Centre D'estudis Avançats De Blanes

30 YEARS

1985-2015

CENTRE D’ESTUDIS AVANÇATS DE BLANES The goal of the project MetaBarPark is to develop and validate a tool (techniques and protocols) to characterize the biodiversity of representative communities of the Marine National Parks using environmental DNA. The Contents of the Bulletin Contents

From the “Aquarium” The Directors of “The Changing paradigms: Our biosphere: to the Centre d’Estu- Centre for Advanced three decades of studying computation and theory dis Avançats de Blanes Studies of Blanes” seagrass ecosystems by for a world in crisis by (CEAB) by María Jesús Teresa Alcoverro David Alonso Uriz

Shifting funds in marine Movement Ecology by Riparian and stream Marker pigments in benthic ecosystems: from Frederic Bartumeus ecosystems: hot spots of palaeolimnology by Teresa survival to plenty and back nutrient retention within Buchaca by Enric Ballesteros catchments by Susana Bernal

The microbial biodiversity Invasive species in a Benthic suspension feeders Aquatic plants and of natural ecosystems by changing sea as indicators of the effects wetland ecology by Emilio O. Casamayor by Emma Cebrian of Global Change on Esperança Gacia littoral ecosystems by Rafael Coma Contents

Advances in knowledge Sponges: archaic Global Change effects on The world symbiotic about the Atlantic Bluefin animals under modern stream biogeochemistry polychaetes revisited by Tuna’s spawning behaviour evolutionary and by Eugènia Martí Daniel Martin. by Ana Gordoa biotechnological prospects by Manuel Maldonado

The Group of Aquatic Ma- The importance of the Stream macroinvertebrates: Socio-Ecology By Rafael crophyte Ecology, GAME taxonomy by Enrique surviving to Global Change Sarda by Miguel Ángel Mateo Macpherson and cyanotoxins by MariÁngels

New tools for biodiversity From taxonomy to Biodiversity, ecology Capacity building of the assessment by Xavier molecular ecology and and conservation in high Centre for Advanced Turon biotechnology: the mountain lakes by Marc Studies of Blanes SPONGES as an excuse by Ventura (1990-2015) María Jesus Uriz Medsoul is a coordinated project, which aims to contribute to the needs of the prioritized challenge about climate change and the efficiency in resource use by providing scientific knowledge and tools to face the management of freshwater resources.

More than 50 years of scientific research in Blanes FROM THE “AQUARIUM” TO THE CENTRE D’ESTUDIS AVANÇATS DE BLANES (CEAB)

By María Jesús Uriz

lanes, “the Costa Brava Portal”, kely triggered by Carlos Faust, who foun- headquarters in the fishermen huts at the as its touristic trademark an- ded the Botanical Garden Mar i Murtra Blanes harbor. When in 1957, the IIP mo- nounces, is geographically loca- with its associated International Station ved to a new building in Barcelona, it did ted on a privileged rocky littoral of Mediterranean Biology in 1920. At the leave a coastal marine laboratory harbo- Bwith spectacular steep cliffs. The beauty beginning of the forties, a young Ramon ring a small public aquarium, which would of the Costa Brava landscape has confe- Margalef, who would become one of the persist in place for 30 years. rred to the village an international tou- best ecologists worldwide, started his ristic reputation. However, the touristic research on freshwater protists in the The Blanes laboratory, commonly known prestige of Blanes did not hamper its pa- dependencies of the Botanical Garden. In as “ the Aquarium” closed in 1987, after rallel trajectory on investigation. 1949, the Consejo Superior de Investiga- retirement of its latest director Manuel ciones Científicas (CSIC) set up in Bla- Rubió. The inauguration of the Centre Indeed, Blanes has had a long tradition in nes one of its four coastal Institutes of d’Estudis Avançats de Blanes (CEAB), scientific research on Natural Systems, li- Fishery Research (IIP) with its provisional also belonging to the CSIC, took place in

More than 50 years of scientific research in Blanes The Aquarium & Laboratory at the Blanes harbor in the seventies. 7 First computers.1985. First sponge meeting.1986.

1985, almost concurrently with the Aqua- The Blanes laboratory had all the requi- perimentation. Despite its small size, this rium pre-closure. This is maybe because sites of a Coastal Marine Station: easy laboratory-aquarium, took benefit of its the CEAB has been commonly regarded access to various Mediterranean marine privileged situation and received scien- as a continuation of the Aquarium of Bla- ecosystems, fluent collaboration with tists from marine research Institutions nes. However, the initial scientific objecti- local fishermen, who facilitated sampling around the world, as well as students ves of the CEAB had little to do with the far from the coast, and an open water from the Spanish Universities for summer research that had been conducted at the system of aquaria, which allowed the stays and PhD researchers on benthic fi- old Laboratory-Aquarium. maintenance of living organisms for ex- shes and invertebrates.

The CEAB team in 1990.

8 Conversely, the CEAB was not initially of the shapes, functioning, and names of found its definite research career on ma- planned to perform research on ma- marine organisms. This unique “experi- rine sciences, but a team of Freshwater rine sciences but to gather scientists ment” bred unexpected results, such as Ecology from the University of Barcelo- from everywhere during their sabbatical some formal collaboration between “the na joined the marine in 2001 and both stays. Federico Mayor Zaragoza, Minis- Intelligent” (as we, the biologists, used to groups were the germ of the current ter of Educación y Ciencia in 1981-1982 name the people of the Artificial Intelli- Departments of Continental Ecology and (UCD), supported by scientists such as gence Department) and “the biologists”. Marine Ecology. Joan Oro, at that time retired from his Co-surpervision of one master and one research activities at the NASA, lead this doctoral thesis, besides several coautho- Comings and goings did not impede the project. However, the replacement of red papers on expert systems for sponge CEAB to find its long-term scientific way: UDC by the Socialist party at the Spa- identification emerged from ideas that the study of aquatic systems and their nish Government in 1982, altered the have grown up during the joint semina- responses to environmental, natural and CEAB exciting formula, which stimulated ries and the daily talks at the CEAB can- man-induced changes. The circle was clo- the creativity of those scientists working teen. sed and the early research on fresh-wa- “apart together“ at the CEAB. Joint se- ter organisms initiated by Margalef at the minars where the speaker lowed down But the CEAB, like any living being does, Blanes Botanical Garden in the forties the difficult terms and concepts of his evolved with time. As originally planned, followed by the investigation on the ma- own field of research to facilitate gene- the group of Artificial Intelligence leaved rine benthos at the old aquarium (IIP) re- ral understanding were organized weekly. the CEAB to form its own Institute in Be- gained prominence to become the only The “marine” learned about solar winds, llaterra in 1994. Few years later (1999), current research lines of the CEAB. Red Giants, White Dwarfs, and fuzzy lo- the Astrophysicists moved to Barcelona gics, while the mathematics, physicists, to take part of the Institut de Ciències de and informatics were fascinated because L’Espai (ICE). The CEAB seemed to have

Second sponge meeting. 1988. Natural Products meeting.1989.

The CEAB team in1991. The CEAB team in 2001.

9 The Operational Observatory of the Catalan Sea (OOCS) studies changes in the marine environment by means of in situ observations, remote observations and statistical and numerical modelling.

The directors of the CEAB THE DIRECTORS OF THE CENTRE FOR ADVANCED STUDIES OF BLANES

Antonio Francesc Maria Jesus Cruzado Esteva Uriz 1985 - 1987 1987 - 1994 1994 - 1998

Enrique Daniel Emilio Ortega Ballesteros Martin Casamayor 1998 - 2002 2002 - 2014 2014 - Present

11 LimnoPirineus is a LIFE + Nature project aimed at improving the conservation status of species and aquatic habitats of European interest in the high mountains of the Pyrenees.

Photography by Eglantine Chappuis Our researchers take the floor CHANGING PARADIGMS: THREE DECADES OF STUDYING SEAGRASS ECOSYSTEMS

cosystems are badly beha- last few decades have seen breath-ta- ved things. More often than king progress in our understanding of not, they do not comply with how these systems work. As marine our most basic expectations benthic ecologists we have been pri- Eof them. As eager students of mari- vileged to witness first hand, and even ne biology, we leap into the water, fi- make a few modest contributions to lled with a text-book understanding the way we look at the marine ben- of how our ecosystems should beha- thos, not merely in the Mediterranean, ve, confident that they will confirm but across the world. The changing our deeply-held convictions of them. paradigm of seagrass meadow functio- Yet the ecosystems that we love have ning is a clear example of how much a perverse way of challenging the- research has changed the way we think se convictions, leaving us profoundly about these systems in the last three frustrated. It is a hard-fought lesson decades. ALCOVERRO, to acknowledge that science is built not so much from an accumulation Around 30 years ago these were TERESA of quantifications-of-the-obvious but ecosystems we thought we knew well. from trying to understand the pieces They were clearly limited and regula- Head of Marine Ecology that don’t quite fit the accepted pa- ted by resources – light and nutrients Department radigms. These misfit pieces are as – seagrass leaves senesced and died, Since 2015

Researcher 1996 - Present

Posidonia oceanica seagrass meadow.

fascinating as they are frustrating, and, making decomposition the most im- if we study them long enough, could portant pathway of nutrient recycling. even be the basis of a whole new pa- Herbivores and other higher trophic radigm – a whole new way of looking groups played minor roles, if they at an ecosystem we thought we knew were important at all. During this de- so well. cade, most research focussed on do- cumenting how seagrasses solved the There are probably few systems as problem of resource acquisition in ripe for these voyages of surprising different conditions of nutrient limi- discovery as benthic ecosystem. It has tation, clonal integration and nutrient been less than half a century since recycling, and the effects of eutrophi- SCUBA diving opened these systems cation and organic matter on seagrass up to detailed investigation, and the meadows. In effect, seagrass meadows were merely underwater grasslands – vory in seagrass meadows. The research any problems thanks to their fantastic just without the herbivores. was patchy and limited to a few regions systems of adaptation including com- in the tropics and in the Mediterranean, pensatory growth and clonal extension. The fact was, that as we studiously me- but from these studies it was becoming Increasingly, our underwater grasslands asured nutrient uptake and decompo- clear that herbivores were much more were beginning to resemble terrestrial sition rates in meadow after meadow, important than previously thought. From savannahs, sculpted by the forces of re- we were being constantly followed by contributing less than 5% of the fate of peated grazing pressure. groups of curious onlooking herbivores, primary production, herbivores began and we eventually had to take notice of to be seen as real ecosystem engineers. Beyond a certain density though, them. The more we looked at the plants And increasingly, it became evident, that herbivores clearly test the adaptive themselves, the more we found that had it was not merely the large megaherbivo- capacity of seagrass. Under these invested heavily in resisting herbivory. If res that were responsible for this offtake. conditions, plants show reduced fitness, herbivores were not important today, Herbivorous fish and sea urchins could sexual reproduction virtually disappears, they certainly played an important role in be equally important functional species, and habitats can undergo major species shaping seagrass adaptations in their long vital in shaping the character of seagrass shifts, leading even to complete meadow co-evolutionary history. The acknowled- meadows. Where they have not suc- extinction. This is particularly true when gement that herbivores were a vital part cumbed to overfishing, fish herbivores high densities of megaherbivores are of this system was slow to take hold, but could consume more than 50% of pri- involved. How ‘natural’ is this excessive around two decades ago, we saw data mary production – a consumption that herbivory? On the one hand, it could be being gathered on herbivores and herbi- the plants appear to tolerate without perfectly normal for seagrass meadows to

Sampling ecosystems of Posidonia oceanica for the monitoring program of “L’Agència Catalana de l’Aigua”. 15 Manipulative experiments with Posidonia oceanica.

appear and disappear, existing in a patchy Seagrass meadows are ideal systems to to have been part of this entire intellectual dynamic equilibrium as herbivores rotate study these landscape-level processes journey – from the initial studies on between fragments, sequentially driving because they are relatively simple resource ecology to the study of trophic each to extinction before moving on. compared to most terrestrial systems, and interactions and seascape ecology and, Most short-lived seagrasses appear well have only few key species of herbivores. more recently, to behavioural ecology. Far adapted to this by investing in dormant from being planned and strategic, these seeds that remain viable in the sand for a How these few herbivores behave transitions have been organic, as we have long time. On the other hand, it is possible becomes critical and very elegantly adapted our studies to each turn in our that the increasing population trends links seascape ecology to ecosystem understanding of the system. From this we see in megaherbivores are far from function through animal movement and changing paradigm, we have learnt clear normal – they are only possible because behavioural ecology. There have been a lessons about what we need to do if the large predators that controlled them series of studies emerging that explore we want to manage and conserve these in the past are now absent. notions of connectivity and fragmentation precious ecosystems. For one, it is critical from the point of view of long-ranging to keep nutrients in check. We also need Green turtles for instance are making an species, and the direct and indirect to think hard about what a ‘pristine’ encouraging recovery all over the world consequence of herbivore choices on seagrass meadow represents – with its while their main predators – several higher trophic interactions. This is leading full complement of herbivores and their species of large sharks – are becoming to an increasing interest in seascapes of dominant predators. Meadows have co- functionally extinct. These ‘unnaturally’ fear – showing that animal behaviour in evolved with this community of species high numbers of green turtles could the presence of their predators can have and can remain healthy and functioning grow way beyond the capacity of seagrass significant functional consequences for only when they are conserved together. meadows to support them, driving the the ecosystems they inhabit. ecosystem to extinction. The jury is still The last few decades have been an out on which of these views is ‘true’. Where we stand today, we realise that we exciting time to be doing research on are only at the beginning of a very long road benthic marine systems and we cannot Space is the final frontier. The last decade towards understanding an ecosystem we wait to see where the next few decades has seen a burgeoning of research on thought we had completely understood will take us on our continuing journey of how trophic processes play themselves a few decades ago. As researchers our discovery of these endlessly fascinating out within the seascape of the meadow. group in CEAB has had the good fortune ecosystems. 16 OUR BIOSPHERE: COMPUTATION AND THEORY FOR A WORLD IN CRISIS

y history here is still CEAB history is 30 years long, but in short. Almost five years just the last 5, I have already witnessed ago, the Summer of important changes that should impro- 2011, I landed at the ve the ability of our center to cope MCenter for Advanced Studies (CEAB- with current research and societal cha- CSIC) in Blanes, a sunny locality llenges. Let me just highlight two on the Northern Catalan Coast. I of them. came right away from the University of Groningen, the Netherlands, where First, I have participated with en- I had been holding a VENI postdoc thusiam in an ambitious project to buy position for three years and enjoying and set up a high performance compu- —sometimes enduring— windy, cold ter cluster, a computational facility for winters, and variable, and too often, the center, the “computational biolo- ALONSO, rainy Summers. Ever since I have been gy laboratory”. Second, I have seen living and working here in Blanes how a small number of people commi- DAVID under a “Ramon y Cajal” fellowship. tted to work on outreach and dissemi- As it is well-known, the consequences nation of scientific culture has grown Ramon y Cajal of the deep financial crisis all over the now into a well-established group in world resulted in Spain in tremendous our center. Several researchers from Researcher budgetary cuts. the staff have been deeply involved in 2011- Present the consolidation of this group, who is As for research, whether in terms of in charge of organizing the CEAB open the GDP percentage devoted to re- doors week every year, seminars, and search, quantity of money invested other events all year around. Myself I or number of researchers, the figures strongly support the group and most have been all declining since 2010. The of its current outreach activities. Re- crisis has been hard for every citizen in cently, the group has obtained funding Southern Europe. Researchers despe- for an original project that works with rately compete for resources to keep School teachers to expand their capa- their research agendas up and run- bilities of teaching science and techno- ning. In particular, I would love to ob- logy in the classroom. tain more money and projects to hire more students and postdocs in order Ecology studies interactions between to enlarge my group and work on tho- organisms within their dynamic en- se research questions I am interested vironments. In particular, most of my in, but current economic context is research focuses on the study of the harsh and poses serious difficulties main factors controling biodiversity for every Spanish research group and community composition across to grow. In spite of all these seve- spatio-temporal scales. Ecological sys- re problems, I have received funding tems are tremendously complex. The from the Spanish Ministry of Economy realization that they are just another and Competitiveness for a research example of a complex adaptive system project that let me hire a great [11] pervades all my research since my postdoc, José Angel Capitán, who just PhD early years. In general, complex recently started a lecturer position at systems can be regarded as ever-adap- the Polytechnic University of Madrid, ting, large networks of individual agents and a motivated PhD student, Vicente interacting through a fluid network Jiménez Ontiveros, who is scheduled structure in a finite number of ways. In to defend his PhD thesis by the end the attempt to understand systems as of 2017. complicated as our brains, global eco-

17 nomy, or coral reef fish communities, in- ther molecules of a gas or electrons in a levels of organization? In which sense is terdisciplinary scientists use techniques, semiconductor, and the macroscopic pro- the whole much more than the sum of models, hypothesis and methods essen- perties of the system as a whole. the parts? In particular, to mention two tially developed by physicists working relevant questions from different fields, on statistical mechanics. In Ecology this How do macroscopic properties we ob- how do consumer beliefs and behaviors approach was initially put forward by serve emerge from the microscopic in- end up determining market prices and James Brown and Brian Maurer [6,13]. teractions between the elements integra- market crashes? How do species compo- Broadly speaking, this is the branch of ting the whole system? The key concept sitional changes along gradients emerge physics devoted to understand the link here is “emergence”. To what extent do from individual interactions and specific between the parts and the whole, be- properties at a given level of organization adaptations to the environment? tween the constituents of a system, whe- result from processes occurring at lower

Figure 1. Colors represent dierent model outputs for each parameter pair, mosquito biting rate, on the horizontal axis, which increases with increasing temperature, and mosquito carrying capacity, on the vertical axis. For instace, increasing temperature can take the system from point C, a malaria-low-incidence state (in orange), to point D, a malaria-high-incidence state (in red). Shaded regions represent bi-stability, this is, situations when high and low-incidence states can be both reached for the same parameter values depending on the history of the system.

The neural network in my brain produ- highly quantitative, and mathematics pro- ms of inequalities similar to the second cing now this text is radically different vide general concepts, models, and fra- law of thermodynamics. from other types of complex networks meworks that apply across disciplinary controling, for instance, global economy. boundaries [8]. We live in the “big As you see, in essence, I am very in- In fact, some scientists think that radical data” age. The comparative analysis of terested in exploring to what extent different systems should necessarily re- big amounts of data from different fields natural systems in their tremendous quire different methodologies, underlying may pave the way to new theories [3]. complexity can be described by and un- hyphothesis, descriptions and interpre- Universal principles should govern our derstood in terms of simple — perhaps tations. ability to predict plausible future states of universal— low dimensional abstractions a given system if we have a fair descrip- and useful approximations. Fruitful, cu- Why should their descriptions have tion of its current state. Determination tting- edge examples of this kind of re- anything in common at all? I believe this of prediction horizons use methods that search are those related to regime shifts criticism is only true to a certain extend. apply across fields [17, 14]. Such general and phase transitions [12,18]. Highly specialized scientists working on principles will have the character of “law the particularities of a certain group of of nature” and, therefore, elegantly, apply These phenomena occur when systems insects only living on a limited number across disciplines. They will not have the shift abruptly from one state to another of host plants are, of course, essential, form of deterministic Newtonian princi- when they are forced across critical but, broadly speaking, modern science is ples, but rather have formulations in ter- thresholds. A macroscopic system pro- 18 perty undergoes an abrupt state shift as mental variability, but much less is known increases over a critical threshold (see a result of a slight change in another va- about how environmental fluctuatons are Fig 1). riable across a critical threshold. This in- actually transduced into population fluc- volves that, close to these critical points, tuations. In 2011 we published a pa- The second contribution I would like to system response can be highly non-linear. per to demonstrate that human-induced mention was done in collaboration with In Physics, a slight increase in tempera- climate change through increasing tem- Teresa Alcoverro and Rohan Arthur ture close enough to the boiling point peratures plays a central role in malaria from CEAB and Aleix Pinyol-Gallemí induces a water-to-gas phase transition. transmission in the highlands of Kenya, who was at that time an undergraduate Surprisingly, these types of critical tran- East Africa [1]. The human-mosquito-ma- student from the University of Barcelona sitions occur in seemingly non-related laria dynamic model I developed, interes- [2]. This contribution is related to systems such as marine systems [15], fi- tingly, shows a critical transition from low my efforts to disentangle the main sheries [16], deserts [9] or societies [7]. to high malaria incidence as temperature drivers of community assembly. How Even more astonishing is the fact that the underlying mathematics across all these different systems is essentially the same.

Although we all like major scientific advances, science makes also progress through incremental improvements. Scientific literature is sometimes boring because it is full of tiny improvements that are sometimes difficult to appreciate. Throughout my research, I always like to keep in mind the big picture because tiny advances, actually, pave the way to truly breakthroughs. Anyway, most of our publications are probably tiny contributions to science, but, in one way or another, here at CEAB, we all share the proud of contributing to the progress of science.

