exemplified by annual herbaceous plants in anthropized areas (Grime and Pierce, 2012). Trait shifts within anthropic bird communities seem to mirror EES predictions, potentially demonstrating that taxa other than plants could follow trait-based pathways shaped by ecological pressures. However, field studies providing empirical evidence are lacking (Grime and Pierce, 2012).

In this study, we use a functional ecology approach to assess whether anthropization favors traits considered advantageous in disturbed environments. We study the resident bird communities of two seasonal forests types in central Mexico: tropical dry forest and oak forest. Both of these ecosystems are imperiled by habitat loss from agriculture and cattle grazing. While several studies in the seasonal tropics have tackled changes in bird communities due to anthropization (MacGregor-Fors and Schondube, 2011; Maya-Elizarrarás and Schondube, 2015; Vázquez-Reyes et al., 2017), they followed the classic species-abundance framework. These works have found losses of species richness and communities dominated by generalist species. In addition, it has been suggested that anthropization drives trait shifts in Neotropical birds (Newbold et al., 2013, 2014). However, whether bird communities exhibit dominance of a trait-based ruderal ecological strategy in response to anthropization remains unknown. Using empirical evidence, we tested whether there was a directional shift in functional traits that could favor birds' success across a gradient of anthropization in seasonal forests of Central Mexico. We hypothesized that anthropization could favor trait patterns that resemble a ruderal strategy in bird communities; thus, we expected that bird traits related to short life cycles, high fecundity, and broader ecological niche requirements would increase in dominance in the more anthropized habitats.

We recorded a total of 83 bird species in our survey. In both tropical forest and the oak forest, most of the CWM values differ among anthropization levels, while patch effects were significant for only two traits (fledgling age and habitat use width within oak forest), suggesting that the overall functional dominance of the bird community showed low spatial variation (Table 2, Fig. 2).

Fig. 2.

Box-and-whisker plots of the CWM for bird traits at each anthropization level in the Alto Balsas region. Significant differences in the PERMANOVA post-hoc tests (p < 0.05) are shown by letters (groups that do not share a letter differ from each other).

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In the tropical forest, bird communities in primary forest had higher body mass, incubation time, and age at fledging than in the secondary growth and human settlements, while clutch size, diet niche width, and nesting substrate width were smaller in the primary forest than in the anthropized habitat. Life span was longer in the primary forest and human settlements than in the secondary growth, while the habitat niche width was narrower in the primary forest and human settlements than in the secondary growth. In the oak forest, the niche width for diet, foraging habitat, and nesting substrate had lower values in the primary and secondary growth than in the human settlements. The hatching and fledging age were higher in the primary forest and secondary growth than in human settlements (Table 2, Fig. 2). Three traits—body mass, clutch size, and lifespan—were unaffected by anthropization level.

In the multivariate trait correlations, the first two components of the PCA (PC1 and PC2, respectively) explained 55.31% of the variance in tropical forest and 41.47% in the oak forest (Fig. 3, Table 3). In the tropical forest, PC1 indicated that larger body mass was associated with longer incubation times, older age at fledging, longer life spans, and narrower habitat and diet niche widths. PC2 showed that species with larger clutch size tended to have wider habitat use, diet and nesting substrate niches and shorter incubation periods. The results of the PCA in the oak forest showed similar associations among traits, but the order of the PC was reversed. PC1 indicated that species with larger clutches tended to have wider habitat use and nesting substrate niches, shorter incubation periods, younger age at fledging, and shorter lifespans (similar to PC1 in the tropical forest), while PC2 showed that birds with large body masses tended to have longer incubation periods and narrower diet niche width (similar to PC1). However, unlike the tropical forest, dominant birds within the primary oak forest tended to have shorter lifespans (Fig. 3, Table 3).

Fig. 3.

Bird trait covariation patterns (weighted-PC × bird abundance) within the tropical forest and the oak forest of the Alto Balsas region. Sketches show the bird species with the highest scores for each PC in the tropical forest (Military Macaw, Bronzed Cowbird) and oak forest (Bronzed Cowbird, West-Mexican Chachalaca). The anthropization level where those birds were mainly recorded are also sketched. The box-and-whisker plots below each PCA biplot show significant differences in the PERMANOVA post-hoc tests as letters between anthropization levels (p < 0.05; groups that do not share a letter differ significantly).

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The PERMANOVA results using the multivariate response variables reinforced the finding that the dominance of birds functional strategies differed among anthropization levels in both forest types (Fig. 3, Table 4). The weighted-PC1 for the tropical forest, and weighted-PC2 for the oak forest showed that dominant birds within the primary forest had larger body mass, longer incubation time, and older age at fledging, and wider habitat use and diet niches than the dominant birds in the secondary growth and human settlements. In the tropical forest, dominant birds in the primary forest also had longer lifespans than dominant birds in the secondary growth and human settlements. The weighted-PC2 for the tropical forest and weighted-PC1 for the oak forest showed that dominant birds in the primary forest had smaller clutch sizes and narrower habitat use than dominant birds in the secondary growth and human settlements (Fig. 3, Table 4).

Our results indicated that large-bodied birds with slow developmental rates are negatively affected by the intensification of human activities, which has been well documented across different ecosystems (McKinney and Lockwood, 1999). The loss of large bird species in anthropized habitats has been explained by the scarcity of the available habitat and resources (McKinney and Lockwood, 1999; Newbold et al., 2013, 2014). The Military Macaw (Ara militaris) is an example of a large forest bird that was excluded from anthropized habitats (Cooke et al., 2019). Macaws are at the “slow” end of the continuum of life-history strategies exhibited by the bird communities studied here, as evidenced by life history trait values, substantially larger than the CWM in tropical forest (i.e.; body mass of 1100 g versus 125.7; life expectancy up to 40 years versus 11.5; incubation time of 26 days versus 15.7; age at fledgling of 96 days versus 18).

