Research Paper

INTRODUCTION

Grazing lands are one of the most widespread forms of human land use globally (Asner et al. 2004, Ellis et al. 2021) and a major driver of deforestation linked to agriculture (Pendrill et al. 2022). In Colombia, livestock grazing is the predominant land use, having expanded either through deforestation or the transformation of native savannas (Etter et al. 2008). Consequently, grazing is considered the second largest threat to birds in the country, impacting 44% of threatened species, with crop-based agriculture impacting 55% (Renjifo and Amaya-Villarreal 2017). However, although livestock exclusion can generally benefit biodiversity (e.g., Filazzola et al. 2020), the dynamics of grazing are more complex in the Llanos, which are characterized by extensive tropical savannas. These savannas present a unique opportunity for high-productivity, low-impact cattle grazing, unlike mountainous regions such as the Andes (Zuluaga et al. 2021). Hence, developing sustainable grazing practices in this region could contribute to both food security and biodiversity conservation in what is considered Colombia’s new production frontier (Lerner et al. 2017, González-Orozco et al. 2023).

Given these complexities, the compatibility of livestock grazing in savanna ecosystems has been called “the cattle conundrum” reflecting the potential of grazing activities to support biodiversity conservation (Veldman et al. 2015). Thus, although intensive grazing reduces bird abundance and species richness (Barzan et al. 2021), moderate grazing with proper management can also support biodiversity conservation, ecosystem services, and climate change mitigation (Barzan et al. 2021, Costa et al. 2022). Despite this potential, avian conservation in grazing systems of South America, such as the Llanos, has received little attention in comparison to other types of agroecosystems like coffee and cacao (Johnson et al. 2011). Furthermore, most research has concentrated on the Andean region (Fajardo et al. 2009, Gilroy et al. 2014, Edwards et al. 2021), where silvopastoral systems have been developed and proven highly effective in maintaining biodiversity and ecosystem services (Calle et al. 2012, Chará et al. 2017).

Based on the potential to synergize conservation and cattle farming in the Llanos (Hoogesteijn and Hoogesteijn 2010), implementing sustainable grazing practices is paramount, especially as agricultural expansion continues to negatively impact native bird communities (Rincon-Parra et al. 2022). One major challenge, common across South American savannas, is the low productivity of conventional grazing practices (Strassburg et al. 2014), which use annual burning and low stocking rates, leaving little land for preservation. Agricultural intensification is therefore a crucial step to free up land for natural habitats (Balmford 2021). However, intensification alone can lead to the collapse of farmland bird populations (Donald et al. 2001) and often falls short of achieving social-ecological goals (Rasmussen et al. 2018). To avoid these pitfalls, efficient land use policies and technical support for cattle farms are needed (Carriazo et al. 2020). In this context, private grazing lands that incorporate conservation efforts could offer a solution for maintaining savanna bird populations (Pavlacky et al. 2021)

This study was conducted on a private cattle farm implementing sustainable intensification through improved grass pastures (Rao et al. 2015). Here, the native savanna was replaced with exotic grass cultivars like Urochloa humidicola cv. Tully (CIAT 679), which offer greater persistence, productivity, and tolerance to the low-fertility, aluminum-toxic acidic soils of the Llanos (Bastidas et al. 2023). As a result, these grasses support higher stocking rates, accommodating 1 animal unit per hectare, whereas up to 17 ha are required per animal unit in natural savannas (Costa et al. 2022). This intensification, combined with management practices such as rotational grazing, increases production on smaller land areas, sparing native savanna. Moreover, the improved pastures eliminate the need for annual burning, a common regional practice that exacerbates biodiversity loss, soil degradation, and carbon dioxide emissions (Huertas Herrera et al. 2021, Costa et al. 2022). Hence, the aim of this research was to evaluate whether rotationally grazed improved pastures can serve as a solution for balancing cattle production with biodiversity conservation, offering a sustainable agricultural model in the Colombian Llanos.

