Evolutionary Ecology (2005) 19: 563–581 DOI: 10.1007/s10682-005-1021-1
Ó Springer 2005
Research article
The latitudinal diversity gradient through deep time: testing the ‘‘Age of the Tropics’’ hypothesis using Carboniferous productidine brachiopods LINDSEY R. LEIGHTON Department of Geological Sciences & Allison Center for Marine Research, San Diego State University, San Diego, CA 92182-1020, USA (e-mail:
[email protected])
Received 7 October 2004; accepted 8 July 2005 Co-ordinating editor: V. Jormalainen
Abstract. The latitudinal gradient in global diversity, in which the number of species decreases away from the tropics, is widely recognized and well-studied but no consensus exists as to its cause. The ‘‘Age of the Tropics’’ hypothesis argues that the tropics have more species because young, ecologically dominant, tropical clades have not had sufficient time to disperse and adapt to colder climates; given time, the tropics act as a diversity pump. This hypothesis is tested using Carboniferous productidine brachiopods, which at that time were a young, ecologically dominant clade that originated in the tropics. A database of geographic occurrences indicates that productidines did not manifest a pattern of dispersal away from the tropics through time. A phylogeny of one productidine clade demonstrates that many lineages contracted, rather than expanded, their ranges over time. The results suggest that the hypothesis that the tropics are a diversity pump cannot be generalized across time and taxa. Key words: center of origin, diversity, latitudinal gradients, paleobiogeography
Introduction The latitudinal diversity gradient, the decrease in biodiversity away from the tropics, is one of the most well-known and well-studied patterns of global diversity (Rosenzweig, 1995). This diversity gradient is recognizable in both marine (Fischer, 1960; Stehli et al., 1967; Sanders, 1968; Stehli and Wells, 1971; Steele, 1988; Rohde, 1992; Roy et al., 1998; Culver and Buzas, 2000; Crame, 2000, 2002) and terrestrial (Dobzhansky, 1950; MacArthur, 1969; Arnold, 1972; Ricklefs and O’Rourke, 1975; Silvertown, 1984; Currie and Paquin, 1987; Collins, 1989; Crane and Lidgard, 1989; Rosenzweig, 1992; Gaston and Blackburn, 1996; Blackburn and Gaston, 1997; Badgley and Fox, 2000; Cardillo, 2002; Lyons and Willig, 2002) systems, and holds for plants and animals (see Willig et al., 2003 for a review of patterns and possible explanations). Determining the processes underlying the diversity gradient would provide
564 critical insights into the question of what factors influence biodiversity, arguably one of the single most important issues facing current and future generations of scientists. Hillebrand (2004) performed a meta-analysis on more than 600 gradients from the literature with the intention of determining which species’ attributes, habitat types, and analytical approaches generated the strongest and steepest gradients. He found that studies conducted on larger scales had both stronger (higher correlation coefficient) and steeper slopes than studies conducted on smaller scales. Among species attributes, body size had the most significant impact; larger animals had stronger and steeper gradients than did smaller animals. The gradient also was stronger and steeper for marine and terrestrial environments than for freshwater systems. Several hypotheses, involving species-area effect (Terborgh, 1973; Rosenzweig, 1992, 1995; Rosenzweig and Sandlin, 1997), mid-domain constraints (Colwell and Hurtt, 1994; Willig and Lyons, 1998; Colwell and Lees, 2000), competition and niche partitioning (Stevens, 1989), predation (Janzen, 1970); differences in seasonality (Pianka, 1966; Sanders, 1968), differences in productivity (Pianka, 1966; Rhode, 1992; Roy et al., 1998), or constancy of resources (Pianka, 1966), have been put forward to explain the diversity gradient, but as of yet, no hypothesis has been universally accepted. Rohde (1992, 1996, 1997) pointed out that many of these hypotheses are circular, or are insufficiently supported by existing evidence. Recently, the ‘‘Age of the Tropics’’ hypothesis (Fischer, 1960) has been suggested again by Crame (2000), in this case for Bivalvia. The Age of the Tropics hypothesis, sometimes referred to as a ‘‘center of origin’’ hypothesis, is based upon the assumption that the modern tropical climate has existed at least since the Eocene and possibly longer (Zachos et al., 2001), whereas modern temperate and polar climates came into existence as a consequence of relatively more recent arrangements of tectonic plates and resulting changes in ocean circulation (Zachos et al., 2001). The Age of the Tropics hypothesis suggests that, given sufficient time, younger, ecologically dominant clades originating in the tropics eventually will expand their ranges, and adapt, into temperate and polar realms. The tropics act not only as a center of origin, but also as a ‘‘diversity pump’’ (Fischer, 1960; Stehli et al., 1969; Jablonski, 1993; Flessa and Jablonski, 1996; Crame, 2000, 2002). By this argument, the latitudinal diversity gradient exists in part because these taxa have not had sufficient time to disperse and to diversify into temperate and polar regions (Stehli et al., 1969; Crame, 2000). The tropics generally are regions of greater competition and predation intensity (Vermeij, 1987), and thus tropical taxa invading temperate realms long have been assumed to have a competitive advantage over existing temperate incumbents (Briggs, 1974). For example, heteroconch bivalves, which are the youngest (Crame, 2000) and most ecologically dominant (Vermeij, 1987; Crame, 2000) clade of