Just to give an idea, let me highlight here only two of my favorite contributions. The big picture of the first one is related to the origins of population variability. A well-accepted reason why populations change in time is environmental temporal variability, such as rainfall and temperatu- Figure 3. Extinction probabilities show a clear signal of average trophic level across seven guilds re. How does environmental forcing in- of coral reef fishes including algal feeders (A), zooplanctivores (Z), omnivores (0), coralivores (C), fluence population dynamics? It is often macroinvertivores (M), microinvertivores (m), and piscivores (P). As shown on the right panel, as tro- said that populations integrate environ- phic levels increases from 2 (herbivors) to 4 (piscivores), the extinction probability per year goes up quadratically, from about 0.1 to 0.4 [redraw from ref 2].

Figure 2. Recovering of a coral reef ecosystem after a coral mass mortality induced by a severe “El Niño” event. [5] 19 predictable is ecological succession? How predictable is community reassembly after a big perturbation? These are central questions in References community ecology. In that paper, we analyzed data from coral reef fish 1. David Alonso, Menno J. Bouma, and 11. Simon A. Levin. Complex adaptive sys- communities aftera El Niño-related Mercedes Pascual. Epidemic malaria and tems: Exploring the known, the unknown bleaching event and revisited warmer temperatures in recent decades and the unknowable. Bulletin of the Ame- Island Biogeography Theory to in an East African highland. Proceedings. rican Mathematical Society, 40(1):3–19, show that extinction rates increase Biological sciences / The Royal Society, 2003. with trophic position, which means 278(1712):1661–1669, nov 2011. that higher trophic guilds, such as 12. Maten Scheffer. Critical Transitions in 2. David Alonso, Aleix Pinyol-Gallem´ı, Nature and Society. Princeton University top predators, are inherently more Teresa Alcoverro, and Rohan Arthur. Press, 2009. susceptible to natural perturbations Fish community reassembly after a coral even in the absence of targeted mass mortality: higher trophic groups are 13. Brian A. Maurer. Untangling Ecological fishing (fig. 3) subject to increased rates of extinction. Complexity. The University of Chicago Ecology letters, 18(5):451–61, may 2015. Press, 1999. Human society faces big challenges, is highly technified, and generates 3. Sandro Azaele, Samir Suweis, Jacopo 14. Nicolas Mouquet, Yvan Lagadeuc, Vin- knowledge and new possibilities at Grilli, Igor Volkov, Jayanth R Banavar, and cent Devictor, Luc Doyen, Anne Duputié, incredible pace. As said, we are in Amos Maritan. Statistical Mechanics of Damien Eveillard, Denis Faure, Eric Gar- the big data age, but also in the age Ecological Systems: Neutral Theory and nier, Olivier Gimenez, Philippe Huneman, of the sixth extinction [10], and Beyond. 2015. Franck Jabot, Philippe Jarne, Dominique in the age of ever increasing social Joly, Romain Julliard, Sonia Kéfi, Gael inequalities. A huge amount of 4. Anthony D. Barnosky, Elizabeth a. Had- J. Kergoat, Sandra Lavorel, Line Le Gall, energy and resources now is routed ly, Jordi Bascompte, Eric L. Berlow, Ja- Laurence Meslin, Serge Morand, Xavier through our social organization mes H. Brown, Mikael Fortelius, Wayne M. Morin, Hélène Morlon, Gilles Pinay, Ro- worldwide. For instance, 20 to 40% Getz, John Harte, Alan Hastings, Pablo a. ger Pradel, Frank M. Schurr, Wilfried Thui- of global net primary productivity is Marquet, Neo D. Martinez, Arne Mooers, ller, and Michel Loreau. Pre- dictive Ecolo- sequestered by humans [4]. Animal Peter Roopnarine, Geerat Vermeij, John gy In A Changing World. Journal of Applied agriculture is responsible for W. Williams, Rosemary Gillespie, Justin Ecology, (AUGUST):n/a–n/a, 2015. Kitzes, Charles Marshall, Nicholas Matzke, about one third of global fresh water David P. Mindell, Eloy Revilla, and Adam B. 15. Peter J Mumby, Alan Hastings, and He- consumption in the world today and Smith. Approaching a state shift in Ear- len J Edwards. Thresholds and the resi- for up to 91% of Amazon destruction. ths biosphere. Nature, 486(7401):52–58, lience of Caribbean coral reefs. Nature, Agricultural production, processing, 2012. 450(7166):98–101, 2007. transportation and consumption of food are all activities of planetary 5. James P. Gilmour et al. (2013) Recovery 16. Tommi Per, Anna Kuparinen, and En- scale with global impacts on our of an Isolated Coral Reef System Fo- vironmental Sciences. Detecting regime biosphere. llowing Severe Disturbance. Science 340, shifts in fish stock dynamics. Canadian 69-71. Journal of Fisheries and Aquatic Sciences, They conform the so-called food 72(11):1–41, nov 2015. system. These activities use three 6. James H. Brown. Macroecology. The strategic resources —water, energy University of Chicago Press, 1995. 17. Owen L Petchey, Mikael Pontarp, and land— which are at the center Thomas M Massie, Sonia Kéfi, Arpat of most wars and conflicts today. In 7. Jared M Diamond. Collapse: How So- Ozgul, Maja Weilenmann, Gian Marco Pa- the near future, I am very interested cieties Choose to Fail or Succeed. Viking lamara, Florian Altermatt, Blake Matthews, in analyzing in detail the role of Books, New York, 2005. Jonathan M Levine, Dylan Z Childs, Brian food systems in determining critical J McGill, Michael E Schaepman, Bernhard regime shifts across scales. 8. Jordi Bascompte. Las matematicas de Schmid, Piet Spaak, Andrew P Beckerman, la biodiversidad. Investigacion y Ciencia, Frank Pennekamp, and Ian S Pearse. The pages 2–3, oct 2013. ecological forecast horizon, and examples How plausible is a planetary- of its uses and determinants. Ecology let- scale critical transition? Inherent 9. Sonia Kéfi, Max Rietkerk, Minus van ters, 18(7):597–611, jul 2015. complexities to human-dominated Baalen, and Michel Loreau. Local fa- systems make future very hard to cilitation, bistability and transitions in arid 18. Ricard Sole. Phase Transitions. Prince- predict. If forecasting the future is ecosystems. Theoretical Population Biolo- ton University Press, 2011. almost impossible, what we urgently gy, 71(3):367– 379, 2007. need is to start creating now the future we want to live in. Challenges 10. Elisabeth Kolbert. The Sixth Extinction: are global and urgent. I envision a an unnatural history. Bloomsbury, 2014. future where science and technology, an economy for the common good, and real democracy are the central pillars of a new global order. 20 SHIFTING FUNDS IN MARINE BENTHIC ECOSYSTEMS: FROM SURVIVAL TO PLENTY AND BACK

February 1986. My first terspersed small coves. I am here to day at work in a brand develop my scientific career as a ma- new research institute rine ecologist. The best job and place devoted to Marine I could ever imagine. A dream. 11Ecology and Artificial Intelligence close to the city of Barcelona, but I come from the Department of far away enough from Barcelona to Ecology at the University of Barcelona, be in close contact with nature. Its where I had been working in my PhD name, Centre d’Estudis Avançats de thesis between 1981 and 1984 and Blanes (CEAB; Center of Advanced was appointed as teaching assistant Studies from Blanes), is vague enough from 1985 until yesterday. There, to accommodate almost any kind I did not have an office, but a place of scientific discipline that can be in a room plenty of other assistants, BALLESTEROS ENRIC,

Researcher 1986 - Present

First field work expedition carried out by CEAB scientists together with researchers from the Marine Science Institute of Barcelona (ICM). From left to rigth: Andrés Maldonado (ICM), Kike Ballesteros, Iosune Uriz (CEAB) and Jordi Camp (ICM). October 1986, Cabrera, on-board of “Garcia del Cid”.

branded as “advanced”. I suppose technicians and students. This place that it was not an easy task to find a was like an ant’s nest, where I could name for a scientific institute whose hardly concentrate on my work and research areas were marine ecology, prepare my teaching lessons. But I was artificial intelligence and -later on- feeling great. Friendship atmosphere, astrophysics. youth, plenty of interaction with rookie ecologists like me, and with a The building is surrounded by luxu- big boss, Ramon Margalef, idolized by rious Mediterranean pine forests, has everybody. amazing views over the Montseny, a beautiful mountain whose cap is oc- I park my beat-up Citroën in front of casionally covered by snow in winter, the building and I am welcomed by and is located at a 5 minutes drive the oceanographer Dr. Antonio Cru- from granitic rocky shores with in- zado, earlier director of the institute. 21 After a brief walk inside the almost empty for projects (=money)” he asserts. I come buy the basic materials for performing building, he asks me to choose a room. back to my room, sit down, look around our research (microscopes and other All the rooms are completely empty. Four at the echoing walls, and question myself lab material, inflatable boat, tanks, diving walls, that’s it. I choose a big one; it will if coming here has been a smart choice. compressor, van), but most importantly become my office. The warehouse assis- Probably not, but I have to succeed. I am to engage other young people in these tant brings me a table without drawers, a not a person easy to be defeated. Dreams two research lines, whether scholarship chair, and a telephone that he plugs into cannot turn into smoke so quickly! assistants and researchers or emerging the phone connection and places it over professors at the University of Barcelona. the floor. “This is everything”, he tells me. Fortunately, there is another marine bio- These very first years we were able not I am shocked. I leave the room (it does logist at the institute, María Jesús (Iosune) only to survive but we started the basis not deserve the name “office”) to ask Uriz. We join our two single-member for the current Department of Marine Antonio Cruzado if this is a joke. Where teams to apply for the project “Towards Ecology of the CEAB. These projects and I am supposed to put all my books? The a model of organization of Mediterra- energy were key for obtaining new re- laboratory I have in front of my room is nean littoral rocky benthic assemblages”, search positions in the CEAB and for not also completely empty: not even a single which receives funding from the Spanish being absorbed by the powerful Institute test tube. And microscopes? What is this? Government. Iosune also gets the pro- of Marine Sciences based in Barcelona. He replies me that this is everything the ject “Ecological foundations for searching institute will provide me as a new resear- new pharmacological drugs in Mediterra- The collaboration between Iosune cher. He kindly offers me a second chair, nean benthic ecosystems” funded by the and me, essential during these first in case somebody is coming to visit me. company Pharma-Mar. These two pro- years, progressively decreased as she “The first thing you have to do is asking jects allow us to furnish our offices and increasingly focused her research in

Cover image of the Handbook of Coastal Habitats of Catalonia, a study carried out to help policy makers and stakeholders to improve the management of natural resources of the Catalan coast. 22 Carcharhinus albimarginatus, a very common shark species inhabiting the tropical reefs studied by the Pristine Seas project. processes occurring at the level of grants or projects. We also focused in and finishing of the loose ends of the cells, individuals and populations and I other questions that deserved a more last and previous projects but has not gained interest at processes taking place specific, different, or accurate approach, guaranteed the long-term surveys that whether at the community or ecosystem like the populations and communities were in some cases initiated as far away level. A critical year for my research was made up by species of the algal genus as in 1992. We find ourselves again in the 1992, when the invasive seaweed Caulerpa Cystoseira, the Mediterranean underwater path of survival but with the conviction taxifolia, the killer alga, became renowned. ecological relatives of oaks (Quercus) from that most of the investment in money, In order to control the progression the terrestrial environment, or the highly time and energy of two decades has and to study the biology and ecology biodiverse and vulnerable coralligenous been thrown away and with the almost of this alga in the Mediterranean I got outcrops, Mediterranean biogenic reefs certainty that time for long-term surveys European, national and regional funding that only grow at dim light conditions. is over. Moreover, the eagerness has together with other labs in Marseilles and turned up into confusion and frustration. Nice (France). Easy money. I became a However, nothing lasts forever. The Bad feelings if we want to keep moving specialist in marine bioinvasions in a place current economic crisis that so sharply onto science. and time where and when almost nobody stroked Spain from 2009 onwards worked on this issue. Bioinvasions also suddenly cut off most financial revenues. But survivors as we are, we will keep trying. allowed me to start a collaboration with Still, in 2010 we obtained a project to Crisis, also, will not last forever and some the Departments of Environment and/ make a description and cartography of initiatives are emerging. We will try to or Fisheries of regional governments all the littoral habitats from Catalonia, continue monitoring the abundances and (Generalitat de Catalunya, Govern de where we developed a completely new effects of invasive species, try to better les Illes Balears) that lasted for 21 years methodology to map littoral habitats, understand the dynamics of Cystoseira, and progressively broadened to the which are restricted to very small areas the “Mediterranean underwater trees”, implementation of the Water Framework following steep gradients of environmental and will continue surveying the littoral Directive, the Habitats Directive and factors. This project finished in 2013 and sublittoral assemblages for temporal the creation and management of Marine (http://mediambient.gencat.cat/ca/05_ changes in relation to anthropogenic Reserves. Thanks to the plenty of money ambits_dactuacio/patrimoni_natural/ disturbances. Moreover, our engagement I was able to build up a team of specialists sistemes_dinformacio/habitats/habitats- in the Pristine Seas project of that excelled in the knowledge of different litorals-/) and the extension to be done in National Geographic (http://ocean. taxonomical groups and methodologies. the sublittoral zone down to 135 meters nationalgeographic.com/ocean/explore/ Monitoring projects were put in place depth (the continental shelf) was stopped pristine-seas/) is exciting, as this project is and carried on during several years. In due to funding restrictions. The awarding becoming the most relevant contribution this period of time we also obtained of a CSIC project with internal funds to marine conservation ever. Surrender is some of the so-called “competitive” (2013-2016) has allowed the continuation not a word in our dictionary. 23 MOVEMENT ECOLOGY

ovement is one of the opportunities to test and develop core most fundamental features theory in contexts as different as mi- of life on Earth. The change gration, foraging, invasion biology, or of location by organisms epidemics [5]. Macross multiple spatial and temporal scales quilts our planet in a rich ta- The Movement Ecology paradigm pestry of phenomena with diverse [1, 2] has emerged as a framework implications for ecosystems and hu- that places animal motion as the cen- mans [1]. Movement plays a major role tral theme in order to stimulate the in determining the fate of individuals, development of new methods and to the structure and dynamics of popu- promote understanding of the causes, lations, communities and ecosystems; consequences, underlying mechanisms, and the evolution and diversity of life. and emergent spatiotemporal patterns It is a crucial component of almost any of all movement phenomena. The de- ecological and evolutionary process, velopment of world-wide movement including major issues associated with databases such as Movebank (www. habitat fragmentation, climate change, movebank.org) is facilitating the stora- BARTUMEUS, biological invasions, and the spread of ge and exchange of data and requires pests and diseases [2]. revolutionary improvements in data FREDERIC management, processing, and analyti- Recent developments in GPS trac- cal techniques, at least as challenging Head of Continental of king and remote sensing are enabling as the bioinformatic revolution of ge- detailed tracking of animal locations nomics and proteogenomics [6]. This Ecology Department (including humans) concurrently with exciting context is attracting renewed Since 2015 acquisition of landscape data and in- interest to the study of animal move- formation on individual physiology ment and dispersal processes, bringing and behavioural status. The availability together specialists from a wide range Research Professor of better tracking and bio-logging te- of disciplines [7, 8]. 2003 - Present chnologies [3, 4] is challenging researchers’ ability to make sense of the re- Traditional modeling and quantifica- sulting data, but also creating exciting tion of animal movement is based on

Fish tracking with acoustic telemetry in the Medes Islands. the solid grounds of random walk and di- been acknowledged as one of the ‘core’ through bio-logging devices, we may im- ffusion theory [9, 11] but because of the problems in movement ecology and the prove our understanding of how animals lack of adequate empirical data, the me- ‘essential link’ to make inferences be- allocate time to different tasks (behaviou- chanistic links between movement pat- tween animal movement and population ral modes) and how this allocation chan- terns and animal behaviour have remained dynamics [1, 12, 15, 16]. As physiological ges depending on the interaction between poorly understood [1,12,13]. The main and other information becomes available animal internal motivations and different challenge in modern movement research is to use a new generation of highly-resolved, massive, movement data to improve our understanding on the mechanistic links between behavioral processes and movement patterns [12-14]. Our research at CEAB-CSIC strongly contributes in this direction, focusing on the following questions: (A) how to integrate scales from (microscopic) behaviour to (macroscopic) movement patterns, specifically to link individual behaviour with the generalized concept of diffusion, (B) how internal states and information use (organism-environment interactions) modulate movement, specifically in search/foraging processes, and (C) which evolutionary mechanisms link individual motor behaviour, movement patterns, and survival/fitness.

A. Integration of Scales: from behavioural Modes to Anomalous Diffu- sion.

Behavioural modes are movement sequences of steps, turns, and stops associated with the fulfillment of a particular goal. The segmentation of trajectories into such basic functional units has

Behavioural Annotation in Migration of Pandion haliaetus. Data from: Raymond Klassen. Migration Ecology Group. Dep. Animal Ecology. Lund, Sweden.

25 environments, thus providing a mecha- havioural modes (dynamic brownian bri- biotelemetry data analysis of free-ran- nistic way to model movement patterns dges, behavioural change point analysis) ging animals will definitively bring light to conditional on individual state [13]. One and the development of generalized-di- the problem of information use and may expect that the mixture of behaviou- ffusion mathematical frameworks (con- memory [13, 16] and will clarify the ral modes viewed over a sufficiently long tinuous time random walks, generalized distinction between pure search (non-in- time period can be described as a simple diffusion equations) provide the adequate formed movement) and taxis (informed (normal) diffusion. However, recent em- template to develop powerful mechanis- movement) in foraging processes [21, 22]. pirical results show that animals [17-19], tic and predictive tools for large-scale A new and promising research line con- including humans [20], can spread faster movement and spreading patterns, from sists on studying foraging/search eco- (superdiffusion) or slower (subdiffusion) large-scale foraging to invasive processes. logy in high-throughput, large-scale, than what would be expected from clas- experimental setups with the use of sic diffusion theory (normal diffusion). B. Search Behaviour: Information model organisms. The goal is to link This fact raises the need to extend the Use and Organism-Environment In- different levels of biological organization classic theory of diffusion towards teractions. (genetic, neurological, physiological, and new mathematical frameworks ca- ecological) with large-scale properties of pable to accommodate the so-ca- Our understanding of how individuals in- movement (type of diffusion, front wave lled anomalous diffusion. The new tegrate different sources of information propagation, search efficiency, waiting ti- generation of movement data, together in order to make foraging/navigation mo- mes). with new statistical analyses targeting be- vement decisions is still poor. Detailed

