Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353 – 367 www.elsevier.com/locate/palaeo
Correlation between environment and Late Mesozoic ray-finned fish evolution Lionel Cavin a,⁎, Peter L. Forey a , Christophe Lécuyer b a
Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK b Laboratoire UMR CNRS 5125 ‘PEPS’, Université Claude Bernard Lyon 1, France Received 13 June 2005; received in revised form 21 July 2006; accepted 28 August 2006
Abstract In order to better understand the parameters that drove evolution of actinopterygian fishes from the Late Jurassic to the Late Cretaceous (this being the time of diversification of crown group teleosts, by far the dominant fish group today), we define three environmental indicators, which are detectable as concordant patterns in the geological and fossil records. These are 1) freshwater radiations, 2) vicariant events and 3) sea temperature. We mapped the indicators onto a phylogeny of the Late Jurassic–Palaeocene actinopterygian taxa, and plotted the variations against time for each of the indicators. Our results show that for several of the marine clades, diversity is positively correlated with sea temperature and for one clade negatively correlated with sea temperature. The marine radiation is very important in the mid-Cretaceous, especially in the Tethys, which may have been a centre of origin for some clades. Vicariant events occurred in both marine and freshwater groups, and are abundant during the opening of the south Atlantic in the Early Cretaceous. Freshwater radiations, forming in some cases species flocks, are especially evident in the basal Cretaceous in Asia. Although these results are affected by biases related to the fossil record and to its study, we propose that these global patterns are genuine and reflect the strong impact of the Earth system on the evolution of fishes in the Late Mesozoic. © 2006 Elsevier B.V. All rights reserved. Keywords: actinopterygii; diversity; Jurassic; Cretaceous; sea temperature; vicariance
1. Introduction The main issues dealing with long-term forces that drive biological evolution are closely associated with the spatial and temporal scales of the object under study. Observations obtained through the fractual lens of biological processes identify speciation as the key to
⁎ Corresponding author. Present address: Département de Géologie et Paléontologie, Muséum d'Histoire naturelle de la Ville de Genève, 1 Route de Malagnou, Case Postale 6434, CH-1211 Genève 6, Switzerland. Tel.: +41 22 418 6333. E-mail address:
[email protected] (L. Cavin). 0031-0182/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2006.08.010
broader patterns, but the search of the cause of speciation is difficult when we deal with distributions and phylogenies of modern organisms only (Barraclough et al., 1998; Barraclough and Nee, 2001). In biogeographical studies for instance, information about time of events should be added to phylogenetic and geographic data in order to detect vicariant and dispersal patterns (see for instance the “biogeochronological paradigm”, Hunn and Upchurch, 2001; Upchurch et al., 2002). Similarly, studies searching for correlations between environment and evolution also get a broader significance when the fluctuations over time of indicators of the physical and biotic parameters of the Earth system are included in the analysis. A recent example using reef
354
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
production as a case study shows that a broad time scale study may provide a good test for hypotheses built up on time-frozen modern observations (Kiessling, 2005). Both extinction (Raup, 1986; Taylor, 2004) and diversification processes shape the curve of life diversity, but here we deal with mechanisms related to diversification only. One of the broad issues we are concerned with is how the biotic versus physical parameters affect the diversification of organisms and the evolution of ecosystems. The structure of the ecosystems and the moving equilibrium of ecological communities have been regarded as the major factors shaping the evolution of organisms, even when external conditions remain constant (Van Valen, 1973). On the other hand, physical parameters of the Earth system have been proposed as a prime engine in driving evolution (Vermeij, 1995). A possible test of these theories is the search for correlations (or mismatches) between parameters of the environment, exemplified by indicators recorded in the geological record, and taxonomic diversity. Any attempt to discover global long-term environmental factors acting on the diversification of life should deal with clades characterized by (1) a reasonably good fossil record, (2) a phylogenetic framework that allows us to detect vicariant events (Wiley, 1988) and to assess the quality of the fossil record (Hitchin and Benton, 1997 for instance), (3) a systematic structure that allows us to identify speciose monophyletic groups confined to ecological/geographic units (e.g. a lake or river system) and (4) an array of taxa that encompasses a broad range of environmental niches in order to compare the respective impacts of the environmental factors on their diversity. Such opportunities are rare. Most of the marine protists and invertebrates groups with biomineralized skeleton have a good fossil record but their phylogenies are generally poorly resolved and/or they occupied restricted environmental niches. Tetrapod remains have more complex morphology allowing the discovery of robust phylogenies, but they have, however, an overall rather poor fossil records with most of the clades occupying narrow-range environmental niches (mainly terrestrial with some clades in aquatic environments). A potentially better case study is that of the ray-finned fishes (actinopterygians). The ca. 27,000 living species of actinopterygians (Froese and Pauly, 2006) make up more than half of the living vertebrates. They occur from the highest Himalayan streams to the depths of the Mariana trench, from freezing antarctic waters to desert hot springs where the water is just below boiling point. They can do anything that the rest of the vertebrates can do, including breathing air, flying and they have a bewildering array
of feeding and reproductive strategies, including using a ‘placenta’ in some species (Bond, 1996). The broad ecological range occupied by actinopterygians today was probably quite similar in the Cretaceous because no other vertebrate groups competed with actinopterygians in their niches at that time. Considering the range of actinopterygian ecosystems occupied today as being representative of the palaeoecology of ray-finned fishes in the Cretaceous, they form a good proxy to study how vertebrates responded to global changes during the last half of the Mesozoic. Also, the late Jurassic and Cretaceous was a time when the initial diversification of crown group teleosts was taking place. Teleosts (about 23,000 living species) make up 90% of modern fish faunas. Moreover, the fossil actinopterygian record is reasonably good. True, it pales into insignificance when measured against ammonites or foraminifers, but within the vertebrates it is excellent being very widespread in time and space. Because of the broad ecological niches occupied by ray-finned fishes today, the modalities and processes of speciation events are diverse (see below). In the Cretaceous, we assume the array of processes was probably as broad as today. 2. Methods The methods used in this study consist of (1) identifying indicators of the physical and biotic parameters of the environment co-incident with cladogenetic events that are detectable in the fossil and geologic records, (2) mapping these indicators onto a phylogeny of actinopterygians and (3) computation of the amounts of each of the indicators against time in order to detect global trends in actinopterygian evolution correlated with features of the Earth system. 2.1. Database The database we use is a compilation from primary literature about worldwide late Jurassic–Palaeocene actinopterygians, including the literature concerned with dating fish assemblages and palaeoecology. The database gathers information on taxa worldwide ranging from the Late Jurassic to Palaeocene (the list of the fish assemblages with the names of genera are available as complementary information online, Appendix 1). Only data that are based on skeletal material are considered, because otolith data provide a distorting signal (only material referable to Recent groups are hitherto recognised). In order to avoid circular reasoning information on the age of the fossil bearing deposits are
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
ignored when the dating rests partly or entirely on the composition of the fish assemblages. The dating of fish occurrence is often coarse-grained, generally straddling a complete, a half or a third part of a geological stage. The method compares variations through time of potential environmental forcing factors with a justified phylogeny. A composite tree constructed from many indpendent studies and including all actinopterygian genera occurring from the Late Jurassic to the Palaeocene was built up (the phylogenetic tree with additional data about palaeoenvironments and modes of cladogenetic events are available as complementary information online, Appendix 2). We did not use a formal supertree method (Roshan et al., 2004 for instance) because the source phylogenies of actinopterygian subgroups generally deal with taxonomically restricted clades lacking overlapping leaf sets. Furthermore, we are unable to define enough homologous characters to cover the extreme morphological variation encompassed by all actinopterygians without introducing a plethora of question marks that would be detrimental for our need for resolution. Instead, the tree used here is built up by anchoring available local phylogenies on a backbone cladogram of actinopterygians (Appendix 2). While the actinopterygian phylogenetic bush is far from being resolved, the morphospace is not evenly occupied and clusters of monophyletic low-rank taxa are easily recognised. They are generally gathered within systematic ranks, such as orders (i.e. Pachycormiformes, Pycnodontiformes, Ichthyodectiformes, Tselfatiiformes,…) or families (i.e. Aspidorhynchidae, Dercetidae, Enchodontidae,…), that can be attached to the backbone cladogram. For computation purposes and for mapping the environmental indicators on the phylogeny, we need to include the extension range (Smith, 1994) as well as the ghost lineages sensu Norell (1992) to complete the missing parts of the tree. Because speciation occurs at the species/populations interface, it is claimed that methods should focus at that level to understand the processes (Losos and Glor, 2003). However, the species level fails in computations of biodiversity through long time interval for two reasons. First the discrepancy between the cladistic phylogenetic patterns and the biological speciation processes. Second, because of the lack of overlap between the plethora of fossil species concepts and the biological species concept. When generic inter-relationships are not resolved within a clade but the genera have different ranges, the extension range of a genus extends backwards to the beginning of the observed stratigraphic range of the next older taxon of that clade. A node on which we map an environmental indicator binds both genera. Accord-