565 Bivalvia, in terms of both diversity and individual abundance, also have the steepest latitudinal diversity gradient of any bivalve group in the Recent (Crame, 2000). In contrast, older bivalve clades are more prevalent in temperate and polar regions, and have a gentler latitudinal gradient (Stehli et al., 1969; Crame, 2000). This pattern has been used to argue that heteroconchs, whose primary radiation occurred during the Cretaceous (Crame, 2000), have not had time to diversify into cooler climates, and thus are driving the latitudinal pattern of diversity for Bivalvia (Crame, 2000, 2002). Although inverse correlations between clade age and slope of the diversity gradient are consistent with the Age of the Tropics hypothesis, such evidence does not refute other hypotheses. I advocate testing these hypotheses through deep time, and within a phylogenetic context, to determine if and how the global distributions of clades have changed. Although the existence of the latitudinal diversity gradient has been documented for several clades at different times in the geologic past (Stehli et al., 1969), the examination of the gradient through successive time intervals for any clade has been done only rarely (see Silvertown, 1984, and Crane and Lidgard, 1989, for exceptions), and never previously within a phylogenetic framework. Changes in climate through time would have a profound effect on seasonality, productivity etc. If such factors are the primary influence over the latitudinal diversity gradient, then the slope of the diversity gradient should change as global climates cooled and warmed (Valentine, 1984). In contrast, if the latitudinal diversity gradient is primarily a function of clade age, an inverse relationship between time and the slope of the latitudinal diversity gradient should exist for a dominant clade (Stehli et al., 1969; Crame, 2000). In this paper I document changes in the latitudinal diversity gradient of productidine brachiopods (Phylum Brachiopoda, Subphylum Rhynchonelliformea, Class Strophomenata, Order Productida, Suborder Productidina) during the Carboniferous period (360-286 Ma). A biogeographic analysis of a clade that went extinct prior to the development of more recent climate patterns provides a test of whether the Age of the Tropics hypothesis can be generalized through time. The Late Carboniferous is an appropriate analog for the Pleistocene– Recent. Both time periods experienced (a) ‘‘icehouse’’ conditions with major glaciations (Veevers and Powell, 1987; Frakes et al., 1992) (b) frequent fluctuations in sea-level (Ross and Ross, 1987; Frakes et al., 1992); (c) atmospheres low in CO2 (Berner, 1994; Bruckschen et al., 1999); (d) enhanced weathering of terrestrial sediments (Bruckschen et al., 1999); and (e) oceans in which aragonite is the dominant phase of calcium carbonate (Hardie, 1996). Although the Late Carboniferous saw an icehouse planet, the Earth previously had experienced more globally widespread tropical conditions in the Devonian and Early Carboniferous. Thus, the Late Carboniferous tropics
566 (i.e. tropical conditions) were older than the temperate and polar climates of the time. An additional factor in choosing the Late Carboniferous is that this temporal interval had the lowest origination and extinction rates of any interval in the Paleozoic (Stanley and Powell, 2003; Bambach et al., 2004). Productidines radiating in the Early Carboniferous experienced a long interval of time during the Late Carboniferous comparatively unaffected by taxonomic turnover at the genus level. Consequently, interpretations of changes in the slope of the diversity gradient are less likely to be confounded by rapid increases in origination or extinction; changes in the gradient are more likely to be a function of dispersal or range contraction. In terms of diversity, biovolume, and individual abundance, productidine brachiopods were among the most ecologically dominant clades of Carboniferous oceans (Muir-Wood and Cooper, 1960). Late Paleozoic productidines had latitudinal diversity gradients similar to that of modern heteroconchs (Figure 1; also compare Bambach, 1990 with Crame, 2000). Productidines also are one of the last brachiopod clades to evolve – as with bivalves, there is a strong inverse correlation between brachiopod clade-age and tropicality. In brief, Late Carboniferous productidines were chosen as the subject of this research because productidines provide a study group phylogenetically independent of Recent clades, but experiencing conditions similar to those of the Recent.
