The decline of farmland birds in Spain is strongly associated to the loss of fallowland

Abstract

Farmland bird populations have strongly declined across Europe over the last decades due to agriculture intensification, despite successive reforms of EU’s Common Agricultural Policy (CAP). In parallel, CAP has led to a reduction of fallow land, a critical habitat for biodiversity in agroecosystems. Fallow land in Spain, a country harboring the largest European populations of many endangered farmland birds, has decreased by 1.1 million ha in 15 years. The significant positive relationship between yearly change rates of the Spanish Farmland and Cereal Bird Indices (FBI and CBI) and fallow surface change highlights the adequacy of fallow land cover as an indicator of the state of farmland bird communities at country level. Moreover, the strong and positive association between the reduction in abundance of the fallow specialist little bustard and fallow surface suggests a potential causal link between these two factors. These results highlight the need for a new CAP that guarantees the maintenance of fallow land in European agroecosystems if farmland bird populations are to be conserved.

Full text

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The decline of farmland birds in
Spain is strongly associated to the
loss of fallowland
Juan Traba
1,2 & Manuel B. Morales1,2
Farmland bird populations have strongly declined across Europe over the last decades due to agriculture
intensication, despite successive reforms of EU’s Common Agricultural Policy (CAP). In parallel, CAP
has led to a reduction of fallow land, a critical habitat for biodiversity in agroecosystems. Fallow land
in Spain, a country harboring the largest European populations of many endangered farmland birds,
has decreased by 1.1 million ha in 15 years. The signicant positive relationship between yearly change
rates of the Spanish Farmland and Cereal Bird Indices (FBI and CBI) and fallow surface change highlights
the adequacy of fallow land cover as an indicator of the state of farmland bird communities at country
level. Moreover, the strong and positive association between the reduction in abundance of the fallow
specialist little bustard and fallow surface suggests a potential causal link between these two factors.
These results highlight the need for a new CAP that guarantees the maintenance of fallow land in
European agroecosystems if farmland bird populations are to be conserved.
Farmland is the most important habitat for bird conservation in Europe, harbouring more than 50% of bird
species in the European Union (EU) and 55% of European bird species listed in the IUCN Red List1,2. Moreover,
European farmland birds are used as general indicators of the quality of agricultural habitats for biodiversity
through an ocial agri-environmental indicator, the Farmland Bird Index (FBI)3.
Agriculture intensication is the main driver of the current biodiversity loss in Europe4 and considered to
be the major cause of farmland bird declines across the continent2. Agriculture intensication is a multifactorial
process acting at eld and landscape level4,5, one of whose main consequences is the loss of environmental hetero-
geneity at dierent spatial scales5,6. At eld scale, yield and revenue maximization has led to an increase of inputs
and agrarian operations (e.g. soil disruption though ploughing) that have severely reduced local biodiversity7,8,
including arable plants, invertebrates and birds9. is process has also led to the loss of semi natural elements
of elds and their close neighbourhood (e.g. eld margins), further contributing to biodiversity declines7,8. At
landscape scale, land consolidation and disappearance of yearly (or longer) crop rotation have favoured landscape
simplication and homogenization, through the loss of non-cultivated elements (e.g. margins, hedges, fallow and
wasteland), further reducing habitat availability for wildlife10–12. EU’s Common Agricultural Policy (CAP) has
been one of the main drivers of agriculture intensication in Europe13, promoting landscape homogenisation,
increased use of agrochemicals and the abandonment of less productive elds4,5, despite some eorts to reverse
the biodiversity loss through the application of agri-environmental schemes (AES)14. Moreover, AES have been
only partially successful due to unclear objectives, design deciency and low uptake15, and dierent global e-
ciency evaluations have yielded mixed results16,17. In synthesis, agriculture intensication can be considered the
major cause of farmland bird and other taxa declines across the continent2,4,6.
e proportion of fallow land can be used as a measure of landscape scale heterogeneity and thus of agricul-
ture intensication18,19. Fallow land is the cultivated land that is not seeded for one or more growing seasons20.
us, fallows include dierent semi-natural grasslands and pastures that will eventually be ploughed for a new
crop cycle19. Adequately managed, fallows are one of the most important habitats for wildlife, and particularly for
farmland birds, in agricultural landscapes, due to the high diversity and abundance of food resources that they
provide such as weeds, seeds, and invertebrates, as well as vegetation cover for foraging or nesting6,21. In Spain
and other Mediterranean countries, fallows have been crucial for the maintenance of farmland biodiversity18,22.