355
ing to this rule, we always choose the shortest possible range extension among the available solutions (Fig. 1A). Details of the structure of the tree are provided in Appendix 2 on line. Pattern versus process: We recognise several situations in which processes recognised in modern speciation events may potentially disturb the search for a morphological species-level phylogenetic pattern. 1) Some modes of speciation lead to paraphyletic morphospecies (Omland et al., 2000 for instance) (Fig. 1B). 2) Some species may have a hybrid origin in plants (Rieseberg, 1997) but also in animals, including fishes (DeMarais et al., 1992; Smith, 1992a) (Fig. 1C). 3) A single species can produce several sister-species at different times, making the ghost lineage concept meaningless at the species level (Fig. 1D). For instance, Echelle and Echelle (1992) found that a widespread costal species of pupfish in southeastern USA, Cyprinodon variegates, was ancestral to four species from inland drainages. This corresponds to the “budding cladogenesis”, in which the ancestral species survive cladogenesis and can produce any number of descendants (Wagner, 2000). The fossil species concept: Although on rare occasions fossil species may represent genuine biological species and speciation events may be studied directly through the analysis of the fossil record (Lazarus, 2001; Benton and Pearson, 2001), in most cases the fossil species concept does not cover the biological species concept (Bock, 2004), especially for vertebrates. It has been shown that the genus is a much reliable rank on which biodiversity analyses are based (Forey et al., 2004). Fish diversity is here measured by using the genus as the standard unit, which we use as a proxy for real biodiversity where species fail (Sepkoski, 1998). 2.2. Environmental indicators (Fig. 2) Here we define the environmental indicators characterizing fish cladogenesis. The environmental indicators as defined here form the broad frameworks in which patterns of cladogenesis are observed. The speciation processes beyond the patterns are not distinguishable at this time scale, but a rapid survey of processes in action today, especially in fishes, may help to better appreciate the array of mechanisms that presumably occurred in the Cretaceous.
356
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
Fig. 1. Schematic charts showing a rule applied in this study (A) and possible discrepancies between evolutionary processes at the species level and the recognition of morphological-based cladistic patterns (B–D). A, When the genera within a clade have different ranges (1) but generic interrelationships are not resolved (2), the extension range of a genus extends backwards to the beginning of the observed stratigraphic range of the next older taxon of that clade (3). A node binds both genera (white spot). B–C, A fossil or Recent morpho-species may correspond to a paraphyletic genomic taxon (B) or to a hybrid taxon (C). D, (1) A “budding speciation”, in which the ancestral species “a” survives cladogenesis and produces two descendants (white spots). The black sections represent the observed occurrences and the grey ones represent the unknown stratigraphic ranges. (2) The reconstructed cladogram based on (1), and (3) the reconstructed tree in time showing wrong ranges.
2.2.1. Freshwater radiations Today both allopatric and sympatric processes drive fish speciation in freshwater environments. Allopatric speciations occur through the creation of barriers, such as oceanic basin and transcontinental seas between two land masses (see next section), mountain ranges (He et al., 2001) and lake fractioning (Beheregaray et al., 2001). Sympatric speciations occur in a single place and are driven by behavioural, genetic or physiologic causes (Via, 2001) and may lead to species flocks in restricted lakes or river systems. Sympatric speciations occur in a
wide array of fish taxa ranging from lampreys (Salewski, 2003) to chichlids (Shaw et al., 2000 for instance). Subtle geographic differences between populations of a single lake may trigger speciation (Knight and Turner, 2004), but these processes are regarded as sympatric at a broader geographical scale, especially when we deal with the coarse fossil record. Allopatric speciations, through the creation of geographical barriers, can be detected by the vicariance biogeographic method. But because the geological record is imperfect, only some of the barriers, such as epicontinental seas or ocean basins,
Fig. 2. Recognised environmental indicators that shaped Late Mesozoic actinopterygian evolutionary history.
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
are easily detectable (Eastern and Western continental faunas separated by the North American Interior Seaway and African–South American faunas separated by the Proto-South Atlantic respectively for Cretaceous examples). Barriers due to changes in the geomorphological local landscape, such as new patterns of river drainages, may have dramatic effects of fish distribution and speciation (Mayden et al., 1992; Smith, 1992b; Unmack, 2001; Dergam et al., 2002) but they are hardly visible in the Mesozoic geological record because fossil fish remains from these events are generally gathered together in the same geological formation. Freshwater events due to barriers easily inferred in the geological record, mainly land masses becoming separated by marine barriers, are grouped here under the “vicariance indicator” discussed in the next section. Freshwater speciation due to barriers not visible in the geological record (most of the superficial geomophological barriers), or to biological or micro-environmental factors without any physical barriers (sympatric speciations) are gathered here under the name “freshwater radiation”. In our database, we define a freshwater radiation when two or more genera occurring in a freshwater environment are considered to be their closest relatives (Fig. 3A and B), or when one or more genera are known with several well-defined species in the same formation (Fig. 3C). In some cases, the freshwater radiation recorded in the fossil record may represent species flocks (see discussion below). 2.2.2. Vicariant events It is usual in vicariance biogeography studies to look at terrestrial and freshwater organisms because it is thought that their distributions are more closely constrained. For fishes, this situation occurs when two genera, or a genus and its sister group, are recorded in continental sediments from two land masses separated by an epicontinental sea or an oceanic basin. However, it is equally true that the distributions of most marine coastal fishes, living on the continental shelf, are also tightly constrained by physical parameters. Barriers preventing fish dispersal are marine currents, surface gradients of temperature and salinity, great depths (Pequeno and Lamilla, 2000) or freshwater and sediment outflows from rivers (Rocha, 2003). Marine fish species separated by such barriers may show vicariant patterns that could be detected by vicariance biogeographical tools in the same way as for continental organisms. Modern examples today are the classic eastern Atlantic– eastern Pacific/Caribbean track defined by Rosen (1975), the vicariance between Australia and Antarctica for some notothenioids (Bargelloni et al., 2000), the
357
Fig. 3. Schematic patterns for the recognition of freshwater radiation and vicariant event on the basis of a phylogeny and the fossil record.
vicariance between east and west coasts of Australia following periods of sea level and climate changes for the cirrhitoids (Burridge, 2000), and between Atlantic and Indo-Pacific for species separated by the Isthmus of Panama (Bernardi et al., 2004). In our database, we define a vicariant event when two occurrences from two different formations are sistergenera (Fig. 3D), or situated in a pectinated position in the tree (Fig. 3E). The later situation is not a vicariant case sensu stricto as the vicariance actually occurred between the genus in the lowermost pectinated position and its complete sister-clade. But the approximation made here is justified, as the phylogeny we used cannot pretend to get the same resolution as a phylogeny of modern organisms. We also record a vicariant event when a single genus is known by several well-defined species in two different formations, even if the mutual relationships between species are not resolved (Fig. 3F). 2.2.3. Sea temperature Direct impacts of an increase of available energy (temperatures) are thought to trigger a burst in fish diversity by shortening the generation time via higher productivity affecting food supply and growth rate and possibly through higher mutation rate (Rohde, 1992).
