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Perspectives in Plant Ecology, Evolution and Systematics 14 (2012) 303– 309

Contents lists available at SciVerse ScienceDirect

Perspectives in Plant Ecology, Evolution and Systematics

j o ur nal homepage: www.elsev ier .de /ppees

esearch article

he dispersal of Halimeda in northern hemisphere mid-latitudes:alaeobiogeographical insights

arkus Reutera,∗, Werner E. Pillera, Sylvain Richozb

Institute for Earth Sciences, Graz University, Heinrichstrasse 26, 8010 Graz, AustriaCommission for the Palaeontological and Stratigraphical Research of Austria, c/o Institute of Earth Sciences, University of Graz, Heinrichstrasse 26, 8010 Graz, Austria

r t i c l e i n f o

rticle history:eceived 23 August 2011eceived in revised form 2 March 2012ccepted 20 March 2012

eywords:alaeobiogeographycologyceanographylimate changeediterranean

ersian Gulf

a b s t r a c t

The bryopsidalean alga Halimeda gained an important role as carbonate producer in Cenozoic tropicalcoral reefs and became a significant constituent of the modern Mediterranean seaweed flora. There are,however, open questions at which time the thermophile alga appeared in the cooler Mediterranean Seaand why it is not detected in coral reefs of the modern Persian Gulf. To unravel the biogeography andecology of Halimeda at its northern margin of distribution, we use fossil Halimeda records of the CentralParatethys/Medditerranean for comparison of the geological, (palaeo)ecological and evolutionary disper-sal constraints of the alga in the Miocene and Holocene Persian Gulf. The revealed spatial and temporaldistribution patterns of Halimeda in the regions of the Mediterranean and Arabian seas identify watertemperature as the major ecological constraint and the extreme Plio-Pleistocene climate changes as themotor for the dispersal and evolution of Halimeda in higher latitudes. Generally, the distribution of trop-ical species in higher latitudes was related to warm climate intervals during the Neogene. Accordingly,the available (palaeo)biogeographic data implies that the warm-adapted ancestors of the present-dayMediterranean H. tuna population possibly entered the Mediterranean Sea during the mid-Pliocene globalwarmth and became isolated during subsequent cooling. It also implies that the warm Persian Gulf water

is probably unsuitable for the cool-adapted H. discoidea population in the Gulf of Oman and that its tropicalancestors could have reached the Gulf of Oman only during a Pleistocene glacial phase when monsoon-induced upwelling of cold water in the Arabian Sea was reduced and the Persian Gulf fell dry. This exampledemonstrates the limitation of the actualistic palaeontological approach when using biota at the edgesof their distribution range as palaeoclimate proxy.

Iai1TcActb2

ntroduction

Halimeda Lamouroux (Chlorophyta, Bryopsidales) is a seg-ented calcified green alga, which is amongst the most important

ontributors of aragonite sediments to modern tropical and sub-ropical carbonate environments. Although there are contradictoryiews on its first appearance either in the Permian or Late Cre-taceous (Schlagintweit, 2010), the algae assumed its role aselevant sediment producer only in the early Cenozoic and retainedt until present-day (Hillis, 2001). After the final closure of theethyan Seaway has disconnected the Mediterranean Sea and

ndo-Pacific Ocean during the Middle Miocene (Harzhauser et al.,007a) Halimeda became an important member of the Late Mioceneediterranean carbonate factory (Braga et al., 1996; Pedley, 1996).

∗ Corresponding author.E-mail addresses: markus.reuter@uni-graz.at (M. Reuter), werner.piller@uni-

raz.at (W.E. Piller), sylvain.richoz@uni-graz.at (S. Richoz).

LsccesBc

433-8319/$ – see front matter © 2012 Elsevier GmbH. All rights reserved.ttp://dx.doi.org/10.1016/j.ppees.2012.03.003

© 2012 Elsevier GmbH. All rights reserved.

