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The sea-skater Halobates (Heteroptera:Gerridae) – probable cause forextinction in the Mediterranean andpotential for re-colonisation followingclimate changeLanna Cheng a , Jakob Damgaard b & Romain Garrouste c da Scripps Institution of Oceanography, University of California, SanDiego, California, USAb Laboratory of Molecular Systematics, The Natural HistoryMuseum of Denmark, Copenhagen, Denmarkc Département Systématique et Evolution, Muséum Nationald'Histoire Naturelle, UMR 7205, Paris, Franced PROTEE (EBMA), Université du Sud – Toulon-Var, La Garde,France

Available online: 19 Apr 2012

To cite this article: Lanna Cheng, Jakob Damgaard & Romain Garrouste (2012): The sea-skaterHalobates (Heteroptera: Gerridae) – probable cause for extinction in the Mediterranean andpotential for re-colonisation following climate change, Aquatic Insects: International Journal ofFreshwater Entomology, DOI:10.1080/01650424.2012.643024

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The sea-skater Halobates (Heteroptera: Gerridae) – probable cause forextinction in the Mediterranean and potential for re-colonisationfollowing climate change

Lanna Chenga*, Jakob Damgaardb and Romain Garroustec,d

aScripps Institution of Oceanography, University of California, San Diego, California, USA;bLaboratory of Molecular Systematics, The Natural History Museum of Denmark, Copenhagen,Denmark; cDepartement Systematique et Evolution, Museum National d’Histoire Naturelle, UMR7205 Paris, France; dPROTEE (EBMA), Universite du Sud – Toulon-Var, La Garde, France

(Received 14 December 2010; final version received 25 May 2011)

Sea-skaters in the genus Halobates Eschscholtz 1822 include some of the mostspecialised water striders and are found in tropical and subtropical seas aroundthe world. Even though species ofHalobates occur in both the Atlantic Ocean andthe Red Sea, no extant sea-skater has been reported from the Mediterranean Sea.A fossil, Halobates ru!oi Andersen et al., 1994, described from Middle–UpperEocene (45 Ma) Italy indicates that sea skaters were present in this part of theworld in the past. Other geological evidence points to dramatic changes in theMediterranean Sea during the Tertiary and Quaternary that may have led to theirlater extinction. In this paper we review briefly the distribution, systematics,evolution and ecology of Halobates, and discuss the potential for theMediterranean to be recolonised following expected environmental changes dueto global warming.

Keywords: Gerridae; sea-skater; Halobates; Mediterranean Sea; evolution; globalwarming

Introduction

Pleistocene glaciation had unparalleled impacts on the biota of the northernhemisphere and was probably the single most significant event in shaping its presentday flora and fauna (Hewitt 2000). Enormous glaciers covered most of themountainous areas, sea level dropped by more than a hundred metres, and land notcovered with ice turned into tundra. Living organisms were forced southwards towarmer climates, survived in ice-free refugia, or simply faced extinction as theirhabitats vanished. Even though glaciations were far more extensive in NorthAmerica, their impacts were more destructive on the European biota due to the east–west oriented mountain ranges, which acted as formidable dispersal barriers. Whenthe flora and fauna retreated during glacial maxima and dispersed during inter-glacials, only relatively few founder populations remained. As a result, the Europeanflora and fauna is surprisingly poor compared to areas in North America or Asia at

*Corresponding author. Email: lcheng@ucsd.edu

Aquatic Insects2012, 1–11, iFirst article

ISSN 0165-0424 print/ISSN 1744-4152 online! 2012 Taylor & Francishttp://dx.doi.org/10.1080/01650424.2012.643024http://www.tandfonline.com