METHODS

Study area

This research was conducted in the high plains of the Colombian Llanos, known as the altillanura, an area characterized by well-drained natural savannas and extensive riparian forests (Estrada-Villegas et al. 2022). Fieldwork took place primarily at Hacienda San José (HSJ), a private cattle farm in the municipality of La Primavera, Vichada, Colombia (5°54′52.48″ N, 69°37′12.54″ W; Fig. 1). Established in 2014, HSJ practices sustainable intensification of livestock production through the use of improved pastures managed under rotational grazing with higher stocking rates (Costa et al. 2022). HSJ also maintains buffer zones of native savanna extending 200 m around riparian forests, as well as three connectivity areas that are 200 m wide and 3 to 4 km long, one of which preserves the native savanna vegetation. Notably, the native savanna in HSJ has been free from cattle grazing or annual burning for the past seven years. This is in contrast to most of the region where conventionally managed native savannas experience uncontrolled grazing and annual burning (Romero-Ruiz et al. 2010, Huertas Herrera et al. 2021).

Three distinct land-use management regimes were surveyed within the savanna ecosystem of the study area, characterized by a mosaic of open grasslands, scattered shrubs, and mostly fire-adapted Chaparro trees (Curatella americana). These management regimes were (1) improved pastures (IP) with rotational grazing and no burning, (2) preserved native savanna (PNS) without burning or cattle grazing, and (3) conventionally managed savanna (CMS) with annual burning and uncontrolled grazing. Although Chaparro and other trees were retained in the IP areas, native shrubs were less prevalent. The buffer zones with native savanna of HSJ were excluded from the survey because of the predominance of riparian bird species.

Sampling design

I aimed to compare avian density estimates, species richness, and evaluate community differences within the three management regimes. I used distance sampling (Buckland et al. 2001) with line transects to derive density estimates corrected for species probability of detection, which are typically low for savanna birds (Diefenbach et al. 2003). This method is particularly effective in open terrain (Buckland 2006) and can yield more accurate abundance estimates than other methods, such as point counts with N-mixture models (Campomizzi et al. 2020). Additionally, abundance estimates from distance sampling have shown strong correlations with those from more intensive territory mapping for migrant and breeding birds (Gale et al. 2009, Campomizzi et al. 2020).

Distance sampling for IP and PNS was conducted at HSJ (Fig. 1), and for CMS took place in neighboring properties. I used 500-m line transects spaced at least 300 m apart, each considered as an independent spatial replicate. Birds were recorded up to a maximum distance of 100 m from the centerline. Four transects were established for both the PNS and CMS management regimes. The PNS transects were placed within one of the connectivity corridors and covered a uniform area (Fig 1). In the CMS management regime, the transects were likely subject to varying levels of burning and grazing over time, but these areas appeared to be in a similar condition during the survey, and had not undergone the annual burning. In contrast, eight transects were established in the IP management regime to account for the high spatial heterogeneity observed, ensuring adequate sampling coverage (Roswell et al. 2021). I did not differentiate between rotational grazing periods or types of improved grasses because the main focus was on the broader effect of the IP management regime on community-level responses for comparison with the other management regimes.

Field surveys

Birds were surveyed during two sampling events (Buckland 2006), timed to cover both the rainy and dry seasons. The bird community in the high plains of the Llanos is not as heavily influenced by seasonality as in the flooded plains, but bird activity tends to increase during the rainy season when breeding occurs. The first survey took place from 8 to 13 November 2023, near the end of the rainy season (September–November), whereas the second survey was conducted from 23 to 25 January 2024, in the middle of the dry season (December–February). The first survey required a longer duration because of adverse weather conditions, including heavy rain, wind, and poor visibility.

Sampling was conducted in the morning and afternoon. Transects were walked at a slow pace of 1 km/h to ensure an appropriate search effort (Diefenbach et al. 2003), which aids robust estimation of the shape of the detection function (Prieto Gonzalez et al. 2017). A rangefinder (Nikon Forestry Pro II) was used to calculate the distance (r), and a compass app to measure the angle of detection (θ) relative to the transect line. Only species that used habitats within the transects were counted, and flyovers were excluded from the study. The majority of individuals were observed, with a few instances where I pinpointed their exact location based on vocalizations. The IP land use was surveyed by walking on secondary roads that are only transited by HSJ personnel (Fig 1). These roads were between 2 and 6 m wide, and birds detections increased near the roads. Statistical methods were used to account for excess detections near the centerline of the transect.

To assess the completeness of the survey effort at HSJ, I obtained a savanna bird list from the Tomogrande field station located 120 km south of HSJ, a comparable site in the region with over 10 years of surveys (Estrada-Villegas et al. 2022). From an initial list of 63 species (Estrada-Villegas et al. 2022), I excluded nocturnal birds, swifts (flyovers), and the Black Vulture (Coragyps atratus) because it is mostly a human commensal, leaving 52 species as a benchmark of upper local species richness. Furthermore, I evaluated sampling effort for each management regime, using the iNEXT package (Hsieh et al. 2016) to estimate sample coverage with 95% confidence intervals. Sample coverage measures how representative the samples are of the bird community in each management regime (Roswell et al. 2021). Overall, sampling completeness was high, and further surveys were not required.