Contrary to the tropical forest, body mass, clutch size, and lifespan of the bird community did not differ among anthropization levels in the oak forest, and the PCA explained a lesser amout of variance. This could be the result of ecological and anthropic factors limiting the body size of the birds in the oak forest. For example, acorns do not have a fleshy mesocarp and are therefore not trophic resources for large-bodied birds (Ramírez-Bastida et al., 2015). This includes species such as the macaws, which consumes fleshy fruits as its main source of food (Contreras-González et al., 2009). This contrasts with the high diversity of trees with zoochoric fruits in the tropical forest. Secondly, in our study region, as in the rest of Mexico, even primary oak forests are impacted by cattle ranching and firewood extraction, which may negatively affect large-bodied birds (Maya-Elizarrarás and Schondube, 2015). Besides, the bird communities in the Alto Balsas basin are subject to loss of taxonomic differences due to anthropization (Vázquez-Reyes et al., 2017). In this process, certain tropical forest birds, such as the West-Mexican Chachalaca (Ortalis poliocephala) and the Russet-crowned Motmot (Momotus mexicanus), reach the highlands covered by oak forests. Finally, local inhabitants mentioned that the Band-tailed Pigeon (Patagioenas fasciata; body mass 360 g, CWM = 40.5 g) was present in the area, but was hunted in the region until 20 years ago. Notably, after a decade of survey, the lack of records suggests that this species is locally extinct (Vázquez-Reyes et al., 2018). Together, these factors may explain the lesser functional differentiation among the anthropization levels in the oak forests in comparison to the tropical forest.

The strong dominance of bird species with high fecundity and wider niches for both nesting substrate and habitat use in the human settlements suggests that those birds are favored by anthropization. For example, the Bronzed Cowbird (Molothrus aeneus) has an abundance up to 8 times higher than any other species within the human settlements. The hatching and fledging times (11 days each) of cowbirds chicks are shorter than the CWM values detected in the human settlement sites of both the tropical forest (13.2 and 15 days) and the oak forest (13.7 and 15.7 days). This is likely facilitated by the fact that cowbirds are interspecific nest parasites, which lay their eggs exclusively in the nests of other species, allowing them to invest most of their reproductive effort in egg production and minimizing parental effort (Mermoz and Ornelas, 2004). This allows cowbirds to be extraordinarily fertile, laying up to 40 eggs yearly (Billerman et al., 2021), placing them at the extreme “fast” end of the functional strategies’ axis described for birds (Cooke et al., 2019).

Nevertheless, having a fast-life pace is not the only biological factor that makes a bird successful in anthropized habitats. Having generalist strategies of resource use is also critical to adapt well to ecologically unstable conditions promoted by the frequent and intense perturbations within the anthropized habitats (Sol et al., 2017; Ducatez et al., 2018). Indeed, the dominance of generalist species is a well-documented pattern (Lepczyk et al., 2017). In our study, the most abundant species in the human settlements were generalist birds, such as the native Bronzed Cowbirds and Inca Doves (Columbina inca), but also the non-native House Sparrow (Passer domesticus) and Rock Pigeon (Columba livia). These species have wide substrate nesting niches and can use both natural and artificial resources for nesting, supporting the idea that generalist birds are more efficient in exploiting resources in anthropized habitats (Davey et al., 2012; Lepczyk et al., 2017).

Conversely, the Pale-billed Woodpecker (Campephilus guatemalensis) is a specialist bird that has been excluded from the human settlements. This species was recorded only in the primary tropical forest. Its exclusion may be due to the fact that they depend on large mature trees to excavate their nesting cavities (Monterrubio-Rico and Escalante, 2006). Similarly, in the oak forest, the Mountain Trogon (Trogon mexicanus) and the White-striped Woodcreeper (Lepidocolaptes leucogaster), both of which depend on forest cover for nesting and feeding (Ramírez-Bastida et al., 2015), were excluded from the human settlements.

The patterns of covariation of multiple traits favored by selective pressures can be defined as ecological strategies (Keddy, 1992; Diaz et al., 2004; Shipley, 2010). Therefore, identifying the dominant traits in anthropized habitats could suggest recognizable ecological strategies among birds (Cooke et al., 2019). The pattern of trait covariation detected in our study as a response to anthropization intensity is very similar to the ruderal strategy of herbaceous plants that are highly successful in anthropized habitats (Grime, 1977). Like the ruderal plants, successful birds in the anthropized habitats tend to have short life cycles and developmental times, high fecundity, and the ability to use a wide range of resources, analogous to high ecological plasticity among plants (Grime, 1977). Following the theory of Ecological Evolutionary Strategies, these ruderal traits may favor individual fitness in environments where disturbance is frequent and resource availability unpredictable (Grime and Pierce, 2012). Overall, similar functional responses between birds and plants to anthropized habitats suggest that the “ruderal strategy” could also be used by birds. Our findings show that functional traits-based ecology is a promising tool to assess patterns and to achieve generalizations on the biodiversity changes, under the rampant anthropization of the forest ecosystems of the world (Luck et al., 2012; Salgado-Negret and Paz, 2016).

Fieldwork was funded with grants from CONACyT (152060-B, AGNS and 220265, LDVR) and CONANP (PROCER/DRCEN/003/2015 and /06/2016, Naturam Sequi-LDVR). The Postdoctoral Fellowship (DGAPA-CTIC-UNAM) and SIJAC-UNAM programs (2019/AS/00212/857022) provided support to LDVR during the manuscript writing. HP thanks the sabbatical fellowship from DGAPA, UNAM.

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.