358
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
Indirect effects are diverse, such as increased ocean stratification (Price et al., 1998) and modification of sea water chemistry through hydrothermal activity and plankton production (Leckie et al., 2002). For all fully or mostly marine higher taxa, mainly monophyletic groups, we tested the correlation between diversity and the upper ocean temperature. A curve of upper ocean temperatures from the Late Jurassic to the end of the Cretaceous Tethyan domain was drawn up from the oxygen isotope data of fish tooth enamel. Evolution of isotopic temperatures from the Bajocian to the Maastrichtian that were calculated from the δ18O of fish tooth enamel assuming a δ18O of seawater = 0. This hypothesis has been retained considering both the tropical paleolatitudes of western Europe and the absence of polar ice-caps as a first approximation. Tooth enamel remains the best biomineral to estimate Pre-Cenozoic marine temperatures (Picard et al., 1998; Lécuyer et al., 2003). The greater resistance of enamel to diagenesis than either dentine or bone was already emphasized by earlier studies performed on Mesozoic vertebrate teeth (Kolodny et al., 1996; Sharp et al., 2000). Indeed, apatite crystals that make up tooth enamel are large and densely packed, and isotopic exchange under inorganic conditions has little effect on the oxygen isotope composition of phosphate even at long geological time scales (Kolodny et al., 1983; Lécuyer et al., 1999). Oxygen isotope analysis of apatite from modern selachians has shown that isotopic temperatures reflect the average temperature of the seawater layer in which the fish lives (Picard et al., 1998). The 18O/16O ratio recorded in fish tooth phosphate during its formation depends on both temperature and the isotopic composition of the environmental water. Knowledge of the δ18Oseawater is therefore crucial for the temperature calculation. Variations in the oxygen isotope composition of seawater are governed by several factors including (1) the evolution of the mass of continental ice that modifies the δ18O of seawater by preferentially storing 16O in ice; (2) local evaporation/precipitation ratio and continental run off that influence both the salinity and the local δ18O of seawater. The Cretaceous period has often been considered to be ‘ice-free’ because of the absence of glacial deposits during its major part. This would correspond to a δ18O for ocean water close to − 1‰ SMOW (Standard Mean Ocean Water), as suggested for an ice-free Earth by Shackleton and Kennett (1975). However, ice caps (though probably smaller than today) may have been episodically present during the earliest Cretaceous (De Lurio and Frakes, 1999; Price, 1999) and even during the mid-Cretaceous (Ramstein et al., 1997; Stoll and Schrag, 2000). Consideration must also be given to the
fact that at tropical latitudes, the evaporation/precipitation ratio tends to be higher than 1 resulting in increased salinity and δ18O values of surface waters. Therefore, Pucéat et al. (2003) calculated marine paleotemperatures for δ18Oseawater values of − 1‰ and 0‰ by using the fractionation equation determined by Kolodny et al. (1983). Because of the mobility of fishes through the water column, these temperatures were considered as upper ocean and not sea surface temperatures. The similarity of the oxygen isotope curve as measured for bioapatites from platform environments (Pucéat et al., 2003, Fig. 2) with those for foraminifera and bulk carbonates (Huber et al., 1995; Clarke and Jenkyns, 1999) that were deposited in deeper waters and at other paleolatitudes (Frakes, 1999) indicates that they recorded global climatic signals. Major cooling events at the million-year scale can be identified: (1) during the Berriasian–Valanginian and (2) during the earliest Late Valanginian. A third cooling event happened during the earliest Aptian. A progressive warming characterized the Aptian–Turonian interval that corresponds to a climatic optimum, then upper ocean temperatures decreased until the Maastrichtian. Temperature differences between climatic extremes of the Valanginian and Cenomanian–Turonian are estimated to have been close to 10 °C. 3. Results Fig. 4 shows the total number of actinopterygian genera (observed + ghost) from the Oxfordian to the Maastrichtian according to the palaeoenvironment where they lived, together with the evolution of isotopic upper ocean temperatures from the Bajocian to the Maastrichtian calculated from the δ18O of fish tooth enamel assuming a δ18O of seawater = 0. This hypothesis has been retained considering both the tropical paleolatitudes of western Europe and the absence of polar ice-caps as a first approximation. Euryhaline taxa are those found in both freshwater and marine deposits, or in deposits with both marine and freshwater influences. Over the entire time interval under study the actinopterygian diversity shows fluctuations reflecting apparent stochastic changes that, over the total time period considered here remain at the same level. Therefore these data are in accordance with the hypothesis of an equilibrium in the number of species reached in the Mesozoic (Alroy et al., 2001) rather than with the hypothesis of a progressive increase in post-Palaeozoic species diversity (Sepkoski, 1997), for the Cretaceous at least (an important rise of percomorph diversity happened in the Tertiary).
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
359
Fig. 4. Total number (observed + Lazarus + ghost) genera of actinopteygians from the Oxfordian to the Maastrichtian according to the palaeoenvironment where they lived and upper ocean temperature.
For the marine clades, we tested the correlations between their diversity and sea temperature during the Oxfordian–Maastrichtian interval (Table 1). Marine genera as a whole, ichthyodectiforms, elopomorphs, tselfatiiforms, clupeomorphs, pachyrhizodontoids + protobramoids, salmoniforms, aulopiforms and basal acanthomorphs show significant positive correlations with sea temperature. Pycnodontiformes, macrosemiiforms, pachycormiforms, marine gonorhynchiforms, beryciforms, marine perciforms and tetraodontiforms show no correlation with sea temperature. IonoscopiTable 1 Coefficients of correlation between upper ocean temperature and fish diversity
Fish taxa Marine genera Pycnodontiforms Macrosemiiformes Ionoscopiforms Pachycormiforms Ichthyodectiforms Elopomorphs Tselfatiiforms Clupeomorphs Pachyrhi. + proto Gonorhynchiforms Salmoniforms Aulopiforms Basal acanthomorphs Beryicforms Perciforms Tetraodontiforms
r
N
0.580⁎⁎⁎ NS NS −0.492⁎ NS 0.422⁎ 0.455⁎ 0.558⁎⁎ 0.595⁎⁎ 0.565⁎⁎ NS 0.516⁎⁎ 0.392⁎ 0.758⁎⁎ NS NS NS
258 29 8 7 8 17 27 18 6 11 6 11 31 20 28 3 9
N, sample size; NS, non significant, ⁎ P b 0.05; ⁎⁎ P b 0.01; ⁎⁎⁎P b 0.001. Basal acantho: Myctophiformes, Ctenothrissidae, Pattersonichthyidae, Pateropercidae, Pharmacichthyidae, Polymixiiformes, Sphenocephaliformes.
