www.nature.com/scientificreports
OPEN
Alien plant invasions of protected areas in Java, Indonesia Michael Padmanaba1,2, Kyle W. Tomlinson1, Alice C. Hughes1 & Richard T. Corlett 1
Received: 13 March 2017 Accepted: 31 July 2017 Published: xx xx xxxx
Alien plants are invading protected areas worldwide, but there is little information from tropical Asia. Java has the longest record of human occupation in Asia and today supports 145 m people. Remnants of natural ecosystems survive in 12 small National Parks surrounded by dense human populations, making them highly vulnerable to invasions. We surveyed eight of these, along a rainfall gradient from lowland rainforest with >3000 mm annual rainfall to savanna with 1000 people km−2), and rapid economic growth has transformed the Javan landscape, with most cultivable land cleared of its natural vegetation cover by the middle of the 20th century14, 16, and an increasing area since then covered in human settlements, industrial developments, and infrastructure. However, Java also has 12 well-protected National Parks that contain the last significant remnants of the major natural ecosystem types on the island. Although these are all small17, and were all subject to human and volcanic disturbances in the past, they still support populations of Java’s remaining large vertebrates (primates, deer, banteng) whose visibility attests to the low hunting pressure, as does the survival of the last Javan rhinoceros population on Earth in Ujung Kulon National Park. The more 1 Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan 666303, China. 2University of Chinese Academy of Sciences, Beijing, 100049, China. Correspondence and requests for materials should be addressed to M.P. (email: [email protected])
Scientific Reports | 7: 9334 | DOI:10.1038/s41598-017-09768-z
1
www.nature.com/scientificreports/ National Park
2011
2012
2013
2014
2015
Ujung Kulon
6,691
7,433
9,248
12,429
15,150
Gunung Gede Pangrango
88,953
85,486
139,767
165,823
154,948
Gunung Merapi
193,779
72,797
100,965
200,308
254,000
Gunung Merbabu
26,789
25,662
25,012
11,220
42,828
Bromo Tengger Semeru
125,471
275,874
545,648
571,158
474,011
Meru Betiri
2,443
3,342
9,055
60,092
89,071
Alas Purwo
90,875
100,315
121,818
133,557
132,220
Baluran
28,851
32,674
39,874
60,385
93,054
Table 1. Numbers of visitors 2011–2015 to the eight National Parks in Java surveyed in this study. Data from Directorate of Forest Conservation and Environmental Services at the Ministry of Environment and Forestry.
accessible parks are very popular at weekends with Javanese from the cities, and visitor numbers are increasing rapidly (Table 1), but human recreational pressures appear to be generally well-managed. All these parks, however, exist as widely separated islands in a highly-modified, densely populated, agricultural matrix, with little or no buffer between the two. The small size of the parks, their isolation, and the heavy human pressures are all expected to increase the risk of biological invasions. A recent global review found that invasive alien plants are present in almost all protected areas, although they are generally less prominent than in unprotected areas1. As a case study, the Javan parks have the advantage that they are spread across the full range of physical environments and natural ecosystems in Java, from lowland and montane rainforests in the west to dry savannas in the east. Moreover, these are also fairly representative of similar ecosystems across Southeast Asia11. Java is extreme in the magnitude of the human pressures, but protected areas across the tropics are becoming increasingly isolated as human populations on their borders increase18. Previous studies in Java have looked at individual parks19–23, but no previous study has made use of the full range of terrestrial environments represented in the park system. This study therefore attempts to answer three main questions about invasive alien plant species in Java’s National Parks. 1. Which alien plant species are invading and where? 2. What factors determine which species invade which parks? 3. What factors control their distributions and abundances within parks?