Movement behavioural landscapes using seabird trajectory variables and a mutivariate unsupervised classification algorithm (t-SNE algorithm). 26 C. Evolution of Movement: Com- evolution of simple motor systems [29]. parative Movement Ecology and Even complex animals have to find an References Model Organisms’ Experimenta- effective way to explore the environ- tion. ment when insufficiently equipped or insufficiently informed. The physiology 1.Nathan et al. PNAS 105: 19052 (2008) The lack of adequate empirical data and of how this happens has been little in- 2.Nathan. PNAS 105:19050 (2008) mechanistic approaches has constrai- vestigated. Based on international co- 3.Cooke et al. TREE 19:334 (2004) ned evolutionary thinking on large-scale llaborations at CEAB we are working properties of movement up to recently. with model organisms (such as C. 4.Rutz & Hays. Biol. Lett. 5:289-292 (2009) The massive and new generation of data elegans) to explore behavioural available will allow to perform com- intermittence as an evolutionary 5.Cagnacci et al. Phil Trans R. Soc. B parative analyses across species to template, and to unveil the main 365:2157 (2010) in order look for phylogenetic sig- sources and fundamental structu- 6.Mount. Bioinformatics: Sequence and natures [23, 24] or detect the histo- re of random animal motility[12, Genome Analysis (Cold Spring Harbor rical signature of key innovations 22, 30, 31]. Lab Press(2004) [25] related to movement traits and/or 7.Giuggioli & Bartumeus. J. Anim. Ecol. properties. We are particularly interes- The study of Movement Ecology at 79:906 (2010) ted on the evolution of behavioural CEAB should promote the develop- 8.Shamoun-Baranes et al. Biol. Lett. intermittence and its role in gover- ment of a comprehensive and integra- doi:10.1098/rsbl.2011.0764 (2011) ning random motor output. Evidence tive view of organism movement and 9.Turchin. Quantitative Analysis of Mo- of randomly generated action (action a better understanding of the causes, vement (Sinauer,Sunderland, MA) (1998) that is distinct from reaction because it mechanisms, patterns, and consequen- 10.Okubo & Levin. Diffusion and Eco- does not depend upon external stimuli) ces of all movement phenomena. The logical Problems: Modern Perspectives can be found in ‘simple’ organisms [26- ultimate goal is to provide a compre- (Springer, NY)(2001) 28] . Hence, behavioural output can be hensive understanding of animal move- 11.Berg. Random walks in Biology (Prin- independent of sensory input. This is in ment from and ecological and evolutio- ceton Univ. Press) (1983) line with the fact that in early develop- nary standpoint of view based on field 12.Bartumeus. Oikos 118:488 (2009) ment of individual organisms the motor and lab experimental data, and to be on system slightly precedes the sensory the lead of such a new and exciting re- 13.Morales et al. Phil Trans R. Soc. B system. Merely being actively disper- search field. 365:2289 (2010) sed in space should have favoured the 14.Schick et al. Eco Letts 11:1338 (2008) 15.Owen-Smith et al. Phil Trans R. Soc. B 365:2267 (2010) 16.Smouse et al. Phil Trans R. Soc. B 365:2201 (2010) 17.Bartumeus et al. PNAS 100(22):208 (2003) 18.Bartumeus et al. Current Biology 20:1-8 (2010) 19.Franks et al. J. Exp. Bio 213:1697 (2010) 20.González et al. Nature 453: 779 (2008) 21.Bartumeus et al. Ecology 86:3078 (2005) 22.Bartumeus. Fractals 15(2):151 (2007) 23.Verdú et al. Journal of Ecology 97:1171 (2009) 24.Gómez et al. Nature 465:918 (2010) 25.Ree. Evolution 59:257 (2005) 26.Korobkova et al. Nature 428: 574-578 (2004) 27.Maye et al. Plos ONE 2 (2007) 28.Brembs. Behavioural Processes 87:157-164(2011) 29.Heisenberg. Nature 459:164 (2009) 30.Bartumeus & Levin. PNAS 150(49):19072 (2008) 31. Salvador et al. J Royal Soc Interace 11, Movement modes classification and flow of a foraging seabird. 20131092 (2014) 27 RIPARIAN AND STREAM ECOSYSTEMS: HOT SPOTS OF NUTRIENT RETENTION WITHIN CATCHMENTS

ater quality is a major transform and retain nutrients. We Societal Challenge wi- seek to understand by which mecha- thin the EU Research nisms these biogeochemical hot spots and Innovation Program- can improve water quality, quantify Wme Horizon 2020. Despite decades of their contribution to nutrient reten- economic investment and technologi- tion at relevant ecosystems scales, and cal improvement, half of the freshwa- investigate under which conditions ter bodies in Europe are still affected water quality-related ecosystem servi- by high nutrient loads from diffuse and ces are maximized. The results obtai- point sources. Chronic nutrient fer- ned have important implications not tilization causes eutrophication pro- only for ecosystem conservation pur- blems and threatens ecosystem’s and poses but also provide scientific-based BERNAL, human’s welfare. In the Mediterranean knowledge for ecosystem restoration basin, increasing aridity and water de- actions and integrated management of SUSANA mand from urban areas turns water catchment water resources. quality in a tremendous economic and Ph.D. Associate / Programa technological challenge for Society. Fu- Riparian zones are well-known for JIN-Jóvenes Investigadores ture climate scenarios stress smaller being natural filters of nutrients 2009 - Present groundwater reservoirs and lower arriving from adjacent landscapes, stream discharges and consequently nitrogen (N) in particular. Since freshwater bodies will become extre- the 1980s, the number of studies mely vulnerable to nutrient excesses. showing the N buffering capacity of Within this context, ecosystems that riparian ecosystems has continuously can naturally contribute to improve increased. The acquired knowledge stream water quality in Mediterra- has had important implications on nean regions are thus, essential from environmental protection protocols, an ecologic, environmental, and social such as keeping riparian buffer strips in perspective. agricultural landscapes. Most of these studies, however, have been conducted In the last years, the Integrative in temperate regions where the Freshwater Ecology Group has focu- N buffering capacity of riparian sed an important part of its research ecosystems relays mostly on microbial on identifying landscape units with denitrification, that is the release of N a disproportionally high capacity to to the atmosphere by transforming

Mediterranean headwater stream flanked by a riparian forest of Alnus glutinosa and Sycamore sp. Fuirosos, Montnegre-Corredor Natural Park, Vallés Oriental (NE Spain). (Fig. 1). nitrate to N2 gas. Denitrification is increase catchment N retention by 30- uptake is typically assessed at small scales an anaerobic process which requires 50% on an annual basis. These findings (< 300 m reach lengths) and during water-logged soils. In Mediterranean highlight that the mechanisms responsible particular periods. By combining synoptic zones, anaerobic conditions are rarely for N retention in riparian zones can approaches and hydrological models, met because riparian soils are not differ greatly between climatic regions. we have shown that net uptake can water saturated and thus riparian Thus, a good understanding of both decrease nutrient fluxes by 4-40% within denitrification is minimal. Conversely, we soil processes and hydrological linkages few kilometres in headwater streams. have shown that Mediterranean riparian between stream and riparian systems Further, we have found that gross primary soils are hot spots of N supply because is crucial for evaluating the potential of production by stream algae can control intermediate soil moisture conditions these ecosystems to reduce catchment N day-night variations of stream nutrient stimulate organic matter mineralization loads in Mediterranean regions. concentration, and that this fine-scale and nitrification (the microbial dynamics can resonate at larger scales transformation of ammonium to nitrate). and ultimately decrease stream N loads. Our model predictions suggest that this pattern will be accentuated in the future These results support the idea that because warming will burst nitrification streams can contribute to improve water in Mediterranean riparian soils. Moreover, quality at the catchment scale and thus, the proliferation of N2-fixing species such these ecosystems could ameliorate the as the invasive black locust (Robinea risks associated to nutrient excesses. pseudoacacia) could further enhance However, the capacity of urban streams the role of riparian forests as N sources to retain N is still under debate. There by adding N into the riparian soil and is little evidence of the ability to store providing N-rich leaf litter to stream N of stream biota and/or to remove N biota. perpetually via denitrification. Detail of a streambed with cobbles and gravels. High supply of N by riparian soils could These substrates are colonized with microbial Are urban streams N saturated? Or else, severely diminish the N buffering capacity biofilms capable to transform and retain nutrients are we missing the relevant time scales at of Mediterranean riparian ecosystems from the water column. which crucial steps of the N cycle occur? and increase the amount of N entering Can restoration actions help to enhance to the stream via groundwater and/or In addition to riparian zones, streams the retention of nutrients, pathogens and surface flow. Nonetheless, Mediterranean can further contribute to improve water other contaminants in urban streams? riparian zones can still act as N buffers, quality because they are highly reactive These questions will be the focus of though their potential for N retention may ecosystems. Headwater streams have a our research in the upcoming years and be more related to geomorphology and large capacity to transform and retain hopefully we may be able to provide hydrology than to soil biogeochemistry. nutrients within relatively short distances. some answers to water stakeholders and For instance, we have recently showed Yet, the influence of in-stream processes Society sooner than later. that hydrological retention of stream on annual catchment budgets is still water within the alluvial aquifer could poorly understood because nutrient

Tree roots submerged in the stream boulders covered with algal biofilms. Stream-riparian interface at Font del Regàs, a subhumid headwater These two types of primary producers contribute to decrease stream stream within the Montseny Natural Park (La Selva, NE Spain). nutrient concentrations, especially during the vegetative period. 29 MARKER PIGMENTS IN PALAEOLIMNOLOGY

akes are excellent ‘sentinels of In that context, the research we have change’ because they can pro- been conducting was initially focused vide insight into the effects and in the study of high mountain lakes mechanisms of global change in the Pyrenees and started with the Lthrough their sediments natural archi- development of new pigment-based ves. Broadly defined, palaeolimnology methods to reconstruct long-term is the study of the physical, chemical, changes in lake primary production. and biological information stored in At long time scales (i.e. from a few lake deposits using different indirect decades to millennia) the key element indicators, the so-called proxies. The controlling primary production in study of lake sediments, and specifica- mountain lakes is the coupling of lly the biotic and abiotic components lake dynamics with the catchment that integrate information from the biogeochemistry. Phosphorus is a scarce water column, catchment area, and at- element at those altitudes; therefore, mosphere, can help asses baseline con- it is efficiently retained by vegetation. ditions for different physical, chemical, The research conducted showed how BUCHACA, and biological systems (e.g., climate, sensitive those ultraoligotrophic lakes nutrients, ecosystem functioning), as are to a small increase in phosphorus TERESA well as the impacts of and recovery ti- loading and, on the other hand, how mes after disturbances of ecosystems. efficient in retaining phosphorus is the At CEAB vegetation-soil complex, when it is not Some of the most widely used bio- mechanically affected (e.g. catchment 2003 - Present logical proxies in palaeolimnological studies include pollen, diatoms, chry- Ph.D. Associate sophyte scales and cysts, plant ma- crofossils, cladocera, chironomids and organic geochemical proxies. Organic geochemical proxies are contained on the amount and composition of organic matter in lacustrine sediments and include among others, concentration and accumulation rate of organic carbon, Corganic/Ntotal ratio, composition of 13 15 δ Corganic and δ Ntotal and pigments of photosynthetic organisms. Higher plants, algae and microbes synthesize a variety of pigmented organic compounds for use in photosynthesis. Chlorophyll a is the most common, but aquatic plants have evolved caro- tenoid compounds that enable photosynthesis in the absence of the red wavelengths absorbed by chlorophyll a. Photosynthetic organisms have a cha- racteristic composition of pigments depending on the Division or Class where they belong which allows the utilization of pigments as taxonomical markers that may allow to infer the algal assemblages growing in the lake in the past.

Sediment record retrieved from Lake Redon (Central Pyrenees) covering the Holocene period. anthropogenic perturbations). poor lakes to increased nutrient loading, earlier for the likewise species-poor The wider knowledge of taxonomic introduction of non-native species, such alpine lake ecosystems. specificity and about diagenetic processes as fish, and climate change as shown All these studies rose up the issue of the involved made possible to extend the application of pigment-based methods to study trophic interactions in lakes that had been receiving an anthropogenic impact along the last decades and then we focused attention on lakes from the Azores Archipelago. With these studies we found that the composition of zooplankton, and microbial and algal assemblages changed rapidly after the perturbation, and the covariance between fish stocking, nutrient loading and enhanced temperatures captured most of the variability in algae accumulation, and thus likely in lake primary production as well. Our study demonstrated the sensitivity of these remote species- Field work in the island of Sao Miguel (Azores Archipelago).

Lake Furnas (Azores Archipelago). 31 References

Buchaca T, 2009. Pigments indica- dors: estudi del senyal en estanys dels Pirineus i de la seva aplicació en paleolimnologia. Institut d’Estu- dis Catalans.

Buchaca T, Catalan J, 2007. Factors influencing the variability of pigments in the surface sediments of mountain lakes. Freshwater Biology 52: 1365-1379.

Buchaca T, Catalan J, 2008. On the Sampling fish populations in Azorean lakes. contribution of phytoplankton and benthic biofilms to the sediment relative importance of climate change and by nutrient fertilization. The increase in record of marker pigments in high nutrient inputs. Whereas the cumulative cyanobacteria in areas most impacted mountain lakes. Journal of Paleo- impact of climate change on freshwater by anthropogenic change (lowland limnology 40: 369-383. ecosystems has been relatively gradual, regions with agriculturally developed Buchaca T, Skov T, Amsinck SL, the onset of modern agricultural watersheds) followed our hypothesis, Gonçalves VM, Azevedo JMN, practices and human-mediated changes however, we were surprised to see Andersen TJ, Jeppesen E, 2011. to atmospheric and hydraulic loads has that cyanobacteria also increased in Rapid ecological shift following certainly resulted in an accentuated numerous remote, alpine lakes. In these piscivorous fish introduction to nutrient signal in recent decades. Such relatively remote sites, the temperature increasingly eutrophic and warmer evidences suggested that the relative signal and atmospheric nutrient loading Lake Furnas (Azores Archipela- contribution of climate change and is likely to have played a more important go, Portugal): a palaeoecological nutrient inputs to lake ecosystems is role than run-off from agriculture or approach. Ecosystems 14: 458-477. a scale-dependent process. Therefore, point source nutrient enrichment. by considering data at spatio-temporal Skov T, Buchaca T, Amsinck SL, Lan- scales we examined larger gradients of Future directions in our research dkildehus F, Odgaard B, Azevedo climate and anthropogenic change, which interests point to enlarge knowledge J, Gonçalves VM, Raposeiro PM, allow for a broader generalization of the on ecosystem responses to climate Andersen TJ, Jeppesen E, 2010. response of temperate to subarctic lakes variability by looking for relationships Using invertebrate remains and to multiple stressors. This study provided between Late Glacial and Holocene pigments in the sediment to infer the first quantitative evidence across climate variability in Western Europe changes in trophic structure after north temperate to subarctic latitudes and changes in lake primary producer fish introduction in Lake Fogo - a that cyanobacterial expansion has been assemblages using marker pigments as crater lake in the Azores. Hydro- non-linear over time, disproportionate proxies in the sediment record. biologia 654: 13-25. relative to other algae and induced mainly Taranu ZE, Gregory-Eaves I, Leavitt PR, Bunting L, Buchaca T, Catalan J, Domaizon I, Guilizzoni P, Lami A, McGowan S, Moorhouse H, Morabito G, Pick F, Stevenson MA, Thompson PL, Vinebrooke RD, 2015. Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the anthropocene. Ecology Letters 18: 375-384.

In situ sediment core subsampling. 32 THE MICROBIAL BIODIVERSITY OF NATURAL ECOSYSTEMS

onservation biology is the ties among their daily worries and stra- scientific study of biodiversity tegic planning, beyond the concerns for oriented to protect species, pathogens. Threats on microorganisms habitats, and ecosystems from have been not considered as part of the Cunsustainable exploitation, uncontro- natural resources management policies lled extinctions and the increasing or in the estimation of the influence of weakening of biological interactions. human activities in nature. Microscopic Conservation biology involves the in- organisms have been therefore mostly teraction among apparently unrelated excluded in conservation studies. disciplines such as social and natural sciences, economics, and computatio- In the early 90s of the past century, nal and political sciences, among others, the International Programme of promoting integrative and transdisci- Biodiversity Science DIVERSITAS, a plinary views on ecosystem health and program promoted among others by aiming to formulate scientific basis for the International Council of Scientific CASAMAYOR, the best practices in natural resource Unions (ICSU) and now migrated to both management. Unlike with plants and Future Earth (http://www.futureearth. EMILIO O. animals, microscopic organisms have org/) and the Intergovernmental been mostly excluded in conservation Science-Policy Platform on Biodiversity studies and microbiology has developed and Ecosystem Services (IPBES), tried to At CEAB as a scientific discipline lacking of a natu- reverse this view highlighting the crucial 2003 - Present ral history background. Microorganisms role that microbial biodiversity plays in are however fundamental components the maintenance of many ecosystem to maintain the ecological integrity of services. The term ‘ecosystem services’ Director any ecosystem. Apparently, the study describes ecosystem resources Since 2014 of microorganisms lacks of naturalistic and processes that benefit human attractive and of conservation-orien- society, and its identification and value tated perspectives because of cells in- quantification can provide additional Researcher conspicuousness, low probabilities of arguments for the protection of species extinction, and potential widespread and ecosystems that could easily reach distribution. Therefore, environmen- public opinion and policy decisions. tal managers and lawyers, citizens, and DIVERSITAS emphasized the immense stakeholders in general have obviated genetic diversity of microorganisms the fate of natural microbial communi- and their crucial and unique roles as

Unknown extremophile microbes inhabiting a salt lake (salada) in Monegros. 33 basic components of food webs and ecosystem functioning, suppression taxonomic and functional diversity. biogeochemical cycles and ecosystem of diseases organisms, provision of They have successfully combined services, and included “microbial clean water through the respiration multidisciplinary approaches from biodiversity” within the nine fundamental of organic carbon, denitrification, and different scientific disciplines such as cross-cutting research themes of critical other metabolic processes, and to gain microbiology, ecology, biogeochemistry, importance for biodiversity science. The insights into the functioning and microbial molecular biology, bioinformatics and Microbial Biodiversity programme urged regulation of biogeochemical cycles. The computational science and have efficiently to develop innovative methods and programme also urged to explore major linked available information on microbial techniques to accelerate the discovery issues concerning the conservation, origin, diversity within a worldwide network. and characterization of microbial diversity, and maintenance of microbial biodiversity. This sustained effort circumvented some and to establish reliable databases In 2007, I was appointed as a member of of the methodological and conceptual to collect and exchange information the Spanish committee of DIVERSITAS concerns that had strongly limited the on the biological characteristics of to help to achieve some of the ambitious general perception of how important microorganisms. It was particularly aims of the international programme. For microbes are for Earth biodiversity and encouraged to improve the knowledge in the last 20 years, and mainly over the initiated the effective transplantation of freshwater microbial diversity to increase past decade, microbial ecologists have concepts and basic knowledge from the the available understanding of the developed, optimized and standardized general ecology grounded on plants and effects of microbial diversity on aquatic powerful methods to capture microbial animals to microbial ecology.

Sampling high-altitude Lake Redon in the Pyrenees in winter. Sampling a deep karstic lake in Central Spain.

Sampling an inland salt lake in Monegros. Sampling coastal salt ponds in the Mediterranean area. 34 Ponds, (iv) reactive biofilms in streams, (v) the Aerial plankton, (vi) Coastal and Marine Systems, and lately (vii) the Gut microbiome, to develop, improve and test methodologies and theories and to unveil the composition and functioning of the microbial component. Because of the high specific activity, abundance and versatility, microorganisms are primarily responsible for the main biogeochemical cycles, controlling rates of the chemical transformations. They also have a key role in the remineralization and the conversion of dissolved organic carbon in particles, and are also the main primary producers in much of continental aquatic ecosystems both by photosynthetic and chemosynthetic metabolisms. In fact, microorganisms are most abundant and most genetically and physiologically diverse living beings. They constitute a Artemia salina (0.5 cm length), one of the main microbial predators in the saladas of Monegros. large part of the global biomass with an evolutionary history present for In 2003, thanks to the Ramon y Cajal Change Ecology, (ii) Microbial processes more than 3/4 of the Earth history. The initiative of the Spanish Government and Biogeochemical cycling (mostly C, N, long interaction with the geological and the support of the Limnology group and S cycles), (iii) Microbial biogeography component has certainly promoted a headed by Professor Jordi Catalan, I and Global bacterial dispersal, (iv) Life highly sophisticated microbial biochemical joined the Center for Advanced Studies in in Extreme Environments, (v) Molecular machinery. Blanes and launched the current Microbial Ecology and Evolution, and (vi) Data Ecology team, pionnering some of the mining, Metagenomics and Ecoinformatics. Currently, most of our field research is above mentioned issues for more than carried out in three freshwater inland si- 12 years already. The team has carried We used a wide array of environments tes: out research activities under different and natural model systems such as (i) research topics for instance (i) Microbial Sulfurous and Karstic lakes, (ii) Alpine (i) the Limnological Observatory of the Ecology, General Ecology, and Global and Polar areas, (iii) Saline lakes and Pyrenees (Spanish version here) (LOOP)

Cold, wet and misty in the winters of Monegros. 35 a LTER site within the National Park of Aiguestortes i Estany de Sant Maurici focusing on the microbial ecology of an alpine lacustrine district and interconti- nental airborne bacterial dispersal

(ii) the protected area of Monegros De- sert looking at the microbial ecology of shallow saline lakes (RAMSAR site “Saladas de Sástago-Bujaraloz”) and the dynamics and adaptations of microbial communities to frequent environmental stress and highly dynamic ecosystems

(iii) the karstic area of Lake Banyoles (RAMSAR site) studying the microbial ecology of anoxic and sulfurous (euxinic) environments as a proxy to infer past Earth conditions

We use powerful molecular biology tools on microbial physiology and ecosystem processes to link microbial biodiversity and biogeochemical cycling studies, especially for chemoautotrophic prokaryotes, archaea and the nitrogen and sulfur cycles. Our approach ranges from gene to ecosystem and from single cell physiology to emerging ecological patterns. We are also looking for ecological thresholds for microbial diversity distribution along environmental gradients and for the bridges between the ecology of macroorganisms and microorganisms, addressing questions regarding spatial and temporal patterns of microbial diversity, community ecology, functional diversity, microbial dispersal, and community assembly. We are also interested in examining the response of aquatic bacterial communities to global ecosystems change especially in highly sensitive high mountain lakes areas as early warning systems of global processes and in the exacerbated interactions of microbes with the nitrogen cycle. Finally, we look at the microbial metagenomics data using statistical and theoretical approaches of General Ecology within an Looking forward to unveil new microbial secrets. evolutionary framework.

Despite this successful research period, and classified in relation to each other with strong ecological and evolutionary microbial ecology is still in its infancy enabling the fast and proper universal background such as zoology and botany, predicting microbial species distributions communication among microbial should not be an unbeatable barrier across landscapes, understanding why ecologists, a high-quality census needs anymore. In fact, microbial systems may some areas have high or low species still of methodological improvements. push forward traditional disciplines and richness, or highlighting whether or Genomes and metagenomes currently theoretical ecology to new unexplored not vulnerable groups of microbial available are growing exponentially and frontiers. The Center for Advanced species or microbial processes exist, single cell genomics and in silico genome Studies of Blanes has the potential to missing useful information for land reconstruction permits to reach the successfully achieve this goal. and ecosystems management. There genetic potential of a microorganism is considerable biodiversity to be without culturing. The inadequacy of explored yet and although microbes can methods and conceptual separation currently be reasonably well identified of microbiology from natural sciences 36 INVASIVE SPECIES IN A CHANGING SEA

he Mediterranean Sea can be understanding of the spatiotemporal considered one of the hottest range and magnitude of these impacts hotspots of marine bioinva- remains critically poor. sions on earth (Rilov and Ga- Tlil 2009). It probably hosts the greatest It is accepted that main processes de- pressure of introduction vectors in the rived from climate warming and invasi- oceans: Suez Canal, intense maritime ve species interact simultaneously in a traffic and aquaculture. High anthropo- complex manner. The success of an in- genic pressures besides a high variabi- troduced species in getting established lity of environmental conditions makes and behaving invasive often depends the Mediterranean a region particular- on how suitable climatic parameters ly prone to marine bioinvasions and a are in the region of introduction. For special site for studying the main pro- example, global warming is claimed to cess involved in biological invasions. promote the spreading of alien species CEBRIAN, (Walther et al. 2009); however, this However, invasive species are by no would not apply for cold-affinity spe- EMMA means the only problem threatening cies (e.g. Womersleyella setacea; Ce- marine diversity. Climate change is brian & Rodriguez Prieto 2012). Ph.D. Associate also impacting on marine environ- 1997 - 2015 ments worldwide and the Mediterra- Likewise, some studies suggest that ha- nean Sea does not escape from this bitats degraded by global warming are global trend. Moreover, climate change more likely invaded than nearly-pristi- can cause impacts both directly, as well ne habitats, envisaging explicitly or not, as synergistically with invasive species a cause and effect link between climate

Lophocladia Iallemandii, invasive filamentous red algae in the Mediterranean Sea, the Red Sea and the Indo-pacific zone.

