Università degli studi di Cagliari

CORSO DI DOTTORATO IN SCIENZE E TECNOLOGIE DELLA TERRA E DELL'AMBIENTE

INDIRIZZO BOTANICA AMBIENTALE E APPLICATA

Ciclo XXX

TITOLO

DISTRIBUTION, ECOLOGY AND CONSERVATION OF BRYOFLORA IN THE MEDITERRANEAN TEMPORARY PONDS

DOTTORANDO: Dott.ssa Giorgia Filippino COORDINATORE DOTTORATO: Prof. Pierfranco Lattanzi TUTOR/RELATORE: Dott.ssa Michela Marignani Prof.ssa Annalena Cogoni

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Index

1. Introduction and objectives 3

2. Materials and methods 4

2.1 Compile the first bryoflora of Mediterranean temporary ponds 4

2.2 Determine the impacts of the main environmental factors on bryophyte

composition in Mediterranean temporary ponds. 4

2.3 Study the spatial distribution of bryophytes within the temporary ponds 5

3. Results of the first year 6

4. Planning for the next years 13

5. References 14

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1. Introduction and objectives

In the Mediterranean region temporary ponds are classified among the most biologically and

biogeographically interesting ecosystems. The elevated biodiversity found in temporary ponds has

been attributed to their high spatio-temporal variability (Florencio et al. 2009; Bagella et al. 2010).

Moreover, even if they cover little areas, these habitats are home of a rich biodiversity caused by a

typical small-scale zonation (Bagella et al. 2009b; Caria et al. 2013). In each pond, three belts can

usually be identified: an internal belt (I) in the toe slope, a central belt (C) in the foot/back slope and

an outer belt (O) in the upper slope position (Casas et al. 1998; Rhazi et al. 2001).

The damp habitats with a seasonal presence of surface water are potential bryophyte habitats. This

is especially true in the Mediterranean areas where water availability is a key factor for those plant

groups, requiring it for the completion of their life cycle at the reproductive stage. Despite their

important ecological functions in those fragile environments, bryophytes are neglected or

undervalued in most monitoring and conservation actions.

The objectives of the research project to conduct during the PhD program will follow a multiscale

approach:

MACROSCALE - The Mediterranean basin context

i) compile the first bryoflora of Mediterranean temporary ponds define a list of bryophyte

species typical of the habitat “3170* Mediterranean temporary pond” to be used as a

reference list to complete the habitat description

ii) REGIONAL SCALE – The island contextdetermine the impacts of the main environmental

factors on bryophyte richness and composition in Mediterranean temporary ponds

LOCAL SCALE – Spatial distribution and spore bank

iii) study the spatial distribution of bryophytes within the temporary ponds.

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iv) analyse bryophyte’s spores in Mediterranean temporary ponds to identify what are the

species that show a better fitness for survival and adaptation to these environments.

The activities carried out during the first year of doctorate include i) compile the first bryoflora of

Mediterranean temporary ponds, ii) determine the impacts of the main environmental factors on

bryophyte composition in Mediterranean temporary ponds ii) study the spatial distribution of

bryophytes within the temporary ponds.

2. Materials and methods

2.1 Compile the first bryoflora of Mediterranean temporary ponds

To compile the first bryoflora of Mediterranean temporary ponds, we compared the bryoflora

composition of temporary ponds in Sardinia (Italy) with the available bibliographical data on

temporary ponds in the Mediterranean (Spain, France and main Mediterranean islands such as

Balearic Islands, Corsica, Sicily) (Casas et al. 1998; Hugonnot 2002; Cogoni et al. 2009; Pericàs et

al. 2010). We created a georeferenced database of 212 bryophyte species, which included 166

Bryophyta, 44 Marchantiophyta and 2 Antocerothophyta.

2.2 Determine the impacts of the main environmental factors on bryophyte composition in

Mediterranean temporary ponds.

To determine the impacts of the main environmental factors on bryophyte composition in

Mediterranean temporary ponds and study the small-scale spatial zonation distribution of

bryophytes within the ponds we selected the island of Sardinia (Italy), the second largest island in

the Mediterranean basin. To obtain an even distribution of representative sites on the island, we

selected nine sites from the existing literature (Cogoni et al. 2006, Desfayes 2008; Bagella et al.