Materials and methods A database of 921 genus-region combinations through the seven Carboniferous stages (Table 1) was compiled from the primary literature. A genus-region refers to a specific combination of one genus in one region during one stage. Sepkoski and Kendrick (1993) demonstrated that diversity patterns at the genus level often are adequate proxies for species patterns. Regions represent geological basins, or networks of smaller, interconnected basins, during the Carboniferous; 27 such regions were identified (Table 2). The use of these regions does not imply biogeographic provinces, but rather represents relatively small, discrete, geographic units that could be identified consistently through the seven stages. As size of geologic basins varies with changes in sealevel or tectonics, size of these regions also varies. For each stage, regions were classified as either tropical (between 25° north and 25° south of the equator) or temperate/polar (=extratropical), based on plate tectonic reconstructions for the Carboniferous (Scotese and McKerrow, 1990; Golonka and Ford, 2000). The strict definition of the tropics is based on an astronomical phenomenon, the Earth’s obliquity (tilt) relative to the elliptical plane, and is not defined by climate (although the distribution of solar insolation varies with obliquity). The
567
Early Carboniferous
(a)
80.0%
60.0% 50.0% 40.0% 30.0%
60.0% 50.0% 40.0% 30.0%
20.0%
20.0%
10.0%
10.0%
0.0%
0-15
16-30
31-45
Latitude
> 45
Gzhelian Kasimovian Moscovian Bashkirian
70.0%
Percent Genera
Serpukhovian Visean Tournaisian
70.0%
Percent Genera
Late Carboniferous
(b)
80.0%
0.0%
0-15
16-30
31-45
> 45
Latitude
Figure 1. Latitudinal diversity gradients of productidine brachiopod genera (by percentage) for the seven Carboniferous stages. Latitude divided into 15° bins. Data presented as two graphs for clarity. (a) Early Carboniferous. (b) Late Carboniferous.
position of the Tropics (the positions of the Tropic of Cancer and Tropic of Capricorn) through time has probably not varied from 21–25° North and South of the equator (Zachos et al., 2001); this maximum extent is used herein to define the tropics. It also should be noted that the effect of obliquity on the distribution of solar insolation creates a tropical zone (25° north and south) that varies little in mean monthly temperature within the band (Terborgh, 1973), i.e. seasonality is significantly lower within the tropical zone than in the extratropics. Thus, the difference in climate between two locations at 30 and 35° North may be greater than the difference between two locations at 5 and 20° North, and taxon richness may not vary with latitude in a linear fashion. Consequently, this study employs a simple categorization of regions and taxon distribution into tropics versus extratropics, as well as the more traditional approach of examining diversity along latitude. This is not to suggest that the distribution of tropical climate conditions did not vary during the Carboniferous; rather, the use of a simple binary (tropical vs. extratropical) categorization for regions and their constituent taxa may identify patterns