n the recent, Halimeda is globally represented by around 50 speciesnd occurs abundantly in reef regions worldwide, where it flour-shes in a variety of environments at depths ranging from <1 m to50 m (Hillis, 2001; Kooistra et al., 2002; Verbruggen et al., 2009).herefore, the alga is usually considered as indicator of past tropi-al sea surface temperatures in the geological record (Flügel, 1988).lthough it is known that within the sections Rhipsalis, Micronesi-ae, Pseudo-opuntia and Opuntia there is a marked conservatism forropical temperatures, several niche shifts into colder water haveeen documented within the section Halimeda (Verbruggen et al.,009). Modern Mediterranean Halimeda tuna (Ellis and Solander)amouroux populations for instance occur at sites with seasonalea surface temperature (SST) minima around 10 ◦C and the H. dis-oidea Decaisne population at the coast of Oman is affected byold upwelling water (Verbruggen et al., 2005, 2009). The north-

rnmost Halimeda occurrence is that of H. tuna on the Balearichelves in the Mediterranean Sea (Fornos et al., 1992; Canals andallesteros, 1997; Fig. 1). Based on molecular phylogenetics, it isonsidered that the invasion of tropical seaweeds such as Halimeda

304 M. Reuter et al. / Perspectives in Plant Ecology, Evo

Faw

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adwttpSti(tntrflwr(oldnb2peak is represented by the Halimeda specimens reported by Bucuret al. (1993) from the eastern part of the Central Paratethys (SimleuBasin, Rumania; Fig. 2b).

ig. 1. Study areas (1: Mediterranean Sea and Central Paratethys; 2: Persian Gulfnd Gulf of Oman; black stars: northernmost Halimeda occurrences at the recent;hite star: northernmost occurrence in the Miocene Central Paratethys).

nto temperate waters occurred due to global cooling since theate Paleogene (Verbruggen et al., 2009). At this time thermophilelgae may have been dispersed during periods of minimal glacia-ions across low latitudes (Hommersand, 1986; Verbruggen et al.,005). However, so far no palaeontological findings confirm theseypotheses.

Curiously, Halimeda is insignificant for carbonate productionn warm semi-enclosed shallow epicontinental seas such as theolocene Persian Gulf (Fig. 1) and the Middle Miocene Paratethysea (Hughes Clarke and Keij, 1973; Lees, 1975; Sohrabipour andabiei, 2007; Piller and Harzhauser, 2005; Riegl et al., 2010). Theeasons for this restriction are largely unclear. For the Persianulf the absence of certain, elsewhere important, skeletal con-tituents in carbonate sediments (e.g. Halimeda) is suggested to behe result of particular environmental factors or dispersial limita-ion since the Flandrian transgression (Purser and Seibold, 1973).n contrast, findings of Halimeda in Langhian and Serravallian lime-tones (Bucur et al., 1993, 2011) indicate that the alga was at leastemporarily able to migrate from the Mediterranean Sea into theentral Paratethys. Major constraints for the calcification of Hal-

meda are temperature, nutrients, salinity, alkalinity, pCO2 andg/Ca ratio of the ambient seawater (e.g. Drew and Abel, 1995;

iber and Irlandi, 2006; Stanley, 2008; Demes et al., 2009; Ries,009). Semi-enclosed shallow-marine water bodies such as theersian Gulf and the Central Paratethys are prone to rapidly switch-ng environmental conditions (Latal et al., 2006). This affects theistribution of marine biota, which live at their ecological limitsecause critical habitat thresholds are frequently crossed. There-ore, the comparison of carbonate production, oceanography, andlimate at different times with and without Halimeda occurrencesn the Central Paratethys and with the modern Persian Gulf condi-ions may offer an opportunity to shed light on the constraints foralimeda at its northern limit.

alimeda in the Paratethys Sea

The Paratethys Sea originated during the latest Eocene andarly Oligocene as a northern satellite basin of the Tethys Ocean

F1iaS

lution and Systematics 14 (2012) 303– 309

nd spread from the Rhone Basin in France towards Inner Asiauring its maximum extent (Rögl, 1998; Fig. 2). The Middle Mioceneas the climax of the Paratethyan carbonate production. At this

ime the southern part of the Central Paratethys was located athe transition zone between the tropical and temperate carbonaterovinces somewhat above 34◦N palaeolatitude (Esteban, 1996;cholger, 1998) what corresponds to the present-day position ofhe Libyan Sea (Eastern Mediterranean Sea). Middle Miocene Hal-meda were recorded by Bucur et al. (2011) from early Badenian=Langhian p.p.) bioclastic limestones overlying coral patch reefs inhe Transylvanian Basin (southeastern Central Paratethys, Ruma-ia; Fig. 2a). A new early Badenian Halimeda find originates fromhe Styrian Basin (Austria) in the southwestern Central Paratethysegion (Fig. 2a). At this locality Halimeda segments occur in theanking sediments of coral patch reefs. This succession is correlatedith the transgression of the TB 2.4 sea level cycle and has been

