Algae

I TA L I A N H A B I TAT S Pools, ponds and marshes 11 Italian habitats Italian Ministry of the Environment and Territory Protection / Ministero dell’Ambiente e della Tutela del Territorio Friuli Museum of Natural History / Museo Friulano di Storia Naturale · Comune di Udine I TA L I A N H A B I TAT S Scientific coordinators Alessandro Minelli · Sandro Ruffo · Fabio Stoch Editorial committee Aldo Cosentino · Alessandro La Posta · Carlo Morandini · Giuseppe Muscio “Pools, ponds and marshes · Small water bodies, oases of biodiversity” edited by Fabio Stoch Texts Marco Cantonati · Luca Lapini · Giuseppe Oriolo · Sergio Paradisi · Margherita Solari · Fabio Stoch · Michela Tomasella English translation Elena Calandruccio · Alison Garside · Gabriel Walton Illustrations Roberto Zanella except 98 (Andrea Toselli) Graphic design Furio Colman Pools, ponds and marshes Small water bodies, oases of biodiversity Photographs Nevio Agostini 104, 106, 135 · Archive Museo Friulano di Storia Naturale 52, 58, 61, 96, 107/1, 108, 130, 131, 138, 140 · Archive Museo Friulano di Storia Naturale (Tomasi) 51, 53, 57 · Marco Cantonati 34, 35, 36 · Vitantonio Dell’Orto 6, 8, 40, 55, 56, 102, 111, 112, 116, 117, 123, 125, 128, 129, 136 · Cristiano Francescato 45, 46, 47, 50 · Luca Lapini 109, 121, 143 · Francesco Lillo 26, 68 · Federico Marrone 141 · Ugo Mellone 10, 12, 103, 124, 149 · Michele Mendi 113, 114, 115, 118, 119 · Eugenio Miotti 94, 97, 99, 100, 101 · Giuseppe Muscio 24, 134, 148 · Paolo Paolucci 120, 122 · Ivo Pecile 75 · Leonardo Pupi 29 · Mario Saccomano 62, 105, 107/2, 137 · Alfio Scarpa 133 · Margherita Solari 144 · Fabio Stoch 11, 15, 16, 17, 20, 21, 22, 23, 25, 27, 48, 63, 69, 70, 85, 87, 91, 126, 141, 147 · Damiano Vagaggini 59, 60, 64, 66, 67, 72, 74, 76, 77, 78, 79, 80, 81, 84, 93 · Augusto Vigna Taglianti 88 · Roberto Zucchini 9, 14, 28, 30, 32, 38, 44, 49, 73, 82, 83, 86, 110, 127, 142, 145, 146 © 2005 Museo Friulano di Storia Naturale, Udine, Italy All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, without the prior permission in writing of the publishers. ISBN 88 88192 22 0 ISSN 1724-6539 Cover photo: Pond in the Po Delta (Emilia-Romagna, photo V. Dell’Orto) M I N I S T E R O D E L L’ A M B I E N T E E D E L L A T U T E L A D E L T E R R I T O R I O M U S E O F R I U L A N O D I S T O R I A N AT U R A L E · C O M U N E D I U D I N E Italian habitats Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Fabio Stoch Small water bodies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 Fabio Stoch 1 Caves and karstic phenomena 2 Springs and spring watercourses 3 Woodlands of the Po Plain 4 Sand dunes and beaches 5 Mountain streams Algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29 Marco Cantonati Flora and vegetation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 Giuseppe Oriolo · Michela Tomasella Invertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 Fabio Stoch Fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95 Sergio Paradisi 6 The Mediterranean maquis 7 Sea cliffs and rocky coastlines 8 Brackish coastal lakes 9 Mountain peat-bogs 10 Realms of snow and ice Amphibians and reptiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103 Luca Lapini Birds and mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 Luca Lapini · Sergio Paradisi Conservation and management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 Luca Lapini · Giuseppe Oriolo · Sergio Paradisi · Fabio Stoch · Michela Tomasella Suggestions for teaching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143 Margherita Solari Select bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151 11 Pools, ponds and marshes 12 Arid meadows 13 Rocky slopes and screes 14 High-altitude lakes 15 Beech forests of the Apennines Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153 List of species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 Algae M ARCO CANTONATI ■ Algae and small water bodies In the previous chapters, we have shown that the words small water bodies actually include a great variety of environments. They are often small, shallow, and ephemeral. In the plains, where they are usually found, organic matter and nutrients accumulate and these very shallow water bodies can therefore be very rich in nutrient mineral salts that favour the natural development of algae. The following description of algae found in small bodies of water reviews the few studies devoted to different types of environments. We shall see how algal Alpine watering-hole reddened by algae populations differ and follow their