Introduction
In the beginning of the twentieth century, whale hunters intensively used the maritime Antarctic and South Shetland Island Archipelago (Tønnessen & Johnsen, Reference Tønnessen and Johnsen1982). Admiralty Bay, inner King George Island, is an area of outstanding environmental, historical and scientific interest where remnants of former sealing and whaling activities still remain. Sheltered harbours and accessible beaches enabled an early start to whaling activities in Admiralty Bay. The bay offered protection for ships during the nineteenth and early twentieth century hunting seasons, and the ruins of installations from the latter period still remain (Rakusa-Suszczewski, Reference Rakusa-Suszczewski1998).
Humpback whales (Megaptera novaeangliae Borowski) were the most intensively captured, and after ca. 1914, fin whales (Balaenoptera physalus L.), blue whales (Balaenoptera musculus L.) and, to a lesser extent, sei whales (Baleanoptera borealis Lesson) were also captured. According to data from International Whaling Statistics (1931), 183, 791, 930 and 1743 whales were captured in the South Shetland Islands region in 1906, 1907, 1908 and 1909, respectively (Rakusa-Suszczewski, Reference Rakusa-Suszczewski1998). The activity on the islands remained substantial until ca. 1960 when Norwegian–British Antarctic whaling came to an end (Proulx, 1986). In the Admiralty Bay area, the modern whaling industry began in 1906, when this area was used as a harbour for whale-catchers and factory ships until 1931. Evidence of the industry remains in the form of whale vertebrae present on many of the beaches (Miller, 2007). These bones remain as heritage of the whaling period, together with buildings and wooden and metal objects.
Kittel (Reference Kittel2001) catalogued the whaling objects in the Admiralty Bay area and mapped the bones found on the beaches and surrounding areas. The largest accumulations of whale bones, mainly vertebrae, ribs and small fragments of other bones, are found at Hennequin Point, Keller Peninsula (near the Brazilian station) and near the Arctowski Station (Poland) (Fig. 1a). In the last decade, several research groups have visited Hennequin Point (62°03′40″–62°05′40″S and 58°23′30″–58°24′30″W), most have been Brazilian researchers studying vegetation and seabird diversity (Victoria et al., Reference Victoria, Albuquerque, Pereira, Simas, Spielmann and Schaefer2013).
a. King George Island, Antarctic, showing Hennequin Point (arrow), Admiralty Bay, where lichen and moss species were sampled from whale vertebrae. b. Distribution map of vertebrae (black dots) on the raised beaches typical of the study area. c. Photographs of the study area presenting an example of a whale vertebra, in the foreground, with notable colonisation by multiple lichens.
The Antarctic flora is composed mainly of bryophytes and lichen species adapted to harsh conditions, including low temperatures and a short photoperiod. The flora comprises 111 moss species and 360 lichen species (Ochyra et al., Reference Ochyra, Smith and Bednarek-Ochyra2008; Øvstedal & Smith, Reference Øvstedal and Smith2004); however, recent studies suggest that lichen numbers may reach 500 species (Øvstedal & Schaefer, Reference Øvstedal and Schaefer2013). There are only two species of native angiosperms described from Antarctica, Deschampsia antarctica Desv. and Colobanthus quitensis (Kunth.) Bartl. (Smith, Reference Smith and Laws1984). Plants are limited by low water availability and low temperature ranges (Gignac, Reference Gignac2001; Longton, Reference Longton, Taylor and Leviton1982). Since ice-free areas are scarce and growth conditions are restrictive, the area around Admiralty Bay is a useful model for monitoring changes in environmental conditions.
Lichens are the dominant species in most habitats of the Antarctic biome, with a few exceptions. However, their occurrence and development are restricted by local environmental conditions, such as substratum instability, rock type and surface texture, permanent shading from direct solar radiation, excessive exposure to strong and abrasive wind action, mineral particles and ice crystals and, in the close proximity of bird colonies, the impact of disturbance and toxic levels of certain chemical elements (Smith, Reference Smith and Riffenburgh2007). Some species are abundant and form distinct communities in habitats receiving nutrient enrichment (especially from nitrogenous compounds in meltwater run-off and in aerosol form) from seabird colonies (Jablonski, Reference Jablonski1986); although lichens may develop dense stands even in some nutrient-deficient habitats (Albuquerque et al., Reference Albuquerque, Victoria, Schunemann, Putzke, Gunski, Seibert and Pereira2012).