Density estimates

I estimated bird density at the community level for each management regime (Mulwa et al. 2012). The survey data for each management regime was pooled from the two sampling events to enhance the robustness of the results. Pooling increases the sample size and helps to account for seasonal variation in bird detectability and abundance, providing a more comprehensive representation of the bird community across different environmental conditions (Buckland et al. 2015). Analyses were performed using the R package Distance (Miller et al. 2019). Model checking followed a two-step process: First, detection functions were visually inspected to assess whether the fitted shapes indicated any violation of model assumptions (Thomas et al. 2010). Second, Q-Q plots were visualized, and goodness-of-fit was evaluated using the Cramer-von Mises (C-vM) or Chi-Square tests for binned data, via the gof_ds() function of the Distance package (Miller et al. 2019). To quantify the precision of the estimates, I applied a bootstrap method for uncertainty estimation with resampling at the transect level (Buckland et al. 2015) with the bootdht() function. This involved 400 bootstrap replicates (Newson et al. 2005) to generate the mean, 95% confidence intervals, and coefficient of variation.

Detection functions were fitted to each management regime. For the CMS management regime, a half-normal function without truncation provided a good fit. PNS data were binned into 10 m intervals (Buckland et al. 2001) and truncated at 50 m because of excess detections in the first few meters. For the IP management regime, the data had an inflated number of centerline detections (detections at zero distance) and at distances less than 5 m. These might have occurred because sampling on roads increased species detectability (Cooke et al. 2020). To address this, a hazard-rate detection function was selected, which is better suited for data with a wide detection shoulder (Clark 2016), that is, with detection probabilities close to one in the first distance intervals. Additionally, left truncation was applied to mitigate centerline detection bias (Buckland et al. 2001), and right truncation was set at 80 m.

Community analyses

I began analyzing community composition across the three management regimes. Bird species were classified into three habitat types: open areas, savannas, and woodlands. Woodland species were typically associated with scattered trees and riparian forests within the savanna. Open area species are generalists that can use different habitats with sparse vegetation. Conversely, savanna birds are specialists who make little use of other habitats. The classification followed Vickery et al. (1999) with modifications to fit the local context. Furthermore, I calculated the relative abundance of species for each management regime and created rank-abundance curves to visualize patterns of species richness and evenness (Magurran 2004).

To compare species richness between management regimes, I estimated asymptotic species richness with the newly developed omega estimator (Ω). This is a robust, bias-corrected estimator that accounts for spatial variability in species abundance and across sites, to infer observation probabilities that adjust the estimated species richness (Tekwa et al. 2023). The precision of the omega estimator was quantified using a block bootstrapping procedure that accommodated for dependencies within species and across spatial sampling units, using the function estimateRichness() of the Richness package with default settings (Tekwa et al. 2023).

To evaluate community differences between management regimes, I used the statistical package PAST (Hammer et al. 2001). First, I ran a permutational multivariate analysis of variance (PERMANOVA; Anderson 2017) based on the Bray-Curtis distance measure with 9999 permutations and a post-hoc pairwise comparisons test. I then used SIMPER analyses (Clarke 1993) to compute the average overall dissimilarity between management regimes based on the contribution of each species to dissimilarity. Last, an indicator species analyses (Dufrêne and Legendre 1997) identified species most strongly associated with each management regime, expressed as indicator values (IndVal%) based on their relative abundance and occurrence. Statistical significance was assessed by random reassignment across different groups (9999 permutations). The formula used to calculate IndVal (%) was as follows:

(1)

where A_ij is the relative abundance of species i in group j, and B_ij is the relative frequency of occurrence of species i within group j.

RESULTS

I recorded 36 species in the study area, of which 11 were savanna specialists, 19 from open areas, and 6 were woodland species. (Table 1). The observed species richness from the two sampling events is approximately 70% of the bird list of the Tomogrande field station with over 10 years of surveys (Estrada-Villegas et al. 2022). The recorded species were composed of resident birds. Although migrants such as Bobolinks (Dolichonyx oryzivorus) use the region as a major stopover (Renfrew et al. 2013, Bayly et al. 2018) they have been detected in April and May, which fell outside of the sampling period.