biological cycle in the several types of ponds, pools and other artificial standing waters. ■ Pond algae Unlike lakes, the main characteristic identifying ponds, caused by their shallowness, is the prevailing importance of littoral environments. Colonisation by higher plants or macrophytes is potentially possible throughout the pond. One of the most important ecological characteristics of ponds is the subtle competitive balance between algae and aquatic plants. More precisely, on one hand there are microscopic algae living in open water (phytoplankton) and, on the other, macrophytes. Besides these two direct contenders, this competition has other leading actors: microscopic algae developing on macrophytes (epiphytes), planktonic crustaceans that control the development of Diatoms of the genus Fragilaria 29 30 phytoplankton by filtering it while feeding, planktivorous fish which prey on crustaceans at sight, and fish-eating fish that feed on the planktivorous species. All conditions contributing towards keeping the water clear, favour good penetration of light which, in turn, facilitates the colonisation and growth of several submerged aquatic plants on which rich periphyton develops. These primary producers use up most of the nutritive minerals available, to the detriment of phytoplankton, which can only develop to a limited extent. By contrast, conditions favouring water turbidity challenge macrophytes and can shift the competitive balance in favour of phytoplankton: ponds will therefore lack submerged aquatic plants and the water will be greenish and turbid. Algae in fish-farming ponds. Man sometimes eliminates macrophytes intentionally. This is what happens in fish-farming ponds, where macrophytes are either cut or removed by herbicides. Phytoplankton can therefore develop freely, as it has no competitors among primary producers, and nutrients are available in great quantities due to the fact large numbers of fish are fed on special food supplied from outside the pond. This in turn leads to reduced numbers of macrofilterers, which are eliminated by planktivorous fish. These conditions favour the development of blue-green algae (cyanobacteria), which may be numerous enough to give rise to large, gaudy water blooms (flos aquae, Desmid of the genus Cosmarium water flower). The most typical cyanobacteria causing these blooms are Microcystis aeruginosa, Aphanizomenon flos-aquae, Anabaena spp . and Planktothrix (Oscillatoria) rubescens. Algae in watering holes. Another very particular type of pond is interesting (and unfortunately at risk of extinction): watering holes. The rich algal populations in these environments are mainly composed of green algae. The most peculiar are filamentous green algae of the order Zygnematales - the genera Spirogyra, called water-silk, with spiralling chloroplasts, and genus Zygnema, with starshaped chloroplasts - and oedogoniales (genus Oedogonium, the cells of which have a series of peculiar caps (rings at the end of older cells), due to the particular cellular division and growth of the two-layered cell wall, the number of which corresponds to the number of cellular divisions). These algae form dense populations on the bottom, from which entangled mats may become detached and float to the surface, covering most of it. Spirogyra is the most common genus and forms dense floating mats at various levels, Zygnema generally forms floating mats, and Oedogonium is often epiphytic and gives rise to dense, filamentous covers along the stems of higher plants. In watering holes, the filamentous, unbranched yellow alga xanthophyte, Tribonema forms floating mats at various levels. A typical feature of this alga is its cell wall, made up of two overlapping parts, so that its filaments are composed of H-shaped cell wall pieces. In these ponds, plankton often contains green coccal algae, some of which may form flos aquae, like that formed by cyanobacteria. There are also genera like Microcystis, Chroococcus and Nostoc , which form round, brown, jellified floating colonies near plant stems, diatoms (bacillariophytes), euglenoids and desmid green algae, and sometimes volvocales (genera Pandorina and Volvox). Algae in ox-bow ponds. A special group of ponds (old river channels) gives rise to a particular environment and reveals great algal biodiversity. Recent, exhaustive research on algae of ox-bow, ponds and pools of the river Oder (Germany) shows that flooding is a rejuvenating or vivifying moment for these environments. The turbulence of the river water allows cells, usuallly incapable of autonomous