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The diversity and structure of plant communities in the maritime Antarctic is shaped by southern giant petrel’s (Macronectes giganteus) breeding activities

Abstract

Southern giant petrels (Macronectes giganteus) are found in the Antarctic. They build their nests with rock fragments, disturbing large areas during incubation and chick feeding periods; however, their impact on vegetation is unknown. Thus, we aimed to evaluate the effect of Petrel nests and associated breeding activities on the diversity and structure of cryptogam communities of Stinker Point, Elephant Island. We selected 13 nests in February and March 2012 and continue the monitoring in 2018. The area of direct influence of breeding activities was photographed to calculate plant community coverage. The results demonstrated that species richness, community coverage and composition, and beta diversity showed significant differences between active and inactive nests. The linear mixed-effect models revealed that the positive effect of nest area mainly caused variation in community coverage, but had a negative effect on beta diversity. Sphaerophorus globosus (lichen) grew around the inactive nests, sometimes forming a ring up to 1 m in diameter. This ring was then surrounded by the Chorisodontium acyphyllum moss colonized by S. globosus, and a final ring of Sanionia uncinata, colonized by the same lichen. Recently constructed nests are generally surrounded by Prasiola crispa and Sanionia uncinata carpets.

Key words
formations; phytogeography; plant; succession

INTRODUCTION

The Antarctic (continental and maritime) is home to various seabird species, such as penguins, seagulls and petrels (Petry et al. 2018PETRY MV, VALLS FCL, PETERSEN ES, FINGER JVG & KRÜGER L. 2018. Population trends of seabirds at Stinker Point, Elephant Island, Maritime Antarctica. Antarct Sci 30(4): 220-226.). These nest areas can affect plant communities (i.e., species richness, community composition, and structure of cryptogams), acting as microhabitats or habitat filters. However, these microhabitat factors are still poorly understood since previous studies have been restricted to evaluating the relationship of nutrient input and soil properties with plant communities (Poelking et al. 2015POELKING EL, SCHAEFER CEGR, FERNANDES FILHO EI, DE ANDRADE AM & SPIELMANN AA. 2015. Soil-landform-plant-community relationships of a periglacial landscape on Potter Peninsula, maritime Antarctica. Solid Earth 6: 583-594., Schmitz et al. 2018SCHMITZ D, PUTZKE J, ALBUQUERQUE MP, SCHÜNNEMAN AL, VIEIRA FCB, DE VICTORIA FC & PEREIRA AB. 2018. Description of plant communities from Half Moon Island, Antarctica. Polar Res 37: 1523663., 2020a, b, 2021). Furthermore, most studies in Antarctica are confined to changes in species richness and composition of cryptogam communities shaped by environmental filtering, such as soil texture, soil fertility, and topographical factors (Poelking et al. 2015POELKING EL, SCHAEFER CEGR, FERNANDES FILHO EI, DE ANDRADE AM & SPIELMANN AA. 2015. Soil-landform-plant-community relationships of a periglacial landscape on Potter Peninsula, maritime Antarctica. Solid Earth 6: 583-594., Schmitz et al. 2020aSCHMITZ D, SCHAEFER CEGR, PUTZKE J, FRANCELINO MR, FERRARI FR, CORRÊA GR & VILLA PM. 2020a. Pedoenvironmental gradient shapes non-vascular species assemblage and community structure in Maritime Antarctica. Ecol Indic 108: 105726., bSCHMITZ D, VILLA PM, PUTZKE J, MICHEL RFM, CAMPOS PV, MEIRA NETO JAA & SCHAEFER CEGR. 2020b. Diversity and species associations in cryptogam communities along a pedoenvironmental gradient on Elephant Island, Maritime Antarctica. Folia Geobot 55: 211-224., 2021SCHMITZ D, VILLA PM, MICHEL RFM, PUTZKE J, PEREIRA AB & SCHAEFER CEGR. 2021. Species composition, diversity and coverage pattern of associated communities of mosses-lichens along a pedoenvironmental gradient in Maritime Antarctica. An Acad Bras Cienc 94: e20200094. DOI 10.1590/0001-3765202120200094.), with limited studies on habitat filtering (i.e., microhabitats such as rocks and nests of birds).