Results
Most environmental variables were associated with the west-east gradient of declining rainfall and/or the 0–3158 m gradient in altitude (Supplementary Table S1). Ujung Kulon is the wettest park, with a mean annual rainfall of 3515 mm, while Baluran is the driest, with only 1095 mm. Alas Purwo is the warmest, with a mean temperature of 27.8 °C and Gunung Merbabu the coolest, with a mean of 11.6 °C. At the plot scale, mean temperature ranged from 8.9 °C in the coolest plot in shrubland at 3152 m on Gunung Merbabu to 30.5 °C in the warmest plot in savanna at 68 m in Baluran. In Gunung Gede Pangrango, mean temperature declined regularly with altitude while minimum and maximum temperatures declined significantly, but less regularly (Supplementary Fig. S1). No data logger recorded frost during the study period. Frosts have been reported to occur in Java above 1500 m, but only in depressions and never on slopes24. Humidity declined but not significantly. Most soil variables varied widely within parks and the ranges overlapped among parks (Supplementary Table S1). Soils were generally sandy and acidic, except in the two driest parks, where the soils were generally alkaline. In Gunung Gede Pangrango, soil organic carbon, silt, and nitrogen increased significantly with altitude, while clay declined, but the scatter was large (Supplementary Fig. S2). All parks had sample plots with low and high tree cover, but the mean cover was highest in Ujung Kulon and lowest in Baluran. A total of 67 invasive alien plant species (IAS; Supplementary Table S2) were found in the sample plots, with 261 (64.8%) of the 403 plots containing at least one. Seven species were found in only a single plot and almost half (33) only in one park. The families Asteraceae (18 species), Fabaceae (10), Solanaceae (7), and Euphorbiaceae (5) accounted for most species. There were four species of trees, all in the Fabaceae, and four lianas, while the rest were herbs (39) or shrubs (20). A large majority of species were from the Neotropics (53), followed by the temperate zone (7; all from the northern hemisphere except for Fuchsia magellanica from temperate South America), Africa (4), India (1), and Australia (1) (Supplementary Table S3). The temperate zone species were all found only or largely above 2000 m. More than half the total species (40) were already reported in Java in the nineteenth century (Supplementary Table S3). It is noticeable, however, that Ageratina riparia (first recorded in Java in 1963) and Chromolaena odorata (1940s) are among the most abundant IAS in the parks they have reached. The numbers of species recorded in each park ranged from eight in Ujung Kulon and Alas Purwo, which are on isolated peninsulas at opposite ends of Java, to 27 in Meru Betiri (Table 2), and was not correlated with the number of plots sampled (Spearman’s ρ = −0.11, p = 0.80). Only two species, Chromolaena odorata and Lantana camara, were found in all eight parks (Supplementary Table S2), and in Gunung Gede Pangrango they were both only found outside the plots at low elevation. C. odorata was also among the three most frequent species in five parks (Table 2). Clidemia hirta was found in all but the two driest parks, but was sparsely distributed everywhere. Elephantopus scaber, Hyptis capitata, and Passiflora foetida were in all lowland parks but none of the mountain parks, while Ageratina riparia and Austroeupatorium inulaefolium were in all mountain parks but none of the lowland parks. Moreover, P. foetida was the most frequently recorded species in lowland Baluran, while A. riparia was the most frequent in all the mountain parks (Table 2). Acacia decurrens was frequent in three mountain parks but absent from all the others. Some of the species found in only one park—Acacia nilotica in Baluran, and Scientific Reports | 7: 9334 | DOI:10.1038/s41598-017-09768-z
2
www.nature.com/scientificreports/
National Park
Land area Total (km2) Total plots alien spp.