adiometrically dated by a volcanic ash layer to 14.39 ± 0.12 MaReuter and Piller, 2011; further references therein). After a phasef siliciclastic sedimentation during the early Sarmatian (=Serraval-ian p.p.) oolites and coquina-dominated sands started to spreaduring the late Sarmatian (=Serravallian p.p.) in shallow-marineearshore settings and on shallow shoals giving rise to small car-onate platforms (Piller and Harzhauser, 2005; Harzhauser et al.,007b; Piller et al., 2007). This second Middle Miocene carbonate

ig. 2. Palaeogeographical maps of the Middle Miocene Mediterranean region (Rögl,998; a: early Badenian/Langhian p.p.; b: early Sarmatian/Serravallian p.p.). Hal-

meda occurrences in the Central Paratethys (CP) are highlighted by yellow dots. Therrows indicate marine connections between the Paratethys, (Proto-)Mediterraneanea and Tethys. Doubtful marine connections are marked by question marks.

M. Reuter et al. / Perspectives in Plant Ecology, Evo

Fig. 3. Correllation chart showing the stratigraphic distribution of Halimeda (stars)and the main palaeogeographic and climatic events in the Middle Miocene CentralPtP

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aratethys (after Harzhauser et al., 2007b; de Leeuw et al., 2010). The correlation ofhe chronostratigraphy of Gradstein et al. (2004) with the regional stages followsiller et al. (2007) and Lirer et al. (2009); BSC: Badenian salinity crisis.

eological dispersal barriers

Vicariance and diversification of Halimeda lineages are mainlyttributed to the formation of geological barriers (e.g. closure ofhe Tethyan Seaway; Verbruggen et al., 2009). The Persian Gulf isonnected via the Strait of Hormuz with the Gulf of Oman (Ara-ian Sea) that enables the entry for reef corals and a variety ofther shallow-marine biota which are associated with Halimeda inhe Gulf of Oman but not for Halimeda (Hughes Clarke and Keij,973; Sohrabipour and Rabiei, 2007; Riegl et al., 2010; Fig. 1).imilar to this configuration the Trans-Tethyan Trench Corridoronnected the Central Paratethys with the Western Tethys/Proto-editerranean Sea during the early Badenian via Slovenia (Piller

t al., 2007; Figs. 2a and 3). Not only coral reefs but also Halimedaere situated at the northern entrance to this marine gateway in

he Styrian Basin. Rögl (1998) postulated also an open connec-ion to the Eastern Paratethys and from there into the Westernethys/Proto-Mediterranean Sea and Eastern Tethys (Fig. 2a). Thisastern seaway is, however, still controversial (Piller et al., 2007).he southwestern seastrait was finally closed in the late Bade-ian (Piller et al., 2007; Fig. 3). Therefore, the Sarmatian Centralaratethys became nearly completely sealed off (Fig. 2b). Dur-ng the Sarmatian the Central Paratethys was only connected

ith the Eastern Paratethys and from there with the Mediter-aneran Sea (Rögl, 1998) and possibly also with the Westernndo-Pacific (Filipescu and Silye, 2008; Fig. 2b). These marine pas-ages must have provided access for Halimeda to the eastern Centralaratethys.

abitat suitability in Middle Miocene Central Paratethysnd modern Persian Gulf – a comparison

emperature

The distribution of marine green algae is known to be stronglyoverned by temperature (van den Hoek, 1982). Tropical Halimedapecies have similar requirements than coral reefs (>18 ◦C duringhe cold season; Hillis-Colinvaux, 1980), while their cool-adaptedelatives tolerate seasonal sea surface temperatures (SST) minimaround 10 ◦C in the Mediterranean Sea (Verbruggen et al., 2009).he Middle Miocene Halimeda records in the Central Paratethysuccession correspond with two negative shifts in oxygen isotopealues both coinciding with warm climate intervals (Harzhauser

t al., 2007b; Fig. 3). The early Badenian oxygen isotope excur-ion is interpreted as to represent the global Mid-Miocene Climateptimum (Harzhauser et al., 2007b). For this climate intervalalaeotemperature estimates based on stable isotopes suggest a

aRtt

lution and Systematics 14 (2012) 303– 309 305

ST seasonality of 13–28 ◦C in the southern Central ParatethysBojar et al., 2004; Latal et al., 2006). However, these estimatestrongly rely on the �18O composition of the seawater, which canary locally due to evaporation and mixing with freshwater inhe relative restricted Paratethys basins (Harzhauser et al., 2007b).ccordingly, the composition of echinoid and mollusk faunas asell as the occurrence of complex coral reefs and Avicennia man-

roves indicates a higher minimum SST of 18 ◦C (Harzhauser et al.,007b; Kroh, 2007; Fig. 3). For the onset of the Middle Miocenelimate transition in the middle Badenian the decline of coral reefsnd thermophilous mollusk taxa indicates a drop in the mini-um SST from 18 ◦C to 14–15 ◦C (Harzhauser et al., 2007b; Fig. 3).

