Globalization of trade is increasingly leading to the introduction of species outside their native distribution ranges. These alien species, once introduced and successfully established, may become invasive and expand their ranges, severely affecting ecosystems and economies [1
]. Several authors have analyzed the economic impacts of invasive forest pests or other invaders [1
], but there are comparatively few assessments of the potential ecological effects of biological invasions at the forest landscape scale. Some studies have evaluated the effects of invasive forest pests on local forest species composition, structure, or functioning [6
]. There is, however, a significant lack of knowledge on the wider-scale impacts that invasive forest pests may have on the performance, conservation goals, or functioning of protected area (PA) networks at a regional or national level.
As invasive species cause some of the greatest conservation problems in PAs worldwide [9
], studies that can guide the related management and control efforts are urgently needed. In networks of PAs, biological invasions may disrupt the functional corridors and connectivity between PAs that serve native species of conservation concern. Poor PA connectivity for native flora and fauna may eventually reduce native genetic and species diversity in forest ecosystems due to the reductions in gene flow, in metapopulation dynamics, and in the ability of species to shift their ranges as a response to climate change, among other factors [10
]. For these reasons, the United Nations Convention on Biological Diversity (CBD) adopted a Strategic Plan for Biodiversity for the 2011–2020 period, in which the international community agreed, under Aichi Target 11, to make efforts towards well-connected systems of PAs [12
]. Recent assessments have shown, however, that most of the countries lag behind the PA connectivity target for the year 2020, and that considerable efforts are needed to improve the connectivity of PA systems globally [13
The presence of the pine wood nematode (PWN; Bursaphelenchus xylophilus
Steiner & Buhrer, 1934 (Nickle, 1970)) in Europe for almost two decades has caused a considerable ecological, social, and economic impact [14
]. The PWN, which is native to North America, can cause severe tree wilt and ultimately kill coniferous trees in a matter of weeks [15
] under suitable climatic conditions that trigger the pine wilt disease. European and Asian coniferous tree species, which have not evolved alongside the parasite, are particularly vulnerable to it [17
]. After causing massive mortality in Asia [18
], PWN was first detected in Europe in 1999, in the Setubal area of Portugal, near Lisbon [19
]. Since then, it has quickly expanded, aided by the native insect Monochamus galloprovincialis
], its only known vector in Europe, and by the transport of infected wood [21
]. Currently, the PWN outbreak encompasses more than 30% of mainland Portugal. Beyond the obvious potential economic impacts due to the loss of products with market value [2
], the epidemic of this invasive pest may cause the greatest damage due to the loss of non-market ecosystem services [22
]. Important and fragile Mediterranean coniferous forests may be altered, and their biodiversity and connectivity impacted, due to the expansion of the PWN.
Here, we assess the impact of the spread of the invasive pine wood nematode (PWN) on the Natura 2000 network of protected areas (PAs) in mainland Portugal, considering both the individual PAs and the corridors between PAs. The Natura 2000 network of PAs in the European Union (EU) is one of the largest coordinated international actions for biodiversity conservation. The aim of this network is to ensure the long-term persistence of Europe’s most valuable and threatened species and habitats, listed under both the Birds Directive (79/409/EEC, amended as 2009/147/EC) and the Habitats Directive (92/43/EEC), many of which are forest habitats and forest-dwelling species. Currently, the Natura 2000 network consists of more than 27,000 sites covering 18.1% of the EU territory and 20.6% of Portugal’s land area [23
]. The Natura 2000 sites in Portugal include forest habitats that have been declared as priority habitats for conservation in the EU legislation, such as coastal and inner wooded dunes with Pinus pinaster
and/or Pinus pinea
(habitat 2270 in Annex I of Directive 92/43/EEC).
Our assessment relies on a combination of recently developed methods for connectivity modelling in heterogeneous landscapes. Using these methods, we map the corridors between Natura 2000 forest sites, characterize the width of the permeable land strips along these corridors, prioritize the key corridors in which to concentrate conservation management efforts, and identify the bottlenecks (weak sectors) along these priority connectors. Then, using data on the observed PWN range for 2016, we examine the extent to which the coniferous forest habitat patches and connectivity providers in this network of PAs are being compromised by the pine wilt disease. In doing so, we provide both an assessment of these important landscape-level ecological impacts of an invasive forest pest, and highlight particular areas in which concentrated control could mitigate the PWN impacts on key native forest habitats and corridors. More generally, our study proposes and demonstrates a methodological approach that can be used to assess these impacts and priority control areas for other invasive forest pests.
