Effects of livestock on vegetation and arthropod community
Livestock grazing reduced vegetation cover and height, prompting trophic
cascade effects on arthropod community. Grass cover differed among
control trees of different farms due to differences in grazing
intensity. Moreover, it was higher beneath the canopies of trees
subjected to one-year and long-term livestock exclosures. Those places
with lower grass height and cover (control trees in all farms) exhibited
lower species richness and diversity. Grass height is a fine predictor
of plant and insect diversity under contrasting grazing intensities
(Kruess & Tscharntke, 2002).
Livestock and phytophagous arthropods compete for the same food
resource: vegetation. Competition takes place through direct and
indirect interactions; both affect each other directly by decreasing
food resources (density-mediated interaction (Dennis et al., 2008; Evans
et al., 2015; Feeley et al., 2006; Werner & Peacor, 2003)). The
interaction is, however, frequently asymmetrical due to differences in
body size that also favour other antagonistic interactions, such as
incidental intraguild predation of phytophagous arthropods by livestock
(Canelo et al., 2021b; Gómez & González-Megías, 2002; Zamora & Gómez,
1993). Moreover, the negative effects of livestock go beyond
phytophagous arthropods and extend to predators and parasitoid species,
which may also be incidentally predated by livestock albeit at lower
rates than herbivores (Berman & Inbar, 2022). Predatory arthropods also
suffer the scarcity of prey (phytophagous invertebrates) due to
livestock grazing (King et al., 2014; Prieto-Benítez & Méndez, 2011).
The richness and diversity of arthropods increased after livestock
exclusion, but, surprisingly, it did not increase with the length of the
exclusion period: it peaked at short-term (one year) exclosures; only
Family level diversity was significantly higher at long-term exclosures
compared to control trees. After one-year of livestock exclusion,
vegetation cover was higher and medium-sized grass prevailed. This meant
more food for herbivore arthropods –owing to the lack of competition
with livestock–, a greater availability of refuge, and reduced
intra-guild predation risk. Local herbivore arthropods at the excluded
trees may increase their population size and new species may arrive from
neighbouring areas (Catford et al., 2012; Harvey et al., 2016; Townsend
et al., 1997). Higher grass cover in one year-exclosures was also
related with an increase of arthropod functional diversity, including an
increase in parasitic species. Therefore, the increase in primary
production triggers a bottom-up trophic cascade at this initial period.
This quick peak supports the predictions of the intermediate disturbance
hypothesis (IDH).
The intermediate disturbance hypothesis predicts a peak of species
richness at intermediate levels of disturbance. Within the context of
our study, this would be the situation after one year of livestock
exclusion. The sequence would be: high disturbance (livestock present),
time-spaced disturbance (one-year exclusion, the disturbance starts to
disappear) and no disturbance (ten-years exclusion). Shortly after
exclusion, grass cover increases and vegetation composition changes
(Sims et al., 2019). In parallel, microhabitat heterogeneity increases
(Song et al., 2020), what favours species with different habitat and
food requirements (for example, open-habitat omnivore generalists,
herbivore specialists, or parasitoids) (Stephan et al., 2017). For
instance, it has been shown that, in Mediterranean regions, bee and ant
richness increases after a wildfire due to the new niches created
(Vidal-Cordero et al., 2023).
Certain species find a suitable habitat at the recently-undisturbed
areas (one-year exclosures), where they may arrive from the
surroundings, and establish in the short-term. This could explain the
similarity between arthropod communities under the one-year-exclusion
trees seen in the Z-diversity graphs. Nevertheless, after 10 years of
livestock exclusion, the competition between arthropods increases. Grass
cover and height increase, and the habitat becomes more homogeneous.
According to the competitive exclusion principle (Hardin, 1960; McPeek,
2014), species which compete strongly for the same resource cannot
coexist; one of them will overtake the other. This is what may happen in
long-term exclosures, the lack of grazing homogenizes the habitat and
promotes competition among herbivores. However, the homogenization of
the habitat may favour certain specialists: as times go by the overall
number of species will be slightly reduced, some will disappear, but
others may increase their abundance.
The slight decrease in taxonomic richness and diversity does not mean
that arthropod communities become homogeneous at long-term exclosures,
rather, they differed a lot among them and compared to the trees of the
other categories. Species composition differed with respect to
short-term exclosures probably because certain some taxa (like
Colembolla) disappear as grass height increases. On the other side, the
rather large variability within long-term exclosure trees shown in the
Z-diversity analysis indicate that communities diverged towards
different and unique species compositions. Further studies considering
additional functional traits will help to understand the process
underlying such temporal changes in arthropod communities.
In summary, our results support the intermediate-disturbance hypothesis
(Connell, 1978; Gao & Carmel 2020; Roxburgh et al., 2004; Svensson et
al., 2007; Yan et al., 2015). Arthropod diversity peaks after short-time
livestock exclusion, where vegetation cover has increased compared to
control trees but habitat heterogeneity is still higher than at
long-term exclosures dominated by tall grass. Regarding the
livestock-driven biological control of acorn pests (Canelo et al.
2021b), the present study shows that intensive grazing does reduce
arthropod taxonomic richness and diversity. Our results also put forward
that the recovery after livestock exclusion is fast.
Thus, the proposed rotative
management combining, within the same dehesa farm, plots with temporary
increased grazing and short-term livestock exclosures, would be
appropriate. This innovative livestock management would increase the
productivity of Iberian oak savannas by reducing acorn pests, while also
preserving its unique and rich arthropod biodiversity.
DATA AVAILABILITY
All sequencing raw data has been deposited at NCBI’s Short Read Archive
(SRA) under project PRJNA928708. Multiplexing information, sample
metadata, vegetation raw data, as well as COI and 16S metabarcoding and
functional traits datasets, can be found along with the supplemental
material.
AUTHOR CONTRIBUTIONS
TC, RB and JB conceived and designed the study; TC, AG and CP-I
conducted the sampling; TC and DM carried out the laboratory work and
the bioinformatic processing; TC, DM and SC performed the data analysis;
TC wrote the first draft, and TC and DM prepared the manuscript and the
figures. All authors reviewed and contributed to subsequent drafts of
the manuscript.
ACKNOWLEDGEMENTS
We are indebted to Rodrigo Esparza-Salas for his assistance in the
laboratory and to E. Morano for his help during the fieldwork. The
authors would like to acknowledge support from Science for Life
Laboratory, the National Genomics Infrastructure, NGI, and Uppmax
(Swedish National Infrastructure for Computing) for providing assistance
in massive parallel sequencing and computational infrastructure. We are
grateful for stakeholders of “Finca Casablanca” and “Finca Las
Carboneras” for their good disposition to conduct this study.
TC was supported by a Margarita Salas postdoctoral fellowship (Ayuda del
Programa de Recualificación del Sistema Universitario Español -
NextGeneration EU, MS-20). DM was supported by the European Union’s
Horizon 2020 research and innovation programme under the Marie
Skłodowska-Curie grant agreement no. 642241 (BIG4 project,
https://big4-project.eu). This research was funded by the project
AGL2014-54739-R from Spanish Ministry of Economy and Competitiveness and
the European Social Fund (Spanish National Plan for Scientific and
Technical Research and Innovation).
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Table 1 . Taxonomic identifications summary.