Assessing Environmental Conditions of Antarctic Footpaths to Support Management Decisions

Journal of Environmental Management 177 (2016) 320e330

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Journal of Environmental Management

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Research article Assessing environmental conditions of Antarctic footpaths to support management decisions

* Pablo Tejedo a, , Javier Benayas a, Daniela Cajiao b, Belen Albertos c, Francisco Lara d, Luis R. Pertierra a, Manuela Andres-Abell an e, Consuelo Wic e, Maria Jose Lucianez~ d, Natalia Enríquez d, Ana Justel f, Günther K. Reck b a Departamento de Ecología, Universidad Autonoma de Madrid, C/ Darwin 2, ES-28049 Madrid, Spain b Instituto de Ecología Aplicada ECOLAP-USFQ, Universidad de San Francisco de Quito, P.O. Box 1712841, Quito, Ecuador c Departamento de Botanica, Universidad de Valencia, Avda. Vicente Andres Estelles s/n, ES-46100 Burjassot, Spain d Departamento de Biología, Universidad Autonoma de Madrid, C/ Darwin 2, ES-28049 Madrid, Spain e Departamento de Ciencia y Tecnología Agroforestal y Genetica, Universidad de Castilla-La Mancha, Avda. Espana~ s/n, ES-02071 Albacete, Spain f Departamento de Matematicas, Universidad Autonoma de Madrid, C/ Francisco Tomas y Valiente 5, ES-28049 Madrid, Spain article info abstract

Article history: Thousands of tourists visit certain Antarctic sites each year, generating a wide variety of environmental Received 18 September 2015 impacts. Scientific knowledge of human activities and their impacts can help in the effective design of Received in revised form management measures and impact mitigation. We present a case study from Barrientos Island in which a 6 April 2016 management measure was originally put in place with the goal of minimizing environmental impacts but Accepted 10 April 2016 resulted in new undesired impacts. Two alternative footpaths used by tourist groups were compared. Both affected extensive moss carpets that cover the middle part of the island and that are very vulnerable to trampling. The first path has been used by tourists and scientists since over a decade and is a marked Keywords: Barrientos Island route that is clearly visible. The second one was created more recently. Several physical and biological Trampling impact indicators were measured in order to assess the environmental conditions for both paths. Some physical Precautionary Principle variables related to human impact were lower for the first path (e.g. soil penetration resistance and Microbial activity secondary treads), while other biochemical and microbiological variables were higher for the second Moss communities path (e.g. b-glucosidase and phosphatase activities, soil respiration). Moss communities located along the Collembola new path were also more diverse and sensitive to trampling. Soil biota (Collembola) was also more abundant and richer. These data indicate that the decision to adopt the second path did not lead to the reduction of environmental impacts as this path runs over a more vulnerable area with more outstanding biological features (e.g. microbiota activity, flora and soil fauna diversity). In addition, the adoption of a new route effectively doubles the human footprint on the island. We propose using only the original path that is less vulnerable to the impacts of trampling. Finally from this process, we identify several key issues that may be taken into account when carrying out impact assessment and environmental management decision-making in the Antarctic area. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction

The primary international legislation concerning Antarctica is the Antarctic Treaty. It was signed in 1959, came into force in 1961, and applies to the area south of 60 S latitude (Convey et al., 2012). It * Corresponding author. places pre-existing national territorial claims in the region in E-mail addresses: [email protected] (P. Tejedo), [email protected] (J. Benayas), [email protected] (D. Cajiao), [email protected] (B. Albertos), abeyance, and prohibits military activity, nuclear explosions and the [email protected] (F. Lara), [email protected] (L.R. Pertierra), manuela. disposal of radioactive waste material, whilst promoting interna- [email protected] (M. Andres-Abell an), [email protected] (C. Wic), mjose. tional cooperation in scientific investigation in Antarctica and rec- [email protected] (M.J. Lucianez),~ [email protected] ommending measures for the preservation and conservation of (N. Enríquez), [email protected] (A. Justel), [email protected] (G.K. Reck). http://dx.doi.org/10.1016/j.jenvman.2016.04.032 0301-4797/© 2016 Elsevier Ltd. All rights reserved. P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330 321 living resources in Antarctica [Article IX, para 1 (f)]. Since 1959, the the island, which is known to be very vulnerable to trampling Antarctic Treaty has expanded into the Antarctic Treaty System, (Pertierra et al., 2013). The new path runs partly along the course of which includes other legal instruments designed specifically for the a small snow melting stream, hypothetically reducing the area of protection and management of Antarctic environment. The main direct contact between visitors and mosses. In theory, if visitors legal text devoted to the conservation of the marine and terrestrial kept inside the track of the new path, the visual impact generated ecosystems in the Antarctic region is the Protocol on Environmental would be less than that produced by the old path, which is clearly Protection to the Antarctic Treaty. This was signed in 1991 and visible from several points of the island. entered into force in 1998. It assigns a degree of special conservation During the 2011e12 austral summer season, significant damage to the entire Antarctic Treaty area. It contains six annexes: (I) to important moss beds on the middle part of the island was Environmental Impact Assessment; (II) Conservation of Antarctic recorded in the vicinity of the Lower Path as a result of repeated foot Fauna and Flora; (III) Waste Disposal; (IV) Marine Pollution; (V) traffic(Ecuador and Spain, 2012). Numerous footprints and sec- Protected Areas; and (VI) Liability. Environmental management and ondary treads were observed alongside this path, with some new conservation should be a priority within the Antarctic Treaty area muddy areas created by trampling. This level of damage is an since the footprint of human activities is increasing (e.g. Tin et al., exception in Antarctica, and similar situations are only present 2009; Chown et al., 2012; Convey et al., 2012 and Hughes et al., marginally in the vicinity of research stations where human 2013). Today, there are over 100 research facilities in Antarctica. frequentation is high. This information was presented to the CEP, At least 4000 national operator staff (Council of Managers of which recommended restricting access to the paths crossing Bar- National Antarctic Programs, 2012) and up to 34,000 tourists go to rientos Island, allowing access only for scientific research and Antarctica each year (International Association of Antarctica Tour monitoring related to the recovery of the site (Antarctic Treaty Operators, 2015). Biological communities on ice-free coastal areas Secretariat, 2012). The CEP also proposed to the Parties to under- are particularly exposed to potential human impacts, as their level take active work in the area, to design and implement appropriate of resilience is largely unclear (Turner et al., 2009). This context surveys and monitoring plans that will help the CEP to inform makes it essential to consider whether current conservation and decisions on future management actions. protection of Antarctica's environmental values are effective. This paper reports the first progress on this monitoring effort. Monitoring studies are an important tool in achieving this objective. The main aim of the research was to highlight the importance of Here we present a case study developed at an Antarctic site: scientific research in guiding decision-making processes, as part of Barrientos Island. This is a small island located at the north an adaptive management model. In our case, this framework was entrance to English Strait, between Robert and Greenwich Islands, applied to determine which route would be more effective in in the South Shetland archipelago, Antarctica (62 240 S, 59 470 W, reducing the environmental impacts of visitors' foot traffic. The Fig. 1). It has many attractive features including geological forma- choice was based on results from a global assessment that included tions (columnar basalt outcrops and 70 m steep cliffs), extensive physical and biological indicators collected on Barrientos Island in moss carpets covering the center of the island (unusual in 2013, with the exception of Collembola, which were sampled dur- Antarctica), and numerous seabird and mammal breeding colonies. ing 2012. Our experience shows the importance of looking at 'the The island's outstanding biological and geological richness has whole ecosystem' when making decisions about environmental resulted in its inclusion among the sites with high diversity in the management in Antarctica. We have also identified a number of key third edition of the Antarctic Peninsula Compendium (Naveen and issues that need to be taken into account in Antarctic environ- Lynch, 2011). It has also aroused the interest of Antarctic tour op- mental management. We hope our findings will help other erators. The number of visitors exhibited a positive trend up until research teams design appropriate strategies to improve the con- 2007e08 season, with a certain decline in recent years (Fig. 2), like servation of Antarctic terrestrial ecosystems. most of the tourist sites in Antarctica. In 2014e15 Barrientos Island received 5262 visitors while a record high of 7240 visitors was 2. Material and methods recorded in the 2006e07 season. Barrientos Island is among the fifteen most visited sites in the Antarctic Peninsula (International 2.1. Study paths Association of Antarctica Tour Operators, 2015). It is less than three nautical miles from Greenwich Island, where the Ecuadorian Both assessed paths begin in the primary landing area located in research station Pedro Vicente Maldonado is located (62 270 S, the south-eastern beach of Barrientos Island. They meet at a small 59 440 W). This summer-only station was opened in 1990 and, for a pass that join with a third path (Western Tip Path) that runs to the number of years, has been welcoming scientists from different western end of the island (Fig. 1). Although the start and end for nations to conduct research on Barrientos Island. Since 2011, our both paths are coincident, they follow different routes most of the research group has enjoyed the support of Maldonado station in way. The route of the Lower Path runs at a lower altitude until it our tourism monitoring activities on Barrientos Island. meets the Upper Path. This explains the terms selected for the In 2005, in response to the large number of visitors to the island, routes. The Lower Path runs largely along the South beaches to the Antarctic Treaty Consultative Meeting (ATCM) adopted a first avoid different sub-colonies of penguins, while the Upper Path list of visitor site guidelines to manage the human presence at this crosses some penguin nesting areas. Moss carpets lie in the middle site in order to avoid disturbances to local flora and fauna. These part of the island. The Lower Path runs through part of the mosses guidelines were initially validated by the ATCM's Committee for with the exception of a section that follows the course of a small Environmental Protection (CEP). The CEP was an advisory set up stream. Part of the Upper Path runs along the outer edge of the moss under the Protocol on Environmental Protection to the Antarctic carpets, close to a small rocky rise where moss carpets are absent. Treaty to provide advice and formulate recommendations on The length of both paths is quite similar (750 m for the Lower Path environmental matters to the ATCM. One of these proposals was and 670 m for the Upper Path) and there are no steep slopes. Before the adoption of a new footpath, identified as the Lower Path in this the access restriction proposed by the CEP, the Lower Path was used work, replacing the footpath traditionally used by visitors to cross more intensively than the Upper Path. During the 2011e12 tourist the middle part of the island (hereafter referred to as the Upper season, about 41% of tourism expeditions used the Lower Path, Path). The reason for this change was to minimize the pressure over while 24% used the Upper Path (Ecuador and Spain, 2012) and 34% the extensive moss carpet area that is covering the middle part of remained on the beach located close to the penguin colony at the 322 P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330

Fig. 1. Map of Barrientos Island showing the Lower Path and the Upper Path. Physical variables (i.e. track width and soil penetration resistance) and plant coverage were recorded along part of the sections of the paths in Closed Area B marked by a grey envelop (see the text for further details). Four star-shaped symbols indicate sites where soil temperature sensors were buried, while six round dots indicate where samples for biochemical and microbiological variables were obtained. Soil fauna was recorded at the six locations indicated by crosses. To determine the basic soil properties (chemical variables) several simple samples were obtained along the assessed section of each path to build a final composite sample. The bottom panel of the figure shows a representative image of each path. Lower Path is on the left and the Upper Path is on the right. These images show the conditions in the vicinities of each path used as control areas (3 m from the center of the track). eastern tip. In February 2012 and 2013, we visited the two paths 2.2. Physical and chemical variables and assessed different physical-chemical, biochemical-microbiological, flora and faunal variables. These variables were used to answer two questions. 1) Are there significant differences between both paths regarding the soil on which they ran? 2) Are there differences in the basic soil features P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330 323