(Cebrian et al. 2012). Given the spread warming and the success of biological of invasive species throughout the Me- invasions (e.g., Bianchi 2007, Galil et al. diterranean and the projected trajec- 2007, Occhipinti-Ambrogi, 2007, Sta- tory for climate change in this region, chowicz et al. 2002). However, results the likelihood of further negative im- arising of some empirical systems do pacts on native biological diversity is not support this idea (Verdura et al. high. Despite this looming disaster, our 2015), but reveal instead conflicting re- 37 sults that have provoked intense debate. promote, or in contrast limit, habitat (Cebrian & Ballesteros 2009, 2010). We’ve shown that the synergy of both invasibility. Once an exotic has been Consequently, one aspect that deserves perturbations may lead to further introduced, resistance to invasion greatly further investigation is whether more di- indirect but dramatic consequences on varies among recipient assemblages verse communities should be less suscep- the persistence of populations that have (Levine & D’Antonio 1999; Lonsdale 1999; tible to invasion or not. The contrasting already been affected by global warming Kennedy et al. 2002). Some studies have patterns found between studies may be (Cebrian et al. 2012; Linares et al. 2012; investigated native ecosystems features partially driven because almost all mani- De Caralt & Cebrian 2013). We’ve also (biodiversity, or direct competitors of pulative diversity-invasibility experiments been aware of the dramatic decline invasives) determining the susceptibility carried out so far in marine environments of many key species in shallow water to be invaded. We have reported the have used small, simple model systems, Mediterranean habitats (Ballesteros 2009; limited role of the native herbivorous mostly early successional aquatic micro- Cebrian et al. 2011), which could facilitate sea urchin Paracentrotus lividus to resist cosms (e.g. Stackovicz et al. 1999; Stac- the spread of invasive algae thriving in the Caulerpa cylindracea invasion (Cebrian et kowicz & Byrnes 2006; Marrafini & Ge- same habitats (Cebrian and Ballesteros, al. 2010), and the uncertain role of Salpa ller 2015). There is increasing concern if 2009, 2010; Cebrian & Rodríguez-Prieto salpa (Tomas et al. 2011), but further the results from these experiments can 2012; Linares et al. 2012; Cebrian et al. experimental studies are needed to be generalized in mature systems with 2012) and provided an striking example of elucidate which factors provide resistance complex community structure such as climate-mediated range shifts of invasive to macroalgal invasions to the native forests. species into temperate seas (Vergés et al. assemblages. Theory suggest that healthy 2014). and diverse ecosystems, as those attaining To know how diversity in marine com- Good Environmental Status, improve plex communities may prevent alien inva- However, one challenge that arises for both the resistance and the resilience of sion, or in contrast, if habitats less diverse managing marine environments in the face native ecosystems to climate change and (as those probably already affected by of climate change and biological invasions bioinvasions, but no MPAs, for instance, climate change) are more vulnerable to is to study why some habitats are more where healthy benthic ecosystems are invasions is for us a priority. likely to be invaded than others (habitat thriving, can stop the blooms of the invasibility) and how global warming may invasive algae once they are introduced

38 Caulerpa cylindracea, a very aggressive invasive algae very extended across the Mediterranean sea, originally coming from Australia. BENTHIC SUSPENSION FEEDERS AS INDICATORS OF THE EFFECTS OF GLOBAL CHANGE ON LITTORAL ECOSYSTEMS

n a world rapidly affected by All these definition are of interest global change, many organisms within the context of understanding and communities are responding the effects that the dynamics of through changes in abundance an species can have on an habitat, Iand distribution. In the marine realm, especially if the factors that affect an habitat alteration and climate change species dynamics become substantially are among the main factors affecting modified by environmental climate the functioning of the organisms. In change. The first one because it this context, species invasion are re- includes the species most usually cognized as a major problem causing considered when addressing the effects large modifications on ecosystem of invasive species. The second one COMA, structure and function. The main con- because some native species exhibit a cern is how these changes are going to behaviour of rapid population growth RAFEL affect the services that marine ecosys- that can be defined as invasive (native tems provide to us (food, climate and outbreaks). The third one because Scientist natural hazards regulation, nutrient cy- the widespread occurrence of these 1996 - Present cling, nursery, commercial and recrea- species represents a potential for a tional activities...). behavioural change from harmless to harmful in the habitat. Several definitions of invasive species can be considered if a geographic Attenuation of climate change requi- (introduced-native) and an impact res the involvement of all major coun- criteria (harm-no harm) are used. tries, an issue that takes time due to From a narrow to a very broad political and economic implications. definition, invasive species can be Meanwhile, there is an urgent need for defined as those introduced species clear indicators of the rate of change that affect an habitat or region, as related to warming and other human those introduced or native species activities. To contribute understanding that affect an habitat or, as those of the rate of change of the marine widespread introduced species ecosystem, the factors, the processes currently harmless to native habitats. and the mechanisms involved. We fo-

Figure 1. In situ long-term examination of demographic parametres of a coral species. 39 At present, the coral species Oculina pa- tagonica appears as among the dominant species most clearly responding to the main global change alterations. The species has recently been exhibiting an invasive behavior with a drastic increase in abundance and distribution that affects the most productive Mediterranean benthic community, the shallow photo- phillous infralittoral. Our current investigation focus on the study of this coral species in order to determine its rate of change, the main factors that are affecting this rate, the processes that are been affected from this dominant species and the involved mechanisms. To this end: a) Figure 2. Field trip on SCUBA along the Mediterranean coast to assess population status field examination of labeled colonies and of indicator species. areas on multiple sites and conditions is been conducted in order to determine cus on the study of indicator species that of the population dynamics of indicators recruitment, survival and growth (Fig.1); can be considered as representative of species is crucial to distinguish change b) field surveys are been regularly perfo- the main dynamic of the community. The from natural oscillations. med along the Mediterranean littoral of demographic parameters are the main the Iberian peninsula to examine changes determinants of the fluctuations of a po- Our research concentrates on the study in abundance and size structure of the pulation. The study of their variability and of suspension feeder indicator species populations (Fig. 2); c) field experiments of the main factors that drive them is fun- that are important contributors to the are been conducted; and d) experimental damental to distinguish natural fluctua- structure, functioning and/or biomass of studies of different hypothesis are been tions from those induced by anthropoge- different sublittoral benthic communities tested on aquaria to determine cau- nic stressors. Then, the long term study such as gorgonians, sponges and corals. se-effect relationships (Fig. 3).

Figure. 3. Experimental hypothesis testing on aquaria of cause-effect relationships. 40 AQUATIC PLANTS AND WETLAND ECOLOGY

quatic plants are organisms and physico-chemical variables that secondarily adapted to living we use both for management and in aquatic environments. conservation studies as well as They can be ferns or for niche modelling. Our group is Aflowering plants and require special pioneer in detailed mapping of plant adaptations for living submerged in communities in lakes which allows water, or at the water’s surface. They upscaling any lake function mediated by are often referred to as macrophytes macrophytes (e.g. nitrogen emissions, when including macroalgae. Ecologically, carbon balance) at the ecosystem level. they are key elements of water bodies Long term monitoring of this flora has such as estuaries, wetlands, stream allowed unique studies of resilience riparian zones, ponds, shallow lakes and recovery of endangered species and also marine coastlines, where in front of perturbations. Current they can cover huge areas. By having research focus is on conservation of aquatic plants as model organisms our species and ecosystems threatened GACIA, research group uses disciplines such as by climate change, habitat loss and community ecology, functional ecology, introduced fish species. Our large ESPERANÇA ecophysiology, biogeochemistry, biodiversity and environmental data genetics and modelling to answer set is being used for meta-ecology Scientist target environmental questions for studies at regional and global scale 1993 - Present aquatic ecosystems in front of global in collaboration with scientists from change. We base most of our research abroad. in fieldwork that we approach both observationally and experimentally. Ecological functions of seagrass MAIN FIELDS OF EXPERTISE: meadows

Aquatic plant community ecology The functioning of seagrass ecosys- in shallow lakes tems is also a focus of research. Sea- grass meadows are pivotal structural Most of our research is being conducted and functional elements in coastal in the littoral of shallow lakes and waters and we have developed tools ponds with particular attention to to assess the capacity of seagrasses Pyrenean flora. We have gathered a (mainly Mediterranean Posidonia ocea- large (> 200 water bodies) data base nica) to attenuate erosion, retain se- on macrophyte species presence diment and control biogeochemical

Figure 1. Isoetes lacustris L. at 5 m in Estany de Cabanes, National Park of Aiguestortes, Pyrenees (©EBallesteros). 41 cycles in the littoral. We have also con- have found that some ponds, temporary same tool has proven useful for studying tributed to gain knowledge on the role pools and the less abundant karstic physiological aspects of nitrogen use in of seagrass ecosystems in the carbon ba- lakes are the systems most affected by aquatic plants such as nitrogen uptake lance in tropical and temperate meadows. human pressures. We also confirmed that and retention. We are also expanding the We currently work on the role of sea- this area is a hotspot for macrophyte potential of aquatic plants as indicators grass meadows as biodiversity hot-spots biodiversity because of the diversity of of human perturbations to wetland as well as on the use of associated meso- water body typologies (i.e. karstic lakes, species exposed to metal pollution. grazer communities to assess ecosystem reservoirs, alpine lakes, ponds, temporary We have worked in paddy fields, heavily quality. ponds, meanders) and the Mediterranean impacted water bodies, and recently at weather. We also confirmed that the Urban River Laboratory, an open Macrophytes as indicators of anthro- biodiversity of aquatic plants is threatened air flume system working at the outflow pogenic stressors mainly because of water scarcity of a wastewater treatment plant. In this and habitat loss (mostly temporary facility we aim at improving the quality Species community composition has long pools). Our group also explores water of grey water (outfall of the treatment been used as an indicator of water quality quality (i.e. eutrophication) in riverine plants) before entering streams in order in continental stagnant water bodies. In macrophytes by using other indicators, to improve water and ecosystem quality Catalonia we have conducted extensive such as the nitrogen stable isotopic in our heavily perturbed streams. macrophyte and water quality surveys and signal of the plants themselves. The

Figure 2. Reeds in the Natural Reserve at Flix reservoir, Ebro river.

References

Chappuis, E.M., Gacia, E., Ballesteros, E. 2011. Changes in aquatic macrophyte flora over the last century in Catalan water bodies.Aquatic Botany 95:268-277. Chappuis, E.M., Ballesteros, E., Gacia, E. 2012. Distribution and richness of aquatic plants across Europe and Mediterranean countries: patterns, environmental driving factors and comparison with total plant richness. Journal of Vegetation Science 23(5): 985-997. Gacia, E., Marbà, N., Cebrián, J., Vaquer-Sunyer, R., Garcias-Bonet, N., Duarte, C.M. 2012. Thresholds of Irradiance for seagrass (Posidonia oceanica) meadow metabolism: An experimental approach. Marine Ecology Progress Series 466, 69-79. Peipoch, M., Gacia, E., Pastor, A., Ribot, M., Riera, J., Sabater, F., Martí, E. 2014. Intrinsic and extrinsic drivers of autotrophic N cycling in stream ecosystems: Results from a translocation experiment. Limnology and Oceanography 59(6):1973-1986. Soto, D.X., Roig, R., Gacia, E., Catalan, J. 2011. Differential accumulation of mercury and other trace metals in the food web components of a reservoir impacted by a chlor-alkali plant (Flix, Ebro River, Spain): implications for biomonitoring. Environmental Pollution 159:1481-1489. Vila-Costa, M., Pulido, C., Chappuis, E.M., Calviño, A., Casamayor, E., Gacia, E. 2015. Macrophyte landscape modulates lake ecosystem-level 42 nitrogen losses through tightly coupled plant-microbe interactions. Limnology and Oceanography DOI 10. 1002/lno.10209. ADVANCES IN KNOWLEDGE ABOUT THE ATLANTIC BLUEFIN TUNA’S SPAWNING BEHAVIOUR

he Atlantic Bluefin Tuna is a capture fishery and the tuna caught in singular and emblematic spe- the Balearics are transferred to tuna cies given its physiology, its transport cages which are transported migratory behaviour and its and transferred to the fish farm Thigh economic value, which is why it facilities in L’Ametlla de Mar. So the has been investigated by many research “where” was the tuna transport cage groups. Nevertheless, until seven years and the “when” was while travelling to ago absolutely nothing was known the farm. about its spawning behaviour. This is where the CEAB reached a milestone We designed a fishing mechanism to worldwide as it was the first centre to collect plankton from the front and determine this species’ reproduction. rear of the tuna transport cage, and samples were collected day and night The triggering factor behind this re- during the 8-day voyage. It worked: the GORDOA, search line was casual as result of lis- result was the mass collection of eggs tening stories and checking their truth- at night from the rear of the cage. This ANA fulness. Was all of that happened while was how the spawning of the Atlantic chatting with the master of a tuna pur- Bluefin Tuna was determining for the Scientist se seiner, he told us: “whon full moon first time, and was later filmed in the 1992 - Present nights, tuna suddenly stop, and they do ULTIMATUN documentary. to spawn because I´ve seen a huge mi- lky stain covering the surface of the Since then, tuna transport cages have sea”. That’s how it all started, we wan- become experimental platforms which ted to verify what he said, and then set have allowed us to study in depth the up the experimental design machinery: spawning behavior of bluefin tuna. Where? When? How? Since 2009, in the framework of a re-

Bluefin tuna (Thunnus thynnus) in the Mediterranean Sea, an emblematic species fished for centuries. The setting up on where and when search and contract with the Balfegó was opportunistic, based on existing Group, around 600 tuna spawners are fishing facilities. The L’Ametlla de Mar transported to waters south off Ibiza, tuna purse seiners catch tuna in the which is a round trip from l’Ametlla Balearics exploiting the tuna spawning de Mar. The spawning behavior of this aggregations which occur in late group is monitored nightly for 2 mon- spring and early summer. This is a live- ths. 43 This monitoring has allowed us to learn fixed cages. The CEAB presents annually different reproductive aspects: when at the International Commission for the the spawnning peak takes place (around Conservation of Atlantic Tunas (ICCAT) eferences St. John; 23rd June); the timing pattern the catch rates of the purse seiners R (between 02:00 a.m. and 05:00 a.m.); the fleet in the Balearics grounds, along with consequences of such behaviour; the the size and ages structure. Gordoa, A, Olivar, MP, Arévalo, R., Viñas, J., Molí, B., Illas, X. 2009. Determination of Atlantic bluefin tuna (Thunnus thynnus) spawning time within a transport cage in the western Mediterranean. ICES Journal of Marine Science. 66, 2205-2210.

Ultimatún (2011) Documentary produced by Fernando López-Mirones (ORCAFIL- MS and New Atlantis). www.ORCA-FILMS. com.

Gordoa, A. Carreras, G. 2014.Determina- tion of temporal spawning patterns and hatching time in response to temperature of Atlantic Bluefin tuna (Thunnus thynnus) in the Western Mediterranean. PLoS ONE 9(3):e90691.doi:10.1371/journal. pone.0090691. Ana Gordoa is interviewed by a Spanish TV channel on her work on bluefin tuna. Gordoa, A., Sanz, N., & Viñas, J. 2015. Indivi- individual spawning duration (some 30 We encountered different problems dual Spawning Duration of Captive Atlantic Bluefin Tuna (Thunnus thynnus) Revealed by days); the effect of atmospheric instability while investigating on transport cages, Mitochondrial DNA Analysis of Eggs. PloS on spawning (it can inhibited for a few problems which have actually become one, 10(8), e0136733. days); the hatching and its acceleration study elements. Mass presence of Pelagia with temperature (from 45h. to 23h.). noctiluca jelly fish juveniles proved an Gordoa, A. 2010. Temporal pattern of daily Moreover, the implemented fishing inconvenience for spawning sampling CPUE on the bluefin tuna(Thunnus thynnus) mechanism is currently used to collect as they clogged sampling nets. Did they in the western Mediterranean spawning eggs for culture. also impact on tuna offspring? Were area. Collect. Vol. Sci. Pap. ICCAT, 65(3): 828- they able to ingest tuna eggs despite 836. Beyond this species biology, we have their small size? Gordoa, A. 2015. Catch rates and catch also investigated its fishery from the structure of Balfegó purse seine fleet in Ba- eco-efficiency perspective to annual We are currently attempting to answer learic waters from 2000 to 2014; two year variations in fishing efficiency. These these questions. The experimental of size frequency distribution based on vi- results, along with the spawning results showed their voracity, and gave deo techniques. Collect. Vol. Sci. Pap. ICCAT. 71 behavior results, have enable to provide the highest ever rates observed for (4): 1803-1812. advice about the optimum fishing period juvenile jellyfish stages (0.3 – 1.3 cm). for fishing sustainability purposes, which We continue with this research line Gordoa, A. 2010. An indirect Approach to acts as the basis for some modifications in order to estimate its impact on the estimate the Fattening Factor of Atlantic Bluefin Tuna (Thunnus thynnus) on Tuna Far- made to its regulation. Atlantic Bluefin Tuna’s offspring success. ms: Ametlla de Mar Facility as a Case Study. Collect. Vol. Sci. Pap. ICCAT. 65 (3):848-857. In the next phase: from the fishery to This research requires an infrastructure the farm, with research carried out (transporting fleet, tuna, ships, feeding Gordoa, A., Acuña, J. L., Farrés, R., & Bacher, in the growth and fattening of tuna in at high sea, etc.) that is only available K. 2013. Burst Feeding of Pelagia noctiluca captivity. Until 2013, the fattening factor in the tuna purse seiner fishing and ephyrae on Atlantic Bluefin Tuna (Thunnus was basic to estimate the weight of farming sector, without their active thynnus) Eggs. PloS one, 8(9), e74721. tuna fish on the date they were caught. collaboration this work would not be Gordoa, A., Carreras, G., Sanz, N., & Viñas, Nowadays, the size of caught specimens possible. J. (2017). Tuna Species Substitution in the can be known thanks to the stereo Spanish Commercial Chain: A Knock-On cameras, which measure tuna when Effect. PloS one, 12(1), e0170809. transfered from transport cages to SPONGES: UNCONVENTIONAL ARCHAIC ANIMALS UNDER MODERN EVOLUTIONARY AND BIOTECHNOLOGICAL PROSPECTS

ponges make the phylum Po- tablishing homology and equivalence rifera, regarded to be —not to tissues and organs of other animals. without controversy— the oldest lineage among the living The structural and functional Sanimals. They are unconventional ani- uniqueness of the sponge body mals. In exhibition halls and aquaria, favoured these organisms to be sponges often disappoint to non-spe- initially considered multicellular cialist audiences anger for excitement, protists related to choanoflagellates, because they are sessile organisms rather than animals. Only at the very that do not display noticeable body end of the 19th century were sponges behaviours. They lack muscles, sensory re-interpreted as animals, because organs, nerves, and any coordinating spermatozoa and oocytes —the MALDONADO, neural centre, performing slow body cells that all animals use for sexual movements that can only be percei- reproduction— were discovered MANUEL ved through time-lapsed systems or in some species of the group. Even alike approaches. They also lack mou- after the gametes clearly pointed Researcher th and anus, and even a digestive tube. sponges to be animals, zoologists 1989 - Present There are neither respiratory nor di- were not prone to thinking of these gestive systems for oxygen and food weird organisms as “real” animals and processing, and excretory organs for erected the subkingdom “Parazoa” elimination of metabolic wastes and to segregate sponges from the rest detoxification are lacking as well. Cells of “real” animals (i.e., subkingdom have to deal individually with oxygen, “Eumetazoa”). This condition of “para- food, and wastes, sometimes by me- animals” lasted virtually for the entire chanisms that are unique in the animal 20th century. The advent of molecular kingdom. techniques in the 21st century has doubtlessly proved that sponges have Certainly, the extreme anatomical animal genomes and, surprisingly, simplicity of sponges has troubled bio- less unconventional than expected. logists of all epochs at the time of es- For instance, sponges posses the

Monospecific sponge ground made by a dense population of the hexactinellid Sericolophus hawaiicus at 400 m deep on the continental slope of Kona Island (Hawaii, USA). 45 same repertory of neural genes than additional mystery, some of which provi- ted by the activity of a complex universe ctenophores, a group of predatory de them with biotechnological appeal. Be- of microbes, including archaea, bacteria, swimming animals that comparatively cause lacking organ systems, their physio- cyanobacteria, dinoflagellates, diatoms, display plenty of coordinated movements logy must run by “alternative” pathways. and fungi, among others. After three and behaviours. Why sponges decades of chemical trials, do not express those neural sponges rank at the top genes and persist as inert- among the organisms pro- like, behaviour-less animals ducing chemical compounds remains both a mystery and a with potential biological and stimulating scientific challenge. pharmaceutical interest. To The good news are that date thousands of singular sponge genomes are now bioactive molecules have becoming a hot subject. They been isolated from spon- are thought to treasure pivotal ges, being still unclear which information to understanding of them are produced by the evolutionary transition the sponge cells themsel- from the putative unicellular ves, the microbes hosted by protist ancestor to the the sponges, or a combined multicellular level and organ action of both. After the systems characterizing animals. initial thrill of discovering a In just a few decades sponges promising therapeutic drug, have therefore gone from being the problem shifts to how an almost ignored animal group Picture taken by high field emission scanning electron microscopy, showing obtaining it in large amounts that received little scientific two of the millions of aster-like spicules that constitute the siliceous for further developing the as- attention to be radiant stars at skeleton of the demosponge Chondrilla caribensis, collected from Lee says and trials and, if needed, the vortex of an international Stocking Island (The Bahamas). commercialization. Man-ma- multi-laboratory battle to de chemical synthesis is often crack the secret of the origin of animals. It is believed that it results in an intricate either unachievable or unaffordable. Mas- and not yet well-understood network of sive collection of sponges from the field Yet sponges posses more singularities and metabolic and cellular steps, often assis- is neither sustainable nor possible. For

Diver taking pictures of sponges at the sublittoral of the Chafarinas Islands (Spain). 46 Individual of the keratose demosponge Ircinia fasciculata, monitored as part of a study investigating events of massive mortality in this species apparently triggered by a unresolved combination of pathogens and global warming. instance, it has been calculated for a compound of interest that by collecting to extinction the entire world population of its source sponge, the obtained amount of compound would not be enough to complete the tests for the pre-clinical trial of the drug and, consequently, there would be nothing left for commercialization. For the past 20 years, research grants aimed to find a solution to this “supply problem” have eco- nomically sustained a myriad of laboratories worldwide, pur- suing to produce large amounts of sponge compounds by culturing sponges, sponges cells, and sponge microbes. So far, none has been successful. The “supply problem” remains as a major factor preventing rapid development of new marine drugs, as well as a major scientific and biotech challenge.