The relationship between mechanical, chemical and mineralogical soil properties and the type of substratum are likely to influence lichen distribution. Substrate pH changes may also affect the formation of lichen stems. Garty et al. (1974) found that Squamarina species were located on soils with low shrinkage rates, but when the shrinkage rate increased above five per cent the lichens colonised rock and moss instead. Gaio-Oliveira et al. (2005) found that, in non-polar environments, changes in nitrogen concentrations had significant effects on the thallus development of Xanthoria parietina. (L.) Th. Fr. Armstrong (1990) used the same species in an experiment to evaluate the effect of pH change on growth by exposing samples to droppings from a variety of birds. Treatment with bird droppings was essential for the survival of X. parietina thalli on siliceous rock away from the sea, suggesting that this species may be more responsive to changes in pH than nitrogen concentration. In any areas of land where ideal growing conditions do not exist, whale bones may support species establishment.
The most important substrata for the development of native apophytic flora are whale bones, especially vertebrae (Olech, Reference Olech1996). The occurrence of flora on whale vertebrae is related to microclimate conditions and nutrients retained in the bone pores (Olech, Reference Olech1996). However, detailed information about which species can colonise this type of substrate are lacking. Are all species of lichen able to grow on whale bones deposited on the shores of the Antarctic ice-free areas? Does this new substrate represent a possibility for an expansion of plant communities or only a small group of species?
With increased human activity in Antarctica, anthropogenic impacts on terrestrial ecosystems may become a reality, as shown in other ecosystems already affected by human activity. Some of these changes are increasingly visible, especially by changes in vegetation and geographical scale due to the introduction of non-native species, such as Poa annua L. (Olech, Reference Olech1996). The whale bone remnants of the Antarctic hunting era could be considered an important substrate which affects the distribution of mosses and lichens in the Antarctic environment.
The aim of this study was to identify lichen and plant species growing on whale bones at Hennequin Point and to compare the results with similar approaches in other areas of maritime Antarctica.
Materials and methods
Sample collections
Seventy (70) whale vertebrae on the beach at Hennequin Point, King George Island, Antarctica, were sampled (Fig. 1b) during the austral summer 2010–2011. The bones sampled were previously mapped by Kittel (Reference Kittel2001). The upper surface of each vertebra was analysed to verify the presence of lichens and mosses (Fig. 1c). Photographs were taken of each visible plant or lichen found growing on the bones. Small samples were collected, especially for those species that require microscopic analysis for identification, from each bone using a knife or chisel. The specimens found were identified based on specialist literature: bryophyte identification was based on Ochyra (Reference Ochyra1998) and Ochyra et al. (Reference Ochyra, Smith and Bednarek-Ochyra2008), and lichen identification was based on Øvstedal & Smith (Reference Øvstedal and Smith2001) and Redon (Reference Redon1985). The findings were compared with other reports of lichen and moss occurrences on whale bones available in the published literature (Kim et al., Reference Kim, Ahn, Hong, Andreev, Lim, Oh and Hur2006; Olech, Reference Olech1996).
In order to represent the complexity of the surface of the whale bones and to estimate its microtopography, a photographic survey was carried out. Each whale vertebrae sampled in Hennequin Point was photographed to determine the percentage of lichen or moss coverage (referred to hereafter as plant coverage [PC]). For this analysis, two bones with high density coverage and two with low density coverage were selected. Each image was submitted to a treatment where an average value was computed for each pixel. To calculate an average value, the wavelengths in the visible band, R, G and B, were divided by three using the Geographic Information System (GIS) of the QGIS software; the resultant image formed is called the simple band image (ImgS). To determine percentage of exposed bone, manual contour and creation of a vector layer of the bone (Lim) was performed, in which only bone was contained in the image. With the ImgS for each bone and its Lim vector layer, a cut was made using the trimming tool from the same program, to obtain an image of the inner part of the bone (ImgEX).
To distinguish the surface of the bone from the surface covered with lichen or moss, a script was created in the R program (R Core Team, Reference Core Team2017). The main package used in this script was ‘raster’ (Robert, Reference Robert2015). The ‘K-means’ tool (R Core Team, Reference Core Team2017) was used to group the reflectance values for each pixel of each ImgEX in order to differentiate between PC and bone (clusters 1 and 2, respectively). The number of pixels representing each of the two clusters was calculated and their percentages obtained. Finally, for visual exemplification, an image was generated showing the clusters obtained.