Fig. 2. Evolution of the number of visitors and tourists at Barrientos Island (1989e90 to 2014e15 seasons). Visitors include tourist guides, staff members of expeditions and tourists. Source: International Association of Antarctica Tour Operators (2015). between the more impacted (0 m) and the control (3 m) areas? In method, drying the sample at about 115 C and measuring the mass other words, does the presence of the path generate a significant difference before and after drying. change of basic soil properties? Track width and soil penetration resistance were recorded every 2.3. Biochemical and microbiological variables 10 m along sections of each path. These sections were selected from the middle part of the island which is covered by mosses. Other These data answered the same questions presented in Section sections of the paths cross substrates that are not directly compa- 2.3, but with a focus on soil biochemical and microbiological fea- rable: the Lower Path crosses a cobble beach while the Upper Path tures. Three points were randomly selected along each path within crosses ornithogenic soils. In total, 260 m of the Lower Path and the comparable sections. Soil samples were obtained at 0 and 3 m 110 m of the Upper Path were assessed for these two variables. from the center of the track. Samples were taken from the upper Snow on some sections of the paths impeded assessment at more 10e15 cm layer, because a large portion of microbial activity occurs locations on each path and along comparable section lengths on in these horizons (García et al., 2003). The soil samples were stored both paths. For soil penetration resistance, 5 replicas per point were at 4 C(Andres-Abell an et al., 2011) until they underwent obtained using a manual precision penetrometer ST-308 (Eurosite, biochemical and microbiological analysis in Spain. Samples were Ancona, Italy), both in the center of the path (zone of maximum sieved (<2 mm) and all debris and plant remains were removed impact) and 50 cm to either side (used as control areas). In addition, before analysis. Urease activity was determined by staining the we studied two more physical variables. First, we recorded sec- ammonium released into the incubation solution at 37 C for 2 h ondary treads along the entirety of both paths, registering the following the methods reported by Kandeler et al. (1999). Alkaline length and the occupied surface for each detected secondary sec- phosphatase and b-glucosidase activities were determined tion. Secondly, soil temperature was recorded at two selected following the methods reported by Tabatabai and Bremner (1969), points for each path using a soil temperature sensor (Thermochron and Tabatabai (1982), respectively. Soil dehydrogenase activity was ® IButton DS1921G-F5, Maxim Integrated, San Jose, USA). Mea- determined by using 1 g of soil, and the reduction of p-iodoni- surement was obtained at locations which are comparable in terms trotetrazolium chloride (INT) to p-iodonitrotetrazoliumformazan of soil type and orientation. At each point, two temperature data was measured by a modification of the method reported by García loggers were buried at 5 cm depth (i.e. 4 sensors per path). These et al. (1993). Basal soil respiration was also analyzed by placing 15 g sensors were programmed to register the temperature every 4 h of soil moistened to 50e60% of its water-holding capacity (water during 9 days. Temperature is a major limiting factor for biota in potential: 0.055 Mpa) in hermetically sealed flasks and incubating Antarctica. Therefore, it was important to assess if there were dif- for 20 days at 28 C. The CO2 released was periodically measured ferences between the two paths. (every day for the first four days, then after this, weekly) using an Basic soil properties were assessed at the center of each path infrared gas analyzer (Toray PG-100, Toray Engineering Co. Ltd., and in a control area, 3 m away from the center. Composite samples, Japan). The data were summed to give a cumulative amount of CO2 each 1 Kg, were built by taking and mixing small soil samples released after 20 days of incubation. All these previous variables collected from nearby points. Samples were sieved (<2 mm) and all were obtained by duplicate per point (2 replicates), using the debris and plant remains were removed before analysis. Electrical average for calculations. Finally, the microbial biomass carbon was conductivity and pH were measured in this composite sample in a determined by Vance et al. (1987) method adapted by García et al. 1/5 w/v aqueous solution using a pH-meter (Navi Horiba D-54). The (2003). In this case, only one data point was obtained because a total organic carbon was determined by the Walkley and Black larger volume of soil was needed for its determination. method (1934), based on the oxidation with K2CrO7, and the organic matter was determined by multiplying the total organic 2.4. Flora survey carbon content by 1.728. The total phosphorus content was determined by the method of Olsen et al. (1954). Total nitrogen was The non-vascular cryptogam communities present in the sur- fi determined using Kjeldhal's method modi ed by Bremmer (1965). roundings (i.e. first 3 m) of both paths were characterized following Total carbonates were measured by evaluation of the HCl excess the classifications by Smith (1996), Ochyra et al. (2008), Carvalho with NaOH. Soil moisture was determined using the gravimetric et al. (2009) and Pertierra et al. (2013) (Table 1). We focused on 324 P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330

Table 1 Classiﬁcations of cryptogamic vegetation types and communities used in this study.