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2009a, 2009b, 2009c, 2013), choosing ponds meeting the Habitats Directive’s criteria for

“Mediterranean temporary ponds, 3170*" (Williams 1987; 2006; Keeley and Zedler 1998;

Yaverkovsky et al. 2004). In the selected sites, a total of 33 temporary ponds of natural origin

covering a range of altitudes and substrates were surveyed (Zoccheddu, unpublished data). For the

bryophytes sampling we utilized the method adopted for the vascular flora surveys of the

Mediterranean temporary ponds (Bagella et al., 2009b).

To describe the bryoflora of Mediterranean temporary ponds in Sardinia we analyzed the flora in

terms of species richness and composition, chorological and ecological elements. To test if there are

differences among sites and ponds, in terms of species composition, we performed a

PERMANOVA (non-parametric multivariate analysis of variance, Anderson 2001), using a nested

design (factors: Belts (Pond(Sites), 999 permutation, Unrestricted permutation of raw data, Jaccard

resemblance). To understand if environmental variables have an influence on the composition of

bryophytes in temporary ponds in Sardinia and quantify the proportion of variance that can be

explained by these variables, we performed a distance-based redundancy analysis (dbRDA), using

Jaccard similarity, using a set of environmental predictors.

2.3 Study the spatial distribution of bryophytes within the temporary ponds

To study the spatial distribution of bryophytes within the temporary ponds, we followed the

zonation scheme proposed for Moroccan ponds and for les basses de l’Albera (Casas et al. 1998;

Rhazi et al. 2006) which is based on water depth at the beginning of the season, morphology of the

pond and type of vegetation present. Accordingly, three belts were recognized in the temporary

ponds: a central belt (C), an intermediate belt (I), and an outer belt (O). To test if bryophytes

respond to the water table fluctuation, showing a typical small-scale spatial zonation and understand

if there are species or life form/strategies typical of those belts, we performed a Principal

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Coordinates Analysis (PCoA) on the composition of the three belts in the different sites using

species, chorotypes, life form, life strategy and the ecological character “humidity”

The contribution of a particular species as indicator of a specific belt wasassessed by performing an

indicator species analysis (Dufrêne and Legendre 1997).

Analysis were performed using the R package indicspecies version 1.7.4 (De Cáceres and Legendre

2009; De Cáceres et al. 2010, 2013).

3. Results of the first year

First results were reported in the attached paper, currently under review, and presented at

international congresses.

Paper under review

1) Annalena Cogoni, Giorgia Filippino*, Michela Marignani. Small-scale pattern of bryoflora in

Mediterranean temporary ponds – hints for monitoring. Under review. (for a complete

paper see Annex I). *corresponding author

Abstract

In the Mediterranean region temporary ponds are classified among the most biologically and

biogeographically interesting ecosystems. Despite their important ecological functions in those

fragile environments, bryophytes are neglected or undervalued in most monitoring and conservation

actions. We studied the composition and the small-scale spatial zonation of bryophytes within

Mediterranean temporary ponds, to identify indicator species useful to characterize the spatio-

temporal variability observed, and suggest elements to carry out simple monitoring based on

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dominant life form and strategy. Bryophytes are distributed in concentric belts (outer, central, inner)

according to their tolerance to floods: we observed a gradient from the outer belt, mainly composed

by colonist and perennial such as Pottiaceae and Brachytheciaceae, to the more humid inner one

where annual shuttle such as Ricciaceae dominate. We found significant species associated with

belts, such as Tortella squarrosa in the outer belt, Fossombronia caespitiformis in the central belt

and Riccia canaliculata in the inner belt. Bryophytes can be used as bioindicators of the state of

conservation of Mediterranean temporary ponds: the presence of indicator species and the

distribution of dominant life form/strategies in the different belts allow to monitor over time the

changes in the flood level.

Oral presentations at international conferences

1) Bagella Simonetta, Boix Dani, Caria Maria Carmela, Compte Jordi, Gascón Stéphanie,

Filippino Giorgia, Pisanu Stefania, Pittao Elena, Sala Jordi, Cogoni Annalena. “Paulis”

Project: A Challenge from a neglected habitat. International Symposium of Mediterranean

Temporary Ponds, Sassari, April 15-16-17, 2015.

