cyanobacteria in ambient springs - 《湖泊科学》cyanobacteria in ambient springs: diversity;...

REVIEW PAPER

Cyanobacteria in ambient springs

Marco Cantonati • Jirı Komarek • Gustavo Montejano

Received: 24 August 2014 / Revised: 30 January 2015 / Accepted: 12 February 2015 /Published online: 21 February 2015� Springer Science+Business Media Dordrecht 2015

Abstract Although neglected for a long time by freshwater-ecology research, springs are

very important habitats for biodiversity conservation. They are multiple ecotones, and are

characterized by a remarkable variety of environmental conditions (e.g., from highly-

shaded to UV exposed, from permanent discharge to intermittent flow, from still water to

strong currents, from extremely-soft to carbonate-precipitating water, etc.). Moreover,

springs are often amongst the last high-integrity, oligotrophic freshwater habitats in

densely populated areas. Because of the high quality of their waters, the main impact

affecting springs is capturing and water diversion. Climate-change driven reduction in

precipitations in many areas is likely to determine an aggravation of this impact. It is thus

important to document the rich and peculiar biodiversity of springs, also to establish

reference conditions for bioassessment methods. Especially in non-acidic springs with

running water, and coarse lithic substrata, cyanobacteria are often one of the most taxa-rich

and abundant groups of photoautotrophs. The relatively-scarce information available in the

literature is mostly referred to similar habitats, and not to spring habitats in the narrower

sense. Papers dealing with the cyanobacteria of ambient springheads (=eucrenal) world-

wide are still very rare. These were reviewed separating ambient springs in temperate and

Communicated by Anurag Chaurasia.

M. Cantonati (&)Museo delle Scienze - MUSE, Limnology and Phycology Research Unit, Corso del Lavoro e dellaScienza 3, 38123 Trento, Italye-mail: [email protected]

J. KomarekFaculty of Biological Sciences, University of South Bohemia, Ceske Budejovice, Czech Republic

J. KomarekInstitute of Botany AS CR, Dukelska 135, 379 18 Trebon, Czech Republic

G. MontejanoFacultad de Ciencias, Laboratorio de Ficologıa, UNAM-Universidad Nacional Autonoma de Mexico,Avenida Universidad 3000, Ciudad Universitaria, 04510 Coyoacan, Federal District of Mexico City,Mexico

123

Biodivers Conserv (2015) 24:865–888DOI 10.1007/s10531-015-0884-x

warm climate, and with special attention to key species, to cyanobacterial strategies al-

lowing survival in oligotrophic headwaters (e.g., nitrogen fixation, phosphatases, anti-UV

compounds, etc.), and to distribution patterns. The review also hopes to bolster new

interest and research on this topic, and suggests some promising research directions.

Keywords Springs � Cyanoprokaryotes � Oligotrophy � Radiation � Nitrogen � Discharge

fluctuations

Introduction

Cyanobacteria are well adapted to oligotrophic environments, and are generally among the

dominant primary producers in spring habitats. Cyanobacteria or cyanoprokaryotes (Komarek

and Golubic 1990) are the most ancient oxygenic photoautotrophs, colonize a wide variety of

habitats including extreme ones, are important primary producers at the global scale (e.g.,

Sciuto and Moro 2015). Despite the many problems related to the application of species

concepts to these asexual prokaryotes, cyanobacteria include a remarkable diversity of mor-

photypes and genotypes (including cryptic species and genera) (Dvorak et al. 2014, 2015).

Springs are extremely diverse ecotones, which can be classified according to different

criteria derived from hydrology, geology, hydrochemistry, water temperature, ecology, and

human use (Glazier 2009). Various cyanobacterial taxa, which are very diverse in de-

pendence on environmental conditions, are important in the ecological system of springs,

but are also very variable in springs of various types. Springs are extremely endangered in

populated countries, and the study of the dominating cyanobacterial microflora is important

in relation to the control and conservation of water sources.

When several organism groups are used for spring classification (e.g., Spitale et al. 2012a),

cross-taxon congruency is weak (as shown by Nascimbene et al. 2011 for crenic photoau-

totrophs including cyanobacteria and algae). Thus spring conservation plans should not use

one group as a surrogate but consider different groups of organisms. Springs characterized by

a temperature approaching the mean annual air temperature (MAAT) in the drainage basin,

have traditionally been called cold springs, but they should be renamed ambient springs,

because cold springs should be those that have temperatures below the MAAT. By contrast,

thermal springs have water temperatures clearly higher than MAAT, while hot springs have

temperatures exceeding human-body temperature (Glazier 2009). Using a set of available

estimates, it was concluded that there should be worldwide on land (not considering

Antarctica) probably more than four ambient springs per km2 (global total [57 9 106).

Thermal springs would be much rarer: global total [105 (Glazier 2009). Most springs show

hydrochemical characteristics consistent with the general lithological classification of the

aquifer. However, several cases of springs with ‘‘special’’ hydrochemistry, characterized by

high concentrations of one or more ions and/or elements (e.g., sulphate, sulphide, iron,

arsenicum, copper etc.) also exist: these are called mineral springs. Most hot springs are also

mineral springs (e.g., Castenholz 1969).

Spring habitats are multiple ecotones (subaerial-submersed, springhead-spring stream,

groundwater-surface waters). They are of special relevance for biodiversity conservation

because of the high diversity they host. However, studies dealing with different organism

groups showed that high species numbers are generally found not in single springs but in

regional pools including sufficient numbers of sources representative of the different spring

types and geological substrata (Nascimbene et al. 2011; Cantonati et al. 2012a). Spring

866 Biodivers Conserv (2015) 24:865–888

123

assemblages moreover include high proportions of rare and red list taxa, and species that

are too sensitive to colonise other freshwater habitats that are more impacted in densely

populated and highly exploited geographic areas [named least-impaired habitat relicts

(LIHRe) by Cantonati et al. 2012a]. The main cause of this high diversity is likely to be the

remarkable variety of environmental conditions that the individual springs can represent

(e.g., from highly-shaded to UV exposed, from highly-stable, permanent discharge to

markedly-fluctuating or even intermittent flow, from still water to strong currents, from

extremely-soft to petrifying water etc.).

Starting from the three basic spring types (rheocrenes = flowing springs, helocre-

nes = seepages, limnocrenes = pool springs), several others were added, the main ones

being hygropetric springs or rock-face seepages, and the so called tufa springs, that should

more appropriately be named spring-associated-limestone (SAL) sources (Sanders et al.