In terms of sampling completeness for the three management regimes, the IP sample coverage was 0.99 (95% CI [0.97–1.00]), for the CMS was 0.95 (95% CI [0.90–0.99]), and for the PNS was 0.87 (95% CI [0.80–0.95]). Hence, even if more surveys were conducted, the sampling would be representative of each management regime. The rank-abundance curves indicated that the three communities were characterized by a few dominant species (Fig. 2). The observed species richness was highest in the IP with 30 species, followed by the PNS with 16 species and the CMS with 14. Many savanna specialist birds were found at the IP (Table 1), though not exclusively. These included species such as meadowlarks, the Grassland Sparrow (Ammodramus humeralis), seedeaters like the Grassland Yellow Finch (Sicalis luteola), and raptors such as the Aplomado Falcon (Falco femoralis) and the Burrowing Owl (Athene cunicularia).

The omega estimator (Ω) calculated an asymptotic species richness for the IP at 42.3 species, followed by the PNS at 23.2 species, and 19.5 species for the CMS (Table 2). The PNS and CMS had similar density estimates (4.4 ind/ha and 4.5 ind/ha, respectively) but the CMS had a wider confidence interval and coefficient of variation (Table 2). For the CMS, a half-normal detection function without adjustments or truncation provided a good fit (C-vM statistic = 0.083, p = 0.672). For the PNS, binning data and truncation improved model fit, X² (3, N= 37) = 7.55, p = 0.056. The highest species density was found in the IP (10.6 ind/ha). In this case, the hazard-rate detection function with left and right truncations provided an appropriate goodness-of-fit (C-vM statistic = 0.108, p = 0.548).

For the IP, the Grassland sparrow had the highest relative abundance (21.2%), followed by the Eastern Meadowlark (Sturnella magna; 10.4%), and Red-breasted Meadowlark (Leistes militaris; 9.1%). For the PNS, it was the Fork-tailed Flycatcher (Tyrannus savana; 18.9%), followed by the Wedge-tailed Grass-Finch (Emberizoides herbicola; 16.9%), and the Grassland Sparrow (17.0%). For the CMS, it was the Fork-tailed Flycatcher (16.4%), followed by the Wedge-tailed Grass-finch and the Plumbeous seedeater (Sporophila plumbea), both at 14.5%. Species relative abundances values are shown in Table 1.

Bird community differences were found between management regimes (PERMANOVA, F = 1.824, p = 0.003). Importantly, the pairwise differences were statistically significant between the IP with both the CMS (p = 0.001) and the PNS (p = 0.002), but not between the two (p = 0.381). A SIMPER analysis computed based on the contribution of each species to dissimilarity showed that the overall average species dissimilarity across management regimes was 79.4%.

Based on the indicator species analyses, four species were significantly associated with any given management regime (Fig. 3). The IP had the Grassland Sparrow and the Eastern Meadowlark with IndVal 52.9% (p = 0.044) and 69.2% (p = 0.012), respectively. The Wedge-tailed Grass-Finch was associated with the PNS (IndVal 41.7%, p = 0.027) and the Grass Wren (Cistothorus platensis) with the CMS (IndVal 50.0%, p = 0.048). We also found another species, the Bearded Tachuri (Polystictus pectoralis), a savanna specialist bird, only in the PNS and CMS management regimes.

DISCUSSION

In this study, I surveyed birds across three different land-use management regimes at Hacienda San José, a private cattle farm located in the high plains of the Colombian Llanos. The aim was to assess whether improved pastures (IP), managed through rotational grazing and the exclusion of burning, could sustain savanna bird populations. The IP regime was compared to preserved native savanna (PNS) and conventionally managed savanna (CMS), the latter being subject to heavy grazing and annual burning outside of HSJ. The results revealed that IP had the highest species richness and density, supporting a substantial portion of savanna bird populations. This is consistent with other research suggesting that moderate grazing intensity can be compatible with biodiversity conservation (Ahlering and Merkord 2016, Barzan et al. 2021). However, the preservation of native savanna vegetation remains essential. The findings show that savanna specialists are strongly associated with the native savanna, where they occur in higher abundances, even in small remnant patches surrounded by intense agricultural production (Staude et al. 2021), such as the PNS in the study area.