Plots with Tree/ liana aliens count
Shrub/ herb cover
Ujung Kulon
786.2
6
0.41
Gunung Gede Pangrango
Gunung Merapi
Gunung Merbabu
Bromo Tengger Semeru
Meru Betiri
Alas Purwo
Baluran
219.8
64.1
57.3
502.8
554. 0
430.2
239.4
55
32
48
38
94
14
41
81
8
14
13
14
23
27
8
24
24
38
31
72
14
13
63
0.02
0.19
4.31
1.21
1.34
4.36
0.07
3.33
15.14
18.69
21.49
28.10
12.68
2.28
5.4
Most common aliens
N of Plots
Hyptis capitata
2
Lantana camara
2
Ageratina riparia
15
Brugmansia candida
5
Solanum americanum
4
Passiflora ligularis
4
Ageratina riparia
29
Chromolaena odorata
21
Acacia decurrens
15
Ageratina riparia
30
Austroeupatorium inulaefolium
21
Acacia decurrens
15
Ageratina riparia
46
Chromolaena odorata
43
Acacia decurrens
21
Eleutheranthera ruderalis
12
Mikania micrantha
11
Chromolaena odorata
9
Chromolaena odorata
13
Hyptis capitata
6
Passiflora foetida
24
Acacia nilotica
21
Chromolaena odorata
18
Table 2. Invasive alien plant species number and abundance in the plots (each 10 m × 5 m) surveyed in eight National Parks in Java. Alien trees and lianas in the plots were counted and alien shrub and herb covers were estimated.
Brugmansia candida and Passiflora ligularis in Gunung Gede Pangrango—were frequent where they occurred. Indeed, A. nilotica now covers more than 60 km2 of Baluran after being first planted there in 196922. No invasive species were found on eight 50-m transects from trails into the forest in Ujung Kulon, and few penetrated more than 10 m from the trails in Gunung Gede Pangrango. In Alas Purwo and Baluran, invasive species were rare or absent on transects with high canopy cover, but in areas of with low or no canopy cover all the common invasives spread to the limits of the transects. In Baluran, Acacia nilotica, Ageratum conyzoides, Hyptis suaveolens, Mimosa pudica, and Passiflora foetida were particularly common on the transects. In agreement with the patterns described above, the PCA ordination of the park × species matrix separated the four lowland parks from the four mountains, and Gunung Gede Pangrango from the other mountains (Fig. 1A). The first two principal components accounted for more than half of the variation in the data, where PCA1 explained substantially more variation (37.8%) than PCA2 (17.3%). Only altitude and soil total nitrogen were significantly correlated with these two axes. The species ordination separated three clusters, representing lowland-only species (all of tropical origin), high altitude species (tropical or temperate), and species only found on Gunung Gede Pangrango (tropical or temperate), with the more widespread species spread between them (Fig. 1B). The PCA on the plot × species matrix, excluding plots without IAS, showed a similar pattern to the PCA for park × species, except that there was considerable overlap, with some plots from different parks sharing similar invasive species compositions, and the first two principal components accounted for only 15.8% and 11.8% of the variance (Fig. 2). Significantly associated environmental variables were altitude, slope, soil total N, available potassium, clay content, silt content, trail width, and native shrub cover. Not surprisingly, given the large differences between parks in the range of values shown by each environmental variable, the drivers identified by the park-level generalized linear mixed models (GLMM) varied among parks (Table 3). However, canopy cover had a significant negative impact on the numbers and abundances of IAS in most lowland parks, while altitude had a significant negative impact in most mountain parks, as well as Baluran and Alas Purwo. Other patterns were more idiosyncratic, including positive effects of trail width on number of alien species in Baluran and total nitrogen in Bromo Tengger Semeru, and negative effects of slope and total nitrogen in Alas Purwo, and clay in Ujung Kulon and Gunung Merbabu.