2010). Spring types can be identified and characterized also by means of benthic algae

(Cantonati et al. 2012b).

Springs are very heterogeneous not only at the scale of habitat but also at the scale of

microhabitat, i.e. the different substrata within a spring (the most common ones are lithic

material, bryophytes, surface sediment, and organic debris). Springs are thus often said to

be microhabitat mosaics (Hajek et al. 2011; Hajkova et al. 2011; Cantonati et al. 2012a).

While cyanobacteria in hot springs have been more in depth studied and even recent

review papers are available (e.g., Ward et al. 2012), cyanoprokaryotes in ambient springs

are a neglected topic, in spite of ambient springs being numerous and widespread and of

the high ecological and evolutionary interest of cyanobacteria. When they are considered,

they are often studied in the frame of all benthic algae (this includes all prokaryotic and

eukaryotic algae that are macroscopic or form thalli or generate colorations visible by the

naked eye; Cantonati et al. 2012b).

The relatively-scarce information available in the literature is mostly referred to similar

habitats and not to the springs sensu stricto. There is, for instance, typically confusion

between springs and spring-fed streams, and not rarely it is virtually impossible to dis-

tinguish the data relative to springs from those referred to the running-water systems

studied (e.g., Hu and Xie 2013). Moreover, spring studies including cyanoprokaryotes are

rare (e.g., Dell’Uomo 1975), and were mainly carried out in the framework of researches

focused on other topics (e.g., hygropetric habitat, Golubic 1967; mountain streams, Kann

1978). Some of the early studies on periphyton algae in springs indicated that these

environments host no specific spring species (e.g., Whitford 1956; Whitford and Schu-

macher 1963), while a more recent investigation described a new red-alga species sup-

posed to be exclusive of spring habitats (Vis and Sheath 1996).

A literature search of the Institute for Scientific Information (ISI) Web of Knowledge

(publication period: all years, updated 9 August 2014, databases = SCI-EXPANDED,

SSCI, A and HCI) for the keyword ‘‘spring*’’, refining the search to the web-of-science

category ‘‘marine freshwater biology’’, and then searching within the results for ‘‘cyano*’’

yielded 515 articles. However, direct inspection of titles and abstracts revealed that the

majority of these papers (490) were wrong matches (e.g., ‘‘spring’’ was the season etc.).

Thirteen were devoted to cyanobacteria in hot springs, while only twelve were really

dealing with cyanoprokaryotes in ambient springs.

The aim of this paper is to review the sparse and limited literature available on

cyanoprokaryotes in ambient springs to stimulate further research, and suggesting

promising research directions. The focus is on the biodiversity of cyanobacteria in ambient

springs, on their distribution in the different spring types, on cyanobacterial adaptations to

Biodivers Conserv (2015) 24:865–888 867

123

these special environments, and on the conservation status and impacts menacing this

component of ambient-spring biodiversity.

Cyanobacteria in ambient springs: diversity; main characteristics, rare taxa(temperate climate) (Fig. 1a–l)

The number of cyanoprokaryote taxa found in ambient springs is about 15-20 taxa every 10

springs investigated, and the number of cyanoprokaryote taxa per spring varies between 0 and

10 with an average of 4 (Table 1). A prevalence of coccoid types, with proportions typically

between 50 and 60 %, is evident. The most frequent and abundant genera are Chamaesiphon

(Fig. 1a, b, j), Tapinothrix (Fig. 1c), Phormidium (Figs. 1e, f), Leptolyngbya, Heteroleibleinia

(Fig. 1d), Pleurocapsa. Rare species include: Chamaesiphon amethystinus (Fig. 1j), Xeno-

tholos kerneri (Fig. 1k), Cyanodermatium sp., Myochrotes myochrous (Fig. 1i), Petalonema

spp., Tapinothrix bornetii (type species of the genus Tapinothrix), Gloeothece rupestris. The

most commonly studied spring type are rheocrenes, and consistently investigations focused

mostly on the epilithon (the most common substratum in this spring type; Table 1), more rarely

on the epibryon (Hasler and Poulıckova 2005; Cantonati 2008).

Some species are recorded frequently from springs (e.g., Chamaesiphon amethystinus,

Starmach 1929; C. confervicola-type species of the genus Chamaesiphon Golubic 1967; Ho-

moeothrix juliana, Komarek and Kann 1973), but none of them seems to thrive in spring

habitats only. In a longitudinal zonation study, Spitale et al. (2012b) found several species in the

eucrenon (spring head sensu stricto) (Chamaesiphon confervicola, C. investiens var. roseus,

Cyanodermatium sp.), whereas Chamaesiphon fuscus, C. polonicus, and Leptolyngbya frigida

were more abundant in epirhithral downstream sections (spring-fed stream).

Cyanobacteria in the different spring types

Helocrenic and limnocrenic springs

Early studies focusing on epilithon (Cantonati et al. 1996) noted that cyanoprokaryotes

were scarce or absent in helocrenic and limnocrenic springs in which muddy substrata

prevail, and rocky material is often unavailable. Cantonati et al. (1996) proposed the

following potential causes for the lack of cyanobacteria in these spring types: absence of

appropriate substratum for epilithic taxa, acidic conditions and high values of free carbon

dioxide often found in these spring types. Later studies confirmed this observation (Can-

tonati 2008; Cantonati et al. 2012b).

However, a cyanobacterial microflora of richness comparable to that usually found in

epilithon studies could be illustrated by Hasler and Poulıckova (2005), who studied epi-

bryon cyanoprokaryotes in Western Carpathian helocrenic springs. Cyanobacteria, how-

ever, were absent from acidic springs in this study as well, and were documented from

circumneutral and alkaline springs only.

Rheocrenic springs on siliceous substratum

There is a clear difference between the cyanoprokaryote assemblages in flowing springs on

siliceous and carbonate substratum. Even taxa vicariant in springs on the two substrata


123

Fig. 1 Some representative, characteristic, and rare cyanoprokaryotes from temperate-climate ambient-temperature springs. a Chamaesiphon confervicola, b Chamaesiphon starmachii, c Tapinothrix janthina(scale bar = 3 lm), d Heteroleibleinia purpurascens, e Phormidium favosum, f Phormidium retzii (? violetapex of P. insigne filament); g Tolypothrix penicillata (scale bar = 150 lm), h Rivularia biasolettiana(SAL spring) (scale bar = 50 lm), i Myochrotes myochrous (scale bar = 20 lm), j Chamaesiphonamethystinus, k Xenotholos kerneri (scale bar = 15 lm), l Schizothrix tinctoria (scale bar = 2 lm). If nototherwise stated, the scale bars equal 5 lm


123

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sco

nsi

der

ed;

elev

atio

nra

ng

e(m

a.s.

l.);

mic

roh

abit

atco

nsi

der

ed

No

.o

fta

xa

fou

nd

%C

.%

F.