More recently, other elements of the sponge body have attracted biotechnological interest: their bones! Again, unlike in most other animal groups, the bones of most sponges, called spicules, are not based in the metabolism of calcium. In contrast, they have transparent, glass bones, made of silica (Si

O2), which is virtually the same material used in windows and mirrors. To form their skeleton, the silica is polycondensed (silicification) within the sponge body using the dissolved silicic acid available in seawater. The process is controlled by an enzyme called silicatein, which, as far as it is known, is exclusive to sponges. It was long known that mammals’ bones experience slight silicification during its early growth, particularly long bones, such as the femur, the head and neck of which require trace deposits of silica for a regular View of the manned submersible “Piscis V” from the University of Hawaii development. Recent biomedical research has demonstrated ready to be launched (with Dr. Craig Young and Dr. Manuel Maldonado that mammal bone fractures heal comparatively faster if inside) to investigate a bathyal population of hexactinellid sponges at sponge silica dust is injected in the bone injure. The results Kona Island (Hawaii, USA). 47 ty in environmental sciences. Although some sponge species are seasonal, most sponges are long living, with life spans that range from decades, to centuries and even millennia. Their bodies are therefore living archives that can potentially testi- fy about major changes in the concentration of heavy metals, organo chlorine pesticides, and other sublethal pollutants in aquatic systems. Although a comprehensive protocol for a routine universal use of sponges as bioindicators is still to be developed, the few available studies indicate that sponges are great accumu- lators of a wide variety of compounds associated to the rising of industrialization of human societies. A calibration system to quantitatively translate the message of their accumulating activity is the only missing piece for their application as reliable bioindicators. Histological section of an embryo brooded by the coral excavating sponge Thoosa mismalolli as part of a study on coral destruction in reefs of the Mexican Pacific. Sponges have also attracted interest for their potential to deal with organic pollution. A sponge is able to filter thousands of litres of water through its body daily, retaining virtually 100% of the bacteria, cyanobacteria, and the phytoplankton smaller than 10µM, which makes the base of the sponge diet. Such an amazing filter-feeding capacity can be used to alleviate the charge of bacteria and toxic microphytoplankton from waters where sewage pollution or red tides can be a problem (aquaculture farms, closed bays, etc).

The above handful of examples illustrates the interest that the primitive and simple sponges can have for biotechnology, material science, and engineering. It happens that during the past 30 years, the Centre for Advanced Studies of Blanes (CEAB- CSIC) has seeded a slowly growing group of sponge experts. In its origin, the pioneering bet on sponges - at that time a group of organisms with neither much Community of tropical marine sponges dominated by Tedania ignis (fire sponge) andHalicondria “scientific glamour” nor biotech interest bowerbanki growing on the roots of red mangrove tree at Twin Cays (Belize). - was risky, with mistrust that it could lead to a high competitive scientific ca- rrier. At the CEAB’s 30th anniversary, it even improve when the bone wound is material, the micro-arrangement of is to celebrate that, in the long run, with treated directly with the silicatein enzyme. nanometre-thick concentric silica layers much hard work and some good luck, the The use of sponge silicatein is therefore that conform the spicules appears to “sponge bet” has brought back to the sparking a new generation of therapies be very suitable for efficient multimodal CEAB a good deal of national and inter- for regeneration of bone fractures. light transmission with insignificant losses national recognition. The CEAB’s sponge of intensity and wavelength. Both the research has renowned international re- The sponge silica is also in the spotlight cytological process of silica production putation, being their sponge experts con- of optical research. During the biological and the internal ultrastructure of sulted and supported by major funding process of silicification, the sponge spicules are now under close scientific agencies and research institutions world- cells select against the heavier isotopes scrutiny, becoming inspirational sources wide. Happy anniversary to the CEAB of silicon, yielding an isotopically light for the formulation of a new generation and its long standing commitment to the silica. This high-purity material behaves of materials for led, optic fibre, and sponges. as an efficient optic fibre during light semiconductor elaboration. 48 transmission. Besides the purity of the Sponges have also potential applicabili- GLOBAL CHANGE EFFECTS ON STREAM BIOGEOCHEMISTRY

uring more than two decades, dered as nutrient retention hotspots research in our team, included within the fluvial networks. We have in the Integrative Freshwater also been able to quantify particular Ecology Group at the CEAB, processes associated with nitrogen cy- Dhas focused on understanding how cling (assimilatory uptake, nitrification in-stream biogeochemical processes and denitrification) at whole-reach contribute to regulate the nutrient scale and how nitrogen from stream inputs from adjacent catchments and water is transferred into stream food what are the controlling factors and webs. These studies highlight the high mechanisms involved on nutrient bioreactive capacity of streams. Never- cycling along the river networks. In theless, this capacity is highly variable particular, we have focused on the among streams and over time within study of biogeochemical processes a stream. This variability is influenced associated with the cycling and by environmental factors, such as nu- transport of bioreactive elements (i.e., trient availability, discharge and water MARTÍ, carbon, nitrogen and phosphorous). residence time, as well as by the stream Availability of these elements can be metabolism (gross primary production EUGÈNIA a limiting factor for the ecosystem’s and respiration), which dictates the nu- productivity, but at the same time, an trient demand by in-stream biota. Scientist excess of them can cause pollution and 1999 - Present eutrophication problems. Ultimately, Global change encompasses changes our research contributes to assess in climatic conditions (temperature factors controlling the water quality and water availability) and in land uses of streams and rivers, which it is an within the catchments derived from important issue since human activity human activity. The consequences of depends on the quantity and quality of these changes on the ecosystems; this freshwater resource and in particular, on the quantity and quality of freshwater resources, are Our research in relatively pristine of current social concern. Most of headwater streams has shown that the streams draining catchments in they can contribute to retain 50% of the Mediterranean region are highly nitrogen inputs from their adjacent modified by land use transformations, catchments; and thus, they are consi- which affect the hydrology, channel

Permanent stream in Santa Fe del Montseny (c. 1000 m.a.s.l), in winter. 49 morphology and chemistry of the streams, Within this context, we have examined which can decrease the potential lethal and in turn, alter their metabolism and the effects of urban activity; in particular, effect of this nitrogen form on stream nutrient retention capacity. For instance, the effects associated with point sour- biota. In contrast, lack of nitrate removal nutrient retention efficiency is lower in ces from wastewater treatment plant along the receiving streams suggests that the denitrification capacity is limited, despite conditions for this process (i.e., low oxygen concentration and high availability of dissolved organic carbon) seem to be optimal. This results in a net export of nitrate from these streams with further implications for downstream ecosystems. In this sense, our current research focuses on understanding factors that may control denitrification in WWTP-influenced streams. The working hypothesis is that, despite inputs from effluents are rich in dissolved organic carbon; the quality of this carbon source may limit its use for denitrification in receiving streams.

Considering that WWTP effluents are also sources of microbes, among them pathogens, another question we are currently addressing is to estimate how pathogens persist along the receiving Intermittent stream in Arbucies (c. 200 m.a.s.l.), under summer drought conditions. streams and how this is related to the biogeochemical reactivity of these streams receiving high nutrient loads (WWTP) effluents on streams. Despite ecosystems. Results from this research derived from human activity. In addition, technological advances in WWTP opera- have implications not only for ecosystem we have found that land use changes tion, effluents constitute a source of nu- health, but also for human health. To not only increase stream water nutrient trients, emergent pollutants and microbes experimentally address these questions, concentration, but, in the case of to streams, which generate abrupt physi- over the past year, our research team, nitrogen, they can also modify the relative cal, chemical and biological discontinuities in collaboration with UB and Naturalea proportion of nitrate and ammonium. along the stream continuum. These dis- members, has built the Urban River continuities reduce the efficiency of nu- Laboratory (http://www.urbanriverlab. While diffuse inputs from agricultural trient retention and increase ecosystem com). This is an open-air research platform activity increase stream water nitrate respiration in receiving streams. However, consisting of 18 flumes (12 m long and concentration, point source inputs from remarkable inputs of ammonium from 60 cm wide), which receive inputs from urban activity tend to increase ammonium WWTP effluents are effectively reduced a WWTP effluent. This research platform concentration. These two dissolved within relatively short stream distances is fully supported by a local water inorganic nitrogen forms can undergo (i.e., few hundreds of meters). These lon- management agency (Consorci per a la different biogeochemical process; and gitudinal changes are coupled with increa- Defensa del Conca del Riu Besòs), which thus, changes in their relative proportion ses in nitrate, suggesting a dominance of manages water resources (quantity and affect the in-stream cycling and ammonium transformation rather than quality) in the Besòs catchment. downstream transport of this element. uptake. In addition, we have observed that Overall, results indicate that ammonium abundance of ammonia oxidizers (both Ultimately, we expect that research from is more biogeochemically reactive bacteria and archaea) is higher in recei- this platform will contribute not only to within the stream, while nitrate is more ving streams; probably because inputs of generate basic research knowledge, but subjected to downstream transport. these microbes from WWTP effluent are also to provide insights that may help able to colonize the substrata of receiving stakeholders to develop management Urban areas are dominant landscape streams. strategies to both preserve stream components of catchments in the Medi- ecosystem’s integrity and improve the terranean region; and forecasts for global Together these results indicate that quality of freshwater water resources for population dynamics point at a higher streams receiving inputs from WWTP humans. concentration of humans in urban areas. effluents are hotspots of nitrification, 50 1998 – 2015: THE WORLD SYMBIOTIC POLYCHAETES REVISITED

he information on symbiotic 1998, and compared the results with polychaetes was scattered those compiled this year. The result among different types of li- proves a significant increase in the terature and it was not until number of known symbiotic polychae- TMartin and Britayev (1998) that an ex- tes: almost 60% more species (582) haustive analysis was done. This review and relationships (1530) are current- included more than 400 references ly known. Among them, 459 species and discuss on the characteristics of all and 1164 relationships correspond to symbionts known to date. As a result, commensals, and 126 and 373 to para- a total of 375 species (292 commen- sites, respectively. sals, 81 parasites) and 969 relationships (713 commensals, 253 parasites) were Considering commensal polychaetes, compiled. The authors, however, con- nine families have been newly repor- sidered their contribution as a war- ted as including symbiotic representa- MARTIN, ning on the interest of this topic more tives. The aphroditids, chaetopterids, than a closing publication, thus stating orbinids, pholoidids, scalibregmatids DANIEL “The aim of the review is, therefore, to and sigalionids include only one new attract the attention of scientists to - report each, while fabriciinid and sibo- Researcher and to encourage further studies on glinids include two and eighteen, res- 1993 - Present - the ecology of this particular and di- pectively. However, most of them are verse group of symbionts”. Coinciding involved in a single relationship. The with the celebration of the CEAB 30th polynoids are still the most diverse fa- anniversary, I decided to check whe- mily and has experienced the highest ther this objective has (or not) been increase in number of known species, achieved nowadays. together with syllids. Both families altogether represent almost a 50% of Having this in mind, I undertake an ex- all newly reported commensal species haustive revision of the literature on and more than 50% of the newly re- symbiotic polychaetes produced since ported relationships. They also include

Medioantenna variopinta on its host cnidarian Solanderia secunda from Sulawesi (Indonesia). 51 some of the most spectacular species, like tes, six families have been newly repor- by a re-evaluation of the association as a the bright coloured polynoid Mediona- ted as including symbiotic species: hesio- commensalistic or mutualistic, with the tenna variopinta (Di Camillo et al., 2011). nids, serpulids, polynoids, phyllodocids), most typical example being that of the Commensal polychaetes have even been typhloscolecids, and fabriciids, which sponge associated species of Haplosyllis reported from the fossil records, with the range from one to eight newly reported (Lattig and Martin, 2011a). Finally, bryo-

Haplosyllides aberrans parasitizing the shrimp Platycaris latirostris which, in turn, lives symbiotically with the cnidarian Galaxea astreata.

host being a deep-sea sea urchin. species and one to thirty relationships. zoans, cirripeds, ctenophores, echiuroids, In turn, the spionids experienced the holothuroids, nemerteans, phanerogams Concerning the hosts, polychaetes were highest increase in newly reported spe- and tunicates did not vary from 1998 to already known to live commensalistically cies and relationships, with more than 2015. with many marine macroinvertebrates, so 70% and 90% of the total, respectively. As that only cephalopods and tunicates have it occurred among commensals, some fa- The updated information of symbiotic been newly reported as host since 1998. milies (i.e. alciopids and lumbrinerids) did polychaetes also allows me to infer some Cnidarians are the group that increased not vary from 1998 to date. general trends. One of the most consis- more in number of newly reported spe- tent concerns the degree of specificity of cies and relationships, including more than Overall, the number of newly reported the associations. For instance, the num- 30% of the total in both cases. Sponges parasitic species is much lower than the ber of symbionts living in association with include about 20% of the newly reported commensal ones, so that there are less a single host decreased a little bit, but hosts and about 10% of the relationships, groups newly reported as hosts (i.e. de- still dominates and represents a bit more most of them in association with syllids capods, chaetognats, and brachiopods). than 50% of the total. Conversely, some of the so-called “Haplosyllis spongicola” si- In turn, decapods, gastropods, and cni- things have not changed and, for instance, bling-species complex (Lattig and Martin, darians included the highest number of the increasing amount of new knowled- 2009, 2011a, b; Lattig et al., 2010a; Lattig et both newly reported species (61%, 27% ge does not allow me to assess whether al., 2010b). On the other hand, numerous and 20%, respectively) and relationships some of these associations are really sin- groups did not vary from 1998 to date (83%, 16% and 10%, respectively). Cu- gular or, instead, they are qualified as so (among them, the cirripeds, foraminifers, riously enough, cephalopods, ophiuroids, due to a lack of real information. In some isopods, nudibranchs, polyplacophorans, and sponges decrease both in number cases, I suspect that the second possibili- and vestimentiferans). of newly reported host species and re- ty could be more feasible, and this seems Considering now the parasitic polychae- lationships. In most cases this was caused to be confirmed by numerous recent

52 studies. For instance, the hesionid Oxy- seven relationships (five commensal References dromus humesi, previously known from a and two parasitic) were newly reported single record in Congo living in associa- each year until 1998. From this year on Di Camillo, C.J., Martin, D., Britayev, T.A., tion with one species of tellinid bivalve, these numbers have increased to thirteen 2011. Symbiotic association be- is now known to be associated to two (eleven commensals, two parasites) and tween Solanderia secunda (Cnida- more tellinid species in Iberian waters thirty eight (twenty nine commensals, ria, Hydrozoa, Solanderiidae) and (Martin et al., 2012; Martin et al., 2015). nine parasites), which overall represents Medioantenna variopinta sp. nov. The syllid Haplosyllis chamaeleon, consi- a rhythm five times higher, both in terms (Annelida, Polychaeta, Polynoidae) dered a Mediterranean endemism living of species and relationships. from North Sulawesi (Indonesia). in association with Paramuricea clavata, is Helgoland Marine Research 65, 495-511. now known to live also in Cantabrian wa- Modestly, I would really like to think that Koch, H., 1846. Einige Worte zur En- ters in association with Paramurica grayii part of this recent increasing interest on twicklungsgeschichte von Eunice, (Lattig and Martin, 2009), and Haplosylli- symbiotic polychaetes, as well as the fact mit einem Nachworte von A. Koe- lliker. Neue Denksch. Allg. schweiz. Ges. des aberrans, previously synonymized with that researchers pay more attention to ges. Naturw. 8, 1-31. H. floridana and living in association with the peculiarities of the symbiotic rela- Lattig, P., Martin, D., 2009. A taxonomic sponges, is now a valid species reported tionships (rather than simply reporting revision of the genus Haplosyllis as a parasite of coral-symbiotic shrimps new species or relationships), was trigge- Langerhans, 1887 (Polychaeta: Sylli- (Martin et al., 2009). In turn, at the other red by our 1998 paper. Thus, I am conclu- dae: Syllinae). Zootaxa 2220, 1-40. extreme of the distribution, the number ding this contribution to the CEAB’s 30th Lattig, P., Martin, D., 2011a. Sponge-as- of polychaetes being involved in nume- anniversary by confirming that we were sociated Haplosyllis (Polychaeta: rous relationships (i.e. more than 10) al- not wrong with our intended purpose for Syllidae: Syllinae) from the Carib- most doubled from 1998 to date. There- the 1998 review, as the particular mode bean Sea, with the description of fore, I may conclude that there seems to of life of the symbiotic polychaetes are four new species. Scientia Marina 75, be trend in which symbiotic polychaetes nowadays becoming more and more at- 733-758. are often involved in relationships being tractive to researchers. Lattig, P., Martin, D., 2011b. Two new en- much more complex than expected. I am Finally, in agreement with the objectives dosymbiotic species of Haplosyllis almost certain that this trend will be con- of the volume in which this contribution (Polychaeta: Syllidae) from the In- firmed, as new knowledge will be further is integrated, and taking into account the dian Ocean and Red Sea, with new data on H. djiboutiensis from the generated. modern perception of science, I would Persian Gulf. Italian Journal of Zoology like to state that the next logical step in 78, 112-123. The information summarised above this filed should be to be able to trans- Lattig, P., Martin, D., Aguado, M.T., 2010a. partially responds my initial question. fer the interest on symbiotic polychaetes, Four new species of Haplosyllis However, I have not yet analysed the which is currently almost fully restric- (Polychaeta: Syllidae: Syllinae) from rhythm of production of new knowledge ted to the academic world, towards a Indonesia. Journal of the Marine Biolo- before and after 1998. A quick view on non-specialised audience. gical Association of the UK 90, 789-798. these rhythms certainly points on a Lattig, P., Martin, D., San Martín, G., 2010b. marked difference. Effectively, since the Syllinae (Syllidae: Polychaeta) from first know symbiotic polychaete was Australia. Part 4. The genus Ha- described by Koch (1846), an average of plosyllis Langerhans, 1879 (Poly- three symbiotic species (two commensal Zootaxa chaeta: Syllidae: Syllinae). and less than one parasitic) and about 2552, 1-36. Martin, D., Aguado, M.T., Britayev, T.A., 2009. Review of the symbiotic genus Haplosyllides, with description of a new species. Zoological Science 26, 646-655. Martin, D., Britayev, T.A., 1998. Symbio- tic polychaetes: Review of known species. Oceanography and Marine Bio- logy: An Annual Review 36, 217-340. Martin, D., Cuesta, J.A., Drake, P., Gil, J., Pleijel, F., 2012. The symbiotic hesionid Parasyllidea humesi Pettibone, 1961 (Annelida: Polychaeta) hosted by Scrobicularia plana (da Costa, 1778) (Mollusca: Bivalvia: Semelida- de) in European waters. Organisms Diversity & Evolution 12, 145-153. Martin, D., Nygren, A., Hjelmstedt, P., Drake, P., Gil, J., 2015. On the enigma- tic symbiotic polychaete “Parasylli- dea” humesi Pettibone, 1961 (He- sionidae): Taxonomy, phylogeny and behaviour. Zoological Journal of the Oxydromus humesi from Cádiz Bay (Spain). Dorsal and ventral view of the anterior Linnean Society 174, 429-446. and posterior ends. THE GROUP OF AQUATIC MACROPHYTE ECOLOGY (GAME)

he origins of the Group of University of Perth, Australia. Since Aquatic Macrophyte Ecology then, GAME has found in CEAB-CSIC (GAME) go back to the year the ideal headquarters where to 2000. That year, using a rather develop its scientific activities and is Tartisanal but very effective field coring proud to be one of the active groups method, it was possible to sample a witnessing and celebrating its 30 years 5m-long core of the peaty sediments of existence! formed by the Mediterranean seagrass Posidonia oceanica in the small bay of The Core 2000 revealed two impor- Portlligat, located in the north of the tant facts: 1. the sediments underlying Costa Brava, Spain. The ‘Core 2000’ the seagrass P. oceanica were highly has been since then the backbone organic and contained a remarkable of the Group giving birth to two stock of organic and inorganic carbon pioneering research lines nowadays and 2. the core represented a perfect MATEO, widely recognized and followed all chrono-sequence spanning over 4000 over the world. Since inception of years of age. These two facts turned MIGUEL ÁNGEL the Group, it has been directed by Dr. out to become the scientific founda- Miguel Ángel Mateo Mínguez, at that tions for two fertile research lines re- Scientist time a contracted researcher at the levant for the global carbon cycle and Plant Physiology Department of the for the use of marine paleo-archives 2004 - Present University of Barcelona. When awarded for the study of change in the coastal with a Ramon y Cajal Fellowship in ecosystem over the Holocene Period. 2004, Dr. Mateo and his team moved During the last 15 years, in the fra- to the Centre for Advanced Studies mework of 15 competitive projects, of the Spanish Council for Scientific GAME has been one of the leading Research (CEAB-CSIC). Four years groups on seagrass ecology, gaining later, he was appointed CSIC tenured an outstanding reputation in the area researcher and, more recently, of carbon biogeochemistry in coastal Adjunct Professor at the Edith Cowan marine ecosystems, and the leading