otherwise difficult to discern and may better facilitate identification of dispersal events. Genera from a given stage were identified as tropical, temperate (=extratropical), or pandemic, based on their distributions. Similar to Recent bivalves (Stehli et al., 1969), the great majority of productidine genera at each stage were either tropical or pandemic. Regions (and their constituent genera) were also classified into 15° latitudinal bins (0– 15°, 16–30° etc.) for the purpose of examining and comparing latitudinal gradients from stage to stage. One disadvantage of examining the Carboniferous is that, for the most part, gradients can only be examined from 0 to 60° because of the arrangement of tectonic plates at that time. North of 60° was open, deep ocean during the Carboniferous, unsuitable as an environment for productidines, and unlikely to be preserved to the fossil record. The massive Gondwana
568 Table 1. Stages of the Carboniferous period Division
Stage
Age (Ma)
Late Carboniferous
Gzhelian Kasimovian Moscovian Bashkirian Serpukhovian Visean Tournaisian
296–290 303–296 311–303 323–311 327–323 342–327 354–342
Early Carboniferous
Table 2. Geographic regions used in the present study Region
Location
T
V
S
B
M
K
G
North American Midcontinent S. Laurentia (New Mexico-Arkansas) Klamath (California, Nevada) Canadian Rockies (Alberta) Yukon & NW Territories Amazonia (Brazil) Argentina Western Europe (UK, Ireland, Belgium) Central Europe (Germany, Poland) Southern Europe (Spain, Italy, Balkans) North Africa (Libya, Egypt) Ukraine (Donets Basin) Russia Arctic Russia Kazakhstan Siberia NW China Mongolia (Altay) NE China Central China (Shaanxi) Southern China (Yunnan, Guangxi) Japan SE Asia (Burma – Melesia) Tibet Himalaya (Pakistan, Kashmir, Nepal) NW Australia Eastern Australia
40 32 39 52 65 25 40 53 51 46 30 47 56 66 51 55 42 45 47 34 25 37 18 37 32 16 21
1 1 1 1 1 0 0 1 1 1 0 1 1 1 0 0 0 0 0 1 1 1 1 1 0 1 1
1 1 1 1 0 0 0 1 1 1 0 1 1 1 0 0 0 0 1 1 1 1 1 0 0 1 0
1 1 1 1 0 0 0 1 1 1 1 1 1 0 0 0 0 0 1 1 1 1 1 0 0 1 0
1 1 1 1 0 0 0 1 1 1 1 1 1 0 0 0 0 0 0 1 1 1 1 0 0 1 0
1 1 1 1 0 0 0 1 1 1 1 1 1 0 0 0 0 0 1 1 1 1 1 0 0 0 0
1 1 1 1 0 1 0 1 1 1 1 1 1 0 0 0 0 0 1 1 1 1 1 0 0 0 0
1 1 1 1 0 1 0 1 1 1 1 1 1 0 0 0 0 0 1 1 1 1 1 0 0 0 0
N 95 W N 105 W N 117 W N 117 W N 130 W S 52 W S 68 W N 01 W N 15 E N 13 E N 16 E N 39 E N 38 E N 56 E N 63 E N 95 E N 88 E N 97 E N 122 E N 108 E N 105 E N 138 E N 99 E N 80 E N 76 E S 126 E S 148 E
Location refers to the latitude and longitude of the modern approximate center of region. A ‘‘1’’ indicates that the region was identified as Tropical during that stage; ‘‘0’’=Not Tropical. An underlined number indicates that no productidines have been reported from that region for that stage. T = Tournaisian, V = Visean, S = Serpukhovian, B = Bashkirian, M = Moscovian, K = Kasimovian, G = Gzhelian.
land-mass was located in south boreal and polar regions. Although coastline certainly existed south of 60°, this region was heavily glaciated for much of the Carboniferous. Thus, almost all of the regions containing productidines in the database are between 60° North and 60° South.