1Terrestrial Ecology Group, TEG-UAM, Department of Ecology, Universidad Autónoma de Madrid, Darwin, 2,
E-28049, Madrid, Spain. 2Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad
Autónoma de Madrid, Darwin, 2, E-28049, Madrid, Spain. Juan Traba and Manuel B. Morales contributed equally.
Correspondence and requests for materials should be addressed to M.B.M. (email: manuel.morales@uam.es)
Received: 28 January 2019
Accepted: 14 June 2019
Published: xx xx xxxx
OPEN
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In spite of its relevance for wildlife and of more than two decades of EU’s agri-environmental measures aiming at
preserving farmland biodiversity, the surface of fallow land has signicantly decreased in Spain during the same
period (Fig.1), implying a loss of 1.1 million ha. Such decrease has been specially marked aer 2008, when EU
regulations put an end to farmers’ obligation to keep fallow 10% of their land. In neighbouring Portugal, fallows
have decreased by 24.4% in only three years, between 2013 and 201623.
In the Iberian Peninsula, dry cereal farmland, also known as cereal-steppe22, is the dominant agricultural hab-
itat and hosts important populations of threatened steppe and farmland birds, including species whose European
or world strongholds are found in Iberia22. Overall, more than 80% of steppe bird species show an unfavourable
conservation status in Europe1.
Parallel to the decline of fallows, the populations of most of Spanish farmland bird species have declined
during the 1990–2000 period1 and aerwards24. A species of particular conservation concern is the little bus-
tard Tetrax tetrax, an endangered steppe bird included in the Annex I of EU’s Birds Directive whose popula-
tions have declined by 50% between 2005 and 201625. e little bustard is a fallow specialist linked to cereal
steppes21,26,27 whose negative trend in Spain between 1998 and 2017 - based on data from the Spanish Common
Bird Monitoring Program (CBMP)24 - could be associated to the negative trend of fallow surface over the same
period.
Declines are similar or even stronger in other globally threatened farmland birds24. ese bird declines could
also be associated with the decrease of fallow surface in Spain, but information on this regard is lacking. e aim
of this work is to test the relationship between farmland bird trends and changes in fallow surface in Spain. More
specically, we examine the relationship between changes in fallow land and the change rate in the population
index of a fallow specialist, the little bustard, and the general FBI for Spain. Additionally, we examine the relation-
ship of changes in fallow land with a combined population index of those species considered as cereal specialist
(i.e. more abundant in cereal farmland than in other agricultural landscapes) under the Spanish CBMP (the cereal
bird index, CBI) in order to assess the potential impact of fallow loss in the most extended agricultural system
of the country28. According to the habitat relationships of these species described in the literature, we expect a
close association of changes in the two combined indices considered (FBI and CBI), as well as the little bustard
population index, with fallow trends.
Results
In Spain, young and old fallows signicantly decreased since 2002 (Fallows: −16.1%; Old Fallows: −41.8%;
Fig.1). e change rate of the little bustard population index during the period 2002–2017 was strongly cor-
related with the change rate of fallow surface over the same period (adjusted R2 = 0.761; p < 0.0001; Fig.2A).
When the change rate of the Spanish FBI was considered, the association with the fallow surface trend was again
strongly signicant (adjusted R2 = 0.644; p < 0.001; Fig.2B). Finally, when the change rate in the Spanish CBI was
considered, the association with fallow trend was even more signicant (adjusted R2 = 0.668; p < 0.001; Fig.2C).
Discussion
ese results indicate a nation-wide relationship between the temporal trend in the amount of a particular habitat
type linked to extensive agriculture, that is fallow land, and the population trends of farmland birds. e relation-
ship is highly explicative for the global Spanish farmland bird and the cereal specialist indices, and particularly
for the fallow specialist and strongly declining little bustard. e decline is especially pronounced when the yearly
change of fallows falls below −20% and the values of the three indices dramatically collapse.
