INTRODUCTION
Global biodiversity is declining continuously in the Anthropocene (Dirzo
et al., 2014), which has been widely attributed to conversion from
natural landscapes to agriculture, pastures and urban settlements (Foley
et al., 2005; Newbold et al., 2016). Recent findings revealed that
intensive human land-uses cause species losses and filter specific sets
of functional traits, with homogenizing effects on entire biotic
communities (Gámez-Virués et al., 2015; Newbold et al., 2015, 2020).
This has severely altered ecosystem functioning, which largely relies on
biodiversity (Soliveres et al., 2016; Barnes et al., 2017). Although
biodiversity decline is broadly attributed to intensive land-uses,
current evidence of land-use impacts is mostly based on studies focused
on isolated land-use types, such as urbanization (Monteiro-Júnior et al.
2014), agriculture (Gossner et al., 2016), or pasture (Wang et al.,
2018). Consequently, most studies fail to capture the complexity of
biodiversity responses to intensive cover of multiple land-uses that
operate simultaneously in multiple ways.
Recent evidence shows that taxonomic richness responses to intensive
human land-uses differ among trophic groups (Allan et al., 2014; Le
Provost et al., 2021), suggesting that using taxonomic richness alone
hinders generalizing overall biodiversity responses of entire
communities to land-use changes. For improved clarity herein, we define
‘community’ as all the biota of an ecosystem, and ‘assemblage’ as any
taxonomic subset of the ecosystem (e.g., fish, arthropods, macrophytes;
Fauth et al. 1996). The problem of focusing on taxonomic richness can be
mitigated by using trait-based approaches, and empirical evidence has
shown that different biotic assemblages sharing similar traits often
respond similarly to intensive land-use (Gámez-Virués et al., 2015;
Newbold et al., 2020). For instance, intensive land-use impacts may be
stronger for large apex consumers, as they are disproportionately
vulnerable to human pressures (Estes et al., 2011; Enquist et al.,
2020). Moreover, biodiversity changes at the level of one assemblage may
cascade to other assemblages. For example, there is evidence that
changes in plant diversity have strong bottom-up effects on the
diversity of arthropods (Scherber et al., 2010). Similarly, subtle
shifts in diversity of apex consumers (e.g., fish) may exert cascading
effects on the diversity of primary consumers (Duffy et al., 2007;
Antiqueira et al. 2018). Such intensive land-use impacts on the
diversity of plants and apex consumers likely alter the structure of
entire communities with negative consequences for ecosystem functioning.
Human land-uses have severely altered ecosystem functioning through
direct and biodiversity-mediated indirect pathways (Barnes et al.,
2017). Direct effects involve changes in environmental quality. This is
particularly true in aquatic ecosystems where loss of riparian
vegetation, decrease in depth, depletion in oxygen availability and
increased nutrient inputs cause deterioration in water quality and
compromised ecosystem functioning (Walker & Walters 2019). Indirect
effects are more difficult to predict because they manifest via multiple
biodiversity facets such as taxonomic and functional diversities (Le
Provost et al., 2020; Moi & Teixeira de Mello, 2022). Given that both
taxonomic richness and functional traits underlie the ability of
ecosystems to maintain their functions (Leitão et al., 2018; Le
Bagousse-Pinguet et al., 2019), a joint evaluation of these two facets
of biodiversity is essential to understanding how intensive human
land-use alters ecosystem functioning. Human land-use may weaken the
linkages between organisms, threatening, in turn, the capacity of
biodiversity to promote ecosystem functioning (Eisenhauer et al., 2019).
Recent analyses revealed that the indirect effects of intensive human
land-uses could be as strong as associated direct effects (Moi &
Teixeira de Mello, 2022). Thus, there is an urgent need to disentangle
the direct and indirect effects of human land-uses on ecosystem
functioning.
Here, we tested how the intensification of multiple human land-uses
types affects taxonomic and functional diversities of three stream
assemblages (fish, arthropods and macrophytes). We further investigate
the direct and indirect (biodiversity-mediated) effects of intensive
land-use cover on ecosystem functioning (Figure S1). We used a database
of 61 stream sites dispersed across an area of 507,003 km² in two
Neotropical areas (Amazonia and Uruguay; Figure 1) that harbor
exceptionally high levels of biodiversity (Antonelli et al. 2018). We
sampled streams spanning different cover of land-use types: agriculture,
pasture, urbanization, and afforestation (Figure 1b,c). Those four human
land-uses have expanded globally, largely due to the rapid expansion of
commercial monocultures such as soybean and cereals, as well as
livestock grazing, cities, and eucalyptus, pine and oil palm plantations
(Grimm et al., 2008; Gossner et al., 2016; Maloney et al., 2020). We
decomposed functional diversity into three independent trait categories:
(i) recruitment and life-history, (ii) resource and habitat use, and
(iii) body size, all of which can mediate cross-assemblage responses to
intensive land use (Gámez-Virués et al., 2015; Benejam et al., 2016). As
a measure of ecosystem function, we focused on standing fish biomass,
which is a commonly used metric of ecosystem functioning, underpinning
ecosystem services, such as fisheries production and food supply
(Benkwitt et al., 2020).
We accounted for the effects of climate (temperature and precipitation),
local environmental factors (sediment heterogeneity and water quality
deterioration), and stream morphology (depth) to test the hypothesis
that taxonomic richness, functional diversity, and diversity of trait
categories are negatively affected by intensive human land-use types. We
also predicted that (i) fish, arthropod, and macrophytes assemblages
would respond differently to different land-use types (Hughes et al.,
2009); (ii) apex consumers (fish and arthropods) would be more strongly
affected by intensive land-uses than primary producers (macrophytes);
(iii) negative effects of intensive human land-uses on plant diversity
would have cascading effects on arthropod and fish diversities, leading
to declines in standing fish biomass; and (iv) indirect
(biodiversity-mediated) effects of intensive land-uses on standing fish
biomass would be as strong as the direct effects. Our findings suggest
that intensive agriculture, pasture, and urbanization had consistently
negative effects on taxonomic and functional diversities of fish,
arthropod, and macrophyte assemblages, as well as declines in standing
fish biomass, through both direct and indirect effects.