%H

.%

Cy

.N

o.

of

tax

ap

ersp

rin

gav

erag

e(m

in–

max

)

Mai

nsp

ecie

sN

ote

san

dta

xa

of

spec

ial

inte

rest

Ref

eren

ces

Peg

o-O

liv

am

arsh

(Eas

tIb

eria

nP

enin

sula

6R

hin

arid

clim

ate

4–

75

25

10

02

–3

Calo

thri

xp

ari

etin

a,

Ho

mo

eoth

rix

juli

an

a,

Lep

toly

ng

bya

an

gust

issi

ma

,S

chiz

oth

rix

fasc

icu

lata

,T

ap

ino

thri

xcr

ust

ace

a

IMP

OR

TA

NT

NO

TE

:O

nly

mac

roal

gae

con

sid

ered

.

Can

tora

l-U

riza

and

Ab

oal

-S

anju

rjo

(20

10);

Gar

cıa

and

Ab

oal

(20

14);

Gar

cıa-

Fer

nan

dez

(20

14);

Gar

cıa-

Fer

nan

dez

and

Ab

oal

(per

son

alco

m.)

Peg

o-O

liv

am

arsh

(Eas

tIb

eria

nP

enin

sula

)

2IS

Pin

arid

clim

ate

52

06

02

09

01

–3

Calo

thri

xp

ulv

inata

,P

ho

rmid

ium

terg

esti

nu

m,

Ta

pin

oth

rix

vio

lace

a

Imp

ort

ant

no

te:

on

lym

acro

alg

aeco

nsi

der

ed

Can

tora

l-U

riza

and

Ab

oal

-S

anju

rjo

(20

10);

Gar

cıa

and

Ab

oal

(20

14);

Gar

cıa-

Fer

nan

dez

(20

14);

Gar

cıa-

Fer

nan

dez

and

Ab

oal

(per

son

alco

m.)

Vo

lusi

aB

lue

Sp

rin

g,

Blu

eS

pri

ng

Sta

teP

ark

,O

ran

ge

Cit

y,

Flo

rid

a,U

SA

1R

h-c

a;E

l1

52

77

30

58

15

Het

erole

ible

inia

kuet

zingii

,L

epto

lyn

gb

yasp

p.,

Osc

illa

tori

asp

p.,

Ph

orm

idiu

mcf

.re

tzii

Sti

cho

sip

hon

wil

lei,

Xen

oth

olo

ske

rner

i

Weh

r(p

erso

nal

com

m.)


123

Ta

ble

1co

nti

nued

Geo

gra

phic

loca

tio

nN

o.

of

spri

ng

sst

ud

ied

Ty

pes

of

spri

ng

sco

nsi

der

ed;

elev

atio

nra

ng

e(m

a.s.

l.);

mic

rohab

itat

con

sid

ered

No

.o

fta

xa

fou

nd

%C

.%

F.

%H

.%

Cy.

No

.o

fta

xa

per

spri

ng

aver

age

(min

–m

ax)

Mai

nsp

ecie

sN

ote

san

dta

xa

of

spec

ial

inte

rest

Ref

eren

ces

Sp

rin

gs,

Flo

rid

aS

tate

,U

SA

30

Rh-c

a,S

u1

05

31

60

93

3A

mp

hit

hri

xsp

.,C

alo

thri

xsp

.,L

yngb

yaep

iph

ytic

a,

Lyn

gb

yaku

tzin

gii

,L

yngb

yan

ord

ga

rdh

ii,

Osc

illa

tori

asp

lend

ida,

Ple

cto

nem

aw

oll

ei,

Xen

oco

ccu

ssp

.(h

ard-w

ater

spri

ng

s)

Wh

itfo

rd(1

95

6)

Pan

uco

Riv

erb

asin

,ce

ntr

alM

exic

o

14

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a,L

i-ca

;6

0-5

00

23

45

43

61

02

3B

lenn

oth

rix

ga

nes

hii

,C

ha

ma

esip

ho

nco

nfe

rvic

ola

,C

yano

cyst

ism

exic

an

a,

Het

erole

ible

inia

spp

.,H

om

oeo

thri

xju

lia

na,

Hyd

roco

ccus

rivu

lari

s,H

yell

acf

.fo

nta

na,

Mer

ism

op

edia

gla

uca

,P

leuro

capsa

min

or,

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plo

cast

rum

mu

elle

ri,S

tich

osi

pho

nfi

lam

ento

sus,

Xen

oco

ccu

sw

ille

i,X

.ke

rner

i

Cha

ma

eca

lyx

caly

cula

tus,

C.

swir

enko

i,C

hlo

rog

loea

epip

hyt

ica,

Hye

lla

kall

igra

mm

os,

Ro

mer

iasp

.,S

tich

osi

ph

on

exig

uu

s,S

.sa

nsi

bari

cus,

Xen

oth

olo

sh

ua

stec

an

us,

Xen

oco

ccus

bic

ud

oi

Mo

nte

jan

oet

al.

(20

00);

Car

mo

na-

Jim

enez

and

Mo

nte

jan

o(1

99

3)


123

Ta

ble

1co

nti

nued

Geo

gra

phic

loca

tio

nN

o.

of

spri

ng

sst

ud

ied

Ty

pes

of

spri

ng

sco

nsi

der

ed;

elev

atio

nra

nge

(ma.

s.l.

);m

icro

hab

itat

con

sid

ered

No

.o

fta

xa

fou

nd

%C

.%

F.