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similar latitudes. For instance, the Gerridae (Hemiptera: Heteroptera: Gerromor-pha) in Europe is today represented by only one subfamily, Gerrinae, with onespecies of Limnoporus Stal, 1868; three species of Aquarius Schellenberg, 1800; and13 species and two subspecies of Gerris Fabricius, 1794; none of which are endemicto the continent (Aukema and Rieger 1995). In contrast, North America has fourspecies of Limnoporus, five species of Aquarius and 10 species of Gerris, whiletemperate and subtropical East Asia has three species of Limnogonus, two species ofAquarius and 12 species of Gerris (Andersen 1995; Damgaard and Christiansen2007), and both areas are furthermore inhabited by representatives of several othergenera and subfamilies of water striders (Andersen 1982). Of particular interest forthe present study is the presence of halobatine water striders in East Asia, comprisingspecies in the freshwater genus Metrocoris Mayr, 1865 and in the marine generaHalobates Eschscholtz, 1822 and Asclepios Distant, 1915. The genus Halobatesoccurs in its highest species diversity further south, in Malesia (Chen, Nieser andZettel 2005) and Australia (Andersen and Weir 2004) and is found in all warmoceans and seas (Andersen and Cheng 2004). Why it is completely absent from theMediterranean Sea at present is surprising, since this sea is functionally connected toboth the Atlantic Ocean and the Red Sea where Halobates occurs. That theMediterranean acted as a refugium for the European species surviving the glaciationperiods is shown by a phylogeographic study of the river skater Aquarius najas (DeGeer, 1773), which revealed that the genetic diversity in central and northern Europe isbut a tiny distillate of what is found around the Mediterranean Sea (Damgaard 2005).

In recent years a wealth of fossil gerrids, both compression fossils and amberenclosures, have been discovered in Tertiary deposits in Europe, demonstrating a farmore diverse European fauna in earlier days (Andersen 1998; Damgaard 2008a).One compression fossil from Middle–Upper Eocene (45 Ma) marine deposits nearVerona, Italy has been assigned to the genus Halobates as H. ru!oi (Andersen,Ferma, Minelli and Piccoli 1994) (Figure 1) showing that sea-skaters were present inthe Mediterranean region during geological times. If correctly interpreted, this fossilraises the question of if and why Halobates became extinct in the Mediterranean Sea,or if they have been simply ignored by oceanographers and entomologists. In thispaper we review the distribution, ecology, systematics and evolution of Halobates inorder to seek possible explanations for their possible extinction, and discuss thepotential for them to recolonise the Mediterranean Sea.

Extant Halobates and their distribution

The family Gerridae, with eight subfamilies, over 70 genera and at least 700 speciesknown worldwide is the second largest family of semi-aquatic bugs, onlyoutnumbered by the Veliidae with around 900 species (Polhemus and Polhemus2008). The majority of gerrids are predators and/or scavengers on limnicenvironments, such as streams, rivers, ponds and lakes, but a fair number of speciesbelonging to 10 di!erent genera are found in marine environments (numbers ofdescribed species in brackets): Asclepios (3), Halobates (46), RheumatobatesBergroth, 1892 (11), Pseudohalobates J. Polhemus & D. Polhemus, 1996 (1),Rheumatometroides Hungerford & Matsuda, 1958 (8), Stenobates Esaki, 1927 (10),Stenobatopsis J. Polhemus & D. Polhemus, 1996 (1), Telmatometroides J. Polhemus,1991 (1) Thetibates J. Polhemus & D. Polhemus, 1996 (2), and Naboandelus Distant,1910 (2).

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The most well studied marine gerrid is, undoubtedly, Halobates, the only genuswith representatives in the open ocean. There are 46 described species that fallinto two distinct groups. The majority belong to the coastal group that are found in

Figure 1. (A) Fossil Halobates ru!oi Andersen et al., 1994 from Eocene deposit ‘Pesciara diBolca’ in northern Italy; (B) fossil reconstruction; (C) male of extant Astrobates rivularisAndersen and Wier (from Andersen and Cheng 2004).

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near-shore habitats associated with mangroves or coastal vegetation in the Indo-Pacific or Australasian region, and two freshwater species from Australia. Nocoastal Halobates species are known from the Atlantic Ocean. Coastal Halobates areusually absent from islands with rocky shores devoid of vegetation (Andersen andCheng 2004). Five species are, however, pelagic and unique in living permanently onthe open ocean where no other insects have been able to survive (Cheng 1989).