forms show a significant negative correlation with sea temperature. A composite cladogram of actinopterygians, on which are mapped the environmental indicators that better characterized evolution of each group from the Late Jurassic to the end of the Cretaceous is available as complementary information on line (Appendix 2). Recognition of water temperature as the main forcing environmental parameters rests on mathematic correlations, while freshwater radiation and vicariant events are recognised based on the palaeodistributions of the taxa. Details of these events are explained below. Some of the clades, especially those with both marine and freshwater representatives, such as the amiiforms and the clupeomorphs, are characterised by a variety of environmental parameters that forced their evolution. Recent examples of clades with small numbers of species that show various modes of speciations, are members of the marine family Notothenioidae (Bargelloni et al., 2000) or species of the freshwater catfish genus Noturus (Grady and LeGrande, 1992). However, most of the clades show a single main environment indicator during their late Mesozoic evolution, although we are aware than our methods may only correlate very general environmental indicators with a cladogenetic pattern. 4. Discussion Various biases and parameters not included in this study may affect our reading of the fossil fish record. For instance, effort sampling and amount of available studies distort the signal provided by the fossil record. Sea level fluctuations (and volume of rocks) have an important control by skewing the signal in affecting the available fossil record, but also have a direct impact on
360
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
biological evolution (common cause) (Smith et al., 2001; Peters, 2005). Analysis of the average ghost lineage duration of actinopterygians from the Late Jurassic and the Cretaceous show us, however, that vagaries of the total diversity reflects at least in part genuine taxonomic fluctuations. The data show that the average ghost lineage duration drops synchronously with the rise of diversity observed at the early-late Cretaceous boundary. This indicates that most of the new taxa are the result of biological diversifications rather than simply the product of better samplings due to lagerstätten effects (Cavin and Forey, work in progress). 4.1. What pushed ray-finned fishes to evolve in the Late Mesozoic (Fig. 5) In Fig. 5, we plotted the number of events for each of the environmental indicators against time. All the identified cladogenetic events are artificially pushed backwards on the time scale because of the imprecise stratigraphic resolution of the actinopterygian database. For instance, a peak of freshwater radiation in the basal Cretaceous is actually documented by a radiation event observed in the late Jurassic. In the Late Jurassic, few environment indicators are detected. In marine environments, the ichthyodectiforms, alongside the first salmoniforms (Orthogonikleithridae [Arratia, 1997]) and the first elopiforms (Elopsomelos [Arratia, 2000]) are clades varying in diversity together with sea temperature. In the Late Jurassic and Early Cretaceous, ionoscopifoms show a negative correlation with sea temperature, which is unique among the studied taxa. Today, some clades are specialised to cold waters and show a higher diversity in cold water, such as the notothenioids (Bargelloni et al., 2000). Thus, admitting that fish response to changes over time is the same as response to changes in latitude and temperature today, we suggest that ionoscopiform fishes formed a clade of fishes adapted to cold-waters. This hypothesis, however, rests on a small sample and need to be tested by additional data. In the Late Jurassic an interesting marine vicariant event occurred between the aspidorhynchids Belonostomus in Laurasia and Vinctifer in Gondwana (Brito, 1997). In continental environments, we have an indication of a freshwater flock in African pleuropholids, with five genera described in the Kimmeridgian of the Republic Democratic of Congo (Saint-Seine, 1955). A peak in freshwater radiations and a peak in freshwater vicariant events are observed in the Tithonian but they are centered on the poorly dated basal Cretaceous
Chinese fish faunas. Because freshwater radiations may be extremely rapid in young lakes (Seehausen, 2002) where they can form species flocks, we regard these freshwater radiations as contemporaneous with the time of their deposition, i.e. basal Cretaceous. The vicariant events observed in these east Asian localities, based in part on the presence of ghost lineages, indicate a surprising split between China and North America (peipiaosteids/acipenseroids, Plesiolycoptera/other hiodontids). These unexpected links, already pointed out by Grande and Bemis (1991) and Grande et al. (2002), also occurred in the Tertiary for the clupeomorph Diplomystus (Chang and Chen, 2000). The Tertiary distribution can be easily explained by the presence of a “freshwater Arctic Ocean” allowing freshwater dispersals (Chang and Maisey, 2003), but the early Cretaceous pattern is more difficult to explain. A closed Pacific in the Upper Triassic–Lower Jurassic has been suggested as a possible explanation of the repeated examples of the same biogeographical pattern (McCarthy, 2003). However, caution should be used in the search of a tectonic explanation for this pattern, because today apparent freshwater vicariant patterns may hide dispersal events, when some of the involved taxa or some of their developmental stages are able to cross marine barriers. A recent example of such dispersal was described in the galaxiids (Waters et al., 2000). The various freshwater Chinese localities, gathered within the older “Lycoptera fauna” and the younger “Mesoclupea fauna” (Chang and Miao, 2004), yield evidence for several freshwater radiations within the acipenseriform peipiaosteids (at least three species in two genera [Jin, 1999]), the halecomorphs sinamiids (seven species in two genera [Chang and Jin, 1996]), the “pholidophoriform” siyuichthyids (seven species in five genera [Chang and Jin, 1996]), the possible ichthyodectiforms (Mesoclupea) and the osteoglossomorphs (lycopterids and basal hiodontids). Some of these taxa spread into adjacent areas, such as central Asia, Korea (Lee et al., 2001), Japan (Yabumoto, 1994) and SouthEast Asia for sinamiids (Cavin et al., in press). Much more work is needed now to better understand the phylogenetic relationships among the taxa that form these radiations, which sometimes constitute species flocks. During the Early Cretaceous vicariant events between Africa and South America are observed in different groups of fishes, as already described by Maisey (2000). The splits occurred possibly within the polypteriforms (Gayet, 2001), the gars Obaichthys/ Oniichthys (Cavin and Brito, 2001), the halecomorphs Calamopleurus/Maliamia (Grande and Bemis, 1998),
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
361
Fig. 5. Number of genera affected by three environmental indicators through time, with some of the major events in the Earth system history (see text for details). Ionoscopifoms, whose diversity shows a significant negative correlation with sea temperature, are not shown on the chart.
possibly the heterotin osteoglossomorphs Laelichthys/ Paradercetis (Bonde, 1996; Taverne, 1998), the gonorhynchiforms Tharrias/Parachanos (Grande and Poyato-Ariza, 1995, 1999), the paraclupeids Ellimma/ Ellimmichthys (Chang and Maisey, 2003), as well as species within some of these genera (Calamopleurus [Forey and Grande, 1998], Ellimmichthys [Maisey, 2000], Dastilbe [Maisey, 2000], Pachyamia [Grande and Bemis, 1998]). The opening of the South Atlantic is well-documented by vicariant events in tetrapod vertebrates, as well as by the complementary dispersal events observed in marine invertebrates between the Caribbean Tethys and the South Atlantic. An interesting but still unexplored group that show hints of vicariance between Africa and South America alongside a freshwater radiation in Asia (Cavin and Suteethorn, 2006) is the early Cretaceous semionotids. We know little about the basal Cretaceous marine fish faunas, but indirect evidence shows that proportionally few originations occurred during this time interval. Sixty percent of the marine families known in the early Aptian are also known in the late Jurassic, about 30 Ma earlier
(pycnodontids, macrosemiids, ionoscopids, ophiopsids, aspidorhynchids, ichthyodectids), and only 40% (crossognathids, phyllodontids, notelopids, chanids) originated within that time interval. By comparison from the 20 marine families known in the early Campanian, 3 of them (15%) were present in the early Aptian 30 Ma earlier and 17 (75%) originated during that time interval. The mid Cretaceous witnessed major global changes in the Earth system triggered basically by a rise in oceanic crust production and/or oceanic volcanism. The main impacts of these changes on the marine fish environments are a rise of the sea level stand and a rise in sea temperature, both reaching their maxima in the Cenomanian (Gale, 2000 for an overview). The rise in oceanic crust production, together with the rise in sea temperature, begins in the Aptian, which marks the starting point for the rise in marine fish diversity. The number of cladogenetic events expressed by the sea temperature indicator starts to rise in the Barremian (smeared backwards because of the sampling bias explained above) and a maximum stand in the Albian corresponding to the maximum Cenomanian diversity
362
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