Abstract

The widespread of the toponym “Paule” and of other vernacular names such as “Piskina”, “Padule”,

“Lakku” used in the Sardinian languages for designing temporary wetlands suggest a high number

and a strong perception at local scale of these habitats in the past. In spite of this, the lack of

information on their ecology, biodiversity, temporal dynamics and spatial distribution at regional

scale, has made it difficult an adequate consideration in conservation programs. The opportunity of

Nature 2000 network was notbeen adequately exploited because the habitats 3110, 3120 and 3170*,

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to which Mediterranean Temporary Wetland could be referred, were rarely recognized inside SIC

and protected areas, or left outside their boundaries. Moreover the available scientific literature was

little and difficult to access.

“Paulis” project, funded in 2012 by the Region of Sardinia - Regional Law 7 August 2007, n. 7:

'Promotion of scientific research and technological innovation in Sardinia', was aimed to capturing

the interest on these neglected habitats through the implementation of scientific and educational

products.

The researches carried out by the team of the project have provided the following deliverables:

scientific papers on: taxonomic and functional diversity of vascular plants, bryophytes and

macroinvertebrates living in Sardinian Mediterranean Temporary Ponds; spatial and temporal

variability of the habitat and the biotic communities; main drivers of biodiversity; seed and spore

soil bank as reserve of biodiversity;

map of habitat distribution at regional scale;

data-base of vascular plants, bryophytes and macroinvertebrates;

interactive guide to the flora http://dryades.units.it/stagnisardi_en/;

assessment of several species according to IUCN categories and criteria;

priority lists for the conservation of sites and species.

The dissemination of the information and an increased awareness of public, environmental

managers and policemen is being promoted through the presentation of communications and posters

in congress and seminars, the participation to public events, the engagement of students, the

creation of a website http://paulisproject.jimdo.com/english/ and a facebook community

https://www.facebook.com/paulisproject?ref=hl, the organization of a photo contest and of the

present International Symposium on Mediterranean Temporary Ponds.

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Will these actions effective for containing the threats on this habitat in Sardinia

2) Cogoni Annalena, Filippino Giorgia, Zoccheddu Monica, Marignani Michela. Bryoflora of

temporary ponds in the mediterranean basin – hints for management and conservation.

International Symposium of Mediterranean Temporary Ponds, Sassari, April 15-16-17, 2015.

Abstract

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In the Mediterranean region temporary ponds are classified among the most biologically and

biogeographically interesting ecosystems. Despite the important ecological functions of bryophytes

in those fragile environments, they are neglected or undervalued in most management actions. We

surveyed the bryoflora composition and distribution within 33 Mediterranean temporary ponds in

Sardinia (Italy). The bryoflora is composed by 139 taxa, (119 Bryophyta, 19 Marchantiophyta and 1

Antocerothophyta), accounting for 28% of the total Island bryoflora. Among those, Petalophyllum

ralfsii, Cephaloziella calyculata and Fossombronia pusilla are critically endangered and Riccia

huebeneriana and Hypnum revolutum var. revolutum, are reported for the first time in Sardinia.

Three belts were recognized in temporary ponds: a central belt, an intermediate belt, and an outer

belt. Species showed a spatial pattern within the temporary ponds, from species Pottiaceae and

Brachytheciaceae, with the life strategy colonist and perennial, to species Ricciaceae with life

strategy annual shuttle. Species as Scleropodium touretti and Tortella squarrosa are significantly

associated with the outer belt, however the Riccia canaliculata is significantly associated with the

central belt, because it occurs in these belt only. Those information are useful to build up a

scientifically sound knowledge useful for future effective conservation actions. Posters

presentations at international conferences

Filippino Giorgia, Marignani Michela, Dia Maria Giovanna, Campisi Patrizia, Cogoni

Annalena. Biogeographic distribution of bryoflora in the mediterranean temporary ponds.

International Symposium of Mediterranean Temporary Ponds, Sassari, April 15-16-17, 2015.