Under the habitat filtering approach, microsite conditions can shape plant communities and filter species with similar attributes to colonize and grow in these microhabitats (Bao et al. 2019BAO F, VILLA PM, RODRIGUES AC, SCHMITZ D, ASSIS MA, ARRUDA R & POTT A. 2019. Topography and seasonality promote taxonomic beta diversity of seedlings in a tropical wetland. Oec Aust 23: 917-925., Campos et al. 2020CAMPOS VP, VILLA PM, SCHAEFER CEGR, ALVES NUNES J, POREMBSKI S & VIANA NERI A. 2020. Community composition, beta diversity and structure of high altitude grasslands along an altitudinal gradient in southeastern Brazil. Rev Biol Trop 68(3): 977-986., Cifuentes-García et al. 2020CIFUENTES-GARCÍA LM, VILLA PM, FERNANDES PERALTA D & BOND SCHWARTSBURD P. 2020. Bryophyte community diversity and structure associated with Asplenium auritum fern (Aspleniaceae) in a Brazilian Atlantic forest fragment. Rev Biol Trop 68(1): 230-241.). Thus, the patterns of diversity (richness and composition) and structure (coverage) of cryptogam communities in Antarctica are scale-dependent according to habitat filtering and promote high species turnover (beta diversity) along habitats such as pedoenvironments (Schmitz et al. 2020a, b, 2021). Beta diversity explains the temporal and spatial changes in plant community composition (Bao et al. 2019BAO F, VILLA PM, RODRIGUES AC, SCHMITZ D, ASSIS MA, ARRUDA R & POTT A. 2019. Topography and seasonality promote taxonomic beta diversity of seedlings in a tropical wetland. Oec Aust 23: 917-925., Campos et al. 2020CAMPOS VP, VILLA PM, SCHAEFER CEGR, ALVES NUNES J, POREMBSKI S & VIANA NERI A. 2020. Community composition, beta diversity and structure of high altitude grasslands along an altitudinal gradient in southeastern Brazil. Rev Biol Trop 68(3): 977-986., Nunes et al. 2020NUNES J, VILLA P, NERI A, SILVA W & SCHAEFER C. 2020. Seasonality drives herbaceous community beta diversity in lithologically different rocky outcrops in Brazil. Plant Ecol Evol 153(2): 208-218. doi: 10.5091/plecevo.2020.1668.); for example, the percentage of dissimilarity in the species composition of two communities (Koleff et al. 2003KOLEFF P, GASTON KJ & LENNON JJ. 2003. Measuring beta diversity for presence–absence data. J Anim Ecol 72: 367-382., Anderson et al. 2011ANDERSON MJ ET AL. 2011. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14(1): 19-28., Anderson & Walsh 2013ANDERSON M & WALSH D. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83(4): 557-574.).

Macronectes giganteus (southern giant petrel) reproduces in the Maritime Antarctic, and little is known of its impact on vegetation near the nesting area. Its breeding range extends from approximately 40°S (Gough Island) to 68°S in West Antarctica and sub-Antarctic islands and areas around the Antarctic Peninsula (Creuwels et al. 2005CREUWELS JCS, STARK JS, WOEHLER EJ & RIBIC CA. 2005. Monitoring of a southern giant petrel Macronectes giganteus population on the Frazier Islands, Wilkes Land, Antarctica. Pol Biol 28: 483-493.). Only a small number (~1%) of the population breeds on the coast of the Antarctic continent or certain South American island shores (Woehler et al. 2003WOEHLER EJ, RIDDLE MJ & RIBIC CA. 2003. Long-term population trends in southern southern giant petrels in East Antarctica. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, Van der Vies SM & Wolff WJ (Eds), Antarctic biology in a global context. Backhuys Publishers, Leiden, p. 290-295., Patterson et al. 2008PATTERSON DL, WOEHLER EJ, CROXALL JP, COOPER J, PONCET S, PETER HU, HUNTER S & FRASER WR. 2008. Breeding distribution and population status of the Northern giant petrel, Macronectes halli and the southern giant petrel M. giganteus. Mar Ornith 36: 115-124.). The nests are mainly built in colonies established in open spaces of variable size. On the South Shetland Islands, the petrel’s sole egg hatches during the first weeks of January, with the rookery period slightly longer than three months; parental care rarely extends longer than the fourth week of life (Cooper et al. 2001COOPER J, BROOKE MD, BURGER AE, CRAWFORD RJM, HUNTER S & WILLIAMS AJ. 2001. Aspects of the breeding biology of the northern giant petrel (Macronectes halli) and the southern giant petrel (M. giganteus) at sub-Antarctic Marion Island. Int J Ornith 4: 53-48., Conroy 1972CONROY JWH. 1972. Ecological aspects of the biology of the Giant Petrel, Macronectes giganteus (Gmelin), in the maritime Antarctic (Vol. 75). British Antarctic Survey, 74 p., Otovic et al. 2018OTOVIC S, RILEY M, HAY I, MCKINLAY JOHN, VAN DEN HOFF J, & WIENECKE B. 2018. The annual cycle of southern giant petrels Macronectes giganteus in East Antarctica. Mar Ornithol 46: 129-138.). This period causes various impacts on vegetation in the surrounding nesting area, mainly by feces deposition, rock removal, landing and departure movements, and other adult and chick disturbances that have not yet been evaluated.