Previous studies about the impacts of the pine wood nematode (PWN) have mainly focused on economic aspects [2
]. In particular, the economic impact of the PWN has been estimated at 1.0 billion €/year in Europe [2
] considering wood and wood production losses. Other important PWN effects are not easily quantified in economic terms and include changes in soil properties and pine forest communities [6
], in landscape structure and forest succession [8
], and in regeneration [16
]. These effects, however, have been mostly studied outside Europe. The consequences of changes in the structure, function, and composition of the PWN invaded ecosystems and landscapes are still largely unknown in Europe. This is particularly the case for the potential impacts of the PWN, or of other damaging invasive forest pests, on the functionality of protected area networks.
With about 21% of mainland Portugal under Natura 2000 protection and a PWN outbreak that has already expanded, after almost two decades, to more than 30% of the country, the forest habitats in the Natura 2000 network might be facing new, and poorly understood, challenges. Given that the PWN is able to kill susceptible coniferous trees in a matter of weeks [15
] and that we have found that, as of 2016, half of all Natura 2000 coniferous forests are already within the areas infected by the PWN, the impact and pressures of the PWN might become more relevant to the conservation and management of coniferous forest ecosystems and priority habitats in Portugal. High mortality rates have been reported or are expected in PWN-infected coniferous forest stands in Asia and Europe [46
]. The oldest and biggest pines seem to be more affected by the PWN-caused mortality, as reported in the Tróia peninsula, near the city of Setúbal, in Portugal [14
]. These old large trees are also those that may have a higher conservation and biodiversity value [48
], as well as a particularly important role in the sequestration of new carbon in the forest [50
]. The PWN-caused mortality in coniferous forest may, therefore, result in large shifts in forest community composition, canopy structure, and related ecological functions and processes. These shifts may be particularly significant in unique Mediterranean habitats such as the coastal and inner wooded dunes with Pinus pinaster
and/or Pinus pinea
, which have been included in the European lists of priority habitats for conservation (Annex I of Directive 92/43/EEC), and which we have here shown to be largely distributed in areas under the impact of PWN spread.
In certain areas, the PWN may disincentivize the planting or maintenance of tree species that are susceptible to it, which can have an additional knock-on effect on biodiversity if it indirectly promotes the planting of non-native tree species, specifically Eucalyptus. In fact, according to the results of the 6th Portugal National Forest Inventory, the area covered by Eucalyptus species in Portugal has increased by 13% between the years 1995 and 2010, in contrast with the 27% reduction in the area occupied by maritime pine (Pinus pinaster
Ait.) in the country [24
]. In 63% of the area lost by Pinus pinaster
, no other tree species have been introduced to replace that niche, while the remaining 27% has been planted with Eucalyptus. Although these trends may be driven by multiple incentives [51
] and a complex set of causes, including market demands and species productivity in each particular location, the expansion of PWN is likely to aggravate, through direct and indirect mechanisms, the decline of some pine tree species and forest habitats in Portugal.
The ability of wildlife species, and of the genes and propagules they carry, to move across heterogeneous landscapes is critical for maintaining regional population persistence and to allow native biota to shift their ranges in response to climate change [52
]. The connectivity of the PA system in Portugal strongly depends on the permeability of the unprotected landscapes [13
]. Here, we have shown that coniferous forests cover a large portion of the corridors that best allow forest species to traverse these unprotected landscapes in their movements between Natura 2000 sites. Furthermore, these coniferous corridors are strongly affected by the PWN range expansion, even more so than the coniferous forests within the protected Natura 2000 sites. Our findings suggest that the PWN expansion may significantly weaken the functionality of the network of Natura 2000 forest sites in Portugal, by having a particularly large effect on the more fragile and narrow parts of the priority corridors (their bottlenecks), in which the decline of pine forest cover may be most damaging to the connectivity of the PA system. The fact that the coniferous forest in these key corridors is significantly more affected by the PWN spread than the forest within the Natura 2000 sites may be a consequence of the modalities and patterns of PWN spread in Portugal. These modalities are, on the one hand, the natural spread of the nematode by the dispersal flights of its only known vector in Europe, the longhorn beetle Monochamus galloprovincialis
], and, on the other hand, the human-mediated dispersal of the disease through the accidental transportation of infected beetles in timber trade vehicles [21
]. While vector beetle dispersal may operate similarly, and with the same intensity, in protected or unprotected forests, the human-mediated dispersal is strongly linked to human population and road density and to the presence of the wood processing industry [53
]. All these anthropogenic factors may be considerably lower in the Natura 2000 sites than in the coniferous forest in the corridors outside the PA system, which may be embedded in, or closer to, landscapes with a more intense human footprint.