Results
Species composition and richness on whale vertebrae
Fifteen lichen and two moss species were identified growing on the whale vertebrae found on the beaches at Hennequin Point, King George Island. Olech (Reference Olech1996) and Kim et al. (Reference Kim, Ahn, Hong, Andreev, Lim, Oh and Hur2006) found 19 lichen and two moss species on whale bone substrata. These papers also reported algae species growth on these substrata, but these are not evaluated in the present work.
The richest and most diverse flora compositions were found on the bones compared with the immediate surrounding areas on the beaches. Species observed in the surrounding areas were predominantly epilithic found on sea cliffs. Many species that occur preferentially in sites at much higher elevations relative to the sea level (15–300 m above sea level, for example) are growing on the whale bones on the beaches, suggesting that this alternative substrate enables the emergence of these species closer to the sea.
Fig. 2 shows the four bones selected for further analysis and the cluster patterns obtained. Two bones had high density PC (class I; Fig. 2a,c) and two had low density coverage (class II; Fig. 2e,g). The pattern of surface roughness is quite different between the class I and class II bones. Class I bones have a higher apparent roughness (Fig. 2a–d) than class II, which have a smoother surface with rough edges (Fig. 2e–h). PC is a function of the bone reflectance pattern at wavelengths in the visible band (R, G and B), whereby the PC increases with the roughness of the bone surface (Table 2). In summary, these patterns demonstrate that more complex bone surfaces favour plant growth.
Photographs of whale bones (a., c., e. and g.) showing plant colonisation and ImgEX images showing the respective cluster patterns (b., d., f. and h.). Class I, high density plant coverage (PC); class II, low density PC. Cluster 1, standard PC; cluster 2, bone surface.
Lichen and moss species identified on whale bone substratum at Hennequin Point. Also presented are the most common substrata and localities relative to sea level for each species.
*Non-fertile specimens.
The number of pixels analysed for each bone and percentage plant coverage (PC) for each sample.
b, d, f and g represent part labels in Fig. 2.
The most common plant communities established on beaches in the maritime Antarctic that are associated with pebbles and fragmented rocks, such as moss carpet formations and fruticose and crustose lichen formations, were both found in the Hennequin Point area in the 2004–2005 austral summer (Victoria et al., Reference Victoria, Albuquerque, Pereira, Simas, Spielmann and Schaefer2013). In fact, the latter community (invariably with Buellia spp., and usually Lecidea cancriformis C. W. Dodge & G. E. Baker, Rhizoplaca aspidophora (DC.) Leuckert & Poelt., Pleopsidium chlorophanum (Wahlenb.) Zopf., Carbonea spp., Acarospora spp. and several other crustose species) is less frequent and has been replaced by moss carpets of Sanionia uncinata (Hedw.) Loeske observed in the 2010–2011 austral summer.
Discussion
Of the species identified on whale bones by Olech (Reference Olech1996) and Kim et al. (Reference Kim, Ahn, Hong, Andreev, Lim, Oh and Hur2006), Acarospora macrocyclos Vain., Lecania brialmontii (Vain.) Zahlbr., Rhizoplaca melanophthalma (DC.) Leuckert & Poelt., Syntrichia magellanica (Mont.) R.H. Zander (cited as Tortula grossiretis Cardot) were also found in the present study. The moss S. magellanica and the lichens Caloplaca sp. and Buellia anisomera were the most frequent species found on the whale vertebrae sampled. These species are the most common in the maritime Antarctic plant communities and are recognised as pioneer species in non-vegetated sites (Victoria et al., Reference Victoria, Pereira and Costa2009b), probably because of their ideal growing condition (Olech, Reference Olech2004).
The moss species Hennediella heimii (Hedwig) R. H. Zander and the lichens Bacidia stipata I. M. Lamb., Buellia anisomera Vain., Cystocoleus ebeneus (Dillwyn) Thwaites, Huea cerussata (Hue) C. W. Dodge & G. E. Baker, Lecidea sciatropha sciatrapha Hue, Ochrolechia parella (L.) A.Massal., Parmelia saxatilis (L.) Ach. and Psoroma cinnamomeum Malme were found growing on whale bones for the first time. Psoroma cinnamomeum, considered a muscicolous species, was recently documented on King George Island (Olech, Reference Olech2004). Ochrolechia parella has only been reported at one site at Hennequin Point up to 50 m above sea level and it occurs mainly on inland hills in other areas of Admiralty Bay (Olech, Reference Olech2004); this occurrence near the shore was unexpected. In contrast, the moss Hennediella heimii is commonly found in areas of salt spray deposition (Ochyra et al., Reference Ochyra, Smith and Bednarek-Ochyra2008), such as where the whale vertebrae surveyed in the present study often occur. Some species identified by Kim et al. (Reference Kim, Ahn, Hong, Andreev, Lim, Oh and Hur2006) on whale bones were not found in the present survey.