movement, like those of centric diatoms (with radial symmetry and therefore round), to float. During flooding, the phytoplankton in these ponds is similar to that of rivers and is composed of centric diatoms and green chlorococcal algae. The slowing down of the current as the river recedes causes centric diatoms, especially large ones, gradually and inexorably to settle, as the plankton becomes richer in motile algae - those with flagella, 31 32 which beat the water and allow the organisms to move independently of water movement. The water in ponds isolated from the river can frequently be overturned by wind, alternating short periods of stagnation (when phytoplankton mostly contains cryptophytes), with long intervals (sometimes lasting six weeks or more), when the phytoplankton contains dinoflagellate algae which develop from cysts (resting stages of these algae). These are then followed by cyanobacteria, including species with special cells called heterocysts, which fix atmospheric molecular nitrogen and make these algae especially competitive when water in the pond lacks inorganic nitrogen (this occurs when the nitrogen has been consumed for the development of other algal groups, like chlorophytes). The next flood brings forth a new cycle. In Italy, research on an ox-bow close to the town of Pavia, which is only seldom and marginally flooded by the river Ticino, has revealed the complexity of the types and genera of algae as the months pass. Diatoms (Fragilaria spp ., Melosira varians, Asterionella formosa) form a dominant group in late winter and early spring, as their growth is favoured by low temperatures, overturn of water by the wind, and larger quantities of silica (which makes up their frustules). In late spring and early summer, the dominating algae are dinoflagellates (Ceratium hirundinella) followed, in summer, by green algae (Pediastrum spp.) and, in late summer-early autumn, by cyanobacteria (Microcystis aeruginosa). Desmid of the genus Closterium ■ Algae in pools Algae in pools include species coming from the soil (e.g., diatoms of the genus Hantzschia and several Chlorophyceae), and species suviving as cysts (resting stage) inside sediments accumulating on the bottom (golden algae or chrysophytes, for istance, which easily form cysts and may colonise clearwater pools. Other algae must produce devices that enable them to be carried by the wind to these small pools. A special adaptation to long periods of drought is the typical capacity of several algae in ephemeral water to produce zygotes with thick, robust, cell walls. Well-known are the so-called zygospores of several green algae (Zygnematales, Oedogonium, etc.). Algae in temporary mountain pools. Phytoplankton in temporary mountain pools that are only occasionally visited by cattle, and therefore have only limited nutrient supply, is mainly composed of chlorophytes. As regards density, the largest amount is represented by tiny flagellate (ultra- and nanoplankton). After the thaw, dinoflagellates prevail, followed by blue-green algae and, in terms of algae biovolume, diatoms (mostly acidophilous taxa of the genera Eunotia and Pinnularia, according to the lithology of the substrate, composed of quartzose feldspathic sandstone in the Tuscan Massif). Later, the most important algae are dinoflagellates (Peridinium umbonatum ) and green algae (the volvocales Hafniomonas montana). Other important algae are desmids (Cosmarium, Staurastrum ), filamentous green algae (Ulothrix, belonging to the Ulotrichales and Zygnametales Mougeotia and Zygnema), and sometimes cyanobacteria (Pseudoanabaena, Planktothrix) and chrysophytes (Mallomonas). After summer drought, phytoplankton generally contains green algae. Algae in Alpine watering holes. Again in mountain environments, Alpine watering-holes are special because they are temporary and small, but at the same time rich in algal nutrients. The Italian limnologist Edgardo Baldi carried out research in the western and eastern Alps, highlighting their peculiarities - the unusual combination of environmental features common to plains water bodies (richness and variety of life due to organic matter supply from grazing livestock) and mountain ones (low temperatures and long periods of freeze, quality of supply water, unique populating possibilities provided by the Alpine environment). Watering-holes in Alpine areas mainly host desmids, filamentous green algae (particularly Zygnematales) and chlorococcal chlorophytes (Scenedesmus, Pediastrum). 