The five pelagic Halobates species (H. germanus White, 1883; H. micansEschscholtz, 1822; H. sericeus Eschscholtz, 1822; H. sobrinus White, 1823; and H.splendens Witlaczil, 1886) are widely distributed in tropical and sub-tropicalwaters of all three major oceans and occupy an area roughly between latitudes408N and 408S. All five species are found in the Pacific Ocean, two occur in theIndian Ocean (H. micans and H. germanus), and only H. micans is found in theAtlantic Ocean (Figure 2). Although H. micans occurs in all three oceans it hasnever been reported from the Red Sea. Unlike H. micans, which favours moreopen waters, H. germanus occurs closer to continental and island shores (Cheng1989) and has been collected in the Red Sea (Figure 3). Among the nine coastalspecies known to occur in the Indian Ocean, only H. hayanus White, 1883 and H.melleus Linnavuori, 1971 (Figure 4) have been collected from the Red Sea. Thelatter has also been collected near Eilat and the Gulf of Aqaba (Andersen andCheng 2004).

Biology and ecology

Detailed life history and behaviour studies have been conducted only on a fewHalobates species. Reviews of published literature can be found in Herring (1961),Cheng (1973, 1985) and Andersen and Cheng (2004). Although winged forms can berather common in many freshwater Gerridae, they are not known in any Halobatesspecies. Winglessness is apparently an adaptation to their extremely stableenvironment with no apparent physical barriers.

Figure 2. Halobates micans Eschscholtz, 1882, known locations in the Atlantic and easternPacific Oceans (modified from Cheng 1989).

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The eggs of coastal Halobates are laid on submerged roots and branches ofmangroves or on fringing rocks, while those of pelagic species are laid on anyfloating material the gravid female encounters (Cheng 1985). Embryonic develop-ment and hatching may take a week to a month, depending on environmentaltemperature (Cheng and Pitman 2002). There are five larval stages, each lasting froma week to 10 days. Sexes are not separable until the final instar. Females of mostspecies are slightly larger than males. Mating takes place usually with the malemounting the female. Pairs may remain in copula for several hours but mateguarding has not been observed in any coastal species. How the sexes meet or locate

Figure 3. Halobates germanus White, 1883, known locations in the Red Sea, Indian andwestern Pacific Oceans (modified from Cheng 1989).

Figure 4. Known locations of coastal Halobates hayanus White, 1883 (.) and H. melleusLinnavuori, 1971 (~).

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one another is not known. A surface-active sex attractant was found in a coastalmarine Veliidae Rhagovelia (Trochopus) plumbea Uhler, 1894 (Cheng and Roussis1998). Although preliminary studies indicated that such an attractant probably alsooperate in Halobates, further field studies are needed to confirm this (Tsoukatou,Cheng, Vagias and Roussis 2001).

Halobates are predators or scavengers and feed on their prey by piercing andsucking (Cheng 1974). Coastal species depend largely on insects fallen onto the seasurface for food. Pelagic species have been observed to feed on any zooplanktonorganisms trapped at the sea–air interface. Cannibalism is common (Figure 5)especially when food is in short supply (Cheng 1985). Thus in their natural habitatyoung nymphs of coastal Halobates species are often found in small pools amongmangrove roots close to shore while adults and older nymphs can be found in openwaters away from land, either singly or in aggregates. Such aggregations may consistof several tens or hundreds of individuals and may serve to deter predators or act asarenas for mate finding (Birch, Cheng and Treherne 1979; Foster and Treherne1981).

The main predators of pelagic Halobates are seabirds, though they have beenfound in the stomachs of surface-feeding fish and sea turtles (Cheng, Spear andAinsley 2010). Coastal Halobates also fall prey to shore birds, fish, lizards andoccasionally predatory flies (Andersen and Cheng 2004). However, sea-skaters arerarely preyed upon in general due to their agility. They can move at a speed of 1 ms71 and also jump to a height of 5 cm or more (Cheng 1985).

Pelagic Halobates are seldom found close to shore but large populations canoccur in near-shore bays or be stranded on the beach after storms or followingstrong onshore winds (Cheng 1981; Garrouste and Cheng 2009).

