In Europe, nephropathia epidemica (NE) is a zoonotic disease caused by Puumala virus (PUUV). The main role in the virus transmission mechanism is played by a common arvicoline rodent species, the red bank vole (Myodes glareolus
), that is native in Western Europe forests and acts as the virus reservoir [1
]. The favourable habitat for bank voles in Belgium is broad-leaved forests (BLF) where illumination, soil and humidity conditions give rise to the existence of a moderately dense understory vegetation layer [2
]. Similar to other forest fauna species, the bank vole population depends on interannual as well as on long term variations in the habitat conditions. Consequently, understanding and monitoring key factors associated to changes in the bank vole habitat is crucial to assess future implications of environmental changes for public health. Specially when, as cited by Clement et al.
], different studies have shown the positive correlation between rodent density and prevalence of hantavirus infection.
One of the clearest evidences of the impact forest ecosystem variations can have in bank vole populations, and thus in human PUUV infections, is the mast phenomenon. The mast phenomenon is the abnormal abundant production of acorns, nuts and seeds by some tree species in certain years, also known as mast years. Several studies have demonstrated the impact of the mast phenomenon on rodent populations [5
]. As for hantavirus infections in Belgium, recent studies [4
] clearly show how masting can be connected to the observed temporal pattern of NE. The fact that several dominant tree species in Belgian BLF, like oaks (Quercus
spp.) and beech trees (Fagus sylvatica
), are known to have mast years, underlines the importance of tracking spatio-temporal patterns in vegetation dynamics.
Another key influencing parameter that determines rodent populations is the length of the forest growing season [11
] since it affects the number of breeding events. Changes in the length of the growing season have been mentioned as one of the possible effects of climate change affecting the primary productivity of plants [12
These vegetation-related phenomena and their link with epidemiologic pattern of NE highlight the need of exhaustive vegetation monitoring techniques. In this respect, remote sensing (RS) can offer valuable techniques and data sources to expand the knowledge on the linkages between spatio-temporal aspects of vegetation and disease occurrence. Various studies have confirmed the potential of RS in epidemiologic analyses [14
In recent years valuable scientific contributions have increased our understanding of different aspects of the multiple interactions that determine the occurrence of NE in Belgium [3
] as well as in other West European countries [4
]. Undoubtedly, the interest in NE in Belgium has grown as consequence of the increased number of reported cases in recent years as it has been recorded by the Belgian Institute of Public Health [23
]. The analysis of disease cases reports indicate that the incidence of NE is not uniformly distributed throughout the Belgian territory. Wallonia—southern Belgium—is clearly the region where most of the cases are reported. Based on the CORINE2000 Land Cover map (CLC2000) [24
], we estimated that this region encompasses 84% of Belgian broad-leaved forests and 88% of Belgian mixed forests.
The analysis of the annual reports on NE cases in Belgium shows that the occurrence of peaks follows more or less regular intervals which can be associated to mast years, as pointed out by Tersago et al.
] and Clement et al.
]. These authors found that NE outbreaks show a positive correlation with autumn temperatures and summer temperatures one and two years before the peak, respectively.
Although the ties between vegetation and NE in Belgium and other West-European countries have been emphasized repeteadly in recent literature [3
], little research has been conducted towards the exploration of RS techniques as a source of information on the dynamics of vegetation. In this study, the increasing availability (in time and space) of RS data sources is used to assess whether time series of satellite derived vegetation indices (VI) could provide valuable insights on the connections between vegetation dynamics and the epidemiological pattern observed in recent years in Belgium. Specifically, the objective of this study is to assess whether there is a relation between phenological parameters of BLF, as derived from spaceborne time series of vegetation, and the observed temporal NE pattern. The analysis is based on spaceborne data acquired by the MODIS sensor on board the Terra satellite for the period 2000–2008 and was conducted on 10 major forested areas in southern Belgium.
The geographic coordinates of the sampled sites delimited an area equivalent to 97 pixels, representing more than 2,000 hectares of BLF. The sampled sites vary in terms of forest density and composition as well as in their spatial relation with other land cover classes. These elements exerted a great influence in the computed EVI values and partially explain the differences among sites. Despite the heterogeneity of sites, the derivation of phenological information revealed the existence of general phenological patterns in BLF which probably impacted the observed NE number of cases.
Annual VI’s of forested areas in temperate regions can be represented as unimodal functions with a maximum value in the summer after a monotonous increase in spring and followed by a monotonous decrease towards a minimum value in the winter. Such functions are shaped by the amplitude and phase which are strongly related, in the case of VI, to the difference between the maximum value and the base value, and to the LGS, respectively. The function is not necessarily symmetrical, which means that the maximum EVI value is not always reached at the middle of the growing season. The LGS and amplitude values are presented in Figure 4
One of the most remarkable observed phenomena was the gradual increase in LGS in the period 2001–2007. Fitting these values to a linear function produced positive slope values for all sites, as can be seen in Table 1
. The hypothesis that the slope value was statistically equal to zero was tested and, due to the difference in slope steepness and reduced number of years in the analysis, the hypothesis could not everywhere be rejected at a significance level of 0.05.