It is important to bear in mind, however, that this assessment considered only trends in fallow surface, but
not changes in fallow management. Unfortunately, available ocial statistics on this regard are fragmentary and
do not cover the entire period considered in our analysis, although they clearly indicate a trend to increasing
eld-level intensication. Overall pesticide sales in Spain increased by 5% between 2011 and 20163, and commer-
cialization of herbicides and fungicides increased by 16.2% and 21.2%, respectively, between 2011 and 201728.
Similarly, the use of Nitrogen mineral fertilizers increased in the country from 55.0 kg/ha to 63.6 kg/ha on average
between 2011 and 2016, although that of Phosphorus slightly declined from 11.2 kg/ha to 10.7 kg/ha in the same
Figure 1. Temporal trend in the surface occupied by fallow land in Spain (2002–2017). e linear regression
line is shown in blue, and 95% Condence Intervals in grey (linear regression: adjusted R2 = 0.800; p < 0.0001).
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period3. In parallel, direct seeding or no-till farming, an agrarian technique with minimum soil disturbance but
using herbicide for weed control, has signicantly increased by 122.6% between 2008 and 2016, while the surface
of non-managed fallows has decreased by 35.62% in the same period28. ese management changes are expected
to have important negative eects on biodiversity, including bird species4. Nevertheless, the decline in fallow
surface is not the only large scale land-use change occurring in Spain in this period. More specically, irrigated
woody crops (i.e. olive groves and vineyards), which are largely unsuitable for farmland birds22 have increased by
105% between 2004 and 2017, yielding a surface gain of ca. 416,000 ha5,28.
In any case, our assessment of bird trends in relation to fallow surface shows how a widely recognized and
large-scale indicator of agriculture intensication like fallow land cover19 and an ocial EU indicator of the general
environmental status of farmland like the FBI can be inter-related to assess the overall health of a country’s agroe-
cosystems. is is corroborated by the subset of species more clearly dependent on cereal farmland, the agricultural
system where fallows have traditionally been more important due to crop rotation18,19. In addition, cereal farmland
is being particularly aected by the mentioned growth of intensive woody crops. ese conclusions were consistently
reinforced when we examined the trend of the little bustard, a fallow specialist linked to cereal farmland26,27.
Fallows are a key component of farmland heterogeneity in the Iberian Peninsula18,19,29. At landscape scale, fal-
lows provide a habitat that most farmland birds use complementarily to others (e.g. cereal crops, wastelands) for
dierent vital functions such as foraging, mating or nesting29,30. Moreover, in intensive farmland, fallows can be
Figure 2. Relationship between species and fallow land annual change in Spain between 2002 and 2017. (A)
Little bustard (adjusted R2 = 0.761; p < 0.00001). (B) Farmland birds (adjusted R2 = 0.644; p < 0.001). (C) Cereal
birds (adjusted R2 = 0.668; p < 0.001). Linear regression lines are shown in blue, and 95% Condence Intervals
in grey.
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the only habitat where limiting resources like food or adequate nesting sites are found (Moreira et al.30,31, Morales
et al.21,32). At the eld scale, adequately managed fallows can full most requirements of fallow specialists, which
benet from their heterogeneous vegetation structure. For example, little bustard females require more vegeta-
tion cover for nesting, but a relatively open structure at certain height for anti-predator survey, while males select
lower vegetation cover to perform their sexual display21. However, fallows are highly variable in their structure
depending on their age, local soil conditions, water availability and management, among other factors33. As a
consequence, not all fallows are equally suitable for the dierent species, which means that at large spatial scales
such diversity of fallow characteristics should be promoted to maintain rich farmland bird communities31. In this
context, not only the loss of fallows in cereal farmland, but also the intensication of their management, which
leads to bare and resource-depleted ploughs, or heavily herbicide-treated no-till elds, poses a serious threat to
farmland bird populations and helps understand our results on the combined indices used.