We observed that saxicolous species found growing on the whale vertebrae were not found on the surrounding pebbles on the beach. Plant growth limited to bones is probably related to the rich mineral content of the whale bones and the establishment of bird foraging/resting areas around the intertidal zone (Albuquerque et al., Reference Albuquerque, Victoria, Schunemann, Putzke, Gunski, Seibert and Pereira2012). Skuas and sea gulls nesting near the whale bones could increase nutrient composition, mainly nitrates derived from guano. The whale vertebrae act as alternative substrates for the Antarctic plant communities, since all species found in the present work are usually epilithic (Olech, Reference Olech2004; Øvstedal & Smith, Reference Øvstedal and Smith2001).
For bones with much more complex surface roughness and microtopography patterns almost half of the surface was covered with lichens or mosses (Fig. 2e–h). PC was much higher for these bones even when they were located in the same area as a bone with a class II pattern. The smoother surface of the class II bones is possibly a disadvantage for colonisation of plants (Fig. 2f,h), with a percentage coverage of 17.87–27.63% (Table 2). It can be clearly observed in these examples that a greater roughness at the edges favoured plant colonisation. The surface roughness may be associated with bone density. One theory that gains strength from this analysis is that greater roughness would favour the presence of plant tissues in deeper parts of the bones. However, to prove this hypothesis a bone profile analysis would be required, which was not performed in the present study. In summary, greater surface roughness and complexity in the microtopography influences lichen and moss colonisation of whale bones.
Considering the physiognomy and floral composition of the plant communities of ice-free areas in Admiralty Bay, evidence shows that these communities differ from those found on other islands of maritime Antarctic, probably because of the concentration of birds in the area and the distinct topography (Victoria et al., Reference Victoria, Albuquerque, Pereira, Simas, Spielmann and Schaefer2013). Moss formations are more expressive and complex in ice-free areas, and they occur mainly in tufts and carpets in lower areas such as on beaches and drainage lines (Victoria et al., Reference Victoria, Costa and Pereira2009a). However, moss cushions can be found in rocky outcrops of marine raised beaches and/or rock platforms and on rocks next to bird colonies (Jablonski, Reference Jablonski1986; Pereira & Putzke, Reference Pereira and Putzke1994). Studies show that lichens and mosses grow relatively slowly in polar regions compared with other environments (Havström et al., Reference Havström, Callaghan, Jonasson and Svoboda1995; Scott, Reference Scott, Kerry and Hempel1990; Seppelt, Reference Seppelt, Zoltan and Lloyd2011); however, Sancho et al. (Reference Sancho, Green and Pintado2007) observed the fastest reported growth rates for crustose lichens species in the Dry Valleys, with 100-fold higher rates than previously reported globally. Therefore, studies on the growth rate of lichens on alternative substrates are needed. The stable environment inside the bone is suitable for the growth of numerous organisms, including cyanobacteria and fungi (Raabová & Kovácik, Reference Raabová and Kovácik2013). These microenvironments may contribute to lichen and moss colonisation by acting as a trap for propagules and helping them to avoid abiotic stress; however, this assumption needs to be evaluated in further studies.
Evidence shows that whale carcasses act as dispersal and evolutionary stepping-stones between marine habitats (Distel et al., Reference Distel, Baco, Chuang, Morrill, Cavanaugh and Smith2000; Smith et al., Reference Smith, Kukert, Wheatcroft, Jumars and Deming1989), but whale bones deposited on beaches have not been evaluated in this regard. Specific studies are required to assess whether bones may also contribute to species dispersal in terrestrial environments.
Comparisons with previous surveys show an increase in the number of species growing on whale bones, with seven new lichen species identified. A long-term monitoring study is necessary to clarify the changes in diversity of plant colonisation of this substratum. Bone remnants are ecologically important and impact nutrient cycling in nature.
Acknowledgements
This work was supported by the Brazilian Antarctic Program through the National Council for Research and Development (CNPq; process no. 574018/2008), Research Foundation of the State of Rio de Janeiro (FAPERJ; process E-26/170.023/2008), Ministry of Environment (MMA), Ministry of Science and Technology (MCT) and Interministerial Commission for Sea Resources (CIRM), whom the authors thank for the financial and logistic support needed to perform this study.