%H

.%

Cy

.N

o.

of

tax

ap

ersp

ring

aver

age

(min

–m

ax)

Mai

nsp

ecie

sN

ote

san

dta

xa

of

spec

ial

inte

rest

Ref

eren

ces

Am

acuza

cR

iver

Bas

in

3R

h-c

a;8

00

10

02

16

21

74

7–

Aphanoth

ece

mic

rosc

opic

a,

Ble

nn

oth

rix

ga

nes

hii

,C

alo

thri

xb

raun

ii,

Ch

am

aes

iph

on

con

ferv

ico

la,

Mic

roco

leus

lacu

stri

s,P

ho

rmid

ium

retz

ii,

Ple

uro

capsa

min

or,

Scy

ton

ema

coa

ctil

e

Cham

aec

aly

xsw

iren

koi,

Ha

pa

losi

ph

on

wel

wit

schii

,S

tich

osi

ph

on

san

sib

ari

cus,

Xen

oco

ccu

sb

icud

oi,

Xen

oco

ccu

sla

mel

losu

s

Val

adez

-C

ruz

etal

.(1

99

6)

C.

cocc

oid

;F

.fi

lam

ento

us

no

n-h

eter

ocy

tou

s;H

.h

eter

ocy

tou

s;%

Cy.

%o

fcy

ano

bac

teri

ao

ut

of

all

ben

thic

alg

ae;

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hel

ocr

enes

;L

ili

mn

ocr

enes

;R

hrh

eocr

enes

;H

yh

yg

rop

etri

csp

rin

gs;

sisi

lice

ous

subst

ratu

m;

caca

rbo

nat

esu

bst

ratu

m;

SA

Lsp

ring-a

ssoci

ated

-lim

esto

ne

sourc

es;

ISP

inla

nd

sali

ne

spri

ng

s;Ir

iro

nsp

ring

s;S

usu

lfu

rsp

ring

s;R

Gro

ck–gla

cier

spri

ngs;

Ffo

un

tain

s.M

icro

hab

itat

con

sid

ered

:E

lro

cky

mat

eria

l(e

pil

ith

on),

Eb

bry

oph

yte

s(e

pib

ryo

n),

Ss

surf

ace

sedim

ent,

Ep

bry

oph

yte

s?

vas

cula

rp

lan

ts(e

pip

hy

ton

).N

om

encl

atu

reo

fo

lder

pap

ers

was

up

dat

ed


123

Ta

ble

2C

yan

ob

acte

ria

inam

bie

nt

spri

ng

s:en

vir

on

men

tal

det

erm

inan

tsan

dad

apta

tio

ns

En

vir

on

men

tal

det

erm

inan

tA

dap

tati

on

so

fsp

ring

cyan

obac

teri

aS

tru

ctu

reo

rp

igm

ent

inv

olv

edT

axa

Ref

eren

ce

Hig

hir

rad

ian

cean

dh

igh

UV

Ph

oto

pro

tect

ion

.S

elec

tiv

ead

sorp

tio

no

fU

Vra

dia

tio

nS

cyto

nem

in,

MA

As

–C

anto

nat

iet

al.

(20

12

b,

20

14a)

;C

aste

nh

olz

and

Gar

cia-

Pic

hel

(20

12)

Sh

adin

gC

hro

mat

icad

apta

tio

nP

hy

coer

ith

rin,

ph

yco

cyan

in,

chlo

rop

hyll

.V

aria

ble

rati

os

Ch

am

aes

iph

on

sta

rma

chii

,C

.co

nfe

rvic

ola

,P

leu

roca

psa

au

ran

tia

ca

Can

tonat

iet

al.

(20

12

b,

20

14b)

‘‘P

urp

le’’

spec

ies

As

abo

ve

bu

tst

able

rati

os.

Het

erole

ible

inia

purp

ura

scen

s,P

ho

rmid

ium

tin

cto

rium

Can

tonat

iet

al.

(20

12

b,

20

14b)

Dis

char

ge

flu

ctu

atio

ns,

des

icca

tio

nT

hic

ksh

eath

sC

alo

thri

xp

ari

etin

a,

Ch

am

aes

iph

on

po

lon

icu

s,C

.st

arm

ach

ii,

Ple

uro

capsa

au

ran

tia

ca,

Glo

eoca

psa

spp

.

Can

tonat

i(2

00

8);

Can

tonat

iet

al.

(19

96,

20

12

b);

Mai

er(1

99

5);

Rott

etal

.(1

99

9);

Ges

ieri

chan

dK

ofl

er(2

01

0);

Ges

ieri

chan

dR

ott

(20

04)

Res

tin

gst

ages

Nutr

ients

:nit

rogen

Dia

zotr

ophis

mH

eter

ocy

tes

To

lyp

oth

rix

pen

icil

lata

Can

tonat

i(2

00

8);

Can

tonat

iet

al.

(19

96,

20

12

a,b,

c);

Ges

ieri

chan

dR

ott

(20

04)

Het

ero

cyte

sin

SA

Lsp

rin

gs

tofi

xat

mo

sph

eric

Nd

uri

ng

des

icca

tio

np

erio

ds

Myo

chro

tes

myo

chro

us,

Pet

alo

nem

aa

latu

mG

esie

rich

and

Ko

fler

(20

10)

Nutr

ients

:phosp

horu

sU

tili

zati

on

of

org

anic

ph

osp

ho

rus

com

po

und

sH

airs

–C

anto

nat

iet

al.

(20

12

b);

Mu

no

z-M

artı

net

al.

(20

14)

Chem

ota

xis

Cal

yp

tra

–M

uno

z-M

artı

net

al.

(20

14)

Str

on

gcu

rren

tH

igh

ly-e

ffec

tiv

ead

hes

ion

mec

han

ism

s,to

ugh

and

flex

ible

fila

men

ts

Ad

hes

ion

pad

sC

ham

aes

iphon

gei

tler

i,C

.st

arm

ach

ii,

C.

fusc

us,

Cla

stid

ium

rivu

lare

,C

.se

tig

eru

m,

Ple

uro

copsa

au

ran

tia

ca,

Sti

cho

sip

hon

pse

udo

po

lym

orp

hu

s,T

apin

oth

rix

vari

an

s,H

eter

ole

ible

inia

purp

ura

scen

s

Can

tonat

i(2

00

8);

Can

tonat

iet

al.

(19

96,

20

12

b);

Ges

ieri

chan

dK

ofl

er(2

01

0);

Bac

khau

s(2

00

6);

Ges

ieri

chan

dR

ott

(20

04)


123

Ta

ble

2co

nti

nu

ed

En

vir

on

men

tal

det

erm

inan

tA

dap

tati

on

so

fsp

ring

cyan

obac

teri

aS

tru

ctu

reo

rp

igm

ent

inv

olv

edT

axa

Ref

eren

ce

?Gra

zin

g,

?co

mp

etit

ion

wit

ho

ther

ph

oto

auto

tro

ph

s

To

xin

(mic

rocy

stin

)p

rod

uct

ion

–R

ivu

lari

asp

p.,

To

lyp

oth

rix

dis

tort

a,

Sch

izo

thri

xfa

scic

ula

taA

bo

alet

al.