In this study, we aimed 1) to evaluate the pattern of species richness, community composition, and structure of cryptogam communities around southern giant petrel (Macronectes giganteus) nests (inactive and active), and 2) to test the main effects of nest area on community coverage, species richness, and beta diversity on Stinker Point, Elephant Island, Maritime Antarctica.

MATERIALS AND METHODS

This study was carried out at Elephant Island, Maritime Antarctica (61°07ʹ S 55°03ʹ W) in February/March 2012 and continue the monitoring in February/March 2018. The central area is completely ice-covered and the coastal areas are ice-free, although access is difficult because of the steep cliffs and strong wind and wave action. Specifically, the sampling area was at Stinker Point (61°13ʹ25ʺ S 55°21ʹ35ʺ W), one of the largest coastal ice-free areas (4.5 × 1.8 km) with the richest flora and fauna of the island. This area is limited on the north by the Sultan Glacier and on the south by the Endurance Glacier (Pereira & Putzke 1994PEREIRA AB & PUTZKE J. 1994. Floristic composition of Stinker Point, Elephant Island, Antarctica. Korean J Pol Res 5: 37-47.). The Emílio Goeldi Refuge, a Brazilian facility, named after the Swiss-Brazilian naturalist and zoologist Emílio Augusto Goeldi. It was built in 1988, being the structure located on Stinker Point, Elephant Island (61° 3’ 0’ S 55° 12’ 0” W). The refuge can accommodate up to six people (Figure 1).

Figure 1
Schematic map of the South Shetland Islands (a), Elephant Island (b), Stinker Point (c), and the area studied (d).

A survey was done using drone photography and visiting the areas) to record all active nests when the group first arrived at the area and then kept monitoring to see which nests were abandoned. This was done to avoid impact over the giant petrel population. We have chosen to this study 13 nests in 2011/2012 early abandoned by the southern giant petrels (called active nests) found on the Brazilian refuge plateau area (750 × 462 m) or nests abandoned for more years (called inactive). The same nests studied in 2012 were also studied in 2018, being photographed to calculate the coverage of each plant/lichen species and to determine vegetal composition. From the nests found, the 13 chosen to do this study were also distanced from active nests still occupied by adults. This was done just to avoid disturbance to the reproductive populations. Some nests studied were abandoned for more than one year, since almost all the rock fragments were covered by vegetation, indicating no recent disturbance. These nests were also photographed to understand the plant succession around these nests after stopping disturbance (Table I). So, the nests were classified as inactive (abandoned for more than one season, with rocks of the main structure of the nest almost completely covered by vegetation, named P1, P2, P10, P11, P13, P14) or active (nests actively used for bird breeding each year, since rocks were clean of vegetation and clearly moved to structure the nest; named P3, P5, P6, P7, P8, P15 and P16).

Table I
Geographical location, area directly affected and altitude of the nest studied.

A square was delimitated from the area surrounding the nest (named the area of direct influence) using the disturbances provoked by the parents and chick, such as dislocated stones, landing marks, deposited feces and disrupted vegetation. The images were taken in 2012 from a one-meter-high positioned camera (Canon EOS 550D – 14 Megapixels) and fused to form one large and complete image of the nest and surroundings. In 2018, the same nests studied in 2012 were photographed using a drone Phantom F-4 and the Agisoft software to generate a complete figure and a map of nest distribution. To better understand plant organization, the dominant species were colored using the original photos as a reference to draw a diagram of the plant distribution surrounding the nest, and CobCal software was used to calculate the covered area and percentage.