stand. At that time sea temperature is still positively correlated with the diversity of some of the old Jurassic groups, i.e. the ichthyodectiforms, elopomorphs and salmoniforms, but is especially correlated with several new groups such as the tselfatiiforms, aulopiforms and the basal acanthomorphs. All of the Cenomanian Tethyan fish assemblages share a large part of their taxa compared as distinct from the more endemic boreal Chalk fish fauna (Forey et al., 2003), as well as sharing numerous new taxa appearing for the first time in the fossil record in the Tethyan localities (especially in the three Lebanese localities, Hakel, Hajula and Namoura, but also in Israel, Adriatic region and Morocco). The Tethys may have been a Cretaceous centre of origin for fishes (Cavin et al., 2005), just as the Indo-West Pacific is thought to be a centre of origin (Mora et al., 2003; Briggs, 2003) for modern fishes. But it is difficult to distinguish a genuine ancient centre of diversification from an artificial centre based on the biases of the distribution of the fossil record. However, if we compare the Cenomanian fish assemblage of the British Chalk to the three Lebanese Cenomanian localities, only 9 of the 19 Cenomanian Chalk families (47%) occurred for the first time in the worldwide fossil record, while 22 of the 32 Lebanese families (69%) occurred for the first time in the worldwide fossil record. The higher proportion of new families in the Tethys may indicate a genuine centre of origin. This higher origination rate could be expected in low latitude environments if the energy supply (sea temperature) is regarded as the main factor in fish speciation. However, we should keep in mind that the Chalk fish assemblage is preceded by the Gault fish assemblage, while only a few fish assemblages are known in the late Early Cretaceous of central Tethys. That could partly explain the apparent burst in Tethyan diversity compared to the boreal succession. The boreal assemblages show evidences of vicariant events within the ichthyodectiforms between the Chalk seas of North America and Europe at the beginning of the Late Cretaceous. These events are poorly documented so far, but they rest on the presence on both continents of different species of Ichthyodectes, Xiphactinus, Prosaurodon and Saurodon (Cavin and Forey, in press). The freshwater fish faunas of that time are poorly known because of the high sea stand. However, Gayet et al. (2002) described a freshwater flock based on identification of isolated pinnules that may have occurred among African polypteriforms. In the Late Cretaceous, the signals provided by the environmental indicators are less good. There are possibly some new marine groups affected by sea temper-
ature, such as the albulids and the clupeomorphs, but the phylogenies within these clades are still too imperfectly resolved to provide a reliable signal. In freshwater environments, there are clues of a freshwater radiation among South American catfishes (Gayet, 2001) and possibly the esociforms (Grande, 1999) and phyllodontids (Estes, 1969) in North America, although the latter family remains phylogenetically and taxonomically enigmatic. Finally, there are some clues of vicariant events in the terminal Cretaceous, but they indicate unlikely geographical links and are probably the result of misidentifications or wrong relationships. These are a sister-group relationships between the osteoglossid Phareodus in India (Prasad, 1989; Mohabey and Udhoji, 1996) and Brychaetus in Bolivia (Gayet, 1991), of the percichthyid Percichthys in Bolivia (Gayet and Meunier, 1998) and Properca in Europe (known as a ghost lineage in the Late Cretaceous) and the more likely polyodontid Paleopsephurus in North America and the modern Chinese Psephurus. Molecular-based phylogenies and the occurrences of Cretaceous taxa, which imply the presence of their sister-groups at the same time, both indicate the existence of taxa in the Cretaceous not found in the fossil record so far. In particular, it is likely that the incipient diversifications of the major osteoglossomorph clades, such as the osteoglossiforms (Kumazawa and Nishida, 2000) and the mormyriforms (Alvez-Gomez, 1999), together with ostariophysan clades, such as the cypriniforms and the characiforms (Orti and Meyer, 1997; Alvez-Gomez, 1999; Saitoh et al., 2002; Filleul and Maisey, 2005), occurred in the Late Cretaceous, or even earlier (Peng et al., 2006), but their fossil records are still elusive. During our survey, the diversity of several clades does not appear to be forced by one of the three indicators defined here (“palaeonisciforms”, pycnodontiforms, semionotiforms, pachycormiforms, beryciforms, perciforms and tetraodontiforms). Hypotheses to explain these situations are plenty, and encompass the incompleteness of the fossil record, the poorly resolved phylogenetic relationships and/or sampling biases. However, there are modern examples of recent speciation events which are driven by factors not considered in our study. Marine fish species complexes may be triggered by local ecological parameters such as depth segregation or sexual selection in the northeastern Pacific Sebastes for instance (Alesandrini and Bernardi, 1999), by successive colonisations of refuge areas due to sea level variations during glacial/intergacial cycles for the bleniids (Almada et al., 2001), or by several historical factors such as periodic expansions of ice
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
sheets, movement of the Polar Front, variations in oceanic currents for the notothenioids (Bargelloni et al., 2000). The current palaeoenvironmental, stratigraphic and phylogenetic resolutions of our database are far from being precise enough to allow an assessment of these types of factors in a global survey of marine Late Mesozoic fishes. But we could expect to include some of these parameters in geographically and temporally more restricted future studies. Similarly, we cannot map an environment indicator to all recorded freshwater cladogenetic events. But some recent speciations in freshwater environments are driven by complex and mixed physical and historical factors (Oberdorff et al., 1997) that are beyond the resolution of detection in this study. Finally, it is possible that the diversity of some marine clades, such as the pycnodontiforms and possibly the tetraodontiforms, is controlled by the amount and diversity of available reef. 4.2. Correlation between fish diversity and sea temperature: towards an explanation Correlation need not necessarily imply causation and here we discuss more deeply the nature of the possible direct and indirect impacts of sea temperature on fish diversity through time. The correlations observed above are considered as limiting guidelines in the search for explanation. Correlation between Cretaceous actinopterygian diversity and fluctuating temperature has its modern analogue in species richness and latitudinal gradients where temperature and diversity are correlated for fishes (Rohde, 1992) and other groups. For foraminifera, the gradient through time has been generated by differences in the rate of increases during the Cainozoic (Buzas et al., 2002) and for the bivalves the gradient was already present in the Late Jurassic but became steeper during the Cretaceous and Cainozoic because of the radiation of tropical groups (Crame, 2002). Today, coral diversity, however, is only weakly correlated with the latitude (Fraser and Currie, 1996). Currie (1991) proposed that increased solar energy at low latitudes may result in increased productivity, energy turnover or niche partitioning, leading to more opportunities for speciation. In a review of the possible primary cause to explain the Recent latitudinal gradient, Rohde (1992) concludes that the primary cause is the effects of solar radiation (temperature) on evolutionary speed due to shorter generation times, higher mutation rates, and increased selection pressure. This hypothesis is partly supported by Buzas et al. (2002), who observed that a high rate of origination and extinction of foraminifera in the tropics, alongside the presence of many
363
rare endemic species, produce a larger component of short-lived evolutionary trials than in temperate realm. These hypotheses contradict time hypotheses, e.g. those that assume communities diversifying with time and, accordingly, that low latitude communities are older than high latitude communities. The correlation found here between sea temperature and fish diversity confirms that time hypotheses are unsatisfactory to explain the Recent latitudinal gradient, as sea temperature has a synchronous (in a geological sense) link with fish diversity (the fish diversity curve is not postponed respective to the temperature curve). Solar energy may affect fish speciation directly, but may also affect speciation is other groups ecologically closely related to the marine actinopterygians. The midCretaceous was a time of rapid radiation and turnover in the marine plankton, benthic foraminifera and molluscs (Leckie et al., 2002). Among these groups, the plankton constitutes the base of the trophic pelagic chain on which depend so many marine fishes. Major changes in the abundance and composition of the plankton would certainly affect the evolutionary dynamic of the fishes occupying the higher levels of the food chain. Reef production through time, on the other hand, is more easily compiled as they produce carbonate, which can be measured (Kiessling et al., 2000). Today, the diversity of some coral reef fishes shadows that of the hermatypic (reef building) corals (Rosen, 1988) leading to the possibility of a common underlying effect. In a multiregression analysis of several environmental descriptors, Fraser and Currie (1996) found that coral diversity is better correlated to available energy. They also identified a good correlation between regional coral and fish diversity. In a study of long-term fluctuations in the carbonate production of Phanerozoic reefs, Kiessling et al. (2000) have shown that reefal carbonate production is controlled by eustatic sea level fluctuations, oceanic production rates, atmospheric CO2 concentrations, global climatic modes (greenhouse versus icehouse), mean global precipitation, continental runoff and global nutrient levels. 5. Conclusion The results presented here suffer from two main weaknesses which are the patchy spatial and temporal distributions of the data and their extremely coarsegrained resolution. This situation contrasts sharply with the fine molecular phylogenetic species-level biogeographic studies performed today on living organisms. However, we propose that the results we obtained here provide complementary information on the long-term