569 A concern of any biogeographic study is the potential bias created by differences in geographic area between geographic zones, i.e. diversity is greater in a given region because the area of that region is larger. Independent of real biological species-area effects, there also is the potential for artifactual bias in that more species may be found in a larger sampling area. This problem is further complicated when examining biogeography through deep time. In the present study, the primary concern is that differences in area between tropical and temperate zones would create an artifactual bias when comparing the diversity of tropical zones to that of temperate zones. To account for such bias, the area of epicontinental seas was used as a proxy for accessible fossiliferous rock in the Recent. The areas of tropical epicontinental seas, and of extratropical epicontinental seas, were calculated (Table 3) for each of four of the Carboniferous stages (Visean, Serpukhovian, Moscovian, Gzhelian), using an imaging program (TPSdig, courtesy of James Rolfe) to digitize the outlines of the seas on Scotese global reconstruction maps (www.scotese.com). This analysis was performed only on these four stages because maps defining the positions of epicontinental seas were available only for those four stages. The maps use a Molleweide projection, which preserves area relationships. A linear regression was then performed to determine the amount of variation in number of taxa attributable to area. Recent taxon-area curves are not linear, however, within a given order of magnitude of area, the relationship between area and taxa often is linear. On the spatial scale of all tropical and all non-tropical epicontinental seas for a given stage, a linear relationship probably is an appropriate null hypothesis; nonetheless, to account for the possibility that the relationship is not linear, both generic richness and area were log-transformed, which is standard procedure for taxon-area analysis, and a linear regression also performed on the log-log data. The regression analyses of productidine genera on area do not indicate that a significant proportion of variation in generic richness from tropical to temperate zones is due to area (Figure 2; Linear Adj. R2=0.26, p=0.11; Log–log Adj. R2=0.006, p=0.35). Although area must have some influence on the distribution of the brachiopods, and likely has an influence through time, there clearly is a biogeographic signal independent of area within each time stage. As described previously, the intent of this research is to test the Age of the Tropics hypothesis, specifically whether the latitudinal diversity gradient for a given clade is primarily a function of time and clade age. If the hypothesis is correct, then taxa and lineages originating in the tropics should, given sufficient time, disperse outside of the tropics. This is tested herein in three ways. (1) Tropicality, the proportion of taxa living only in the tropics, is calculated for each stage in the Carboniferous, and the resulting pattern through time
570 Table 3. Comparison of observed distribution of genera with area of epicontinental seas
Visean Tropical Visean Temperate Serpukhovian Tropical Serpukhovian Temperate Moscovian Tropical Moscovian Temperate Gzhelian Tropical Gzhelian Temperate
Observed genera
Area (pixels)
86 57 36 20 22 18 35 15
7912 7134 4628 6187 4277 5765 4345 6402
is examined. Similarly, generic richness relative to latitude was plotted into 15° bins for each stage. The use of these two methods effectively examines the problem at two different bin sizes. Assuming that high tropical origination rates at the genus level do not characterize the clade for tens of millions of years, widespread dispersal of the clade into extratropical regions would eventually result in a diversity gradient with a gentler slope, and in lower tropicality through time. Lack of such a pattern would fail to corroborate the Age of the Tropics hypothesis. (2) Examination of tropicality across higher taxa, based on global compilations, may not capture specific events. Consequently, changes through time in tropicality of individual genera were analyzed to determine if the pattern of change through time was statistically significant. At each stageboundary, those genera surviving to the next stage were classified into one of four categories: (a) tropical-only taxa that remained tropical-only; (b) tropical-only taxa that expanded into extratropical regions during the next stage; (c) pandemic taxa that remained pandemic; and (d) pandemic taxa that range-contracted to become tropical-only during the next stage. As the analysis includes only those taxa that survive from one stage to the next, the changes in distribution are thus calculated independently of those taxa that go extinct during a stage. McNemar’s chi-square test was used to determine if the tropicality of surviving genera changes significantly from stage to stage. A standard chi-square test is inappropriate here because that test assumes independence among samples. This assumption clearly is not met in the present study as the durations of some genera are longer than a single stage; the tropicality of one stage is potentially influenced by that of the previous stage. McNemar’s chisquare surmounts this problem by analyzing only the changes from stage to stage; changes within one stage are independent of changes in the previous stage.
571
100 90
Generic Richness
80 70 60 50 40 30 20 10 0
0
2000
4000
6000
8000
10000
Area (Pixels) Figure 2. Scatterplot of productidine generic richness versus area (pixels) of epicontinental seas. Each point represents either all tropical (solid diamonds) or all non-tropical (open diamonds) epicontinental seas for one of the four stages (Visean, Serpukhovian, Moscovian, Gzhelian) for which reliable paleoshoreline reconstructions were available.
