Marine Biology '2001) 138: 11±22 Ó Springer-Verlag 2001
G. M. Wellington á D. R. Robertson Variation in larval life-history traits among reef ®shes across the Isthmus of Panama
Received: 19 January 2000 / Accepted: 26 September 2000
Abstract We tested the hypothesis that regional dier- variation within regions) occur in both families and ences in oceanic productivity have led to the evolution of evidently overwhelm any eect of regional variation in predictable patterns of regional variation in life-history productivity. Reassessment of data that takes into traits of pelagic larvae of tropical reef ®shes. To do so we account such phylogenetic eects questions previous compared larval traits 'egg and hatchling size, larval conclusions about the existence of regional dierences in growth rate and duration, and size at settlement) among larval traits among damsel®shes in the West Paci®c and closely related reef ®shes from the Atlantic and Paci®c the Caribbean. coasts of the Isthmus of Panama. This comparison provides a control for phylogenetic eects because those regions shared a common fauna prior to the rise of the Introduction Isthmus 3.5 million years ago, subsequent to which each fauna evolved independently under a very dierent Phylogenetic background productivity regime. We measured larval traits of 12 benthic-spawning damsel®shes 'Pomacentridae: Abu- Considerable recent progress has been made in our un- defduf, Chromis and Stegastes) and 13 pelagic-spawning derstanding of the biology and ecology of coral reef wrasses 'Labridae: Bodianus, Halichoeres and Thalasso- ®shes, particularly for benthic juveniles and adults ma). These included members of each genus on each side 'Doherty 1991; Sale 1991). The vast majority of tropical of the Isthmus and four sets of transisthmian sister reef ®shes have a juvenile pelagic stage at the beginning species of pomacentrids. Among the pomacentrids we of their life, but much less is known about the biology of found consistent transisthmian dierences in hatchling this stage. Recent studies that examined the biology of size, but not in other larval traits. Essentially the reverse larval reef ®shes have focused on their identi®cation, pattern occurred among the labrids ± larval growth behavior, ecological requirements, patterns of distribu- and duration diered consistently among congeners in tion in the open ocean and how oceanic processes in- the two regions, but without consistent dierences in ¯uence the spatial and temporal dynamics of settlement hatchling size or size at settlement. Neither relationship of larvae to the reef at the end of their pelagic lives 'e.g. is predicted by the regional-productivity hypothesis. Jones et al. 1999; Robertson et al. 1999; Swearer et al. Most of the dierences were quite small. Stronger phy- 1999). In comparison few studies have examined the logenetic eects on larval traits 'inter- and intrageneric enormous variation that occurs in larval life-history patterns from an evolutionary perspective, and much of that attention was directed to biogeographic questions 'Thresher and Brothers 1985, 1989; Leis 1991; Victor Communicated by N. Marcus, Tallahassee 1991). Thresher '1982) examined variation in egg size among G. M. Wellington '&) reef ®shes in the two most-studied parts of the tropics ± Department of Biology and Biochemistry, Program in Ecology and Evolutionary Biology, the Caribbean and western Paci®c. He noted that in two University of Houston, Houston, TX 77204-5513, USA of three families of benthic-spawning ®shes, eggs of Fax: +1-713-7432636; West Paci®c species were substantially larger 'in volume) e-mail: [email protected] than those of Caribbean species. Thresher adapted ex- D. R. Robertson isting hypotheses concerning the relationship between Smithsonian Tropical Research Institute 'Panama), size at hatching and variation in larval food availability Unit 0948, APO AA 34002-0948, USA 'larger larvae have greater reserves and hence have 12 higher survivorship under low food availability ± geminates in Chromis 'Bermingham et al. 1997), and the Cushing 1967; Bagenal 1971) and proposed that those construction of a global phylogeny of the labrid genus regional dierences in egg size represented evolutionary Thalassoma 'G. Bernardi et al., unpublished). As yet responses to regional dierences in productivity: in re- there have been no comprehensive genetic studies of the gions of lower productivity, selection has favored the other two labrid genera, Bodianus and Halichoeres, production of large eggs to provide increased provi- which limits our interpretations of transisthmian pat- sioning of hatchling larvae. terns in these two groups. Thresher and Brothers '1989) extended and presented additional data relevant to the ``regional-productivity hypothesis'' by proposing that in regions of low pro- Climatological and geological setting ductivity higher provisioning of hatchlings leads to higher larval growth rates and a reduction in the time Marine climatology in Panama is directly in¯uenced by spent in the larval stage 'the pelagic larval duration or the position of the Inter-Tropical Convergence Zone PLD). However, as Victor '1986) pointed out, there is 'ITCZ). There the rainy season occurs from May to no a priori reason to expect that, under low productivity December, when the ITCZ is positioned north of Pan- conditions, high hatchling provisioning will lead to ama. During this period warm water conditions, light higher growth throughout the larval stage and hence to a variable winds and high cloud cover prevail on both reduced PLD, because greater food availability in high sides of the Isthmus. When the ITCZ shifts south of productivity conditions could lead to compensatory in- Panama 'January±April), the northeast tradewinds blow creases in larval growth rates. across the Isthmus. During this period there is reduced The aim of the present study was to test the regional- rainfall in the Gulf of Panama, as well as intense wind- productivity hypothesis as proposed by Thresher '1982) driven upwelling. In the Gulf of Panama the mean sea- and Thresher and Brothers '1989), and the modi®cation sonal sea surface temperature 'SST) 'between 1993 and of it proposed by Victor '1986). Perhaps the best test of 1996) was 2.6 °C, with minima during the dry and wet an evolutionary hypothesis