Nevertheless, a clear increasing trend in the LGS is observed and site specific conditions may explain the differences in magnitude. The satellite data of the Sivry-Rance, for instance, are strongly influenced by important agriculture areas. This explains that this and other sites showed a mild increase in LSG during the considered period. The increasing trend in LSG was more evident in highly dense forest complexes like the forests in Saint-Hubert, the French Ardennes, Leglise or Wellin.
Complementary to the gradual increase in LGS, it is observed from the derived phenological data that the year preceding the highest NE peaks (2005, 2008 and locally, 2007) manifested a rapid green-up process together with a slow senescence, i.e
., the annual EVI signal is asymmetrical with a longer period after the EVI peak has been reached. This can be derived from the ratio increase rate/decrease rate illustrated in Figure 5
shows also the amplitude values obtained from the EVI signal. For almost all sites, an increase in the amplitude value was observed in the year 2003. This is the effect of a low base value (average of the minimum values to the left and right of the annual EVI peak) caused by rainfall deficit. As shown in Figure 6
, the year 2003 was characterized by temperatures above the average combined with rainfall deficit. The heat conditions of 2003 and 2006 have been proposed as the triggering factor of abundant seed production in the subsequent year and, therefore, explaining also the NE peaks of 2005 and 2008, respectively [9
]. Another remarkable aspect of the amplitude lines is an incipient increasing trend from the year 2006 onwards. Although the dataset is not yet large enough to statistically confirm this trend, it appears to be a response to warmer conditions in combinations with non-dry years. Interestingly, this increase in amplitude occurs when high seed production are reported to occur in two consecutive years (2006 for beech, 2007 for oak), as presented in Table 2
Most of the discussion about vegetation dynamics and NE incidence is focused on the mast phenomenom and other aspects of vegetation dynamics have been underestimated. Our results and the extensive literature on phenological changes due to climate change suggest the need of studying vegetation dynamics as related to NE incidence from a broader perspective. The increase in frequency of the mast phenomenon in recent years (see for instance the years 2006 and 2007 in Table 2
) can probably be situated in more encompassing trends of phenological changes taking place in vegetative systems.
Previous studies have already stressed the importance of vegetation phenology in rodents population. Stenseth et al.
, for instance, succesfully tested the hypothesis of the seasonal length as an explanatory variable of cyclicity in gray red-backed vole (Myodes rufocanus
) populations [36
]. Klemola et al.
proposed the onset and duration of the growing season of plants as determining factors of reproduction in rodents [11
]. Knowing the importance of voles demography in NE [2
], it is not surprising that the recent increase of NE reported cases has taken place in a context of gradual increase in LGS. An extended growing period will not only increase the number of breeding ocassions for rodents [11
], but can enhance ecosystems carrying capacity. Our findings are coincident with other studies on phenology in which an enlargement of the growing period has been reported together with an early onset of photosynthetic activity [29
]. These phenological trends have been attributed to global climate change and, in the case of the early spring onset, to increase in temperatures during that period [21
Given the fact that we rely only on MODIS-derived data, statistical analysis on annual parameters do not have enough degrees of freedom to support conclusions at a high level of significance. Yet, evidence in literature of linkage between climate and onset and length of growing season showed a good correlation with our data as well. The correlation coefficients in Table 3
show that the temperature in the second quarter of the year and the date of start of the growing season tend to be negatively related; i.e
., the warmer it is in spring the earlier the growing season starts. Furthermore, the figures in Table 3
suggest that the LGS is positively correlated with the temperature in June. Remarkable low correlation values were detected where the adjacency effects of neighboring land cover classes is expected to be the greatest: site 4.
The high ratio increase/decrease of the growing period appeared to influence the NE mechanics given that the highest values occured in the growing period preceding the highest NE peaks. Those years were also characterized by high tree seed production. This suggests that the rodent population and the interactions amongst individual rodents are impacted by at least two factors: the crop production abundance of beech and oak, and the favourable and long conditions to mate. This combined effect might explain outstanding NE peaks in 2005 and 2008 in contrast to other mast years resulting in less outspoken NE peaks.
Longer periods of milder weather conditions and greenness in the forest as well as positive changes in forest growth as consequence of climate change may also be an important aspect attracting humans to forest [38
], thereby increasing exposure risk. The most important factor leading to NE is without doubt the degree of human exposure to aerosolized excreta of bank voles. Although this exposure does not occur exclusively in forested areas, outdoor activities in vole infested environments may imply a great risk. This can be exemplified with the first NE outbreak documented in Germany, with 24 cases within two weeks during a winter bivouac of the U.S. Army on a vole-infested terrain near Ulm (S.-Germany) in January 1990. During the same winter period, not a single civilian case of NE was registered in the whole same region [39
]. Works cited by Clement et al.
] refer also to the risk of infection campers and trekkers face when sleeping among rodent burrows or in confined places infested with rodents like caravans, mountain refuges, hunting lodges, fishing cabins, etc