Plant species were identified using specific literature such as Putzke & Pereira (2001)PUTZKE J & PEREIRA AB. 2001. The Antarctic mosses: with special reference to the South Shetland Islands. Canoas: Editora da ULBRA, 196 p., Ochyra (1998)OCHYRA R. 1998. The Moss Flora of King George Island, Antarctica. Kraków: Polish Academy of Sciences, W. Szafer Institute of Botany, 279 p. and Ochyra et al. (2008)OCHYRA R, LEWIS-SMITH RI & BEDNAREK-OCHYRA H. 2008. The Illustrated Moss Flora of Antarctica. Cambridge: Cambridge University Press, 709 p. for mosses and Redón (1985)REDÓN J. 1985. Liquenes Antárticos. Instituto Antártico Chileno, 21 lam, 121 p., Øvstedal & Lewis-Smith (2001)ØVSTEDAL DO & LEWIS-SMITH RI. 2001. Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge: Cambridge University Press, 424 p. and Olech (2004)OLECH M. 2004. Lichens of King George Island Antarctica. Kraków: The Institute of Botany of The Jagiellonian University, 391 p. for lichens. The collected specimens were dried and deposited at the Bruno Edgar Irgang Herbarium (HBI) of the Universidade Federal do Pampa (UNIPAMPA - São Gabriel – Rio Grande do Sul state - Brazil).

Data analysis

From the 13 nests studied to identify plant species associated (named P1 to P16), there were classified 6 nest as inactive (P1, P2, P10, P11, P13 and P14) and 7 as active (P3, P5, P6, P7, P8, P15 and P16). Data analysis was conducted mainly using R 3.6.0 Environment (R Development Core Team 2019R DEVELOPMENT CORE TEAM. 2019. R version 3.6.0. In. R Foundation for Statistical Computing, Vienna, Austria.). The PC-Ord 5.15 software (McCune & Mefford 2006MCCUNE B & MEFFORD MJ. 2006. PC-ORD: Multivariate analysis of ecological data. Version 514 for Windows [Users Guide] MjM software design.) was used to analyze the similarity of species between nests. “ggplot2” package (Hadley 2015HADLEY W. 2015. R ggplot2 package: An implementation of the grammar of graphics. http://ggplot2.org, https://github.com/hadley/ggplot2. Accessed January 2021.
http://ggplot2.org...
) was used to create graphical illustrations of the results. In general, we analyzed the data by comparing communities between active and inactive nests as described above. To compare the means of cover between the two types of nests using the Wilcoxon test, we first tested the normal distribution using the Shapiro-Wilk test and evaluated the Q-Q graph. Then we evaluated the homogeneity of variances using the Bartlett test (Crawley 2013CRAWLEY MJ. 2013. The R Book, second ed. Wiley, London, 1080 p.).

Species richness, community composition, and dissimilarity

The sampled-based rarefaction and extrapolation approach (Chao et al. 2014CHAO A, GOTELLI NJ, HSIEH TC, SANDER EL, MA KH, COLWELL RK & ELLISON AM. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84(1): 45-67.) was used based on 100 replicate bootstrap runs to estimate 95% confidence intervals of interpolated and extrapolated curves (Colwell et al. 2012COLWELL RK, CHAO A, GOTELLI NJ, LIN SY, MAO CX, CHAZDON RL & LONGINO JT. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1): 3-21.) for species richness comparisons between sampling active and inactive nestsinactive using the “iNEXT” package (Hsieh et al. 2016HSIEH TC, MA KH & CHAO A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7: 1451-1456.). Thus, whenever the 95% confidence intervals did not overlap among rarefaction and extrapolation curves, there were significant differences (p < 0.05) (Colwell et al. 2012COLWELL RK, CHAO A, GOTELLI NJ, LIN SY, MAO CX, CHAZDON RL & LONGINO JT. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1): 3-21.).

A non-metric multidimensional scaling (NMDS) analysis based on Jaccard dissimilarities using the “metaMD”’ function (Clarke 1993CLARKE KR. 1993. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143., Oksanen et al. 2018OKSANEN J ET AL. 2018. ‘Vegan’: Community Ecology Package. R package version 2.4-6. https://cran.r-project.org/web/packages/vegan/vegan.pdf (June 16, 2020, date last accessed).
https://cran.r-project.org/web/packages/...
) and permutational multivariate analysis of variance (PERMANOVA, 9999 permutations) based on the “adonis” function was used to compare community composition between nests groups. Furthermore, we used the “MDSrotate” function, which rotates an external environmental variable (coverage and area) to be parallel to the first multidimensional scaling dimension (Oksanen et al. 2018OKSANEN J ET AL. 2018. ‘Vegan’: Community Ecology Package. R package version 2.4-6. https://cran.r-project.org/web/packages/vegan/vegan.pdf (June 16, 2020, date last accessed).
https://cran.r-project.org/web/packages/...
). All different functions of NMDS are available within the “vegan” package (Oksanen et al. 2018OKSANEN J ET AL. 2018. ‘Vegan’: Community Ecology Package. R package version 2.4-6. https://cran.r-project.org/web/packages/vegan/vegan.pdf (June 16, 2020, date last accessed).
https://cran.r-project.org/web/packages/...
).

