There is a lack of studies that directly investigate temporal trends in wildlife responses to fragmentation and even fewer that evaluate how matrix use changes through time (but see5,29). Consequently, in contrast to the evaluation of species responses to spatial features, which has received some attention in the bat conservation literature, temporal variation, and in particular how bat responses to fragmentation are shaped by changes in matrix condition, remains little explored24. Here, we show that most phyllostomid bat species and Pteronotus parnellii benefited from the increased permeability of the matrix associated with the maturation of the secondary regrowth surrounding the BDFFP fragments, and that specialist and generalist species exhibited contrasting responses to matrix regeneration across the study landscape.

As hypothesized, we found that the maturation of second growth surrounding the BDFFP fragments lead to a landscape-wide increase in the occupancy and abundance of specialists, while reducing the occupancy and abundance of generalists in secondary forest sites. Our results therefore mirror the recovery documented for beetle30 and bird31 assemblages following the development of secondary vegetation in the matrix at the BDFFP. However, it is worth emphasizing that the BDFFP is surrounded by vast expanses of continuous forest harbouring healthy source populations and is buffered from selective logging, fires, species invasions, and many other ancillary threats plaguing contemporary tropical fragmented landscapes25. The recovery here documented is therefore likely to represent a best-case scenario and patterns reported might be harder to observe under conditions that increasingly characterize the majority of human-modified tropical landscapes.

The sole reliance on mist-netting data precludes a complete overview of the effects of second forest regeneration on the BDFFP chiropteran fauna as a whole since, with the exception of P. parnellii, Amazonian aerial insectivorous bats (a diverse group that includes the families Thyropteridae, Furipteridae, Mormoopidae, Emballonuridae, Vespertilionidae, Molossidae and Natalidae)32 are not effectively sampled with mist-nets33. However, we anticipate that old-growth specialist aerial insectivores are likely to have benefited from the maturation of second growth surrounding the BDFFP fragments in a similar way than their phyllostomid counterparts and to the aerial insectivore P. parnellii.

Our results contrast with the catastrophic faunal declines observed in rodent communities by Gibson et al.11 in the forest islands of the Chiew Larn reservoir in Thailand. Whereas most species of the mega-diverse bat assemblage at the BDFFP increased in occupancy and abundance across the second growth-dominated landscape, in the land-bridge island system in Thailand and, during a similar time window (~20 years, Gibson et al.11; ~15 years, our study), most species became extinct in forest fragments surrounded by a static matrix (water). The recovery observed at the BDFFP was mostly due to the recolonization of previously deforested areas and forest fragments by specialist species, which increased in all sampled habitats during the second period. This recolonization is likely attributable to an increased diversity of food resources in the matrix, allowing to fulfil the energetic requirements of a larger set of species other than generalists. Additionally, many specialist bats at the BDFFP are highly edge-sensitive34,35,36 and consequently the maturation of the secondary vegetation adjoining fragment edges might have increased habitat suitability by reducing the magnitude of edge effects across the landscape. Notwithstanding major morphological and ecological differences between rodents and bats, the widely different trajectories exhibited by assemblages inhabiting true island systems11 and fragments embedded within a regenerating matrix (this study) highlight the potential of second growth forests to mitigate fragmentation-related extinctions.

In spite of the signs of recovery exhibited by specialist species across our study landscape ~30 years after forest clearance, our results do not support an increase in assemblage similarity between continuous forest and secondary forest over time. This, together with evidence that bat assemblages in smaller fragments (≤10 ha) and secondary forest sites still differ considerably from continuous forest in terms of species richness, evenness, composition and abundance34,37, suggests that the second growth matrix at the BDFFP still acts as an environmental filter. This filtering shapes bat assemblages in a trait-mediated manner, selectively benefiting bat species with a phytophagous diet and reduced body mass38,39. Similar pervasive consequences of forest clearance can still be detected in birds40,41,42 and primates43 in the BDFFP landscape, highlighting that, although second growth can be of conservation significance, primary forest is of irreplaceable value23,44.