Type of Community References Description formation

Alga sheet Prasiola crispa association Smith (1996) Assemblage formed or completely dominated by the foliose green alga Prasiola crispa, forming loose convoluted sheets. Mainly on wet soils and commonly associated with biotically disturbed habitats. Bryophyte Sanionia-Warnstorfia Ochyra et al. (2008)/Pertierra Extensive carpets formed by Warnstorfia sarmentosa and/or W. fontinaliopsis, and a variable carpets and association et al. (2013) proportion of Sanionia georgicouncinata, covering heavily flooded soils. mats Sanionia georgicouncinata New association here Moss carpets of Sanionia georgicouncinata developed on slopes where water flows. The soil association proposed has lower water content and in accordance, the more hygrophilous mosses of the genus Warnstorfia are totally absent. Tall moss Bryum pseudotriquetrum- Smith (1996)/Ochyra et al. Community mainly constituted by Sanionia uncinata with a variable proportion of Bryum cushions Sanionia uncinata (2008)/Carvalho et al. (2009) pseudotriquetrum, forming tall moss cushions and occasionally deep undulationg carpets. (hummocks) association Mainly developed on drainage areas. Sanionia uncinata- Carvalho et al. (2009)/ Assemblage formed by large hummocks of Sanionia uncinata, irregularly patched with turfs Polytrichastrum alpinum Pertierra et al. (2013) and cushions of Polytrichastrum alpinum that can be abundant. Polytrichum piliferum and association Ceratodon purpureus may also occasionally be found. It occurs on well drained soils on seepages areas not permanently wetted.

plant communities for this part of our study since they are easier to (1999). The species Hypogastrura viatica (Tullberg, 1872) was clas- monitor than single species. The type of plant community that was sified according to Jordana et al. (1997), owing to the fact that it is a present was recorded every 10 m along a section of 430 m for the cosmopolitan species. Having identified the specimens, we ob- Lower Path and 360 m for the Upper Path, producing abundance tained the following data for each path: total number of individuals, data for each plant community. This assessment was only con- mean number of specimens at each sampling point (and the stan- ducted in the middle part of the island, which is mostly covered by dard error of the mean), relative abundance of each species, total the moss carpet. Plant diversity comparisons for the two paths richness, Shannon-Wiener index and evenness. The equations were were conducted using community richness s (total number of similar to those described in Section 2.4, but using Collembola different plant communities along the path), Shannon-Wiener in- species instead of plant communities (i.e. s is replaced by the total 0 0 0 dex H , H max and Pielou's evenness index J , given by the equations: species richness of Collembola for each path). The number of specimens and the richness were also obtained for each sampling XS 0 0 0 0 H point. H ¼ ðp Þðlog p Þ H ¼ log sJ¼ i 2 i max 2 H0 i¼1 max 2.6. Statistical analyses where pi is the proportion of 10 m subsections belonging to the i 0 Several results are summarized reporting the mean and stan- plant community in each path. H max is the theoretical maximum dard error of mean. Mann-Whitney non-parametric tests were for the Shannon-Wiener index, i.e. when all pi values are equal. To calculate the indices we only used data from sections where applied to compare the two paths at the same distance (i.e. 0 or vegetation was present in the surroundings of the path. Therefore, 3 m) for physical-chemical, biochemical and microbiological vari- those sections where the paths ran through an area of bare soil ables. Wilcoxon tests were used for comparisons of these variables were not considered (i.e. 27% of the assessed section for the Lower at 0 and 3 m using pairs of data from the two paths. Kruskal-Wallis Path, and 22% for the Upper Path). tests were applied for comparisons of soil penetration resistance between the center of the path and the two external control areas. Significance level for null hypothesis rejection was established at 2.5. Fauna survey 0.05 for all the tests. The software used for the statistical analysis © © was IBM SPSS Statistics 19 (SPSS, Inc.). Free-living terrestrial fauna was obtained from three soil samples of approximately 500 cm3 from each path, taken at represen- 3. Results tative points along the track. Samples included the top 8 cm of soil, following the methodology used in previous studies (Tejedo et al., 3.1. Physical and chemical variables 2005, 2009, 2012). The vegetation community in the area close to the sampling point was also registered. Fauna were extracted using The mean track width of the Lower Path was 1.68 ± 0.21 m the Berlese-Tullgren funnel technique. Animals collected under the (260 m recorded), and 3.42 ± 2.74 m over the section of the Upper desiccating soil were preserved in 99% ethanol before being sorted Path that was assessed. Only 110 m of the Upper Path was assessed under a dissecting microscope. For the rest of the analysis, only due to the presence of snow over the path during the fieldwork Collembola were used since it was the only taxon present in all season. Soil penetration resistance in the center of the Lower Path samples with high abundances (mites, nematodes and tardigrades was 1.32 ± 0.98 Kg/cm2. The value obtained from the Upper Path were absent in some samples, or appeared in very low numbers). was lower (1.19 ± 0.39 Kg/cm2) but the difference between the two Collembola are sensitive to trampling, showing a clear decrease in values was not statistically significant. Soil penetration resistances abundance when a certain level of trampling has been exceeded were lower in control areas than in the center of both paths (Fig. 3). (Tejedo et al., 2005, 2009). This makes them suitable for monitoring Along the Upper Path the center of the track presented a statistically purposes. Specimens were cleared in lactic acid over a one-week significantly higher soil penetration resistance (p-value 0.001). Soil period. Collembola were mounted on slides using Hoyer's solu- penetration resistances along the Lower Path had a higher variance tion and identified to species level under a phase contrast micro- and differences were not statistically significant (p-value 0.458). scope. Identification was done following Salmon (1962), Wise Secondary treads were only detected along the Lower Path. In total, (1970a, 1970b, 1971), Greenslade (1995, 2006) and Convey et al. 10 sections occupying 327 m and affecting an area of 385.3 m2 were P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330 325

there was more soil moisture in the surrounding areas, meanwhile along the Upper Path the reverse trend was observed, with a slightly higher soil moisture in the path itself.