A two-way cluster analysis (also known as biclustering based on Jaccard dissimilarity) was used to assess similarities and differences in species composition between nest groups using PC-Ord 5.15 software (McCune & Mefford 2006MCCUNE B & MEFFORD MJ. 2006. PC-ORD: Multivariate analysis of ecological data. Version 514 for Windows [Users Guide] MjM software design.).

Beta diversity between nests

The beta diversity analysis (calculated based on the average species composition of each nest) proposed by Anderson (2006)ANDERSON MJ. 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1): 245-253. was used to evaluate the differences of taxonomic composition between nests based on Jaccard dissimilarities with incidence data using the “betadisper” function, and permutational analysis of multivariate dispersions (PERMDISP) of the vegan package (Oksanen et al. 2018OKSANEN J ET AL. 2018. ‘Vegan’: Community Ecology Package. R package version 2.4-6. https://cran.r-project.org/web/packages/vegan/vegan.pdf (June 16, 2020, date last accessed).
https://cran.r-project.org/web/packages/...
). In this analysis, greater dispersal of data points indicated greater species composition variability between groups using PERMANOVA (based on Monte-Carlo with 9999 permutations), which can then be considered a measure of beta diversity (Anderson 2006ANDERSON MJ. 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62(1): 245-253., Anderson & Walsh 2013ANDERSON M & WALSH D. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83(4): 557-574., Nunes et al. 2020NUNES J, VILLA P, NERI A, SILVA W & SCHAEFER C. 2020. Seasonality drives herbaceous community beta diversity in lithologically different rocky outcrops in Brazil. Plant Ecol Evol 153(2): 208-218. doi: 10.5091/plecevo.2020.1668.).

Linear mixed models

We used linear mixed-effects models (LMMs, with random and fixed effects) to test the main effects of nest area (explanatory variables) on community coverage, beta diversity, and species richness (response variables). Sample sites were considered random effects (1|plots) in all models. The most suitable residuals distribution and link function (i.e., normality was confirmed by the Q-Q graph and Shapiro–Wilk test) was evaluated (Zuur et al. 2009ZUUR A, IENO EN, WALKER N, SAVELIEV AA & SMITH GM. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, USA, 574 p., Crawley 2013CRAWLEY MJ. 2013. The R Book, second ed. Wiley, London, 1080 p.).

RESULTS

The disturbance area by southern giant petrels through trampling, feces deposition, and rock movements (the area directly affected) was found to be from 3.2 (nest 8) to 46.1 m2 (nest 11, which had another nest adjacent), accounting for 194.3 m2 of the area under the direct influence of the 16 nests (Figures 2 and 3, Table I). Considering the mean value found (13.9 m2/nest), it was estimated that the total nests (n = 320) accounted for 4.448 m2 of directly affected plateau, corresponding to 1.3 % of the total plateau area (346.5 m2 total area investigated) (Figure 3).

Figure 2
General view of the 13 nests studied: a = P1; b= P2; c= P3; d= P5; e= P6; f= P7; g= P8; h= P10; i= P11; j= P13; k= P14; l= P15; m= P16.
Figure 3
Map of all the southern giant petrel nests found in the Refuge Plateau of Stinker Point (white dots = petrel nests; black square = Brazilian Goeldi Refuge; squares with a number = altitude).

Five mosses, one fruticose lichen, one foliose lichen, one Antarctic grass (Deschampsia antarctica), one alga (Prasiola crispa) and various unidentified muscicolous lichens were found growing associated with the 16 studied southern giant petrel nests. The lichen species Sphaerophorus globosus (with a total occupied area of 31.8 m2, was found in six nests) and the moss Chorisodontium acyphyllum (19.5 m2, found in 8 nests) showed the highest coverage (Table II). The greatest number of species found in a single nest was five (nest 3), and the lowest was a single species (Prasiola crispa – nest 8).

Table II
Plant species cover (%), area of rocks covering the soil used in the nest building and surroundings (%) and total area (m2) around giant petrel nests in Stinker Point – Elephant Island.

Community coverage showed significant differences between nest types, where the inactive nest coverage was twice as high as that of active nests (Figure 4). The community species richness differed between the two nest types. However, the results showed an overlap in the confidence interval of the curves, indicating that the differences were not significant (Figure 5a). Conversely, when the community composition variability was analyzed, significant differences were observed between nest types (Permanova: F 1,11 = 5.25, p < 0.001), with marked variation in area and coverage (Figure 5b–c). This result was corroborated by comparing species distribution between nest types using a two-way cluster dendrogram, where a marked species-specific difference was observed (Figure 6).