Some members of the GAME team celebrating the success of a mission in Cabrera Island (Balea- ric Archipelago, Spain), on board the R/V García del Cid. June 2015. From left to right, Prof. Dr. Paul Lavery (ECU, CEAB-CSIC), Oscar Serrano (ECU, CEAB-CSIC), Eduard Serrano (CEAB-CSIC), Dr. Ambra Milani (front, CEAB-CSIC), Anna Thoran (behind, CEAB-CSIC, UWA), Nerea Piñeiro (USC- CEAB), Carmen Leiva (CEAB-CSIC), and Prof. Dr. Miguel Angel Mateo (CEAB-CSIC, ECU). Photo by the Group of Aquatic Macrophyte Ecology (GAME). group in paleo-ecology using the seagrass 2012 the team was requested by the the origins of metal pollution in the sedimentary archive. Apart form other IUCN to prepare a report on the role Mediterranean, a 2012 key publication important contributions in the field of of seagrass ecosystems in climate change in Nature which synthesised the global seagrass ecology (1. use of stable isoto- mitigation, and has recently been granted stocks of carbon captured in seagrass pes as environmental, trophic, and phy- by the EU LIFE program to coordinate ecosystems, and a synopsis of the effects siological tracers, 2. population ecology, the development of a Mediterranean- of climate change on Mediterranean 3. environmental diagnosis using aquatic region research initiative on the storage seagrasses appeared in 2014.

Factor scores of a Principal Component Analysis using various proxies along the ‘Core 2000’ of Posidonia oceanica sampled in Portlligat. This figure reveals a growing environmental instability towards recent times, initiated ca. 1300 years ago and probably reflecting the impact of the humanization in the Western Mediterranean. Source: Leiva, C. (2015) Posidonia oceanica (L. Delile) and carbon stable isotopes: a proxy for paleoenvironmental reconstructions and ecosystem management. Master Thesis, University of Barcelona. macrophytes), the work of the Group of carbon in seagrass ecosystems and has focused on the cycling of carbon and its incorporation into carbon trading other nutrients in benthic marine ecosys- schemes. tems and beach ecosystems. The Group has applied its knowledge to the develop- GAME has been publishing extensively ment of ecosystem mass balances, the es- on marine ecology, biogeochemistry timation of regional carbon storage (CO2 and global change. Its publications are sequestration) and the paleo-reconstruc- highly cited in the literature on marine tion of past environmental conditions. carbon cycling and include significant GAME is widely acknowledged as a lea- works published in Nature, Global ding Group on the study and estimation Biogeochemical Cycles and other leading of carbon stocks and fluxes of Mediterra- marine ecology journals. These works nean seagrass ecosystems, a pre-requisite include: a pioneering publication in 1997 to understanding the role of seagrasses in setting the foundations of the study of carbon sequestration. the long-term refractory accumulation of organic carbon in seagrass sediments, GAME’s expertise in marine carbon another one in 2002 introducing these storage has led to the Group playing a sediments as paleo-archives, one in 2006 central role in the assessment of regional reviewing the knowledge on carbon fluxes and global carbon storage in marine in seagrass ecosystems, two in 2009 and A sediment core from a P. oceanica meadow ecosystems (i.e. Blue-carbon) and, more 2010 presenting the first environmental in the Natural Park of the Cabrera archipela- recently, its incorporation into formal reconstructions using the seagrass go. The shifts between more and less organic climate change mitigation policies. In paleo-archive, one in 2011 establishing episodes are very evident. 55 fostering the aquatic sciences worldwide. from 9 countries, including Australia, An important aspect of GAME is its ex- Brazil, Colombia, Denmark, Germany, perience in the coordination of multi-ins- Italy, Morocco, Spain, Tunisia, and the USA. titutional and multinational research pro- In addition to its Group leader, GAME grams, incorporating both ecological and is currently integrated by a by 3 adjunct socio-economic studies. GAME has coor- professors (Spain and Australia), 2 post- dinated several major national and inter- docs (Spain and USA), one contracted national studies of the Mediterranean re- technician (Spain), 3 PhD students (Spain gion, including North Africa and Australia. and France), 2 master students (Denmark, GAME has no geographical barriers when Perú) and 3 final degree students (Spain). it comes to collaborate and enjoys reu- niting and participating in multinational Between the elaboration of this note and multidisciplinary consortia. GAME is and 2020, GAME will be working on 1. not just an acronym; it is a declaration of the three active projects it is currently intent, of belief for and commitment to leading, funded by the National Research making of science an enjoyable experien- Program, the National Parks Funding ce driven by passion and not by perfor- Scheme, and the EU LIFE program, and mance indicators. This approach has pla- 2. in an University-Industry collabora- ced the Group in an excellent position to tion project funded in Australia. In those facilitate the involvement of researchers projects we are addressing unedited pro- Sampling a marine sediment core in the laboratory. from different nationalities in National, blems of the phenomenon of refractory Regional and International research ini- accumulation from an edaphological pers- In addition to printed scientific papers, tiatives. The countries of origin of the pective, making the first attempts at mo- GAME is also very active in the dissemi- people collaborating or having collabora- delling the carbon accumulation dynamics, nation of its activity in national and inter- ted with GAME amount 20 and include exploring a wide range of new proxies for national conferences (around 200 oral Australia, Brazil, Canada, Denmark, Egypt, the paleo-reconstruction of environmen- presentations), as well as in the media, in- England, France, Germany, Greece, Italy, tal change from local to global scales, and cluding printed press, radio, and television Kenya, Malta, Mexico, Morocco, Portugal, elucidating the source of the dangerous (around 100 participations). Furthermore, Spain, Sweden, The Netherlands, Tunisia, ambient lead concentration in Port Pirie, GAME organizes outreach activities regu- and the USA. Australia. The studies take place mostly in larly to help rising the awareness of the two Mediterranean regions with a high general public on the need to preserve The people that have contributed to presence of seagrass meadows: The Me- our ecosystems (courses, talks, seminars, GAME have been, beyond any doubt, the diterranean Sea, and Western and South and round tables). Finally, through the most important capital of the Group. Australia. participation of its leader in the Board Including Secondary and High school of Directors and in the Publications and students, Degree and Master students, Awards Committee of the Association PhD and Post-doc fellows, contracted for the Sciences of Limnology and Ocea- technicians and researchers, and adjunct nography (ASLO), GAME contributes to doctors, GAME has hosted 32 people

The reef-like, organic-rich structure formed by the Mediterranean endemic seagrass Posidonia oceanica: the mat. Observed in Formentera, Balearic Islands, Spain. Photo by the Group of Aquatic Macrophyte Ecology (GAME).

56 THE IMPORTANCE OF THE TAXONOMY

magine a big dictionary, very big As the eminent ecologist Paul K. and very thick. With many pages, Dayton pointed out: “The last century all of them white, without any has seen enormous environmental word inside. The task of taxo- degradation: many populations are in Inomists is to search “words”, define drastic decline, and their ecosystems and include them into this dictionary. have been vastly altered. These envi- This dictionary is the Nature. Without ronmental crises coincide with the vir- words we can’t write or speak langua- tual banishment of natural sciences in ges, and we can’t understand Natu- academe and research centres”. There re. Any theory, any applied work, any is an urgent need to understand the conservation strategy can be biased causes of the decline, how the species by the wrong use of “words”. Can you interact with other components of the imagine a language that does not up- environment, and how ecosystem in- date its dictionaries? It will soon be tegrity is determined. If we don’t know considered a dead language. It seems which species are involved, we con’t MACPHERSON, that ecology is moving in this direction. understand the problema and find the Our “dictionaries” are becoming ob- solutions. Whitout taxonomy this is ENRIQUE solete and this will ultimately bring us not possible. to an ecology with deficits, founded on Research Professor a taxonomic basis obtained decades or In this gloomy panorama the CEAB 1994 - Present centuries ago. is producing a long list of taxonomic works. “The battle delivered against taxonomy has obtained a victory; nowadays For instance, the recent book of “Guía the classification of an organism has de las macroalgas y fanerógamas mari- become a difficulty.” Ramón Margalef nas del Mediterráneo Occidental” co-au- wrote this statement in 1968 in his thored by E. Ballesteros is charmingly book Principies of Ecological Theory. anachronistic in the best sense of the Since then, the status of taxonomy in word. It is a splendid work that helps the scientific world has fallen increa- to palliate the ignorance about an im- singly. However, it is surprising to ob- portant group due to the lack of wor- serve that many scientific articles are ks like this monograph. published such as those published in emblematic magazines like Science or Fortunately, there are other examples Nature-and TV documentaries warn in our Institute. There is no doubt that us of the importance of biodiversity these works fully accomplish the diffi- and how it is seriously threatened by cult mission of being the tiger shot for insatiable human greed. And it is even future studies on the biology, ecology more surprising to see that scienti- and conservation of our ecosystems. fic community, totally aware of such May be the victory of the battle of ta- threats, ignores or undervalues men of xonomy is not such a victory. science who are trying to find out how many species live in ecosystems and how to identify and distinguish them correctly.

The biased used of the index of impact is leading the Natural Sciences towards a cul-de-sac: the number of taxonomists is decreasing at a dramatic rate and as a logical consequence so are the monographs on flora and fauna.

57 A, Galathea pilosa De Man, 1888, Papua New Guinea, ovigerous female 4.5 mm. B, Galathea pilosa De Man, 1888, Maldives, male 3.6 mm. C, Gala- thea platycheles Miyake, 1953, Madagascar, female 2.2 mm. D, Galathea platycheles Miyake, 1953, Western Australia, ovigerous female 1.9 mm. E, Ga- lathea politula n. sp., Vanuatu, holotype, M 3.5 mm. F, Galathea polydora n. sp., Vanuatu, male 3.3 mm. G, Galathea polydora n. sp., Vanuatu, ovigerous female 2.5 mm. H, Galathea polyphemus n. sp., French Polynesia, male 4.4 mm. I, Galathea providentia Laurie, 1926, Madagascar, female 3.0 mm. 58 STREAM MACROINVERTEBRATES: SURVIVING TO GLOBAL CHANGE AND CYANOTOXINS

o say that global change in ri- all of them. It should be remembered vers is going to be studied is that there are already data showing the a redundancy because it is increase in temperature in mountain impossible to investigate in lakes[2], which in the Pyrenees have Triver ecology without consciously or temperatures with large daily fluctua- unconsciously including the effects that tions in summer, with maximums well global change induces on these ecosys- above 20ºC, because the effect of the tems. The rivers are more or less cha- change Is more evident above the fo- nalized, they have regulated flows, they rest boundary in mountain ranges with receive diffuse and punctual contamina- altitudes such as the Pyrenees. tions from their drainage basin or from other watersheds distanced by atmos- Since the beginning of my research, pheric transport and precipitation, they aquatic macroinvertebrate communi- are interconnected and invaded by ties have been the focus of my studies PUIG, many introduced species that in many on the effects of global change [3], and cases are also invasive. The latter can on climate change in recent years [4]. MARIÀNGELS be found even in high mountain head- Macroinvertebrates allow practical waters, as in the Pyrenees where some approaches for river quality assessment Assistant Director species of predatory fish transform the [5], accurate conservation studies of pristine lakes into eutrophic ones, from their biodiversity, comparative studies Since 2015 which rivers with low quality waters of biological traits and species strate- leave1. gies to assess the resistance and resi- Scientist lience of communities [6] before the The climate change generated by glo- advance of climate change or for mana- 1991 - Present bal change, extends its impact on the gement and restoration models. whole Earth. And in our study areas it emphasizes the temporality of the Me- In fact, the importance of macroinver- diterranean streams and the Pyrenean tebrates lies in their role within the headwaters, as well as the catastro- structure and function of river ecosys- phic effects of droughts and floods in tems as intermediate links between

Tordera river macroinvertebrates (A. García-Rubies). 59 the primary producers, algae and cyano- ver benthic cyanobacteria [7,8] and ben- communities, including paleolimological bacteria that they control, and the high thic-planktonic lake cyanobacteria. reconstructions, to know what strategies predators that consume them (fishes and will allow them to survive and which will amphibians) . This is a classic top-down Nowadays my research focuses mainly not, as well as the role that cyanotoxins control scheme, which can be reversed on the effects of climate change on high can play in these processes. to down-top by toxin production by ri- mountain aquatic macroinvertebrate

Sant Nicolau river from Aigüestortes National Park (Pyrenees) (M.A. Puig).

References

1. T. Buchaca, E. Ballesteros, E. Chappuis, E. Gacia, A. Gallés, A. Miró, V. Osorio, Q. Pou-Rovira, M. A. Puig, I. Sabás & M. Ventura. 2016. Efectes de la presència de diverses espècies de peixos invasors en els estanys d’alta muntanya. X Jornades de Recerca al Parc Nacional d’Aigüestortes i Estany de Sant Maurici: 171-184. 2 J. Catalan & MOLAR project group. 2002. Lake Redó ecosystem response to an increasing warming in the Pyrenees during the twentieth century. Journal of Paleolimnology, 28: 129-145. 3 Ortiz J. & Puig M.A. 2007. Point source effects on density, biomass and diversity of benthic macroinvertebrates in a Mediterranean stream. River Research and Applications, 23(2): 155-170. 4 Puig M.A., Ubero-Pascal N., Amore V. & Fochetti R. 2011. Estrategias de supervivencia ante el cambio global. Las especies de efemerópteros y plecópteros del Parque Nacional de Aigüestortes como paradigma. En: Lucía Ramírez y Benigno Asensio (eds.) “Proyectos de investigación en parques nacionales: 2007-2010”: 233-251. Naturaleza y Parques Nacionales, Serie investigaciones en la red. Edita OAPN, Madrid. 5 Martin Erlandsson, Andrew J Wade, Joan Lluís Riera Rey, Mariàngels Puig, Richard A Skeffington, Sarah J Halliday. 2014. River Arbúcies biophy- sical modelling, final report. Deliverable 5.9, REFRESH project: 1-67pags. Link: http://www.refresh.ucl.ac.uk/webfm_send/2255. 6 Ortiz J., Puig M.A. & Martí E. 2005. Recovery of biotic integrity below a waste water treatment plant effluent input. Hydrobiologia (545): 289-302. 7 Aboal M. & Puig M.A. 2009. Microcystin production in Rivularia colonies of calcareous streams from eastern Spain. Algological Studies 130: 39-52. 8 Sergio Liarte, Nicolás Ubero-Pascal, Alfonsa García-Ayala, and Maria-Angeles Puig. 2014. Histological effects and localization of dissolved Microcystin LR and LW in the mayfly Ecdyonurus angelieri Thomas (Insecta, Ephemeroptera). Toxicon 90: 31-35. SOCIO-ECOLOGY

e live in an era of a ecological systems has been gaining rapid accelerated global acceptance to analyze this complexity. change (planetary- Social-ecological systems (Figure 1) scale changes in the are “complex adaptive systems WEarth system) being human activity, in which humans are part of predominantly the global economic nature and the dynamics of both system, the prime driver of this change. dimensions are strongly linked This global change pattern is driving us at equal weight”. When managed, into a deep environmental crisis. This these coupled co-evolving systems environmental crisis can be described should focus on the ability to respond by observing three main tendencies; to feedbacks from the environment human footprint is increasing, considering the tendencies of planet earth has a bounded carrying ecosystem goods and services that capacity for its natural resources we obtain as benefits from the and the natural capital is degrading. environment. Altogether makes the old concept of SARDA, Sustainable Development “meets The social-ecological paradigm of our the needs of the present without present days recognizes the mutual RAFAEL compromising the ability of inter-associations between human future generations to meet their societies and ecological processes Researcher own needs” difficult to achieve. We that are necessary for the survival of 1990 - Present are running an unsustainable machine both. This paradigm give much more in an unsustainable way. Our Natural importance to the Natural Capital as Capital, the extension of the economic resource provider and put pressure notion of capital to goods and services to better define the sustainable relating to the natural environment development path that we need to is in danger and this jeopardizes our construct for the future of humanity ability to leave a safe environment for “enhancing social capital and economic future generations. prosperity while maintaining the integrity of natural systems and its In today’s world, natural resources potential for the provision of ecological cannot be treated as discrete entities good and services”. that need to be analyzed separately; they are dependent of the social During the last two decades, a re- and economic systems with which search line of the CEAB-CSIC uses they interact. The concept of social- this previous own new definition to

61 develop new research and applications indicates, human systems (people’s concile the theory of Environmental Po- in the frontier between social and natu- capabilities and their activities) become licy with the Practice of Environmental ral systems, how they work and interact, drivers of change (D). They pressure Management. We develop a standardized how to cope with present and emerging, constantly or in pulses natural related system, the so-called Ecosystem-Based local and global environmental problems systems (P). Those Natural systems Management System to bring these is- and the role, if any, that science and regu- (structural units and the functions they sues into real applications (www.msfd. lations might play on it. Different aspects made) alter their status (S) that in turn eu). We are disseminating such system become drivers of research: how to in- can translate into the degradation of with the main goal to apply it into Inte- vestigate and to promote a better care of fundamental natural resources used grated Coastal Zone and Beach Mana- ecosystem service provision, how these by man (natural goods and ecosystem gement structures (http://lagpweb.udg. interacting systems of people and natu- services) diminishing human welfare (W). edu/mevaplaya2/) as well in the adoption re (social-ecological systems) can best be The recognition of such degradation of this scheme into the Conservation of managed to ensure a sustainable and re- should allow man to made adequate the Natural Capital and its use in Mari- silient supply of the essential ecosystem policy responses (R) to solve the ne Protected Areas. Finally, to deal with services on which humanity depends. All pattern of accelerated degradation. our role of responsible civil servants, we of this while developing tools and making The information generated through the are attending today different groups and recommendations to move from present DPSWR framework expressed issues commissions to bring recommendations focused impact-driven policies to more in a highly inter-related form which is into public norms such as the Intermi- desirable state-driven policies. something that we cannot observe if we nisterial Commission to transpose the use other sets of indicators that inform Maritime Spatial Planning Directive, the Social-ecological systems can be analyzed different pieces of the social-ecological “Comissió Sectorial d’Investigació through different information platforms. system puzzle in isolation. i Sostenibilitat” and the “Comitè In our research, we use the proposed de Seguiment de l’Estrategia Mari- Driver-Pressure-State-Welfare-Response Using the social-ecological science and na de la DM levantino-balear”, both (DPSWR) framework to adequately the framework outlined above, we have from the Genetalitat de Catalunya, or the organize information of the interrelation been working on the practical applica- “Commissió de Sostenibilitat de les between the human and the natural tion of the United Nations Ecosystem Comarques Gironines”. sub-systems inside. As the above figure Approach Strategy with the aim to re-

Suncheon Bay Wetland Protected Area (South Korea) a good example between conservation and development 62 NEW TOOLS FOR BIODIVERSITY ASSESSMENT

e are witnessing the six- underfunding, lack of prestige, and lack th big extinction of the of career and employment perspec- history of life in our pla- tives. Taxonomy has failed to keep up net. Unlike the previous with the development of other discipli- Wones, this is caused by human activi- nes of biology, and the result is known ties and their impact on biodiversi- as the “taxonomic impediment”, in ty. Recent updates of the Red List of short, the insufficient taxonomic ex- Threatened Species by the Internatio- pertise to effectively describe the bio- nal Union for Conservation of Natu- diversity on Earth. Taxonomic informa- re show that ca. 33% of the assessed tion is a pre-requisite for all research species are threatened in some way. and management on biodiversity, yet Current estimates place the number for many groups of organisms there of species that go extinct every year are between none and a few persons in the thousands, mostly as a result of in the world that can reliably identify multi-faceted anthropogenic impacts: species. Even well-known taxa often TURON, over-exploitation, habitat destruction, lack specialists knowledgeable of im- climate change, introduced species, portant areas of the planet. Taxonomy XAVIER pollution, ocean acidification…The is badly needed, yet taxonomists are IPBES (Intergovernmental Platform considered as service-providers ra- on Biodiversity and Ecosystem Ser- ther than true scientists. Research Professor vices, the biodiversity counterpart of 2008 - Present the Climatic Change Panel) warns that Biodiversity crisis plus taxonomic oceans in particular are in imminent impediment equals big trouble for peril of an unprecedented marine ex- assessment and conservation of the tinction episode. biota of the planet. Species become extinct at a faster pace than we At the same time, taxonomy, the scien- can describe them. Urgent action tific discipline that deals with the des- is needed to alleviate this problem cription, identification, and classifica- until taxonomy can regain its lost tion of living beings, is suffering from momentum. Hundreds of years of

Figure 1. A square allows delimiting sampling units on rocky bottom communities in Cabrera Island. 63 taxonomic expertise are deposited in initiative devoted to developing short mitochondrial gene Cytochrome Oxidase museum collections (often inaccessible DNA sequences as a global standard for I (COI) has shown an adequate resolving or poorly curated) and taxonomic the identification of biological species. It is power at the species level in most groups. literature (often hard to obtain and the biggest initiative in genetic biodiversi- Even well-seasoned taxonomists now plagued with incomplete descriptions). ty ever undertaken. As of today, there are regularly use barcode sequences to Intensive use of Internet can greatly over 5,300,000 sequences deposited for identify problematic groups, and many contribute via cataloguing, archiving, over 250,000 species. faunistic/floristic works and descriptions and providing unrestricted access to of new species include the generation of taxonomic literature, and indeed there The method of generating short sequence the corresponding barcodes. Obtaining are many important initiatives in these tags as IDs for species has been labelled sequences is nowadays straightforward fields, such as World Register of Marine “barcoding”, a catchy name reflecting the and cheap, and many biodiversity projects Species, Encyclopaedia of Life, Biodiversity similitude of these sequence tags with the even in underdeveloped countries have Heritage Library, to name only a few. barcodes we see in so many shops today. benefitted from this new tool, indirectly Barcoding is not free from problems, accessing the taxonomic knowledge captured in the BOLD project. Barcoding studies have changed our view of extant biodiversity, the overwhelming message being that biodiversity at the species level has been grossly underestimated in many groups, with cryptic speciation phenomena being pervasive.