3.2. Biochemical and microbiological variables

The center of the Lower Path showed statistically significantly higher values than the Upper Path for basal soil respiration, b- glucosidase and phosphatase activities (Table 3, upper side). For the other biochemical and microbiological variables, there were no statistically significant differences between the two paths. This same trend appeared when microbial activity in the control areas (3 m) was compared (Table 3, middle side), with significant differences in the previously cited three variables. Within the Lower Path (Table 3, bottom side), all variables were higher at 3 m, except for dehydrogenase activity (no significant difference) and basal soil respiration (significantly lower). In the Upper Path microbial activity at 0 m was higher for all parameters except for dehydrogenase activity (the same value) and phosphatase activity (significantly lower).

3.3. Flora survey

Five vegetal communities were identiﬁed along the two paths (Table 1). Along the Lower Path, the Sanionia-Warnstorﬁa association was the most abundant plant community (30%, Fig. 4), followed by Bryum pseudotriquetrum-Sanionia uncinata association (23%), Prasiola crispa association (14%) and Sanionia uncinata-Pol- ytrichastrum alpinum association (7%). Bare soil occupied 27% of the surroundings of this path. The Upper Path was dominated by two communities, Sanionia georgicouncinta association (41%), and Sanionia uncinata-Polytrichastrum alpinum association (35%). The surroundings of the rest of the path were occupied by Prasiola crispa association (3%) and bare soil (22%). Plant community richness was higher for the Lower Path (4 against 3 in the Upper Path), Fig. 3. Box-plot for soil penetration resistance recorded in the Lower Path and the and it showed a higher diversity based on a better evenness data 0 0 0 Upper Path. (H ¼ 1.86 vs 1.20, H max ¼ 4.86 vs 5.09, J ¼ 0.38 vs 0.24).

3.4. Fauna survey recorded. Mean soil temperature was 2.5 ± 1.6 C along the Lower Path and 2.2 ± 1.6 C along the Upper Path. The maximum and A total of five Collembola species and 2284 specimens were minimum temperatures were the same along both paths: 0.5 and recorded (Table 4). Cryptopygus antarcticus (Willem, 1901) was the 6.5 C. The highest temperature variation was recorded on 8 most abundant with 2252 specimens, followed by Archisotoma February: 5.5 C for the Lower Path and 6.5 C for the Upper Path. brucei (Carpenter, 1907) (24), Friesea grisea (Schaffer,€ 1891) (4), The lowest thermal oscillation was recorded on 5 February: 0.5 and Folsomotoma octooculata (Willem, 1901) (3) and Hypogastrura 1.5 C, respectively. viatica (1). The Lower Path had a higher abundance (2186 vs 98 No statistically significant differences in soil composition be- specimens, Cryptopygus antarcticus being the most abundant spe- tween the two paths were found when samples obtained at the cies along both paths), richness (4 vs 3 species) and diversity center of the path were compared (Table 2, upper side). pH values 0 (H ¼ 0.479 vs 0.441). However, evenness was higher for the Upper indicated moderate acidity in the soils of the Upper Path and low 0 Path (J ¼ 0.278 vs 0.240). The clear dominance of the species acidity in the Lower Path. Basic nutrients were higher along the Cryptopygus antarcticus in the Lower Path explained the result for Lower Path, with the exception of carbonates, which were present the evenness. Statistically, there were no significant differences in a similar (and low) quantity along both paths. Organic matter between the paths in terms of the abundance of Collembola (p- and soil moisture were also higher along the Lower Path. C:N ratio value ¼ 0.05). All species are native, except Hypogastrura viatica, reflected a higher degree of mineralization of the organic matter which is cosmopolitan and exotic (i.e., is clearly native to another along the Upper Path. This result agreed with the observed per- region and not to the locality under examination). centage of organic matter. The most prominent difference between the two paths was the soil moisture, which was higher for the 4. Discussion Lower Path. The same patterns were observed in those soils close to the tracks that were used as control, i.e. in samples taken 3 m away 4.1. Usefulness and limitations of selected indicators from the paths (Table 2, middle side). Again, there were no significant differences between the two paths. Comparing the data ob- Environmental management decisions should be taken based tained at 0 and 3 m from each path (Table 2, bottom side), we found on the results from holistic assessments that have been carefully no significant differences except for the soil moisture. This variable designed. For such assessments, it is very important to select had a different behavior along each path. Along the Lower Path appropriate indicators. We believe that the set of indicators that we 326 P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330

Table 2 Basic physical and chemical variables. N ¼ 3 for Soil Moisture. Statistically signiﬁcant differences for each variable are shown in bold (p < 0.05).

Area Path pH Electrical conductivity Total phosphorous Total Total carbonates Total organic C:N Organic Soil moisture 1 (mS/m) (ppm) nitrogen (%) (mg CO3 $ g ) carbon (%) ratio matter (%) (%) Center of the path Lower 6.22 26.50 156.03 0.273 0.039 1.40 5.13 2.41 29.50 ± 10.46 (0 m) Upper 5.56 24.50 118.27 0.124 0.042 0.64 5.16 1.10 13.54 ± 0.79 p-value 0.317 0.317 0.317 0.317 0.317 0.317 0.317 0.317 0.05

Area Path pH Electrical conductivity Total phosphorous Total Total carbonates Total organic C:N Organic Soil moisture 1 (mS/m) (ppm) nitrogen (%) (mg CO3 $ g ) carbon (%) ratio matter (%) (%) Surrounding area Lower 6.43 19.50 102.78 0.226 0.036 2.47 10.93 4.25 36.49 ± 17.54 (3 m) Upper 6.16 20.60 80.08 0.123 0.057 0.62 5.04 1.07 12.93 ± 1.10 p-value 0.317 0.317 0.317 0.317 0.317 0.317 0.317 0.317 0.05

Area Path pH Electrical conductivity Total phosphorous Total nitrogen Total carbonates Total organic carbon C:N ratio Organic matter Soil moisture

0m vs 3m p-value Lower 0.18 0.18 0.18 0.655 0.655 0.655 0.18 0.18 0.028 0m vs 3m p-value Upper 0.18 0.18 0.18 0.655 0.655 0.655 0.18 0.655 0.028

Table 3 Microbiological and biochemical variables. N ¼ 6 for all variables, except microbial biomass carbon (N ¼ 3). Statistically signiﬁcant differences for each variable are shown in bold (p < 0.05).