Origin, systematics and evolution

The Gerromorpha is one of the three basal infra-orders of Heteroptera, the othertwo being the Enicocephalomorpha and the Dipsocoromorpha, all of which haveretained fully membraneous wings comparable to those of other hemipterous insects.Fossils of the infra-order Nepomorpha date back to the Mid-Triassic (225 Ma) andare among the oldest known fossil Heteroptera (Grimaldi and Engel 2005). SinceNepomorpha belongs to Pan-Heteroptera, comprising the vast majority of extanttaxa, this means that their sister group, the Gerromorpha, must have been present atthe same time. Despite sharing the same biotopes as the Nepomorpha,gerromorphans are much rarer in deposits of the Mesozoic (Damgaard 2008a).Cretogerris albianus Perrichot, Nel and Neraudeau, 2005 from Lower Cretaceous(100 Ma) French amber was described as the only known Mesozoic gerrid fossil byits authors, and was found with marine micro-inclusions, suggesting that it camefrom a tropical marine forest palaeo-environment (Perrichot et al. 2005). However, itcould not be assigned to any extant subfamily. Since the Gerridae is not that welldefined, particularly with regard to the veliid subfamily Haloveliinae, which is alsorepresented in marine environments (Damgaard 2008b), the correct assignment ofCretogerris is still open for discussion. Considering the age of the Gerromorpha andthe diversity of Cenozoic fossils it is very likely that gerrids were indeed present in theMesozoic, even though the oldest convincing fossils are members of PalaeogerrisAndersen, 1998 (subfamily Gerrinae) from Palaeocene-Eocene (55–54 Ma) mo-claydeposits in Denmark (Andersen 1998; Damgaard 2008a). Water-striders are thus

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Figures 5–8. (5) Halobates micans Eschscholtz, 1882. Adult male feeding on a nymph inFrench Guyana (Photo by Romain Garrouste, 2010); (6) the Earth during Middle Eoceneshowing the Tethys Sea. Arrows show possible routes for Halobates migration (Paleomapfrom www. scotese.com); (7) average sea surface temperature (SST) of Mediterranean for 6November 2007 (from www.oceanoweather.com); (8) average sea surface temperature (SST)of Mediterranean for 28 June 2011 (from www.oceanoweather.com).

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both ancient and highly specialised insects; the fossil Limnoporus wilsoni Andersen1998 from Lower–Middle Eocene (52–47 Ma) deposits in British Columbia is almostimpossible to distinguish from extant relatives occurring in the same area (Andersen,Spence and Wilson 1993).

Halobates is currently subdivided in the pan-tropical subgenus Halobates s.str.comprising the majority of species and Hiliella China, 1957 from Australia andsouthern Papua New Guinea, while Austrobates rivularis Andersen & Weir, 1994from streams in northern Queensland is considered sister group to Halobates(Andersen 1982, Damgaard, Andersen, Cheng and Sperling 2000).

Halobates and the Mediterranean Sea

The Mediterranean Sea originated from the Tethys Sea when the Indian continentrifted to the north to meet Asia and more or less closed this part of the Thethysduring the Tertiary some 6 Ma. The Mediterranean Sea was completely desiccatedabout 5.6 Ma during the Messinian Salinity Crises (Garcia-Castellanos et al. 2009).Any ancestral Halobates living in the ancient Mediterranean would have becomeextinct when this occurred. It was shown that the Mediterranean was refilled fromthe Atlantic Ocean through the present Gibraltar Strait (*358N) some 5.33 Mawithin a relatively short time. The present day distribution of pelagic H. micansextends to latitudes 408N in the Atlantic Ocean (Cheng 1989). If we assume this wasalso its historical range then it is possible for specimens to be carried from theAtlantic into the Mediterranean when the refilling occurred (Figure 6). Why is itabsent?

Extant Halobates are known to live and reproduce successfully only in waterswhere the temperature is above 208C all year round (Cheng 1985). Seawatertemperature in the Mediterranean was known to have been a!ected by Pleistoceneglaciations in the northern hemisphere which began roughly 2.75 Ma (Ruddiman2010). The drop in temperature could have led to the extinction of any ancestralHalobates that might have lived in the Mediterranean after it was refilled followingthe Messinian Salinity Crisis.