Figure 4
Differences in community coverage between nests. The red dots indicate the average values and the shape of the violin indicates the distribution of data variability.
Figure 5
Sampled-based rarefaction (solid lines) and extrapolation curves (dashed lines) of species richness (a) between sampled nests. Rarefaction and extrapolation curves present the lines that represent the mean values and the bands the standard deviation with 95 % confidence intervals. Non metric multidimensional scaling (NMDS) based on species composition from different nests along a coverage gradient (b) and area of nests (c) in Maritime Antarctica.
Figure 6
Species distribution between nests using two-way cluster dendrogram based on the Jaccard dissimilarity metric.

The results on the beta diversity approach showed that the sample points in inactive nests clustered in the multidimensional space, with less distance from the centroid in comparison to active nests, which showed a scattered pattern (Figure 7a). Thus, changes in beta diversity between nest groups (Permanova: F1,11 = 4.04, p < 0.001; Figure 7b) were observed.

Figure 7
Principal coordinate analysis (PCoA) based on the Jaccard dissimilarity metric (a), and differences in beta diversity (b) between sampled nests.

The best linear mixed-effect models showed that variation in community coverage (Est. = 1.11, t = 5.11, p <0.001) was mainly explained by nest area, which had the strongest positive effect (Figure 8a) and negative effect (Est. = -0.10, t = 0.51, p <0.001) on beta diversity (Figure 8b). However, no significant effect (Est. = 0.03, t = 1.47, p = 0.17) was observed on species richness (Figure 8c).

Figure 8
Relationships between the nest area and coverage (a), beta diversity (b), species richness (c) and nest groups (inactive and active). Solid lines represent fitted (predicted) values of the models, and the shaded polygons represent the 95 % associated with the modeled predictions.

These results highlight the relevance of biotic factors (i.e., disturbance by breeding birds) in shaping the structure and composition of cryptogam communities in the Antarctic. Generally, in inactive nests Sphaerophorus globosus grows around southern giant petrel nests forming a ring up to 1 m in diameter. It grows in diameter depending on feces disposal, being more developed when oriented in the predominant wind direction. The Sphaerophorus ring is surrounded by the moss Chorisodontium acyphyllum, which is colonized by Sphaerophorus globosus, usually located in the North/Northwest quadrant, and by a ring of Sanionia uncinata colonized by the same lichen (but not as frequently). Finally, newer active nests are generally surrounded by Prasiola crispa and Sanionia uncinata carpets, which are already growing in the area. Chorisodontium acyphyllum is the last moss species that colonizes the surroundings of nests.

DISCUSSION

We found five mosses, one fruticose lichen (Sphaerophorus globosus), one foliose lichen (Mastodia tesselata), Deschampsia antarctica (Antarctic grass), Prasiola crispa (alga), and various unidentified muscicolous and saxicolous nitrophilous lichens associated with the 13 studied nests. The species are regularly arranged in a definite pattern of zonate circles or semi-circles, never before described around petrel nests in Antarctica. For southern giant petrel nests, likely due to the high nitrogen supply, these succession patterns were found in most nests evaluated. This pattern is not expected to occur in sub-Antarctica breeding sites, as plants are used for nest building in Southern South America and in the South Georgia Islands (Poncet et al. 2020PONCET S, WOLFAARDT AC, BARBRAUD C, REYESARRIAGADA R, BLACK A, POWELL RB & PHILLIPS RA. 2020. The distribution, abundance, status and global importance of southern giant petrels (Macronectes giganteus and M. halli) breeding at South Georgia. Polar Biol 43: 17-34. https://doi.org/10.1007/s00300-019-02608-y.
https://doi.org/10.1007/s00300-019-02608...
). Other Antarctic flying seabirds also do not display this nest construction method, instead of using available plant materials. The skuas (Catharacta spp.) and kelp gull (Larus dominicanus) use mosses and lichens (sometimes also angiosperms) for nest building, while shag (Phalacrocorax atriceps) uses algae and mud (Quintana & Travaini 2000QUINTANA RD & TRAVAINI A. 2000. Characteristics of nest sites of skuas and Kelp Gull in the Antarctic Peninsula. J Field Ornithol 71: 236-249.). Penguins use only rock fragments but gentoo penguins (Pygoscelis papua) are sometimes in slender colonies and close to vegetal formations (Quintana 2001QUINTANA RD. 2001. Nest-site characteristics of a Gentoo Penguin Pygoscelis papua colony at Cierva Point, Antarctic Peninsula. Mar Ornithol 29: 109-112.). The interference of those species on plant formation surrounding their nests still need to be evaluated.