Area Path b-glucosidase activity Urease activity (mmol (N Dehydrogenase activity Phosphatase activity Basal soil Microbial biomass þ 1 1 1 1 1 (mmol eNH4 ) $ g soil $ h ) (mmol (INTF) $ g (mmol (PNP) $ g soil $ respiration carbon (mgC$ g ) 1 1 1 1 1 (PNP) $ g soil $ h ) soil $ h ) h ) (mg CO2 $ Kg ) Center of Lower 82.59 ± 4.89 123.85 ± 20.33 0.026 ± 0.009 49.95 ± 9.22 48.62 ± 15.18 272.98 ± 79.47 the path Upper 28.92 ± 5.58 44.47 ± 5.18 0.007 ± 0.001 9.01 ± 0.86 8.15 ± 1.57 318.35 ± 12.01 (0 m) p-value 0.04 0.06 0.335 0.016 0.01 0.513

Area Path b-glucosidase activity Urease activity (mmol (N Dehydrogenase activity Phosphatase activity Basal soil Microbial biomass 1 þ 1 1 1 1 1 (mmol (PNP) $ g soil $ eNH4 ) $ g soil $ h ) (mmol (INTF) $ g soil $ (mmol (PNP) $ g soil $ respiration (mg carbon (mgC$ g ) 1 1 1 1 h ) h ) h ) CO2 $ Kg ) Surrounding Lower 162.70 ± 54.66 175.53 ± 58.74 0.026 ± 0.007 66.84 ± 16.49 37.85 ± 10.71 1560.08 ± 210.38 area (3 m) Upper 19.96 ± 3.24 40.30 ± 9.66 0.007 ± 0.002 16.28 ± 4.01 8.60 ± 2.11 281.53 ± 124.11 p-value 0.04 0.078 0.078 0.04 0.037 0.05

Area Path b-glucosidase activity Urease activity Dehydrogenase activity Phosphatase activity Basal soil respiration Microbial biomass carbon

0m vs 3m p-value Lower 0.02 0.02 0.158 0.02 0.02 0.03 0m vs 3m p-value Upper 0.02 0.02 0.158 0.02 0.02 0.03

have chosen for this study has proven their efficacy to allow treads are not generated. Ice covers more sections of the Upper Path quantitative comparisons between the two paths. Our working over longer periods of the year, partly protecting the ground surface protocols were designed according to the document Practical from the effects of trampling. This, plus the reduced level of use in Guidelines for Developing and Designing Environmental Monitoring recent years, may be the reasons for the lower soil penetration Programs in Antarctica (Council of Managers of National Antarctic resistance data recorded for the Upper Path. In this regard, results Programs, 2005), thus having the advantage of being relevant to for this variable in 2013 were clearly different from those obtained the context and particularities of the Antarctic continent. A multi- in previous monitoring research carried out by our team in the disciplinary team has enriched the design of fieldwork and the 2008e09 season, when this route was used by the majority of discussion of results. Indicators were selected specifically to allow visitors. In 2008e09, an average value of 5.25 Kg/cm2 was recorded direct comparisons between the two paths. However, this restric- in the center of the track (Tejedo et al., 2012). Nonetheless, the tion also meant that some relevant issues could not be evaluated results from February 2013 were quite similar to those from the directly, e.g. the impact on aquatic communities caused by visitors 2010e11 season, when we recorded 1.43 Kg/cm2 in the most when walk along the stream channel in the Lower Path. Another impacted area of the track (Tejedo et al., 2012). In 2010e11 the use limitation of our selected indicator lies in the fact that some level for the Upper Path was decreasing. These new data suggest recorded faunal groups (mites, tardigrades and nematodes) could that the physical recovery of the first soil surface layer observed in not be used due to their low density in our samples. Other tech- 2010e11 was still ongoing. On the other hand, the Lower Path is niques related to more subjective elements were also excluded, as usually waterlogged due to the presence of the stream channeling in the case of visual impact on the landscape. melt water during the Antarctic summer. As a consequence, visitors tend to leave the route to avoid the muddy areas, creating some secondary treads that seriously affect the surrounding moss car- 4.2. Comparing physical and biological features for the two pets. In our opinion, this is the most serious physical impact assessed paths detected in this study. The physical-chemical soil features are similar for both paths in The Upper Path is wider than the Lower Path, showing a more the central area (0 m) and for the control area (3 m). This is an clearly marked track with less presence of muddy areas. For these expected result as both routes are very close together and are reasons, visitors tend to remain within the path and secondary P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330 327