or the late Sarmatian warm interval water temperatures in theange of 18–26 ◦C are indicated by mass-occurrences of the largeroraminifer Spirolina and stable isotope data from mollusks (Pillernd Harzhauser, 2005; Murray, 2006; Harzhauser et al., 2007b;ig. 3). Even though the seasonal SST changes are regionally veryeterogeneous in the Persian Gulf (offshore: 20–32 ◦C; W Gulf:5.9–35.5 ◦C, lagoons: 15–40 ◦C) they allow extensive coral growthnd the development of several types of coral reef frameworksRiegl et al., 2010). Thus, at least in some parts of the gulf suitablerowth conditions for Halimeda should also exist.

utrients

Low nutrient availability is a factor often associated with thecological success of calcareous green algae and eutrophication is

primary factor leading to their demise (Delgado and Lapointe,994). In particular, elevated phosphate levels are suggested toegatively impact the biomineralization of Halimeda and interruptarbonate accretion by calcareous green algae through overgrowthy faster-growing fleshy algae (Delgado and Lapointe, 1994; Demest al., 2009). At the Middle Miocene Halimeda locality in the Styr-an Basin volcaniclastic sedimentation events from a close volcanicsland complex caused recurrent breakdowns of the carbonate pro-ucers in seagrass and coral reef environments and possibly alsof Halimeda. Biotic successions indicate that the nutrient releaserom dissolved volcanic ashes temporarily impaired the recruit-

ent of reef corals and seagrasses but favored the development oforalline red algae and suspension feeders (Reuter and Piller, 2011).he Persian Gulf water has a relatively low nutrient concentration.his has been attributed to the anti-estuarine circulation where thenly seawater source is the Indian Ocean surface water and Corioliseflection concentrates the incoming nutrients in the northern GulfRiegl et al., 2010). In contrast, surface waters along the coast of thenited Arab Emirates are depleted of nitrite (1.25 times), nitrate

1.72 times), phosphate (1.40 times) and silicate (1.06 times) inhe Persian Gulf compared to the Gulf of Oman (Shriadah, 1997).hort-time eutrophication incidents have been only recorded at theutlet of the Shatt al-Arab river and due to wind-driven (Shamal)pwelling in the northern Gulf (Alosairi et al., 2011; Fig. 4).

alinity

The presence of green algal skeletons in tropical carbonates iselated not only to temperature and nutrients but also to salin-ty (Lees, 1975). The normal marine fauna and flora of the earlyadenian Halimeda localities in the Styrian and Transylvanianasins prove evidence for a stable connection between Centralaratethys and Western Tethys/Proto-Mediterranean Sea (Trans-ethyan Trench Corridor; Fig. 2a) that promotes water exchange

nd normal marine conditions (Piller et al., 2007; Bucur et al., 2011;euter and Piller, 2011). In contrast, the Persian Gulf is amongsthe most saline water bodies in the world. Surface salinities inhe central parts of the Gulf average 37–40 psu, while shallow

306 M. Reuter et al. / Perspectives in Plant Ecology, Evo

Fig. 4. Distribution map of Halimeda discoidea (yellow dots) in the Persin Gulf (PG)and Gulf of Oman (after Wynne and Jupp, 1998; Sohrabipour and Rabiei, 2007)summarizing the main oceanographic features of the region (hatching: upwellingareas; brown area: riverine plume of the Shatt al-Arab river; red areas: high salinitywGR

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ater formation; arrows: water circulation; dashed line: coastline during the Lastlacial Maximum; UAE: United Arab Emirates; redrawn from Johns et al., 1999;ose, 2010).