33 34 Research on Alpine watering-holes on Monte Baldo has shown that desmids, volvocaceous chlorophytes, euglenoids (including red species like Euglena sanguinea), dinoflagellates, cryptophytes, and golden-brown algae (Kephyrion) are very common. Among volvocaceous chlorophytes there is also Volvox, which forms dense, green floating mats in several spots in the pools. This alga has a very peculiar and interesting colonial organisation. The individual biflagellate cells, joined to one another by plasmatic connections, are united in a spherical structure and, although morphologically they all look alike, in fact they carry out different “ tasks” (e.g., only a few carry out reproduction, whereas most are used for photosynthesis and movement). This task division is so marked that the Volvox colony should actually be considered a multicellular individual. It also reproduces in a typical way, both asexually and sexually, giving rise to small colonies which are visible inside the mother colony. Another research on 64 Alpine watering-holes in the Austrian Alps proved the existence of xerotolerant species, i.e, particularly adapted to withstanding long periods of drought (like the desmid Cosmarium nasutum ) and many sphagnophilic acidophiles (like the desmid Euastrum denticulatum). Research has also shown that spring colonisation by algae in spring is very rapid: one pool that had thawed only a few days previously already contained Euglena sanguinea 30 desmid species. In this period, there are few green volvocacean algae and euglenoids due to the transparency of the water, which has not yet been enriched with nutrients by cattle (animals do not graze at high altitudes until the first half of June). Algae in rock- pools. The mountain landscape and low-altitude karstic areas often contain rock-pools. They are generally ephemeral and host a few, highly specialised algae, such as the volvocacean green algae Haematococcus pluvialis (see the section on red blooms, page 36) and Stephanosphaera. The small pools on carbonate rocks sometimes contain tiny dark brown “balls”, which are cyanobacteria of the genus Nostoc . Cysts of Haematococcus pluvialis Algae in temporary Sardinian pools. Research on benthic diatoms in temporary Sardinian pools has proven to be extremely interesting, because very little is yet known about them. Although scientists have focused on various types of aquatic environments, the most interesting diatom communities are found in pools. Pools of various sizes filled with rainwater which floods grassland (a typical example is a pool near Dorgali on the eastern Sardinian coast) do not only contain well-known diatom species known from similar environments, but also several species of the genera Hantzschia and Stauroneis previously unknown to science. However, the most interesting finding was the diatom microflora in the so-called paulis, which are typical basalt rock-pools in the central plateau in Sardinia, called Giara di Gesturi. One species of diatom, Pinnularia atlasi (see photo), which usually lives in the Atlas Mountains, was found in Sardinia for the first time. Its size and particular morphology make it impossible to overlook or confuse it with other, already known algae, and it thus constitutes an interesting biogeographic element of this area (Upper and Middle Atlas Mountains of North Africa and Sardinia). 35 36 Red blooms Alpine watering holes, small, shallow bodies of water rich in organic matter and algal nutrients derived from grazing cattle, may sometimes turn crimson in late spring-early summer. The colour may later darken to violet, and last over the summer and even later. Each year, a particular event, which has been carefully analysed, occurs in the central Apennines, and the same phenomenon occurs in the Alps and other Italian mountain regions (e.g., Nebrodi Mountains, Sicily). In these environments, unicellular algae responsible for red blooms are euglenophytes of the genus Euglena, especially Euglena sanguinea. These algae have tapering vegetative cells, pointed at the rear. They are motile, due to a long flagellum (another, very short one lies inside a deep front invagination called the cytopharynx). In the warmest hours of the day, these algae gather on the surface of ponds, in the water film created by surface tension. The cells of Euglena, especially those in the neustonic phase (see photo), contain a mixture of carotenoids (in the past called haematochrome). Haematochrome is contained in cytoplasm in tiny droplets that generally collect in the middle of the cell. When light becomes intense and the temperature rises, these fatty droplets spread