presence there of the hydrophilic moss carpets. The basic soil data were consistent with previous results (Samsundar, 2011), and are within the usual range for most Antarctic soils (Thomas et al., 2008). Only a relatively high value for phosphorous was recorded, possibly due to feces from local wildlife crossing the trails area (penguins and occasionally seals), surface runoff from some nesting colonies and, to a lesser extent, trampling by visitors. Visitors first visit the nesting area at the beach and therefore their boots are partially covered with guano when they use the paths. There are significant differences between both paths regarding microbiota activity. In general, samples from the Lower Path have a more active microbial community, which produces a higher respiration. Therefore, environmental conditions are less favorable for microorganisms in the Upper Path. The differences could also be due to the presence of a larger amount of organic matter and soil water, in the surrounding area of the Lower Path. As soil organic matter increases, so do other soil properties such as water-holding capacity and microbiological activity. These results are consistent with those obtained in Barrientos Island by Samsundar (2011), who quantified soil DNA by UV spectrophotometry, obtaining a high microbial diversity. Moss communities living in the vicinity of the two paths are all vulnerable to human foot traffic, but to different extent. The Upper Path had communities that were more resistant to trampling. Sanionia-Warnstorfia association was the most abundant community in the Lower Path and it can be damaged by even a single footstep according to previous studies (Pertierra et al., 2013). The Sanionia georgicouncinata community, widespread in the Upper Path,isfloristically close to the Sanionia-Warnstorfia (i.e. they share most of the species) but is less vulnerable to trampling. This is a less hydrophilous community that thrives in soils with a lower soil Fig. 4. Plant coverage in assessed sections of both paths.

Table 4 Data for the soil biota (Collembola) collected in assessed sections of both paths.

Path Lower path Upper path

Collembola 2186 98 Mean ± SEM 728.7 ± 276.3 32.7 ± 10.1 Total richness 4 3 Shannon index (H0) 0.479 0.441 H'max 2.000 1.585 Eveness (J0) 0.240 0.278 Species and relative abundance Cryptopygus antarcticus (99.73%) Cryptopygus antarcticus (73.47%) Friesea grisea (0.18%) Archisotoma brucei (24.49%) Folsomotoma octooculata (0.05%) Folsomotoma octooculata (2.04%) Hypogastrura viatica (0.05%)

Path Lower path Upper path

Site sampling A B C A B C

Cryptogamic Bryum pseudotriquetrum- Sanionia- Sanionia uncinata- Sanionia Sanionia Sanionia uncinata- vegetation Sanionia uncinata Warnstorﬁa Polytrichastrum alpinum georgicouncinata georgicouncinata Polytrichastrum alpinum community association association association association association association Collembola 1280 486 420 31 16 51 Richness 2 3 2 3 1 2 Species and C. antarcticus (1279) C. antarcticus C. antarcticus (417) C. antarcticus (6) C. antarcticus (16) C. antarcticus (50) abundance H. viatica (1) (484) F. grisea (3) A. brucei (24) F. octooculata (1) F. grisea (1) F. octooculata (1) F. octooculata (1)