Discussion
Invasion biologists have recognized the existence of multiple barriers to invasion that must be overcome before a species becomes truly invasive25. The first of these is geographical: an invasive species must be transported, deliberately or accidentally beyond its native range. None of the species identified as alien in this study are native to Java so all must have crossed marine barriers to get there. For species that can establish and spread in the human-dominated matrix, reaching Java is enough to provide an opportunity for invasion. Many of the species
Scientific Reports | 7: 9334 | DOI:10.1038/s41598-017-09768-z
3
www.nature.com/scientificreports/
Figure 1. PCA ordination of the park by alien species matrix showing (A) the eight parks and (B) the alien species. The vectors show the predictors (altitude and soil total N) significantly related to the ordination space at p
OPEN
Alien plant invasions of protected areas in Java, Indonesia Michael Padmanaba1,2, Kyle W. Tomlinson1, Alice C. Hughes1 & Richard T. Corlett 1
Received: 13 March 2017 Accepted: 31 July 2017 Published: xx xx xxxx
Alien plants are invading protected areas worldwide, but there is little information from tropical Asia. Java has the longest record of human occupation in Asia and today supports 145 m people. Remnants of natural ecosystems survive in 12 small National Parks surrounded by dense human populations, making them highly vulnerable to invasions. We surveyed eight of these, along a rainfall gradient from lowland rainforest with >3000 mm annual rainfall to savanna with 1000 people km−2), and rapid economic growth has transformed the Javan landscape, with most cultivable land cleared of its natural vegetation cover by the middle of the 20th century14, 16, and an increasing area since then covered in human settlements, industrial developments, and infrastructure. However, Java also has 12 well-protected National Parks that contain the last significant remnants of the major natural ecosystem types on the island. Although these are all small17, and were all subject to human and volcanic disturbances in the past, they still support populations of Java’s remaining large vertebrates (primates, deer, banteng) whose visibility attests to the low hunting pressure, as does the survival of the last Javan rhinoceros population on Earth in Ujung Kulon National Park. The more 1 Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan 666303, China. 2University of Chinese Academy of Sciences, Beijing, 100049, China. Correspondence and requests for materials should be addressed to M.P. (email: [email protected])
Scientific Reports | 7: 9334 | DOI:10.1038/s41598-017-09768-z
1
www.nature.com/scientificreports/ National Park
2011
2012
2013
2014
2015
Ujung Kulon
6,691
7,433
9,248
12,429
15,150
Gunung Gede Pangrango
88,953
85,486
139,767
165,823
154,948
Gunung Merapi
193,779
72,797
100,965
200,308
254,000
Gunung Merbabu
26,789
25,662
25,012
11,220
42,828
Bromo Tengger Semeru
125,471
275,874
545,648
571,158
474,011
Meru Betiri
2,443
3,342
9,055
60,092
89,071
Alas Purwo
90,875
100,315
121,818
133,557
132,220
Baluran
28,851
32,674
39,874
60,385
93,054
Table 1. Numbers of visitors 2011–2015 to the eight National Parks in Java surveyed in this study. Data from Directorate of Forest Conservation and Environmental Services at the Ministry of Environment and Forestry.
accessible parks are very popular at weekends with Javanese from the cities, and visitor numbers are increasing rapidly (Table 1), but human recreational pressures appear to be generally well-managed. All these parks, however, exist as widely separated islands in a highly-modified, densely populated, agricultural matrix, with little or no buffer between the two. The small size of the parks, their isolation, and the heavy human pressures are all expected to increase the risk of biological invasions. A recent global review found that invasive alien plants are present in almost all protected areas, although they are generally less prominent than in unprotected areas1. As a case study, the Javan parks have the advantage that they are spread across the full range of physical environments and natural ecosystems in Java, from lowland and montane rainforests in the west to dry savannas in the east. Moreover, these are also fairly representative of similar ecosystems across Southeast Asia11. Java is extreme in the magnitude of the human pressures, but protected areas across the tropics are becoming increasingly isolated as human populations on their borders increase18. Previous studies in Java have looked at individual parks19–23, but no previous study has made use of the full range of terrestrial environments represented in the park system. This study therefore attempts to answer three main questions about invasive alien plant species in Java’s National Parks. 1. Which alien plant species are invading and where? 2. What factors determine which species invade which parks? 3. What factors control their distributions and abundances within parks?