Abstract

In Europe, Mediterranean temporary ponds are indicated as priority natural habitats under the

Habitats Directive 92/43/EEC: despite in those habitats bryophytes are recognized to have an

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important ecological function, there are very few studies on the chorological and ecological

characteristics driving bryophytes diversity and on the biogeographical factors influencing species'

variability. We compared the bryoflora composition of temporary ponds in Sardinia (Italy) with the

available bibliographical data on temporary ponds in the Mediterranean (Spain, France and main

Mediterranean islands such as Balearic Islands, Corsica, Sicily) to define their characteristic

floristic composition. A total of 212 bryophyte species, which included 166 Bryophyta, 44

Marchantiophyta and 2 Antocerothophyta are reported. Among these species, those most typically

connected with such habitats are: Archidium alternifolium, Bryum dichotomum, Imbrybryum

alpinum, Fossombronia caespitiformis, Ptychostomum capillare, Ptychostomum pseudotriquetrum,

Riccia beyrichiana, Tortella squarrosa and Trichostomum brachydontium. In particular, Archidium

alterifolium and Bryum dichotomum are the most common species found in Mediterranean

temporary ponds, being surveyed in more that 83% of the investigated ponds. The strictly

hydrophytic taxa are: Drepanocladus aduncus, Leptodictyum riparium, Riccia fluitans and Riella

helicophylla. The genus Riccia is common in these habitat. In a distinctly Mediterranean climatic

context the presence of a large number of Pottiaceae is predictable: they are characterized by

species with a short lifecycle, making them more competitive in areas with a Mediterranean climate.

Several species of conservation concern are present (7 species) highlighting the conservation

importance of this habitat, e.g. Petalophyllum ralfsii in Sardinia. Due to the fragility of the habitat

and its unique ecology, P. ralfsii is potentially threatened by a number of factors including pressure

from tourism, removal, or drying of the thallus due to the reduction of water level or reforestation.

Michela Marignani, Giorgia Filippino, Annalena Cogoni. Seasonal trends and spatial

pattern of bryophytes in mediterranean temporary ponds. European conference, Ecology at

the interface, Rome, 21_25 September.

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Abstract

Despite the important ecological functions of bryophytes in the Mediterranean temporary ponds,

they often are neglected or undervalued. Mediterranean temporary ponds present a small-scale

zonation arranged in inner, central, and outer belt. Bryophytes are distributed in the belts according

to their tolerance floods: we observed a gradient from the outer belt (O), mainly composed by

colonist and perennial such as Pottiaceae and Brachytheciaceae, to the inner one (I) with annual

shuttle such as Ricciaceae. We found significant species associated with belts, such as Tortella

squarrosa in the outer belt, Fossombronia caespitiformis in the central belt and Riccia canaliculata

in the inner belt. The distribution analysis of bryophytes in the belts within the ponds allows us to

suggest the bryophytes as useful bioindicators of the state of conservation of Mediterranean

temporary ponds, since the presence of indicator species in the different belts enables us to monitor

over time the changes in the flood level. Those information are useful to build up a scientifically

sound knowledge useful for future effective conservation actions. Results contribute to the use of

bryophytes as bioindicators in Mediterranean temporary wetland ecosystem and provide a helpful

benchmark to plan effective conservation actions in those fragile environments.

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Other activities

A summary of the activities undertaken during the first year of doctorate is here reported:

Doctoral course: "Introduzione alla statistica" (Prof.ssa Monica Musio).

Tutoring thesis students: “Distribuzione ed ecologia delle briofite nelle zone costiere” Anno

Accademico 2015-2016.

Organizing committee: International Symposium of Mediterranean Temporary Ponds, Sassari,

April 15-16-17, 2015.

Conferences attended: project presentation ENPI ECOPLANTMED and project presentation

ENPI GREATMED, Edificio Sali scelti (Italy) 17-11-2015.

Tutoring course: Botanica generale e sistematica - 1° semestre – Corso di Laurea in Biologia e

Farmacia.

Tutoring stage student: “Analisi di Habitat e specie vegetali ai sensi della Direttiva Habitat

92/43”. Corso di laurea triennale in Scienze Naturali. Anno Accademico 2015-2016.

Research collaboration with the “Saras Ricerche e Tecnologie” Macchiareddu (Assemini)

Cagliari. 23/07-23/10/2015.

4. Planning for the next years

For the next years we will follow the analyses of bryophytes spores in Mediterranean temporary

ponds, to identify what are the species that show a better fitness for survival and adaptation to these

environments. In october 2015, we proceeded with a random sampling in two temporary ponds in

Sardinia and we are optimizing the germination method.