If barcoding changed the way to approach biodiversity studies in the last ten years, a further leap forward has been made possible by the advent of the new sequencing technologies (so-called Next Gene- ration Sequencing, NGS). NGS methods can sequence in parallel heterogeneous mixtures of DNA (as opposed to the traditional Sanger method that generates one sequence at a time). This opened the door to analyse barcode sequences, not specimen by specimen, but using all DNA present in a community in a single run. This new method of biodiversity characterization has been termed metabar- Figure 2. A corer is used to Sample the Maërl community in Cíes Islands. coding, and refers to the sequencing of tags (barcodes) from DNA present in the In recent years we are starting to deposit among which the choice of the adequate community. DNA can come from bulk or- and perpetuate the taxonomic expertise marker, the curation of the databases and, ganismal samples if organisms have been in genetic databases. This is done by ge- above all, the need of a sound taxonomic isolated (from traps, decanted sediments, nerating sequences of organisms iden- expertise to correctly identify the filtered water…), or from environmental tified by taxonomists and making them specimens in the first place. Unfortunately, DNA (eDNA), defined as the genetic ma- public, so that non-specialist people can many of the least-known groups are also terial obtained directly from samples (soil, compare these with sequences obtained among the most difficult to barcode sediment, water…) without first isola- from target specimens to help in their (f.i., small organisms), and a sustained ting any target organism. eDNA includes identification. Genetics does not supplant (and well-funded) effort is necessary DNA inside the organisms and extra-or- taxonomy, rather, it is a way to preserve to populate the databases. However, ganismal DNA in cells, debris, exudates, and to make amenable to others taxono- barcoding has demonstrated now and or as free extracellular DNA. mic knowledge using genetic features in again its utility and has revolutionized addition to the traditional morphological the way in which we identify species and Metabarcoding was invented by micro- characters. The Consortium for the Bar- assess biodiversity. In particular in the case biologists (although the name is not com- code of Life (BOLD) is an international of animals, where the first (5’) half of the monly used in that field), as it was the lo- 64 gical (and perhaps only) way to deal with identification of endangered or pest spe- the resident biota. prokaryote communities, for which ge- cies without actually sampling them, and netic tags based on the 16S rDNA were paleoecology, among others. The spec- In another project (METABARPARK, well known. The next step was to apply trum of potential applications of meta- OAPN) we sought to develop the tech- this technique to microbial eukaryotes barcoding continues to widen. Current nique for complex benthic communities and, only in recent years, metabarcoding cutting-edge issues in metabarcoding in- (rocky substrates and Maërl). Metabar- has started to be assayed on fungi, plant, clude its value as a quantitative tool (with coding has been traditionally used for and metazoan communities using diffe- number of reads as a proxy for biomass homogeneous communities (sediments, rent regions of the 18S rDNA gene. In of a given MOTU), the use of PCR-free soils, water) and its utility in more com- metabarcoding, the main steps are the ex- approaches to avoid potential amplifica- plex habitats remains unexplored. We traction of DNA from samples, the ampli- tion bias, and the possibility of sequencing have developed specific sampling proto- fication of the chosen barcode using uni- all genes present instead of a chosen bar- cols, including fractionation in size classes. versal primers, and the high throughput code (metagenomics, so far only feasible While most metabarcoding studies have (NGS) sequencing of the amplicons. The with prokaryote communities). used the 18S rDNA gene, we have de- sequences are then quality-filtered, arti- veloped a pipeline for the use of COI in facts and chimeras are removed, and MO- We have been developing metabarcoding our samples, thus making the full BOLD TUs (Molecular Operational Taxonomic techniques in two different projects. In database accessible for the taxonomic as- Units) are delineated by clustering simi- the CHALLENGEN project (MINECO) signment of MOTUs. Thousands of MO- lar sequences. The underlying idea is that we have characterized α- and β-diversi- TUs have been identified in four different MOTUs match diversity at the species ty of deep sea sediments from canyons sublittoral habitats in two National Parks level as closely as possible. Then MOTUs in the NW Mediterranean. Micro- and (Cabrera Archipelago and Cíes Islands), are assigned a taxonomic name by com- meiofaunal organisms constitute a black and detailed community analyses have parison with sequences from databases. box in biodiversity studies, and with the been made, including the temporal com- All these steps have many alternatives use of metabarcoding we have identified ponent. The possibility to assess species and can introduce variability in the re- thousands of MOTUs, among which the composition at an unprecedented level of sults. The field is young and new techni- dominant groups were Metazoa, Alveola- detail is becoming a game-changer in the cal and bioinformatics developments are ta, Stramenopiles, and Rhizaria. We have way we monitor biodiversity, often based being made continuously. We are far from detected strong heterogeneity at all levels on partial inventories which may not be a standardized pipeline, but consensus is studied, and have monitored seasonal di- adequate surrogates for the condition of arising in several of the steps. fferences in these communities. We have the whole community. compared the information obtained with Metabarcoding has proven very useful in different extraction protocols, different Let me finish with the words of Wheeler biodiversity assessment and monitoring, genes, and different pipelines. Likewise, we and co-workers (Science, 2014): “Our ge- generating high-quality datasets with an studied the communities using DNA and neration is the first to fully comprehend order of magnitude more species (MO- RNA. While DNA persists in the sedi- the threat of the biodiversity crisis and TUs) and in much shorter times than ments for some time and can correspond the last with the opportunity to explo- traditional methods. It has also been suc- to organisms or remains transported in re and document the species diversity of cessfully applied to studies of ecological the water column, the RNA corresponds our planet. Time is rapidly running out”. dynamics, interactions, symbioses, diets, to the living organisms and represents It’s all in our hands!

Figure 3. Image of the diversity of crustaceans that can be found in the Maërl community. 65 FROM TAXONOMY TO MOLECULAR ECOLOGY AND BIOTECHNOLOGY: THE SPONGES AS AN EXCUSE

Molecular Ecology of the Marine Benthos team

ponges are sessile aquatic Thus, following Dr Rubió’s advise, I animals that remain in place conducted my thesis on taxonomy for years, just filtering water. and ecology of sponges from Indeed, they are not the best Mediterranean fishery grounds, and Sstudy pet for a biologist interested in I could appreciated soon that this animal behavior! This is what I thought specialization had not been a bad when my PhD supervisor (M Rubió) idea at all. Every small contribution suggested sponges as my thesis to- to the field was new: discovering new pic, after having demising my project species for science, finding free sponge proposal on tuna migration along the larvae swimming at sea, associations of Mediterranean. “Almost every thing is sponges with other animals… known about fishes, while roughly nothing is known about sponges” he said. Ecologists from several countries URIZ, And he was completely right… but asked for my collaboration after only for the second part of his asser- understanding that sponges MARÍA JESÚS tion. In the seventies, no many world dominated many benthic assemblages. scientists were really working on This was the beginning of a flourishing Research Professor sponges: none in Spain, one in Japan, research line on sponges at the CEAB 1985 - Present Russia, The Nederland’s, New Zealand, (and in Spain), concomitantly with the Australia, and the UK, and three in rise of sponge science in the world. France, Italy, and USA. And most of More than 30 Spanish and European them were busy at that time just with projects and a series of contracts with sponge taxonomy. the PharmaMar Company have funded a large part of the CEAB research

Figure 1.1. Common Mediterranean sponge without skeleton (Oscarella) (Foto: E.Ballesteros).

Figure1.3. Tubular Sponge (Callyspongia) Figure 1.3. Aquiferous system of Cliona from the Pacific (Foto: MJ Uriz). viridis: choanocyte chambers (cc) connected through small conducts to the large exhaling conducts (arrows) (Foto: D. Rosell). on sponges during the last 30 years. chemical and general ecology, population chance. We discovered mosaic multi-chi- Moreover, numerous publications in genetics, and differential gene expression, merism in sponges during a classical study international journals, and the edition of and a few of them continued working on of population genetics. We found a total several monographic books on sponges, sponges (two at the CEAB) after obtai- of 36 genotypes in 13 sponge individuals, have contributed to confer to the CEAB ning a fix position. sampled at four points of their bodies. a worldwide reputation as a reference Interestingly, larvae produced by the co- “Sponge Center”. Detailing the research conducted on lonies showed diverse genotypes so that sponges at the CEAB during the past 30 no germ line dominance seems to occur Sponges concealed many relevant years would require as many pages as the (Mol Biol Evol 2011, 28, 9). Chimeric indi- facets, the study of which have helped more than 200 published sponge papers viduals had never being found before in to resolve evolutionary, ecological, and contain. Thus, I will take a quick look back natural sponge populations. The hidden biotechnological general issues. They are: through these years and only will men- genetic diversity of chimeric individuals i) The oldest extant animals on Earth -a tion a couple of studies that have repre- might explain why small isolated sponge perfect target for studying the origin of sented breakthroughs in marine science. populations survive for long without ex- the pluri-cellularity-; ii) Key organisms periencing detrimental effects because of in recycling dissolved organic matter We pioneered the Marine Ecology field the genetic drift. in Europe by introducing the ecological principles and methods (Mar Ecol Prog Chimerism is particularly important for Ser 1991, 70) in a discipline dominated by sponges living in seasonal waters with chemists of natural products. For the first dramatically changing conditions. One ge- time, the interactions among sponges and notype could grow particularly quickly in other invertebrates mediated by chemi- some conditions, but lose out in others. If cal substances were analyzed at a com- the going gets tough, the sponge may just munity level, evidencing that most benthic expand the part that is best suited for the species allocated their available energy ei- conditions at hand. This might contribute ther to growth or to defense, according to explain why some encrusting sponges to the Optimal Defense Theory, develo- spend decades continuously shifting in Figure 1.4.Siliceous spicule of ped for plants. shape and size without actually growing an astrophorid sponge (SEM, Foto : MJ Uriz). any bigger. We identified for the first time the spon- in the benthic systems through their ge cells where the bioactive metaboli- Finally, sponges are more than simple abundant associated microbes; iii) Long- tes accumulate, described how they are animals. They harbor from hundreds to living filter feeders that accumulate transported to the sponge periphery thousands of symbiotic organisms, which contaminants from the water and result without causing damage to the sponge particularly suitable for assessing chronic tissues and how they are released to the marine pollution, and iv) The most external medium and remain attached to prolific invertebrate Phylum in producing the sponge surface to protect the sponge bioactive secondary metabolites with from predators (Cell Tissue Res 1996, 285; applications in pharmacology and Mar Biol 1996, 124). Posteriorly, we stu- cosmetics. died the biotechnological applications of sponge bioactive metabolites, focusing on Certainly, along these years, we have des- overcoming the bottleneck for clinical as- cribed numerous new sponge species, as says of sponge-derived drugs, also known well as some new secondary metabolites as “the supply problem”. We proposed from sponges, designed an expert system sponge embryos as a new source of ma- for sponge identification, and contributed terial for cell culture, since embryos con- to clarify the taxonomy and phylogeny of tain high amounts of stem cells, which are Figure 2. A one-week old explant of the sponge the Phylum. But more than this, we have more versatile and resistant to infections Corticium candelabrum from an experimental used the sponges as a model to address under culture than adult cells (Trends in culture to overcome the “supply problem” (see general biological, ecological, environ- Biotechnology 2007, 25, 10). text) for pharmacological trials (Foto: S. De Caralt, MJ Uriz). mental, and biotechnological questions. A dozen of students successfully defen- But, as it often occurs in research, some ded their PhDs on biodiversity, pollution, of our most impacting results rose from 67 include other invertebrates, but chiefly sition of some characteristics of several Obviously, the research performed on bacteria, archaea, and fungi (Environmental extant invertebrates (Evolution 2012, 66, sponges at the CEAB during the thirty Microbiology 2013, 15, 11; 2015, 17, 10). 10). last years could not have been possible This symbiotic way of life is shared with without my pre-and postdoctoral other animals, but rarely the associated The fast development of molecular tools students and technicians, but also microbiome represents, such as in spon- has allowed us to address difficult ques- without the inappreciable collaboration ges, more than 50% of the holobiont bio- tions in an affordable way by analyzing of colleagues who were appealed by mass. genes and controlling factors that deter- the fascinating sponge world. Some of We are currently studying the bacterial mine their expression and function. The them merit particular mention for their communities of sponge assemblages from search of genes and metabolic pathways prolonged partnership such as Xavier temperate and tropical seas, and their involved in the production of bioactive Turon, Kike Ballesteros, Daniel Martin, meta-transcriptomes and genomes, with metabolites of interest for the develop- and Enrique Macpherson. Thanks to all of the idea of finding the evolutionary cau- ment of new drugs against hardly curable them from me and on behalf of sponges! ses and mechanisms that motivated these diseases and their transfection to culti- symbioses to persist since the Precam- vable bacteria, are our next challenges in brian, and their implications in the acqui- years to come.

Figure 3. A chimeric individual of the sponge Scopalina. Letters indicate the presence of four genotypes.

68 BIODIVERSITY, ECOLOGY AND CONSERVATION IN HIGH MOUNTAIN LAKES

he research we are perfor- 1.Introduced species and biodi- ming aims at using high moun- versity. tain lakes of the Pyrenees as A line of research that has as main a natural laboratory to study objective the description of the process Tthe generation of biodiversity, natural of species invasions in high mountain selection and how introduced species lakes of the Pyrenees, and the study of alter natural ecosystems. High moun- the effects of these introductions and tain lakes are an excellent model for their ecological implications for the ecological studies due to their clearly conservation of lake ecosystems. So defined external limits, their extreme far we have focused on the description ecological characteristics and to have of the effects of these invasions a relatively low number of species. In (conservation biology and ecology), addition, the Pyrenees are a separate but we have also started to study this VENTURA, biogeographic region within the Eu- phenomenon as a potential generator ropean continent, and its 4500 lakes of local adaptations in species that MARC and ponds are a relatively recent (from have not been eradicated by the a few to 15,000 years old). All these invaders (Evolutionary Ecology). This Ramon y Cajal Researcher features give these ecosystems a spe- is possible because we were able to 2003 - Present cial value for being used as models of establish the date of introduction of ecological and contemporary evolu- fish in many lakes, and therefore we tionary processes. The main objective are able to study how some species’ of the research group is the study of attributes are correlated with the time local adaptations, eco-evolutionary in- of invasion. teractions and their relationship with biodiversity using as ecosystems high The first step in this line of study was mountain lakes in the Pyrenees. In par- to document the historical factors ticular we have two different lines of that have led to the introduction of study: fish in the Pyrenees (Miró and Ventura

Lake Closell, a fish removal site of LIFE LIMNOPIRINEUS in Alt Pirineu Natural Park. 69 2013, 2015). Secondly, we are describing The consequences of the introduction or adapt to scape predation. At present, the ecological consequences and the im- of fish in mountain lakes mainly derive we are coordinating a project aimed to pact on biodiversity of the lakes of the from the fact that once introduced to improve the conservation of aquatic high introduction of these predators, focusing the lakes they occupy the higher trophic mountain ecosystems of the Pyrenees either on indicator groups of organisms, level that previously did not exist. As a (www.lifelimnopirineus.eu) including the such as amphibians, benthic macroinver- consequence, most of the most conspi- restoration of some lakes to their fish tebrates or planktonic crustaceans (Miró cuous taxa such as amphibians and some free natural state, and the divulgation to 2016), but also from the whole ecosys- macroinvertebrates disappear from the schools and the general public of the bio- tem perspective (Buchaca et al. 2016). lake, others decrease their abundance diversity value of these ecosystems.

The feary shrimp Chirocephalus diaphanus in a temporary pond of Aiguestortes i Estany de Sant maurici National Park. 70 2. Species distributions and local adaptations, a basis to test the im- eferences portance of eco-evolutionary feed- R backs. Alonso, M., and M. Ventura. 2013. A new fairy shrimp Phallocryptus tseren- sodnomi (Branchiopoda: Anostraca) from Mongolia. Zootaxa 3670:349-361. This is the research line that we have been developing for longer time and mainly Buchaca, Teresa; Ballesteros, Enric; Chappuis, Eglantine; Gacia, Esperança; Ga- uses crustacean zooplankton of high llés, Anna; Grau, Berta; Miró, Alexandre; Osorio, Víctor; Pérez, Berta; Pou-Ro- mountain lakes of the Pyrenees to study vira, Quim; Puig, Mariàngels; Sabás, Ibor; Ventura, Marc. 2016. Efectes de la the relative importance of stochastic presència de diverses espècies de peixos invasors en els estanys d¿alta mun- events with respect to the selective tanya. La investigació al Parc Nacional d¿Aigüestortes i Estany de Sant Mau- forces in determining the local genetic rici. X Jornades sobre Recerca al Parc Nacional d¿Aigüestortes i Estany de differentiation of natural populations, Sant Maurici p.171-184 with the ultimate goal of finding cases of eco-evolutionary interactions. These Dufresne, F., S. Marková, R. Vergilino, M. Ventura, and P. Kotlík. 2011. Diversity interactions are more likely in species in the Reproductive Modes of European Daphnia pulicaria Deviates from the with shorter generations and simpler Geographical Parthenogenesis. Plos One 6:e20049. genetic composition such as crustaceans. Understanding the distribution of species Krajicek, M., J. Fott, M. Ventura, R. Sommaruga, M. R. Miracle, P. Kirschner, and and the importance of environmental M. Cerny. 2016. The genus Cyclops (Copepoda, Cyclopoida) in Europe. Zoo- factors in such distribution requires logica Scripta 45 (6), 671-682. the understanding of how local factors affect population dynamics and structure Larsen, T., M. Ventura, N. Andersen, D. M. O’Brien, U. Piatkowski, and M. D. Mc- of the metapopulation. The nature Carthy. 2013. Tracing Carbon Sources through Aquatic and Terrestrial Food of island type of limnetic habitats Webs Using Amino Acid Stable Isotope Fingerprinting. Plos One 8:e73441. creates opportunities for local genetic differentiation and adaptation to develop. Miró, A. 2016. Fish as local stressors of Pyrenean high mountain lakes: Arrival We first studied the species ecology and process and impact on amphibians and other organisms. Phd theses. Univer- changes in ecological characters, both sitat de Barcelona. morphological and biochemical, of some of the crustacean species (Ventura and Miró, A., and M. Ventura. 2013. Historical use, fishing management and lake Catalan 2005, 2008, 2010) and we are characteristics explain the presence of non-native trout in Pyrenean lakes: also developing new tools to study their Implications for conservation. Biological Conservation 167:17-24. trophic relationships (Larsen et al. 2013). At the whole biogeographic scale of the Miró, A., and M. Ventura. 2015. Evidence of exotic trout mediated minnow Pyrenees, we are studying the distribution invasion in Pyrenean high mountain lakes. Biological Invasions 17:791-803. of different groups of species, including amphibians, macroinvertebrates and Ventura, M., and J. Catalan. 2005. Reproduction as one of the main causes of crustaceans. temporal variability in the elemental composition of zooplankton. Limnology and Oceanography 50:2043-2056. To understand the importance of local adaptation we focused first on the Ventura, M., and J. Catalan. 2008. Incorporating life histories and diet quality cladoceran Daphnia longispina Müller in stable isotope interpretations of crustacean zooplankton. Freshwater Bio- 1776, finding that its distribution is logy 53:1453-1469. explained by a single colonization event and subsequent dispersion along the Ventura, M., and J. Catalan. 2010. Variability in amino acid composition of mountains (Ventura et al. 2014). We alpine crustacean zooplankton and its relationship with nitrogen-15 fractio- are also conducting similar studies with nation. Journal of Plankton Research 32:1583-1597. other species of crustaceans such as Daphnia pulicaria Forbes, 1893 (Dufresne Ventura, M., A. Petrusek, A. Miró, E. Hamrová, D. Buñay, L. De meester, and J. et al. 2011, Vergilino et al. 2011). For Mergeay. 2014. Local and regional founder effects in lake zooplankton persist some of the species we have had to after thousands of years despite high dispersal potential. Molecular Ecology solve their taxonomic status, such as for 23:1014-1027. the cyclopoid copepods of the genus Cyclops (Krajicek et al. 2016) or for an Vergilino, R., S. Markova, M. Ventura, M. Manca, and F. Dufresne. 2011. Reticu- anostracean of the genus Phallocryptus late evolution of the Daphnia pulex complex as revealed by nuclear markers. (Alonso and Ventura 2013). Molecular Ecology 20:1191-1207.