Southern giant petrel nests in Antarctica are built using pebbles, with no collection of the surrounding vegetation, unlike other birds such as the skuas (Catharacta spp.) (Albuquerque et al. 2012ALBUQUERQUE MP, VICTORIA FC, SCHUNEMANN AL, PUTZKE J, GUNSKI RJ, SEIBERT S, PETRY MV & PEREIRA AB. 2012. Plant composition of skuas nests at Hennequin Point, King George Island, Antarctica. Am J Plant Sc 3: 688-692.). Therefore, the vegetation around the nesting area is relatively well preserved, despite the long period (approximately three months) of residence of breeding birds in the area (Cooper et al. 2001COOPER J, BROOKE MD, BURGER AE, CRAWFORD RJM, HUNTER S & WILLIAMS AJ. 2001. Aspects of the breeding biology of the northern giant petrel (Macronectes halli) and the southern giant petrel (M. giganteus) at sub-Antarctic Marion Island. Int J Ornith 4: 53-48.). Sometimes, the permanence of females is longer than that of males, despite the imminent failure in reproduction, females can stay on the nest up to one month after male abandonment (Schulz et al. 2014SCHULZ UH, KRÜGER L & PETRY MV. 2014. Southern giant petrel Macronectes giganteus Nest Attendance Patterns Under Extreme Weather Conditions. Zool Sci 31: 501-506.). However, non-breeding individuals and failed breeders also stay in the colony and even on nests during the breeding season. Therefore, the direct impact (when taking non breeders into account) is restricted to trampling during nest building (repair and maintenance), landing and departure, and feces deposition.

In this context, the results of this study corroborate that the nests use or maintenance during breeding bird’s dynamic can be considered a biotic filter that determines marked changes in community coverage, community composition, and species turnover. Specifically, a microhabitats differentiation induced by the nest’s construction (active nests) and abandonment (inactive) dynamics of southern giant petrel is evident, which probably determines the dynamics of colonization, growth and species turnover along succession. Despite not having evaluated the specific cryptogam communities along a succession dynamic, it is assumed that the reproductive behavior variations of southern giant petrel may induce differences on chemical and physical properties of substrates; consequently, it may generate an abiotic filtering and promotes high β-diversity and low species similarity between active and inactive nests. Previous studies showed that pedoenvironmental and soil fertility have significant effects on species composition and beta diversity of cryptogam communities in Antarctica (Schmitz et al. 2020a, 2020b, 2021). Based on gradient analysis, the pedoenvironmental filtering of cryptogam communities has been previously tested on Maritime Antarctica (Schmitz et al. 2020a, b, 2021). However, there are still gaps in knowledge about the effects of bird nest dynamics on cryptogam communities.

Surprisingly, the fruticose lichen Sphaerophorus globosus can survive in the first ring of plants surrounding southern giant petrel nests. Petrels can weigh up to 5.4 kg (Warham 1962WARHAM J. 1962. The biology of the southern giant petrel Macronectes giganteus. Auk 79(2): 139-170.). In Stinker Point, a sample of 23 birds had a mean weight of 4.3 kg (Krüger et al. 2018KRÜGER L, PAIVA VH, FINGER JV, PETERSEN E, XAVIER JC, PETRY MV & RAMOS JA. 2018. Intra-population variability of the non-breeding distribution of southern giant petrels Macronectes giganteus is mediated by individual body size. Antarct Sci 30(5): 271-277.) and movements of adults and chick could easily break this thallus. Lichens are frequently associated with Chorisodontium acyphyllum in Antarctica (Øvstedal & Lewis-Smith 2001ØVSTEDAL DO & LEWIS-SMITH RI. 2001. Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge: Cambridge University Press, 424 p.), including in regions near nests.

The results of beta diversity allow presuming that a deterministic pattern shape by habitat filtering (i.e., Schmitz et al. 2020a, 2021) is possible, which must be proven through the co-variation of nest categories (active and inactive) and nest distribution along environmental gradients. Moreover, the positive relationship of coverage and nests area, and the negative relationship of beta diversity and nests area, may indicate that recently active nests promote higher species richness, community composition variability and beta diversity due to the high resources availability (i.e., nutrients, space) for coexistence during initial successional stages. Conversely, during advanced successional stages on abandoned inactive nests there is lower species richness and turnover due to the high dominance of few species (i.e., higher coverage) and limited resources.