e trends in fallow surface and management discussed here are consistent with the multiscale process of agri-
culture intensication4, producing a loss of landscape heterogeneity and thus habitat availability for the dierent
species10–12,34, along with a depletion of key resources due to eld-level management7,8 erefore, the large-scale
association of Spanish farmland bird trends with the loss of fallow land highlights the urgent need to reverse
the current trend to a highly intensive agriculture in Spain if the European and even world-level population
strongholds of many steppe birds are going to be conserved. To that purpose, the upcoming generation of EU
agri-environmental schemes to be implemented under CAP aer 2020 should encourage the maintenance of fal-
low land. Among the tools that CAP might incorporate would be conditioning the reception of subsidies by farm-
ers to leaving fallow a minimum surface of the land they manage. Moreover, a return to the obligation to keep at
least 10% of their land as fallow may help restore the conditions previous to 2008. At the same time, in order to
guarantee ecologically functional fallows in sustainable and environmentally healthy agricultural landscapes in
Europe, eld-level intensication should be discouraged with the aim of reducing agro-chemical inputs. To that
aim, ambitious regulations addressing all levels of the food production chain up to the consumer are required.
Methods
Estimation of trends in fallow surface. Data were obtained from the National Survey on Agrarian
Surfaces (ESYRCE), of the Spanish Ministry of Agriculture, Fisheries and Food MAPA28, for the period 2002–2017.
ese statistics are collected for all the country’s agrarian districts, although for public use they are scaled up to
the province level. erefore, they synthesize country-wide exhaustive information on agrarian land use change.
We merged surface (ha) of young and old fallows in a single variable; that is, unsown elds lasting for 1 (young) or
more years (old), but always within the rotation cycle. en, to estimate the overall annual rate of change in fallow
surface in Spain, we calculated a yearly rate of change (%) since 2002, this year considered as 0.
Estimation of change rate in bird populations. We used bird data from the CBMP in Spain (SACRE
Program), which is active since 1998. However, since fallow surface data were available only from 2002 onwards,
we selected data for the period 2002–201735. SACRE comprises data from censuses carried out by volunteers
in a set of UTM 10 × 10 km cells distributed across the country (see Supplementary Fig.1), which are sampled
every year, following the same standard methodology35. From these census data, SEO/BirdLife provides a bird
population abundance index for each species and year, estimated using the Trend and Indices for Monitoring
data (TRIM) soware by tting log-linear regression models to count data with Poisson error terms36. From this
index, an annual change rate is estimated for each species, in a way analogous to that described for fallow sur-
face. erefore, the change rate of the TRIM population index can be used as a country-wide estimate of annual
changes in the abundance of a species or group of species37. We used data for the Farmland Bird Index (FBI) in
Spain, a summary population index that includes information from the species classied as common farmland
birds under the Spanish CBMP (see TableS1). e FBI is an ocial indicator of the quality of EU’s agroecosys-
tems for biodiversity, as well as of the eectiveness of agri-environmental measures applied under European
CAP3. e combined population index for the subset of common farmland birds that are particularly abundant
in cereal farmland (Cereal Bird Index, CBI), provided also by SEO/BirdLife, was used to explore the relationship
of cereal farmland specialists with the variation in fallow surface. Finally, we used the little bustard population
index, as an indicator of the response of fallow specialists to changes in fallow surface.
Analyses. To estimate the relationship between bird trends (Little Bustard index, FBI and CBI) and fallow
land, we tted single linear regressions between change rates of bird population indices and the change rate in
total fallow surface over the period considered.
Data Availability
Data would be freely available upon ms acceptance.
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Acknowledgements
We wish to thank SEO/Birdlife and specically to Juan Carlos del Moral and Virginia Escandell for providing
SACRE data. We are grateful to Pedro P. Olea and Jesús Martínez-Padilla for commenting an earlier dra of
the ms. is is a contribution to the Excellence Network Remedinal 3CM (S2013/MAE2719), supported by
Comunidad de Madrid.
Author Contributions
J.T. and M.B.M. contributed equally to the manuscript, including conceptualization, design, data collection and
formal analysis, and writing.
Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-019-45854-0.
Competing Interests: e authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional aliations.
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