that would control for phy- seasons of 18.7 °C 'or lower) and 24.9 °C, respectively logenetic eects would involve comparisons of con- 'D'Croz and Robertson 1997). In contrast, seasonal speci®c populations in regions with diering monthly mean SSTs on the Caribbean side of the isth- productivity. Another course, which we have taken, in- mus diered by only 0.2 °C, with a minimum of 26.6 °C. volves comparisons of congeneric species that had a More importantly, average levels of nutrients and common evolutionary history up to some point in the chlorophyll are consistently higher on the Paci®c side of not too distant past when they separated and evolved in the Isthmus, and phytoplankton and zooplankton isolation under dierent productivity regimes. The clo- abundances are 2±10 times higher and 6±10 times higher, sure of the Central American seaway some 3.5 million respectively, on that coast 'Table 1). Even during the years ago 'Coates 1997) and the subsequent independent non-upwelling season, productivity indicators are still evolution of the reef-®sh fauna on the Caribbean and substantially higher on the Paci®c side than on the Ca- Paci®c coasts of the Isthmus presents such a situation, ribbean side. because waters of the Paci®c coast of Panama, in the The emergence of the Isthmus of Panama, 3to Bay of Panama, have substantially higher productivity 3.5 million years before present 'Keigwin 1982; Coates than those on the Caribbean coast of Panama 'D'Croz 1997) not only resulted in the isolation and subsequent and Robertson 1997). In addition, the presence of divergence of a common Atlantic and eastern Paci®c transisthmian pairs of geminate species that were formed marine biota, but also eected dramatic changes in by the subdivision of a single species during the rise of marine climate, particularly in the eastern Paci®c. Prior the isthmus 'Rosenblatt et al. 1972; Vawter et al. 1980; to formation of the Central American land bridge, the Gorman and Kim 1983) provides a control for phylo- westward ¯owing warm Equatorial Atlantic Current genetic eects in our test. In this regard our study is 'EAC) maintained consistently warm water conditions aided by recent molecular phylogenetic studies of several by Caribbean ¯ow into the tropical eastern Paci®c of the genera we consider here: the establishment of 'Maier-Reimer et al. 1990). Following the closure of the global phylogenies for Abudefduf 'Bermingham et al. Isthmus, the Caribbean region remained under the in- 1997) and Stegastes 'H.A. Lessios and D.R. Robertson, ¯uence of the EAC. In contrast, much of the tropical unpublished), as well as the tentative identi®cation of eastern Paci®c became subject to extensive, strong sea-
Table 1 Summary of oceano- graphic conditions across the Bay of Panama 'Paci®c) San Blas Point 'western Atlantic) Isthmus of Panama for the Bay of Panama, Paci®c and San Dry season Wet season Dry season Wet season Blas Point, Caribbean. From D'Croz and Robertson '1997). Temperature '°C) 25.5 '0.2) 28.1 '0.1) 27.9 '0.0) 28.7 '0.0) Chorolophyll a 'mg m)3) 1.48 '0.07) 0.59 '0.01) 0.36 '0.01) 0.41 '0.02) Values represent means and )1 standard error 'in parentheses) Phytoplankton 'cells ml ) 663.3 '47.3) 166.4 '8.3) 60.3 '2.3) 99.9 '6.0) Zooplankton '´103 sample)1) 8.76 '1.00) 7.02 '0.50) 0.80 '0.03) 1.15 '0.04) 13 sonal upwellings that were induced by easterly trade- taking the average weight of 50 individuals clutch)1 that had been winds passing over three large low-elevation corridors dried for 8 h in a lyophilizer. Hatchlings were weighed on a Cahn Microbalance. 'the isthmuses of Tehuantepec, Papagayo and Panama) Planktonic larval duration was determined by counting the in Central America. number of daily increments in the otoliths 'see Victor 1986; Wel- lington and Victor 1989). Extracted otoliths were cleaned, dried and placed on a microscope slide in immersion oil for at least 2 weeks. Counts were made under a compound microscope at 400´ using transmitted light, with a linear polarizing ®lter between Materials and methods the light source and the slide. For pomacentrids, daily increments were counted using lapillae, while sagittae were used in labrids. Fieldwork Counts for pomacentrids were made from the center 'primordium) of the otolith to a point where the width of the daily increments In this study we surveyed the early life-history traits in 12 species of changed abruptly. This change indicates a shift from a pelagic to pomacentrids 'eight from the Caribbean and four from the Paci®c) benthic existence 'Wellington and Victor 1989). For the labrids, and 13 species of labrids 'seven from the Caribbean and six from counting stopped at the beginning of the ``settlement mark''. That the Paci®c) 'Table 2). Data for eastern Paci®c ®shes were collected mark is composed of fainter increments that are formed over a at Pacheca Island, the most northern island in the Perlas archi- period of several days post-settlement, while these ®sh are thought pelago, Bay of Panama from 17 October 1991 to 15 January 1992 to remain buried in the substratum 'Victor 1982). In labrids, 2 days 'i.e. the end of the wet season to the onset of the dry season). Data were added to the daily increment counts to account for 1 day in on Caribbean species were collected from shallow fringing reefs the egg stage and another prior to formation of the ®rst increment. around San Blas Point along the Caribbean coast of Panama from Using data on hatchling and settler sizes and the pelagic larval 15 February to 15 May 1992 'late dry season through early wet duration, we calculated mean exponential growth rates in both season). To take into account potential eects of water tempera- weight and length terms using the following formula: SL Lhekt, tures on egg and hatchling size 'Chambers and Leggett 1987) our where SL is standard length 'or weight) at settlement, Lh is total sampling was done when temperatures were similar on the two length 'or weight) at hatching 'almost equivalent to standard length sides of the Isthmus. in hatchlings), t is duration of the pelagic stage, and k is the growth At each site several permanent study plots were established in coecient. Similar to Thresher and Brothers '1989), we calculated shallow water rocky habitat and 'Caribbean site only) on adjacent an exponential growth coecient, because