364
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
engines driving evolution. In particular, it shows that the environment parameters forcing the evolution within a single taxonomic group, the actinopterygians, may be gathered into a few broad categories, which vary strongly with time. The main results are (1) although the picture we got is altered by the biases of the fossil record, fish speciation in marine environment varies with some environmental factors related to the available energy. (2) It is demonstrated that the vicariant events are not the only evolutionary process in action over a long time interval and at a large geographical scale at least. (3) Most of the clades, from different taxonomic ranks, appear to be generally forced by a single general indicator. Exceptions occurred when members of the clades can spread between environments. (4) The indicator that best correlates with marine ray-finned fishes is the surface sea temperature. (5) There are indirect evidences that a large portion of the actinopterygian evolution in freshwater environment during the Cretaceous is not detected in the fossil record so far. We should focus research effort on the continental Cretaceous fish localities, which are plentiful but currently poorly studied. Acknowledgments Funding was provided by a Marie Curie Individual Fellowship funded by the Swiss Federal Office for Education and Science (LC, grant n° 02.0335). We thank R. Fortey (The Natural History Museum), M. Wilson (University of Alberta) and A. Gale (The Natural History Museum) for comments on previous versions of the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j. palaeo.2006.08.010. References Alesandrini, S., Bernardi, G., 1999. Ancient species flocks and recent speciation events: what can rockfish teach us about cichlids (and vice versa). Journal of Molecular Evolution 49, 814–818. Almada, V.C., Oliveira, R.F., Gonçalves, E.J., Almeida, A.J., Santos, R.S., Wirtz, P., 2001. Patterns of diversity of the north-eastern Atlantic bleniid fish fauna (Pisces: Blenniidae). Global Ecology and Biogeography 10, 411–422. Alroy, J., Marshall, C.R., Bambach, R.K., Bezusko, K., Foote, M., Fürsich, F.T., Hansen, T.A., Holland, S.M., Ivany, L.C., Jablonski, D., Jacobs, D.K., Jones, D.C., Kosnik, M.A., Lidgard, S., Low, S., Miller, A.I., Novack-Gottshall, P.M., Olszewski, T.D., Patzkowsky, M.E., Raup, D.M., Roy, K., Sepkoski Jr., J.J., Sommers, M.G., Wagner, P.J., Webber, A., 2001. Effects of sampling
standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences of the United States of America 6261–6266. Alvez-Gomez, J.A., 1999. Systematic biology of gymnotiform and mormyriform electric fishes: phylogenetic relationships, molecular clocks and rates of evolution in the mitochondrial rRNA genes. The Journal of Experimental Biology 202, 1167–1183. Arratia, G., 1997. Basal Teleosts and teleostean phylogeny. PalaeoIchthyologica 7, 5–168. Arratia, G., 2000. Remarkable teleostean fishes from the Late Jurassic of southern Germany and their phylogenetic relationships. Mitteilungen aus dem Museum für Naturkunde in Berlin. Geowissenschaftliche 2, 137–179. Bargelloni, L., Marcato, S., Zane, L., Patanello, T., 2000. Mitochondrial phylogeny of Notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Systematic Biology 49, 114–129. Barraclough, T.G., Nee, S., 2001. Phylogenetics and speciation. Trends in Ecology and Evolution 16, 391–399. Barraclough, T.G., Vogler, A.P., Harvey, P.H., 1998. Revealing the factors that promote speciation. Philosophical Transactions of the Royal Society of London. B 353, 241–249. Beheregaray, B.L., Sunnucks, P., Briscoe, D.A., 2001. A rapid fish radiation associated with the last sea-level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proceedings of the Royal Society of London. B 269, 65–73. Benton, M.J., Pearson, P.N., 2001. Speciation in the fossil record. Trends in Ecology and Evolution 16, 405–411. Bernardi, G., Bucciarelli, G., Costagliola, D., Roertson, D.R., Heiser, J.B., 2004. Evolution of coral reef fish Thalassoma spp. (Labridae). 1. Molecular phylogeny and biogeography. Marine Biology 144, 369–375. Bock, W.J., 2004. Species: the concept, category and taxon. Journal of Zoological Systematics and Evolutionary Research 42, 172–190. Bond, C.E., 1996. Biology of Fishes, 2nd edition. Saunders College Publishing, Forth Worth. 750 pp. Bonde, N., 1996. Osteoglossids (Teleostei: Osteoglossomorpha) of the Mesozoic. Comments on their interrelationships. In: Arratia, G., Viohl, G. (Eds.), Mesozoic Fishes-Systematics and Paleoecology. Verlag Dr. Friedrich Pfeil, München, Germany, pp. 273–284. Briggs, J.C., 2003. Marine centres of origin as evolutionary engines. Journal of Biogeography 30, 1–18. Brito, P.M., 1997. Révision des Aspidorhynchidae (Pisces, Actinopterygii) du Mésozoïque : Ostéologie, relations phylogénétiques, données environnementales et biogéographiques. Geodiversitas 19, 681–772. Burridge, C.P., 2000. Biogeographic history of geminate cirrhitoids (Perciformes: Cirrhitoidea) with east–west allopatric distributions across southern Australia, based on molecular data. Global Ecology and Biogeography 9, 517–525. Buzas, M.A., Collins, L.S., Culver, S.J., 2002. Latitudinal difference in biodiversity caused by higher tropical rate of increase. Proceedings of the National Academy of Sciences of the United States of America 99, 7841–7843. Cavin, L., Brito, P.M., 2001. A new Lepisosteidae (Actinopterygii: Ginglymodi) from the Cretaceous of the Kem Kem beds, southern Morocco. Bulletin de la Société Géologique de France 172, 141–150. Cavin, L., Suteethorn, V., 2006. A new Semionotiformes (Actinopterygii, Neopterygii) from Late Jurassic – Early Cretaceous of Northeastern Thailand with comments on the semionotiformes relationships. Paleontology 49, 339–353.
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367 Cavin, L., Forey, P.L., in press. Osteology of Eubiodectes libanicus (Pictet & Humbert, 1866) and some other ichthyodectiformes (Teleostei): phylogenetic implications. Journal of Systematic Palaeontology. Cavin, L., Jurkovšek, B., Kolar- Jurkovšek, T., 2005. The midCretaceous fish assemblages from the Komen–Trieste plateau in Slovenia: its palaeogeographic and palaeoenvironmental significance. In: Poyato-Ariza, F. (Ed.), Fourth meeting on Mesozoic fishes — Systematics, Homology, and Nomenclatur, Extended abstracts, Madrid, Servicio de Publicaciones de la Universidad Aunonoma de Madrid / UAM Ediciones, pp. 67–68. Cavin, L., Suteethorn, V., Buffetaut, E., Claude, J., Cuny, G., Le Loeuff, J., Tong, H., in press. The first sinamiid fish (Holostei, Halecomorpha) from South-east Asia (Early Cretaceous of Thailand). Journal of Vertebrate Paleontology. Chang, M.M., Chen, Y.Y., 2000. Late Mesozoic and Tertiary ichthyofaunas from China and some puzzling patterns of distribution. Vertebrata PalAsiatica 38, 161–175. Chang, M.M., Jin, F., 1996. Mesozoic fish faunas of China. In: Arratia, G., Viohl, G. (Eds.), Mesozoic Fishes — Systematics and Paleoecology. Verlag Dr Friedrich Pfeil München, pp. 461–478. Chang, M.M., Maisey, J.G., 2003. Redescription of †Ellimma branneri and †Diplomystus shengliensis, and relationships of some basal clupeomorphs. American Museum Novitates 3404, 1–35. Chang, M.M., Miao, D., 2004. An overview of Mesozoic fishes in Asia. In: Arratia, G., Tintori, A. (Eds.), Mesozoic Fishes 3 — Systematic, Paleoenvironment and biodiversity. Verlag Dr. Friedrich Pfeil, München, pp. 535–563. Clarke, L.J., Jenkyns, H.C., 1999. New oxygen isotope evidence for long-term Cretaceous climatic changes in the Southern Hemisphere. Geology 27, 699–702. Crame, J.A., 2002. Evolution of taxonomic diversity gradients in the marine realm: a comparison of Late Jurassic and Recent bivalve faunas. Paleobiology 28, 184–207. Currie, D.J., 1991. Energy and large-scale patterns of animal- and plant-species richness. American Naturalist 137, 27–49. De Lurio, J.L., Frakes, L.A., 1999. Glendonite as a paleoenvironmental tool: implications for early Cretaceous high latitude climates in Australia. Geochimica et Cosmochimica Acta 63, 1039–1048. DeMarais, B.D., Dowling, T.E., Douglas, M.E., Minckley, W.L., Marsh, P.C., 1992. Origin of Gila seminude (Teleostei: Cyprinidae) through introgressive hybridization: implications for evolution and conservation. Proceedings of the National Academy of Sciences of the United States of America 89, 2747–2751. Dergam, J.A., Paiva, S.R., Schaeffer, C.E., Godinho, A.L., Vieira, F., 2002. Phylogeography and RAPD-PCR variation in Hoplias malabaricus (Bloch, 1794) (Pisces, Teleostei) in southeastern Brazil. Genetics and Molecular Biology 25, 379–387. Echelle, A.A., Echelle, A.E., 1992. Mode and pattern of speciation in the evolution of inland pupfishes in the Cyprinodon variegatus complex (Teleostei: Cyprinodontidae): an ancestor–descendant hypothesis. In: Mayden, R.L. (Ed.), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, pp. 691–709. Estes, R., 1969. Studies on fossil phyllodont fishes: interrelationships and evolution in the phyllodontidae (albuloidei). Copeia 2, 317–331. Filleul, A., Maisey, J.G., 2005. Redescription of Santanichthys diasii (Otophysi, Characiformes) from the Albian of the Santana Formation and comments on its implications for otophysan relationships. American Museum Novitates 3455, 1–21. Forey, P.L., Grande, L., 1998. An African twin to the Brazilian Calamopleurus (Actinopterygii: Amiidae). Zoological Journal of the Linnean Society 123, 179–195.