(3) Biogeographic range expansion and contraction occurs within actual lineages but patterns of diversity derived from taxon counts may not accurately reflect this. For example, a pandemic genus derived from a tropical genus would not necessarily be identified as a range expansion as the genera have different names. Therefore, as an additional test, phylogenetic analysis, using global parsimony, of one important group of productidines was performed, and biogeographic distribution mapped onto the phylogeny, to determine changes of tropicality within lineages. All Carboniferous genera of the subfamily Overtoniinae, and Devonian outgroup taxa (Brunton and Lazarev, 1997), were included in the analysis. This subfamily was diverse and abundant during the Carboniferous (Brunton and Lazarev, 1997). The Overtoniinae were chosen for analysis because they represent the Productellidae, one of the most primitive, stratigraphically oldest, and yet diverse, productidine clades present in the Carboniferous (Brunton and Lazarev, 1997), i.e. by the end of the Carboniferous, they had longer to diversify and disperse than other productidine clades. The analysis included 18 taxa and 24 characters (19 binary and 5 multistate). All characters were reversible and unordered. The taxon/character matrix and character descriptions are included in the Appendix. The analysis was performed in PAUP* v.4.0b10 (Swofford, 2000), using global parsimony with the branch and bound algorithm.
572 Results Productidine tropicality, measured as the proportion of all productidine genera living only in the Tropics, varied during the Early Carboniferous, an interval of fluctuating climate (Frakes et al., 1992), and then subsequently exhibited a slight increase during the Late Carboniferous back towards levels of tropicality similar to those manifested during the Tournaisian (Figure 3). The absolute number of tropics-only genera remained relatively constant during the Late Carboniferous (Figure 3). Although tropicality fluctuated during the Carboniferous, tropicality during the Gzhelian, the youngest Carboniferous stage, is almost identical to that of the Tournaisian, the oldest Carboniferous stage (Figure 3). Similarly, when diversity patterns are examined along 15° latitude bins, there is little change in the general pattern and slope of the diversity gradient through the Carboniferous (Figure 1). All gradients take the form of a negative logarithmic curve. The slope of the gradient steepens from the Tournaisian to the Visean, flattens to a gentler slope by the Bashkirian and then gradually steepens from the Bashkirian onwards until the Kasimovian and Gzhelian, at which time the slope is almost indistinguishable from that of the Tournaisian. Indeed, all possible pairs of latitudinal gradients (e.g. Tournaisian vs. Visean etc.) through the Carboniferous have correlation coefficients >0.97. Examination of those genera that persist through more than one stage reveals that Tournaisian tropical genera experienced significant change in latitudinal distribution during the Visean, largely due to range expansion (Table 4) in which 12 of 22 originally tropical genera expanded outside of the tropics. However, by the Serpukhovian, many cosmopolitan genera underwent a range contraction (13 of 28 cosmopolitan genera) of roughly equivalent magnitude (Table 4). This pattern of within-genus range expansion and contraction is consistent with previous work on Early to Middle Carboniferous brachiopods (Kelley et al., 1990). Subsequently, and throughout the Late Carboniferous, no statistically significant changes in tropicality within genera occurred (McNemar’s chi-square, Table 4); only one genus expands its range during the Late Carboniferous. The phylogenetic analysis found six equally most parsimonious trees (tree length = 55, retention index = 0.76). The phylogenetic results are largely consistent with the results of the McNemar’s chi-square tests; as with individual genera, Carboniferous overtoniin lineages experienced little or no increase in latitudinal range subsequent to the Visean. The phylogenetic hypothesis has five changes in latitudinal range; four of these changes involve a range decrease (Figure 4). Fourteen Carboniferous lineage segments (branch segments, i.e. any segment from node to node or from node to terminus) potentially could have expanded their ranges from tropics-only to a cosmopolitan distribution. If the
573 100% Productine Genera
90% 80%
20
57
20
22
18
11
15
29
39
22
16
16
17
22
Tour
Vis
Serp
Bash
Mosc
Kas
Gzh
70% 60% 50% 40% 30% 20% 10% 0% Lower Carboniferous Tropics Only
Upper Carboniferous Pandemic
Figure 3. Proportions of productidine brachiopods living only in the Tropics vs. cosmopolitan productidines living both within and outside the Tropics during the Carboniferous. Numbers on bars are the absolute number of genera in each category.
Age of the Tropics and diversity pump hypotheses are correct, then the null expectation would be that many of those 14 lineages would expand, but only one actually did so (Figure 4). Even assuming a null expectation that only half (7 of 14) of the lineages should expand, the observed number of expansions is significantly different from the expected number (binomial, p