(20

05)

‘‘?’

’in

dic

ates

that

the

exac

tad

pti

ve

mea

nin

go

fo

fcy

ano

tox

inp

rod

uct

ion

insp

ring

sst

ill

has

tob

eel

uci

dat

ed


123

could be pointed out (siliceous/carbonate): Chamaesiphon fuscus/C. geitleri, Tapinothrix

janthina (Fig. 1c)/T. varians (Cantonati et al. 1996, 2012b).

Flowing springs on siliceous substratum often host rich cyanobacterial assemblages

including taxa adapted to low conductivity and alkalinity (Chamaesiphon starmachii,

Fig. 1b; Tapinothrix janthina, Fig. 1c), high discharge and strong current (Chamaesiphon

fuscus; Heteroleibleinia purpurascens, Fig. 1d) (Table 2) (Cantonati et al. 2012b).

Rheocrenic springs on carbonate substratum

The few attempts to characterize spring types by means of benthic algae including

cyanobacteria usually point out different kinds of flowing springs on carbonate substratum

e.g.: mid-altitude, oligotrophic rheocrenes; and low-altitude, mostly shaded, slightly

N-enriched rheocrenes. The former are characterized by desiccation-tolerant (Pleurocapsa

aurantiaca), oligotraphentic (Xenotholos kerneri, Fig. 1k), and rheophilic (Tapinothrix

varians) cyanoprokaryotes, whilst the latter host eutraphentic (Pleurocapsa minor; Phor-

midium retzii, Fig. 1f), and large-discharge-preferring (Chamaesiphon geitleri) species

(Cantonati et al. 2012b).

Phormidium retzii was found by Dell’Uomo (1990) to be the dominant cyanoprokaryote

species in a large, low-elevation (100 m a.s.l.), slow-flowing rheocrene (Su Gologone karst

spring) draining limestones on the Isle of Sardinia.

Hygropetric springs

Rock-face seepages are more common on carbonate substratum. Cantonati et al. (1996)

found the highest number of cyanobacterial taxa in a carbonate hygropetric spring, and

Fig. 2 Some representative, characteristic, and rare cyanoprokaryotes from warm-climate ambient-temperaturesprings. a Symplocastrum muelleri, b Blennothrix ganneshi, c Hapalosiphon welwitschii, d Chamaecalyxswirenkoi, e Homoeothrix juliana, f Stichosiphon exiguus, g Xenotholos huastecanus (scale bar = 50 lm),h Chamaesiphon confervicola (scale bar = 10 lm), i Homoeothrix juliana, j Stichosiphon sansibaricus,k Hyella kalligrammos, l Merismopedia cf. glauca. If not otherwise stated, the scale bars equal 5 lm


123

attributed this finding to the fact that hygropetric springs include transition microhabitats to

other biotopes (dripping and wet rock walls). In agreement with this result, Gesierich and

Kofler (2010) noted a large proportion of pseudaerial taxa (e.g., from the genus Gloeo-

capsa) in a carbonate rock-face seepage (Table 2). Rivularia spp. (Figure 1h), Plectonema

tomasinianum, Ammatoidea normannii, Chamaesiphon minutus (mainly as an epiphyte of

other cyanobacteria), and Calothrix parietina were the cyanobacterial indicator taxa of this

spring type identified by Cantonati et al. (2012b).

Spring-associated-limestone (SAL) sources

SAL springs possess very distinctive benthic-algae assemblages in which cyanoprokaryotes

are dominant: Phormidium incrustatum, Tapinothrix crustacea, Myochrotes myochrous

(Fig. 1i), Dichothrix gypsophila, Gloeothece confluens, and Gloeocapsopsis spp. (Cantonati

et al. 2012b). Gesierich and Kofler (2010) found a large SAL spring to be dominated by large

black cushions of an association of pseudaerial cyanobacteria: Myochrotes myochrous and

Petalonema alatum. The relevance of Phormidium incrustatum in SAL springs was con-

firmed by Pentecost (2003), who stated that the species has a worldwide distribution (span-

ning latitudes 54�N–30�S), and that it is common on shaded spring-deposited travertines.

Inland saline springs

According to Garcıa and Aboal (2014), Aboal and Garcıa (personal com.), Cantoral-Uriza

and Aboal-Sanjurjo (2010), the characteristic cyanobacterial taxa of saline springs within a

marsh close to the sea and in an arid climate setting were: Calothrix pulvinata, Phormi-

dium tergestinum, and Tapinothrix violacea (Table 1). MC (unpublished data) found an

inland saline spring draining evaporite formations to include a species of Rivularia (R. sp.

aff. bullata) among the main macroalgae.

Iron springs

Iron springs are often acidic and dominated by filamentous green algae and iron bacteria

(Cantonati et al. 2012b). Accordingly, no cyanoprokaryotes were found by Gesierich and

Kofler (2010) in an iron spring dominated by green algae. Cantonati (2008) found only a

larger thallus of Phormidium corium in an iron spring but this colony thrived on leaf litter

only and did not develop on the stones, heavily encrusted by iron and manganese pre-

cipitates. Guasch et al. (2012) found no cyanobacterial denaturing gradient gel elec-

trophoresis (DGGE) operational taxonomic units (OTUs) in the spring mouth and in the

uppermost part of a canal fed by an iron spring.

Cyanobacteria in ambient springs in warm climate settings (tropical, subtropical,arid) (Fig. 2a–l)

Garcıa and Aboal (2014), Aboal and Garcıa (personal com.), Cantoral-Uriza and Aboal-San-

jurjo (2010) found the following cyanobacterial taxa to be indicators of freshwater carbonate

spring conditions in a coastal marsh: Calothrix parietina, Homoeothrix juliana (Fig. 2e, i),

Leptolyngbya angustissima, Schizothrix fasciculata, Tapinothrix crustacea (Table 1).