various studies on grass beds at a depth of 2±5 m. After removing resident recruits pomacentrids indicate that larval growth is exponential 'Suzuki and small juveniles of pomacentrids and labrids using hand nets et al. 1985; Potthoet al. 1987; Danilowicz and Brown 1992; Al- and anaesthetic, all subsequent newly settled recruits were collected shuth and Tucker 1998). However, we also performed the same from a plot on a daily basis, usually in mid-morning, every day for analyses using linear growth coecients, which produced the same 90 days. Following collection, new recruits were sorted by species, pattern of results as that described below. and a subset of each daily collection was frozen and later analyzed We were able to obtain samples of hatchlings of only seven of to determine dry weights at settlement. To be certain that those the 13 labrid species considered here. However, data on egg dry recruits were in fact day-old settlers, their otoliths were examined weights of all 13 species are available 'Robertson 1996), and we for evidence of daily post-settlement increments. Those having used those data to infer dry weight growth rates of larvae for all post-settlement increments were excluded from analysis of size at species, to avoid biasing results by mixing methods. In doing so we settlement and calculation of planktonic growth rates. made the assumption that, among congeners, the same proportion To determine hatchling size in pomacentrids, egg masses were of an egg is devoted to the hatchling. We used the relationship collected from nests in late afternoon, just prior to evening between egg dry weight and hatchling length in seven species of hatching 'Robertson et al. 1990), and placed in aquaria. Larvae Halichoeres and Bodianus to estimate hatchling lengths for the that hatched that evening were pipetted out, washed several times other congeners for which we lacked hatchlings. in distilled water, and frozen. For labrids, eggs were stripped from gravid females into a petri dish and fertilized with sperm stripped from a male into the dish. Newly hatched larvae obtained 24 h Statistical procedures after fertilization were treated as per pomacentrid hatchlings. Hatchling length represented the total body length in millimeters. We employed a combination of parametric and nonparametric Individual hatchling dry weight measurements were estimated by statistics to analyze the life-history traits. The traits of all species
Table 2 List of reef ®shes species examined in this study Eastern Paci®c Western Atlantic Pomacentridae Abudefduf troschelii Gill Abudefdux saxatilis 'Linnaeus) Chromis atrilobata Gill Chromis multilineata 'Guichenot) Chromis acapulcoensis 'Fowler) Stegastes diencaeus 'Jordan and Rutter) Stegastes ¯avilatus 'Gill) Stegastes dorsopunicans 'Poey) Stegastes leucostictus 'MuÈ ller and Troschel) Stegastes partitus 'Poey) Stegastes planifrons 'Cuvier) Stegastes variabilis 'Castelnau) Labridae Bodianus diplotaenia 'Gill) Bodianus rufus 'Poey) Halichoeres chierchiae Caporiacco Halichoeres bivitattus 'Bloch) Halichoeres dispilus 'GuÈ nther) Halichoeres garnoti 'Cuvier and Valenciennes) Halichoeres nicholsi 'Jordan and Gilbert) Halichoeres maculipinna 'MuÈ ller and Troschel) Halichoeres notospilus GuÈ nther Halichoeres poeyi 'Steindachner) Thalassoma lucasanum 'Gill) Halichoeres radiatus 'Linnaeus) Thalassoma bifasciatum 'Bloch) 14 were evaluated for normality and homogeneity of variances. When least one of these species, because, in the Bahamas, traits did not meet the criteria for parametric analyses, even after larvae of C. multilineata are able to recruit as small as attempts to normalize the data by transformation, we used non- parametric equivalents. Data were analyzed using Systat 'SPSS) 12±15 mm SL 'Wellington, personal observations). and Sigma Stat 'Jandel), except for the comparison of species The most straightforward phylogenetic relationship means in Stegastes and Halichoeres. For these we performed a within Stegastes exists for S. acapulcoensis 'EP) and bootstrap analysis using 1000 iterations 'Efron 1982). S. planifrons 'WA). Although sample sizes for hatchlings Multivariate principal component analyses using the Statistical were too small for statistical evaluation, these data in- Analyses Systems procedure 'SAS 1990) were also conducted to quantitatively compare the multivariate relationship among traits dicate that weight is heavier in S. planifrons 'Tables 3, between western Atlantic and eastern Paci®c species for both 4). Settlers of S. acapulcoensis weighed signi®cantly Stegastes and Halichoeres. To evaluate overall dierences in life more than those of S. planifrons, although there was no traits, we used hatchling 'eggs for labrids) weight, hatchling length, dierence between the two in terms of standard length. settlement weight, settlement length and planktonic larval duration of all individuals of each species. We did not include growth rates PLD was longer for S. planifrons than S. acapulcoensis. in these analyses because they are derived from a combination of Thus, S. acapulcoensis hatches at a smaller size 'weight), PLD and settlement size. For the principal components analyses all grows more rapidly and settles sooner than S. planifrons. measurements were transformed to natural logarithms. The ei- Because a Caribbean sister species to S. ¯avilatus cannot genvalues were statistically evaluated to determine dierences be- tween eastern Paci®c and western Atlantic species. We evaluated be identi®ed in the H.A. Lessios et al. phylogeny the signi®cance of the principal component loading across regions 'unpublished), we compared larval trait values of this by comparing the individual PC values 'eastern Paci®c versus species to the mean values of those traits in the three western Atlantic) using a t-test or the nonparametric Wilcoxon Caribbean members of the S. ¯avilatus clade 'S. di- rank sum test when values could not be normalized. encaeus, S. dorsopunicans and S. variabilis). Relative to the average value for its Caribbean clade-members, S. ¯avilatus had slightly smaller hatchlings 'weight and Results length), slightly larger settlers 'weight and length), but about the same PLD and larval growth rate. The overall Variation in early life-history traits among comparison between EP and WA means for the genus the pomacentrids