Our results have important implications for the interpretation of land-use change studies using space-for-time approaches. Researchers rarely have the opportunity to collect data prior to the main disturbance events that mould humanized landscapes. Consequently, studies often have to rely on nearby sites where the target impact has not yet taken place and assume that these accurately mimic pre-disturbance conditions45. Here, we show that the species richness of generalists and both the species richness and abundance of specialists have increased in our reference sites in continuous forest, indicating considerable temporal heterogeneity in undisturbed forest assemblages over a period of ~15 years. This suggests that space-for-time results may be undermined not only by confounding effects arising from spatial heterogeneity but also by constraints associated with the temporal heterogeneity of the assemblages inhabiting sites used as spatial surrogates. This shifting baseline somewhat limits our capacity to attribute the observed changes in fragment and secondary forest bat assemblages entirely to the effect of matrix maturation. However, the contrasting temporal trends in the species richness of generalists in continuous forest and secondary forest, i.e. increase in continuous forest vs. decrease in secondary forest, indicate that secondary forest regeneration plays an important role in the assemblage dynamics across the landscape. Yet, our limited knowledge of the extent of spatial and temporal dynamics of generalist and specialist species in continuous forest and how these fluctuations may relate to patterns in fragmented landscapes still precludes a full understanding of these systems and therefore should be a high priority for future research.

Despite the controlled, experimental conditions of the BDFFP, our findings add to an increasing body of evidence (e.g.9,15) emphasizing that the transposition of patterns of biodiversity persistence in island ecosystems to fragmented terrestrial settings can be hampered by the dynamic nature of human-dominated landscapes, and consequently predictions under the island biogeographic framework can distort our understanding and misguide conservation strategies. Accordingly, and in light of the contrasting temporal trajectories of specialist and generalist species at the BDFFP, alternative theoretical frameworks, importantly, countryside biogeography46, in which species’ differential habitat affinities can be accommodated, emerge as better suited for forecasting biological changes in human-modified landscapes9.

In spite of some noteworthy regional declines in deforestation rates (e.g. Brazilian rainforests), tropical forest loss has increased by more than 2,000 km2/year since the beginning of the millennium47. Much of these deforested areas will be used to meet the growing demands for food and biofuel of an increasing human population48. However, following forest clearing, some converted areas are allowed to regenerate, giving rise to human-modified landscapes in which secondary forests account for an increasing proportion of total forest cover16. Our results, although contingent on the existence of nearby source populations, add to the evidence that secondary forests offer a tremendous opportunity for both assisted and non-assisted habitat restoration49. Among bats, frugivorous species are effective seed dispersers, especially of pioneer plant species50 and gleaning insectivores play essential roles in the reduction of herbivory levels through trophic control of herbivorous arthropods51. Populations able to persist in primary forest remnants can therefore enhance second growth successional processes and by doing so, aid in maintaining the provision of ecosystem services and improve habitat quality and connectivity in regenerating tropical forests.

To a large extent, the conservation potential of the world’s tropical secondary rainforests depends on the legal framework underpinning their governance. In the Brazilian Amazon, the state of Pará has recently introduced legislation recommending protection of >20-year-old secondary forest (as identified through inspection of satellite images) as well as younger stands depending on the total stand basal area of native trees and palms52. Although legal protection per se does not ensure long-term safeguarding of the services provided by second-growth forests, it represents a critical step towards their management. We therefore urge researchers, practitioners and policy makers to adopt similar protective measures, especially in areas where primary forest is scarce or highly fragmented.

Human-modified tropical landscapes are in continuous flux, with areas of secondary forest being converted to agricultural land and vice-versa. Vegetation disturbances, both anthropogenic and natural (e.g. fire), are irregular in space and time, moulding mosaic landscapes in which the classic split between fragments and matrix is blurred53. The ability of species to persist in such dynamic landscapes will ultimately depend on the interaction between their intrinsic traits (e.g. mobility and life span), interspecific interactions and the availability of habitat capable of meeting their specific resource needs. Although hotly debated23,54,55, the “rescue” potential of secondary forests in these dynamic landscapes is far from negligible16. While adding to mounting evidence that secondary forests are of conservation value, our, and many other long-term studies at the BDFFP (reviewed by Laurance et al.)25 and elsewhere in the tropics (e.g.)17,56 reveal that continuous primary forest and large (>100 ha) forest fragments are of overwhelming importance for the conservation of tropical biodiversity.

Our results show that specialist bats, which occurred at low abundances in secondary regrowth and in forest fragments ~15 years after the experimental clearing, have benefited from the increased permeability of the matrix associated with the maturation of the secondary forest in the matrix during the last 15 years. This suggests that matrix management, and specifically the management of regenerating (secondary) forest can majorly dictate the future of biodiversity in human-modified landscapes, including that remaining in fragments of natural vegetation.