located over soils with a similar geological origin. Comparisons moisture. Therefore, trampling produces denudation in this com- between the center of the track and control areas indicated that the munity but does not create muddy areas. Sanionia uncinata-Poly- presence of both paths and their use by visitors did not affect most trichastrum alpinum association, also abundant in the Upper Path,is of the basic properties of the soil. Significant differences were solely the community on Barrientos Island that is the most resistant to obtained for soil moisture, which was particularly high in the sur- trampling. Finally, Bryum pseudotriquetrum-Sanionia uncinata as- rounding area in the case of the Lower Path in concordance with the sociation, common in the Lower Path and absent in the Upper Path, 328 P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330 is likely to be intermediate in terms of trampling sensitivity, as a safety risks for visitors, since in order to visit both tips of the island, result of its medium water content. movements in motorboats will have to be doubled. We think that Alien mosses or vascular plants were not detected. Bioinvasion proper track design and suitable guidance could lead to the assessment could be difficult since both paths are frequently establishment of a walking tour across the entire island that also affected by natural disturbances from dynamic forces such as snow- minimizes the pressure on the fragile terrestrial ecosystems in the melting or strong offshore winds. However, the greater amount of middle part of Barrientos. organic matter and soil water indicate that Lower Path could be more vulnerable to this threat. In addition, the presence of a stream 4.4. Reflections on how to effectively connect scientific knowledge in this path may facilitate introductions through the washing of and management decisions on Antarctica visitors' boots. According to research conducted in 2007e08 among visitors to Antarctica, footwear is the item that carries the highest The number of visits to some Antarctic sites with high biological propagule load of seeds, and fragments of bryophytes and lichens diversity, such as Barrientos Island, has been growing in recent (Huiskes et al., 2014). Since ice remains longer on the Upper Path it years (IAATO, 2015). It is indispensable to undertake studies to acts as a physical barrier between the first soil layer and visitors, assess the current and potential impacts of human activities in hence reducing bioinvasion risk. Antarctica. The following is a series of reflections on science-based Although alien plants were not detected, a specimen of Hypo- environmental management decision-making that emerged from gastrura viatica, a cosmopolitan Collembola, was recorded on the our experience at Barrientos Island. Lower Path. This species was already recorded in previous seasons A) It is essential to apply the Precautionary Principle. This is at this site by our research team (unpublished data), leading us to particularly relevant when previous scientific information is believe that it has probably successfully established on the island. limited or scarce. The Protocol on Environmental Protection to the H. viatica is usually classified as invasive in Antarctica (Greenslade Antarctic Treaty, signed in Madrid on 4 October 1991, does not and Convey, 2012). It normally occurs as a monoculture and clearly force contracting Parties to take the Precautionary Principle forms large communities (Convey et al., 1999), being able to un- into account in their decision making processes. However, it can be dergo its whole development under water (Witteveen and Joose, argued that such an obligation derives more implicitly from 1988). This last feature may be an advantage for its establishment particular provisions of the Protocol, e.g. Art. 3(2)(c): “activities in on the Lower Path, where soil moisture is higher and where there the Antarctic Treaty area shall be planned and conducted on the basis are more flooded areas. of information sufficient to allow prior assessments of, and informed judgments about, their possible impacts on the Antarctic environment 4.3. Overall considerations from the global assessment and dependent and associated ecosystems and on the value of Antarctica for the conduct of scientific research”. Applying the pre- All these results show that the adoption of the Lower Path cautionary principle becomes necessary if the Protocol is to be resulted in new unnecessary impacts, while it was chosen with the implemented in accordance to its objectives and spirit (Bastmeijer goal of avoiding the visual impacts of the Upper Path. According to and Roura, 2004). The Precautionary Principle was immediately our assessment, the use of the Upper Path would result in the lowest applied as a temporary solution in the case of Barrientos Island. In overall impact. This path has other indirect advantages such as view of the initial reports presented by Ecuador and Spain in 2011, allowing visits to the penguin colony located at the eastern tip of the CEP recommended limiting access to the middle part of the the island. This route quickly leaves the beach zone e an important island, thus eliminating human pressure on the ecosystem of the area that serves as access to the sea for marine animals e thereby area and encouraging research to assess the extent of the problem. reducing interactions between visitors and local fauna in this crit- B) Scientific knowledge is essential to detect a problem and eval- ical area and minimizing stress on marine fauna. Traffic of visitors uate its consequences, but it is only the first step to solving it. Policy around this breeding area should not be a problem if the relevant makers may be aware of the situation and take the necessary guidelines for visitors are respected. These include Guidelines for management measures to control and remediate it. For the paths of visitors to the Antarctic (Resolution 3, Antarctic Treaty Consultative Barrientos Island, the Antarctic Treaty Consultative Parties quickly Meeting XXXIV, 2011, Buenos Aires) and the specific guidelines for understood the scientific arguments presented by Ecuador and Barrientos Island adopted by the ATCM, following recommendation Spain, endorsing the CEP's proposal to restrict access. Moreover, of the CEP. Similar to other sites, it would be sufficient for guides this recommendation encouraged Parties active in the area to and the expedition leaders to provide basic guidance to visitors to cooperate in designing and implementing appropriate surveys that ensure that disturbance to local wildlife is kept to a minimum. The will help inform decisions on future management actions. This first section of the Upper Path is not clearly marked. While this may proposal was crucial for Spanish and Ecuadorian National Antarctic be initially considered as a weakness, guides and visitors have often Programs to receive support to develop the studies presented here. chosen those tracks that generated fewer disturbances to penguins Therefore, although a conservation process can be started from the depending on where chicks and adults were located at each field of scientific research, its solution should involve all stake- moment. Another advantage of this path is that the ornithogenic holders (e.g. Parties, CEP, tourism industry, etc.). soil located in the first section has a sandy texture with numerous C) For an effective communication between scientists and policy pebbles on surface, and hence, has low sensitivity to trampling. makers, an appropriate meeting forum must exist. Regarding envi- A second alternative, which was considered in the past meetings ronmental issues in the Antarctic region, the primary forum is the of the CEP, is to permanently prohibit access to the middle part of annual meeting of the CEP. This event allows issues related to the the island, limiting visits to the eastern and western tips of the implementation of the Protocol on Environmental Protection to the island. We do not consider this option as a suitable choice because Antarctic Treaty e the main document dedicated to the protection it would have three undesirable consequences. 1) Impacts will be of the Antarctic environment under the Antarctic Treaty System e focused in areas where there are very sensitive elements (nesting to be discussed. Thanks to the existence of the CEP meetings, ex- areas of southern giant petrels and penguins, and beaches where changes of information on environmental issues in the Antarctic there are seals). 2) Visitors will not be able to enjoy the landscape region between scientists and managers are possible. dominated by moss carpets in the middle part of the island. 3) The D) Scientific information in which management decisions are based movement of visitors on motorboats will rise, which increases the on should be widely disseminated. Data should be presented in a P. Tejedo et al. / Journal of Environmental Management 177 (2016) 320e330 329 simple and direct way, since potential interested parties are diverse EVA-ANTARCTICA (CTM2009-06604-E) and ALIENANT (CTM2013- and include experts (i.e. researchers and staff of National Antarctic 47381-P), which were supported by the Spanish Government, and Programs), managers (decision makers, representatives of nations Proposal for Tourism Management of Barrientos Island and Sur- and institutions) and general public (conservation Non- roundings (2011e13), funded by the Ecuadorian Government. The Governmental Organizations, journalists, etc.). Conclusions and authors would like to thank Jose Olmedo Moran, Executive Director recommendations should be clear, easy to understand, robust, of the Ecuadorian National Antarctic Program, for his advice and agreed by consensus among stakeholders and action-oriented. The support for this work, and Dr Tina Tin for her constructive and ideal situation is to present this information at CEP meetings and helpful comments during the editing process, which contributed to through scientific journals (which have the added benefit of vali- improving this paper. Many thanks also for the suggestions and dating the work by using the peer-review system) and, if appro- proposals by two reviewers and the Associate Editor. priate, in the media to inform the general public. E) Management decisions should take into account previous sci- References entific knowledge. Numerous references review the efficacy of management measures that have been applied to address envi- Aislabie, J.M., Balks, M.R., Foght, J.M., Waterhouse, E.J., 2004. Hydrocarbon spills on ronmental impacts within the Antarctic Treaty area (e.g. Aislabie Antarctic soils: effects and management. Environ. Sci. 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