Stegastes, based on the conservative bootstrap tech- nique, showed a signi®cant dierence in only one trait: Data on all ®ve basic larval traits 'hatchling weight and on average hatchlings of Caribbean species were 1/3 length, settlement weight and length, and planktonic heavier than those of Paci®c species. larval duration) and two derived traits 'linear and In summary, in ®ve species-pair comparisons there weight growth rate) were obtained for all 12 'eight Ca- were no clear cut patterns of inter-oceanic dierences ribbean and four eastern Paci®c) species sampled. Based among the traits, other than hatchling weights being on a recently constructed phylogeny it appears that higher in West Atlantic species in two of three genera, Abudefduf saxatilus/A. troschelii are valid transisthmian and four of ®ve species-pairs. geminate species 'Bermingham et al. 1997), i.e. species In the PCA analysis of larval traits for Stegastes the that diverged from a common ancestor following the ®rst two principal components accounted for 79% of closure of the Isthmus of Panama. Chromis atrilobata the total variance with the majority of the variance and C. multilineata are look-alike species that have been explained in PC1 'Table 5; Fig. 1a). Here three of the treated as geminates 'Bermingham et al. 1997), although values had highly positive correlations of similar value 'r there is no phylogeny of the genus available to con®rm ranging from 0.418 to 0.538) and the fourth 'hatching that situation. A global phylogeny of the genus Stegastes length) had a high negative correlation. This indicates 'Lessios and Robertson, unpublished) shows that it is that species with larger hatchlings have smaller settle- not possible to designate a sister species for S. ¯avilatus, ment sizes and longer PLDs. The second component, which appears to be equally related to S. diencaeus, with a strong negative correlation between PLD, S. dorsopunicans and S. variabilis. S. planifrons is the hatching and settlement size is consistent with the in- most closely related Caribbean species to S. acapulco- terpretation of PC1. Principal component values for ensis, although there are other eastern Paci®c species and eastern Paci®c and western Atlantic species were not Brazilian species in the same clade. signi®cantly dierent 'P 0.21, P 0.3, respectively). A comparison of the two geminate Abudefduf species Thus there was no overall pattern of dierence in larval 'Tables 3, 4) shows that A. saxatilus 'WA) larvae are traits between the members of these two faunas. heavier but not longer at hatching, and have faster We compared larval growth rate and PLDs of two growth than those of A. troschelii. There were no sig- species-pairs with similar hatchling weights ± C. multi- ni®cant dierences between these species in settlement lineata versus C. atrilobata and S. dorsopunicans versus sizes, but the PLD is marginally '5%) shorter in S. ¯avilatus .InChromis, larval growth was higher but A. saxatilus. In contrast, in the Caribbean Chromis, the PLD longer in the Paci®c species 'C. atrilobata).In C. multilineata, settlement size was slightly smaller, the Stegastes larval growth 'weight) and size at settlement PLD was slightly longer and larval growth rate was were slightly higher in the Paci®c species 'S. ¯avilatus), lower than in C. atrilobata. It should be noted, however, but there was no dierence in the PLDs of the two that size at settlement appears to be ¯exible within at species. Table 3 Summary of early life-history traits for eastern Paci®c 'EP) and western Atlantic 'WA) species of Pomacentridae and Labridae. Values are means SE, sample sizes are in parentheses, range of values in brackets. For Labridae, hatching dry wt is followed in brackets by egg dry wt and paired numbers 'e.g. 50/18), whereby the ®rst value is number of eggs weighed to calculate average egg weight 'mg), and the second value is number of independent samples 'est estimated; SL standard length; TL total length; PLD planktonic larval duration)
Species 'Site) Hatching Settlement PLD 'days) Exponential growth
Dry wt 'mg) TL 'mm) Dry wt 'mg) SL 'mm) Dry wt 'mg) SL 'mm)
Pomacentridae Abudefduf troschelii 'EP) 0.018 0.0015 2.8 0.01 '40) 12.6 1.63 '8) 11.3 0.79 '8) 20.7 0.18 '28) 0.31 0.007 '8) 0.065 0.001 '8) '40/2) [2.60±2.92] [5.6±18] [8.9±17] [19±26] [0.29±0.33] [0.059±0.072] Abudefduf saxatilus 'WA) 0.028 0.0015 2.8 0.02 '40) 16.1 1.22 '11) 11.9 0.19 '11) 19.4 0.32 '18) 0.34 0.004 '11) 0.08 0.003 '11) '40/2) [2.64±3.01] [12±25] [11±12.8] [17±28] [0.32±0.36] [0.077±0.082] Chromis atrilobata 'EP) 0.009 0.0006 2.3 0.02 '80) 52.6 2.27 '11) 20.8 0.26 '11) 29.0 0.44 '50) 0.32 0.009 '11) 0.081 0.002 '11) '40/2) [1.90±2.52] [39±64] [19.5±22] [23±37] [0.27±0.36] [0.068±0.093] Chromis multilineata 'WA) 0.010 0.0002 2.3 0.01'40) 44.6 1.17 '29) 19.2 0.14 '40) 27.2 0.26 '41) 0.43 0.005 '29) 0.078 0.001 '29) '40/2) [2.09±2.45] [31±59] [17.2±2.21] [24±33] [0.36±0.49] [0.063±0.086] Stegastes acapulcoensis 'EP) 0.012 0.0002 2.4 0.02 '49) 13.2 1.20 '19) 10.3 0.12 '53) 24.9 0.17 '101) 0.27 0.004 '19) 0.060 0.001 '19) '3) [2.08 2.60] [5.3±18] [8.8±13.2] [20±29] [0.26±0.30] [0.052±0.063] Stegastes ¯avilatus 'EP) 0.014 0.001 2.3 0.01 '40) 17.8 1.20 '6) 11.6 0.17 '15) 28.2 0.18 '101) 0.19 0.007 '9) 0.058 0.002 '9) '3) [2.04±2.40] [14±21] [10.4±12.8] [24±33] [0.16±0.20] [0.058±0.062] Stegastes diencaus 'WA) 0.019 0.004 2.4 0.08 '40) 10.3 'est) 10.5 0.11 '36) 25.8 0.41 '36) 0.25 0.004 '36) 0.058 0.001 '36) '2) [2.3±2.55] [9.4±11.2] [20±30] [0.21±0.31] [0.051±0.068] Stegastes dorsopunicans 'WA) 0.013 0.0008 2.1 0.02 '40) 17.2 0.68 '26) 11.3 0.14 '26) 29.0 0.15 '29) 0.25 0.002 '26) 0.058 0.004 '26) '2) [1.90±2.31] [13±26] [10.0±12.6] [28±30] [0.24±0.26] [0.056±0.062] Stegastes leucostictus 'WA) 0.028 2.8 0.001 '40) 8.3 0.25 '13) 9.5 0.014 '9) 25.2 0.40 '9) 0.23 0.002 '9) 0.053 0.005 '9) '2) [2.55±2.88] [7.6±9.3] [8.8±10.0] [24±27] [0.21±0.24] [0.046±0.053] Stegastes partitus 'WA) 0.009 0.0008 2.0 0.001 '62) 22.4 1.14 '9) 12.2 0.12 '9) 26.7 0.16 '18) 0.29 0.004 '9) 0.067 0.001 '9) '2) [1.95±2.24] [16±27] [11.5±12.8] [25±28] [0.28±0.31] [0.28±0.31] Stegastes planifrons 'WA) 0.017 0.00005 2.4 0.01 '40) 10.3 0.32 '69) 10.5 0.54 '111) 27.7 0.26 '62) 0.23 0.002 '62) 0.055 0.001 '62) '2) [2.26±2.60] [6.5±18.1] [9.3±13.6] [23±32] [0.19±0.27] [0.044±0.060] Stegastes