Results
Most environmental variables were associated with the west-east gradient of declining rainfall and/or the 0–3158 m gradient in altitude (Supplementary Table S1). Ujung Kulon is the wettest park, with a mean annual rainfall of 3515 mm, while Baluran is the driest, with only 1095 mm. Alas Purwo is the warmest, with a mean temperature of 27.8 °C and Gunung Merbabu the coolest, with a mean of 11.6 °C. At the plot scale, mean temperature ranged from 8.9 °C in the coolest plot in shrubland at 3152 m on Gunung Merbabu to 30.5 °C in the warmest plot in savanna at 68 m in Baluran. In Gunung Gede Pangrango, mean temperature declined regularly with altitude while minimum and maximum temperatures declined significantly, but less regularly (Supplementary Fig. S1). No data logger recorded frost during the study period. Frosts have been reported to occur in Java above 1500 m, but only in depressions and never on slopes24. Humidity declined but not significantly. Most soil variables varied widely within parks and the ranges overlapped among parks (Supplementary Table S1). Soils were generally sandy and acidic, except in the two driest parks, where the soils were generally alkaline. In Gunung Gede Pangrango, soil organic carbon, silt, and nitrogen increased significantly with altitude, while clay declined, but the scatter was large (Supplementary Fig. S2). All parks had sample plots with low and high tree cover, but the mean cover was highest in Ujung Kulon and lowest in Baluran. A total of 67 invasive alien plant species (IAS; Supplementary Table S2) were found in the sample plots, with 261 (64.8%) of the 403 plots containing at least one. Seven species were found in only a single plot and almost half (33) only in one park. The families Asteraceae (18 species), Fabaceae (10), Solanaceae (7), and Euphorbiaceae (5) accounted for most species. There were four species of trees, all in the Fabaceae, and four lianas, while the rest were herbs (39) or shrubs (20). A large majority of species were from the Neotropics (53), followed by the temperate zone (7; all from the northern hemisphere except for Fuchsia magellanica from temperate South America), Africa (4), India (1), and Australia (1) (Supplementary Table S3). The temperate zone species were all found only or largely above 2000 m. More than half the total species (40) were already reported in Java in the nineteenth century (Supplementary Table S3). It is noticeable, however, that Ageratina riparia (first recorded in Java in 1963) and Chromolaena odorata (1940s) are among the most abundant IAS in the parks they have reached. The numbers of species recorded in each park ranged from eight in Ujung Kulon and Alas Purwo, which are on isolated peninsulas at opposite ends of Java, to 27 in Meru Betiri (Table 2), and was not correlated with the number of plots sampled (Spearman’s ρ = −0.11, p = 0.80). Only two species, Chromolaena odorata and Lantana camara, were found in all eight parks (Supplementary Table S2), and in Gunung Gede Pangrango they were both only found outside the plots at low elevation. C. odorata was also among the three most frequent species in five parks (Table 2). Clidemia hirta was found in all but the two driest parks, but was sparsely distributed everywhere. Elephantopus scaber, Hyptis capitata, and Passiflora foetida were in all lowland parks but none of the mountain parks, while Ageratina riparia and Austroeupatorium inulaefolium were in all mountain parks but none of the lowland parks. Moreover, P. foetida was the most frequently recorded species in lowland Baluran, while A. riparia was the most frequent in all the mountain parks (Table 2). Acacia decurrens was frequent in three mountain parks but absent from all the others. Some of the species found in only one park—Acacia nilotica in Baluran, and Scientific Reports | 7: 9334 | DOI:10.1038/s41598-017-09768-z
2
www.nature.com/scientificreports/
National Park
Land area Total (km2) Total plots alien spp.