123

In 14 wells (bir) and four ambient-temperature springs (ain) in the El-Farafra Oasis in

the Western Desert of Egypt, mostly affected by direct human and cattle impact (organic

pollution), the main cyanoprokaryote taxa were the following: Oscillatoria jasorvensis var.

thermalis, Jaaginema thermale, Homeothrix juliana, Oscillatoria animalis, O. princeps, O.

limosa (Saber 2015; personal communication).

Ambient springs in warm climates host a rich and diverse cyanobacterial com-

munity, still poorly-known so far (Table 1). More in-depth, calcareous warm springs

(23–30 �C) are characterized by a complex community that includes epilithic, epi-

phytic, and metaphytic forms. In North America, Whitford (1956) studied 30 springs

in Florida State (USA), with temperatures from 21 to 30 �C. The springs studied

included, hard-water freshwater, oligohaline, mesohaline, and sulphide springs. He

reported 35 species of cyanobacteria. In hard-water freshwater springs the cyanobac-

teria found were: Amphithrix sp., Calothrix sp., Lyngbya epiphytica, Lyngbya kutzingii,

Lyngbya nordgardhii, Oscillatoria splendida, Lyngbya wollei (as Plectonema wollei),

and Xenococcus sp.

Recently Wehr (personal com.) found in Volusia Blue Spring, a karstic spring in Florida

State, Chroococcus sp., Heteroleibleinia kuetzingii, several unidentified species of Lep-

tolyngbya and Oscillatoria, including O. cf. limosa, Phormidium cf. retzii, Pleurocapsa cf.

minor; and the rare Stichosiphon willei, and Xenotholos kerneri.

Several calcareous springs have been studied in the central region of Mexico. Carmona-

Jimenez and Montejano (1993) and Montejano et al. (2000) studied several karstic springs,

with temperatures ranging from 22 to 37 �C (Table 1). Blennothrix ganneshi (Fig. 2b),

Homoeothrix juliana, and Symplocastrum cf. muelleri were widely distributed in all

springs. Particularly noteworthy is the epiphytic cyanobacterial community that includes

common species, such as Chamaesiphon confervicola (Fig. 2h), Chlorogloea epiphytica,

Chamaechalyx swirenkoi (Fig. 2d), Cyanocystis mexicana, Stichosiphon filamentosus,

Stichosiphon sansibaricus (Fig. 2j), Xenococcus bicudoi, Xenococcus willei, and Xeno-

tholos huastecanus (Fig. 2g). Rare species include Stichosiphon exiguus (Fig. 2f) and

Chamaecalyx calyculatus. In habitats with low light intensity, as springs emerging in

caves, it is common to find a special community, dominated by endolithic species of Hyella

(Fig. 2k), that grows together with the red alga Hildenbrandia angolensis.

Valadez-Cruz et al. (1996) studied a calcareous warm spring in the Hidalgo State, in

central Mexico, with temperatures ranging from 29 to 30 �C. Blennothrix ganeshii was the

most conspicuous cyanoprokaryote. Also common were Hapalosiphon welwitschii

(Fig. 2c), Microcoleus lacustris, Chamaesiphon confervicola, Phormidium retzii, and

Scytonema coactile. The epiphytic community includes Chamaecalyx swirenkoi, Sti-

chosiphon sansibaricus, Xenococcus bicudoi, and Xenococcus lamellosus.

A special situation was described by Garcia-Pichel et al. (2002) in a bottom-fed artesian

spring in the Mexican Chihuahuan Desert (Cuatro Cienegas karstic region). Cyanobacterial

centimetre-sized waterwarts, formed by an Aphanothece-like cyanobacterium, where

suspended within a central well by upwelling waters, and supported a community of

epiphytic filamentous cyanobacteria. Waterwarts contained calcite crystals, likely needed

as ballast to prevent washing out of the well.

In a small spring in Sao Paulo State (southeastern Brazil) with contrasting (very-low)

conductivity, two of the four occurring macroalgae were found to be cyanobacteria:

Lyngbya putealis, and Scytonema arcangeli (Necchi 1992).


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Cyanobacterial adaptations to the spring habitat

Ambient-temperature springs are characterized by a large variety of environmental con-

ditions, requiring a diverse set of adaptations to the cyanobacteria that colonize them

(Table 2).

As regards light exposures, adaptation to radiation range from UV exposure to deep

shade, and are similar to those observed for benthic cyanoprokaryotes in lakes with fluc-

tuating water level (Cantonati et al. 2014a, b). Cyanobacteria in high-elevation, hy-

gropetric, SAL springs thus often have yellow-brownish sheaths because of the presence of

the UV absorbing compound scytonemin (Castenholz and Garcia-Pichel 2012). By con-

trast, cyanoprokaryotes in forest springs are often purple-violet, because of permanently or

temporarily (chromatic adaptations) increased phycoerithrin-Chl a and/or phycocyanin-Chl

a ratios.

As regards water-level fluctuations, it might be recalled that many springs, especially on

carbonate substratum, are fed by small and surficial aquifers, and are thus highly unstable.

Cyanoprokaryotes thriving in them thus need to possess adaptations to withstand exposure

(see above) and desiccation. The latter consist usually in mucilages and thick sheaths: a

typical example is Chamaesiphon polonicus, a widespread taxon very common also in

springs both on carbonate and siliceous substratum.

As regards nutrient availability, nitrogen limitation is very rare, even in remote

mountain locations due to diffuse airborne pollution (Waldner et al. 2014). This might

explain the low proportion of heterocytous taxa often found in springs (Table 1). An

exception is represented by SAL springs, in which heterocytous cyanobacteria are well

represented. Gesierich and Kofler (2010) hypothesized that the high proportion of hete-

rocytous taxa in a SAL spring with largely developed hygropetric microhabitat might be an

adaptive strategy to warrant nitrogen supply in periods of desiccation. Diazotrophism in

springs is however likely to be much more widespread than can be suggested by the

occurrence and abundance of heterocytes. On the contrary, phosphorus is commonly

limiting in mountain and oligotrophic springs (e.g., Cantonati et al. 2012c). Adaptations by

cyanoprokaryotes colonizing springs include the production of phosphatases to gain access

to P in organic compounds. This is especially well documented for species provided with

so-called ‘‘hairs’’ (filamentous forms with long tapering ends). Another adaptation of lothic

cyanobacteria to P scarcity is the presence of calyptras, that are supposed to be involved in

the chemotactic location of P-rich microzones (e.g., Munoz-Martın et al. 2014). Phormi-

dium favosum (‘‘autumnale’’ group), one of the most widespread Phormidia in spring

habitats, commonly possesses calyptras on many apices in springs (Fig. 1e).