arts along the Emirates’ coast have salinities of 40–50 psu, risingo 60–70 psu in remote lagoons and coastal embayments (Pursernd Seibold, 1973; Fig. 4). Decreasing species diversity in the Per-ian Gulf correlates with increasing salinity as effect of restrictionHughes Clarke and Keij, 1973). Halimeda has a relatively broadalinity tolerance (20–45 psu) but prefers higher and more stablealinities (Biber and Irlandi, 2006). Accordingly, Halimeda is dis-ributed in other marginal seas with increased salinity comparedo the open ocean (Red Sea: 40 psu, Eastern Mediterranean Sea:8 psu). An increased salinity is suggested for the late Sarmatianentral Paratethys too, due to the formation of pure oolithic car-onate sediments, the thick-shelled mollusk fauna, the occurrencef larger foraminifera as well as various kinds of marine cementsnd stable isotope values in gastropod shells (Piller and Harzhauser,005). In consistence with this observation, already Hughes Clarkend Keij (1973) noted that salinity alone cannot prevent the devel-pment of the full Arabian Sea species compliment in the Persianulf.

lkalinity and pCO2

Aragonite precipitation by Halimeda from seawater solutions isnfluenced by alkalinity and pCO2 (e.g. Stanley, 2008; Ries, 2009).he alkalinity-salinity diagram established by Brewer and Dryssen1985) for the Persian Gulf diverges clearly from the trend estab-ished for the Indian Ocean with a remarkable low alkalinity. The

ost divergent values were found along the Emirates’ coast wherehe greatest carbonate losses occur. High pCO2 values (360 ppm)re recorded in the CO2-rich upwelled water in the Gulf of OmanBrewer et al., 1978). The cooling of this water, by about 4 ◦C, ast flows to the north of the Gulf, would decrease pCO2 by 50 ppm.oss of CO2 due to biological activity (mainly by CaCO3 precipitationccessory by photosynthesis on nitrate) will give the peculiarly low

CO2 values of the today’s Persian Gulf. These peculiar alkalinitynd pCO2 distinguishes the Persian Gulf from other semi-enclosedeas and could be an argument a priori to explain the absence ofalimeda. However, low alkalinity and pCO2 are known to favour

altG

lution and Systematics 14 (2012) 303– 309

he precipitation of aragonite (Stanley, 2008) and should thereforeromote Halimeda. Another evidence that excludes alkalinity asajor constraint for Halimeda in warm semi-enclosed shallow epi-

ontinental seas is its occurrence in the late Sarmatian Paratethysor which a water chemistry highly supersaturated in respect toalcium carbonate and also with high carbonate alkalinity is sug-ested based on the occurrence of aragonite cements, microbialabrics and the disappearance of the serpulid Hydroides in Upperarmatian beds (Pisera, 1996; Piller and Harzhauser, 2005).

g/Ca ratio

The calcareous algae rise during the Cenozoic is linked withhe change from a calcite sea to an aragonite sea (Stanley, 2008;ies, 2009). Several laboratory experiments conducted at stan-ard conditions (1 atm pressure; T = 25 ◦C, pCO2 = 380 ppm) haveemonstrated that low-Mg calcite will precipitate from seawatert a Mg/Ca ratio <2, whereas aragonite and high-Mg calcite will pre-ipitate when Mg/Ca is >2 (Stanley, 2008; Ries, 2009). Halimeda andther calcareous algae began to be important carbonate producershen the Mg/Ca ratio rose from 1.5 in the Cretaceous to 2.5 in the

arly Cenozoic (Ries, 2009) and up to 5.2 in modern oceans. Theariations in seawater Mg/Ca ratio are caused by fluctuation in theate of ocean crust production. The transformation of fresh basalt inreenstone through hydrothermal circulation removes Mg2+ fromhe brine and releases Ca2+ to it (Hardie, 1996; Ries, 2009). Buthese changes are long term global process. Dolomite formationnd the deposition of magnesium sulphate evaporites can locallynfluence the Mg/Ca ratio (Stanley, 2008). In the sabkahs of theouth coast of the Persian Gulf a Mg/Ca ratio up to 40 has been mea-ured (Gunatilaka, 1991). The extensive deposition of dolomite andg-rich evaporites have thus uptaken the Mg, leaving a depletedg/Ca ratio in the water of the Gulf. For seawater with a normalodern Mg/Ca ratio of 5.2 temperature has no influence on the