variabilis 'WA) 0.015 0.0001 2.6 0.02 '40) 14.1 0.47 '18) 10.8 0.08 '18) 25.9 0.16 '20) 0.27 0.002 '18) 0.055 0.004 '18) '2) [2.26±2.62] [11±19] [10±11.1] [25±27] [0.25±0.28] [0.052±0.058] Means Stegastes 'EP) 0.013 0.001 '2) 2.35 0.050 '2) 15.5 2.31 '2) 11.0 0.65 '2) 26.6 1.65 '2) 0.23 0.039 '2) 0.059 0.001 '2) [0.012±0.014] [2.3±2.4] [13.2±17.8] [10.3±11.6] [24.9±28.2] [0.19±0.27] [0.058±0.060] Stegastes 'WA) 0.017 0.003 '6) 2.38 0.122 '6) 13.7 2.16 '6) 10.8 0.37 '6) 26.9 0.65 '6) 0.25 0.01 '6) 0.058 0.002 '6) [0.013±0.28] [2±26] [8.3±22.4] [10.3±11.6] [25.2±29] [0.23±0.29] [0.053±0.067] Labridae Bodianus diplotaenia 'EP) No data 2.2 0.001 '40) 5.3 0.28 '20) 10.2 0.08 '89) 39.7 0.41 '108) 0.15 0.002 '24) 0.040 0.001 '20) [0.0124 0.0095, 50/19] [2.12±2.24] [3.2±9.1] [8.2±11.8] [31±50] [0.17±0.25] [0.034±0.071] Bodianus rufus 'WA) 0.005 '1) 2.4 'est) 6.6 0.16 '29) 11.5 0.09 '96) 36.2 0.42 '105) 0.18 0.002 '29) 0.055 0.001 '29) [0.0182 0.0005, 50/4] [4±9-8.2] [9.5±14.1] [30±56] [0.16±0.20] [0.042±0.061] Halichoeres chierchiae 'EP) 0.004 '1) 1.7 0.01 '40) 3.8 0.25 '24) 10.2 0.05 '89) 28.6 0.34 '106) 0.20 0.006 '24) 0.064 0.002 '24) [0.0095 0.004, 50/14] [1.52±1.76] [1.2±6.3] [9±11.8] [21±37] [0.15±0.28] [0.053±0.077] Halichoeres dispilus 'EP) 0.005 0.0005 '2) 1.7 0.01 '40) 6.5 0.63 '5) 13.6 0.36 '5) 39.2 0.37 '104) 0.19 0.008 '5) 0.057 0.002 '5) [0.006 0.0003, 50/13] [1.60±1.76] [5.1±8.4] [12.7±14.5] [30±50] [0.18±0.22] [0.053±0.065] Halichoeres nicholsi 'EP) No data [0.010 1.7 'est) 3.2 0.22 '10) 10.5 0.04 '58) 30.4 0.29 '102) 0.19 0.004 '12) 0.062 0.001 '10) 0.0005, 50/20] [1.6±4.5] [9.7±11.1] [24±38] [0.16±0.20] [0.055±0.070] Halichoeres notospilus 'EP) No data 1.7 'est) 4.4 0.33 '5) 11.2 0.31 '5) 37.9 0.68 '41) 0.20 0.006 '95) 0.054 0.004 '50) [0.0056 0.0001, 50/3] [3.2±5.1] [10.4±11.8] [29±47] [0.14±0.16] [0.040±0.061] Halichoeres bivitattus 'WA) 0.002 0.0002 '2) 1.9 0.01 '40) 4.0 0.14 '46) 11.2 0.07 '83) 25.4 0.18 '103) 0.28 0.002 '46) 0.082 0.001 '46) 15 16 Variation in early life-history traits among the labrids
It was not possible to make comparisons between transisthmian pairs of sister species of Bodianus, Hali- choeres and Thalassoma, either because they do not exist 'Thalassoma) or because molecular studies that might identify such pairs in Bodianus and Halichoeres have yet to be conducted. However, none of the species in either of those genera represent look-alike pairs that likely represent geminate species-pairs. Hence we rely simply on genus-level paired comparisons. In Bodianus, the Caribbean species B. rufus had larger eggs, larger set- tlers, and more rapid growth with shorter PLD. Much the same pattern of dierence in settlement size, PLD and growth rate occurred between the transisthmian Thalassoma species, except that egg weights do not dier between them 'Tables 3, 4). Regional means for Hali- choeres follow a similar pattern to that found in Thal- assoma ± the Caribbean species had shorter PLDs and higher larval growth rates ± but without any consistent pattern of dierences in either egg weights or settler size. Results of PCA 'Table 5; Fig. 1b) reveal that for Halichoeres the ®rst two principal components account for 87% of the total variance. In PC1 the ®rst three variables are positively correlated with one another but
[11.9±12.2] [27±32]negatively [0.069±0.070] correlated with planktonic larval duration, indicating that smaller sizes in settlement weight and length 'and to a lesser extent hatchling length) are as- sociated with longer PLDs. In PC2, when hatchling length is small, settlement weight and length along with PLD are larger and longer, respectively. Dierences between eastern Paci®c and western Atlantic Halichoeres species were highly signi®cant for both PC1 and PC2, with P < 0.0001 for both components with sample sizes of 44 and 67 for EP and WA species, respectively. Thus, there is solid evidence of a substantial overall dierence between EP and WA species of Halichoeres, but a dierence that is not related to regional dierences in egg size. We compared PLD and growth traits in three trans- isthmian pairs of labrids with very similar egg sizes: the two Thalassoma spp., H. garnoti /H. chierchiae and H. maculipinna/H. dispilus . In all three cases growth was lower and the PLD longer in the Paci®c species 'Tables 3, 4). Dry wt 'mg)[0.0082 0.0002, 50/16][0.0092 [1.79±2.00] 0.0005, 50/18] TL 'mm) [2.3±6.4] Dry wt [9.9±12.9] 'mg) [4.9±5.3] SL 'mm) [22±30] [11.3±12.0] [0.26±0.30] [23±34] [0.075±0.087] Dry [0.26±0.28] wt 'mg) SL [0.079±0.089] 'mm) [0.0061 0.0004, 50/6][0.0096 0.0003, 50/15] [1.52±1.88] [4.0±6.8] [7.1±13.0] [10.8±13.1] [12.1±14.0] [23±27] [28±30] [0.26±0.30] [0.25±0.30] [0.085±0.095] [0.072±0.078] [0.0079 0.0012, 4] [1.7] [3.3±9.7] [10.2±13.6] [28.6±39.2] [0.19±0.20] [0.054±0.064] [0.0083 0.008, 4][0.0058 0.0007, 50/17] [1.24±1.56] [1.7±1.9] [4.4±7.4] [4±9.6] [10.1±13.1] [11.2±13] [39±80] [24.8±29.1] [0.09±0.11] [0.27±0.28] [0.028±0.32] [0.070±0.089] [0.0051 0.00016, 50/95] [1.48±1.76] [3.9±6.2] [10.3±12.9] [38±55] [0.17±0.21] [0.051±0.062] Discussion 'WA) No data 1.7 'est) 9.6 0.73 '9) 13.0 0.27 '9) 28.9 0.15 '13) 0.27 0.003 '9) 0.075 0.001 '9) 'EP) 0.0057 0.0005 '21) 1.4 0.02 '80) 6.4 0.22 '25) 11.4 0.06 '114) 57.9 0.04 '118) 0.10±0.001 '25) 0.03 0.0002 '25) 'WA) 0.002 '1)In this study 1.6 0.01 '60) we compared 5.0 0.21 '16) 11.9 0.17 '16) 44.2 early 0.92 '19) 0.20 0.003 '16) life-history 0.06 0.001 '16) traits in reef 'WA) No data 1.7 'est) No data 12.1 0.15 '5) 29.1 0.12 '58) No data 0.070 0.025 '2) 'WA) No data 1.7 'est) 5.1 0.06 '6) 11.8®shes 0.11 '6) 27.0 across 0.22 '112) 0.27 0.009 '6) 0.082the 0.006 '6) Isthmus of Panama to test the regional- 'WA) 0.004 0.0006 '2) 1.7 0.02 '40) 5.2 0.25 '13) 11.9 0.09 '35)productivity 24.8 0.09 '109) 0.28 0.003 '13) 0.089 0.001 '13) hypothesis. That hypothesis predicts that in regions with lower productivity selection favors greater 'EP) 0.005 0.0005 '2) 1.7 '2) 4.5 0.718 '4) 11.4 0.77 '4) 34.0 2.56 '4) 0.20 0.003 '3) 0.059 0.002 '4) 'WA) 0.003 0.001 '2)provisioning 1.75 0.100 '2) 6.2 1.70of '3) hatchling 12.0 0.27 '5) 27 0.88 '5) larvae, 0.28 0.003 '4) 0.080 with 0.004 '5) the correlate that faster larval growth and shorter PLDs occur in low 'Continued) productivity regions. These predictions are reasonable assuming that those traits covary and are not aected by Halichoeres garnoti Halichoeres maculipinna Halichoeres Halichoeres poeyi Halichoeres radiatus Halichoeres Thalassoma lucansanum Thalassoma bifasciatum Table 3 Species 'Site) Hatching Settlement PLD 'days) Exponential growth Means opposing selective forces. If the productivity hypothesis Table 4 Statistical summary statistics and signi®cance based on either Mann±Whitney t-test 'U), rank sum test 'T), Student's t-test or bootstrappring. Comparison of eastern Paci®c 'EP) and western Atlantic 'WA) species means based on bootstrap analysis, n = 1000 'Efron 1982) '+, sample size too small for statistical analysis; SL standard length; PLD planktonic larval duration; NS statistically insigni®cant)