As regards water motion, large rheocrenes on siliceous substratum and karstic springs

can have important discharge and seasonally strong currents. Cyanobacteria thus need to

firmly anchor themselves to the substratum with adhesion pads etc. The most common

spring cyanoprokaryote species include a large proportion of rheophilic taxa (Table 2).

Aboal et al. (2005) demonstrated that cyanobacterial toxin production is widespread

also in high-ecological-integrity calcareous Mediterranean streams. Since several of the

species for which microcystins production was shown (Rivularia spp., Tolypothrix dis-

torta, Schizothrix fasciculata) occur also in springs, it is very likely that toxins might be

produced by cyanobacteria in ambient springs as well (Table 2). The exact adaptive

meaning of cyanotoxin production in high-integrity running waters still has to be elu-

cidated. One of the most plausible interpretations is that cyanoprokaryotes may use these

toxins for successful competition for space and nutrients with other primary producers, in

particular other algae, and as an anti-grazing defence. This might be particularly


123

important in resource-poor habitats and mostly of small to very-small dimensions, such

as springs.

Impacts and threats for ambient-spring cyanobacteria conservation

In spite of the many impacts affecting spring habitats, springs and spring organisms,

including cyanobacteria, are not at all or little considered by conservation legislation in the

different countries (Cantonati et al. 2012a). The main threat for spring-habitats remains

their systematic use for drinking water supply. This implies the destruction of the original

morphology, a severe impoverishment of the biota (e.g., Zollhofer 1997), and, in particular,

the disappearance of photoautotrophs. Spring capturing and tapping to obtain drinking

water or to generate hydro-electric power will increase even more in the future as a result

of climate change, with a reduction of precipitation being predicted for many areas.

Springs are further exposed to a series of direct (e.g., forest management) and indirect (e.g.,

nutrient or contaminant deposition in the drainage basin) impacts. Because of the small

dimensions and of the importance of the fringing semi-aquatic habitats, springs are ex-

tremely sensitive to disturbance factors, such as trampling damage by cattle, coverage by

sediment, stripping off of the surrounding vegetation, nutrient inputs etc. (e.g., Gesierich

and Kofler 2010, Niedermayr and Schagerl 2010).

Springs in near-natural conditions are continuously reduced in numbers even in pro-

tected areas. Strong and organised initiatives for spring conservation have been undertaken

only in a few countries (cf. Hotzy 2007). Springs are not especially mentioned within the

WFD (European Water Framework Directive, EU-WFD 2000), although the use of phy-

tobenthos (in the restricted sense of diatoms plus macrophytes, rarely all algae including

cyanobacteria and diatoms) is recommended as one key element, beside macroinverte-

brates, for the assessment of ecological water quality in rivers. There is only a general

comment given that attention should be deserved to the interfaces between groundwater

and surface waters.

Only a very-limited number of spring types is mentioned in the Annex I (‘‘Natural

habitat types of community interest whose conservation requires the designation of special

areas of conservation’’) of the 1992 European Union Directive on the conservation of

natural habitats and of wild fauna and flora:—SAL springs, ‘‘7220 Petrifying springs with

tufa formation (Cratoneurion)’’, priority habitat type;—some salt springs, ‘‘1340 Inland

salt meadows (Puccinellietalia distantis)’’;—some mineral-rich springs, ‘‘7160

Fennoscandian mineral-rich springs and spring-fens’’ (EU-HD 1992; Evans 2006; Jokic

and Galz 2007).

Springs and groundwater use is in general regulated by specific legislation, mostly

oriented toward drinking water use related prevention of microbiological contamination.

These regulations require the excavation of the spring mouth down to the bedrock (or

aquifer), and the construction of closed, mostly concrete, housing including several de-

position basins (i.e. a complete spring capturing). This kind of protection is exclusively

oriented toward the use of spring water for drinking water supply but ignores completely

the value of springs as natural habitats. In most disagreements over multiple uses of water,

at the international or local scale, assignment of water to maintain aquatic biodiversity is

usually disregarded (Poff et al. 2003). It is well known that springs are a fundamental

source of good quality water and they frequently occupy a place of distinction in cultures

and mythologies. On the contrary there is still very limited public awareness on the fact

that they are also special habitats of great importance for nature conservation. Biodiversity


123

conservation is a critical test of whether water exploitation or freshwater-habitat alterations

are sustainable. This assumption is a foundation for the use of freshwater organisms as

biomonitors of habitat quality and integrity (Dudgeon et al. 2006).

Freshwater habitats are biodiversity rich but unluckily also human-activities’ hotspots.

This has led to widespread habitat degradation (Strayer and Dudgeon 2010). The threats to

global freshwater biodiversity can be grouped under five interacting categories (Dudgeon

et al. 2006): (1) flow alteration, (2) habitat destruction or degradation, (3) over-exploita-

tion, (4) pollution, and (5) invasion by non-native species (e.g., Allan and Flecker 1993).

Global-scale environmental changes, such as nitrogen deposition (e.g., Waldner et al.

2014), warming, and modifications in patterns of precipitation are superimposed upon all

these threat categories. An emblematic example relative to ambient springs, cyanobacteria,

and allochthonous and invasive species is provided by Florida springs. Stevenson et al.

(2007) showed that almost all large Florida springs had macroscopic algae growing in

them, an average of 50 % of the spring bottoms were covered by macroalgae, and

thickness of macroalgal mats was commonly half a meter. A cyanobacterium, Lyngbya

wollei, was one of the two most common invasive taxa (together with the xanthophyte

Vaucheria spp.).

For freshwater springs in the area of the Pego-Oliva marsh (East Iberian Peninsula) for

which long-term data were available, a change in the distribution and abundance of

Schizothrix fasciculata was observed. While 30 years ago it was more abundant in the

freshwater springs studied, it reduced its occurrence in these habitats but increased its

abundance in the source of a river that was also under observation. This species was found

to prefer low nutrient concentrations, and the changes in its abundance might be a response

to the increasing anthropogenic influences on the marsh (Cantoral-Uriza and Aboal-San-

jurjo 2010; Garcıa-Fernandez 2014; Garcıa and Aboal 2014).

Garcıa-Fernandez (2014), and Garcıa and Aboal (2014), while studying the macroalgae

of the Pego-Oliva marsh (see above) found that the springs, the less disturbed habitats of

the marsh, were rich in taxa linked to oligotrophic conditions and that have restricted

distributions. These species can be considered a LIHRe sensu Cantonati et al. (2012a).