71 Sometimes the fieldwork has to be carried out in remote places and under extreme conditions, but these difficulties do not intimidate CEAB scientists. Our doctoral theses CAPACITY BUILDING OF THE CENTRE FOR ADVANCED STUDIES OF BLANES (1990-2015)

92 DOCTORAL THESES 2015

D’Souza, Elrika (2015) Seagrass ecosystems of the Nicobar and Andaman Islands with emphasis on the Dugong dugon status and distribution. Madurai Kamaraj University (India). PhD Advisor: Teresa Alcoverro Farina, Simone (2015) Scale-dependent factors modulate sea urchin predation in macrophyte ecosystems. Universitat de Barcelona. PhD Advisor: Teresa Alcoverro Llorens, Tomás (2015) Connecting biodiversity and biogeochemical role by microbial metagenomics. Universitat de Barcelona. PhD Advisor: Emilio O. Casamayor Lupon, Anna (2015) The influence of Mediterranean riparian zones on stream nitrogen dynamics. A catchment approach. Universitat de Barcelona. PhD Advisor: Susana Bernal Best Spanish PhD Dissertation in Limnology Research (2014- 2015) Merbt, Stephanie (2015) Microbial nitrification in urban streams: from single cell activity to ecosystems processes. Universitat de Barcelona. PhD Advisors: Eugènia Martí & Emilio O. Casamayor EFFS Award for the best PhD Dissertation in Freshwater Sciences (2015-2016) Ribot, Miquel (2015) Effects of human activities on N cycling in Mediterranean streams: contrasts between nitrate and ammonium dynamics. Universitat de Barcelona. PhD Advisor: Eugènia Martí Roca, Guillem (2015) Tracking environmental change in seagrass meadows: understanding indicator behaviour across space and time. Universitat de Barcelona. PhD Advisors: Teresa Alcoverro & Javier Romero 2014

Ahumada-Semproa, Miguel A. (2014) The Northern Current and its interaction with the Blanes submarine canyon (NW Mediterranean Sea). Universitat Politècnica de Catalunya. PhD Advisor: Antonio Cruzado Bacher, Kathrin (2014) Interactions between fish farming, wild fish populations, local fisheries and society: a case studyin Catalonia, Spain. Universitat de Barcelona. PhD Advisor: Ana Gordoa Peipoch, Marc (2014) The role of primary uptake compartments on stream N cycling, insights from 15N signatures. Universitat de Barcelona. PhD Advisors: Eugènia Martí & Esperança Gacia Rivera Roldon, Carlos (2014) Diatom-based reconstruction of Late Glacial and Early Holocene environment in the Pyrenees. Universitat de Barcelona. PhD Advisor: Jordi Catalan 2013

Caraballo, Tatiana (2013) The ecology of colonial phytoplankton. Universitat de Barcelona. PhD Advisor: Jordi Catalan Cardoso, G. (2013) Development of a model for the study of the dispersion of pollutants from a shrimp farm in the Estero de Urías lagoon complex: an urbanized coastal lagoon (Mexico). Universitat Politècnica de Catalunya. PhD Advisors: Antonio Cruzado & Joan A. Sánchez

74 De Mendoza, Guillermo (2013) Lake macroinvertebrates and the altitudinal gradient in the Pyrenees. Universitat de Barcelona. PhD Advisor: Jordi Catalán Fernández-Guerra, Antoni (2013) Ecology and evolution of microbial nitrifiers. Universitat de Barcelona. PhD Advisor:Emilio O. Casamayor Gera, Alessandro (2013) Landscape fragmentation and resilience in seagrass meadows. Universitat de Barcelona. PhD Advisor: Teresa Alcoverro Ordoñez, Victor (2013) Ecology and genetics of invasive ascidians in the western Mediterranean. Universitat de Barcelona. PhD Advisor: Xavier Turon Pagés, Jordi (2013) The role of herbivores as trophic connectors between marine ecosystems. Universitat de Barcelona. PhD Advisor: Teresa Alcoverro Pérez-Porro, Alicia R. (2013) Differential gene expression along the sponge life cycle. Universitat de Barcelona. PhD Advisors: Iosune Úriz & Gonzalo Giribet de Sebastán Sacristán, Oriol (2013) Chemical and microbial ecology of the demosponge Aplysina aerophoba. Universitat de Barcelona. PhD Advisor: Mikel Becerro Schunter, Celia (2013) Challenges in marine ecology: genomic investigations of dispersal patterns and phenotypic plasticity in Mediterranean Fishes. Universitat de Barcelona. PhD Advisor: Enrique Macpherson Wangensteen, Owen (2013) Biology and phylogeography of the black sea urchin Arbacia lixula (Echinoidea: Arbacioida). Universitat de Barcelona. PhD Advisor: Xavier Turon

2012

Ballen, Miguel Angel (2012) Study of the phagotrophic activity of phytoplankton by cellular analysis techniques. Universitat de Barcelona. PhD Advisors: Jordi Catalan & Marisol Felip Barberán, Albert (2012) Microbial macroecology: understanding microbial community patterns using phylogenetic and multivariate statistical tools. Universitat de Barcelona. PhD Advisor: Emilio O. Casamayor. UB Doctorate Extraordinary Award García Merchán, Victor H. (2012) Population genetic structure and oceanographic discontinuities in decapod crustaceans. Universitat de Barcelona. PhD Advisor: Enrique Macpherson Lozoya, Juan Pablo (2012) Multi-risk assessment and users’s perception: a further step towards Ecosystem-Based Beach Managament. Universitat de Barcelona. PhD Advisor: Rafael Sardá Núñez, Laura (2012) Chemical ecology in the Antarctic marine benthos: natural products and chemical defense in hexactinelid sponges, soft corals and colonial ascidians. Universitat de Barcelona. PhD Advisor: Manuel Maldonado Pineda, Mª Carmen (2012) A global wanderer: biology, phylogeography and resilience of the introduced ascidian Styela plicata. Universitat de Barcelona. PhD Advisors: Xavier Turon & Susana López UB Doctorate Extraordinary Award Serrano, Letzi (2012) Distribution of soft-bottom Polychaete assembalges at different scales in shallow waters of the Northern 2011

Bacardi, Montserrat (2011) Trace element biogeochemistry in high mountain lake catchments: identifying anthropogenic versus natural components from the atmospheric contamination legacy in remote natural areas. Universitat de Girona. PhD Advisor: Luis Camarero Chappuis, Eglantine (2011) The aquatic macrophytes of lakes, ponds and lagoons of Catalonia. Universitat de Barcelona. PhD Advisors: Esperança Gacia & Enrique Ballesteros Gil, Joao (2011) The european fauna of Annelida Polychaeta. Universidade de Lisboa (Portugal). PhD Advisor: Rafael Sardá

75 Serrano, Oscar (2011) Insights in the mat of Posidonia oceanica: biogeochemical sink and paleoecological record. Universitat de Barcelona. PhD Advisor: Miguel Ángel Mateo Soto, David Xavier (2011) Combining trace metal bioaccumulation and stable isotopes to reveal food web structure in freshwater ecosystems. Universitat de Barcelona. PhD Advisors: Esperança Gacia & Jordi Catalán Best PhD Thesis for the Iberian Association of Limnology (biennium 2010-2012) and Finalist of the Best PhD Thesis for The European Federation for Freshwater Sciences (EFFS) Award (biennium 2011-2013) 2010

Argerich, Alba (2010) Hydrological and geomorphological controls on stream nutrient retention. Universitat de Barcelona. PhD Advisors: Eugènia Martí & Francesc Sabater Bernardello, Raffaele (2010) A 3D high resolution coupled hydrodynamic biogeochemical model for the Western Mediterranean Sea. Interannual variability of primary and export production. Universitat Politècnica de Catalunya. PhD Advisor: Antonio Cruzado Bucci, Arianna (2010) Coastal microphytoplankton and microphytobenthos. Diversity, ecology and implications in silicon biogeochemical cycle. Universitat de Barcelona. PhD Advisors: Manuel Maldonado & Zolia Velásquez Cabezas, Patricia (2010) Systematics and evolutionary history of the family Galatheidae (Crustacea: Anomura) in the South Pacific. Universidad Autónoma de Madrid. PhD Advisor:Enrique Macpherson Llirós Dupré, Marc (2010) Diversity, dynamics and activity of mesophilic Archaea in stratified freshwater lakes. Implications in biogeochemical cycles. Universitat de Girona. PhD Advisors: Emilio O. Casamayor & Carlos Borrego Noyer, Charlotte (2010) Relationship between genetic, bacterial, and chemical diversity of the Mediterranean sponge Spongia agaric. Universitat de Barcelona. PhD Advisor: Mikel Becerro Salles, Marta (2010) Cystoseira-dominated assemblages from sheltered areas in the Mediterranean Sea; diversity, distribution and effects of pollution. Universitat de Girona. PhD Advisor: Enrique Ballesteros Sánchez-Cámara, Jaime (2010) “Biology and Ecology of the weedy sea dragon Phyllopteryx taeniolatus (Pisces: Syngnathidae) and its implication in conservation management. Universitat de Barcelona. PhD Advisors: Xavier Turon & David J. Booth Vassal’lo Saco, Jara (2010) Communities of benthic cyanobacteria, production and release of microcystins in the Muga River (NE Iberian Peninsula). Universitat de Girona. PhD Advisor: María Ángeles Puig Villamor, Adriana (2010) Biology and Ecology of Mediterranean rocky bottoms asteroids. Universitat de Barcelona. PhD Advisor: Mikel Becerro 2009

Bartrons, Mireia (2009) Food web bioaccumulation of halogenated compounds in high mountain lake food webs. Universitat de Barcelona. PhD Advisors: Jordi Catalan & Joan Grimalt Calderón, Isabel (2009) Spatio-temporal genetic structure and reproductive barriers in the genus Paracentrotus (Echinodermata: Echinoidea). Universitat de Barcelona. PhD Advisors: Xavier Turon & Cruz Palacín García López, Juan Antonio (2009) Genomic patterns and phenotypic plasticity in prokaryotes analyzed within an ecological framework. Universitat Autònoma de Barcelona. PhD Advisor: Emilio O. Casamayor Hervàs, Anna (2009) Bacterial dispersal on airborne Saharan particles. Survival and colonization in Alpine lakes of the limnological observatory of the Pyrenees. Universitat Autònoma de Barcelona. PhD Advisor: Emilio O. Casamayor Latting, Patricia (2009) Review of species of the genus Haplosyllis (Annelida, Polychaeta, Syllidade): A morphological, morphometric, phylogenetic and ecological approach. Universitat Autónoma de Madrid. PhD Advisors: Daniel Martin & Guillermo San Martín

76 2008

Benito, Gervasio (2008) The role of benthic macroinvertebrates as a bioindicators in the control network of the ecologic quality of basins of Catalonia. Influence of water regime on the structure of the population. Universitat de Barcelona. PhD Advisor:María Ángeles Puig & Miquel Selgot Martínez, Begoña (2008) Assessing the status of coastal waters: monitoring tools based on the ecosystems of Posidonia oceanic. Universitat de Barcelona. PhD Advisor: Teresa Alcoverro 2007

Ariza, Eduardo (2007) A set of indicators as a tool for beach management. Universitat Politècnica de Catalunya. PhD Advisor: Rafael Sardá Blanquer, Andrea (2007) Molecular markers for phylogenetic and population studies of the genus Scopalina (Porifera: Demospongiae. Universitat de Barcelona. PhD Advisor: María Jesús Úriz Brenner-Guillermo, Jorge (2007) Valuation of Ecosystem Services in the Catalan Coastal Zone. Universitat Politècnica de Catalunya. PhD Advisors: Rafael Sardá & José Antonio Jiménez Cebrian, Emma (2007) Sublethal effects of metal contamination on marine sponges: responses at different biological levels. Universitat de Barcelona. PhD Advisor: María Jesús Úriz De Caralt, Sonia (2007) Sponge culture: learning from biology and ecology. Wageningen University (Holland). PhD Advisor: María Jesús Úriz Prado, Patricia (2007) Study of herbivores and their effects on the ecosystems of Posidonia oceánica. Universitat de Barcelona. PhD Advisors: Teresa Alcoverro & Javier Romero Riesgo, Ana (2007) Gametogenesis, fertilization and embryonic development of coastal marine sponges: Ecological and evolutionary implications. Universitat de Barcelona. PhD Advisors: Manuel Maldonado & Mercè Durfort Vergés, Adriana (2007) Defence strategies of marine macrophyte. Universitat de Barcelona. PhD Advisors: Teresa Alcoverro & Javier Romero 2006

Carreras, Josep (2006) Phylogeny, phylogeography and population structure in litoral fishes with different dispersal capabilities. Universitat de Barcelona. PhD Advisors: Enrique Macpherson & Marta Pascual Linares, Cristina (2006) Population ecology and conservation of a long-lived species: the red gorgonian Paramuricea clavata. Universitat de Barcelona. PhD Advisors: Rafael Coma & Joaquim Garrabou Meserburger, Gora (2006) Nutrient dynamics and metabolism in Mediterranean streams affected by nutrient inputs from human activities. Universitat de Barcelona. PhD Advisors: Eugènia Martí & Francesc Sabater 2005

Bartumeus, Frederic Lévy processes in animal movement and dispersal. Universitat de Barcelona. PhD Advisors: Jordi Catalán & Ricard V. Solé UB Doctorate Extraordinary Award and Finalist of the UB Doctor’s Cloister Award Buchaca, Teresa (2005) Pigments indicators: study of lakes in the Pyrenees signal and its application in Paleolimnology. Universitat de Barcelona. PhD Advisor: Jordi Catalán Ramon Margalef of Ecology Award by the Institute of Catalan Studies

77 Ortiz, Jesús (2005) Response of stream benthic communities to changes in discharge and nutrient availability. Universitat de Girona. PhD Advisors: María Ángeles Puig & Manel Poch Pljuscheva, María V. (2005) The population structure and seasonal dynamics of Lepidonotus squamatus (Polychaeta, Polynoidae) in the White Sea. Institute of Animal Ecology (Moscow, Russia). PhD Advisors: Daniel Martín & A.N. Severzov Tridu, Carlo (2005) Implications of Aquaculture Development in the Littoral Zone of the Western Mediterranean. Universitat de Barcelona. PhD Advisor: Rafael Sardá Ventura, Marc (2005) Crustacean zooplankton dynamics in Lake Redon: A stoichiometric, biochemical and isotopic approach. Universitat de Barcelona. PhD Advisor: Jordi Catalán 2004

Mora Crespo, Joan (2004) Design of an environmental information system for use in integrated coastal zone management: application to the Costa Brava. Universitat de Girona. PhD Advisor: Rafael Sardá Raventós, Nuria (2004) Reproduction patterns and early life stages ecology of the nesting fish Symphodus roissali (Risso). Universitat de Barcelona. PhD Advisor: Enrique Macpherson 2003

Grimaldo, N.S. (2003) Evolution of phytoplankton through river, coastal and pelagic systems in front of the Ebro River Delta, Mediterranean Sea NW. Universitat Politècnica de Catalunya. PhD Advisor: Antonio Cruzado 2002

Bahamon, Nixon (2002) Dynamics of Oligotrophic Pelagic Environments: NW Mediterranean Sea and Subtropical North Atlantic. Universitat Politècnica de Catalunya. PhD Advisor: Antonio Cruzado Mariani, Simone (2002) Structure and chemical ecology of sponge larvae and newly recruits. Universitat de Barcelona. PhD Advisors: María Jesús Úriz & Xavier Turon Martí Lluch, Ruth (2002) Spatial and temporal variation of the natural toxicity in benthic communities of Mediterranean caves. Universitat de Barcelona. PhD Advisors: María Jesús Úriz & Xavier Turon UB Doctorate Extraordinary Award Vega, Cristina (2002) Chemical ecology and biological cycle of Zigomycale parishi (Porifera: Demospongiae). Universidad Nacio- nal Autónoma de México (Mexico). PhD Advisors: María Jesús Úriz & J.L. Carballo 1999

Zika, Ulrike (1999) Factors affecting settlement and post- settlement processes in littoral marine fishes, focusing onAidablennius sphinx. Swiss Federal Intitute of Technology Zurich (Switzerland). PhD Advisor: Enrique Macpherson 1998

Pinedo, Susana (1998) Structure and dynamics of Western Mediterranean soft-bottom communities along a disturbance gradient. Natural and man-induced viariability in the bay of Blanes. Universitat de Barcelona. PhD Advisors: Rafael Sardá & Xavier Turon

78 1997 Velasquez, Z. (1997) Phytoplankton in the North West Mediterranean. Universitat Politècnica de Catalunya. PhD Advisor: Antonio Cruzado 1996

Cardell, María José (1996) Structure and dynamics of the benthic macrofauna in marine sediments submitted to domestic and industrial discharges: effect of the waters and residual sludge of the treatment plant of Sant Adrià del Besòs (Barcelonès). Universitat de Barcelona. PhD Advisor: Rafael Sardá Muniz Pereira da Costa, K. (1996) Distribution of nutrients in the western Mediterranean (Gulf of León and Catalan Sea). Influence of physical factors. Universitat Politècnica de Catalunya. PhD Advisor:Antonio Cruzado Rosell, Dolors (1996) Systematics, biology and ecology of the Mediterranean excavating sponges. Universitat de Barcelona. PhD Advisor: María Jesús Úriz UB Doctorate Extraordinary Award 1995

Domingo Gou, Marta (1995) An expert system architecture for taxonomic domains. An application in Porifera: the development of spongia. Universitat de Barcelona. PhD Advisors: María Jesús Úriz & C. Sierra 1994

Becerro, Mikel (1994) Chemically mediated bioactivity of the encrusting sponge Crambe crambe: ecological implications. Universitat de Barcelona. PhD Advisors: Maria Jesus Úriz & Xavier Turon 1993

Alarcón, M. (1993) Simulation of long-range atmospheric transport on the northwestern Mediterranean: models of diffusion processes and career-deposition. Universitat de Barcleona. PhD Advisor: Antonio Cruzado Maldonado, Manuel (1993) The coastal sponges of Alboran: systematics and biogeography. Universitat de Barcelona. PhD Advisor: María Jesús Úriz 1991

Martin, Daniel (1991) Macroinfauna of a Mediterranean Bay: Study of the levels of organization of the populations of Annelida Poliquetos. Universitat de Barcelona. PhD Advisor: Rafael Sardá Varela, R.E. (1991) The deepest chlorophyll: Simulation of physical and biological processes. Universitat Politècnica de Catalunya. PhD Advisor: Antonio Cruzado 1990

Bibiloni, María Antonia (1990) Fauna of Baleares sponges: Qualitative and quantitative variations of the sponge population in a bathymetric gradient. Universitat de Barcelona. PhD Advisor: María Jesús Úriz

79 A CEAB scientists collecting samples and field data in a costal zone by direct sampling and in situ census.

30 YEARS

Centre d’Estudis Avançats de Blanes C/ d’accés a la cala de St. Francesc. 14 17300 Blanes (Girona) Tel 972 - 33 61 01 Fax. 972 - 33 78 06 www.ceab.csic.es