When comparing the PNS and CMS, the PNS exhibit lower sampling completeness but a higher estimate of asymptotic species richness. This suggests that the PNS can support more species than the CMS, which may represent a degraded state of the PNS. Bird density estimates were similar for both the PNS and CMS. However, the CMS showed wider confidence intervals. This increased uncertainty likely stems from variations in grazing and burning intensity that were not evaluated in the surveyed transects. The main limitation of this study, however, is the small area of PNS that was surveyed. Savanna birds can decline more rapidly in landscapes where the extent of native savanna has been reduced (Mahony et al. 2022), affecting groups such as seed-eating birds (Zarco et al. 2019). Therefore, the bird diversity observed in this study likely underestimates the diversity that would be present in a more extensive native savanna ecosystem. Unfortunately, addressing this limitation was not possible because nearly all of the native savanna in the study region is subject to burning and grazing.

The results highlight the importance of preserving native savanna vegetation in the agricultural landscapes of the Llanos region. Some populations of bird species could plummet if only improved pastures remain in the region because they are associated with the PNS or CMS. The indicator species analysis showed that the Wedge-tailed Grass-Finch, which depends on tall grasses, was associated with the PNS because of the presence of this vegetation type. In contrast, the Grass Wren was associated to the CMS, where, despite degradation, is still an extensive area of natural savanna that is crucial for the species (Herkert et al. 2021). Therefore, even the CMS holds value for the conservation of savanna specialist birds. In addition, the Bearded Tachuri was found only in the PNS and CMS, and the Near-Threatened Black-faced Tanager (Schistochlamys melanopis) was only recorded in the PNS, which is commonly associated with wooded savanna, as is the case in a surveyed portion of the PNS.

Overall, these findings underscore the importance of maintaining habitat heterogeneity within the savanna ecosystem for sustaining bird populations (Fuhlendorf et al. 2006, Rahmig et al. 2009, Hovick et al. 2015). A variety of grasses with different heights and densities is important to meet the needs of different species (Vickery et al. 2000, Neilly and Schwarzkopf 2019). For instance, Eastern Meadowlarks and Grassland Sparrows benefited from the improved pastures, similarly to related species in North American agricultural grasslands, which favor short grasses with sparse vegetation (Johnson and Sandercock 2010, Johnson et al. 2019). In contrast, species like Wedge-tailed Grass-Finch prefer tall grasses and dense vegetation that is normally found in the native savanna. The species was also observed outside the survey in tall marginal grasses along narrow roads, suggesting that grassy margins and linear features may serve as important habitat corridors (Cox et al. 2014, Johnson et al. 2019). Notwithstanding, conducting species- specific studies is necessary, as different species hold different responses to management practices and habitat modifications (Neilly and Schwarzkopf 2019).

Given the need for habitat heterogeneity, the expansion of improved pastures over the past decades in the Llanos region (Romero-Ruiz et al. 2012, Vera and Hoyos Garcés 2019) should raise alarms if we are to avoid the loss of grasslands that occurred elsewhere. In North America, nearly 95% of tallgrass prairies have disappeared (Samson and Knopf 1994) and as a result the decline of grassland birds unfolded a major conservation crisis (Brennan and Kuvlesky 2005, Sauer and Link 2011, Rosenberg et al. 2019). Similarly, across the UK, improved pastures produced large changes in bird abundance and species composition (Barnett et al. 2004). The expansion of Pasto Humidola (Urocrhora humidicola) in the Llanos, despite its proven improved agricultural production and environmental benefits (Costa et al. 2022, Bastidas et al. 2023), will require careful land-use planning and management.

In conclusion, although the establishment of improved pastures holds promise for biodiversity conservation in the Llanos highlands, new agricultural projects should prioritize win-win strategies that integrate efficient land-use practices, balancing production with the conservation of the native savanna ecosystems. This approach would help maintain conservation values alongside agricultural productivity (Fischer et al. 2014). Potential land-use management strategies may include (i) incorporating a variety of pasture grasses to be managed at different heights and densities, (ii) adopting sustainable practices like rotational cattle grazing without burning of vegetation, (iii) promoting live fences to enhance habitat connectivity, and (iv) preserving and restoring native savanna vegetation to benefit specialist species. Furthermore, technical knowledge transfer and capacity-building programs for local farmers are needed. Successful models like Hacienda San José are therefore crucial for adapting these practices across other cattle farms, and should continue to lead through adaptive management, contributing to research and knowledge sharing in this relatively understudied region, considered Colombia’s new agricultural frontier.

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