Among drainage basins and water bodies there is relevant species diversification at

smaller geographic scales, and many freshwater species have restricted distribution (e.g.,

Strayer et al. 2004). These features combine with endemism to generate a ‘‘lack of sub-

stitutability’’ among freshwater habitats. It follows that protection of one or a few fresh-

water habitats cannot preserve all biodiversity in a region, or even a substantial proportion

of it (Dudgeon et al. 2006). Investigating springs in the Dolomiti Bellunesi National Park,

about 50 % of the cyanoprokaryotes and algae other than diatoms found could reasonably

be considered rare on the basis of the literature and experience (Cantonati 2008). The high

total number of taxa and the low diversity of the individual sites (Table 1) highlighted

again the marked heterogeneity of spring habitats, and the importance of protecting large

number of springs to preserve aquatic biodiversity (Nascimbene et al. 2011).

In addition, all the main microhabitats should be considered in biodiversity inventories,

as relevant differences among substrata have been demonstrated (Table 1; Cantonati et al.

2012a).

Best management practices (BMP) that are meanwhile established for streams, such as

restoration of old structures no longer in use or more sustainable ways of spring capturing,

are only very seldom applied to springs (and only to very specific spring types, in particular

SAL springs; Jokic and Galz 2007).

Cantonati et al. (2009) had to face the tapping for water abstraction by the local

municipality of one of their long-term monitoring springs (Gerecke et al. 2011). This


123

allowed them to show the potential value of residual habitats for spring biodiversity

conservation. They also noted the paramount importance of substrata, and of their exact

location, in determining which cyanobacteria taxa will colonize the residual habitat.

Conclusions and perspectives

Due to both under-appreciation of spring studies, and increasingly complex (and expen-

sive) approaches required for the characterization of cyanobacteria assemblages in near-

natural habitats, the literature on cyanoprokaryotes in ambient-temperature springs is very

limited.

However, some generalizations are possible. The marked heterogeneity of the spring

habitat requires a diverse set of adaptations (Table 2). Different types of ambient springs

are thus colonized by rheophilic, UV and radiation resistant, shade-tolerant, non-

diazotrophic, P-specialist (hairs and calyptras) cyanoprokaryotes. Cyanobacteria can suc-

cessfully be used to statistically characterize the diverse types of ambient springs (Can-

tonati et al. 2012b). Some morphotypes, e.g., Phormidium retzii in large karstic springs at

low elevation, Homeothrix juliana in ambient springs in arid regions, are regularly reported

from these habitats even from distant geographic locations. Coccoid types appear to

dominate in ambient springs in temperate climate while filamentous types appear to prevail

in ambient springs in warm and arid climates (Table 1).

The in-depth characterization of ambient-spring cyanoprokaryote assemblages is im-

portant because springs are biodiversity-rich but highly menaced ecotones. Moreover, if

adequately known, spring cyanoprokaryotes might provide a valid contribution to the

assessment of the ecological integrity, quality, and value for nature protection of spring

habitats.

If traditional morphotaxonomy is limited by its inability to unveil cryptic diversity, that

appears to characterize many cyanobacterial taxa (Dvorak et al. 2014, 2015), purely

metagenomic approaches to natural communities (e.g., DGGE, and cloning of the 16 S

rRNA gene) are often scarcely informative on the nature and ecological attributes of the

OTUs found (e.g., Junier et al. 2013), and even next generation sequencing approaches are

limited by the availability and correctness of data in molecular databases (GenBank etc.).

Thus, morphological, microscopic analysis still remains the quickest comprehensive

approach to the assessment of cyanobacterial diversity in ambient springs (compare

Manoylov 2014). However, given that these special habitats are still largely understudied,

the likelihood to find also problematic, rare, and new types is high. Molecular and phy-

logenetic studies are a valid support in these studies. These types are however often

difficult and/or time-consuming to cultivate. Therefore, the improvement of isolation and

single-cell and filament sequencing methods and techniques (Mares et al. 2015) will be

very important for research on cyanoprokaryotes in spring habitats. This will be relevant

also in the light of the fact that some of the most widespread taxa in ambient springs (e.g.,

Phormidium retzii), are known to hide cryptic species with different genotypes (Casamatta

et al. 2003). Improved molecular tools could thus allow to recognize spring-specific taxa

out of these apparently ‘‘cosmopolitan’’ species. In general, more widespread use of

molecular markers in the study of cyanobacteria in crenic habitats might help overcome

problems related to the fact that the descriptive literature on cyanobacterial taxonomy is

sometimes controversial, and that morphospecies identification can be doubtful when

morphological variability is high.


123

Most studies of ambient-springs cyanobacteria focused on the epilithon. Other substrata

of the spring microhabitat mosaic need to be more in-depth explored. In particular the

application of recent methods developed for the sampling of lake epipelon (Yang and

Flower 2009; Yang et al. 2010; Poulıckova et al. 2014) might greatly enhance our

knowledge on cyanobacteria in helocrenic springs.

Quantitative studies (e.g., Necchi 1992; Spitale et al. 2012b) occur still relatively rarely.

The same is true for functional aspects. Exceptions are provided by in-depth studies on the

ecophysiology of Lyngbya wollei from Florida springs (e.g., Sickman et al. 2009), and by

the investigation by Camacho et al. (2005), who showed how different ecophysiological

strategies, such as resistance and/or use of oxygen and sulfide, light adaptation, or resis-

tance to high current, allow each of the different microorganisms, including

cyanoprokaryotes, to efficiently colonize several areas within the environmental gradient a

cold sulfur spring. Functional aspects of ambient-spring cyanobacteria deserve more at-

tention in the future.

Some topics that urgently need to be developed in spring research in general (Cantonati

et al. 2012a) should be studied also with a focus on cyanoprokaryotes: continued devel-

opment of habitat-type and geographic-area specific indices to assess the quality of spring

habitats, development and testing of new strategies for non-destructive spring capturing

and for restoration of impacted habitats, improvement of long-term ecological research.

Acknowledgments MC was partially funded by the Autonomous Province of Trento while contributing tothis study. We are grateful to Dr. Nicola Angeli (Museo delle Scienze—MUSE, Limnology and PhycologyResearch Unit, Trento, Italy) for the layout of Fig. 1.

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