atio, for seawater with a ratio between 3.0 and 1.0 a slight changen the temperature and/or pCO2 could cause a threshold changen the oceanic state (Morse et al., 1997). If Halimeda continues torow in the laboratory under calcite-sea conditions it produces upo 46% calcite. Its rates of calcification and primary productivity,owever, diminish significantly (Ries, 2009). Their slower growthates and smaller size would have reduced their ability to com-ete for space and sunlight and their reduced calcification wouldave favoured the grazing by fishes (Ries, 2009). Correspondingly,he Halimeda-free time interval in the Middle Miocene Centralaratethys succession coincides with a phase of massive evaporiteeposition in the Carpathian Foredeep at 13.81 ± 0.08 Ma (Bade-ian salinity crisis; de Leeuw et al., 2010; Fig. 3). Conflictingly withhis interpretation are, however, the anti-estuarine circulations inhe early and middle Badenian Central Paratethys (de Leeuw et al.,010) and Holocene Persian Gulf as well as the short residenceime of the Persian Gulf water (max. 3 years; Alosairi et al., 2011).ue to a counterclockwise circulation direction in the Persian Gulf

Alosairi et al., 2011; Fig. 4) it is unlikely that the Iranian coast isreatly influenced by seawater altered by evaporation.

mpact of Plio-Pleistocene climate changes on the dispersalf Halimeda

In summary, the main environmental controls for the calcifica-ion of Halimeda were identified as temperature, nutrients, salinity,

lkalinity, pCO2 and Mg/Ca ratio. In order to better constrain theimitations of Halimeda these parameters are compared betweenhe Middle Miocene Central Paratethys and the present-day Persianulf because these semi-enclosed shallow epicontinental seas are

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M. Reuter et al. / Perspectives in Plant Ecolog

t the northern margin of the alga’s distribution (Figs. 1 and 2) androne to rapidly switching environmental conditions. This com-arison shows that the Central Paratethys could have been only

ntermittently colonized by Halimeda in the Middle Miocene atimes when climate optima caused tropical water temperaturesith a minimum SST >18 ◦C (Fig. 3). However, the alga was not able

o colonize the warm Holocene Persian Gulf. Short-time eutrophi-ation events affect parts of the Persian Gulf but were also detectedor the early Badenian Styrian Basin (Central Paratethys) at timeshen Halimeda grew. Increased salinities occur in the Persian Gulf

ut do not restrict the settlement of Halimeda in the late Sarmatianentral Paratethys. Although a low alkalinity and pCO2, as present

n the Persian Gulf, stimulate the precipitation of aragonite by Hal-meda, the alga preferred the late Sarmatian Central Paratethys,

hich had, however, a high alkalinity. A depleted Mg/Ca ratio inhe seawater due to extensive deposition of Mg-rich evaporatesnd dolomite is also unlikely due to the anti-estuarine circulationn Central Paratethys and Persian Gulf and the low residence timef the Persian Gulf water.

editerranean region: cool-water adaption as dispersaldvantage

The available palaeobiogeographic data show that Halimeda hasot managed the jump into colder water in the Mediterraneanegion during the Middle Miocene. For the recent Mediterranean. tuna Verbruggen et al. (2005) assumed that its relatively basalhylogenetic position suggests that it is palaeoendemic from theime when the Mediterranean Sea was formed rather than a recentnvader from the Atlantic. This, however, requires assuming thathe lineage that give rise to H. tuna survived the Messinian salinityrisis (MSC), during which the Mediterranean Sea almost com-letely dried up (Verbruggen et al., 2005).

The Late Miocene was a time of global cooling and the northernargin of the tropical coral reef belt had shifted from the Cen-

ral Paratethys into the Mediterranean Sea (Esteban, 1996; Zachost al., 2001). Until the onset of the Messinian salinity crisis atbout 5.96 Ma ago, however, Halimeda occurs always associatedith tropical coral reefs throughout the Mediterranean basins (e.g.raga et al., 1996; Pedley, 1996; Brachert et al., 2007). Due to theate Miocene global cooling and since the initial stages of the MSCere characterized by overall evaporite precipitation, including

alt deposits (“Lower Evaporites”), and were followed by a short-erm (about 200 ka) episode with fresh to brackish environmentsLago Mare Event) these reef systems vanished (e.g. Martín andraga, 1994; Krijgsman et al., 1999; Orszag-Sperber, 2006). Despite

subtle global warming in the Early Pliocene a major temper-ture drop is recorded for the Western Mediterranean Sea aftereflooding at 5.3 Ma based on fossil assemblages in shallow-waterarbonates and stable isotope data of planktic foraminifers (Martínt al., 2010). Martín et al. (2010) considered that the water temper-ture decrease was caused by the opening of the Gibraltar Strait,hich implemented a new current pattern with temperate surfaceaters flowing into the Mediterranean Sea from a more northern,

ooler source area. This new situation caused the final extinctionf tropical coral reefs in the Mediterranean Pliocene and favoredhe development of heterozoan carbonates (Martín et al., 2010). Its therefore unlikely that tropical Halimeda survived the Mioceneo Pliocene transition in the Mediterranean basins. First Mediter-anean cool-water Halimeda were reported from a Late Pleistocene∼100 ka) red algal reef on Rhodes (Greece; Titschack et al., 2008).