Pomacentridae/Labridae Hatching Settlement PLD Growth rate 'days) Dry wt 'mg) Length Weight Length Dry wt 'mg) SL 'mm) [Egg dry wt 'mg)] 'mm) 'mg) 'mm)
Abudefduf troschelii 'EP) vs. A. saxatilis 'WA) + NS NS NS U = 1278 t = )2.71 t = )9.69 P<0.0001 P = 0.027 P = 0.0001 EP>WA EP Table 5 Eigenvectors and eigenvalues 'expressed as proportion of and Victor 1989, 1992; McCormick 1994; Cowen and the total variance) from principal components analyses of eastern Sponaugle 1997; Sponaugle and Cowen 1997). Paci®c and western Atlantic Stegastes 'n = 126) and Halichoeres 'n = 111) For pomacentrids, our comparisons between trans- isthmian sister species provide the most powerful test for Original variables Stegastes Halichoeres evolutionary divergence in traits. However, we found the species-pair of Abudefduf to be the only case that fol- PC1 PC2 PC1 PC2 lowed predictions of the regional-productivity hypothe- Hatching length )0.503 0.268 0.313 )0.632 sis. Neither of the other two transisthmian species-pairs Settlement weight 0.531 0.460 0.620 0.349 'Chromis atrilobata/C. multilineata or Stegastes aca- Settlement length 0.538 0.383 0.628 0.196 pulcoensis/S. planifrons, nor the sister species aggregate Planktonic larval 0.418 )0.755 )0.230 0.663 duration comprised of S. ¯avilatus/S. diencaeus, S. dorsopunicans, Eigenvalue '%) 59.2 20.1 45.2 41.7 S. variabilis displayed a similar pattern. In comparing regional means in Stegastes the only trait that diered across the isthmus was hatchling weight; settlement sizes and larval growth rates, which, under the productivity hypothesis, would be expected to covary, were not re- lated in a consistent manner. Although, on average, hatching weights in western Atlantic Stegastes were about 30% higher than those among the Paci®c species, we found no indications that such dierences were linked to variation in larval growth rates or in the PLD, or were related to dierences in the productivity regime. Our data on egg size and larval development in Bodianus largely follow the pattern predicted by the productivity hypothesis ± larger eggs, more rapid growth and a shorter PLD in the Caribbean species. However, data on Halichoeres and Thalassoma oer equivocal support: the Caribbean species of both Halichoeres and Thalassoma had slightly larger sizes at settlement, slightly shorter PLDs and faster growth rates than Paci®c congeners. In both cases egg weights do not consistently dier between eastern Paci®c and western Atlantic congeners. While those patterns of variation in larval growth and duration are consistent with the pre- dictions of the productivity hypothesis, they were not linked to the predicted pattern of variation in egg weight. Thus the pattern of relationships between hatchling size and larval growth and duration among the labrids is essentially the reverse of that found in the pomacentrids. These two patterns are important observations because the validity of the productivity hypothesis hinges on direct correlations between egg size and subsequent larval growth and development to settlement under dierent productivity regimes. Two recent studies 'Kerrigan 1996; McCormick 1998) on a western Paci®c damsel®sh demonstrated that maternal size and nutritional status can in¯uence Fig. 1a, b Plot of principal component analyses of life-history traits hatchling reserves and body size. Those eects ac- 'see Table 5 for factor loadings). a Stegastes. Represents results based counted for 48% of the 1.2-fold variation in hatchling on data from two eastern Paci®c 'EP) and ®ve western Atlantic 'WA) length found in the latter study. Such a level of vari- species. b Halichoeres. Represents four species of eastern Paci®c and ability in larval length is similar to that in most '18 of 31) four western Atlantic species of the cases of transisthmian dierences between larval traits that we recorded 'Tables 3, 4). However, that level is correct it would help in establishing a coherent theory of intraspeci®c variation is much smaller than the ``in- to explain the observed wide variation in early life-his- terregional'' dierences described by Thresher '1982) tory traits in reef ®shes, both within and between taxa and Thresher and Brothers '1989), as well as the degree and in time and space 'Brothers et al. 1983; Victor 1986, of latitudinal variation in egg size discussed by Thresher 1991; Thresher 1988; Thresher et al. 1989; Wellington '1988). It is also substantially smaller than the two- to 19 threefold variation in larval traits that can occur among nate species, some members of the labrid fauna we congeners at a single location 'see discussion below of considered evidently are more distantly related: ®rst phylogenetic eects). Interpreting the basis of variation there are no look-alike species that are obvious candi- in any life-history trait will be dicult when it is neces- dates for geminate status among the three genera of la- sary to take into account that any single trait is likely brids we considered here. Second, western Paci®c species to be in¯uenced by changing multi-factorial selection of ®shes are known to breach the eastern Paci®c barrier pressures, as well as shifting environmental conditions 'e.g. Rosenblatt and Waples 1986; Robertson and Allen that may indirectly impose energetic constraints on 1996). Such transpaci®c species constitute about 15% of larvae by altering the expression of traits through the the eastern Paci®c shore®sh fauna 'Allen and Robertson maternal eects 'e.g. Cowen and Sponaugle 1997; 1994) and many have resident populations in that region McCormick 1998). It is dicult to attribute many of the 'Rosenblatt et al. 