Plots with Tree/ liana aliens count
Shrub/ herb cover
Ujung Kulon
786.2
6
0.41
Gunung Gede Pangrango
Gunung Merapi
Gunung Merbabu
Bromo Tengger Semeru
Meru Betiri
Alas Purwo
Baluran
219.8
64.1
57.3
502.8
554. 0
430.2
239.4
55
32
48
38
94
14
41
81
8
14
13
14
23
27
8
24
24
38
31
72
14
13
63
0.02
0.19
4.31
1.21
1.34
4.36
0.07
3.33
15.14
18.69
21.49
28.10
12.68
2.28
5.4
Most common aliens
N of Plots
Hyptis capitata
2
Lantana camara
2
Ageratina riparia
15
Brugmansia candida
5
Solanum americanum
4
Passiflora ligularis
4
Ageratina riparia
29
Chromolaena odorata
21
Acacia decurrens
15
Ageratina riparia
30
Austroeupatorium inulaefolium
21
Acacia decurrens
15
Ageratina riparia
46
Chromolaena odorata
43
Acacia decurrens
21
Eleutheranthera ruderalis
12
Mikania micrantha
11
Chromolaena odorata
9
Chromolaena odorata
13
Hyptis capitata
6
Passiflora foetida
24
Acacia nilotica
21
Chromolaena odorata
18
Table 2. Invasive alien plant species number and abundance in the plots (each 10 m × 5 m) surveyed in eight National Parks in Java. Alien trees and lianas in the plots were counted and alien shrub and herb covers were estimated.
Brugmansia candida and Passiflora ligularis in Gunung Gede Pangrango—were frequent where they occurred. Indeed, A. nilotica now covers more than 60 km2 of Baluran after being first planted there in 196922. No invasive species were found on eight 50-m transects from trails into the forest in Ujung Kulon, and few penetrated more than 10 m from the trails in Gunung Gede Pangrango. In Alas Purwo and Baluran, invasive species were rare or absent on transects with high canopy cover, but in areas of with low or no canopy cover all the common invasives spread to the limits of the transects. In Baluran, Acacia nilotica, Ageratum conyzoides, Hyptis suaveolens, Mimosa pudica, and Passiflora foetida were particularly common on the transects. In agreement with the patterns described above, the PCA ordination of the park × species matrix separated the four lowland parks from the four mountains, and Gunung Gede Pangrango from the other mountains (Fig. 1A). The first two principal components accounted for more than half of the variation in the data, where PCA1 explained substantially more variation (37.8%) than PCA2 (17.3%). Only altitude and soil total nitrogen were significantly correlated with these two axes. The species ordination separated three clusters, representing lowland-only species (all of tropical origin), high altitude species (tropical or temperate), and species only found on Gunung Gede Pangrango (tropical or temperate), with the more widespread species spread between them (Fig. 1B). The PCA on the plot × species matrix, excluding plots without IAS, showed a similar pattern to the PCA for park × species, except that there was considerable overlap, with some plots from different parks sharing similar invasive species compositions, and the first two principal components accounted for only 15.8% and 11.8% of the variance (Fig. 2). Significantly associated environmental variables were altitude, slope, soil total N, available potassium, clay content, silt content, trail width, and native shrub cover. Not surprisingly, given the large differences between parks in the range of values shown by each environmental variable, the drivers identified by the park-level generalized linear mixed models (GLMM) varied among parks (Table 3). However, canopy cover had a significant negative impact on the numbers and abundances of IAS in most lowland parks, while altitude had a significant negative impact in most mountain parks, as well as Baluran and Alas Purwo. Other patterns were more idiosyncratic, including positive effects of trail width on number of alien species in Baluran and total nitrogen in Bromo Tengger Semeru, and negative effects of slope and total nitrogen in Alas Purwo, and clay in Ujung Kulon and Gunung Merbabu.
Discussion
Invasion biologists have recognized the existence of multiple barriers to invasion that must be overcome before a species becomes truly invasive25. The first of these is geographical: an invasive species must be transported, deliberately or accidentally beyond its native range. None of the species identified as alien in this study are native to Java so all must have crossed marine barriers to get there. For species that can establish and spread in the human-dominated matrix, reaching Java is enough to provide an opportunity for invasion. Many of the species
Scientific Reports | 7: 9334 | DOI:10.1038/s41598-017-09768-z
3
www.nature.com/scientificreports/
Figure 1. PCA ordination of the park by alien species matrix showing (A) the eight parks and (B) the alien species. The vectors show the predictors (altitude and soil total N) significantly related to the ordination space at p