Molecular phylogenetic studies assume that the Mediterranean. tuna is a palaeoendemic from the time when the Mediterraneanea was formed rather than a recent invader (Verbruggen et al.,005). This requires that the distribution area of the lineage that

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lution and Systematics 14 (2012) 303– 309 307

ave rise to H. tuna must have included the adjacent Atlanticoasts as well where they took refuge during the MSC. Due to thebsence of fossil Halimeda records from the northern African andouthern European Atlantic coasts as well as from the Macrone-ia archipelago in the relevant time interval it is speculative athich point and where the ancestors of the modern Mediterranean. tuna population adapted to cooler water. Two scenarios arelausible. After the MSC the tropical algae may have been dis-ersed during a warm period from this refuge area and became

solated in the Mediterranean Sea, where it provided the founderopulation of the modern cool-water H. tuna. In this case, the dis-ersal event had happened earliest during the mid-Pliocene globalarmth (3.3–3.0 Ma). At this time the land-sea configuration and

ontinental positions were effectively the same as at present, andasic patterns of ocean circulation were similar (Robinson et al.,008). Tropical air surface temperatures were nearly the same asoday, but temperatures at high northern latitudes were higher.he Mediterranean climate was 2–3 ◦C warmer than at present-dayRobinson et al., 2008). Alternatively, the founder population of the

editerranean H. tuna population may have adapted to cooler con-itions already in the Atlantic and entered the Mediterranean Seauring a cooler interval after the MSC. The Neogene Halimeda gap

n the northeastern Atlantic, however, argues against this hypoth-sis. It implies isolation of the tropical Mediterranean populationince the closure of the Tethyan Seaway and the onset of NW Africanpwelling system in the Early to Middle Miocene (Diester-Haas andchrader, 1979; Harzhauser et al., 2007a).

ersian Gulf: cool-water adaption as dispersal disadvantage

Since the geological indications offer no explanation for thebsence of Halimeda in the Holocene Persian Gulf, we can excludelkalinity and pCO2 as limiting factors. Extreme temperatures,igh salinity, sporadic eutrophication and lowered Mg/Ca ratioould constrain Halimeda at the Arabian coastlines. These factorsre, however, not suitable to prevent the algae growing alonghe Iranian coast (Fig. 4). Interestingly, Verbruggen et al. (2005)ave demonstrated that the genotypic cluster formed by H. dis-oidea from the coast of Oman is highly divergent from that ofropical Indo-Pacific specimens. The Arabian Sea, which separateshe Omanian population from the tropical ones is characterizedy monsoon-induced upwelling of cold water (Fig. 4) causing

pseudo-high latitude effect with associated cold-water sea-eed community from which H. discoidea appears to be absent

Verbruggen et al., 2005; Schils and Wilson, 2006). Accordingly,t is considered that the small Omanian population, which seemso be restricted to only a few hundreds of kilometers coastlinehat is slightly influenced by upwelling (Fig. 4), represents a peri-atric founder population, which has diverged strongly from theropical H. discoidea population by genetic drift (Verbruggen et al.,005). Cryptic species with restricted distribution ranges are con-ned to the edges of generic distribution range, often in regionsharacterized by cooler temperatures. Species intolerance to trop-cal temperatures may thus show anti-tropical populations, andeneric isolation of such populations may be promoted throughhe absence of suitable stepping stones in the tropics and the smallverage dispersal distances of most marine algae (Verbruggen et al.,005). This implies that the upwelling areas in the Arabian Seaorm a barrier for tropical Indo-Pacific Halimeda and the coolerater Halimeda population at the coast of Oman is intolerant to

he warm Persian Gulf water. As another option, the high molec-

lar divergence of the Omanian H. discoidea population could belso indicative of an ancient split, making it to a Tethys relic. How-ver, from a palaeobiogeographic point of view it is not plausiblehat Halimeda adapted to cool-water already in the tropical Tethys

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<14 Ma) and then survived in upwelling areas, which were estab-ished not until 5.5–5.0 Ma (Kroon et al., 1991).