throughout the cell, turning it red. This colour and the gathering of cells in a dense layer under the water surface (tens of millions of individuals per litre) may give rise to extensive red blooms in small ponds. In mountain environments, red Marco Cantonati blooms in tiny temporary pools are due to the very common volvocaceoan chlorophyte Haematococcus pluvialis. Its vegetative cells are motile due to two flagella but, when conditions are unfavourable, they turn into round, thick-walled, non-motile cysts. They fill up with the carotenoid astaxanthin and turn deep red in colour. Their dense accumulation on the bottom gives rise to red blooms. The factors causing the accumulation of astaxanthin and the formation of cysts are lack of algal nutrients (inorganic nitrogen, phosphorus) and exposure to sunlight. These mechanisms have been thoroughly analysed, and this alga is now grown in many bioreactors. Astaxanthin is an economically important compound. It is already used in the food industry (it is one of the components of feed for farmed trout and salmon because it gives their flesh a more attractive colour) and it appears to have a hundred times more effective antioxidant properties than vitamin C! ■ Algae in rice-paddies 37 The water regimen in rice-paddies is selective towards taxa, so that they host algae seldom found in other environments, like the green algae Sphaeroplea and Hydrodictyon. The latter, also called “ water net” , is typically found in nutrient-rich water. Its single cells are arranged as sides of polygons (usually pentagons and hexagons) so that the colony looks like a thin-meshed net. It may stretch over a quite large area (according to ancient Chinese books, even up to two metres!). ■ Algae in fountains Algae living in several of the artificial containers made by man are also very interesting. As they are much more stable than the previously described environments, they contain structured communities with several taxa. For instance, Ramón Margalef studied the seasonal changes in algae of a small fountain 1.5 m in diameter (see figure below). Closed, dimly lit environments like tanks are unlikely to be colonised by autotrophs (algae that need light fof photosynthesis). JAN DEC NOV OCT SEPT AUG JULY JUNE MAY APR MAR FEB JAN DEC NOV OCT SEPT AUG JULY 1 2 3 4 5 6 7 8 9 10 11 12 13 Seasonal blooms of algae in a fountain (belt width indicates abundance of species): 1 Cryptomonas erosa (cryptophytes); 2 Peridinium pusillum (dinoflagellates); 3 Cosmarium laeve (desmids); 4 Pandorina morum; 5 Gonium sociale (volvocales); 6 Scenedesmus quadricauda; 7 Pediastrum boryanum boryanum (chlorococcales); 8 Fragilaria construens; 9 Achnanthes minutissima; 10 Synedra radians (diatoms); 11 Spirogyra nivularis; 12 Mougeotia sp. (zygnematales); 13 Cladophora crispata (cladophorales) Pools, ponds and marshes Pools, ponds and marshes I TA L I A N H A B I TAT S Ministero dell’Ambiente e della Tutela del Territorio Museo Friulano di Storia Naturale It was from these considerations that the idea even the necessity - of writing this volume arose. It has the ambitious aim of focusing the attention of the public at large on the intrinsic value of these sometimes tiny bodies of water - small in size perhaps, but of enormous value for the proper knowledge and conservation of our natural resources. 9 788888 192222 The traditional activities associated with these environments have recently been greatly reduced, as man has felt the need to expand his urban and industrial areas, or to practise extensive agriculture at the expense of wetlands. Pools, ponds and marshes have undergone an inexorable and extremely rapid decline, and are now viewed as the some of the most at risk in Europe. H A B I TAT S Pools, ponds and marshes are natural environments which contain everything we may wish to learn about ecology. But the interest and indeed fascination of these environments is not limited to science or teaching. Pools and ponds are part of the tradition of country people and, whether large or small, whether they are reserves of drinking-water or used for irrigation, whether they provide water for farmed livestock or for widelife, they are always to be found near small country villages. I TAL I AN Konrad Lorenz wrote: “...go with a jam jar and a small net to the nearest pond - draw the net a few times through the depth of the pool and you will have a myriad interesting organisms”, and “In the train of the fishing net came the magnifying glass; after this again a modest little microscope, and therewith my fate was scaled”. 11 11