1972; Robertson and Allen 1996). In relatively small transisthmian dierences in larval traits fact, all three endemic eastern Paci®c species of Thalas- to eects of dierences in productivity regimes on larval soma 'T. grammaticum, T. lucasanum and T. virens) are traits when those dierences are within the range of more closely related to western Paci®c species than to normal, within-location intraspeci®c variability. any Atlantic species 'G. Bernardi et al., unpublished Notwithstanding these potential sources of variation, molecular data). why did our results fail to support the productivity hy- In summary, our comparisons of the early life-history pothesis? Although the data from the two regions that traits of reef ®shes across the Isthmus of Panama dem- were originally used to formulate the productivity hy- onstrated some types of variation in larval traits in both pothesis, i.e. the western Paci®c and western Atlantic, do families that were consistent with the regional produc- in fact dier in overall background productivity levels, tivity hypothesis. However, they failed to reveal any variance in productivity in both of these regions can be consistent linkage between egg/hatchling size and larval high both temporally and spatially, as well as site- growth and PLD and productivity dierences ± linkage dependent. In addition to these potential confounding that is a fundamental predictor of the productivity hy- factors, the evolutionary history of the two regions dif- pothesis. Our data also fail to support Victor's '1986) fers considerably. The western Paci®c fauna has had a proposition that increased growth in high productivity much longer period of separation from the Caribbean environments could compensate for lower levels of lar- fauna compared to only 8 million years since the rising val provisioning: growth rates were not higher nor PLDs Central American land bridge began isolating the ma- lower in Paci®c members of pairs of species with similar rine faunas of the eastern Paci®c and Caribbean and the egg/hatchling sizes in either family. We conclude that 3±3.5 million years since the Panamanian isthmus ®nally there is no single factor that is of suciently over- closed 'Keigwin 1982; Coates 1997) and completed that whelming importance that it can account for the diverse isolation. These two potential problems make dierences variation in early life-history traits among these reef in larval traits between the West Paci®c and Caribbean ®shes and that regional variations in productivity have less de®nitive than dierences between closely related little explanatory power. species across the Isthmus of Panama. The data pre- Thresher '1982) and Thresher and Brothers '1989) sented here clearly indicate that similarities and dier- recognized that phylogenetic eects can bias results ences in early life-history traits between geminates and when they considered data from two subfamilies of the other closely related species on opposite sides of that pomacentrids 'Chrominae and Pomacentrinae) sepa- isthmus are not consistent with the productivity hy- rately in their analyses, although the latter authors pothesis. Our principal component analyses show that dismissed the possibility that other phylogenetic or overall there are no clear dierences across the Isthmus sampling eects produced the patterns they described. between closely related species of Stegastes. The PCA However, a combination of the data presented here and plot for Halichoeres con®rms the existence of consider- those published by Victor '1986), Thresher and Brothers able intrageneric variation that exists independently of '1989), Wellington and Victor '1989) and Robertson any ocean eects. '1996) clearly demonstrate that substantially ®ner scale Given that the regional-productivity hypothesis can- phylogenetic eects exist. Such eects include distinct not account for the patterns observed in each group, intergeneric dierences in larval traits: 'i) larval dura- why are there dierences? First, damsel®shes and tions of dierent genera within the subfamily Poma- wrasses have fundamentally dierent modes of repro- centrinae vary by a factor of approximately 2 duction. The requirements, growth trajectories and lar- 'Wellington and Victor 1989); 'ii) egg volumes of dif- val life histories of larvae produced from small, rapidly ferent genera of West Paci®c pomacentrines vary by a hatching pelagic eggs 'of wrasses) may be fundamentally factor of 4 'Thresher and Brothers 1989); 'iii) egg dierent to those of better developed larvae hatched weights of Bodianus species from the WP, EP and Ca- from more slowly developing benthic eggs 'of damself- ribbean are about three times those of eggs of Thalas- ishes). Alternatively, those dierences may be due to the soma species from the same range of sites, while the eggs labrid faunas of the eastern Paci®c and Caribbean being of Halichoeres species from the same three regions are of more distantly related than the pomacentrid faunas. intermediate size 'Robertson 1996); and 'iv) PLDs vary While the pomacentrids have a number of clear gemi- about threefold among dierent genera of WP labrids 20 'Victor 1986). Those ®ne-scale phylogenetic eects also size were reported by Thresher '1982) and Thresher and include considerable variation in larval traits among Brothers '1989) are not possible because there are congeners at a single location within the same region: 'i) no published species-level data. However, as with the egg weights vary almost twofold among Halichoeres pomacentrids the blenniid faunas of those two regions species in both the EP and the Caribbean 'present data); share few genera, and the western Paci®c fauna is much 'ii) egg weights vary threefold among species of the more diverse 'Eschmeyer 1998). The apogonid faunas of Caribbean parrot®sh genus Sparisoma and among Ca- those two regions also include dierent genera and large ribbean members of the serranid genus Serranus 'Rob- dierences in diversity, although the genus Apogon ertson 1996); 'iii) larval weights vary threefold among dominates both faunas 'Eschmeyer 1998). the Caribbean Stegastes species 'present data); 'iv) egg We conclude that a combination of the results pre- volumes of western Paci®c Pomacentrus species vary by sented here, and closer scrutiny of previously published a factor of four 