365
Forey, P.L., Yi, L., Patterson, C., Davies, C.E., 2003. Fossil fishes from the Cenomanian (Upper Cretaceous) of Namoura, Lebanon. Journal of Systematic Palaeontology 1, 227–330. Forey, P.L., Fortey, R.A., Kenrick, P., Smith, A.B., 2004. Taxonomy and fossils: a critical appraisal. Philosophical Transactions of the Royal Society of London. B 359, 639–653. Frakes, L.A., 1999. Estimating the global thermal state from Cretaceous sea surface and continental temperature data. Geological Society of America, Special Paper 332, 49–57. Fraser, R.H., Currie, D.J., 1996. The species richness-energy hypothesis in a system where historical factors are thought to prevail: coral reefs. American Naturalist 148, 138–159. Froese, R., Pauly, D. (Eds.), 2006. FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2006). Gale, A.S., 2000. The Cretaceous world. In: Culver, S.J., Rawson, P.F. (Eds.), Biotic Response to Global Change. The Last 145 Million Years. Cambridge University Press, Cambridge, pp. 1–19. Gayet, M., 1991. “Holostean” and Teleostean fishes of Bolivia. Revista Técnica de YPFB 12, 453–494. Gayet, M., 2001. Biogéographie vs paléobiogéographie : approche concurrente ou complémentaire? Quid des poissons? Biosystema 19, 149–167. Gayet, M., Meunier, F., 1998. Maastrichtian to Early Paleocene freshwater osteichthyes of Bolivia: additions and comments. In: Malabara, L.R., Reis, R.E., Vari, R.P., Lucena, Z.M.S., Lucena, C.A.S. (Eds.), Phylogeny and classification of neotropical fishes. EDIPUCRS, Porto Alegre, pp. 85–110. Gayet, M., Meunier, F., Werner, C., 2002. Diversification in Polypteriformes and special comparison with the Lepisosteiformes. Palaeontology 45, 361–376. Grady, J.M., LeGrande, W.H., 1992. Phylogenetic relationships, modes of speciation and historical biogeography of the Madtom catfish, genus Noturus Rafinesque (Siluriformes: Ictaluridae). In: Mayden, R.L. (Ed.), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, pp. 747–777. Grande, L., 1999. The first Esox (Esocidae: Teleostei) from the Eocene Green River Formation, and a brief review of esocid fishes. Journal of Vertebrate Paleontology 19, 271–292. Grande, L., Bemis, E., 1991. Osteology and phylogenetic relationships of fossil and Recent paddlefishes (Polyodontidae) with comments on the interrelationships of Acipenseriformes. Journal of Vertebrate Paleontology 11, 1–121. Grande, L., Bemis, W.E., 1998. A comprehensive phylogenetic study of amiid fishes (amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history. Supplement to Journal of Vertebrate Paleontology, Memoir 4, 1–690. Grande, L., Jin, F., Yabumoto, Y., Bemis, W.E., 2002. Protopsephurus liui, a well-preserved primitive paddlefish (Acipenseriformes: Polyodontidae) from the Lower Cretaceous of China. Journal of Vertebrate Paleontology 22, 209–237. Grande, T., Poyato-Ariza, F.J., 1995. A cladistic analysis of fossil and living gonorhynchiform ostariophysan fishes. Géobios. Mémoire Spécial 19, 197–199. Grande, T., Poyato-Ariza, F.J., 1999. Phylogenetic relationships of fossil and Recent gonorynchiform fishes (Teleostei: Ostariopysi). Zoological Journal of the Linnean Society 125, 197–238. He, S., Ca, W., Chen, Y., 2001. The uplift of Qinghai-Xizang (Tibet) plateau and the vicariance speciation of glyptosternoid fishes (Siluriformes: Sisoridae). Science in China. Series C 44, 644–651. Hitchin, R., Benton, M.J., 1997. Congruence between Parsimony and Stratigraphy: Comparisons of Three Indices. Paleobiology 23, 20–32.
366
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367
Huber, B.T., Hodell, D.A., Hamilton, C.P., 1995. Middle–Late Cretaceous climate of the southern high latitudes: stable isotopic evidence for minimal equator-to-pole thermal gradients. Geological Society of America Bulletin 107, 1164–1191. Hunn, C.A., Upchurch, P., 2001. The importance of time/space in diagnosing the causality of phylogenetic events: towards a “chronobiogeographical” paradigm? Systematic Biology 50, 391–407. Jin, F., 1999. Middle and Late Mesozoic acipenseriforms from northern Hebei and western Liaoling, China. In: Chen, P.-J., Jin, F. (Eds.), Palaeoworld. Press of University of Science and Technology of China, Hefei, pp. 188–261. Kiessling, W., 2005. Long-term relationships between ecological stability and biodiversity in Phanerozoic reefs. Nature 433, 410–413. Kiessling, W., Flügel, E., Golonka, J., 2000. Fluctuations in the carbonate production of Phanerozoic reefs. In: Insalaco, E., Skelton, P.W., Palmer, T.J. (Eds.), Carbonate platform systems: components and interactions. Geological Society Special Publication, London, pp. 191–215. Knight, M.E., Turner, G.F., 2004. Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi. Proceedings of the Royal Society of London. B 269, 675–680. Kolodny, Y., Luz, B., Navon, O., 1983. Oxygen isotope variations in phosphate of biogenic apatites, I. Fish bone apatite-rechecking the rules of the game. Earth and Planetary Science Letters 64, 398–404. Kolodny, Y., Luz, B., Sander, M., Clemens, W.A., 1996. Dinosaur bones: fossil or pseudomorph? The pitfalls of physiology reconstruction from apatitic fossils. Palaeogeography, Palaeoclimatology, Palaeoecology 126, 161–171. Kumazawa, Y., Nishida, M., 2000. Molecular phylogeny of Osteoglossoids: a new model for Gondwanian origin and plate tectonic transportation of the Asian Arowana. Molecular Biology and Evolution 17, 1869–1878. Lazarus, D.B., 2001. Speciation and morphological evolution. In: Briggs, D.E., Crowther, P.R. (Eds.), Palaeobiology II. Blackwell Scientific, Oxford, pp. 133–137. Leckie, R.M., Bralower, T.J., Cashman, R., 2002. Oceanic anoxic events and plankton evolution: biotic response to tectonic forcing during the mid-Cretaceous. Paleoceanography 17, 1–29. Lécuyer, C., Grandjean, P., Sheppard, S.M.F., 1999. Oxygen isotope exchange between dissolved phosphate and water at temperatures b135 °C: inorganic versus biological fractionations. Geochimica et Cosmochimica Acta 63, 855–862. Lécuyer, C., Picard, S., Garcia, J.-P., Sheppard, S.M.F., Grandjean, P., Dromart, G., 2003. Thermal evolution of Tethyan surface waters during the Middle–Late Jurassic: evidence from δ18O values of marine fish teeth. Paleoceanography 18 (1076), 863–879. Lee, Y.N., Yu, K.M., Wood, C.B., 2001. A review of vertebrate faunas from the Gyeongsang Supergroup (Cretaceous) in South Korea. Palaeogeography, Palaeoclimatology, Palaeoecology 165, 357–373. Losos, J.B., Glor, R.E., 2003. Phylogenetic comparative methods and the geography of speciation. Trends in Ecology and Evolution 18, 221–227. Maisey, J.G., 2000. Continental break up and the distribution of fishes of Western Gondwana during the Early Cretaceous. Cretaceous Research 2000, 281–314. Mayden, R.L., Matson, R.H., Hillis, D.M., 1992. Speciation in the North American genus Dionda (Teleostei: Cypriniformes). In: Mayden, R.L. (Ed.), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, pp. 710–746.