The cryptogam communities in the new area near Goeldi Refuge is mainly composed by the pioneer algal species Prasiola crispa. This macroscopic alga colonizes nests because it is an extremely nitrophilous taxon, found in nesting areas of birds in the north pole, being common in all habitats rich in organic nitrogen (Broady et al. 2012BROADY PA, FLINT EA, NELSON WA, CASSIE COOPER V, DE WINTON MD & NOVIS PM. 2012. Phyla Chlorophyta and Charophyta: green algae. In: Gordon DP (Ed), New Zealand inventory of biodiversity. Vol. 3. Kingdoms Bacteria, Protozoa, Chromista, Plantae, Fungi. Canterbury University Press, Christchurch, NZ, p. 347-381., Richter et al. 2014RICHTER D, PIETRYKA M & MATULA J. 2014. The diversity of cyanobacteria and green algae on ecological different types of vegetation in Horsund area (West Spitsbergen, Svalbard). In: Migała K, Owczarek P, Kasprzak M & Strzelecki M (Eds), New perspectives in polar research. University of Wrocław 1: 137-162., 2015RICHTER D, PIETRYKA M & MATULA J. 2015. Relationship of cyanobacteral and algal assemblages with vegetation in the high Arctic tundra (West Spitsbergen, Svalbard Archipelago). Pol Polar Res 36: 239-260.). Unfavorable habitat conditions caused by constant treading by birds change the algal mat to a monostromatic lamellar, cracked form, which was also observed in our study (Pietryka et al. 2016PIETRYKA M, RICHTER D & MATULA J. 2016. Cyanobacterial and algal diversity in the vicinity of two different seabird colonies in Spitsbergen. Pol Polar Res 37(2): 269-288.). In our study 38,5% of the nests a ring of this alga is found in the first ring together with the rock fragments of the nest (including inactive nests), where feces deposition is higher.

The Antarctic moss turf generally contains the characteristic species Chorisodontium aciphyllum, Polytrichastrum alpinum, Polytrichum piliferum Hedw. and Polytrichum juniperinum Hedw. (Ochyra et al. 2008OCHYRA R, LEWIS-SMITH RI & BEDNAREK-OCHYRA H. 2008. The Illustrated Moss Flora of Antarctica. Cambridge: Cambridge University Press, 709 p.). C. aciphyllum grows directly on rock fragments; however, as the soil is formed, it is replaced by Sanionia uncinata, which is clearly seen on Stinker Point, Elephant Island. This was also the case around the nests, where species occurred according to the presence of soil.

Compared with the plant composition found around the skuas nests (Albuquerque et al. 2012ALBUQUERQUE MP, VICTORIA FC, SCHUNEMANN AL, PUTZKE J, GUNSKI RJ, SEIBERT S, PETRY MV & PEREIRA AB. 2012. Plant composition of skuas nests at Hennequin Point, King George Island, Antarctica. Am J Plant Sc 3: 688-692.), the diversity rates in southern giant petrel nests are slightly lower (4.2 species/nest for skuas and 3.71 for petrels). The main mosses found in skua nests typically occur in plant communities from Antarctic ice-free areas at higher frequencies (Victoria et al. 2009VICTORIA FC, PEREIRA AB & COSTA DP. 2009. Composition and distribution of moss formation in the ice-free areas adjoining the Arctowski Region, Admiralty Bay, King George Island, Antarctica. Iheringia 64(1): 81-91.), such as Sanionia uncinata, which are often observed in association with muscicolous lichen species Cladonia borealis S. Stenroos, Usnea antarctica Du Rietz, and Leptogium sp. This moss species is considered the most abundant associated lichen, occurring together with other fruticose lichen species (Victoria et al. 2006VICTORIA FC, ALBUQUERQUE MP & PEREIRA AB. 2006. Lichen-Moss Associations in Plant Communities of the Southwest Admiralty Bay, King George Island, Antarctica. Neot Biol Cons 1: 84-89.). For southern giant petrel nests, all species found, mainly in the inactive nests, are common in sites with the highest nitrogen content, such as penguin rookeries (Putzke & Pereira 1990PUTZKE J & PEREIRA AB. 1990. Mosses of King George Island, Antarctica. Pes Ant Bras 2: 17-71.).

CONCLUSIONS

The results demonstrate that southern giant petrel (Macronectes giganteus) nest (inactive and active) determine differences in diversity, composition and structure (i.e., community coverage) of cryptogam communities on Stinker Point, Elephant Island, Maritime Antarctica. The concentric rings generated by species composition are exclusive in the nest directly influenced area and may contribute to general vegetation coverage.

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Publication Dates

  • Publication in this collection
    18 Feb 2022
  • Date of issue
    2022

History

  • Received
    18 Apr 2021
  • Accepted
    04 Oct 2021
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