The Persian Gulf basin in its present-day shape originated possi-ly in the late Pliocene (Sohrabipour and Rabiei, 2007). Because oflacioeustasy and its relatively shallow depth, nowhere exceeding0 m, the Gulf has, however, spent much of the Pleistocene emptyf water (Walkden and Williams, 1998). Only in the last 6000 yearshe sea level has approximated to current levels and the present-ay facies patterns became established (Walkden and Williams,998). Due to a reduced strength of monsoon-induced upwelling

n the northern Arabian Sea during the Pleistocene glacials (Sirockot al., 1991), tropical H. discoidea could have only entered the coastf Oman during a glacial maximum when the shallow Gulf wasmerged. The alga must have adapted to cooler water conditionsuring deglacial phases with intensified upwelling. Relic popula-ions of warm water Halimeda that may have survived at this timen the Persian Gulf became extinct at latest during the glacioeustaticea level fall of the Last Glacial Maximum (Fig. 4).

The shallow-silled inflow of the semi-enclosed Red Sea, whichas a similar temperature and salinity range as the Persian Gulf, islso governed by monsoon-driven upwelling (Biton et al., 2010).ence, the Red Sea marine ecosystems have been also very

ensitive to the impact of global and regional changes duringlacial-interglacial cycles and were cyclically affected by moreevere biotic turnovers as a consequence of enhanced restric-ion during glaciations (e.g. Taviani, 1998a,b; Badawi et al., 2005).onetheless, Halimeda occurs in the Red Sea up to the north of theulf of Aqaba (Mergner, 1979). In contrast to the Persian Gulf, theeep Red Sea basin (water depth: max. 2111 m in the central trench,verage 490 m) prevented total isolation and/or desiccation duringhe glacial sea-level lowstands. Therefore it is hypothesized that theed Sea was continuously inhabited by Halimeda, at least over low-mplitude sea-level lowstands, and became quickly re-colonizedrom the Gulf of Aden in the case of a severe, but relative short-term,nvironmental disturbance at the end of a higher amplitude sea-evel fall. This scenario is supported through the high endemismf marine Red Sea biota (e.g. Por, 1989; Türkay, 1996; Allen, 2000;afni, 2008), the record of last glacial deep-sea corals (Taviani et al.,007), and the correlation of submerged reef-terraces with sea-

evel lowstands (Gvirtzman, 1994).

onclusions

The stratigraphic distribution of Miocene Halimeda records inhe Mediterranean region indicates that occurrences of this algaere related to climate optima when minimum sea surface tem-eratures exceeded 18 ◦C. The palaeobiogeographic data allowsetermining the dispersal and diversification events with a bet-er temporal resolution than molecular phylogenetics. For theecent Mediterranean H. tuna it implies that its founder populationnvaded the Mediterranean Sea possibly during the middle Pliocenelobal warmth (3.3–3.0 Ma).

In contrast, the evaluation of sea surface temperature, nutrients,alinity, alkalinity, pCO2 and Mg/Ca ratio in the Central Paratethyst times with and without Halimeda shows that none of thesecological constraints can explain the absence of Halimeda in theolocene Persian Gulf. Molecular genetic studies show that H. dis-

oidea in the Gulf of Oman represents a cryptic species adaptedo cooler water. This suggests that upwelling of cold water in therabian Sea causes a dispersal barrier for tropical Halimeda and

he warm Persian Gulf water is unsuitable for the cool-adapted. discoidea population from the Gulf of Oman. Accordingly, theigration of tropical H. discoidea in the northern Arabian Sea

ould have only occurred during Pleistocene glacial maxima when

E

lution and Systematics 14 (2012) 303– 309

ecreased Indian monsoon activity reduced upwelling intensity.he cool-water adaption must have occurred during an interglacialarming episode. This example contrasts the general dispersal

oncept for tropical biota in the tropical to temperate transitionone, which supposes higher latitude dispersal during warmerlimatic intervals and retreat towards the equator during coolerlimatic intervals.

cknowledgments

We appreciate the constructive comments of four anonymouseviewers. This study was funded by the FWF (Fonds zur Förderunger wissenschaftlichen Forschung) through project P-23492-B17Mediterranean Oligo-Miocene stratigraphy and palaeoecology”nd the Commission for the Palaeontological and Stratigraphicalesearch of Austria (Austrian Academy of Sciences).

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