Although the present day Mediterranean Sea is almost land-locked, it isfunctionally connected to the Atlantic Ocean through the Strait of Gibraltar (Artaleet al. 2006). It is thus likely for H. micans to enter via this route. In addition, entryvia the Suez Canal by the pelagic H. germanus from the Indian Ocean or the coastalH. hayanus and H. melleus from the Red Sea may also be possible. However, theSuez Canal is some 160 km long and there are many obstacles to overcome.Although Halobates are rather adaptable to environmental extremes, we do notknow whether any individual would be able to survive the long journey through theBitter Lakes and other environmental barriers. Perhaps the most obvious way forHalobates to enter from the Red Sea would be as eggs attached to floating objectscarried passively by the current. If any individuals were able to overcome variousobstacles and enter the Mediterranean, would they find conditions suitable for theirsurvival?

It is known that winter temperature in the Mediterranean can be below freezingin many areas, but there exist locations where sea surface temperatures (SST)remained above 188C or 208C all year round, e.g. Gulf of Sirte (Sidra) in Libya,south Tunisian coast, and coastal areas between western Alexandria and the SuezCanal (east of the Nile delta) (Marullo, Santoleri, Malanotte-Rizzoli and

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Bergamasco 1999). It is possible that conditions in these areas would be suitable forthe survival and reproduction of Halobates if it were to reach there. Furthermore,rapid warming of the Mediterranean is expected during the 20th century (Belkin2009). Vargas-Yanez et al. (2010) studied a 1900–2008 temperature time series andshowed that both the upper and intermediate layers of the western Mediterraneanhave warmed throughout the twentieth century. Changes in composition, structureand functional aspects of the marine communities have also occurred, asdemonstrated by the occurrence of large numbers of lessepsian and other sub-tropical species (Francour, Boudouresque, Harmelin, Harmelin-Vivien, andQuignard 1994) as well as changes in biological processes (Parmesan and Yohe2003; Diaz-Almela, Marba and Duarte 2007). Scenarios of climatic changes over theMediterranean basin have been predicted. For example by 2031–2060, when a 28Cglobal warming is most likely to occur, the rate of warming in the Mediterranean isexpected to be around 28C in spring and winter, but almost 48C in summer. Anadditional month of summer days is expected, along with 2 to 4 weeks of tropicalnights (Giannakopoulos et al. 2009). It is thus likely that during late spring,throughout summer and the beginning of fall, when the SST is higher than 208C(Figures 7 and 8), it would be possible for Halobates to reproduce successfully inmany areas in the Mediterranean Sea.

One question that remains unresolved concerns the possible trophic relationshipbetween Halobates and the neustonic biota harbouring its potential food source. TheMediterranean is considered to be an oligotrophic sea with low planktonconcentrations. As a consequence prey organisms may be in short supply exceptduring periods of high seasonal productivity in the Alboran Sea (east of Gibraltar)or around the Suez Canal. The availability of potential prey organisms woulddetermine the success of its colonisation. However, reproductive activity of H.germanus was found to be highest during oligotrophic conditions in the Banda Sea(Cheng, Baars and Oosterhuis 1990). Cannibalism has been observed in severalfreshwater gerrids as well as in Halobates (Cheng 1985) and probably occurs notinfrequently among individuals when there is food shortage. Perhaps this could be anadaptation for the survival of Halobates and other pleustonic organisms (Cheng1975) in marine or large freshwater habitats?

Conclusion

The sea-skater Halobates is unique in many ways. Five species have conqueredthe oceanic habitat. They are able to withstand storms at sea, being tossedaround by waves and have evolved special adaptations to deal with accidentalsubmergence, damaging e!ects of UV irradiation, long periods of starvation andvarious other obstacles for survival in an environment virtually devoid of physicallandmarks or barriers (Cheng 1985). Although the only known fossil Halobateswas discovered along the Italian shore, no extant species has ever been found inthe Mediterranean Sea. Halobates are known to prefer and reproduce successfullyin seas where the temperature is above 208C. Seawater temperature in theMediterranean is expected to rise due to global warming. It is thus likely thatshould some Halobates or viable eggs succeed in entering the Mediterraneaneither from the Atlantic Ocean through the Strait of Gibraltar or from the RedSea via the Suez Canal they would be able to establish themselves in theMediterranean Sea in the foreseeable future.

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Acknowledgement

We thank Danwei Huang, Scripps Institution of Oceanography, for his help in mappingFigure 4, and scotese.com and oceanoweather.com for permission to reproduce Figures 6,7 and 8.

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