McCarthy, D., 2003. The trans-Pacific zipper effect: disjunct sister taxa and matching geological outlines that link the Pacific margins. Journal of Biogeography 30, 1545–1561. Mohabey, D.M., Udhoji, S.G., 1996. Fauna and Flora from Late Cretaceous (Maestrichtian) non-marine Lameta sediments associated with Deccan Volcanic Episode, Maharashtra: its relevance to the K–T Boundary problem, paleoenvironment and paleogeography. Gondwana Geol. Mag., Suppl. vol. 2, Nat. Symp. Deccan Flood Basalts, India, pp. 349–364. Mora, C., Chittaro, P.M., Sale, P.F., Kritzer, J.P., Ludsin, S.A., 2003. Patterns and processes in reef fish diversity. Nature 421, 933–936. Norell, M.A., 1992. Taxic origin and temporal diversity: the effect of phylogeny. In: Novacek, M.J., Wheeler, Q.D. (Eds.), Extinction and phylogeny. Columbia University Press, Cambridge, pp. 88–118. Oberdorff, T., Hugueny, B., Guégan, J.F., 1997. Is there an influence of historical events on contemporary fish species richness in rivers? Comparisons between Western Europe and North America. Journal of Biogeography 24, 461–467. Omland, K.E., Tarr, C.L., Boarman, W.I., Marzluff, J.M., Fleischer, R.C., 2000. Cryptic genetic variation and paraphyly in ravens. Proceedings of the Royal Society of London 267, 2475–2482. Orti, G., Meyer, A., 1997. The radiation of characiform fishes and the limits of resolution of mitochondrial ribosomal DNA sequences. Systematic Biology 46, 75–100. Peng, Z., He, S., Wang, W., Rui, D., 2006. Mitochondrial molecular clocks and the origin of the major Otocephalan clades (Pisces: Teleostei): a new insight. Gene 370, 113–124. Pequeno, G., Lamilla, J., 2000. The littoral fish assemblage of the Desventuradas islands (Chile) has zoogeographical affinities with western Pacific. Global Ecology and Biogeography 9, 431–437. Peters, S.E., 2005. Geological constraints on the macroevolutionary history of marine animals. Proceedings of the National Academy of Sciences of the United States of America 102, 12326–12331. Picard, S., Garcia, J.P., Lécuyer, C., Sheppard, S.M.F., Cappetta, H., Emig, C., 1998. δ18O values of coexisting brachiopods and fish: temperature differences and estimates of paleo-water depths. Geology 26, 975–978. Prasad, G.V.R., 1989. Vertebrate fauna from the Infra- and Intertrappean Beds of Andhra Pradesh: age implications. Journal Geological Society of India 34, 161–173. Price, G.D., 1999. The evidence and implications of polar ice during the Mesozoic. Earth-Science Reviews 48, 183–210. Price, G.D., Sellwood, B.W., Corfield, R.M., Clarke, L., Cartlidge, J.E., 1998. Isotopic evidence for palaeotemperatures and depth stratification of Middle Cretaceous planktonic foraminifera from the Pacific Ocean. Geological Magazine 135, 183–191. Pucéat, E., Lécuyer, C., Sheppard, S.M.F., Dromart, G., Reboulet, S., Grandjean, P., 2003. Thermal evolution of Cretaceous Tethyan marine waters inferred from oxygen isotope composition of fish tooth enamels. Paleoceanography 18, 1–12. Ramstein, G., Fluteau, F., Masson, V., 1997. Existence of an ice cap during the mid-Cretaceous period (120–90 Ma): an AGCM investigation. Annals of Glaciology 25, 198–202. Raup, D.M., 1986. Biological extinction in earth history. Science 231, 1528–1533. Rieseberg, L.H., 1997. Hybrid origins of plant species. Annual Review of Ecology and Systematics 28, 359–389. Rocha, L.A., 2003. Patterns of distribution and processes of speciation in Brazilian reef fishes. Journal of Biogeography 30, 1161–1171. Rohde, K., 1992. Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514–527.
L. Cavin et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 245 (2007) 353–367 Rosen, D.E., 1975. A vicariance model of Caribbean biogeography. Systematic Zoology 24, 431–464. Rosen, B.R., 1988. Progress, problems and patterns in the biogeography of reef corals and other tropical marine organisms. Helgoländer Meeresuntersuchungen 42, 269–301. Roshan, U., Moret, B.M.E., Warnow, T., Williams, T.L., 2004. Performance of supertree methods on various dataset decompositions. In: Bininda-Edmonds, O.R.P. (Ed.), Phylogenetic supertrees: Combining information to reveal the tree of life. Kluwer Academic Publishers, Dordrecht, pp. 301–328. Saint-Seine, P.D., 1955. Poissons fossiles de l'étage de Stanleyville (Congo belge). Première partie: la faune des argilites et schistes bitumineux. Annales Musée Royal du Congo Belge 14, 1–126. Saitoh, K., Miya, M., Inoue, J.G., Ishiguro, N.B., Nishida, M., 2002. Mitochondrial genomics of Ostariophysan fishes: perspectives on phylogeny and biogeography. Journal of Molecular Evolution 56, 464–472. Salewski, V., 2003. Satellite species in lampreys: a worldwide trend for ecological speciation in sympatry? Journal of Fish Biology 63, 267–279. Seehausen, O., 2002. Patterns in fish radiation are compatible with Pleistocene desiccation of Lake Victoria and 14 600 year history for its cichlid species flock. Proceedings of the Royal Society of London. B 269, 491–497. Sepkoski, J.J., 1997. Biodiversity: past, present, and future. Journal of Paleontology 71, 533–539. Sepkoski, J.J., 1998. Rate of speciation in the fossil record. Philosophical Transactions of the Royal Society, London, B 353, 315–326. Shackleton, N.J, Kennett, J.P., 1975. Paleotemperature history of the Cenozoic and the initiation of Antarctic glaciation: oxygen and carbon isotope analyses in DSDP sites 277, 279, and 281. Initial Reports of the Deep Sea Drilling Project 29, 743–756. Sharp, Z.D., Atudorei, V., Furrer, H., 2000. The effect of diagenesis on oxygen isotope ratios of biogenic phosphates. American Journal of Sciences 300, 222–237. Shaw, P.W., Turner, G.F., Idid, M.R., Robinson, R.L., Carvalho, G.R., 2000. Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids. Proceedings of the Royal Society of London. B 267, 2273–2280. Smith, A.B., 1994. Systematics and the fossil record. Documenting evolutionary patterns. Blackwell Scientific, Oxford. Smith, A.B., Gale, A.S., Monks, N.E.A., 2001. Sea-level change and rock-record bias in the Cretaceous: a problem for extinction and biodiversity studies. Paleobiology 27, 241–253.
367
Smith, G.R., 1992a. Introgression in fishes: significance for paleontology, cladistics, and evolutionary rates. Systematic Biology 41, 41–57. Smith, G.R., 1992b. Phylogeny and biogeography of the Catostomidae, freshwater fishes of North America and Asian. In: Mayden, R.L. (Ed.), Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, pp. 778–826. Stoll, H.M., Schrag, D.P., 2000. High resolution stable isotope records from the Upper Cretaceous rocks of Italy and Spain: glacial episodes in a greenhouse planet? Geological Society of America Bulletin 112, 308–319. Taverne, L., 1998. Les Ostéoglossomorphes marins de l'Eocène du Monte Bolca (Italie): Monopterus Volta 1796, Thrissopterus Heckel, 1856 et Foreyichthys Taverne, 1979. Considérations sur la phylogénie des téléostéens Ostéoglossomorphes. Studi e Ricerche sui Giacimenti Terziari di Bolca. VII. Museo Civico di Storia Naturale, Verona, pp. 67–158. Taylor, P., 2004. Extinction and the fossil record. In: Taylor, P. (Ed.), Extinctions in the History of Life. Cambridge Univ. Pr, pp. 1–34. Unmack, P.J., 2001. Biogeography of Australian freshwater fishes. Journal of Biogeography 28, 1053–1089. Upchurch, P., Hunn, C.A., Norman, D.B., 2002. An analysis of dinosaurian biogeography: evidence for the existence of vicariance and dispersal patterns caused by geological events. Proceedings of the Royal Society of London. B 269, 613–621. Van Valen, L., 1973. A new evolutionary law. Evolutionary Theory 1, 1–30. Vermeij, G.J., 1995. Economics, volcanoes, and phanerozoic revolutions. Paleobiology 21, 125–152. Via, S., 2001. Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology and Evolution 16, 381–390. Wagner, P.J., 2000. The quality of the fossil record and the accuracy of phylogenetic inferences about sampling and diversity. Systematic Biology 49, 65–86. Waters, J.M., Lopez, J.A., Wallis, G., 2000. Molecular phylogenetics and biogeography of Galaxiid fishes (Osteichthyes: Galaxiidae): dispersal, vicariance, and the position of Lepidogalaxias salamandroides. Systematic Biology 49, 777–795. Wiley, E.O., 1988. Vicariance biogeography. Annual Review of Ecology and Systematics 19, 513–542. Yabumoto, Y., 1994. Early Cretaceous Freshwater Fish Fauna in Kyushu, Japan. Bulletin of the Kitakyushu Museum of Natural History 13, 107–254.