'Thresher and Brothers 1989); and 'v) data, show that, when phylogenetic eects are taken PLDs vary two-fold among western Paci®c species of into account, those data fail to con®rm the existence of Chromis 'Wellington and Victor 1989). Further, the previously described ``interregional'' patterns that have structures of the Atlantic and West Paci®c faunas of the been used to support the regional productivity hy- three families of benthic-spawning reef ®shes considered pothesis. The simplest explanation for the observed by Thresher '1982) and Thresher and Brothers '1989) patterns of variation in egg and hatchling size, PLDs, 'Blenniidae, Pomacentridae and Apogonidae) dier size at settlement and growth rates is that the eects of greatly in terms of both the occurrence and species phylogeny far outweigh the in¯uence of dierences in richness of genera: for example, 16 of the 20 genera in background levels of productivity in the larval envi- the subfamily Pomacentrinae occur in the West Paci®c, ronment. The diversity of larval traits and interrela- but only six in the Atlantic; only two occur in both re- tionships between those traits that occur among gions, and species in the unshared genera constitute the congeners as well as other confamilials at a single lo- great majority of the West Paci®c fauna 'Allen 1991). cation clearly indicates that larval life histories are in Thus there is a very real potential for sampling eects, fact highly species speci®c. due to phylogenetic 'intergeneric and intrageneric) While phylogenetic eects evidently are an important variation, to have produced the ``interregional'' dier- aspect of interspeci®c variation in the larval life histories ences discussed by Thresher '1982, 1988) and Thresher of damsel®shes and wrasses, we currently have only and Brothers '1989). vague ideas about the mechanisms that might be in- Thresher and Brothers '1989) discussed apparent volved. The less closely related species are, the stronger West Paci®c/Caribbean dierences 'higher in the those eects potentially are. In some genera there is also Caribbean) in PLDs in each of the genera Abudefduf, considerable variation among congeners that live at the Chromis and Stegastes and apparent West Paci®c/ same locality ± variation that is as great as variation Caribbean dierences in egg sizes 'volumes) of both between congeners in dierent regions. Variation in pomacentrids as a family and pomacentrines as a sub- hatchling size, larval growth and settler size among family. However, additional data presented here and in congeners may re¯ect dierences in larval ecology. Wellington and Victor '1989) indicate that genus-level There are, for example, dierences in horizontal distri- mean PLDs do not dier in either Chromis or in Abu- butions of larvae relative to reefs and in diets among defduf in those regions. The same lack of a regional Scomberomorus species 'Jenkins et al. 1984), and dif- dierence appears to hold in Stegastes, although the ferences in horizontal distributions among Plectropomus database is extremely small, both in numbers of species species 'Leis 1986) and Pterocaesio species 'Reader and and individuals sampled. Thresher and Brothers '1989) Leis 1996), as well as dierences is the swimming abili- also described family-level dierences in average egg ties and vertical position in the water column among volumes between western Paci®c and Caribbean poma- larvae of Pomacentrus species 'J. Leis, personal com- centrids, with Caribbean eggs being smaller than western munication). At our Caribbean site there is distinct Paci®c eggs. Inspection of their data shows, however, variation among the seasonal patterns of both spawning that that pattern holds in only one of three genera that and larval recruitment of dierent Stegastes spp. 'Rob- occur in both regions ± in Abudefduf, but not Stegastes ertson 1990, 1992), which may relate in some way to or Chromis. However, limited additional data fail dierences in larval ecology that are re¯ected in the to support the idea of such a dierence Abudefduf: larval characteristics we examined here. However, A. saxatilis 'Atlantic) and A. vaigiensis 'WP), which are within-location variation among congeners also occurs members of the same clade within that genus 'Ber- in relations between the lunar dynamics of spawning and mingham et al. 1997), have almost the same mean egg settlement and in the ecology of settling ®shes. The level dry weight '457 vs. 464 pg, n 64 and 31, respectively; of variation in the lunar patterns of spawning among t-test, NS), although the eggs of A. saxatilis average Stegastes species at our Caribbean site 'Robertson et al. 23% larger in volume 'Robertson, unpublished data). 1990) is greater than that among their lunar settlement Reassessments of genus-level patterns within the two patterns 'Robertson 1992). There is also interspeci®c other families of benthic-spawning reef ®shes 'Blennii- variation in habitat usage by newly settled Stegastes spp. dae, Apogonidae) for which regional dierences in egg 'Wellington 1992; Booth and Wellington 1998; Gut- 21 ie rrez 1998). Intrageneric variation in hatchling size, Gutie rrez L '1998) Habitat selection by recruits establishes local larval growth and settlement size may be linked in some patterns of adult distribution in two species of damsel®shes: Stegastes dorsopunicans and S. planifrons. Oecologica 115: 268± way to either or both of these factors. 277 Jenkins GP, Milward NE, Hartwick RF '1984) Food of larvae Acknowledgements This work represents equal authorship by of Spanish mackerels, genus Scomberomorus 'Teleostei: Scom- GMW and DRR and was supported by grant no. 4610-91 to D.R. beridae), in shelf water of the Great Barrier Reef. Aust J Mar Robertson and G.M. Wellington from the National Geographic Freshwater Res 35: 477±482 Society. Permission to conduct this research was granted by the Jones GP, Milicich MJ, Emslie MJ, Lunow C '1999) Self-recruit- Panama Government and the Kuna General Congress to the ment in a coral-reef ®sh population. Nature 402: 802±804 Smithsonian Tropical Research Institute. We thank A. Cedeno, Keigwin D Jr '1982) Isotopic paleoceanography of the Caribbean I. Hernandez, C. Guerra, L Gutie rrez, S. Swearer and E. PenÄ a for and East Paci®c uplift in Late Neogene time. 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