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5. References

Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral 401

Ecology, 26: 32–46.

Bagella S, Caria MC, Farris E, Filigheddu R (2009a) Phytosociological analysis in Sardinian Mediterranean

temporary wet habitats. Fitosociologia 46:11-26.

Bagella S, Caria MC, Farris E, Filigheddu R (2009b). Spatial-time variability and conservation relevance of

plant communities in Mediterranean temporary wet habitats: A case study in Sardinia (Italy). Plant Biosyst

143(3):435-442.

Bagella S, Caria MC, Zuccarello V (2009c). Small scale plant distribution in Mediterranean temporary

ponds: implications for conservation, International Conference on Mediterranean Temporary Ponds.

Proceedings & Abstracts. Consell Insular de Menorca. Recerca, 14, Minorca, Spagna, pp. 121-127.

Bagella S, Gascón S, Caria MC, Sala J, Mariani MA, Boix D (2010) Identifying key environmental factors

related to plant and crustacean assemblages in Mediterranean temporary ponds. Biodivers. Conserv.

19:1749–1768.

Bagella S, Caria MC (2013) Sensitivity of ephemeral wetland swards with Isoetes histrix Bory to

environmental variables: implications for the conservation of Mediterranean temporary ponds. Aquat

Conserv Mar Freshw Ecosys 23(2):277-290.

Caria MC, Capra GF, Buondonno A, Seddaiu G, Vacca S, Bagella S (2013) Small-scale patterns of plant

functional types and soil features within Mediterranean temporary ponds. Plant Biosyst 149(2):1–11.

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Casas C, Cros RM, Brugués M, Sérgio C, Font J (1998) Els briòfits de les basses de l’Albera, Alt Empordà.

Gea, Flora et Fauna 66:73-80.

Cogoni A, Flore F, Adamo C, Lai R, Scrugli A (2006) Ecology of bryophytes of damp areas at Giara di

Gesturi (Southern Central Sardinia). Bocconea 19:65-76.

Cogoni A, Scrugli A, Cortis P (2009) Bryophyte flora of some temporary pools in Sardinia and Corsica.

Plant Biosyst 143(3):97-103.

De Cáceres M (2013) How to use the indicspecies package (ver. 1.7.1). http://cran.r-

project.org/web/packages/indicspecies. Accessed 26 March 2015.

De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical

inference. Ecology 90(12):3566–3574.

De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of

sites. Oikos 119(10):1674–1684.

Desfayes M (2008) Flore vasculaire herbacée des eaux douces et des milieux humides de la Sardaigne. Fl

Medit 18:247-331.

Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a exible

asymmetrical approach. Ecol Monographs 67(3):345-366.

Hugonnot V (2002) Réserve Naturelle de Roque-Haute (Hérault, France). Flore et végétation bryologiques-

Bilan actuel et analyse bibliographique. Association Loisirs Botaniques, Réserve Naturelle de Roque-Haute.

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Keeley JE, Zedler PH (1998) Characterization and Global Distribution of Vernal Pools. In: Witham CW,

Bauder ET, Belk D, Ferren Jr WR, Ornduff R (ed) Ecology, Conservation, and Management of vernal Pool

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Pericàs J, Fraga P, Mascaró J, Rosselló JA (2010) Les Briòfites a les basses temporals de Menorca. In Fraga

P, Estaún I, Cardona E (ed). Basses temporals mediterrànies. Life Basses: gestió i conservació a Menorca.

Consell Insular de Menorca, Institut Menorquí d’Estudis, pp 169-196.

Rhazi L, Grillas P, Mounirou Touré A, Tan Ham L (2001) Impact of land use and activities on water,

sediment and vegetation of temporary pools in Morocco. Life Sci 324:165–177.

Rhazi L, Rhazi M, Grillas P, Tan Ham L, El Khyari D (2006) Richness and structure of plant communities

in temporary pools from western Morocco: influence of human activities, Hydrobiologia 570:197–203.

Yaverkovski N, Grillas P, Paradis G, Thiéry A, (2004) Biodiversity and conservation issues. Habitats. In:

Grillas P, Gauthier P, Yavercovski N, Perennou C (ed) Mediterranean Temporary Pools 1. Station biologique

de la Tour du Valat, Arles, pp. 13-19.

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