The magnitude of the potential impacts of PWN on the priority forest habitats, corridors, and Natura 2000 sites in Portugal indicates that mitigating their effects on the conservation status of the coniferous forest ecosystems could benefit from spatially-targeted management measures to control the pest’s spread. These measures could include the intensive surveillance of coniferous forests for the early detection and removal of infected trees (before PWN-infected beetles emerge and further infect other trees in the stand), clear-cutting in localized areas to break the continuity of pine forest cover and prevent further PWN spread, mass trapping of the vector beetle, and control of the origin and sanitation of pine wood for transportation [14
], among others. According to recent results [43
], these measures may need to be applied in combination, as part of integrated containment strategies, to increase their effectiveness in halting or slowing down PWN spread. Other longer-term measures that could contribute to enhancing the resilience of the coniferous forest stands to the arrival of the disease are silvicultural treatments, such as thinning, aimed at increasing tree vigor or tree species diversity [56
], or promoting the establishment of pine half-sib families with higher genetic tolerance to PWN [59
]. These measures are of interest because, in more diverse natural areas, the loss or dramatic reduction in density of one species may be more easily compensated by other suitable species filling the new gaps. However, [61
] noted that the changes in canopy structure and stand composition caused by forest pests may trigger subsequent impacts to the community of flora and fauna that inhabit those sites. Such impacts may not be easy to compensate even with dedicated management efforts. A compensatory response by other tree species that grow to occupy the space created by pest disturbances can reestablish some forest services such as carbon sequestration or water regulation or purification, while others could remain permanently disrupted, such as the specific biodiversity supported by the diseased tree species [62
Some of the above-mentioned measures for controlling PWN spread, such as the felling of infected trees and, particularly, clear-cuts to break the continuity of the forest cover, may be in conflict with the aim of maintaining or promoting the connectivity of forest habitats and PAs for native biota. This may be particularly the case when the areas that might be key to containing the spread of the PWN [43
] intersect with important corridors providing connectivity between PAs. The tension between these two potentially conflicting objectives may require further research to elucidate two related interactions: first, the degree to which the spread of the PWN, or of other invasive pests, may be enhanced by the corridor conservation or restoration measures aimed to promote PA connectivity; and second, the degree to which the invasion control efforts may negatively impact, or may be adapted to minimize the impacts on, the connectivity of native species of conservation concern.
Here, we have considered the potential impacts of current PWN spread on Natura 2000 sites and their connectivity, up to 2016. However, predictions of future PWN spread indicate that, in the absence of efficient control measures, the PWN range will continue to expand naturally, through the dispersal flights of the vector beetle, towards the rest of Portugal, and eventually spread into Spain in about five years [43
]. In less than 10 years, it may reach the major forest and climatic corridors that provide a gateway for subsequent expansion towards the rest of the Iberian Peninsula and, in the longer term, towards other European countries [43
]. Therefore, the impacts here reported on the coniferous forest Natura 2000 sites and corridors are likely to be aggravated in the next years.
Our approach and assessment could be refined, either in Portugal or in other areas that may be affected by the PWN in the future, by considering the different susceptibility to PWN infection of individual European pine tree species as reported by recent studies [63
]. The stone pine (Pinus pinea
L.), for example, is considerably less susceptible to PWN infection than Pinus pinaster
]. In the Portuguese purely coniferous forests analyzed here, Pinus pinaster
is, however, much more abundant than Pinus pinea
: 89.5% and 9.5% cover, respectively, according to the COS map of Portugal. The magnitude and patterns of the PWN impacts on the Portuguese Natura 2000 network reported here are therefore unlikely to significantly change by a more detailed characterization of tree species susceptibility. However, between-species differences might be more relevant in specific smaller study areas. Finally, we emphasize that the data on the PWN range that we used describe the areas that are infected by PWN but not tree decline or mortality rates in each site. The latter may be addressed in further studies if such tree-level infection and mortality information becomes available at the national scale or, most likely, in some smaller areas through intense forest surveillance and inventory based on high-resolution remote sensing and/or field data.